Dynamic Aquaria, Third Edition: Building Living Ecosystems

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DYNAMIC AQUARIA

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DYNAMIC AQUARIA BUILDING AND RESTORING LIVING ECOSYSTEMS Third Edition Walter H. Adey Karen Loveland National Museum of Natural History Smithsonian Institution Washington, D.C.

AMSTERDAM • BOSTON • HEIDELBERG • LONDON • NEW YORK • OXFORD PARIS • SAN DIEGO • SAN FRANCISCO • SINGAPORE • SYDNEY • TOKYO Academic Press is an imprint of Elsevier

Academic Press is an imprint of Elsevier 84 Theobald’s Road, London WC1X 8RR, UK 30 Corporate Drive, Suite 400, Burlington, MA 01803, USA 525 B Street, Suite 1900, San Diego, California 92101-4495, USA First edition 1991 Second edition 1998 Third edition 2007 Copyright © 2007 Walter H. Adey and Karen Loveland. Published by Elsevier Inc. All rights reserved The right of Walter H. Adey and Karen Loveland to be identified as the authors of this work has been asserted in accordance with the Copyright, Designs and Patents Act 1988 No part of this publication may be reproduced, stored in a retrieval system, or transmitted in any form or by any means electronic, mechanical, photocopying, recording or otherwise, without the prior written permission of the publisher Permissions may be sought directly from Elsevier’s Science and Technology Rights Department in Oxford, UK; phone: (+44) (0) 1865 843830; fax: (+44) (0) 1865 853333; e-mail: [email protected]. You may also complete your request on-line via the Elsevier homepage (http://www.elsevier.com), by selecting “Customer Support” and then “Obtaining Permissions” British Library Cataloguing in Publication Data A catalogue record for this book is available from the British Library Library of Congress Cataloging in Publication Data A catalog record for this title is available from the Library of Congress ISBN-13: 978-0-12-370641-6 ISBN-10: 0-12-370641-6 For information on all Academic Press publications visit our web site at http://books.elsevier.com Typeset in 10/12pt Palatino by Charon Tec Ltd (A Macmillan Company), Chennai, India www.charontec.com Printed and bound in the USA 07

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Contents

Preface xi Acknowledgments and Dedication

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C H A P T E R

1 C H A P T E R

Introduction

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The Origin of Life: Microcosm Earth 2 Microcosms and Mesocosms of Aquatic Ecosystems 5 Restoration of Damaged Ecological Systems 8 Summary 8 Taxonomic Notes 8 References 9

Substrate: The Active Role of Rock, Mud, and Sand The Solid Earth and Life 44 Chemical Relationships Between Rocks, Sea Water, and Organisms 48 The Solid Earth, Rock, and Model Ecosystems 50 Sediments and Model Ecosystems 51 Geological Storage 59 References 60

P A R T

I PHYSICAL ENVIRONMENT

C H A P T E R

4 C H A P T E R

Water Composition: Management of Salinity, Hardness, and Evaporation

2 The Envelope: Physical Parameters and Energy State

Water Structure and Characteristics 62 Ocean Salinity 63 Hardness of Fresh Waters 67 Water and Model Ecosystems 71 Algal Scrubbing and Water Composition Marine Microcosms and Aquaria 72 Quality of Top-up Water 73 References 73

Temperature 17 Water Motion 23 Tides: Simulating the Effects of Sun and Moon 35 References 41

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Contents

C H A P T E R

C H A P T E R

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The Input of Solar Energy: Lighting Requirements

Organisms and Gas Exchange: Oxygen, Carbon Dioxide, pH, and Alkalinity

Photosynthesis and Its Origin 75 Solar Radiation and Water 79 Light Absorption by Water Plants 82 Light Intensity and Plants 82 Photorespiration 88 Light and Model Ecosystems 89 Light and Physiological Considerations Summary 91 References 92

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6 The Input of Organic Energy: Particulates and Feeding Particulates, Energy Supply, and Aquatic Ecosystems 93 Inorganic Particulates 95 Organic Particulates 95 Humic Substance 97 Particulates and Aquatic Models 97 Biofilms 98 Particulate Import in Aquatic Models 100 Aquatic Ecosystem Restoration 100 References 100

Oxygen Exchange 118 Oxygen, Model Ecosystems, and Ecosystem Restoration 120 Carbon Dioxide Exchange 121 Carbon Dioxide and Global Aquatic Restoration 122 Managing Carbon Dioxide and pH in Microcosms and Mesocosms 124 Gas Exchange and Selected Model Ecosystems 125 References 128 C H A P T E R

9 The Primary Nutrients – Nitrogen, Phosphorus, and Silica: Limitation and Eutrophication Nutrients in Natural Waters 131 Eutrophication and Hypereutrophication of Natural Waters 134 Nutrients and Model Ecosystems 136 Summary 139 References 140

P A R T

C H A P T E R

II

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BIOCHEMICAL ENVIRONMENT

Biomineralization and Calcification: A Key to Biosphere and Ecosystem Function

C H A P T E R

7 Metabolism: Respiration, Photosynthesis, and Biological Loading Metabolism 105 Respiration 106 Bacterial Metabolism 110 Photosynthesis 112 Biological Loading 114 References 115

The Process of Biomineralization 143 The Carbonate System and the Formation of Calcite and Aragonite 143 Halimeda: Photosynthesis-Induced Calcification 145 Calcification in Stony Corals 146 Calcification, Stony Corals, Coral Reefs, and Global Warming 148 Calcification in Mesocosms and Aquaria 150 Coral Reef Aquaria and Stony Coral Calcification 151 References 154

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Contents

C H A P T E R

11 Control of the Biochemical Environment: Filters, Bacteria, and the Algal Turf Scrubber Sterilization Methods 156 Bacteriological Filtration 156 Reef Systems 157 Denitrification 157 Foam Fractionation (Protein Skimming) Photosynthetic Methods 158 Algal Turfs 159 The Algal Turf Scrubber (ATS™) 161 Algal Scrubbers and the Modeling of Ecosystems 165 Summary 168 References 169

Food Webs in Model Ecosystems 195 Establishment of Food Webs 196 Trophic Structure in Aquaria 201 The Organisms 202 References 202

C H A P T E R

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Primary Producers: Plants That Grow on the Bottom Benthic Algae 203 Algae in Model Ecosystems 219 Submerged Aquatic Vegetation 222 Marine SAV and Model Ecosystems 229 Freshwater SAV and Model Ecosystems 231 Emergent Aquatic Vegetation 234 EAV and Model Ecosystems 242 Plant Communities and the Restoration of Wild Ecosystems 250 References 251

P A R T

III BIOLOGICAL STRUCTURE C H A P T E R

C H A P T E R

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Community Structure: Biodiversity in Model Ecosystems

Herbivores: Predators of Plants and Omnivores, Predators of Plants and Animals

The Framework of Biodiversity 173 The Community 175 The Biome 175 Features of Communities 181 The Magnitude of Biodiversity 183 Community Structure and Ecological Models Scaling and Reproduction 186 Model Diversity 187 Summary 189 References 189

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Types of Herbivores 254 Plant Defenses 256 Modifications of Marine and Freshwater Herbivores 257 Herbivores and Model Ecosystems 263 References 265

C H A P T E R

16 C H A P T E R

Carnivores: Predators of Animals

13 Trophic Structure: Ecosystems and the Dynamics of Food Chains Energy Capture and Flow Food Webs 193

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The Carnivore Predator 267 The Prey 268 The Dynamics of Predation 269 Marine and Freshwater Predators 269 Predators and Synthetic Ecosystems 275 References 279

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Contents P A R T

C H A P T E R

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Plankton and Planktivores: Floating Plants and Animals and Their Predators

ECOLOGICAL SYSTEMS IN MICROCOSMS, MESOCOSMS, AND AQUARIA

Plankton Size and Composition 282 The Bacteria 282 Phytoplankton 282 The Planktonic Food Web 286 Mechanisms of Filter Feeding 288 Plankton, Particulates, and Model Ecosystems Wild Ecosystem Restoration 300 References 302

C H A P T E R

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C H A P T E R

18 Detritus and Detritivores: The Dynamics of Muddy Bottoms The Deep Ocean 307 Bacteria 307 Fungi 307 Protozoa 309 Meiobenthos: Protozoans 309 Meiofauna: The Multicellular Invertebrates Macrobenthos 313 Deposit Feeding in Saltwater Soft Bottoms Deposit Feeding in Freshwater Soft Bottoms Carnivores and the Detritivore Community Detritus and Its Role in Model Ecosystems References 327

Models of Coral Reef Ecosystems Modeling Coral Reef Ecosystems 344 Caribbean Coral Reef Microcosm at the Museum of Natural History 345 Coral Reef Microcosm at the Smithsonian Marine Station 353 Great Barrier Reef Mesocosm 353 A 130-Gallon Reef Microcosm 356 Summary 368 References 368 C H A P T E R

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C H A P T E R

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A Subarctic/Boreal Microcosm: Test of a Biogeographic Model The Rocky, Embayed Coast of the Northwestern Atlantic Geological History 371 The Gulf of Maine 376 The Core Subarctic 387 Core Subarctic vs Mixed Subarctic/Boreal 393 A Maine Shore Microcosm 395 An Opportunity to Test Biogeographic Theory 403 References 404

Symbionts and Other Feeders C H A P T E R

Zooxanthellae and Their Animal Hosts 329 Biology and Ecology of Corals 332 The Positive Feedback Loop between Photosynthesis and Calcification 334 Anthozoans and Microcosms, Mesocosms, and Aquaria 335 Parasitism 336 Environment, General Health, and Disease 337 Biodiversity 337 Quarantine (Prevention of Transmission) 337 Disease Treatment in Model Ecosystems 338 References 339

22 Estuaries: Ecosystem Modeling and Restoration Where Fresh and Salt Waters Interact 405 Chesapeake Bay in Mesocosm 406 A Florida Estuary in Mesocosm 416 Nutrient Dynamics in Estuarine Models 439 Estuarine Restoration 439 References 441

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C H A P T E R

23 Freshwater Ecosystem Models A Florida Everglades Stream and Wetland 443 A Blackwater Home Aquarium 450 Restoration of Freshwater Ecosystems 452 References 452

Nutrient Removal from Agricultural Wastewaters (Nonpoint Source) 474 Nutrient Removal from Rivers 479 Bioenergy and Solar Energy Recovery Using ATS Systems 480 Aquacultural Wastewaters 481 Industrial Wastewaters and ATS Systems 484 References 489

P A R T

P A R T

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SUMMARY

THE ENVIRONMENT AND ECOLOGICAL ENGINEERING

C H A P T E R

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24 Organisms and Natural Products: Commercial Ecosystem Culture The Aquarium World 458 Pharmaceutical Culture 462 References 463

C H A P T E R

25 Large Scale: Water Quality Management with Solar Energy Capture The Quality of US Surface and Ground Waters 467 Nutrient Removal from Domestic Wastewaters 468

Microcosms, Mesocosms, and Macrocosms: Building and Restoring Ecosystems, a Synthesis Principles of Ecological Modeling 494 Ecosystems in Home Aquaria 498 Applied Model Ecosystems 499 References 499

Index

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Preface

top priority of all human society. It seems highly unlikely, no matter what our scientific and technical prowess, that humans can survive on this planet, with our few domesticated species, in the midst of a radically altered atmosphere and hydrosphere and a dysfunctional biosphere. It is most discomforting to hear of new plans to purposefully inject pollutants into the stratosphere, to act like a volcanic eruption, or to spray iron dust on the oceans, hopefully to increase photosynthesis, and thereby, at least temporarily, reduce global warming effects. Why is it that so much of our educated humanity cannot conceive of working with our biosphere, using processes that we know well, to solve multiple environmental problems? Ranging from the domestication of a few wild species by chance beginning 10 000 years or more ago to that by design in the last few centuries, human efforts to extend utilization of our biosphere beyond hunter-gathering have almost always been at the level of an individual species. Limited polyculture, as farm ponds, is practiced in some countries, and in the latter half of the 20th century “permaculture,” following some ancient practices on land, advocated polyculture; however, by and large, our domesticates remain monocultures. Compared to the global biodiversity (even the already greatly reduced biodiversity of today), the numbers of domesticated species remain vanishingly small. The intensive management of farms and aquacultures provides one of the most extensive elements of coastal and oceanic pollution and wild ecosystem loss. Unfortunately, especially in western cultures, it remains deeply ingrained that only by optimizing all aspects of single species culture, often at great environmental cost, can we hope to support current human populations. It also does not help that most economic models call for ever-continuing growth, when this is clearly the root of our failure to meet environmental problems. This book focuses on efforts to interact with and effectively “domesticate” at the ecosystem level, to build experimental ecosystems to learn, and to undertake ecological engineering, as interaction with “wild” ecosystems. Ultimately, we propose to optimize biogeochemical function and biodiversity, and to reform

By the mid-20th century, widespread concerns were being expressed for the way in which modern human populations and their industrial endeavors and products were affecting both the environment in which they lived and the planet’s wild populations and their ecosystems. Some predictions for the future were dire, and enough environmental activism developed so that some of the more conspicuous problems (e.g. raw sewage, oil spills, DDT, PCBs, chlorofluorocarbons, and atomic power radioactive materials) were subsequently ameliorated or at least subject to management (though never fully corrected). However, the larger, more widespread, and chronic effluent problems of human society (e.g. nutrients, CO2, and moderately toxic hydrocarbons) have continued to expand their reach into every corner of the biosphere, atmosphere, and hydrosphere. The ever-growing global human population, the continuing process of habitat destruction, and the ever-expanding desire of that population for a western lifestyle, rich in fossil energy use and synthesized products, using abundant raw materials, suggest that these problems, already built up over a century or more, and now growing geometrically with population expansion, are not going to be so easily ameliorated. Atmospheric CO2 increase, with its concomitant global warming, already seems beyond correction to a large percentage of scientists, engineers, and educated public. Yet, the degradation of our natural waters, and especially our oceans, the latter being of considerably greater mass than the atmosphere, is slower to be recognized; and orders of magnitude more difficult to correct. In many coastal waters, decades of environmental effort backed by large financial expenditures have failed to prevent a continuing and serious reduction in water quality. Although, in many countries, regulations to contain the widespread pollution of the atmosphere and natural waters have been initiated, habitat destruction continues and increasing population and advancing prosperity have overcome most efforts to stem the tide of environmental degradation. As some writers have so succinctly stated, we are slowly beginning to stew in our own toxic brew. We are hardly alone in expressing our grave concern for the future of the human race if the full understanding and correction of these issues does not become the

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our relationship to our biosphere. As we explain in this book, symbiosis has been a critical part of organic evolution. Likewise, humans have formed a number of symbioses with plant and animal domesticates. Some very influential and critical scientists have recognized that the human symbioses collectively called farming have been a mixed blessing for the human race. Nevertheless, current human populations are demanding an everexpanding intensive global scale farming that typically uses monocultures to optimize a single return; usually this return is biomass for food, materials, and, more recently, energy. However, the human race also requires ecosystem/biosphere level atmospheric and hydrospheric cleaning, soil structuring services, and general biogeochemical stabilization that our farming symbioses do not and probably cannot provide. Global warming is only one example of human overpowering of those global ecosystem services. As we describe in depth in this book, the experimental study of living ecosystems can lead to “domesticated” ecosystems that are far more efficient at solar energy capture than farm monocultures, without providing the inevitable environmental degradation of those monocultures. We demonstrate that use of such systems can clean up much of the damage already visited on our planet. Significantly increased energy and materials conservation is essential to current and future generations. While this has been locally necessary in the past, as many communities and even civilizations have found out to their detriment, our great numbers and increasing individual requirements have now expanded the conservation requirement to a global level. Unfortunately, we are unlikely to achieve the level of conservation needed to stop the global warming “steamroller,” and ultimately coastal and oceanic depletion, unless we expand the scale and depth of our photosynthetic symbioses to both the landscape and the ecosystem level. Some environmentalists will find the thought of domesticating high-diversity, high-efficiency ecosystems as undesirable, perhaps even encouraging human society to neglect conservation and population reduction. Indeed, this is a potential dilemma. However, even if a broad spectrum of human society could be brought into an extensive conservation mode, the inertia of global population and degradation provides environmental problems that are realistically beyond a simple conservation solution. In the earlier editions of this book, we presented a methodology for re-creating functioning wild aquatic ecosystems for research and education. The underlying philosophy centered on the notion that many of those ecosystems remained in the “wild state” and that it was possible to re-create or model them experimentally. Clearly, there is a broad gradient of ecosystem

degradation, and the waters of the Baltic Sea and Chesapeake Bay are considerably more altered than those around Tierra Del Fuego. However, as we shall point out in our following text, numerous studies and reports declare a global scale alteration of species and community function that is likely to continue and deepen. We have written this 3rd edition on the basic premise that most aquatic ecosystems are no longer “wild,” being subject to significant and negative unplanned and uncontrolled human effects. We now must treat wild ecosystems as controlled systems that must be managed, and human effects ameliorated, just as in our “captive” ecosystems. We have expanded our earlier treatment of “Building Living Ecosystems” to “Building and Restoring Living Ecosystems,” applying much of the original methodology, where appropriate, to “wild” systems management. We show that largescale ecosystem cleaning of human pollution, using solar/algal techniques, can also provide considerable usable energy to replace the fossil fuel use that is responsible for much of the global environmental degradation. Just as we have organized in the past to industrialize, we must now re-organize to more fully integrate with the Earth’s biosphere while switching to renewable energy sources. It has been 15 years since the 1st edition of Dynamic Aquaria was completed; it has gone through several printings, and the response, especially in the academic and professional world, has been quite favorable. Some of the model or controlled ecosystems described in the 1st edition are still in operation. One system, with its mechanical–electrical systems re-built, has now been in operation for over 25 years. A few have been extensively researched, and we can now report in depth on their function. Those long-term systems that have been carefully studied have shown complex community and trophic structuring and extraordinary biotic diversities based on reproductively maintained populations. The scientific context in which our approach to living systems modeling has developed has changed significantly. In the year Dynamic Aquaria was first published (1991), the journal Ecological Engineering also appeared. It has now completed its 15th year and has published over 500 articles. Several scientific studies describing the approaches of other scientists to living systems modeling have also appeared during the same time frame, and more peripherally, but of considerable interest, the Society and journal Restoration Ecology have matured. In the public display/education arena, the Smithsonian exhibit conveying the principles of ecosystem operation to the public at large has now moved to and become the “Smithsonian Marine Ecosystems Exhibit” at Fort Pierce, Florida. However,

Preface

very few large public aquaria built during the past 20 years, unless adjacent to a good and abundant source of high-quality water, have chosen to take an ecological route – for most, the graphic design and artistic backdrop may be ecologically oriented, but the organisms displayed are specimens isolated from a real ecology. This is most unfortunate, because it is only with broader public understanding that the massive loss of diversity, so characteristic of today’s biosphere, can be halted. This must be accomplished through stewardship of the environment and the ecosystems in which organisms live by most of our population. The concept that species can be saved one by one at best applies only to mammals and a few birds and fish, if at all. Finally, the hobby world of aquaria remains in ferment with ideas that still exceed the funding capability of scientific and information systems to test and convey reality. Unquestionably, many new “hobby” techniques, both those tested in the garage and those provided by enterprising businesses, are increasingly capable of culturing many species under optimum conditions of growth and sometimes reproduction. The recent Reef Aquarium “bible” by Delbeek and Sprung is a shining example of progress in the hobby. However, hobby systems mostly remain polycultures, and real ecosystems, consisting of diverse communities of organisms in an environment approaching that of a wild analog and processing energy and nutrients through food webs, are rare. In this edition, we greatly expand on the use of ecosystem modeling techniques to clean natural waters and the atmosphere. We also show how large rivers, bays, and even the ocean and atmosphere can be managed in a far healthier state, and kept that way, if we will only adapt a more conservation-minded and ecosystem-centered approach to the human future. We briefly discuss a critical area of aquatic ecosystem modeling that is especially ripe and far overdue for development, namely systems for identification and extraction of pharmaceutical drugs already developed by a host of wild species. In our anthropocentric arrogance, humans tend to conclude that with our brains, tool use, and language we are far beyond other organisms. Humans have long thought of harnessing a few animal species to “work” for us, and have tried to co-opt the energy storage of a number of plant species; however, for many, most life is thought of as useful only to “tree-huggers” and in the way of our “progress.” We tend to forget the story of penicillin, and the parallel stories of many lesser known drugs. Up to a half century ago, serious bacterial infections often meant death or dismemberment. Then we learned of and eventually co-opted the chemical “invention” of penicillin by the fungus Penicillium. Of

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the many millions of species in the world, most have evolved chemical/ mechanical systems that are of potential use to the human race. Yet, we are forcing them into extinction at ever-increasing rates, every day losing forever invaluable information. Maybe one day we will know so much about genetic codes and cellular and organism development that we can create de novo any organic possibility; and, on the other hand, maybe that day will be as far away as atomic fusion and artificial photosynthesis. In the meantime, it behoves the human race to develop as many symbioses with species and their ecosystems as we can manage. We are an integral part of organic evolution and organic complexity. If we try to escape that fact, a fact as deeply and broadly based as any of our scientific and engineering knowledge, and a narrow parasitism of a few species, the rest be damned, we are likely to commit ourselves to early extinction. Multimillions of species in the past have failed to adapt and traveled that well-worn route. Sooner or later, an astronomical event may well cause our extinction. However, we will just as likely survive a few more million years if we will use our intellect to adapt to the reality of our base in organic evolution. This edition is divided into five broad sections, each containing two to seven chapters. Most chapters begin with a review of the subject matter relative to the larger picture of ecology, ecosystems, and the Earth’s biosphere as a whole. Part of our appreciation of the complexities of smaller ecosystems comes from understanding the more universal context in which all ecosystems operate. Where appropriate, the remainder of each chapter deals with the building of microcosms and mesocosms of ecosystems for research and also gives examples of the unique aspects of small home aquarium systems. Finally, where appropriate, we discuss how the information presented relates to the larger concern of environmental restoration. Part I discusses the physical environment, elements of which at the ecosystem level have often been misunderstood by environmental scientists and ignored by aquarists and hobbyists. We discuss our further understanding of the shapes, material, and construction of the envelope that will hold various size aquaria; the temperature, water composition, and motion; solar energy; and the substrate, or rock, mud, and sand, that makes up the floor of the system and in part provides for all critical geological storage. We also examine the critical role of suspended particulates, inorganic and organic, in aquatic ecosystems. Since it is based in the physical factors discussed in this section, we also present a biogeographic model for the world’s ocean coasts. Much ecosystem modeling is likely to be carried out within the framework of this model.

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In Part II, on the biochemical environment, we discuss the mechanisms of gas and nutrient exchange, as well as the management of animal wastes in small models. We particularly examine “ecosystem metabolism” contrasting the interlocking functions of plants with animals needed for the successful operation of these dynamic ecosystems. We continue to describe our primary means of controlling the biochemical environment by using managed communities of algae, and to thereby achieve the simulation of larger volumes of open water and where appropriate export to other communities or geological storage. Because biomineralization, especially calcification, represents an internal sink and needs special treatment in semi-closed ecosystem models, we provide a chapter reviewing what is known about this complex subject, and we relate this to the management of controlled ecologies. One of our longerlived coral reef models was used to extensively research this subject. Much of this has been published in scientific journals, and the basics are presented in Chapter 10. The ecosystem concept remains a subject of animated scientific debate. However, most scientists would accept for a definition something approaching “diverse communities of organisms, supported and constrained by a given physical–chemical environment, interacting to capture and process energy and nutrients in food webs.” In Part III, we deal with the organisms, their diverse communities, and their food webs. It has been clearly and repeatedly demonstrated that given a reasonable facsimile of the wild environment, with appropriate imports and exports, and a diverse mix of introduced species of the wild biota, the species of ecosystem models will self-organize communities and food webs to process energy and nutrients. Finally, in Chapter 19 of Part III, we introduce symbiosis, and discuss the considerable role that this process has played in organic evolution. As humans continue to push other species “out of our way” and drive ever more of them into extinction, it is essential to remember that a symbiosis or joining together of organisms has often provided a highly successful evolutionary strategy. In Part IV, we present case studies of numerous microcosms, mesocosms, and aquaria. Treatment of the Florida Everglades Mesocosm and the authors’ 14-year-old 130-gallon coral reef is greatly expanded

commensurate with the many years of extensive monitoring data now available. Calcification and biodiversity investigations of the latter, 130-gallon coral reef system, are covered in Chapter 20. Efforts are now under way to apply the concepts presented in this book to commercial-scale culture of organisms and the production of human food. Both concepts will assist in protecting endangered wild communities by greatly reducing wild harvest. Both concepts will circumvent the increasing tendency for wild harvests to lose their economic viability. Equally important, the basic water quality control methodologies described in this book are applicable to relatively inexpensive and high-quality treatment of a broad spectrum of both human wastewaters and the streams, rivers and bays, as well as coastal waters that are impacted by those wastewaters. In Part V, we describe some of the ongoing efforts to make these endeavors commercially viable and environmentally successful at large scale. HydroMentia, Inc. of Ocala, Florida, provides the principal commercial effort to expand these methodologies to landscape scale. Some of HydroMentia’s engineering processes are proprietary, including the use of ATS™ for phosphorus and heavy metal removal. Commercial endeavors should examine the HydroMentia organization website and contact their representatives for further information. Finally, in Part VI, we present a series of principles for establishing and operating living ecosystems. This is where the real scientific learning process begins, in reducing our endeavors to core concepts, each of which we strive to better understand in the framework of the ecological function of the natural world. Most important, we come to understand that the key element to success lies in boundaries, the open end of the definition of an ecosystem. No ecosystem stands alone. Understanding the conditions at the boundaries, the imports and exports, knowing which species must be simulated by human action because scaling factors effectively place them across the boundaries, and, finally knowing where to draw the boundaries to make the modeling effort practical, will determine the magnitude of success. Restoration of human-impacted wild ecosystems differs primarily in scale; the concepts are quite similar.

Acknowledgments and Dedication It has been nearly 30 years since we initiated the development of the concepts presented in this book and began the long process of R&D that produced the very promising array of ideas and working systems now in motion. For those who will open their eyes and minds, we speak of the methods of a new rapprochement with nature. A generation ago, neither the method of experimenting with captured ecosystems nor the concept of learning from, and then “domesticating” ecosystem processes was widely accepted either in the aquarium hobby world or in the science and ecological engineering communities. As exhilarating as these years have been for us, they have not been without physical, emotional, and financial struggles, especially for our far-flung families, students, colleagues, business associates, and financiers. So many people have helped us, we are losing count, and here we can single out only those who were strikingly important in more recent years. We apologize to the far more numerous helpers and facilitators that we do not specifically mention but without whose assistance the accomplishments we present would be far more limited. The contributions of many of these individuals are mentioned in the earlier editions. To all the members of our families, who have inevitably lived with Dynamic Aquaria and its precedent research for decades, we thank each of you for your patience (and guidance). Special tribute goes to Nathene Loveland, Karen’s mother for her encouragement in initiating the R&D endeavor, and for her enthusiasm and multifaceted support, and to Walter Adey Sr., Walter’s father, for a guide to life that lives on. Science and engineering is meant to be questioned, tested and re-tested, but the road of true progress can be long, convoluted and tiresome. To our numerous students and assistants, the energy of youth always made up for whatever we lacked, and we are deeply conscious of the gratitude we owe you. We are especially indebted to our longtime friend, colleague, and student, Sue Lutz; she came to our rescue, to help us meet the various deadlines, while we needed to be on our research vessel in the Canadian Maritimes; without her multifaceted talents we could not have completed this edition. In recent years, Allegra Small and Don Spoon additionally provided the dedicated support that was a requirement for success, and while our colleagues

have been many and their wisdom and effects are always helpful, Pat Kangas has been ever behind the principles and broader goals. And among our long time friends, Susan Bradley has always been ready to come to our rescue, whether for a creative design or technical computer problems, while Addie Moray and Mary Ellen McCaffrey gave unselfishly of their time for some of the administrative tasks. We say again, a book must teach, and while text is paramount, a picture is ever “worth a thousand words.” Again in this edition, photographers Nick Caloyianis and Clarita Berger worked their superb magic to provide what only photography can convey. The erratic path to knowledge in natural history science is, in the end, ever exciting, and because of the “ivory tower” environment in which it is carried out, we would not wish to lose a moment of it. The applied world, and finding the funding to make it happen, can be more brutal. To those engineering colleagues and financial and business associates who have not only traveled with us in our efforts to bring the solar energycapturing and water and atmosphere cleansing process of ATS to a very needy world, but also have picked up the ball and run up-the-mountain when we have tired, we feel a gratitude and comradeship that is inexpressible. At a time when algae was still a bad word, a cousin to red tide and the failed food promise of the 1950s, Don Panoz and Richard Purgason started the ball rolling with Aquatic BioEnhancement Systems. We are especially indebted to the HydroMentia crew, especially Whitcomb and Margaret Palmer on the business and financial side, and Allen Stuart and Mark Zivojnovich on the engineering side. The engineering innovations and managerial devotion of the HydroMentia staff to solving these serious environmental problems is extraordinary by any measure; HydroMentia picked up the ball when it was slowing and we are now approaching the goal posts, at least the ones most visible in the fog of time. Whit especially had the vision, interest, and resources to take the chance on this journey, even when the walls in the fog soared out of sight. We are particularly grateful to both Mark and Allen who provided their consistent support in supplying editing, current data and information for this edition. Above all, we thank all of you for your friendship and

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Acknowledgments and Dedication

ongoing, stimulating interchanges and discussions. HydroMentia, this edition of Dynamic Aquaria, is dedicated to you. Organism culture, by sustainable and non-polluting means, is essential to our future use of organisms from our hydrosphere. However, the “tragedy of the commons” haunts us, and as long as there are “fish in the sea”, the ability to make this shift will be illusory. On the ornamental culture side, we have to take our hats off to Morgan Lidster for his “green thumb.” However, the financial mountain was overpowering, and we now put our hopes in SeaQuest of Utah for further motion in this very challenging arena. Finally, we thank our publisher Dr. Andy Richford, Senior Acquisition Editor, Life Sciences Books of Elsevier and Academic Press in London, for providing us the opportunity to expand and broaden our scope in this edition, and for the unending enthusiasm and encouragement of the Elsevier/Academic Press staff,

especially Melissa Read, Project Manager, of Elsevier Book Productions in Oxford, England, Gregory Harris, the Designer for Elsevier, who stuck with us to create a new cover design, and Pat Gonzalez of Academic Press in San Diego, who helped guide us in the initial process of this endeavor. The global environment is under siege by an exploding human populace driven by pre-historic genes. However, we can think and reason; we are not the deer, rabbits, and lemmings who cannot know they are destroying the environment that they depend on and are heading for population collapse. We can learn and respond to the challenges. We surely must try, because, with our technical prowess and global influence, humans will hardly be alone in this collapse. We salute all of those who have helped us, and often carried us on our way; we think the ideas expressed herein will help in our “coming to terms” with the realities of nature.

C H A P T E R

1 Introduction

This book presents the process of building, managing, and restoring living aquatic ecosystems (in microcosms, mesocosms, and macrocosms) and its background, rationale, status, and future. We argue that there is no qualitative difference between a rationally constructed ecosystem in microcosm and mesocosm and that in a macrocosm. In this book, we use the term macrocosm for a wild ecosystem that has been altered or constrained by human endeavor. Human constraints are largely degrading in effect because they have mostly been performed with little concern for the continued function of the ecosystem. However, they can be constructive, such as a scientific or restorationist effort at repair, revitalization, and even optimization. There has been a tendency on the part of some scientists to regard the modeling of living ecosystems as impossibly complex; that is, they view true ecosystems as beyond human construction. The tendency in mesocosm research today is to restrict efforts to a few species interactions, to keep control and limit the variables, but producing a result that most ecologists would hardly accept as an ecosystem. In the aquarium world, the feeling is widespread that total control over very limited diversity (gardening rather than ecology) is necessary to achieve anything but an explosion of weeds and parasites. Yet, as we shall discuss in this book, since the first edition was published, it has been possible for many years to operate in “aquaria” the most complex ecosystems in the sea, coral reefs; these microcosms of a few cubic meters, behave chemically as wild reefs, and have a biotic diversity per square meter exceeding that known for the wild. Similarly, we demonstrate the ability to produce whole estuaries, for periods of up to a decade, with much of their biotic complexity intact. These estuaries were first attempts and the future bodes well for those willing to move on to larger, more sophisticated, systems. We are not alone

in these endeavors and concepts (e.g. Osmond et al., 2004). However, critically important at this juncture, Petersen et al. (2003) have had the resources to demonstrate a scaling rationale that demonstrates veracity thresholds. In general, as might be expected, larger models can more accurately depict the function of their analog. However, as Petersen et al. (2003) demonstrate, large microcosms and moderate-sized mesocosms have already begun to pass those thresholds; and we expand that concept by greatly increasing the biodiversity and ecosystem linkage of these models. In our view, no longer are there aquatic ecosystems (including the oceans) on planet Earth that have not been significantly altered directly or indirectly by human activities. Many species have been driven to extinction, some as large as the Steller sea cow, and many more have had their ecological role greatly reduced and whole ecosystems altered (e.g. the North Atlantic codfish). Many fresh and coastal waters have been radically altered, some to a nearly “dead” state (e.g. upper Chesapeake Bay); even the open oceans have been degraded by food-chain concentrated toxic compounds that have rendered some organisms infertile and others subject to organ malfunction and cancers. Finally, simply to encompass what would be a very long list, a global girding biome, coral reefs, are facing drastic reduction, if not practical extinction. It has long been accepted by ecologists that ecosystem supports are critically important to the survival of human societies; the advent of concern for the effects of global warming, and the clearly impending collapse of our access to clean water has spread the ecosystem support concern far more widely. We feel that much of the ecosystem damage can be corrected, and our basic standard of living maintained if we greatly increase our efforts now. We have the tools, but time is running out for their application.

1

2

1. Introduction

We start our discussion by demonstrating that the development and evolution of life is very likely an inevitable part of the chemistry of the universe. We demonstrate that the definition of an ecosystem becomes a functional reality given the right physical/chemical (i.e. ecologically engineered) framework, and an appropriately inserted, food web-based collection of species. In this scenario, inserted organisms self-organize into a community of species interacting to process energy and nutrients through a complex of food webs (i.e. an ecosystem). Since no ecosystem stands alone, the key element becomes understanding and re-creating the boundary conditions, the imports, and the exports. The ecosystem is the most complex end-point of biotic evolution, and when the experimental method is applied, and disassembly and reassembly utilized, progress in understanding is most rapid. Scaling becomes our primary difficulty in modeling, because almost by definition, some species are too big or wide ranging for microcosms and mesocosms and others have been fished out or otherwise damaged in macrocosms. We need to know enough about these ecosystems to interact with them to replace or provide the effects (e.g. grazing or predation) of the missing species; the process is continuously heuristic. Because we are inextricably enmeshed in our biosphere and its ecosystems, and because we process global-scale quantities of energy and nutrients, human endeavors must seriously consider the effects those endeavors will have on our ecosystems and how they can be ameliorated. Microcosms and mesocosms are ideally suited for this task (see also Osmond et al., 2004).

THE ORIGIN OF LIFE: MICROCOSM EARTH The four most abundant chemical elements (99%) of most living organisms, by number of atoms, are hydrogen, oxygen, carbon, and nitrogen. The elemental composition of the universe (Figure 1.1) compared to that of the crust of the Earth (Figure 3.6) suggests that living organisms have more in common with the universe as a whole than with the Earth alone. Even the relative proportions of these elements are about the same in living organisms as they are in the universe (although hydrogen is lower), but very different from that in the Earth’s crust. Including the oceans (which are one-sixteenth the mass of the crust) with the crust, in this elemental analysis, has very little effect on the relationship. In the Earth’s crust, by weight, oxygen, silica, aluminum, and iron, followed by sodium, magnesium, potassium, and calcium, are far above the very small percentages of hydrogen, carbon, nitrogen, and phosphorus. If the whole Earth is considered (as an estimate), the big four, at 93%, are iron, oxygen, silica, and magnesium.

In addition to the millions of stars in our galaxy, composed mostly of hydrogen and helium, there are enormous masses of interstellar gas and dust. This interstellar gas and dust is enriched in the heavier elements formed in the cooling, nuclear furnaces of dying stars and then blown into space in supernovae. The prevailing chemistry in these interstellar regions has been called an “organic cosmochemistry” (Oró, 1994). It has been shown that the numerous hydrogen, carbon, nitrogen, and oxygen compounds, identified both in interstellar space and in the comets and meteorites that arrive on Earth, can be abiotically combined in the laboratory to provide water and a number of critical pre-biotic compounds (Table 1.1). A large proportion of cometary material is frozen water and some scientists have demonstrated that the volume of incoming comets has been more than sufficient to provide the Earth’s oceans (Frank and Huyghe, 1990). “Furthermore, a large array of proteinic and nonproteinic amino acids, carboxylic acids, purines, pyrimidines, hydrocarbons, and other molecules has been found in the relatively primitive carbonaceous chondritic meteorites” that have landed on Earth (Oró, 1994). Most theories of the origin of the solar system (e.g. Brown et al., 1992) start with condensation out of a solar nebula. In these models, the inner planets (including Earth) had all of their volatiles (including the principal elements and molecules of life) blasted out of them by the sun as they formed. Newer concepts of the formation of the Earth–Moon system (e.g. Redfern, 2001), mostly evolve around the impact of a Mars-sized object with the early Earth, resulting in the Moon being ejected with many of the planetary dynamic characteristics (orbit, spin, and wobble) formed or altered by the impact. In either case, the Earth started as a rocky “cinder” (like the planet Mercury today). It became revitalized with oceans and gases, most likely, from cometary and meteorite introduction. We now know that at the outer margins of the solar system, there are a large number of ice objects that form the Oort Cloud. These provide the comets that are sometimes perturbed into the inner solar system, where they can impact the planets bringing water and organic compounds (Redfern, 2001). The key to the next step was a planetary mass and temperature environment in which the already omnipresent water components could be present in their liquid phase. While this may have happened on Mars and Venus as well as on planet Earth, it is only on Earth that the conditions for life have remained for 4 billion years. Later cometary and asteroid impacts snuffed out some of that life when they impacted, but so far none have reset the life clock. Chemically, water is a most unusual material. By accepted physical/chemical rules, under normal

The Origin of Life: Microcosm Earth

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FIGURE 1.1 Relative abundances of the chemical elements in the universe (based on silicon as 104). Note that except for the very unreactive helium, the three most abundant elements of life are the same as those in the universe with the critical nutrient nitrogen next in line. From The Biological Chemistry of the Elements by Fraústo da Silva and Williams (1993). Reprinted by permission of John Wiley & Sons, Inc.

pressures, one would expect this ubiquitous compound to exist only as a solid or as a gas, depending on temperature. However, due largely to the polarization of individual water molecules and the tendency of this

compound to form a “semicrystalline” liquid at moderate temperatures, water appears in its most familiar liquid form over a relatively wide temperature range. At the same time, it becomes a “universal” solvent.

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1. Introduction TABLE 1.1 Biomonomers, Biopolymers, and Chemical Properties That Can Be Derived from Interstellar and Cometary Molecules Molecule Hydrogen Water Ammonia Carbon monoxide (Linear nitriles) Formaldehyde Acetaldehyde Aldehydes Hydrogen sulfide Hydrogen cyanide Cyanacetylene Phosphate* (PN) Cyanamide

Formula H2 H2O NH3 CO (H2) H(C)nCN CH2O CH3CHO (CH2O) RCHO (HCNNH3) H2S ( as above) HCN HC3N ( cyanate) PO3 4 ( nucleosides) H2NCN (condensation)

Biomolecules and chemical properties Reducing agent Universal solvent Catalysis and amination Fatty acids (Fatty acids) Ribose and glycerol Deoxyribose Amino acids Cysteine and methionine Purines (e.g. adenine) Pyrimidines Mononucleotides (e.g. ATP) Biopolymers: peptides and oligonucleotides

* Detected in interplanetary dust particles of possible cometary origin and in meteorites. From Oró (1994). Reprinted by permission of Cambridge University Press.

Almost every chemical element that occurs in the Earth’s crust dissolves in water, ultimately finding its way into the sea. Water also has one of the highest capacities of any compound for storing and exchanging heat, and it has great surface tension. Thus, this almost miraculous material is a basic stabilizing element, resisting temperature variations. Most of the above are debated only in the details by scientists today. The critical step, from simple organic molecules, abundant in the colder parts of the universe, to life is where the debate lies. Indeed, this may have not been a step, but rather a flickering, on-and-off process, happening millions of times before taking hold. Was it enough that physical energy inputs, whether from lighting at the surface of the sea or hydrothermal energy at ocean spreading centers (van Dover, 2000), into the primitive ocean soup (water plus simple inorganic compounds) created the next level of complexity of organic compounds? This has been repeatedly accomplished in the laboratory. It may be that anywhere in the universe, except near stars, when the temperature is right and water is liquid, then the organic soup is ready to brew. Water has a tendency, because of its surface tension, to create membranes and “bubble” structures. Lipids, present among the universal, simple, organic compounds, spontaneously accumulate on these “bubbles” to form membranes and cellular structures. This can be abiotically accomplished in the laboratory (Hanczyc and Szostak, 2004). Membranes can isolate, structure, and locate organic reactions making them more efficient than they would be in the greater “soup.”

Thus, while it seems that cellular structures with simple organic compounds would be just “everyday” chemistry in a pre-biotic world, is there an “external” information component required to kick-start life from there? Very long polymers, strings of smaller organic molecules, are the everyday “magic” of organic chemists and industrial plants today, but they are also part of the critical stuff of life. Some scientists would have it that the ordered, endlessly replicating structure of inorganic clay minerals could provide a template against which many simple organic compounds could become polymers. This can be done in the laboratory, and it is an intriguing idea that in the pre-biotic world this is where carbon and silicon chemistry come together. Carbon and silicon are chemically similar, as elements: they form multiple bonds with themselves and many other elements – silicon, one step up on the periodic table, is roughly twice as heavy as carbon. Could it be that silicon, the key chemical element in the crust of cinder Earth, and carbon, coming with water from the cold outer solar system to bring potential life to a later, temperature-moderated Earth, provided the next step up the ladder to full-blown life? In the contact between the primordial water, rich in a wide variety of simple organics and cellular bubbles, and abundant clay minerals formed from erosion of rocks, polymers could have formed from all the types of simpler organics, including nucleic acids. Possibly formed in much the same way, RNA is the basic message carrier of life today, and could well have preceded DNA. This is the so-called RNA world that some researchers see as an essential phase (Orgel, 2004).

Microcosms and Mesocosms of Aquatic Ecosystems

Such RNA in the ammonia, carbon dioxide rich and anaerobic early world, could theoretically exist and replicate itself, becoming more complex, based on natural selection. Eventually, the RNA molecules would have found themselves inside developing cellular bubbles, where they could have co-opted those structures, to spontaneously produce what one would have to call life. This very basic life probably began “soaking up” the organic chemicals of the soup. However, until regular energy sources and a means of synthesizing carbon and nitrogen compounds from CO2 and NH3 (and eventually N2) were tapped to bring reproduction and growth together, the future of this “life” had to be uncertain, and perhaps frequently snuffed out. Eventually, several pathways for fixation of carbon and nitrogen evolved in what could be called primitive bacteria, leading to the highly successful Calvin cycle of cyanobacteria (Raymond, 2005). Tied to solar energy capture by the early photosynthetic bacteria, some 3.5 billion years ago, life became firmly established on Earth. From there, with occasional disruptions, as large comets and asteroids continued to arrive, life was on its way to creating the modern, complex Earth, so fully integrated, at least from its crust to the atmosphere, with life. Today, the overwhelming geochemical evidence is that cellular life formed very quickly in the pre-biotic soup (at 3.6–3.8 billion years ago) within at most a few hundred million years of the formation of a liquid ocean on Earth (Gedulin and Arrhenius, 1994). Furthermore, it is difficult not to conclude that life will form quickly (on a geological scale) anywhere in the universe where the physical conditions for liquid water develop (National Research Council, 1990). The Gaia concept was popular several decades ago and has now faded. The basic premise of Gaia, that some life made more life easier, even possible for more advanced life, is certainly correct. The primordial soup was necessary for the development of cellular systems and the earliest molecular complexes that could be called life. The early bacteria that survived on the soup were a necessary condition for photosynthesis and eventually the symbiotic incorporation of photosynthetic bacteria into early protists to greatly expand the process of pulling CO2 out of the atmosphere and replacing it with oxygen. And so on it went to life on land, eventually to primates and humans. Whatever is to be made of these arguments about the development and expansion of early life, one thing is very clear: photosynthesis eventually came to be the key to most life on Earth. Also, it is likely that the Earth’s crust, biosphere, oceans, and atmosphere together hold more carbon than ever before because of continual outgassing of CO2 from the Earth’s mantle

5

over the last 3 billion years. Photosynthesis “invented” by early life has kept the Earth from the fate of Venus – a boiling, runaway greenhouse – by continually locking a large part of this carbon into semi-permanent storage. By releasing carbon from geological burial to the atmosphere, we are courting both human and biosphere disasters every bit as much as we were (and are) with our nuclear arsenals. Many scientists are more immediately concerned with a global warming that will disrupt many human societies creating global friction. Photosynthesis may be somewhat more effective with higher levels of CO2 (there is still much debate on this point). However, most scientists have concluded that this natural increase of photosynthesis cannot keep up with our destruction of forests and tundra and the release of fossil fuels carbon. Desertification and the reduction of more efficient land photosynthesis by rising sea level, with human societies putting more and more CO2 into the atmosphere in a struggle to obtain energy to survive the harsher conditions, could push us to the high temperatures and sea levels of the Cretaceous with far less land area. Perhaps then modern human societies would collapse (Diamond, 2005) and save the biosphere from a runaway greenhouse tumble. Today, all the Earth is a microcosm, or at least the concepts of microcosm, mesocosm, macrocosm, and biosphere lie a spectrum of overlapping scale. No one doubts any longer that we can affect our Earth on a global scale. The principles that we describe in this book for microcosms and mesocosms are very much the same as what we would use for macrocosms and the oceans. We cannot return to a more simple state where the biosphere can be counted on to “cover up” for us. We must quickly learn to properly manage the biosphere.

MICROCOSMS AND MESOCOSMS OF AQUATIC ECOSYSTEMS Over the last third of the 20th century, scientists in a variety of laboratories around the world have been making significant advances in keeping marine, estuarine, and freshwater organisms in aquaria-like simulations of wild environments; they have generally been referred to as model ecosystems or microcosms. Some of these become quite large, and when they exceed a few thousand gallons in water volume, they are sometimes called mesocosms. There is no sharp line between the microcosm and the aquarium. Perhaps it is best to draw the line at the point where the desire for strict ecosystem simulation is relaxed because of size, cost, or interest. The older literature on “ecological microcosms” or

6

1. Introduction

“controlled ecologies” was reviewed by Adey (1987; 1995), Adey and Loveland (1998), and Kangas and Adey (1996). Petersen et al. (2003) point out that mesocosms have become as numerous as field studies and they provide citations that would allow an extensive review of recent literature. Osmond et al. (2004) discuss the use of a very large mesocosm (Biosphere II) in the context of global climate change, and argue for the much wider use of mesocosms to understand and solve our global change problems. In the Earth’s biosphere no ecosystem stands alone. Indeed, as we noted above, the primary energy source for the biosphere itself is derived externally from the sun; the remainder internally, from the Earth’s heat. Most of the original biotic materials came from outside the Earth and, to some extent, are still arriving; the remainder derive by erosion from the Earth’s crust. External solar and lunar cycles are also important sources of information. The boundaries of an ecosystem are entirely arbitrary. However, whether carrying out pure field research or drawing boundaries for modeling purposes, drawing those boundaries so that crossboundary interchanges can be known and measured or estimated is a key to success. All ecosystems have crossboundary interchanges, and the microcosm builder must know what those interchanges are and simulate them accordingly or the model ecosystem will have little relationship with the wild analog. When modeling boundaries are established for most aquatic ecosystems, water inflow and outflow are important parameters. In many cases (e.g. coral reefs and rocky shores), where local biomass exceeds diurnal recycling capabilities, incoming water quality is crucial to ecosystem function, and when it is not possible to provide that flow from an undamaged wild source ecosystem, a water quality management system is established. There are three basic approaches to the management of water quality in aquatic models (i.e. to match the lack of highquality incoming water). One approach is abiological, in which chemical methods such as ozonation and physical methods such as physical filtration, protein skimming, and ultraviolet radiation are used to offset the effects of a poor water quality. These methods are almost always used with the second, more generalized, approach of bacteriological filtration, which is employed in various forms and has been used in virtually all aquarium systems (and sewage systems) of the past 50 years. The bacteriological (or biological) filter is a device of almost infinite variety used to maximize surfaces with bacterial cultures (i.e. bacterial films) in close contact with flowing water of the system being managed. The purpose is threefold: (1) the trapping and breakdown of organic particulates; (2) the degradation of the

universal waste products urea and highly toxic ammonia to the less toxic nitrite and thence to the least toxic nitrate; and more recently (3) either in special anaerobic chambers, or in open-aerated trickle systems, the denitrification of nitrate nitrogen to atmospheric gas nitrogen. Either separately or in conjunction with the above systems, oxygen input into the aquarium and carbon dioxide release from the aquarium are maximized to support not only the organisms being maintained, but also the essential respiration activity of the bacteria. The respiration of the bacteria in these filters releases considerable carbon dioxide, which can significantly acidify the culture. Thus, buffering with calcium carbonate in a wide variety of forms is often used. Hendal (2006) and Delbeek and Sprung (2005) provide recent reviews of these methods for aquaria. In most cases, these methods are sufficient to maintain many organisms. However, they rarely achieve the quality of unpolluted wild waters. The basic principles of bacteriological filtration (and sewage treatment) lie in the assumption that microbes have been the dominant force controlling water quality in the wild. However, this is likely to be incorrect, since far more organic material is stored in soils and geological sediments than exists in the biosphere. In addition, the Earth’s atmosphere is rich in oxygen and, prior to human involvement, was very poor in carbon dioxide. Higher plants and algae have created far more organic matter than microbes have degraded, with a concomitant production of oxygen and removal of carbon dioxide from the biosphere. Thus, plants have been and (until humans started burning coal and oil and using rivers to dump their wastes) remain the dominant force controlling Earth’s water and atmospheric chemistry and particularly the needs of higher animals. Humans assume that lack of raw materials to maximize production is a basic need that must be managed; thus, the primary requirement is rapid breakdown of all organics to basic mineral elements (carbon, nitrogen, phosphorus, sulfur, silica, etc.). We disagree with this concept. Primary productivity in the wild is sometimes limited by the lack of “nutrients.” On the other hand, excess nutrients usually result in unstable (bloom) conditions. Farming and aquaculture almost invariably add nutrients to drive productivity of a single organism. However, the result is either unstable or semistable, requiring continuous careful management to avoid a variety of “crash” scenarios. Biospheric, and ultimately ecosystem, stability lies not in the rapid breakdown of organics but rather in emphasis on their storage as either plant biomass or geological materials. Stability in the biosphere, in most wild ecosystems, and in microcosms and mesocosms must lie in competition for scarce

Microcosms and Mesocosms of Aquatic Ecosystems

resources including carbon and nutrients. In aquaculture systems designed to produce food, these requirements are reduced locally to maximize growth, but must be managed in a broader context, or they will be passed onto wild ecosystems where degradation is inevitable. It is probably best to recycle all human organic wastes, but the next best approach would be to pump them into sealed oil wells or deep mines (geological storage). Had that been done for the last century, we would be faced with neither global warming nor polluted rivers and coasts and could perhaps tap the resulting methane gas for energy. We have not taken that approach and, at this stage, we need to quickly organize to emphasize the locking up of nutrients, including carbon in plant (including algal) biomass. The third approach, which we describe in this volume, is to match an undegraded analog wild ecosystem as closely as possible with the microcosm or mesocosm of interest, in terms of physical and chemical characteristics, cross-boundary exchanges, and as many organisms, with their food webs, as possible. In some cases, especially for smaller systems, human manipulation must account for the cross-boundary exchanges of organisms that have a significantly larger territory in the wild than is available in the model. Water quality control of high biomass of benthic systems usually involves open water exchange with phytoplankton-dominated communities in the wild. We simulate this process with algal photosynthetic systems, allowing production and export or recycling of biomass (and nutrients) as appropriate. Foam fractionation, filtration, and engineered bacterial systems are not generally employed because they remove plankton and swimming or floating larvae on the one hand and unbalance water chemistry on the other. In Chapter 25, we describe several large-scale systems for the closed or semi-closed aquaculture of food fish. These systems use the same Algal Turf Scrubber (ATS™) systems described in this book for controlling water quality in microcosms and mesocosms. Technically these aquaculture operations are quite successful, and indeed one system is still operating as a commercial endeavor after 10 years. However, until truly sustainable wild fisheries, without habitat degradation, can become the rule, and a cost is levied on nutrient release from aquaculture, it will be difficult for these sustainable methods to be truly cost competitive. The hobby aquarium industry, in its public education effects, can have an incalculable positive effect on the need for public understanding of biology and ecology. Since it is “hands on” per unit effort it is probably far more effective than text book/lecture education. However, as practiced today, there are enormous losses

7

of organisms in the commercial aquarium trade. The suffering of the animals is deplorable, and there exists the very real possibility that intensive collection will deplete the environment and upset the balance of natural communities. While large numbers of plants and animals may die in the wild during environmental extremes, in general, human impacts are becoming severe enough to shift the delicate survival balance negatively for many species and even for ecosystems. For recreation and education purposes, we cannot accept subjecting organisms to stressful conditions beyond their normal environmental range. Even for research purposes, it is crucial that scientists be sensitive to the health of the organisms involved and to the potential negative impacts of collecting. Open water culture can help in some situations, and are increasingly important in coral reef culture. However, through the use of ecosystem techniques, culture systems can produce most of the organisms (and live rock) used in the aquarium trade, and distributors, dealers, and hobbyists can maintain functioning systems and reduce losses dramatically. Indeed, experimental ecosystems and their organisms can be maintained separately from wild ecosystems and endangered organisms can be nurtured for return to the wild. Zoological parks have made a strong entrance into this arena in recent decades, and now public aquaria, with sufficient financial and scientific expertise, can do likewise. Many freshwater fish have been bred in aquaria, and in the past decade increasing numbers of marine species of fish have been also. Because of our success in breeding hundreds of species of marine invertebrates and plants in our ecosystem tanks, the prognosis for greatly reducing wild collecting is encouraging, and we describe systems for accomplishing this objective. We also describe culture systems that can be used for identifying organisms that have potential for the production of pharmaceutical drugs and for initial harvest culture until the synthetic equivalents can be produced. As we have pointed out, there is already a large applied world that uses microcosms as tools for testing the fates of pollutants in wild ecosystems and hopefully developing standards for lessening pollutant loads as a result. These testing procedures use either highly simplified ecosystems or a few species without a real ecology. However, the results derived would be more applicable to the real world if the models used were the more complex systems that we describe in this book. Of equal interest, it has long been known that up to a certain level, ecosystems have a considerable capability for accepting polluting elements and degrading or detoxifying and storing them. We have much to learn from ecosystems in this respect, as we detail in Part V. However, what is most

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1. Introduction

relevant in the real world, where efficiency counts, is that knowledge gained, through models, of ecosystem processes can lead to more economic means of handling large quantities of pollutants and keeping those pollutants from degrading wild ecosystems.

(microalgae). The ATS™ was derived from mesocosm R&D, and is itself a biodiverse ecosystem that provides multi-solutions. It demonstrates the great potential of microcosm and mesocosm research, but in the solution of grave problems of mankind.

SUMMARY RESTORATION OF DAMAGED ECOLOGICAL SYSTEMS We have used the term macrocosm for wild ecosystems that have come under the significant influence of human activities and are in need of restoration to prevent loss of biodiversity and the degraded provision of “ecological services” to human society. It may be that most ecosystems on Earth are now macrocosms, but there is certainly a broad gradient between those in great need of repair and those minimally affected. There is no lack of understanding of the current, serious nature of our loss of ecosystem function and support. We cite two recent authors: Jared Diamond (2005) calling notice to the global level of ecosystem degradation that can lead to social collapse, and Robert Livingston (2006) calling notice specifically to serious aquatic ecosystem degradation. There is considerable scientific consensus that human society, in its alteration of the biosphere, is approaching a number of thresholds beyond which ecosystem supports will begin to fail and potentially cause social collapse. There are many dimensions to the loss of ecosystem supports: for example Diamond (2005) lists 12 key problems. As we discuss in Chapter 25, a number of these relate to a need to restrict human population growth and human demand for continued resources as well as the increasing number of invasive species caused by globalization (see also Ruiz and Carlton, 2003). However, better than half of the basic problems relate to water and atmospheric quality control and to fisheries. We describe in Chapter 25 how in working with numerous microcosms and mesocosms, we have identified a practical methodology for solving these problems using large-scale solar energy capture through algal photosynthesis. These ATS™ systems have already been scaled up to a module size of up to 5 acres and 40 Mgpd by HydroMentia, Inc. of Ocala, Florida. HydroMentia offers nutrient, toxics, and atmospheric carbon removal with water oxygenation and bioenergy supply as by-products at the scale of large rivers (formal designs for ATS™ systems up to 1500 acres, processing billions of gallons per day, have been developed). There are numerous other approaches to bioenergy, which are also carbon neutral, but they either add to nutrient problems (e.g. corn, soy, and switchgrass) or are monocultural in their solution

It is quite reasonable that we wish to understand in depth the complex ecosystem processes in which we are enmeshed. It may well be essential to our continued existence as a species. To develop ecosystems in microcosms, mesocosms, and aquaria, and to control their relationship to the rest of the world is simply the experimental method of science at the most complex scale of biology. The ecosystem is the exquisite potential of the universe, and we can capture it and look at it logically for understanding or for its intrinsic beauty. To build and control ecosystem models and to use the knowledge and techniques gained to restore damaged ecosystems is an essential endeavor.

TAXONOMIC NOTES As we have noted, the biological world is far more complex than the chemical world. While the core chemical elements and compounds have a standard terminology that has long existed for chemistry, the biological world remains in flux. The Linnean system has been backed up by a formal, international system for the standardization and stabilization of nomenclature, but the result is hardly stable. Some of these changes are reflected in advances in our understanding of organismic evolution, prodded on by a rapidly advancing knowledge of what is called “molecular biology,” the documentation of genetic coding. Unfortunately, some change also comes from nomenclatural wrestling. For basic reference we provide a modern “tree of life” (Figure 1.2) from Knoll (2003); the volumes of Parker (1982) can continue to fill in that framework down to family and genus. In our descriptions of microcosms and mesocosms, as one part of the demonstration of “success” or veracity of modeling of an analog wild ecosystem, we provide species lists. Since these lists were accomplished, some genus and species names have changed. In this edition, we have not “updated” these changes because it would have meant returning to the specialists that identified the flora and fauna in the first place, or in some cases finding new specialists, and this would have changed the basic function of the volume very little. In most situations, field guides will provide the older names along with their newer versions.

References

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FIGURE 1.2 Family tree of eukaryotes and ancestral bacteria (there are other, more distantly related bacteria, such as the Archaea, that are minimally shown). All of the major lines of eukaryotes, including the five major groups, had already formed well back in the pre-Cambrian, probably before the major animal groups evolved. After Knoll (2003).

References Adey, W. (1987) Marine microcosms. In: Restoration Ecology. W. Jordan, M. Gilpin, and J. Aber (Eds). Cambridge University Press, Cambridge. Adey, W. (1995) Controlled ecologies. In: Encyclopedia of Environmental Biology. W. A. Nierenberg (Ed.). Academic Press, San Diego. Adey, W. and Loveland, K. (1998) Dynamic Aquaria: Building Living Ecosystems, 2nd edn. Academic Press, San Diego. Brown, G., Hawkesworth, C., and Wilson, R. (1992) Understanding the Earth. Cambridge University Press, Cambridge. Delbeek, C. and Sprung, J. (2005). The Reef Aquarium, Science, Art and Technology, Vol. III. Ricordea Publishing, Coconut Grove, Florida.

Diamond, J. (2005) Collapse: How Societies Choose to Fail or Succeed. Viking Penguin, New York. Frank, L. and Huyghe, P. (1990) The Big Splash. Birch Lane Press, Secaucus, New York. Fraústo da Silva, J. and Williams, R. W. (1993) The Biological Chemistry of the Elements. Clarendon Press, Oxford. Gedulin, B. and Arrhenius, G. (1994) Sources and geochemical evolution of RNA precursor molecules: the role of phosphate. In: Early Life on Earth. S. Bengston (Ed.). Columbia University Press, New York. Hanczyc, M. and Szostak, J. (2004) Replicating vesicles as models of primitive cell growth and division. Curr. Opin. Chem. Biol. 8: 660–664.

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Hendal, J. (2006) Advanced Marine Aquarium Techniques. TFH Publications, Neptune City. Kangas, P. and Adey, W. (1996) Mesocosms and ecological engineering. Ecol. Eng. 6(1–3): 1–224. Knoll, A. (2003) Biomineralization and evolutionary history. Rev. Mineral. Geochem. 54: 329–356. Livingston, R. (2006) Restoration of Aquatic Systems. Taylor and Francis, Boca Raton, Florida. National Research Council (1990) The Search for Life’s Origins: Progress and Future Directions in Planetary Biology and Chemical Evolution. National Academy Press, Washington, DC. Orgel, L. (2004) Prebiotic chemistry and the origin of the RNA world. Crit. Rev. Biochem. Mol. 39: 99–123. Oró, J. (1994) Early chemical stages in the origin of life. In: Early Life on Earth. S. Bengtson (Ed.). Columbia University Press, New York. Osmond, B., Ananyev, G., Berry, J., Langdon, C., Kolber, Z., Gunghai, L., Monson, R., Nichol, C., Rascher, U., Schurr, U., Smith S., and Yakir, D. (2004) Changing the way we think about global change

research: scaling up in experimental ecosystem science. Glob. Change Biol. 10: 393–407. Parker, S. (1982) Synopsis and Classification of Living Organisms. Vols 1 and 2 McGraw-Hill, New York. Petersen, J., Kemp, W. M., Bartleson, R., Boynton, W., Chung-chi Chen, Cornwell, J., Gardner, R., Hinkle, D., Houde, E., Malone, T. H., Mowitt, W., Murray, L., Sanford, L., Stevenson, J. C., Sundberg, K., and Suttles, S. (2003) Multiscale experiments in coastal ecology: improvising realism and advancing theory. Bioscience 53: 1181–1197. Raymond, J. (2005) The evolution of biological carbon and nitrogen cycling – a genemic perspective. Rev. Mineral. Geochem. 59: 211–231. Redfern, R. (2001) Origins: The Evolution of Continents, Oceans and Life. The University of Oklahoma Press, Norman. Ruiz, G. and Carlton, J. (2003) Invasive Species. Island Press, Washington, DC. van Dover, C.-L. (2000) The Ecology of Deep-Sea Hydrothermal Vents. Princeton University Press, Princeton, New Jersey.

P A R T

I PHYSICAL ENVIRONMENT


C H A P T E R

2 The Envelope Physical Parameters and Energy State

The shape and size of an aquatic ecosystem relative to its controlling physical and energy parameters can determine the basic character of the system. This is especially true of the thickness of the water mass and its relationship to the bottom. A 100-meter-deep lake of several square kilometer surface dimensions, all other factors aside, would be dominated by true plankters, normally living most of their lives suspended in mid and surface waters, with little benthic (or bottom) influence, whereas the shallow stream or narrow lagoon of a few meters in depth is very much benthic dominated. Light enters only through the air–water interface of a water ecosystem, and the shape of the containing body of water relative to depth, as well as water turbidity, determines the basic photosynthetic vs heterotrophic (nonphotosynthetic feeding) character of the ecosystem. The direction of current flow and wave action through an aquatic system relative to the position and orientation of the communities present is critical to simulate in any ecosystem model, or else the character of the communities and the abundance of its various species will change in the microcosm or mesocosm. The all-glass aquarium, ranging from about 40 liters (10 gallons) to 1000 liters (250 gallons) is a standard and highly reliable piece of equipment in the aquarium industry (Color Plates 1 and 2). Likewise, because of its low cost and availability, every effort is generally made to use all-glass aquaria for microcosm work. Indeed, by drilling holes to attach pipes and linking all glass tanks in complex arrays, many aspects of wild ecosystems can be modeled with reasonable accuracy. We talk about the issue of scaling later, but anyone wishing to simulate the planktonic aspects of an ecosystem, not overwhelmed by the benthic communities, is likely to be seeking tanks with radii greater than

1–2 meters. The construction of molded fiberglass tanks or poured concrete or concrete block tanks sealed with a wide variety of commercially available sealants has considerable advantages for systems larger than about a thousand liters. This is also true when the mesocosm modeler departs from the purely aquatic systems and enters the realm of wetlands, marshes, and swamps, where the key species are either large individuals or the very nature of the community (e.g. a marshland) requires a large area compared to water and sediment volume. Each of the aquaria, microcosms, and mesocosms described in Chapters 20–23 illustrates the process of designing envelope (tank) shapes to fit the functional requirements of the enclosed ecosystems. Whether they are fully successful or not is limited only by the ingenuity and financial resources of the human builders (Figure 2.1). Ideally, the microcosm or mesocosm envelope would be like that of the boundary of the mathematical modeler, a theoretical boundary controlling access but not having any inherent characteristics. Of course, that is not possible, for two primary reasons. First, walls, whatever their nature (unless rather esoteric measures are used to prevent organisms and organic molecules from using their surfaces) are effectively hard bottoms. In an aquatic model of an ecosystem dominated by hard bottom communities that may not make a difference (remembering however, that especially in marine and estuarine systems that some species have larvae that must escape into the plankton for the early part of their lives). The important of the walls is less, as is often the case in an all-glass system, if the walls are frequently scraped. However, for a small model of a planktonic system, the presence of uncleaned walls may prevent the system from being plankton dominated. Second, walls of living models

13

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2. The Envelope

FIGURE 2.1 Diagrammatic illustrations of two very different types of ecosystem models (a coral reef and a mangrove/swamp sandy shore) showing spatial configurations, water movement, controls, and energy supply as well as the basic materials used in construction. Both of these models are streated in considerably more detail in Chapters 20 and 22.

consist of real materials. To some degree, they interact with the water of the ecosystem they contain. For most purposes, glass and many plastics are ideal in this respect. There are few aquatic systems in which the slow leaching of silica into the water column would be a problem, and barring the significant presence of ultraviolet radiation, most plastics that one might use for walls (polyester, polyvinyl chloride (PVC), polyethylene) are

characterized environmentally by their long-term stability and a lack of leachable compounds.

Glass Glass tanks constructed commercially offer many advantages to the hobbyist and even to the scientist and aquarium distributor. Technically, a glass is any

15

The Envelope

molten rock that has cooled so rapidly that crystals have not had a chance to form. In the context of this book, glass is silica (SiO2) or uncrystallized, amorphous quartz. In practice, commercial glass is an alloy typically also containing oxides of sodium (Na2O) and calcium (CaO). This soda and lime glass is the oldest, cheapest, and easiest to fabricate. Many other glasses now exist. For example, borosilicate (borax, sodium borate, plus silica) is the base of chemical and kitchenware glasses such as Pyrex and Kimax. Lead is used in “crystal” glasses. Some commercial “glasses” for specialized uses do not even contain silica (see e.g. Bansal and Doremus, 1986). Soda–lime glass (simply glass in the rest of this discussion) is quite transparent and very hard. Very few minerals, such as diamond and carborundum, are harder or more resistant to weathering and most chemicals. Theoretically glass is stronger than steel even in tensile strength. Also, most glass components (silica, calcium, and sodium) in microquantities not only are nontoxic, but they are also needed micronutrients for almost any ecosystem. Most of these points are well known and along with the viewing characteristics are the primary reasons for the traditional aquarium use of glass. It is the theoretical qualification in the strength characteristics of glass that is puzzling and sometimes leads to the choice of other materials. Glass is brittle. It shows little plastic deformation or give before fracture. A very carefully drawn rod of glass can have extraordinarily high strength and, theoretically, could replace steel in rigid steel cable. However, it flaws easily and cracks can start at flaws, greatly reducing strength. Also, even though glass has great weathering resistance, it does in fact react slowly with water (some SiO2 groups being replaced by SiOH). This effect is particularly seen at flaw points on the glass surface from which crack development is accelerated. Glass is relatively cheap. Silicon is one of the more abundant elements of the Earth’s crust. As long as weight is not a significant factor (and this is likely true in aquarium situations because of the proportionally large weight of water), 10 to 1 safety factors placed on normal working strengths will easily solve the indeterminant strength characteristics. There is a considerable literature that relates glass thickness to dimension characteristics currently in use in the commercial aquarium field (see, e.g. Adey and Loveland, 1991). This applies to all glass tanks or glass in steel or concrete structures. Generally, in all glass tanks it is the sealant that begins to fail with minor leakage long before there are glass problems. In very sensitive situations, safety glass or tempered glass can be used as an extra safety factor, although safety glass eventually delaminates and tempered or “heat-strengthened” glass can fail explosively.

We have used heat-strengthened, laminated glass successfully. With three 0.5-inch panels and two 0.030-inch plastic laminate layers, little visual distortion occurs and cost is minimal.

Acrylic The primary competitor with glass for small aquarium construction or for ports in larger tanks is acrylic sheet (Plexiglas, Lucite, etc.). Acrylics are made of synthetic hydrocarbons and can be colorless and transparent (see e.g. Levy and DuBois, 1984). Like glass, their strengths in actual practice are significantly lower than the theoretical values. The strength of acrylic is generally taken to be somewhat less than that of glass. Where weight is a factor, acrylic is about 40% the density of glass, a feature readily apparent to anyone who has carried glass and plastic aquaria. Using the same care as for silicone cement attachment of glass, acrylic-soluble cements can be used to fuse acrylic sheets together. While some brands of acrylics are harder than others, all acrylics are more or less subject to intensive scratching by organisms with shells or teeth. Also algal, bacterial, and protozoan growths (aufwuchs) are inevitable (and desirable) on available surfaces of all ecosystems. If visibility is to be maintained, the glass or acrylic surfaces must be regularly cleaned either by organisms or by hand. In time, this process tends to reduce the transparency of the hardest acrylic. Care also has to be taken in construction of complex structures to allow for the considerable flexibility of acrylic sheets. In public viewing areas, where absolute safety is demanded, and where unplanned impact from a hard object, such as a tool or a bottle, is possible, acrylics have much to offer. Nevertheless, in the past we have chosen safety glass (multilayered glass with thin acrylic sheets molded between) in these situations. This laminated glass product provides the advantages of both materials in aquaria and microcosm construction.

Fiberglass-Reinforced Plastics In the mid-size enclosure range of 300–10 000 gallons, composite plastic tanks are preferable to all-glass or acrylic units. The base material for these tanks is polyester resin, usually with glass cloth or mat reinforcing. Polyester resins have good strength, toughness, and chemical resistance characteristics. Most importantly, polyesters adhere well to other materials, particularly glass and wood. The composite material of polyester resin and glass cloth or matting has a flexural strength of nearly 10 times the practical strength of glass and can exceed that of magnesium alloys. Equally important, the polyesters are catalyzed resins, and setting time as a

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2. The Envelope

function of temperature and catalyst quantity (which is on the order of drops per gallon) is relatively uncritical. As in all plastics, avoiding contamination, especially by oils and greases, in mixing and application is critical. Although almost any technique will “work,” strength and longevity will be severely compromised by any, but a technique of scrupulous cleanliness and reasonable adherence to time, temperature, and catalyst quantity tables. Fiberglass unfortunately is not transparent, and therefore glass or acrylic panels must be used where side viewing is required.

Reinforced Concrete Where weight and space are not factors, and tank size exceeds 10 000 gallons, reinforced cement block or concrete is the material of choice. Particularly in larger dimensions, these structures should be designed by experienced engineers. However, it is essential to convey the special problems of water, salt water, and ecosystems to the responsible engineers. An engineer will easily appreciate the corrosion problems, but the sensitivity of ecosystems to contamination by metals must also be conveyed. Also, concrete is porous and blocks can gradually disintegrate when constantly submerged. The inside surfaces of these construction materials must be coated with an impervious layer. Because this is the same problem, in reverse, as the leaking of building foundations in wet areas, engineers and contractors will understand the sealing problems. However, the final internal coatings should be epoxy or butyl rubber to prevent any water contamination. The function of one of the largest mesocosms attempted to date was severely compromised by unsealed concrete (Marino and Odum, 1999).

Toxic Elements and Compounds Many chemical elements and compounds are toxic to life. Some of these are only mildly poisonous and are often required by organisms as elements in small quantities and only become toxic in excess. Others are always toxic and only concentration determines effect. Many organisms have evolved the ability to produce poisonous organic compounds, primarily as a means of defense or to facilitate food capture. Humans have been highly successful at learning the chemical possibilities of the Earth, both inorganic and organic. Some of the toxic productions of humans are solely for industrial purposes, but in many cases have been allowed to leak into the wild environment. Other elements and compounds have been developed specifically to kill undesirable organisms. Unfortunately, many chemicals that are directed toward specific pest species work their way through ecosystems and become major

controlling elements of biological function. DDT is a classic case, and Silent Spring (Carson, 1962) presents a grim reality that could have been (and may yet be – PCBs followed and now a new generation of synthetic herbicides, pesticides, and hormones are escaping into our streams and rivers). DDT was, hopefully, caught in time (it is still found in whales and birds in the remote reaches of oceans). Also, many pesticides banned or highly controlled in the United States are used in massive quantities elsewhere (including DDT). Chlorine used for water “purification” in swimming pools, sewer outflows, and drinking water supplies deserves close attention. We may yet destroy ourselves and our higher animal and plant associates through chemistry intended for “better living” if we do not rapidly learn more care in this regard. These matters we discuss further in Chapter 4. The aquarist operates mini ecosystems that, because of their small size, are particularly susceptible to contamination by external and internal pollutants. In Chapter 4, we discuss the potential problems that can derive from the water source. Here, we briefly discuss potential material problems that apply equally to the envelope, plumbing, heating and cooling, tide creation, and light supply elements as well as to the substrate. These involve mostly structural elements and thus primarily metal contamination, though many other possibilities exist. Glass, acrylics, epoxies, polyesters, polypropylenes, polyethylenes, nylons, Teflon, and silicones, among others, are structural materials commonly used in aquarium construction. When properly cured these materials are generally inert, nonbiodegradable, and nontoxic. In some cases fungicides might be added to the materials in use, and these should be guarded against. Many metals find their way into construction processes and must be avoided. Except for perhaps lead, mercury, cadmium, chromium, nickel, and silver, metals can have micronutrient uses in organic processes (e.g. iron, zinc, and copper) and are not a problem in small quantities. Nevertheless, in abundance even these can cause severe problems. Copper is one of the most insidious of metal problems for the aquarist. In ionic form it is placed in municipal water systems to kill algae; it is also abundant around human and aquarium situations as copper wiring and piping. Stainless steel, in addition to iron (which is probably the most acceptable of metals, often a micronutrient), has alloy metals such as chromium and nickel. While possibly acceptable in fresh-water use, stainless steels should be avoided around salt-water ecosystems. Titanium may be acceptable, especially in cooling systems, though the final environmental word has not been received on this metal. Zinc as “galvanizing” is often used to coat iron and steel to reduce corrosion. It is particularly toxic when

17

Temperature

dissolved, and in abundance, and should be strictly avoided. Galvanized and stainless steel will be recommended by engineers to solve structural problems where corrosion is a potential difficulty; however, they should not be allowed into aquatic life processes in abundance. Many plants take up metals and incorporate them into their structure. Some geological prospecting can be carried out by looking at the plants that either concentrate the element of interest or show a characteristic response. If algal turf scrubber (ATS™) control systems are used, the algal turfs, also take up many metals (including heavy metals) preferentially, and with the ultraviolet component of especially metal halide lamps, many toxic organics are also broken down. We discuss these issues in Chapter 25.

Plumbing and Electrical PVC piping has become a standard part of western human society, and once manufactured appears to offer no toxicity concerns either to aquatic systems or humans. PVC pipe does have surfaces that are ideal for the attachment of many organisms. If this is a problem either ecologically or from a maintenance concern, then design and construction must allow ports or similar devices for regular cleaning. Likewise, electrical systems should be designed as they would be for wet areas in general, using equipment for exterior and all-weather use as well as ground fault interrupters (GFIs) or breakers. GFIs are relatively expensive and prone to random failure and short life. However, they are necessary to preserve human life. Thus, the consequences of their unreliability must be avoided by design; for example, critical pumping, lighting, or heating functions must consist of dual units on separate breakers.

TEMPERATURE While the temperature of stars ranges from about 3000°C to 20 000°C, the mean temperature of the universe is about –235°C. The surface of most of the planets of the solar system generally ranges from below –100°C to ⫹100°C, beyond the range of most life as we know it. The Earth is in a narrow range of distance from the sun that allows liquid water to be present, and the size of the Earth ensures that it can be present in the atmosphere. Abundant water is a major element in limiting the temperature range on Earth from about –50°C (–68°F) to about ⫹50°C (122°F). However, to a large extent this extremely small temperature range also results from the activities of organisms over billions of years. The

gradual uptake and storage of carbon dioxide (CO2) as well as the release of oxygen (O2) by plants, over geologic time, has created an atmosphere and biosphere that greatly limits temperature extremes on planet Earth. The vegetated surface itself limits temperature variation because of its large water content and indirectly through the control of water movement. In part, this phenomenon is the basis of the Gaia concept: the presence of life on Earth has progressively made a relatively inhospitable environment ever more conducive to even more sensitive and complex life.

Physiological Factors Under water, the temperature extremes are much smaller than they are on land. However, some very important temperature-controlled factors are operating in addition to direct temperature effects. For example, oxygen solubility, and thus the amount of oxygen available to the gills of an aquatic animal, is quite temperature dependent (low at tropical temperatures and nearly twice as high near 0°C). Tropical and temperate zones have existed for billions of years on the Earth. Arctic and subarctic zones, on the other hand, have come and gone. Only a few million years have been available for the evolution of new organisms, and cold-water mechanisms and ecology, in the most recent set of glacial cycles (Pleistocene, Quaternary). This basic limiting factor, along with the strong seasonal cyclicity, is the main reason why colder regions have fewer species and thus less complicated ecologies than the tropics. The most important factor limiting the majority of organisms to relatively narrow temperature or biogeographic zones is a basic chemical limitation. Rates of chemical reactions, including those characteristics of organic processes, are a function of temperature, and the thousands of different reactions that occur in any organism are mutually tuned to a limited temperature range. Chemists and physiologists say that Q10 ranges from 2 to 3, meaning that any given chemical reaction doubles or triples its rate for every 10°C rise of temperature. Since many mutually dependent chemical reactions in an organism are not likely to have the same Q10 values, relatively small temperature changes can quickly unbalance an organism’s critical chemistry. Thus, organisms are at a constant risk of poor health and death when the temperature exceeds the ranges, too high or too low, to which they have become genetically and environmentally adapted. There are two generally applicable subrules that apply to the physiological temperature extreme capabilities of organisms. First, most organisms can acclimatize considerably given the time to do so. This rule applies to both individuals (within a time frame of

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2. The Envelope

FIGURE 2.2 Activity and mortality of marine/aquatic organisms is much more sharply tied to higher rather than lower temperatures. (A) Intertidal barnacle activity (upper intertidal, solid line; lower intertidal, dotted line). (B) Mortality rates of a number of marine crustaceans as they approach their upper temperature limits. After Levinton (1982). Reprinted by permission of Prentice Hall, Englewood Cliffs, New Jersey.

days to months) and populations (many years). Thus, a subarctic clam that might quickly expire given a temperature of 15°C in March would find that same temperature quite optimal in August. A second rule of thumb is that individual organisms, as well as whole populations, are typically nearer their lethal point at the high-temperature end of the scale of survivorship than at the colder end (Figure 2.2). Temperatures several degrees above the normal high temperature range of a population would likely be more dangerous than temperatures several degrees below the normal low temperature. This relationship can be both complex and farreaching. For example, as we will discuss in more depth

in Chapter 21, Strongylocentrotus drobachiensis, the green sea urchin, an algal grazer, is a keystone species in the North Atlantic Subarctic. At higher temperature levels, but still well below its lethal temperature, S. drobachiensis is subject to a protozoan disease. Because of this, at temperatures only a few degrees above optimum, populations are subject to alternate build-ups and crushes, as peak summer temperatures vary from year to year. An even bigger issue concerns the very future of coral reefs. Temperatures just a few degrees higher than normal in tropical waters cause corals to lose their zooxanthellae, with many dying. With global warming coral reefs will likely radically change their community structure and combined with additional atmospheric

19

Temperature

FIGURE 2.3 Gonad development in the starfish Pisaster ochraceus from the intertidal of northern California. Note that while some seasonal reproductive cycles are tied to day length, this animal reaches its peak reproduction shortly after average temperatures reach their minimum for the year [1955 (•); 1956 (ⴰ)]. After Levinton (1982). Reprinted by permission of Prentice Hall, Englewood Cliffs, New Jersey.

CO2 (and lower ocean pH) may stop growing altogether (see Chapters 10 and 20). Beyond concern for the extreme ranges and the short-term survivorship of organisms and their populations, there is also a need to consider normal life cycles, whether temperature determines breeding (as it often does) (Figure 2.3), and whether feeding patterns (and the availability of feed) and migration are also determined by temperature.

Temperature Characteristics of Biomes and Rivers Most people are aware that the major biomes (terrestrial life zones) of characteristic terrestrial plants and animals change radically with temperature. From the polar north southward, the polar south northward, and downward from the tops of high cold mountains, the tundra, taiga (conifer forests), and hardwood forests form circumpolar or circummountain bands. Around the warm equatorial and subequatorial bands of the Earth, water supply rather than temperature is the primary factor determining biome type. These bands, generalized for all continents, are shown in Figure 2.4. A standard plant hardiness map for North America

would show something similar for the use of a gardener, though not usually with the natural water supply component. Although perhaps more muted (as is temperature change), the same kinds and ranges of life zones or biomes occur under water. These biomes are partly determined by temperature, and substrate becomes more crucial and rainfall only indirectly of interest. In general, fresh-water streams follow a temperature pattern similar to that of the terrestrial life zones. However, small spring-fed, especially forested area streams are more controlled by ground-water temperature and therefore have a small temperature range (Figure 2.5). Passing downstream, as branches meet and the flow grows, streams warm or cool according to air temperature and range becomes quite large. Finally in larger streams and rivers, temperature fluctuations tend to reduce again as the greater volume is more subject to long-term factors. Rivers can become complex biomic entities as they flow for hundreds or thousands of miles changing radically in temperature characteristics, and therefore in the organisms that make up their biological communities.

Temperature Characteristics of Lakes If they are large enough, lakes can have a considerable ameliorating effect on the local terrestrial climate. In temperate and colder regions, the lake climate itself is always considerably more moderate than the surrounding terrestrial climate. Because the maximum density of water (including the ice phase) lies at about 4°C, cold-climate lakes in the winter have relatively warm deep water (the hypolimnion) while the surface is frozen and the upper few meters lie near 0°C (Figure 2.6). During the summer, lake surface waters warm considerably and, barring strong winds or other factors, become stable and stratified. The surface layers (or epilimnion) become nearly as warm as the average monthly terrestrial air temperatures, while the bottom water temperature typically ranges from 6°C to 15°C, in temperate climates. The temperature change from shallow to mid depths, called the thermocline, is often sharp. Because the hypolimnion is often relatively isolated, in lakes excessively rich in organic material, bottom waters can become anaerobic in summer if they lie beyond the maximum penetration of light. In the fall, as surface temperatures chill and the water becomes heavier, these lakes “overturn,” mixing the water and taking on the same temperature from top to bottom. Tropical lakes, on the other hand, while showing the same basic tendency to stratify, may have a surface to bottom temperature difference of only a few degrees centigrade. Similarly, though much colder, Arctic lakes

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2. The Envelope

FIGURE 2.4 Idealized terrestrial biomes or large areas of similar climate, mostly determined by temperature and to a lesser extent rainfall. I. Tropical zones: (1) equatorial rain forest; (2) tropical rain forest with trade wind, orographic rain; (3) tropical-deciduous forest (and moist savannas); (4) tropical thornbush (and dry savannas). II. Extratropical zones of the Northern Hemisphere: (5) hot desert; (6) cold inland desert; (7) semidesert or steppe; (8) sclerophyllous woodland with winter rain; (9) steppe with cold winters; (10) warm-temperate forest; (11) deciduous forest; (12) oceanic forest; (13) boreal coniferous forest; (14) subarctic birch forest; (15) tundra; (16) cold desert. III. Extratropical zones of the Southern Hemisphere: (17) coastal desert; (18) fog desert; (19) sclerophyllous woodland with winter rain; (20) semidesert; (21) subtropical grassland; (22) warm-temperate rain forest; (23) cold-temperate forest; (24) semidesert with cushion plants, or steppes; (25) subantarctic tussock grassland; (26) inland ice of the Antarctic. After Walter (1979).

can have the same temperature from top to bottom in summer.

Marine Biogeography Even more than in lakes, the marine environment varies relatively little in temperature, and marine organisms have evolved to be able to withstand only small changes in ambient temperature. The maximum

temperature range throughout the world’s oceans, outside of very restricted salt ponds or tidal pools, is about 32°C (58°F), as opposed to about 100°C (180°F) in the land environments. The yearly ranges in any one locality, even coastal localities, are much more restricted, ranging from as much as 20°C (36°F) in some temperate or subarctic coastal areas to as little as 3–5°C (5.5–9°F) in some tropical, boreal, and arctic coastal zones. In general, the daily and weekly changes at a given depth in

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Temperature

FIGURE 2.5 Maximum daily temperature range as a function of stream order (0⫽spring, then numbered as streams join). The smallest, spring-fed streams and larger rivers are least affected by local climate. Mid-level streams can change radically on a day-to-day basis and follow atmospheric climate closely. From Vannote and Sweeney (1980).

coastal and ocean waters are measured in no more than tenths of a degree centigrade (Thurman and Webber, 1984). Most organisms in the biosphere are “cold” or “cold-blooded,” poikilothermic in scientific terminology. Unlike birds and mammals (homeotherms), which, with adequate energy or food supply, can handle a wide range of temperatures, invertebrates, most fish, amphibians, reptiles, and plants can do little or nothing to control their temperature. They function in accordance with the temperature provided to them by the ecosystem or ecosystems to which they are adapted. Some of these species function over relatively wide temperature ranges (eurytherms); others are much more limited (stenotherms). Any given species is subject to a wide range of environmental variables, and the regional temperatures over which a species ranges are not all likely to be optimum for growth and reproduction. Those optimum temperatures are narrow and generally changing with time, but lie within the regional range. Embedded in the terrestrial biomes shown in Figure 2.4, which depend on temperature and rainfall (more generally climate), are biogeographic regions. For example, the narrow equatorial zones are characterized by tropical rainforest which has similar physical, chemical, and ecological characteristics around the world. However, South American, South African and South Asian, and the Australasian rainforests are occupied by different species; they have developed in tune to the same kind of environment, but the genera and species that have resulted from evolution over the last 100 My, largely in isolation, are quite different. Marine ecosystems have the basic equivalent of the biomes; e.g. oceanic plankton/nekton systems, deepwater benthic or bottom systems, and a wide variety of coastal muddy, sandy, rocky, and coral reef shores, all under a wide variety of temperature conditions. Here, we will concentrate on the shore systems, the rock shores, and coral reefs most likely to be modeled.

Coastal marine ecosystems have characteristic yearly temperature ranges, usually following a more or less sinusoidal pattern with a peak and a minimum following solar peak and minimum by 1–2 months. Marine temperature patterns are related to ocean currents, the orientation of coastlines, and the relative “continentality” of the coast, as well as to latitude. Figure 2.7 shows a contour plot of miles of coastland for the world’s oceans. Clearly, there are extensive lengths of coastline for some summer/winter temperature signatures (what we will loosely call shore climate) and very little or none at other signatures. The last 2–5 million years has been characterized by alternating glacial and interglacial stages. Fortunately, the ocean surface temperatures, summer and winter for the last glacial stage at 18 thousand years, have been determined by studying the fossil planktonic community that has rained into the extensively core-drilled ocean sediments (Climap Project Members, 1976). Using a similar plot for 18 thousand years overlain on the plot of Figure 2.7, it has been possible to estimate what shore climate signatures were constant over the last several million years (Adey and Steneck, 2001). Shown as a contour plot in Figure 2.8, these are the shore climates to which most current existing rocky shore species have evolved. These are the biogeographic regions of the rocky shore biome and they are shown geographically in Figure 2.9. They correspond closely with the classic biogeographic regions determined from the distribution of marine fish and invertebrates (Briggs, 1974). In Chapter 21, we discuss in more depth what this means to the modeler of ecosystems.

Model Ecosystems and Temperature Matching the temperature pattern of any given ecosystem model with that of its wild analog is not a difficult technical problem given the enormous diversity and sophistication of the equipment available. To

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2. The Envelope

FIGURE 2.6 Yearly temperature (°C) ranges surface to deep water in arctic to tropical lakes. (A) Arctic; (B) tropical; and (C) temperate, continental. After Hutchinson (1957). Reprinted by permission of John Wiley & Sons, Inc.

achieve a high precision of measurement, recording and controlling can be a significant cost factor. However, it is the resulting requirement for heating and especially cooling, depending on the circumstances, that is likely,

in the long term, to be the controlling cost element. Since the situations are likely to vary widely, for each of the myriad systems to be considered, we discuss heating and cooling for each of the examples given in Chapters 20–23.

23

Water Motion

FIGURE 2.7 Distribution of temperature characteristics of rocky ocean shore in the world’s oceans. Each contour represents one nautical mile square (1 minute of latitude; a nautical mile ⫽ 6080 feet or 1870 meters). Note that overlapping coast patterns (e.g. Indo-Pacific and tropical East Pacific; New Zealand and Australia) are separated by the amounts shown to reduce confusing overlap. This diagram shows that large areas of coastline occur under certain temperature regimes. For example, hundreds of nautical miles of coast (in the Mediterranean) have a temperature regime of 24–26°C in summer and 10–16°C in winter; on the other hand there is virtually no rocky shore that is 20–24°C in summer and 6–10°C in winter. From Adey and Steneck (2001).

This will give the modeler a perspective on the heating and cooling problems likely to be encountered in a specific case (Table 2.1). Temperature sensing and control units can provide significant contaminating problems; for example, copper heating or cooling coils are rarely acceptable. Beyond contamination issues, for the simplest situations, we suggest the control heating/cooling equipment available at larger, more sophisticated aquarium outlets or the options suggested by Spotte (1995). For more sophisticated systems with greater precision of control, especially when daily and seasonal ranges are to be matched, the equipment offered by most of the larger scientific and laboratory supply or medical companies provides a full range of options. Glass, plastic, or ceramic surfaces in contact with water are almost always preferred to metal surfaces or contacts.

WATER MOTION Natural waters, to varying degrees, are very much chemical soups. The possibilities for chemical interactions on a large scale are greater in water than in any other environment on the Earth. They are probably greater than anywhere else in the universe, except where water might be present. On the other hand, simple diffusion of an element or an ion through water can be very slow. As we discuss in Chapter 4, even though water allows most elements and many compounds and gases into its loose chemical structure, often as weakly charged ions, the rate of mixing and interacting can be limited in the short term by the rate of diffusion. Indeed, the very structural factors that allow water to be the ultimate solvent, and thus the chemical soup, also provide significant limitations to diffusion and therefore to the rates of reactions.

24

2. The Envelope

FIGURE 2.8 Distribution of average temperature characteristics of rocky ocean shores in the world’s oceans for the past 3 million years (Pleistocene). This diagram is derived by obtaining the glacial coastal temperature range (after Climap Project Members, 1976) and multiplying (for each degree square) times existing coastal temperature range (Figure 2.7). Basically it shows expected species concentrations for rocky coasts. From Adey and Steneck (2001).

Organisms are rarely static? (though resting overwintering, overdrying stages, and seeds can be amazingly long lasting). The basic unstable nature of individual life requires a constant flow of energy and materials to keep the biological and ecological processes operating. Whether it is the stirring of water in the home or laboratory, the wind blowing across a lake, waves crashing on a rocky shore, or tides coursing in and out of a bay, all significantly contribute to ecological and ecosystem processes. These physical energy inputs force the mixing required to varying degrees by living organisms to carry out an active life. Scientists have been examining the direct effects of waves and currents on physical variables such as oxygen and temperature and directly on individual species for a long time. These forms of physical energy have a major impact on primary ecosystem processes such as photosynthesis and respiration (Leigh et al., 1987; Nixon, 1988; Adey and Hackney, 1989; Carpenter et al., 1991).

It is now recognized that wave action and the orbital water motion it creates in the upper layers of oceans and lakes can increase phytoplankton photosynthesis (Marra, 2002). Figure 2.10 shows the contrast between the muddy bottom infaunal biomass, with depth, in fresh and marine waters. Nixon (1988) relates the approximate one-half order of magnitude difference between marine and fresh waters to the driving effects of tide and wind (waves and current). Note that the one lake that approaches marine situations in benthic biomass is the large Lake Michigan. All forms of mixing accelerate chemical and therefore biological processes up to a certain saturation point beyond which other factors (light intensity, temperature, chemical concentration, etc.) begin to be limiting. Thus, waves, currents, and tides should not be omitted from the ecosystem model any more than from the wild community (Color Plates 9, 41, and 46). They

25

Water Motion

FIGURE 2.9 Major biogeographic provinces of rocky shore in the world’s oceans. These are the coastal areas that one would expect to have strongly distinctive flora and fauna; the unhatched areas between the provinces are transitional. From Adey and Steneck (2001).

TABLE 2.1 Heating and Cooling of Selected Model Ecosystems Described in Chapters 20–22 Heating

System (Normal temperature range) Coral reefs 3000-gallon reef, Smithsonian (25–28°C)

Type

Cooling Heat exchanger

Type

2000 W, titanium coated, immersion heater (Process Technology, Inc.)

None

Two titanium immersion water chillers, 1 hp each (Aqua-Logic)

130-gallon reef, home system (25–28°C)

Two 100-W glass aquarium heaters for winter minimum

None

Air-conditioned room held at 23°C; no supplemental cooling

750 000-gallon reef Great Barrier Reef Marine Park (25–29°C)

Open air at Townsville, QLD, Australia; supplemental heating from scrubber lights and immersion heater if necessary

Water chiller

Temperature-controlled room; no supplemental heating

Air-conditioned room and input sea-water cooled with an immersion chiller

Estuaries Chesapeake estuary (20–28°C, summer) (4–6°C, winter)

Heat exchanger

None

Plastic tubing coils in tidal reservoir

Florida Everglades estuary (25–28°C, summer) (18–21°C, winter)

Propane-heated greenhouse Three 4000-W immersion heaters (Process Technology, Inc.)

None

One titanium water chiller, 2 hp (Universal Marine Industries)

Plastic tubing coils in water distribution tower

Florida Everglades fresh water (25–28°C, summer) (20–22°C, winter)

Propane-heated greenhouse Immersion heater as necessary

None

One titanium water chiller, 2 hp (Universal Marine Industries)

Plastic tubing coils in upper pool

Three titanium immersion water chillers, 1 hp each (Aqua-Logic)

None

Maine coast 2500-gallon Maine rocky shore (12–15°C, summer) (4–6°C, winter)

None needed

26

2. The Envelope

FIGURE 2.10 Comparison of the biomass of soft bottom infauna in marine, estuarine, and fresh-water environments. After Nixon (1988), with mean curves fitted by eye. Weights are shell-free, ash-free dry weights. The wider curve to the right represents salt and brackish water. The narrow curve to the left/center represents fresh water.

need not be, and often cannot be, of the great force and energy that they sometimes are in the wild. However, wild levels during storms are often far above saturation levels in terms of their effects on ecological processes. On the other hand, storm or even weekly or monthly high waves or currents may determine community structure in many cases. If these high-energy communities are to be simulated, at least in a localized way within a model system, then steps need to be taken to provide strong point sources of physical energy.

Currents in Fresh Waters Currents, sometimes extreme, occur in streams and rivers. Those currents control mixing and circulation, as well as the nature of bottom sediments (see below). That currents also occur in lakes and are of great importance is not as widely recognized (Figure 2.11). As we noted above, lakes are also mixed by wind and,

in colder climates, by autumn and spring overturns (Figure 2.6). Overturns result from surface cooling in the autumn (or heating in early spring) when the surface waters become heavier than deeper waters. Under some conditions, particularly in warmer and less windy seasons, or in the tropics where lakes can be warm at the surface year round, the surface waters become warm, light, and strongly stratified. When this happens, mixing with deep-water stops. If the bottom sediments are even moderately rich in accumulated organic material, bacteria, worms, and clams in the mud can use up all of the available oxygen and leave the bottom sediments and even some of the bottom water virtually dead. This is more likely to happen in lakes with greater nutrient input, and therefore higher productivity levels (Figure 2.12). Lake Tanganyika in East Africa is a well-known example of such a lake, with about 90% of its total volume being permanently devoid of oxygen.

Water Motion

27

FIGURE 2.11 Surface current patterns in Lake Constance, Switzerland. Average rates in shallow water are 10–20 cm/s and reach 27 cm/s at some localities. After Hutchinson (1957). Reprinted by permission of John Wiley & Sons, Inc.

FIGURE 2.12 The relationship of stratification (as shown by temperature curves) and oxygen in different types of lakes (Feforvatn: biologically sterile; Breiter Lucin: intermediate; Green Lake: highly productive). [O2] ⫽ oxygen observed; [O2]s ⫽ saturation level at temperature; ␪ ⫽ temperature; 䉮 ⫽ bottom. From Hutchinson (1957). Reprinted by permission of John Wiley & Sons, Inc.

It is also not unusual for even quite large lakes and estuaries to become unnaturally anaerobic due to the nutrifying effects of human activity. Chesapeake Bay in eastern North America, one of the largest estuaries in the world, is just such an example. A deoxygenated layer began to appear in deeper waters during the summer in the 1950s. In spite of great effort and expense to reduce nutrient loading over the last 30 years, population growth in the watershed has offset improvements

and the dead zone has continued to grow (Price, 2005). Unfortunately in these cases, since phosphorus does not diffuse easily through oxygenated sediment, slight deoxygenation releases stored phosphorus in large quantities. This triggers more surface productivity and a “snowballing” of deoxygenation. Many lakes in populated or heavily farmed areas have reached a similar state, and now the northern Gulf of Mexico, off the Mississippi River, has developed a large, hypoxic zone.

28

2. The Envelope

Currents in the Marine Realm In open, shallow-water marine environments constant and relatively rapid turnover of living biomass is the rule, longevity the exception. Organic-rich sediments, equivalent to marshes on land, can form in deeper water, in the extensive shelf environments and in protected lagoons and bays. These organics can become geologically stored for hundreds of thousands or millions of years. However, the short-term in-situ storage of biomass as in terrestrial forests and swamps does not readily occur in the near-coastal marine or aquatic realms. A rapid exchange of gases (oxygen, carbon dioxide), metabolites (food, nutrients, nitrogenous wastes), and salts and minerals between aquatic organisms and their watery environment is the normal state in high-energy environments. On the other hand, these low-biomass, high-water quality zones remain in that state in large measure because of export and storage of organics elsewhere, whether in deeper water or in lagoons and bays. The world’s oceans develop major surface currents (Figure 2.13). These currents are created primarily by prevailing winds, modified by Coriolis (Earth rotational) and density forces as well as by land geography. While moderate in rate, ocean currents can, however, reach several knots (e.g. the southern Gulf stream). Ocean currents provide mixing and heat transfer for the entire ocean, and consequently the atmosphere. They are major factors in determining weather patterns. Below several hundred meters, circulation generally is slower and is driven

primarily by density as established by salinity and temperature (Figure 2.14). As in lakes, the limited circulation in deep water results in oxygen depletion (Figure 2.15). However, in this case because of the enormous depths involved, the organic material raining from the surface is largely broken down within the upper 1000 meters. The oxygen minimum occurs in the 500–1500-meter range, and oxygen concentrations generally increase in even deeper water. The deep and bottom waters are generally very cold and relatively oxygen-rich, being derived from very slow-moving bottom currents from the surface waters of the Arctic and Antarctic.

Wave Action While the larger-scale circulation of the ocean is in large measure driven by long-term wind stress, wave action more directly and strongly mixes the surface layers of water. Figure 2.16 shows how a wave, whether a wind wave or swell, disturbs, and mixes surface waters by its motion. Waves driven for several hours or more by any wind over 12–15 knots and for a distance of over several miles can have large effects on the shore and the biological and ecological processes of that shore. Most oceanographic text books provide tables or graphs for predicting wave heights, wavelengths, and their frequency. Marine literature, including sailing directions, and maritime forecasts, provide similar information. Waves can accomplish more than circular internal motion and turbulance when they are driven against

FIGURE 2.13 Surface circulation of the world’s oceans. After Kennett (1982).

29

Water Motion

FIGURE 2.14 Primary vertical circulation in the Atlantic Ocean. Temperature in °C. After Thurman and Webber (1984). Copyright © 1984 by Scott, Foresman and Company. Reprinted by permission of Addison-Wesley Educational Publishers.

FIGURE 2.15 Oxygen concentrations with depth in the Atlantic and Pacific Oceans (ml oxygen per liter). After Kennett (1982).

a shore. For example, a rich shallow-water coral reef, with its extraordinary respiration and primary productivity, resembles a city in that it requires continuous exchange with the adjacent ocean and lagoon. With a greater concentration of plants and animals than it can support within itself, the wild coral reef experiences rapid oxygen depletion of the strongly inflowing, oxygen-rich ocean water during the night (Figure 2.17). It is the

trade wind seas that drive water across the reefs and prevent serious oxygen depletion over the reef communities.

Water Motion and Model Ecosystems The role of wave surge as an important mixing element is easily seen in a reef microcosm where a

30

2. The Envelope

FIGURE 2.16 Motion of water particles in wind-driven waves. The circles describe the extent of orbital movement of individual water particles. After Thurman and Webber (1984). Copyright © 1984 by Scott, Foresman and Company. Reprinted by permission of AddisonWesley Educational Publishers.

well-defined flow and surge are present (Figure 2.18). This irregularly oscillating inflow across the reef closely matches that measured by the same means in the wild. Removal of the surge component alone markedly reduces photosynthesis and oxygen production (Figure 2.19). On quiet nights in a high-biomass wild reef, low current and surge can result in low oxygen concentrations. A well-developed reef community would quickly expire under the stagnant conditions of a nonflowing, unaerated, closed-system aquarium because of oxygen drawdown and carbon dioxide and ammonia pollution; this can occur rapidly with any appreciable animal load.

While wave period can be simulated easily in an aquarium or mesocosm, wave height, except in the largest mesocosm (see Figure 2.20) will not likely be fully matched. Consideration of the wild environment in this respect should at least lead the scientist and aquarist to attempt a partial match and to consider the effects of reduced wave energy. Traditional aquaria often employ bubblers or aerators to achieve water motion with its resulting atmospheric exchange. Although a bubbler can induce some water movement when set up as an airlift, it is relatively inefficient at creating currents and cannot create

Water Motion

31

FIGURE 2.17 Oxygen reduction at night in water driven over a Caribbean coral reef by the trade wind sea and swell. 1, Front of forereef; 2, back of forereef; 3, front of backreef; 4, back of backreef. Note the oxygen increase at night between forereef and backreef (i.e. 2–3), in the surf zone, due to input from the atmosphere. After Adey and Steneck (1985).

FIGURE 2.18 Wave surge and current in the Smithsonian coral reef model. See Figure 20.1. The mean inflow (across the reef) is about 0.1 ft/s, but the oscillation (or surge) is very marked.

a surge. Filter devices usually have associated drive pumps. However, they are rarely used to establish current or waves, although that possibility sometimes exists. Even a pump of very high rating could provide little flow if the filter unit itself is partially clogged. Newer pumping devices often include “power heads” and are capable of producing locally high current zones

(though see our discussion on the effects of bubblers and centrifugal pumps, below). In shallow coastal and shore communities, marine or fresh water, on which this book focuses, water motion occurs as a result of simulated tides, currents, wave action, and its resulting surge. Many devices have been constructed to create waves in tanks for experimental purposes, including

32

2. The Envelope

FIGURE 2.19 Reduction of oxygen production with reduced wave action in coral reef microcosm algal scrubber (Adey and Hackney, 1989).

FIGURE 2.20 Pneumatic wave drive system used in Australian Great Barrier Reef aquarium at Townsville.

33

Water Motion

push boards and large pistons. Most recently a pneumatic device has been extensively used for creating waves in swimming pools, and a version of this device has been used on several large mesocosms (Figure 2.20). For most mesocosms and aquaria a variation of the simple dump bucket (Figure 2.21) is the most reasonable approach in terms of cost and maintenance. If the dump rate is matched to the natural frequency of the tank (determined by “rocking” or seiching the tank water mass by hand), a high surge rate can be created. Often, however, it is desirable to slightly mismatch wave dump with natural frequency to avoid waves that become excessive. If diaphragm pumps are used (Figure 2.22), a surge or seiching motion can also be created by periodic suction. Moderate waves, created by the techniques described in this chapter and in Chapters 20–23, are normally sufficient to maintain community structure on the scale of days and perhaps weeks. However, many ecological communities, especially those of rocky shore and reef environments, are partly structured by occasional

strong wave action. It is often necessary in models of these systems, especially in the smallest microcosms and aquaria, to create occasional unusual turbulence either by hand or with apparatus designed for this purpose.

Pumps Among the wide variety of pumps available for moving water in microcosms, mesocosms, and aquaria, the most commonly used is the centrifugal/impellor pump. These can be inexpensive, reliable, and quiet, and a wide choice exists to fit almost any system design. Submersible impellor pumps are readily available and can be quieter and esthetically more desirable than those designed for operation in air as they can be hidden within a tank. However, with plumbing failure they also have the potential for pumping a tank virtually dry unless the intake is placed very high. Submersible pumps also tend to raise system temperatures, and some varieties have the potential for leaking oil.

FIGURE 2.21 Photographs of dump-bucket wave maker. Note that these devices are highly sensitive to weight shift and easily become unbalanced with algal growth. Proper setting of the hinge axis and the use of friction-minimum bearings that will not corrode are essential. We have found that Teflon against Teflon is the only foolproof method, although Teflon against other plastics is usually acceptable. We have also used Nylatron, as the axis against a Teflon bearing.

34

2. The Envelope

FIGURE 2.22 The 30-rpm, 5-gpm diaphragm pumps as installed in a 130-gallon scrubber-operated reef aquarium (see Figure 20.18). The dark area to the right is a refugium. The scrubber unit is off the photo to the right (see Color Plates 8A and 8B). Photo by Nick Caloyianis.

The unfortunate difficulty with most impellor pumps is that their internal turbulence, pressure, and shear forces kill many plankters and the swimming or floating reproductive states of plants and animals. We have been able to demonstrate a greater than 90% mortality of large zooplankters, such as Artemia salina, on passing through such a pump. Impellor pumps select plankton populations in a system, killing some and effectively enhancing others. This is the basis for the development of tinted waters (yellow or green) in some systems and not in others (see also discussion in Chapter 6). We have experimented with alternatives to the ubiquitous impellor pumps. Among the possibilities are relatively large diameter diaphragm pumps that contain “flapper valves” and alternate relatively slowly from a slight suction to a slight pressure (Color Plates 2, 4–6). Some compressed-air-driven types for transferring corrosive slurries in the chemical and other industries work quite well and are easily available. However, they are expensive and often quite noisy. We have designed and

extensively used the bilge pump system shown in Figure 2.22 on many small aquarium systems (see Chapters 20–23). Sophisticated engineering and manufacture for a mass market could make these pumps “standards.” Archimedes’ screw pumps are ancient devices used centuries ago, particularly in irrigation. Today, they still merit usage in sewage plants where a simple, virtually uncloggable pump to move large quantities of water at minimal height is desired. We have had experience with several, large Archimedes’ screw pumps in mesocosm systems. They are unexcelled at lifting large quantities of water without significantly disturbing plankton, or even larger invertebrates and fish (typically they lift to a distribution reservoir). However, Archimedes’ screw pumps have a tendency to burn out drive motors, during restart (under heavy water loading) during power outages. Also, the primary lower bearing is subject to corrosion and wear. Both of these issues are minor engineering problems. Recently, a promising “bubble-lift” pump that uses large bubble “bursts” injected into a chamber from a

Tides: Simulating the Effects of Sun and Moon

low-pressure, high-volume compressor has been developed. This is basically a smaller version of the wave generator shown in Figure 2.20. Because a single bubble on the order of several hundred milliliters to a liter or two (depending on pump dimension) will lift a relatively large volume of water, the bubble surface that traps plankton is greatly limited. Thus, the “skimming effect” of standard aerators or bubblers, which removes plankters, particulates, and large organic molecules, is partly avoided. Centrifugal pumps that lack impellors and have simple discs, or discs with grooves or ridges, called discflow pumps, are used in the food-processing industry to pump a wide variety of foods. These pumps are an acceptable alternative to the impellor pump replacements described above when the values of a centrifugal pump are needed. Since disc-flow pumps are not yet being built for the mass market, they tend to be relatively expensive. On the other hand, we have found them to be highly reliable (see Chapter 22) and acceptable in maintaining diverse plankton communities. Pumping rates vary from system to system. At the Smithsonian, the coral reef system overturned approximately every 60 minutes, and the Maine rocky-shore, mud-flat tank overturned approximately every 45 minutes. The small, home, 130-gallon reef described in Chapter 20 overturned every 20 minutes. The 750 000gallon reef system at Townsville, Australia (Chapter 20), is completely pumped around every 2.9 hours (Jones, 1988). There is no way to arrive at an ideal rate without taking oxygen measurements in the fully functioning system (see Chapter 8) and comparing actual currents and surge, depending on design, with the wild analog. The mean flow rate across the St. Croix analog coral reef is 10 cm/s, three times as high as that in the Smithsonian model at 3 cm/s. On the other hand, turnover time (ocean water replacement) on the wild reef averages about 6 hours compared to 1 hour in the model mentioned above. Thus, these related parameters are both within the right order of magnitude, but displaced in opposite directions because of critical size restrictions in the model. A secondary and related parameter, water quality in the model as measured by dissolved oxygen concentration, is remarkably close to that in the wild (see Figure 8.9). This kind of give and take matching is crucial to the modeling process. In general, warmer and smaller microcosms and aquaria should turn over more frequently than larger and colder systems. Oxygen solubility in cold water is almost twice that in tropical waters (see Chapter 8). Therefore, drawdown for a given biological load is less critical in cold water. Also, smaller systems will usually be more overloaded than larger ones. Thus, greater circulation in proportion to volume is desired.

35

Many factors determine actual pumping rate compared to the rate given on the pump or pumps. Besides the pump rating, water delivery rate is a function of both suction and delivery heights, length of flow, and the size of the pipe, as well as any restrictions to flow. Bacterial filtering devices can greatly reduce actual output, as well as destroying plankton. It is inappropriate to use such filters in model aquatic ecosystems unless they mimic a desirable feature of a wild system (e.g. a large filter feeder). In our discussions below we refer to actual flow. In general, if algal scrubbers are used to control water quality, a minimum rule-of-thumb flow rate over the scrubbers is 40 liters (10 gallons) per minute per one square meter (10.6 square feet) of scrubber surface. If this rate is not acceptable for achieving the currents desired, then a separate recycling pump can be used, either on the primary tank or on the scrubbers. A simple device that combines scrubbing with current, wave action, and wave surge is shown in Color Plate 9 and Figure 2.1. This “dump scrubber” is particularly effective when minimum space is available in a small system and the desirability of mounting all apparatus directly on top of the tank is a foremost consideration. It is best to split up the pumping among as many small pump units as economically and physically feasible, thereby lessening the threat to the whole system when a pump breaks down, as it inevitably does. There should always be backup pumps readily available. Beyond the inevitable contamination, we remind the modeler, whatever the level, that the single most frequent source of massive failure is catastrophic leakage usually from plumbing. Also, pumps and electricity will fail. If there is a dynamic water mass (i.e. water in transit) in a system, adequate sump volume (e.g. the tank itself) must be allowed.

TIDES: SIMULATING THE EFFECTS OF SUN AND MOON The ebb and flow of tides is one of the most fascinating aspects of the sea. Even though lakes show seasonal or meteorological changes in level, tidal effects are virtually absent, and on some ocean coasts (e.g. the southwestern coast of Norway), tides are small enough to be more or less negligible. However, as we pointed out above, bottom biomass in lakes is generally less than in the sea, probably in large part due to tidal effects (Figure 2.10). Many biological communities (e.g. salt marshes and rocky intertidals) depend entirely on tides, and it has been demonstrated that the mixing effects of tides provide an energy subsidy to ecosystem function (Figure 2.23). In addition, many organisms

36

2. The Envelope

FIGURE 2.23 Energy flow diagram developed for the Narragansett Bay ecosystem. Note that tide has been given a major controlling role both on solar input and on export from the bay. The boxed form of tidal attachment also indicates tidal effects driving all levels of the ecosystem. After Kremer and Nixon (1978).

key important elements of their life cycles, particularly reproduction, to the tides and to the moon (Palmer, 1995). Sophisticated lighting control systems for home aquaria have begun to include a moon component. As an example of the complex ways in which tides and moon, together and separately, can affect an organism (and therefore a community), we cite the case of the Caribbean/West Indian magpie shell, Cittarium pica. This large, rocky intertidal and upper subtidal snail, characteristic of exposed wave-beaten shores, achieves some gastronomic use in the Caribbean. Three to five days after the new moon (i.e. during the darkest nights of the month), the males and females crawl into exposed tide pools at high tide. When tide level lowers sufficiently to isolate the pool, the snails start releasing eggs and sperm into the water. (It is not known whether elevated temperatures, hydrostatic pressure, lack of wave action, or some other factor alerts the animal that the pool is isolated.) Fertilization takes place in the pool and the developing larvae are washed into the ocean as the rising tide floods the pools. This complex and multi-keyed reproductive pattern offers many advantages. To an animal living on a wavebeaten shore where eggs and sperm released into the water would have a difficult time coming together

before being washed out to sea, it provides a more precise way to ensure fertilization of large numbers of eggs. Also, the tide pool situation is one that is difficult for many fish to occupy. Wrasses, for example, would otherwise eat the eggs as they are released. Thus, the tide pool provides relative freedom from fish predation and it seems likely that in part this also has resulted in the evolution of this curious pattern. A similar reproductive keying to spring – higher high tides on sandy California beaches – is practiced by a fish, Leuresthes tenuis, the grunion. Thurman and Webber (1984) describe this process and its relationships to tide in some detail. The intertidal zone itself is truly the interface between the terrestrial and the marine, and this area is the most easily accessible of marine environments. Many scientific studies have been carried out in the intertidal zone and some excellent books describe it (Raffaelli and Hawkins, 1996; Haywood, 2004). One of the finest of the classic works is Between Pacific Tides (Ricketts et al., 1985), first written in 1939 and now in its fifth edition. In particular, the rocky intertidal and salt marshes, restricted to the intertidal zone, are important subjects for model ecosystems and we describe several of these models in later chapters.


Ocean Tides Average ocean tides measure 2–3 feet (0.6–1.0 meters) from high to low water, but they can range from virtually nothing to 50 feet (15 meters), depending on special geographic features. Generally, any body of water has a natural frequency of oscillation as a standing wave. This can be demonstrated in an aquarium by “pushing down” on the water on one side in a pulsing manner until the entire mass starts “rocking.” When the natural frequency of a body of water is close to that of the sun/moon-created tidal wave, tide heights can become much larger than those in the open ocean. The English Channel, the Gulf of Maine, the St. Lawrence River Estuary, and the semi-enclosed waters north of Australia are well known for their extraordinary tides. Tides are typically semidiurnal, with two high points and two low points a day, each one about 6 hours and 10 minutes apart and more or less equal in height. However, diurnal tides of one high and one low daily, or combinations, mixed tides, somewhere in between, are not uncommon (Figure 2.24). The Florida Everglades coast, for which we discuss modeling in depth in Chapter 22, has a nearly perfect mixed diurnal/ semidiurnal tide. In this case, the Atlantic Ocean has a

37

semidiurnal tide, the Gulf of Mexico, a diurnal tide. The southwest Florida coast is where they meet. Every 2 weeks when the sun and moon are on the same side of the Earth, and also when they are on opposite sides, the Earth has large “spring” tides. Roughly 7 days after a spring tide, when the sun and moon form right angles to the Earth, “neap” tides occur. These are a third to a quarter smaller (Figure 2.25).

The Intertidal Zone The intertidal band of bottom or shore between high and low tides is a difficult region for living organisms to occupy. Relatively few plants and animals have adapted to this zone. It is alternately cooled and wetted with salt water, sometimes frozen in the winter, dried and baked by the sun in the summer, and sometimes flooded with totally fresh water during heavy rains at low tide. Depending on tidal range and slope of the shoreline, it can be quite narrow or many miles wide. It is neither marine nor terrestrial. On rocky shores it is dominated by relatives of primarily marine groups, on marshes and swamps mainly by terrestrial-derived species. Environmentally difficult as the intertidal zone

FIGURE 2.24 Distribution of tide heights around North America. After Thurman and Webber (1984). Copyright © 1984 by Scott, Foresman and Company. Reprinted by permission of Addison-Wesley Educational Publishers.

38

2. The Envelope

FIGURE 2.25 A variety of tidal curves from ports scattered around the Earth, September 1958. After Gross (1982).

can be, for those organisms able to withstand its rigors successfully, competition and predation are generally reduced and for the plants both maximum light and a very reliable water supply can be achieved. The intertidal zone itself is often strongly subzoned, and such zonation can be related to patterns of tidal form and height. Typically, worldwide, the basic pattern of zonation from top to bottom in the rocky intertidal is: (1) a black band of blue green algae and lichens (in the spray zone or just at or above the highest regular

tides); (2) a periwinkle snail or littorinid snail zone (roughly the upper half of the tide zone); (3) a white and very rough barnacle zone (the lower half of the regular tide); and finally (4) a mussel zone between neap and spring low tides. Specific areas have even more characteristic communities, such as the rockweeds (brown algae) and Irish moss (red algae) of the North Atlantic (see Chapter 21). Some of the most interesting marine and estuarine plants and animals richly occupy the intertidal zone and form unique and highly productive


communities (Figures 2.26 and 2.27). In more protected areas salt marshes and mangrove swamps cover many square miles and provide extensive habitats for intertidal organisms, insects, and birds. These too are strongly zoned to the tide (see Color Plate 40), even when beyond the limit of salt water (Odum et al., 1984). Extensive mud flats, often found in protected areas having extreme tide ranges, can become rich reservoirs of organic particulates. These organic-rich, muddy bottoms are largely derived by wash-in from more exposed areas and from streams and rivers. Tidal flats are occupied by a host of small invertebrates, including many clams prized as human food.

Tides and the Model Ecosystem While a few research systems have been built particularly to investigate the effects of oil on rocky shores and marshes, and some of the more progressive public aquaria have constructed ecological models to show the effects of tides in appropriate tanks, tidal models are rarely constructed. This situation is peculiar since accomplishing a rather accurate intertidal simulation is not difficult.

39

Whether tides should be considered a factor in a microcosm depends on the marine community being simulated. None of our coral reef tanks, all based on Caribbean reefs, has had a tidal element. While in some places of very high wave energy the intertidal algal ridge is one of the most fascinating communities on Caribbean reefs, for most reefs in this region tides are relatively unimportant. On the other hand, on the Australian Great Barrier Reef, tides of 3–10 feet (1–3 meters) are an extremely important ecological element. The Great Barrier Reef Marine Park reef aquarium in Townsville, Australia, provides a moderate tide range. In the simulations of the rocky Maine coast and Chesapeake Bay and the Florida Everglades described in this book, tides were too important to ignore and are critical elements. Developing a tidal system in a closed microcosm is in part a matter of time-regulating higher and lower water levels. This is most easily accomplished by temporarily storing water at times of low tide in a separate reservoir (Figure 2.28, and Figures 22.8 and 22.9). The tidal reservoir can also serve as a fine-sediment settling trap and refugium for the numerous worms and small crustaceans that characterize deeper-water mud bottoms. As we discuss throughout this book, refugia and

FIGURE 2.26 The vertical zonation of organisms occurring on intertidal rocky shores on the Pacific coast. Reprinted from Ricketts et al. (1985), revised by David W. Phillips, with the permission of Stanford University Press.

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FIGURE 2.27 The vertical zonation of intertidal organisms on hard bottoms of the Atlantic coast. Modified after Gosner (1978). Reprinted by permission of Houghton Mifflin Co.

FIGURE 2.28 Photograph of tidal controller attached to a tidal reservoir on the Maine coast microcosm. The center motor rotates approximately twice a day to create the semidiurnal component. The outer motor rotates once every 2 weeks to create neaps and springs.

41


settling traps are critical elements of model ecosystems that allow the simulation of much larger wild environments. If it is desirable to save space, two separate reservoir systems or two separate parts of the same tank can be operated on alternate tide cycles. In our Florida Everglades mesocosm, the estuary served as the tidal reservoir for the Gulf of Mexico portion of the system. Pumps first pumping in one direction (to the reservoir) and then in the other direction (back to the main tank) can also be used; however, unless a complicated multiple pump arrangement is employed, the result is a sawtooth tidal pattern rather than the sinetype curve of the wild. The sawtooth curve reduces by about 25% the total times of high and low tide. We have designed a water-level tidal management system based on interval timer control of stepping motors (Figure 2.28 and Color Plate 41; see also Figures 22.7–22.9). This method creates pure semidiurnal tides and provides for biweekly springs and neaps as well as for the 50 minutes’ daily timing advance to “follow the moon.” The approach is generally trouble-free and inexpensive. The system can easily be adapted to a diurnal tidal cycle simply by changing the timing on the primary stepping motor drive. Stepping motor control can be modified to simulate virtually any tidal cycle, even a mixed diurnal/semidiurnal tide. Mud flats and rocky shores are relatively easy to establish and manage in an intertidal microcosm. Some care should be taken to stock organisms at their proper zonal level, and this can be quite difficult when a large vertical tidal zone in the wild analog is reduced to a relatively narrow zone in the model. However, community adjustments in the microcosm generally develop slowly over many months without detrimental effects. Rocky intertidals in particular are adjusted in the wild to wave action, with given zonal bands being higher with increased wave action (Figure 2.27). Also, rocky intertidals are notoriously patchy, with the effects of settlement, wave action, local terrain, and local predation varying widely. These effects have been favorite subjects for studying the dynamics of community structure (see Haywood, 2004). In an aquarium or small mesocosm, the available shore can become a single patch changing from time to time. The process can be altered and directed by the “disturbance” of the aquarist. Algal, mussel, and barnacle zonation on the rocky intertidal of an aquarium system, with the grazers and predators that occupy the same environment, can be an exciting model to manage. Marsh communities are considerably more sensitive to tidal levels than rocky intertidals. In microcosms of small or microtidal ranges (less than 2 feet in the wild), it is important to place the sod surface of marsh grasses at the equivalent tidal level so that total exposure (and

submergence) times in the microcosm are the same as in the wild. Marsh vertical ranges are always much smaller than the total tide, generally occupying only the upper half of the tide range.

References Adey, W. and Hackney, J. (1989) Harvest production of coral reef algal turfs. In: The Biology, Ecology and Mariculture of Mithrax spinosissimus Based on Cultured Algal Turfs. W. Adey (Ed.). Mariculture Institute, Washington, DC. Adey, W. and Loveland, K. (1991, 1998) Dynamic Aquaria: Building Living Ecosystems, 1st and 2nd edn. Academic Press, San Diego. Adey, W. and Steneck, R. (1985) Highly productive eastern Caribbean reefs: synergistic effects of biological, chemical, physical and geological factors. In: The Ecology of Coral Reefs. M. Reaka (Ed.). NOAA Symposium Series on Underwater Research, Vol. 3. Washington, DC. Adey, W. and Steneck, R. (2001) Thermogeography over time creates biogeographic regions: a temperature/space/time-integrated model and an abundance-weighted test of benthic marine algae. J. Phycol. 37: 677–698. Bansal, N. and Doremus, R. (1986) Handbook of Glass Properties. Academic Press, Orlando, Florida. Briggs, J. C. (1974) Marine Zoogeography. McGraw-Hill, New York. Carpenter, R., Hackney, J., and Adey, W. (1991) Measurements of primary productivity and nitrogenase activity of coral reef algae in a chamber incorporating oscillatory flow. Limnol. Oceanogr. 36: 40–49. Carson, R. (1962) Silent Spring. Fawcett Crest, New York. Climap Project Members (1976) The surface of the ice-age earth. Science 191: 1131. Gosner, K. (1978) A Field Guide to the Atlantic Seashore. Petersen Field Guide Series, Houghton Mifflin, Boston. Gross, M. G. (1982) Oceanography: A View of the Earth. Prentice Hall, Englewood Cliffs, NJ. Haywood, P. (2004) A Natural History of the Seashore. Collins, London. Hutchinson, G. E. (1957) A Treatise on Limnology, Vol. 1. Wiley, New York. Jones, M. (1988) The Great Barrier Reef Aquarium: A Matter of Scale. Northern Reg. Eug. Conf. (Australia), Townsville, June 10–13. Kennett, J. (1982) Marine Geology. Prentice Hall, Englewood Cliffs, NJ. Kremer, J. and Nixon, S. (1978) A Coastal Marine Ecosystem Simulation and Analysis. Springer-Verlag, Berlin. Leigh, E., Paine, R., Quinn, J., and Suchanek, T. (1987) Wave energy and intertidal productivity. Proc. Natl. Acad. Sci. USA 84: 1314–1318. Levinton, J. (1982) Marine Ecology. Prentice Hall, Englewood Cliffs, NJ. Levy, S. and DuBois, J. H. (1984) Plastics Product Design Engineering Handbook. Chapman and Hall, New York. Marino, B. D. V. and Odum, H. T. (1999) Biosphere 2, Research Past and Present. Elsevier Science. An Elsevier Science Publication, Ireland. Reprinted from Ecological Engineering Spec. 13(1–4). Marra, J. (2002) Approaches to the measurement of plankton production. In: Phytoplankton Productivity. P. J. leB. Williams, D. Thomas and C. Reynolds (Eds). Blackwell Science, Oxford. Nixon, S. (1988) Physical energy inputs and the comparative ecology of lake and marine ecosystems. Limnol. Oceanogr. 33: 1005–1025. Odum, W., Smith, T., Hoover, J., and Mclvor, C. (1984) The Ecology of Tidal Freshwater Marshes of the United States East Coast: A Community Profile. U.S. Fish and Wildlife Service OBS-83/17. Palmer, J. (1995) The Biological Rhythms and Clocks of Intertidal Animals. Oxford University Press, London.

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Price, J. (2005) Chesapeake Bay an Undeclared Ecological Disaster. Chesapeake Bay Ecological Foundation. On-line piece, Sunday, October 23, 2005. Raffaelli, D. and Hawkins, S. (1996) Intertidal Ecology. Chapman and Hall, London. Ricketts, E., Calvin, J., Hedgpeth, J., and Phillips, D. (1985) Between Pacific Tides, 5th edn. Stanford University Press, Stanford, CA. Spotte, S. (1995) Captive Seawater Fishes. Science and Technology. Wiley, New York.

Thurman, H. and Webber, H. (1984) Marine Biology. Addison-Wesley Educational Publisher, Menlo Park, CA. Vannote, R. and Sweeney, B. (1980) Geographic analysis of thermal equilibria: a conceptual model for evaluating the effect of natural and modified thermal regimes on aquatic insect communities. Am. Nat. 115: 667–695. Walter, H. (1979) Vegetation of the Earth, and Ecological Systems of the Geo-Biosphere. Springer-Verlag, New York.

C H A P T E R

3 Substrate The Active Role of Rock, Mud, and Sand

In the first two editions of this book, we emphasized the construction of living models or microcosms and mesocosms of aquatic ecosystems. Our logic at that time in presenting a background chapter on geology, including the origin of the rocks that provided the base of some aquatic ecosystems and the sediments that provided the base of other ecosystems, was that the nature of the substrate was critical to the character and function of the ecosystem being modeled. Also, the salinity of the oceans and coasts and the chemical composition of fresh waters is determined by the nature of the rocks over and through which the water flows. This might have seemed quite remote for the oceans, but now we know more about the hydrothermal vents along ocean ridges and how sea water is constantly circulating and chemically interacting with hot and even liquid ocean crust (van Dover, 2000). Also, with human mining, and coal and oil extraction from the Earth’s crust, we have become aware of the extensive changes to streams and rivers, the Earth’s atmosphere and even the chemical character of the oceans (e.g. Kleypas et al., 1999). In this edition, we have changed our focus somewhat and argued that all ecosystems on Earth are controlled by human activity and are in effect macrocosms. It is simply a matter of scale between the microcosms and mesocosms that we build for research, education or hobby, and those macrocosms, altered by human activity, that we seek to restore to a pre-industrial state (or at least rehabilitate). In ecosystem restoration, it is even more important that the restorer understand the geological background and framework of the ecosystem being treated. Although here we present a basic background in geology and sedimentology, we recommend that the modeler and restorer, before initiating work, review one of the broader texts that have evolved in the

last decade to bring the relatively new science of plate tectonics into a modern framework that includes the life sciences (e.g. Redfern, 2001; Marshak, 2004). That review should be followed by a more detailed examination of local geology and sedimentation. Lithospheric activity, centered on plate tectonics, determines the shapes of seas and oceans and greatly constrains open ocean currents. The position of continents, also constantly moving, relative to the Earth’s axis, along with the major ocean currents, over geological time is a very important factor in global climate. Even more directly, along coastlines and mid-ocean ridges, and of course in fast-moving streams and along the shores of larger lakes, rock provides a surface to which organisms attach and from which they interact in myriad ways with the aquatic environment. The processes of weathering, transportation, and sedimentation, whether on continental shelves or in the deep ocean, result in the constant geological-scale sequestering of carbon and other nutrient and mineral (i.e. elemental) requirements used in the building of living cells and tissues. Thus, ultimately, the underlying lithosphere or rock, in its interaction with the atmosphere and the hydrosphere, or liquid water envelope, determines the concentrations and thus the availability of many of the basic chemical building blocks of life in the ocean. Except in closed basins and areas of high evaporation relative to precipitation, fresh waters are transient sites for elements, mostly in low concentrations, on their way to the sea. It is perhaps not unreasonable for the modeler or aquarist working on an oceanic plankton community to regard the ocean characteristics, for all practical purposes, as independent from the lithosphere. For the ocean restorationist, however, that would not be the

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case, for most ocean and coastal pollution today derives from land/river/bay run-off. And for benthic (bottom), shoreline, and of course stream, river, and lake shore situations, the presence and nature of the rock bottom, and the sediments derived from those rocks, can be crucial to the function of both a wild ecosystem and its model. It might make the modelers’ endeavors easier to regard that surface of rock as a theoretical boundary, an attachment but nothing more, like the glass of the model’s wall. Perhaps in some cases, a smooth basalt bottom for example, this might actually be the case. In most cases, however, the geological world is less remote from the needs of the modeler or ecological restorer than a preliminary look might suggest.

THE SOLID EARTH AND LIFE The Earth, as viewed from space, with approximately 70% of its surface covered with water, would be most appropriately called “planet water.” The size of the Earth, its distance from the sun, and its moderate level of internal energy production have allowed it to retain a massive volume of water (in the liquid state). This water, as we described in Chapter 1, was probably brought to Earth early in its development by comets. However, the retention of the water, more than any other single factor, has led to the development and evolution of life. However, if the hard surface of the Earth, the lithosphere, were smooth (i.e. nearly spherical), then the solid Earth would be covered uniformly with approximately 2600 meters (8000 feet) of ocean. Although life probably would have developed and evolved under such a regime, without a more active inclusion of the lithosphere in the atmosphere–hydrosphere interaction, it would certainly be far less diverse. Probably it would still be very primitive, as it was several billion years ago.

Our planet still has considerable heat (from gravitational collapse and radioactivity) in its hot, liquid or semi-liquid interior. The hard, semi-plastic crust of the Earth caps a slowly churning mantle cauldron. This has given rise to a rather remarkable evolution of the surficial crust that has been a major catalyst to the evolution of life and in many ways determines and constrains its ecology today. The “boiling up” of this mantle cauldron has gradually concentrated relatively light minerals particularly rich in silica, aluminum, and potassium in scattered “floating mounds” called continents, which are raised above the generally heavier calcium-, magnesium-, and iron-rich crust of the Earth (Figure 3.1). The oceans, occupying primarily the deeper parts of this twolevel surface (Figures 3.2 and 3.3), have a mean depth of 3730 meters, while the continents are slightly raised (above sea level) to an average height of 870 meters. Through the process of plate tectonics (continental drift), the boiling up of the Earth’s cauldron is constantly splitting the crust, changing the shape of both continents and oceans (Figure 3.4). When pieces of the crust driven by the cauldron collide, earthquakes, mountain chains, and sometimes very active volcanoes are created and ocean levels are changed (Marshak, 2004). Thus, there has been throughout much of the Earth’s history, and is certainly on-going today, a very active relationship between the Earth’s lithosphere, with its minerals and elements, and the hydrosphere, the originator of life. This relationship is strengthened by the continuous formation of limestone and other sediments in which living or recently dead organisms play a crucial role. Sedimentary rocks or structures include those that are formed largely by the skeletons or even the organic matter of dead organisms (coal, oil shales). The Earth’s crust is a melange of rocks created by tectonic and volcanic activities, and the results of the reworking of those rocks by atmospheric and hydrospheric processes.

FIGURE 3.1 Schematic section of the crust of the Earth at about 3.8 billion years BP. Prior to this point most of the crust was oceanic (basaltic), and creation of crust at ocean-spreading centers (a) was followed by subduction back into the mantle with little change. At the time shown, the fractionated lighter material of future continents (b) has been minimal and usually subducted with the basaltic crust (1). However, larger pieces (2) are beginning to survive, eventually leading to full continent formation. From Lowe (1994).

The Solid Earth and Life

FIGURE 3.2 Hypsographic curve of the distribution of the amount of Earth surface at different elevations. After Kennett (1982).

FIGURE 3.3 Worldwide plate system showing the placement of “raised” continents and oceanic crust with its deep ocean. Continental margins are shallow coastal areas, presently submerged but belonging to continents, and are shown cross-hatched. The ocean ridges form over hot up-flowing areas in the underlying mantle and are sites of new ocean crust formation. Ocean crust slides away from the ridges and sinks and melts in the subduction zones. Volcanic hot spots are mostly on ridges or subduction zones, though a few (like the island of Hawaii) are isolated beneath either ocean crust or continents. After Gross (1982).

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FIGURE 3.4 Development of oceans through seafloor spreading: (A,B) formation of rifts; (C) rift valley with lakes stage (see Figure 3.5); (D) “Red Sea” stage; (E) young ocean stage, subduction started on right; passive margin on left. After van Andel (1985).

Crucial additions to an already active rock, water, and atmosphere interface, changing mostly on the scale of many millions of years, are major alterations of overall Earth climate on the scale of tens to hundreds of thousands of years. Partly due to slight cyclical changes

in solar radiation and the orbit and rotation of the Earth, and partly due to the change of the positions of continents and sea bottom relative to ocean currents, cooling of the poles results in large-scale glaciation. These “continental” glaciers produce both radical alterations in

The Solid Earth and Life

47

FIGURE 3.5 Formation of large continental lakes by rifting of the Earth’s crust. After Burgis and Morris (1987).

rock weathering (by ice) and sea-level changes. Even in mid-latitudes, sea-level changes resulting from the locking of water in ice caps near polar regions and the bending of the Earth’s crust as weight distribution of ice and water changes result in marked alterations of both coastal areas and, as the gradient changes, the lakes and streams that drain into them. In addition, while some lakes and rivers can result from tectonic effects, for example, the African Rift Valleys (Figure 3.5) and the Andean lakes, the majority of lakes and drainage in high latitudes results from either the scouring or the mounding-up of sediment by glaciers. The Great Lakes

in North America are an example of this process. Elsewhere, a variety of local factors such as volcanism, beach drift along the shore, rivers that change their course, and of course human activities result in lake and estuary formation. Stream formation results from the run-off of rain working against tectonism, that is, major Earth movements, and the relative resistance of the underlying rocks to stream erosion. Clearly human activity can radically alter many of the above described relationships and ecological restoration is equally possible as long as these relationships are understood and managed.

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CHEMICAL RELATIONSHIPS BETWEEN ROCKS, SEA WATER, AND ORGANISMS The universe is heavily dominated by the very light elements of hydrogen and helium in the atomic fires of the stars (see Figure 1.1 in Chapter 1). As the temperatures of these fires degrade, as a star ages or as fragments are spun off in collisions or super novae, heavier elements are formed. In general, with increasing atomic weight, elements decrease in abundance according to a

logarithmic curve. In small planets near the sun, such as the Earth, the lightest elements are lost to space. The net result for the crust of the Earth (Figure 3.6) is a skewed logarithmic, normal curve of abundance with the lightest elements depleted, the light to mid-weight elements from oxygen to iron most abundant, and heavier elements scarce to rare. The very unreactive noble gases, helium, neon, argon, etc., are anomolously low in abundance. Pure water, possibly fractionated from the crust early in the Earth’s cooling cycle, was more likely

FIGURE 3.6 Diagram showing the abundance of chemical elements in the Earth’s crust in relation to the use of those elements by living organisms. The principal elements of life (CHON) are light, relatively abundant, and also form water and the Earth’s atmosphere. It is significant that nitrogen is the least abundant of the principal life elements in the crust, requires energy to remove from the atmosphere, and is the most critically limiting nutrient in the aquatic environment. The remaining organic macronutrients are drawn from the elements that form the salts of the sea, which in turn are the next heavier and most abundant elements of the Earth’s crust. The micronutrients (with the outliers molybdenum and iodine) are the lesser abundant and/or heavier elements of the main group. Note that aluminum, titanium, chromium, and nickel lie within the main group and are essentially unused by organisms. Modified after Bricker and Jones from Salbu and Steinnes (1995) and Parker (1967).

Chemical Relationships between Rocks, Sea Water, and Organisms

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FIGURE 3.7 Concentration of some elements of sea water in relation to residency time of those elements in sea water. Data derived from Millero and Sohn (1992) as mean of river input and sediment rate calculations.

“rained-in” from space later. Virtually all chemical elements occur in the sea, as we shall see in Chapter 4. However, the heavier elements are poorly represented. The dominant elements dissolved in ocean water are mostly those that are also moderately abundant in the Earth’s crust. However, the proportions are not the same primarily because in the Earth’s crust most elements appear as components of minerals. As the minerals of a rock exposed to atmosphere, rain, and inorganic and organic acids dissolve in water, some elements are very mobile and move easily into streams flowing to the sea. Others tend to be re-bound in new minerals and stay in the crust or in sediments. To make matters more complex, sedimentation tends to further fractionate some elements (e.g. calcium, carbon, and magnesium) into new sedimentary rocks, and these rocks, common in terrestrial environments, tend to

react more with the water cycle than the igneous rocks. Ultimately, the concentration of elements in sea water is a function of their residence time (Figure 3.7) as determined by rate of incoming (from rivers) and outgoing (to sediments). Thus, of the top 12 elements, by weight, in the salts of sea water, chlorine at 19 000⫹ mg/liter in sea water forms only about 0.03% of the Earth’s crust, while silica, the dominant element of the Earth’s crust (28.5%) is an important, but minor component of sea water (4 mg/liter). The top six elements of sea salt (chlorine, sodium, magnesium, sulfur, calcium, and potassium) are all “conservative.” They are required by organisms and concentrated to some degree, especially calcium. However, their relative requirement is minimal and the concentration of the large quantity in the sea is not affected by the activities of organisms. Many of the

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primary chemical components of organisms (carbon, nitrogen, and oxygen) relate more to the Earth’s atmosphere (and are gases dissolved in sea water) than to sea salts. Oxygen and hydrogen can enter the biosphere through the splitting of water in photosynthesis. However, phosphorus, iron, and silica, ultimately derived from dissolution of the Earth’s crust, are organically required elements in sea water that can be very limiting to the production of plants and therefore animals. In very pure (oligotrophic) waters, other elements can also limit plant production, though such limitation usually relates only to calcium, magnesium, or potassium. In general, the chemistry of life utilizes light elements (less than atomic number 35) that are also abundant and reactive. However, elements that tend to form insoluble compounds or become locked up by mineralization processes have generally been “avoided” by organisms. In the universe, aluminum is more abundant than sodium and calcium, and in the Earth’s crust it is lesser only than oxygen silica in abundance. However, it approaches being rare in sea water, having a residence time of about 100 years, and is unused by organisms. Iron is also one of the more abundant elements in the universe and in the Earth’s crust. Because it readily oxidizes to insoluble forms, its abundance in the sea is very low. However, it is crucial to all organisms. It can be surmised that before algae provided oxygen gas (dioxygen) in abundance to the Earth’s atmosphere (and ocean) iron was abundant and it became key to many life processes. It is possible that “life” nearly extinguished itself, a few billion years ago, by producing oxygen, which then combined with iron (as iron oxide) to deplete this element from the seas. Some scientists have suggested that replacing iron in the open ocean, through a massive, human industrial chemistry-type operation could solve the problem of excess atmospheric carbon dioxide by increasing open ocean photosynthesis now limited by lack of sufficient iron. More recent field research has indicated that the effects are minimal and the costs high, and as we discuss in Chapter 25, there are other routes to increasing photosynthesis at large scale that are more efficient and provide additional benefits (see ATS). However, this is the kind of global scale restorationist thinking that is required to solve our overwhelming dominance of the biosphere.

THE SOLID EARTH, ROCK, AND MODEL ECOSYSTEMS It may seem remote to equate the activity of the lithosphere with the Earth’s water on a geological scale to that relationship over a few years in an aquarium or

mesocosm. However, because of the scaling factor the substrate can be crucial when interfacing with a small, enclosed body of water. Of course, rocks (or gravel) that are iron-rich, lead-rich, arsenic-rich, etc., particularly in a small system, cannot be used without an understanding of the export mechanisms of those elements from the system (see, e.g. Chapter 11). It is particularly important to ask what rock substrate is in contact with the ecosystem to be modeled in the wild: for example, carbonate rock for a reef, marine, or any hard-water system, or a silica-rich hard rock for a black or other soft-water ecosystem. Buffering and the carbon dioxide/pH cycle in relationship to carbonate substrate are specifically discussed in depth in Chapter 8. Rock substrate is often crucial in structuring a community in that it supplies a secure base for those organisms able to tightly attach. In addition, the spaces of cracks or voids, sometimes abundantly available, provide greatly increased surfaces for attachment and spaces for hiding. The aquarist should try to match the configuration, or spatial heterogeneity, of the wild analog as closely as possible, and the restorationist may need to consider the changes that could have occurred due to human activity (e.g. a sediment coating on rock surface). However, the sediments, in themselves, are a more critical concern, and that is what we concentrate on here. Generally, whether dealing with a fresh- or a saltwater environment, there is a strong relationship between current and wave energy and the coarseness or fineness of the bottom sediments (Figure 3.8). In microcosms, mesocosms, and aquaria, sediments that have the same physical characteristics as those in the systems being modeled should be used. Strong wave action or currents, whether on exposed lake or ocean coasts or in a mountain stream, give rise to exposed bedrock or large cobbles or boulders providing a bare (or usually algalcolonized) rock. In an aquarium or mesocosm environment, if these surfaces are to be preserved as in the wild, equivalent or at least sufficient wave or current action must be present. Otherwise the surface will become coated with fine sediment and will fail to recreate the wild ecosystem. There is a major difference between a bare rock bottom to which organisms must attach (or bore as in softer rocks), and over which water must have considerable motion, and a sediment bottom. As we discuss further in Chapter 23, in fresh-water environments, human changes have often meant changing the water energy/sediment relationships, and these are the first corrections that need to be made. In Chapters 20–23, we discuss a variety of ecosystems in mesocosms and aquaria with and without bare rock and coral rock substrate. It is best to discuss these on an individual basis, because the very layout of this

Sediments and Model Ecosystems

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FIGURE 3.8 Relationship between the movement of sediment and the grain size of the sediment as a function of water velocity. After Davis (1983).

substrate often provides the primary habitat for the ecosystems. This chapter mostly deals with finer substrate, and although there is considerable overlap with Chapters 6 and 18, the generalities will be discussed here.

SEDIMENTS AND MODEL ECOSYSTEMS As quieter water is approached, whether in widened areas or billabongs (ox bow lakes) in a stream, in a lake small enough to prevent large waves, or in a bay or coastal lagoon along a sandy coast, the sediment becomes progressively finer from gravel, to sand and silt, to a soupy, silty-clay mud. Coarse sands or gravels are perhaps the most difficult benthic environments for organisms to adapt to, and there are relatively few species within sand and gravel habitats. To remain sand, the bottom must stay in motion (and clay and silt remain suspended), and therefore special adaptations are required by any organisms that will inhabit such bottoms. A few larger animals, such as the Donax clam and the amphipod Neohaustorius have developed rapid burrowing techniques (Figure 3.9). The mole crab familiar to beach naturalists along the extensive mid-Atlantic US outer banks is another example. Otherwise, organisms must be small (less than 0.5 millimeter) and worm-like, so that the sand grains appear large to them, and have the capability to rapidly burrow: these are the relatively poorly known meiofauna (Higgins and Thiel, 1988) (Figure 3.10). Even bacterial numbers tend to be limited in sand and gravel since their organic substrates are often “washed out” (Table 3.1). Sandy shores have a rather long profile in the energy regime required to keep them sandy. In model construction there is little use in trying to sandwich a

sandy beach between a dune and a wave-broken sandy bottom within a few meters. It does not work in the wild, as many coastal landowners have found to their chagrin, and it does not work in an aquarium or mesocosm (Figure 3.11; Chapter 22). With difficulty, sandy beaches can be simulated in mesocosms. In aquaria and microcosms, it is extremely difficult, unless it is the only community included. As we discuss in Chapter 12, the break between high-energy shores with rock or mobile sand substrate and a quieter mud or sandy-mud bottom is ecologically great. We treat them as separate biomes, the highest community level differentiation. Generally, algae occupy the highly disturbed but stable rocky shores and higher plants (marsh plants and submerged aquatics) dominate the finer, less energetic shores. Even in a lake this differentiation is apparent. Large lakes lack reed beds on most shores (except in protected coves), and very small lakes are usually continuously rimmed with emergent aquatic flowering plants. In the ocean, this relationship is also apparent. The outer shores, depending on sediment supply, range from rock with more or less abundant macroalgae to bare sand. Mostly, the only plants from the high-water line seaward on rocky bottoms are algae (including lichens). On the other hand, in deeper waters, in protected bays, or behind reefs and barrier islands, mud bottoms prevail and the marsh communities and their flowering plants dominate the landscape. Finer sediments, sandy-silt to silty-clay mud, typically have a very rich fauna, usually richer than a rock or boulder surface, though probably not richer than a coral reef. On a typical rocky shore, there are dozens of common species of algae, barnacles, snails, and small crustaceans in what appears to be an extremely rich

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FIGURE 3.9 Two moderate-sized invertebrates from a sandy surf zone. The sand digger (Neohaustorius) (D) and the clam Donax (A–C) are among the few macrofauna to adapt to the sandy surf zone. After Thurman and Webber (1984). (A–C) Copyright © 1984 by Scott, Foresman and Company. Reprinted by permission of Addison-Wesley Educational Publishers. (D) After Lippson and Lippson (1997), The Johns Hopkins University Press, drawing by Alice Jane Lippson.


FIGURE 3.10 Meiofauna (small invertebrates, less than 1 millimeter and greater than 42 µm) in relation to fine sand grains. Three phyla are represented: (A) polychaete worm; (B) mollusk; (C) arthropod; (D) polychaete worm; (E) arthropod mite. After Thurman and Webber (1984). Copyright © 1984 by Scott, Foresman and Company. Reprinted by permission of HarperCollins Publishers.

TABLE 3.1 Numbers of Bacteria in Sediments of Differing Grain Sizea

Sand Silt Clay Colloidal sediment

Grain size (µm)

Water content (%)

Bacteria (ⴛ 10–3/gⴚ1)

50–1000 5–50 1–5 ⬍1

33 56 82 ⬎98

22 78 390 1510

a

After Rheinheimer (1985).

FIGURE 3.11 Generalized characteristics of sandy beaches and of wave action on those beaches. After Kennett (1982).

rocky intertidal and subtidal flora and fauna. On the other hand, in the very uniform and often vacantappearing muds on the bottom of adjacent bays, hundreds of species of worms, amphipods, and clams, to mention a few, are largely hidden beneath the surface. An examination of numbers of macroinvertebrates occurring in the soft sediments of 13 estuaries and bays

53

scattered around the world yielded figures from 722 to 30 000 individuals/m2, the mean number being 7400 individuals/m2 (Maurer et al., 1978). Some of the life habitats of these organisms are shown in Figure 3.12. The communities of such bottoms can also change radically with time and location over several miles. Sometimes they can be quite patchy even on a local scale (Figure 3.13). Functionally the same kinds of organisms occupy muddy bottoms in fresh waters. However, here the insects, particularly larval forms (Figure 3.14), almost absent from the marine environment, become extremely abundant, while the dominant worms are oligochaetes (earthworm relatives) rather than polychaetes. Muddy bottoms are typically collection areas for large quantities of fine organic material from “producer ecosystems” such as coral reefs and rocky shores to mud flats and lagoons, or from terrestrial sources such as forests and fields to streams and lakes. This abundant food source gives rise to the rich diversity of species and feeding types that typically occupy the mud or sandy-mud bottom. In spite of the very active reworking of the mud by the infauna, or by fish, crabs, and even diving birds seeking food, the abundant bacterial activity on the organic particulates provides for strong oxygen utilization. Anaerobic conditions typically exist close to the surface, and hydrogen sulfide production occurs within a few centimeters (Figure 3.15). This sediment chemistry is very different from that of most soils in the terrestrial environment and provides a strong control on the structure and function of the biological community. This leads in turn to a limitation of the fauna to those animals that can reach the water/sediment interface or can pump oxygen-rich water through their tunnels. Some animals in this situation have high levels of oxygen-carrying compounds in their bloodstreams or in a few cases have the capability of surviving anaerobically, at least partially, through fermentation. In fresh waters (see Chapter 23), large numbers of submerged aquatic flowering plants tend to dominate over the algae on shallow sediment bottoms (Table 3.2). Although in proportion to terrestrial environments, few species of flowering plants occur in the sea (Figure 3.16), those that do occur can occupy very large areas of shallow, well-lighted bottoms. In the tropics, mangroves (aquatic trees) form very extensive swamps in muddy marine or brackish intertidal zones (see Chapter 22). In colder waters, grasses and sedges develop broad wet grasslands, or marshes, in the same habitat. As we have reviewed above, fine sediment bottoms in the wild are typically very active and rich communities that are important components of their ecosystems. This flora and fauna should also be equivalently

54

3. Substrate

important in mesocosms and aquaria. If enough light is present, algae and flowering plants (particularly in fresh water) are able to photosynthesize and to provide new production directly to grazers or to detritus in the community. Algae derive most if not all of their nutrient supply directly from the water. Many of the higher plants, however, extract their nutrient needs from the sediments (as on land). This provides an important link between buried organic materials and their nutrients and the overlying water. Equally important, the algae, and especially the flowering plants, act to trap and thereby increase sedimentation processes that are often needed in model ecosystems. In general, this is an extremely important issue for the aquatic restorer. A good example are the processes that are leading to the loss of wetlands in the Mississippi delta. With levees transporting fresh water directly to the Gulf of Mexico and cut channels bringing salt water into the fresh/brackish marshes, the extensive silt-trapping submerged and emerged aquatic plant marshes are disappearing making the entire region vulnerable to destruction by hurricanes. As we have noted, whether shallow or deeper, fine sediment bottoms are generally receivers of abundant organic detritus, plant fragments, dead animals and animal parts, and animal feces (Figure 3.17). Much of this “waste” organic material tends to be infractile to higher animals. On the other hand, it is easily utilized and fully broken down to carbon dioxide, water nutrients, and minerals by a host of bacteria. Most of the bacteria are, in turn, utilizable as food by many inhabitants of the sediment bottom, particularly clams, worms, and insect larvae. Even though the sediment tends to be anaerobic at or immediately below the surface, many

organisms are able to work the rich organic load by drawing in oxygenated water from above the mud. Traditionally, aquarium practice has been to avoid the natural detrital processes and to keep the equivalent bacteria in filters that to some extent act like a very reduced bottom community. However, in a filter the

FIGURE 3.12 Selected infauna from muddy marine bottoms. (A) left to right Macoma clam, cockle, polychaete worm, Mya (soft shell clam), polychaete worm, and snails; (B) Arenicola, a polychaete worm – the food is organic particulates in the sediments, water moved through is used to receive oxygen; (C) Chaetopterus polychaete worm – a feeder on detritus particles suspended in the water column; (D) Amphitrite, a polychaete worm that feeds on surface deposits of organic particulates. After Thurman and Webber (1984). Copyright © 1984 by Scott, Foresman and Company. Reprinted by permission of HarperCollins Publishers.


FIGURE 3.13 Results of the analysis of the soft bottom macroinvertebrate (greater than 1 µm) communities from Delaware Bay in two successive years (1972; 1973). Although most of the same species occur in the 2 years, none of the “community” groupings is obviously the same. This analysis includes 169 species: 40.8% annelid worms; 28.9% arthropods; 17.8% molluscs; 7.1% bryozoans; and 5.4% miscellaneous phyla. By feeding types the species could be grouped as 45% deposit feeders; 24.8% suspension feeders; 18.3% carnivores; 10.7% omnivores; and 2.2% miscellaneous. After Maurer et al. (1978).

55

56

3. Substrate

FIGURE 3.14 Life cycle and predators of mayflies. The flying stage is reproductive only and lasts for quite a short time. The larval stages of many species are burrowers in soft sediments of lakes, ponds, and streams. After Burgis and Morris (1987).

FIGURE 3.15 Distribution with depth of oxygen and hydrogen sulfide in a muddy bottom. This profile typically occurs over a few to at most a few tens of centimeters from the mud/water surface. After Levinton (1982). Reprinted by permission of Prentice Hall, Englewood Cliffs, New Jersey.

TABLE 3.2 Plants Dominating Sediment Bottoms in Temperate Lakes and Their Patterns of Change with Time (Succession)a Trout Lake (Wisconsin)

The English (Cumbrian) lakes Successions in deep water

Overall line succession and decrease in depth of water

Soil type

Successions in shallow water

Very fine, rich, inorganic silted substrates with little organic matter

Increase in fineness and richness of silt

Najas

(Nitella)

Isoetes

Submerged linearleaved association (especially Potamogeton spp.)

Potamogeton pusillus

(Nitella) Potamogeton

Potamogeton obtusifolius

Potamogeton praelongus

Sparganium minimum

Potamogeton alpinus

Nymphaea and Nuphar

Stony and sandy substrates poor in basic silts, and eventually organic

Fine inorganic soils with continued silting Littorella

Increase in organic content

Largely organic soils with sparse silting

Funcus bulbosus var. fluitans

Myriophyllum– Potamogeton– (Nitella)

(Chara)– Najas– Potamogeton (Chara)– Najas– Vallisneria

Potamogeton Funcus perfoliatus bulbosus var. fluitans Nymphaea or Nuphar

Potamogeton natans

Severe wave action; rather coarse gravelly and sandy substrates

Ceratophyllum Linear-leaved Potamogeton spp.

Lobelia

Myriophyllum

Sheltered soils rich in silt and organic sediment

Exposed to slight waves; silted and sandy soils with some organic sediment

Typha

Schoenoplectus– Phragmites

Potamogeton natans

Carex or Equistum

Nymphaea– Potamogeton– Sagittaria

Elodea– Najas– Potamogeton

Sagittaria– Sparganium– Typha

Eleocharis– Equisetum– Schoenoplectus

Isoetes– Funcus– Lobelia

Barren a

In all the above successions, only the dominant(s) of each community is indicated. Algal dominants are enclosed in brackets. After Sculthorpe (1985).

58

3. Substrate

5 mm

FIGURE 3.16 Characteristic marine flowering plants from muddy sand and muddy bottoms: (A) the tropical Thalassia testudinum (turtle grass), a dominant of many reef lagoons; (B) the cold-water Northern Hemisphere Zostera marina (eelgrass). Note that neither species is a true grass. After Dawes (1981). Reprinted by permission of John Wiley & Sons, Inc.

variety and capability of the bacteria are limited. Few or no animals are present to eat the bacteria and, in turn, fish and larger invertebrates do not have a rich, smaller invertebrate bottom on which to browse. Thus, aquarium procedures in the past have tended to shortcircuit the natural cycling processes. This results in loss of valuable energy to the many larger members of the community. Microcosms, mesocosms, and aquaria that by design do not have a fine sediment community should have a separate sediment trap that periodically can be partially drained of sediment. Particularly if a system needs to be driven faster than normal for scaling reasons, or if import and export are desired because of the size and coverage of the model ecosystem, organic sediments can be used as an export tool. In the wild, nutrients are exchanged between sediments and the water column in a variety of pathways. Detritus to bacteria to worms to fish is an important

pathway for recycling nitrogen and phosphorus. Another pathway is through the root hairs, rhizomes, and up into the leaves of higher plants, to be eaten by fish or snails or become more detritus. Some nitrogen in the anaerobic sediments is denitrified to a gaseous form and lost to the atmosphere. As long as the sediment surface is aerobic, phosphorus tends to remain locked in the sediments, since iron oxides under these conditions link up with and trap phosphorus. When, because of excess organic material, the normally subsurface zero-oxygen levels extend into the water column, producing dead zones, stored phosphorus tends to be released. Sulfur also is utilized by bacteria and becomes the very odiferous hydrogen sulfide that one associates with anaerobic conditions. In nutrient-poor lakes, phosphorus tends to become the limiting nutrient because it is locked in sediments by high oxygen levels. In richer lakes and estuaries

59

Geological Storage

FIGURE 3.17 Generalized feeding patterns in a typical shallow-water, soft-bottom community.

with large amounts of sediment in contact with the water, phosphorus tends to be released in abundance and is responsible for algal blooms if nitrogen is available. In the open ocean where fine organic sediments are deep and to a large extent out of reach of the shallow water column, nitrogen and phosphorus tend to be closer in importance with the final limitation usually belonging to nitrogen. For the restorer of degraded lakes and estuaries, this is frequently the first and foremost issue to be addressed. Once human eutrophication has allowed spring planktonic algal blooms to increase bottom organic biomass and bring the anaerobic zone up to the sediment surface and into the water column during the summer, previously stored phosphorus is released causing a further cascade of degradation. Simply cutting off the nutrient supply will no longer work in these cases, and radical methods such as chemical precipitation or sediment dredging are extremely expensive and sometimes prevent full restoration. In Chapter

26, we discuss large-scale, photosynthetic procedures for solving these problems, combining nutrient removal with oxygen injection.

GEOLOGICAL STORAGE Bioturbation (or bottom disturbance) by animals and the rooting and shooting activities of flowering plants in shallow water are processes that continuously return the energy and chemical elements of organic sediment to the water column. However, in many cases sedimentation is rapid enough to bury organic materials out of reach of living processes for geological time. This could be thousands of years for lakes or fresh-water environments or millions of years for marine situations. On the Earth, a significant part of the plant primary production that has occurred in the past 500 million years has been stored as coal, oil, gas, and oil shales.

60

3. Substrate

Limestone production likewise is indirectly related to the photosynthetic process. As we shall discuss further in Chapter 8, virtually all carbon on the Earth’s surface and in its crust has been cycled through organisms, yet it has been estimated that greater than 1600 times as much organic carbon is buried in the Earth’s crust as exists in the biosphere proper. Most of this buried carbon was derived from the process of photosynthesis and was removed, as carbon dioxide, from the atmosphere. Photosynthesis, in the first few billion years of Earth’s history, also resulted in the evolution of oxygen into the atmosphere. During the past century, most human management of the Earth’s organic resources (historically including sewage treatment and aquarium management) is philosophically based on rapid recycling of readily available raw materials (nutrients). In more recent prehuman history of the Earth’s biosphere, organic storage and great limitation of available nutrients has been the rule. This is undoubtedly a major factor providing long-term stability to our biosphere. Likewise in modern organic waste management, it is important to keep nutrients locked in biomass, either active or stored. In addition to algal turf scrubbing (or other plant removal) to simulate model communities characterized by organic sediment burial, a storing or exporting sediment trap is necessary. There are many ways to do this, and several units are described in Chapters 20–26. Sometimes, when export, in the time frame of the model planned, is not desired, and bottom disturbance is not excessive, the basin of the tank itself becomes the sedimentation trap and organic storage facility. Separate settling traps, within the model plumbing, with tap-off valves, can also be used as refugia (Chapter 12).

Aquatic Ecosystem Restoration and Sedimentation In several subsections in this chapter, we have noted the relationship of anthropogenic sedimentation, both increased and decreased on the health of wild ecosystems needing restoration. In general, ecosystems dominated by submerged aquatic vegetation (SAV) tend to be damaged by excessive siltation from land development and farming and ecosystems dominated by emergent aquatic vegetation (EAV) tend to be damaged by the removal of periodic sedimentation (see also Chapter 14). However, other aquatic ecosystems can also be highly sensitive to sedimentation processes. Among the most important of these are coral reefs. Frequently these tropical systems have been damaged or virtually

destroyed by increased run-off, with heavy sediment loadings, related to logging and shore development. If this is past activity, and significant sedimentation is no longer present, then transplantation of a new community of reef organisms from a viable host reef is probably appropriate (Precht, 2006). If moderate run-off is still occurring, then it is possible that the ATS system described in Chapter 25 can assist in ameliorating the effects. Heavy sedimentation will have to be blocked by physical settling ponds or lagoons or any restoration efforts on coral reefs are likely to be unsuccessful.

References Burgis, M. and Morris, P. (1987) The Natural History of Lakes. Cambridge University Press, Cambridge. Davis, H. (1983) Depositional Systems: A Genetic Approach to Sedimentary Geology. Prentice Hall, Englewood Cliffs, New Jersey. Dawes, C. (1981) Marine Botany. Wiley Inter-Science, New York. Gross, M. G. (1982) Oceanography: A View of the Earth. Prentice Hall, Englewood Cliffs, New Jersey. Higgins, H. and Thiel, H. (1988) Introduction to the Study of the Meiofauna. Smithsonian Institution Press, Washington, DC. Kennett, J. (1982) Marine Geology. Prentice Hall, Englewood Cliffs, New Jersey. Kleypas, J., Buddemeier, R., Archer, D., Gattuso, J.-P., Langdon, C. and Opdyke, B. (1999) Geochemical consequences of increased carbon dioxide on coral reefs. Science 284: 118–120. Levinton, J. (1982) Marine Ecology. Prentice Hall, Englewood Cliffs, New Jersey. Lippson, A. J. and Lippson, R. L. (1997) Life in the Chesapeake Bay, 2nd edn. Johns Hopkins University Press, Baltimore. Lowe, D. R. (1994) Early environments, constraints and opportunities for early evolution. In: Early Life on Earth. S. Bengtson (Ed.) Columbia University Press, New York. Marshak, S. (2004) Essentials of Geology. Norton and Company, New York. Maurer, D., Watling, L., Kinner, P., Leethem, W., and Wethe, C. (1978) Benthic invertebrate assemblages of Delaware Bay. Marine Biol. 45: 65–78. Parker, R. (1967) Data of Geochemistry, 6th edn. USGS Prof. Paper 440-D. Precht, R. (2006) Restoration of Coral Reef Ecosystems. Coral Reef Restoration Handbook Taylor and Francis, CRC, Boca Raton. Redfern, R. (2001) Origins: The Evolution of Continents, Oceans and Life. University of Oklahoma Press, Norman. Rheinheimer, G. (1985). Aquatic Microbiology, 3rd edn. Wiley, New York. Salbu, B. and Steinnes, E. (1994) Trace Elements in Natural Waters. CRC Press Boca Raton, FL. Sculthorpe, C. (1985) The Biology of Vascular Plants. 1985 reprint of 1967 edn. Koeltz Scientific Books, Konigstein. Thurman, H. and Webber, H. (1984) Marine Biology. Merrill Publishing, Columbus, Ohio. van Andel, T. (1985) New Views of an Old Planet. Cambridge University Press, Cambridge. van Dover, C.-L. (2000) The Ecology of Deep-Sea Hydrothermal Vents. Princeton University Press, Princeton, NJ.

C H A P T E R

4 Water Composition Management of Salinity, Hardness, and Evaporation

Virtually, all chemical elements dissolve in water. Many are rare in natural waters and of little consequence; most of the more common elements occur in ionic form and often in element combinations. Some elements are fairly common in many natural waters and sea water has a suite of elements that are largely fixed in their percentage composition. Many chemical elements occur in aquatic organisms; some are essential to organism function and are highly concentrated over their concentration in the ambient water. Those that are concentrated more than about 104 times can be limiting for the growth of organisms; however, when these elements greatly exceed normal concentrations in ambient water, they can also lead to the disruption of community structure and function. These latter elements are called nutrients (mostly nitrogen, N; phosphorus, P; iron, Fe; and silicon, Si); they require special attention and we treat them in greater detail in Chapter 9. The conservative elements provide those salts that change little in abundance except for freshwater dilution. Here we also cover the micronutrients and the relationship of all chemical elements of the hydrosphere and the Earth’s crust. In our view, “natural waters” significantly unaffected by human activity have virtually ceased to exist, and in this chapter we introduce the more important nonnutrient additions of industrial and agricultural societies. The chemistry of the aqueous medium or hydrosphere as a whole is highly variable over the face of the Earth. Even the ocean, the most constant of waters, varies considerably in some aspects of its chemical composition as coasts and rivers are approached. At the same time, aquatic organisms are much less chemically removed from the water medium than their terrestrial counterparts are from the atmosphere. In the

overall course of organic evolution, cell walls developed very early, perhaps 3.5 billion years ago, perhaps in a pre-life chemical process; they would have provided an efficiency advantage to many organic processes that previously had to compete in the larger oceanic soup. Likewise, the first closure of vascular or blood systems, some 1 billion years ago, took the previously open sea water that used to carry food and oxygen to each cell and isolated it, as a transporting medium, in blood vessels and body cavities. This isolating device provided more control and allowed the development of larger organisms. However, to obtain oxygen from water, gills, devices basically arranged to bring water in as close a contact as possible to the flowing blood, had to be developed. Even more recently, in a geologic sense, perhaps 400 million years ago, fish entering fresh waters for the first time evolved kidney glomeruli. Once the salt balance between inside and outside changed, these were necessary to constantly pump out the fresh water that now continuously flowed into the blood through the gills (Evans, 1993). These bony (teleost) fish then returned to the sea, millions of years later, having evolved to a lower level of salts in the blood. Then, for the marine teleost, the problem changed to a need to continually drink water and excrete salt. Gills and bladders also became involved in this need for osmotic balance (Jobling, 1995). While kidneys have gradually evolved to become much more complex and varied structures, the problem of sensitivity to the aqueous medium remains. Many algae and small invertebrate animals, being essentially isotonic (same internal salinity) with sea water, remain extremely sensitive to changes in the chemical composition of water. Others, such as anadromous fish, can move salts or water in or out as

61

62

4. Water Composition

required, and thus have adapted to manage enormous changes in salinity. Yet, they remain quite sensitive to acidity changes and it is unfortunate that one of the more routine human additions to the atmosphere, industrial stack emissions that result in acid rain, has devastated fish populations in the streams and lakes of thousands of square miles of Scandinavia and northeastern North America. In addition, human additions of heavy metals, especially Mercury, into the aqueous environment has resulted in government warnings about the edibility of fish such as tuna. Also, pesticides, herbicides, antifouling agents (tributyltin), industrial chemicals (PCBs, for example), and hormones have had significant effects on flora and fauna. These effects extend to the open ocean, and it has been widely documented that PCBs and dichlorodiphenyltrichloroethane (DDT) occur in penguins, whales, and polar bears at the northernmost and southernmost reaches of the sea. These matters we discuss further below. In the establishment and operation of model ecosystems, and in any attempt to

ameliorate the effects of human pollutants on the natural environment, an understanding of the basic nature of the chemical composition of water and its effects on organisms is essential. In the pages that follow we will provide a basic understanding of that water chemistry and present a rationale for dealing with human pollutants (the macro nutrients are treated separately in Chapter 9).

WATER STRUCTURE AND CHARACTERISTICS Water is a most extraordinary compound. Because of its unusual molecular structure (Figure 4.1), it has a number of unexpected chemical characteristics that are generally favorable to life on Earth (Table 4.1). Its change of density with temperature (most dense at 3.98°C) is crucial for freshwater ecosystems to function in cold climates. If it were a more normal chemical compound, more dense below zero, all but the largest

FIGURE 4.1 Molecular structure of water at different temperatures and in different states. Liquid water is a “semisolid” because of the asymmetric and charged nature of the molecule. It is this “mixed” state that gives rise to most of its “miraculous” qualities (see Table 4.1). (A) After Thurman and Webber (1984). Copyright © 1984 by Scott, Foresman and Company. Reprinted by permission of HarperCollins Publishers. (B) Pauling’s self-clathrate water model. (C) Frank and Wen’s flickering clusters model. B and C after Horne (1969). Reprinted by permission of John Wiley & Sons, Inc.

63

Ocean Salinity

bodies of water in colder climates would freeze to the bottom, and only the surface would melt in summer. Even more important to life as we know it is the dissolving power of water. Allowing virtually every naturally occurring element and most compounds into its semi-open liquid structure, in the natural environment water becomes the universal soup in which a very large number of chemical interactions become possible. The clusters or “spheres of hydration” shown in Figure 4.1 also form around many ions and minerals and organic aggregates providing for most of the extraordinary characteristics.

OCEAN SALINITY The salinity of the open oceans has a rather uniform chemical composition in both time and space (Tables 4.2 and 4.3) that ranges from about 34 to 37 parts per thousand (ppt) or 3.4% to 3.7% by weight. In the chemist’s language, this is 34 000–37 000 mg/liter (ppm). Sodium

(Na⫹at 30.61%) and chlorine (Cl⫺ at 55.04%) make up over 85% of this salt, and only four additional elements, sulfur as sulfate (SO42⫺ at 2.71%), magnesium (Mg2⫹ at 3.69%), calcium (Ca2⫹ at 1.16%), and potassium (K⫹ at 1.10%), bring the composition to over 99%. As we discussed in Chapter 3, the residence time of an element in sea water (between river delivery and sedimentation removal) determines the ultimate concentration in sea water. When sea water is diluted by rivers and streams, along an ocean coast, the proportional chemical composition remains essentially unchanged, though the total quantity of salts drops with dilution. Evaporation, precipitation, and river supply certainly affect sea-water salt composition, and for that reason the surface waters of the major oceans and seas can vary slightly in salinity. Also, variation can occur on a geologic time scale. For example, it is known that epicontinental or enclosed seas have often dried up, leaving large salt beds. In the case of the Mediterranean in the late Miocene epoch, 5–6 million years ago, repeated isolation and complete evaporation probably also affected salt composition of the

TABLE 4.1 Unusual Physical Properties of Water and Their Importance in Biological/Ecological Systemsa Property

Comparison with other substances

Importance in physical/biological environment

Heat capacity

Highest of all solids and liquids except liquid NH3

Prevents extreme ranges in temperature Heat transfer by water movements is very large Tends to maintain uniform body temperature

Latent heat of fusion

Highest except NH3

Thermostatic effect at freezing point owing to absorption or release of latent heat

Latent heat of evaporation

Highest of all substances

Large latent heat of evaporation extremely important in heat and water transfer of atmosphere

Thermal expansion

Temperature of maximum density decreases with increasing salinity. For pure water it is at 4°C

Fresh water and dilute sea water have their maximum density at temperatures above the freezing point. This property plays an important part in controlling temperature distribution and vertical circulation in lakes

Surface tension

Highest of all liquids

Important in physiology of the cell Controls certain surface phenomena and drop formation and behavior

Dissolving power

In general dissolves more substances and in greater quantities than any other liquid

Obvious implications in both physical and biological phenomena

Dielectric constant

Pure water has the highest of all liquids

Of utmost importance in behavior of inorganic dissolved substances because of resulting high dissociation

Electrolytic dissociation

Very small

A neutral substance, yet contains both H⫺ and OH⫺ ions

Transparency

Relatively great

Absorption of radiant energy is large in infrared and ultraviolet. In visible portion of energy spectrum there is relatively little selective absorption, hence is “colorless.” Characteristic absorption important in physical and biological phenomena

Conduction of heat

Highest of all liquids

Although important on small scale, as in living cells, the molecular processes are far outweighed by eddy conduction

a

From Sverdrup et al. (1942). Reprinted by permission of Prentice Hall, Englewood Cliffs, New Jersey.

64

4. Water Composition TABLE 4.2 Elements Present in Sea Watera (at greater than 6.10ⴚ6 mg-atoms/liter)

Element Chlorine Sodium Magnesium Sulfur Calcium Potassium Bromine Carbon Strontium Boron Silicon Fluorine Nitrogen (ionic) Aluminum Rubidium Lithium Phosphorus Barium Iodine Arsenic Iron Manganese Copper Zinc Lead Selenium Cesium Uranium Molybdenum Thorium Cesium Silver Vanadium Lanthanum Yttrium Nickel Scandium Mercury Gold Radium

mg/kgb Clⴝ19.00 0/00

mg-atoms/liter Clⴝ19.00 0/00

Atomic weight (1940)

1/atomic weight

18980 10561 1272 884 400 380 65 28 13 4.6 0.02–4.0 1.4 0.01–0.7 0.5 0.2 0.1 0.001–0.10 0.05 0.05 0.01–0.02 0.002–0.02 0.001–0.01 0.001–0.01 0.005 0.004 0.004 0.002 0.0015 0.0005 ⬍0.0005 0.0004 0.0003 0.0003 0.0003 0.0003 0.0001 0.00004 0.00003 0.000006 0.2⫺3 ⫻ 10⫺10

548.30 470.15 53.57 28.24 10.24 9.96 0.83 2.34 0.15 0.43 0.0007–0.14 0.07 0.001–0.05 0.02 0.002 0.014 0.00003–0.003 0.0004 0.0004 0.00015–0.000 0.00003–0.000 0.00002–0.000 0.00002–0.000 0.00008 0.00002 0.00005 0.00002 0.00001 0.000005 ⬍0.000002 0.000003 0.000003 0.000006 0.000002 0.000003 0.000002 0.0000009 0.00000001 0.00000002 0.8⫺12 ⫻ 10⫺13

35.457 22.997 24.32 32.06 40.08 39.096 79.916 12.01 87.63 10.82 28.06 19.00 14.008 26.97 85.48 6.940 30.98 137.36 126.92 74.91 55.85 54.93 63.57 65.38 207.21 78.96 132.91 238.07 95.95 232.12 140.13 107.880 50.95 138.92 88.92 58.69 45.10 200.61 197.2 226.02

0.02820 0.04348 0.04112 0.03119 0.02495 0.02558 0.01251 0.08326 0.01141 0.09242 0.03564 0.05263 0.07139 0.03708 0.01170 0.14409 0.03228 0.00728 0.00788 0.01335 0.01791 0.01820 0.01573 0.01530 0.00483 0.01266 0.00752 0.00420 0.01042 0.00431 0.00714 0.00927 0.01963 0.00720 0.00125 0.01704 0.02217 0.00498 0.00507 0.00442

a Virtually all the gases of the atmosphere are also present, and together these provide a wide variety of organic and inorganic chemical compounds. Adapted from Sverdrup et al. (1942). Reprinted by permission of Prentice Hall, Englewood Cliffs, New Jersey. b The salinity for which these element concentrations are tabulated is 34.3 ppt. Each value should be multiplied by 1.043 to obtain an equivalent to a salinity of 35.8 ppt, a level more appropriate for coral reef systems.

world’s oceans by several parts per thousand. (This in turn may have affected world climate by increasing sea ice formation because of general lowered salinities.) Marine chemists have traditionally separated the chemical elements dissolved in sea water into conservative and nutrient categories. The conservative elements are relatively abundant in sea water, particularly in proportion to their requirements by organisms. The nutrienttype elements are relatively low in concentration in sea water and are needed in proportionally large quantities by organisms, particularly phytoplankters and other

algae. The concentration of other mostly very minor elements can also be affected by chemical reactions, especially in sediments. Sea water near sea floor spreading zones where there is active interchange between hot, forming ocean crust and sea water can be locally altered (van Dover, 2000). Table 4.4 shows the relationship between the principal elements in oceanic phytoplankton (excluding carbon, hydrogen, and oxygen) and the mean sea-water concentrations of those elements. Clearly, limiting status is conferred both by the functional requirements of

65

Ocean Salinity TABLE 4.3 Ionic Composition of Sea Watera (at greater than 10ⴚ12 M) Element

Chemical species

Molar

µg/liter (ppb)

H He Li B C N O F Ne Na Mg Al Si P S Cl Ar K Ca Ti V Cr Mn Fe Ni Cu Zn As Se Br Kr Rb Sr Mo Cd Sb Te I Xe Cs Ba U

H2O He (gas) Li⫹ B(OH)3, B(OH)⫺ 4 HCO3⫺, CO2⫺ 3 , CO2 ⫺ N2, NO⫺ 3 , NO2 , NH4⫹ H2O, O2 F⫺, MgF⫹ Ne (gas) Na⫹ Mg2⫹ Al(OH)⫺4 Si(OH)4 3⫺ ⫺ HPO2⫺ 4 , PO 4, H2PO4 ⫺ SO2⫺ 4, NaSO 4 Cl⫺ Ar (gas) K⫹ Ca2⫹ Ti(OH)4 H2VO⫺4, HVO 2⫺ 4 Cr(OH)3, CRO2⫺ 4 Mn2⫹, MnCl⫹ Fe(OH)⫹2, Fe(OH)⫹4 Ni2⫹ CuCO3, CuOH⫹ ZnOH⫹, Zn2⫹, ZnCO3 ⫺ HAsO2⫺ 4 , H2AsO 4 SeO2⫺ 3 Br⫺ Kr (gas) Rb⫹ Sr2⫹ MoO2⫺ 4 CdC12 Sb(OH)⫺6 HTeO⫺ 3 ⫺ IO⫺ 3, I Xe (gas) Cs⫹ Ba2⫹ UO2(CO3)4⫺ 2

55 1.7 ⫻ 10⫺9 2.6 ⫻ 10⫺5 4.1 ⫻ 10⫺4 2.3 ⫻ 10⫺3 1.07 ⫻ 10⫺2 55 6.8 ⫻ 10⫺5 7 ⫻ 10⫺9 4.68 ⫻ 10⫺1 5.32 ⫻ 10⫺2 7.4 ⫻ 10⫺8 7.1 ⫻ 10⫺5 2 ⫻ 10⫺6 2.82 ⫻ 10⫺2 5.46 ⫻ 10⫺1 1.1 ⫻ 10⫺7 1.02 ⫻ 10⫺2 1.02 ⫻ 10⫺2 2 ⫻ 10⫺8 5 ⫻ 10⫺8 5.7 ⫻ 10⫺9 3.6 ⫻ 10⫺9 3.5 ⫻ 10⫺8 2.8 ⫻ 10⫺8 8 ⫻ 10⫺9 7.6 ⫻ 10⫺8 5 ⫻ 10⫺8 2.5 ⫻ 10⫺9 8.4 ⫻ 10⫺4 2.4 ⫻ 10⫺9 1.4 ⫻ 10⫺6 9.1 ⫻ 10⫺5 1 ⫻ 10⫺7 1 ⫻ 10⫺9 2 ⫻ 10⫺9

1.1 ⫻ 108 6.8 ⫻ 10⫺3 180 4440 2.8 ⫻ 104 1.5 ⫻ 105 8.8 ⫻ 108 1.3 ⫻ 103 1.2 ⫻ 10⫺1 10.77 ⫻ 106 12.9 ⫻ 105 2 2 ⫻ 106 60 9.05 ⫻ 105 18.8 ⫻ 106 4.3 3.8 ⫻ 105 4.12 ⫻ 105 1 2.5 0.3 0.2 2 1.7 0.5 4.9 3.7 0.2 6.7 ⫻ 104 0.2 120 8 ⫻ 104 10 0.1 0.24

a

5 ⫻ 10⫺7 3.8 ⫻ 10⫺10 3 ⫻ 10⫺9 1.5 ⫻ 10⫺7 1.4 ⫻ 10⫺8

60 5 ⫻ 10⫺2 0.4 2 3.2

From Spotte (1979). Reprinted by permission of John Wiley & Sons, Inc.

the phytoplankton and by the abundance of the element in sea water. Sodium and chlorine have higher concentrations in plankton than any other element except carbon, nitrogen, and oxygen. However, because of the high concentration of these elements in sea water, neither can ever be limiting. Silica, on the other hand, is moderately abundant in sea water. Yet, its great requirement by diatoms for their cell walls, when they explode in spring blooms, results in frequent limitations.

Nitrogen, phosphorus, and iron are the classic limiting nutrients. Nitrogen and phosphorus (also the principal eutrophication nutrients) we treat in depth in Chapter 9. Iron requires special mention, not because it is likely to be either limiting or superabundant in microcosms and mesocosms, but because it has been suggested that it is limiting for photosynthesis, far from shore in the large southern ocean; some scientists have suggested that it might be possible to counter global warming by introducing iron into the southern

66


C o n s e r v a t i v e

— —

N u t r i e n t

TABLE 4.4 Relative Abundances of Elements in Marine Phytoplankters and in Sea Watera

Nitrogen (N) Phosphorus (P) Silica (Si) (diatoms) Iron (Fe) (other than diatoms) Vanadium (V) Silica (other than diatoms) Carbon (C) Iron (diatoms) Copper (Cu) Cobalt (Co) Manganese (Mn) Zinc (Zn) Aluminum (Al) Magnesium (Mg) Potassium (K) Calcium (Ca) Sulfur (S) Fluorine (F) Boron (Bo) Sodium (Na) Chlorine (Cl) Bromium (Br)

Concentration in phytoplankton (wt./100 g)

Concentration in sea water (wt./m3)

Concentration factor

SW/Plankton

5g 0.6 g 10 g 1g 3 mg 0.5 g 30 g 40 mg 5 mg 0.05 mg 2 mg 20 mg 1 mg 0.4 g 1g 0.5 g 1g 1g 2 mg 3g 4g 2.5

300 mg 30 mg 500 mg 500 mg 0.3 500 mg 28 g 50 mg 10 mg 0.1 mg 5 mg 5 mg 120 mg 1.3 kg 390 g 416 900 g 1.4 g 5g 10.75 19.3 kg 66 g

1.6.105 2.105 2.105 2.105 1.105 1.104 1.07.104 0.8.104 5.103 5.103 4.103 40.108 83 3.07 25.8 12.02 11.1 7.15 4 2.8 2.07 0.37

0.06* 0.05* 0.05* 0.05* 0.1 1.0 1.0 1.3 2 2 2.5 4 120 300 390 830 900 1400 2500 3600 4800 26 000 (Rejected)

* Frequent limitations a Modified after Millero and Sohn (1992).

ocean. This we discuss in more depth later in this chapter. Even the elements most frequently limiting primary production by algae, nitrogen, and phosphorus are not limiting in very low-nutrient coral reef environments. In most reefs, strong current flow from the open ocean constantly brings a new supply of low-concentration nutrients. Many algae are quite capable of obtaining those nutrients even at very low concentrations; this is so as long as there is abundant physical energy (current and wave action) that prevents microzones of low concentration against cell walls, where there is an active uptake gradient. In addition to carbon, nitrogen, and phosphorus (and of course hydrogen and oxygen as water and ions), another six elements (sodium, potassium, calcium, magnesium, sulfur, and chlorine) are essential to all life. Ten other elements, including iron, manganese, silica, copper, zinc, and boron, are required by most organisms and another ten by a few organisms. Figure 4.2 shows diagrammatically the relationship between the chemical elements, in the standard framework of the periodic table, and their function in living organisms (see also Frausto da Silva and Williams, 1991). Here, it is possible to see the role that some toxic elements play in the basic chemistry of life. Each column in the table signifies the number of electrons in the

outer ring of the atom, thereby dictating basic chemical reactivity. The elements in each column have a chemical similarity, but the atoms are progressively heavier and larger lower in the table. Thus, cadmium (Cd) and mercury (Hg) chemically react like zinc (a minor nutrient) but being larger atoms are likely to replace zinc in an organic molecule but then twist the molecule out of shape. Thus, the general toxicity of these elements. Likewise, arsenic (As) below phosphorus and nitrogen is a general biotic poison. Most important for the modeler, who is typically working with a relatively limited volume of water, any element present in organisms could theoretically be limiting and thereby function as a nutrient-type element. For example, in the operating of coral reef environments in aquaria or mesocosms, due to potentially high calcification rates in those systems, calcium can enter “geological” storage. Even though it is returned from geological storage by boring organisms net calcification rates can be very high, resulting in depletion in the water column. In some reef systems, we have also seen reductions in strontium and potassium, though those reductions in concentration were probably not of concern. However, any element on the upper twothirds of the list in Table 4.4 could be a problem at

Hardness of Fresh Waters

67

FIGURE 4.2 The chemical elements of living organisms and their primary function in relation to the periodic table of the elements. Modified from Frausto da Silva and Williams (1991).

model scale and should at least be occasionally monitored. The primary nutrients, including nitrogen, phosphorus, silica, carbon, and calcium, we treat in depth in later chapters. In practice, in any model system in which import and export of organics is similar to that in the wild analog and, in the case of salt- or hard-water systems, it is necessary to maintain a minimal water exchange to prevent salt drift. Chemical elements can be lost to the atmosphere, as anyone who has operated salt-water systems in a greenhouse can attest. Fresh waters, on the other hand, vary widely in salinity (generally called hardness) from those of virtually pure water to very high levels for lakes with no outflow, that is, endorheic lakes (Table 4.5). The Dead Sea (226 ppt) and the North American Great Salt Lake (203 ppt) have salinities far above that of the ocean and chemical compositions that vary considerably from those in the ocean. On the average, rainwater has a salinity of about 0.008 ppt and is slightly enriched in calcium and sulfate, though near sea coasts a considerable increase in chlorine can be found (Hutchinson, 1957). River waters average 0.1–0.16 ppt, though those draining predominantly igneous rock areas are typically below 0.05 ppt. Rivers usually do not extend

above 0.2 ppt, barring human effects or the localized leaching of salt beds. The River Jordan reaching 7.7 ppt is an example of salt bed leaching and evaporation effects. The ionic composition of fresh waters, even those of far less extreme characteristics, can have significant effects on biota. Hutchinson and Edmonson (1993) offer numerous examples of control or rejection of some species because of water composition. In the modeling of freshwater systems, basic considerations of design, in most cases, will include salinity or hardness.

HARDNESS OF FRESH WATERS Water hardness is handled a little differently from salinity in that in some countries the degree is the unit of measure. One German degree of hardness equals 10 mg/liter (ppm) of calcium and magnesium oxide or 17.8 ppm of CaCO3 in the USA. This is not at all equivalent to salinity in that a relatively low salinity water rich in calcium and magnesium could have a relatively high degree of hardness. On the other hand, a fresh water rich in sodium chloride alone could have a very low

68

4. Water Composition TABLE 4.5 Chemical Composition of Selected Lakes Dominated by Different Anions (%)a Na

K

Mg

Ca

CO3

SO4

Cl

SiO2

23.69 10.12 0.17 10.67 4.37

52.68 21.53 0.09 13.11 Trace

5.76 8.16 6.68 7.22 0.28

2.68 32.36 55.48 41.47 66.37b

3.84 – – 1.95 Trace

16.8 0.56 0.48

56.5 2.58 0.47

1.8 70.5 48.4

2.5 1.1 21.8

12.88 5.58 2.27 0.53 8.41

34.76 44.63 30.87 38.68 51.56

7.35 7.64 22.09 5.67 2.87

2.88 4.55 7.97 13.85 3.88

Chloride waters Bear River Upper, Wyoming Lower, Utah Great Salt Lake, Utah Jordan at Jericho Dead Sea

33.17 18.11 11.14

1.66 1.14 2.42

6.86 4.76 2.76 4.88 13.62

Sulfate waters Montreal Lake, Saskatchewan Redberry Lake, Saskatchewan Little Manitou Lake

4.9 12.0 16.8

2.3 0.85 1.0

10.8 12.3 10.9

Carbonate waters Silvies River, Oregon Malheur Lake, Oregon Pelican Lake, Oregon Bluejoint Lake, Oregon Moses Lake, Washington

10.42 2.45 24.17 5.58 29.25 3.58 37.70 2.62 19.86

4.49 20.54

3.13 4.13 2.62 0.63 7.25

3.9 0.03 0.019 25.13 2.89 1.21 0.55 5.06

(AlFe)2O3

Salinity (mg/kg)

– 2.53 – 1.45 –

185 637 203 490 7700 226 000

0.5 0.07 0.21

150.5 12 898 106 851

0.08 Trace 0.02 0.02 1.11

163 484 1983 3640 2966

a

After Hutchinson (1957). Reprinted by permission of John Wiley & Sons, Inc. And 1.78% Br.

b

TABLE 4.6 Hardness Scales for Fresh Watersa dGH ⫽ dKH ⫹ pH GH ⫽ total hardness (dGH ⫽ German total hardness) KH ⫽ carbonate hardness (dKH ⫽ German carbonate hardness) PH ⫽ permanent hardness Carbonate hardness based on bicarbonate is not permanent because the CO2 can be driven off by boiling. The remaining calcium and magnesium by definition determines permanent hardness. Total hardness can be illustrated as follows: Degrees of hardness 0–4° dGH ⫽ very soft 12–18° dGH ⫽ fairly hard 4–8° dGH ⫽ soft 18–30° dGH ⫽ hard 8–12° dGH ⫽ medium hard over 30° dGH ⫽ very hard One degree of hardness ⫽ 10 mg/liter of CaO or MgO a

Partly after Riehl and Baensch (1987).

hardness. Nevertheless, the mean river of Hutchinson (1957) with a salinity of 0.13 ppt would have a hardness of about 1.9° (i.e. very soft). The standard terminology relating degrees of hardness to descriptive elements is given in Table 4.6. Unfortunately, hardness through calcium is tied to the very nonconservative carbonate system, as measured by pH. The pH is very much affected by organism respiration and photosynthesis and is treated at length in Chapters 8 and 10. In practice, these two can be handled separately as long as one remembers that there can be a connection. Hard waters usually have a high pH. The status of a wild freshwater community that one wishes to simulate can be determined within the range

of the standard hardness test kit. If one is creating a synthetic system, the best manuals describing standard aquaria fish usually provide optimum numbers for each species. Many fish species can adapt to a wide range of hardness, particularly if it is changed gradually. Generally, with freshwater systems, as long as evaporation is not excessive and the hardness of the replacement water is not too high, occasional small volume changes (1 gallon a week for a 70-gallon system) are sufficient to prevent salt buildup and the effective development of an endorheic or salt lake in the aquarium or mesocosm environment. As discussed below, algal scrubbers tend to adjust disproportionate elements as long as the system is not allowed to become too unbalanced. The difficulties arise in fresh- or salt-water microcosms or aquaria when the fresh water being used to replace evaporated water is excessive in certain ions, typically those of the elements calcium, iron, sulfur, or magnesium. Even in models of soft to medium-hard water ecosystems, it is important to occasionally carry out an analysis of the spectrum of inorganic elements. A standard commercial test for tap or drinking waters will usually suffice. We have worked with a hard water on the Atlantic Coastal Plain that is rich in both iron and sulfur. Even though a standard water softener is used on the well water, the taps and sinks have excessive iron staining and water out of the tap has a sulfurous odor, particularly in dry years. The water softness, as an ion exchange system, also introduces a small amount of sodium chloride. We have successfully solved this problem by using

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Hardness of Fresh Waters TABLE 4.7 Concentrations of Selected, Analyzed Chemical Elements, Ions, and Compounds from a Variety of City Water Suppliesa Parts per million, mg/liter Element, ion, or compound *Aluminum Arsenic Barium Cadmium *Chlorine-free *Chloride Chromium *Copper *Fluoride *Iron Lead Manganese Magnesium Mercury Nickel *Nitrate (as N)b *Phosphate (as P)b Potassium Selenium Silver *Sodium Strontium *Sulfate Zinc Total trihalomethanes Endrin (pesticide) 2.4-D (pesticide)

Boston ? ⬍0.005 ⬍0.1 ⬍0.002 12–44 ⬍0.005 0.01–0.08 0.06–0.98 0.02–0.16 ⬍0.002 0.01–0.05 .5–2.4 ⬍0.001 ? ? ? 0.9–2.3 ⬍0.005 ⬍0.005 7.2–26.3 ? 8.3–14 ⬍0.02 ? ? ?

Chicago

Dallas

Baltimore

0.45–0.5 ⬍0.005 ⬍0.05 ⬍0.001 ? 10.9–11.1 ⬍0.003 ⬍0.003 0.92–0.93 ⬍0.010 ⬍0.003–0.010 0.001–0.002 12.3–12.5 ⬍0.0005 ⬍0.003 0.25–0.26 0.010–0.018 1.5 ⬍0.001 ⬎0.001 5.8–6.0 0.119–0.142 26.4–27.5 0.004–0.005 ? ? ?

? ⬍0.005 ⬍0.05 ⬍0.001 2.12–2.29 15–27 ⬍0.01 ⬍0.01–0.02 0.77–0.78 ⬍0.01–0.01 ⬍0.005 ⬍0.005 3–5 ⬍0.001 ⬍0.01–0.01 0.22–0.45 0.03–0.09 3.7–4.8 ⬍0.001–0.001 ⬍0.01 11.0–28.5 0.10–0.25 31–50 ⬍0.01–0.02 0.0227 ND ND

0.08–0.16 ⬍0.005 0.021–0.03 0.001 ? 18–22 ⬍0.001 0.004–0.006 0.9–0.97 0.02 ⬍0.001 0.01 4.4–6.2 ⬍0.0005 ? 1.7 0.01 2.2–2.6 ⬍0.005 ⬍0.005 7.1–8.3 ? 13.6–15 0.028–0.038 41 ⬍0.04 ⬍0.05

Los Angeles ND–0.2 ND–0.02 ND ND 18–127 ND ND 0.1–0.7 ND–0.07 ND ND 5.7–27 ND ? ND 0.02–0.07 3.6–4.8 ND ND 37–86 ? 28–232 ND 13–72 ND ND

San Francisco

Washington, DC

0.02–0.08 ND ND–0.01 ND 0.4–0.7 2–19 ND–0.001 ND–0.015 0.3–1.2 ND–0.06 ND–0.001 ND–0.01 ? ND ? 0.04–0.1 0.002–0.017 0.2–0.8 ND ND 1.0–15.5 ? 1.6–3.6 ND–0.010 0.063–0.075 ND ND

0.042–0.2 0.000–0.001 0.028–0.07 0.0–0.00 1.6–2.1 15.6–29.0 0.0–0.006 0.001–0.110 0.93–1.14 0.001–0.07 0.0–0.001 0.001–0.004 6–11 0.0000–0.0003 0–0.003 1.29–2.67 00–0.14 2.11–3.27 0.0–0.002 0.0 4.8–15.6 0.093–0.24 22.1–48.9 0.0–0.005 26–137 ND ND

Note: Tap waters can have additional or increased contamination levels. ND, not determined. These data are from the 1980s. Few, if any, large metropolitan water systems would lack free chlorine or trihalomethanes today. a Sources: Indicated metropolitan water authorities. b Reactive. *Added in treatment, in part or whole.

a separate water softening algal scrubber system. Excess calcium, iron, and sulfur are either taken up by the algae or precipitated out on the surfaces of the cells and removed at harvest time. A reverse osmosis (RO) unit can be used following a water softener if the volume requirements are not too great. The character of well waters varies widely, and it would be impossible to cover the problems of microcosm and mesocosm water supplies for all cases. In general, if a standard water softener does not solve the problems, we have found that a separate algal turf scrubber (ATS) managed water reservoir (see Chapter 11) adjusted for nutrient levels and pH can remove almost any contaminant including heavy metals. In general, city or town waters provide more serious problems. While rarely are city tap waters saline or hard compared to average natural waters (Table 4.7), the salinity of an aquarium or microcosm can become

that of an endorheic, or closed basin lake, if topping up for evaporation continues for some time and water exchange with waters of the character of the analog of the model is not carried out. However, the primary problem with city tap water is the additives used to control human pathogens, to adjust the taste, to control algae in artificially eutrophic reservoirs, or to reduce corrosion in pipes (Table 4.8). The addition of chlorine is well known and is the primary characteristic that renders tap waters objectionable to humans. It is added to kill pathogens, but the chlorine also would kill most of the animals that one would wish to maintain in an ecosystem. Fortunately, being in the gaseous state it is more or less easily removed by bubbling or allowing the water to stand for several days. Since chlorine in combination with organic compounds occurring naturally forms compounds (trihalomethanes; see Table 4.7) that have been shown to be

70

4. Water Composition TABLE 4.8 Chemicals Typically Used in the Treatment of City Water Suppliesa Chemical

Purpose

Aluminum as aluminum sulfate (Al2(SO4)3, 18 H2O) Ammonium hydroxide (NH4OH) Carbon, activated (C) Chlorine or chloramines (Cl2) (NH2Cl, NHCl2, NCl3) Copper sulfate (CuSO4) Fluorosilicic acid (H2SiF6) Ferric chloride (FeCl3) Hexametaphosphate (PO3)6 Lime (CaO, Ca(OH)2) Sodium chlorite (NaClO2) a

Clarification Taste and odor control Taste and odor control Sterilization Algal reduction Dental decay reduction Clarification Reduce corrosion in metal pipes pH adjustment Taste, odor, and algae control

Sources: Metropolitan water authorities as given in Table 4.7.

carcinogens, some cities have started to add chloramines instead of chlorine to control human pathogens. Unfortunately, chloramines are more toxic than chlorine to fish and invertebrates and are more slowly lost to the atmosphere than chlorine. Copper sulfate is added to many drinking water systems that include reservoirs to prevent the excessive algal growth that sometimes results from artificially high nutrient levels. Unfortunately, the copper is also toxic to the algae that is necessary to maintain virtually all natural, aquatic ecosystems. Finally, a major problem of many city tap waters is that they are eutrophic, that is, excessive, particularly in dissolved nitrogen and phosphorus. While additional chemical treatments are available to remove all of these contaminants, we prefer physical (RO) and plant production (algal scrubbing) methods for cleaning tap waters to levels acceptable for ecosystem management. Scrubbers utilized in this way are typically dominated by blue-green algae. We have limited our discussion of water composition to the inorganic elements, mostly those existing in solution as charged ions, either alone or in combination with oxygen and sometimes hydrogen. However, natural waters also include abundant particulates both inorganic and organic, and aquatic ecosystems cannot function normally without the particulate “soup” that is often present in the wild. Many of the smaller organic particulates can be regarded as dissolved organics, the boundary between particulate and dissolved being quite arbitrary. In this book we treat the particulate components primarily in Chapters 3, 6, 17, and 18. Finally, anthropogenic pollutants, inorganic and organic, cannot be ignored in any natural waters that might be used for source or exchange. POPs (persistent organic pollutants), like DDT and its breakdown products, and PCBs have reached every corner of the globe (Turosov et al., 2002). Penguins, seals, and whales in Antarctica and polar bears in the Arctic have DDT and PCBs in their tissues. Although often concentration of

these and other anthropogenic organic compounds (which are now banned in the USA) are extremely low in sea water, they tend to be concentrated “up food chains,” especially in fatty tissues, until very toxic levels are developed in top predators (e.g. Laws, 1993). While the half-life of many of these compounds in the sediments of lakes and estuaries may be only 10–15 years, in the biosphere they can be 150 years or more. For example, while 7–16 ppm of PCBs in milk is highly toxic to infant monkeys, Beluga whales were found in the St. Lawrence estuary (which is a highly mixed body of water with extensive deep water oceanic injection) with 575 ppm PCB in their livers and 1750 ppm in their milk (Laws, 1993). Heavy metals from industrial activities and sewage (e.g. mercury, Farago, 2000), and organometals like tributyl tin (a now banned antifouling agent) tend to be thought of as local pollutants, mostly in harbors where boats are concentrated and mixing minimal (and where very serious and lethal effects on mollusks have been documented). However, years after use was discontinued in the USA and Canada, the livers of Beluga whales in the St. Lawrence estuary (again, a very large and well-mixed body of water) were still contaminated with tributyltin (Preston, 2002). The problem of toxic compounds has gone well beyond immediate solution in the ocean. Only time (probably measured in decades and centuries) and future prevention of release of toxic compounds to natural waters can eventually solve this problem. Even when concentrations of many of the newer industrial, agricultural, and pharmaceutical compounds are not directly lethal, they can function as endocrine disrupters preventing or reducing reproduction and having drastic effects on invertebrate and fish populations (Pellerito et al., 2002). As we discuss in depth in Chapter 25, most if not all of these compounds can be removed from lake and river waters along with nutrients, though considerable public and political will is required to do so.

Algal Scrubbing and Water Composition

WATER AND MODEL ECOSYSTEMS In earlier editions, we discussed our preference for using natural waters from unpolluted habitats to initiate model ecosystems. On occasion, in the 1980s and 1990s, we went as much as 50 miles offshore in the mid-Atlantic region to obtain water suitable for starting large model coral reef systems. However, for most aquarists, including university researchers modeling ecosystems, highquality natural waters may simply not be available. To emphasize the magnitude of the problem, we cite Turosov et al. (2002) (National Library of Medicine). “Due to its stability and its capacity to accumulate in adipose tissue, it (DDT) is found in human tissues, and there is now not a single living organisms on the planet that does not contain DDT.” PCBs, mercury, and probably numerous other compounds of modern civilization have already achieved or are approaching the same state. However, the microflora and microfauna appropriate to a model system is likely to be obtained only from natural waters. The rational approach today is to use RO water adjusted to salinity with the highest-grade sea salts, or prepared with reagent, or better, analytical grade chemicals appropriate to the type of hardness desired (for fresh waters) to fill the system. Once an aquarium, microcosm or mesocosm is operating as a physical plant, algal scrubbers (see Chapter 11), and 5–10% additions of natural water can be added to introduce microflora and microfauna and clean up micro contaminants. The gradual introduction of macro organisms to build up community structure can then be carried out with the occasional natural water aliquot. As we describe in depth in Chapter 11, if the ATS methodology is employed (with routine harvest), heavy metals will be captured by the algae and most organic pollutants will be broken down and the carbon removed from the water column of the system along with the algal harvest. When substrate and organisms from the natural environment are introduced, as we describe above, microorganisms will be brought in with them. They cannot be avoided, unless one wishes to select all organisms, including protozoans and microbes, individually (a virtually impossible task) and then pass them through sublethal or other baths selective for the desired organisms. The sterilization approaches of modern medicine are not applicable to the synthesis of most ecosystem models. Quarantine of fish, especially those purchased, and particularly those from fresh water, is essential to avoid occasional serious disease problems. On the other hand, if the organisms are in a healthy environment and the ecosystem is managed properly, disease will be minimal. We discuss these matters further in Chapters 19 and 26. However, as we have recently learned from hard experience, today, any coastal waters are suspect for

71

disease and toxic introduction, and a pre-treatment water system with ATS clean-up is desirable. Once a microcosm, based on the principles discussed in this book, is established, water changes should be minimal and aimed primarily at preventing evaporative “salt drift” in sea waters and the change in the proportional salt content caused by evaporative accumulation in fresh waters. In short, very minor water changes should be made to avoid drift in conservative elements that would create a “Great Salt Lake” or endorheic basin. As we discuss in Chapters 7–11, nonconservative or nutrient-type elements should be maintained dynamically by balanced system loading.

ALGAL SCRUBBING AND WATER COMPOSITION In both our mesocosm and aquarium endeavors, we have emphasized the use of plants, mostly algae, to manage water quality. This is part of a broader tendency in environmental water management today called phytoremediation, and we treat the subject in some detail in Chapter 25. As we discuss in many places in this book, the key to ecosystem management is stability achieved by locking nutrients up in biomass rather than by using bacterial filtration to rapidly reduce all nonliving organics and organism excretions to freely available elements and ions. The algal scrubber is the principal technology in this management system and is discussed in depth in Chapter 11. Algal scrubbing is used primarily to maintain a balance, to simulate the effects of the larger body of lowanimal biomass water that balances out the requirements of high-biomass systems. This might be smoothing out the differences between day and night in small model ecosystems or between seasons in large mesocosms. If there is no import to a system, because it is large enough and rich enough in photosynthetic plants to provide sufficient energy to the community of organisms maintained, then export is not required. The algae are removed by scrubbing as a daily, weekly, or seasonal requirement and are dried and eventually returned to the system. Thus, there is little chance for the removal of critical elements from the water medium. However, when the aquarist is running a dynamically balanced system with significant input (usually dried or live food) and export, either because the model has excessive biomass and is being driven hard or because the input and export simulate similar features in a wild ecosystem, then imbalances are theoretically possible. The algal turfs of scrubbers are communities, typically with many species from most algal divisions, and thus tend to be self-balancing. Algae and other aquatic

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plants synthesize a wide variety of organic compounds including many vitamins (Ragan, 1981). It is unlikely in diverse communities of fifty to several hundred species of plants that contain many herbivores, even in relatively small models, that lack of algal-synthesized organic compounds would hinder ecosystem development. On the other hand, many algae have requirements for inorganic micronutrients, such as iron, calcium, manganese, molybdenum, boron, cobalt, copper, and iodine that could theoretically provide such limitations by locking up elements of concern. Moe (1989) discusses removal of trace elements particularly by ozonation and protein skimmers, but also through uptake by algae. Iodine, particularly needed by crustaceans for molting, was cited as a characteristic problem. We refer to a general pattern of crustacean success in our systems (Chapters 20–23), where extensive algal scrubbing has been used for many years. For one particularly successful coral reef model, we describe more than 9 years of continuous molting in a single individual of rare reef lobster. In addition, after 10 years of continuous operation that never included a mass water change (beyond a standard 2% per month to prevent salt drift), the Smithsonian Coral Reef contained concentrations of iron, manganese, silica, copper, and strontium that remained very close to or slightly above concentrations in Delaware coastal waters (the source of top-up water at that time). On the other hand, as we describe in detail in Chapters 10 and 20, in coral reef models with abundant calcifiers, high temperatures and light levels with extensive photosynthesis, the “sinking rate” of calcium and carbon in carbonate skeleta and shells is very high (see also Chapter 3, re: geological storage). This can lead to calcium and alkalinity depletion followed by slower growth rates of calcifying organisms. It is essential in this situation to maintain calcium and alkalinity concentrations at or above levels typical for the open ocean (420 mg/liter and 2.43 meq/liter). The addition of calcium and bicarbonate in this case simulates delivery to wild reefs by equatorial and tidal currents as well as trade wind seas, and cannot be regarded as “undesirable”; if one’s purpose is modeling, these additions are equivalent to that in the wild and are required for ecosystem function. In a research laboratory, the limiting or potential limiting of chemical elements in ecosystem models can be extensively monitored and appropriately adjusted. For the researcher with more limited resources or a hobbyist, a commercial water analysis service may do, although sufficient accuracy and precision needs to be demanded. Following a few simple rules (that are, in effect, what happens in the wild) will avoid most problems: (1) do not run import and export highly out of balance (see Chapter 11); (2) use a wide variety of

FIGURE 4.3 Conversion graph for obtaining salinity from specific gravity and temperature.

living and dried foods; (3) in the long term utilize small water changes (constant “new water” exchange is a feature of wild ecosystems); and (4) where calcification is an important and extensive feature of a model ecosystem, be certain that calcium carbonate, especially as aragonite, is readily available and alkalinity is within normal range (see also Chapters 8 and 10). For the latter, standard, inexpensive test kits are available. However, especially for calcium, the accuracy and precision are marginal.

MARINE MICROCOSMS AND AQUARIA An attempt to faithfully re-create a marine system must include monitoring of salinity levels and a knowledge of daily, weekly, and monthly salinity variations in the wild. Normal ranges of salinity for most nonestuarine coastal situations are 28–34 ppt for colder waters (with a variation of no more than several ppt a day) and 34–37 ppt for tropical oceanic situations (varying no more than 0.5 ppt daily). (The idiosyncrasies of brackish water aquaria are discussed in Chapter 22.)

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References

provides about the same precision. Both devices require very careful observation and conversion for effective use on reef systems. For other coastal communities and estuaries, either device is quite adequate. The infrared-level sensors, now easily available, are generally quite accurate. The sensors themselves need to be wiped off every few weeks to avoid failure. Failure of a water-delivery system can be just as disastrous as the jamming of a heater. A check of the tank twice daily can prevent the problem from becoming critical. However, continuous pumping of fresh water for hours can destroy a sensitive marine microcosm. We use manually filled freshwater reservoirs for replacement water. The reservoirs contain the maximum amount of water that can safely be pumped in between checks.

QUALITY OF TOP-UP WATER

FIGURE 4.4 Tap water cleaning system consisting of a laboratorygrade RO unit, a reservoir, and an algal scrubber.

Evaporation is an on-going process with all open tanks, and generally at least daily replacement of evaporated water is necessary. Manual topping up to a mark is acceptable for cold-water or brackish systems that normally experience wide salinity swings. But for controlling salinity in tropical reef tanks, precision leveling devices now available from most aquarium stores and laboratory supply houses should be used. The hydrometer measures salinity by specific gravity (or density) and is the least expensive and most troublefree device of this type. A conversion is required (Figure 4.3) because temperature is also an important parameter relating salinity to specific gravity. Also, hydrometers must be calibrated for reading variation as a function of temperature away from the standard for which they are calibrated at the factory. However, even the larger hydrometers are difficult to read with a consistent effective precision of better than ±0.2 ppt. A refractometer costs a little more and is easier to use. However, it

For coral reef systems, high-grade distilled water is recommended for evaporative replacement water, because many contaminants continually placed in a closed tank are generally not removed by evaporation. Poor input water quality is a key element tending to degrade model ecosystems. As we discuss in depth in Chapters 11 and 25, many pollutants are broken down and removed from ecosystem models through the use of algal turf scrubbers. The reverse osmosis and laboratorygrade deionizer system that we used for the Chesapeake mesocosm are illustrated in Figure 4.4. In this case an algal scrubber unit is also used because it produces lower nitrogen input levels than the reverse osmosis unit. Such a system will also remove heavy metals and synthetic organic contaminants where that is necessary. City tap waters and many private well waters are unsuitable for direct long-term evaporative water replacement to ecosystem models. The long-term result of intensive evaporation of water is an alteration of the salt composition of a system. A 0.5–1.0% per day exchange with a high-quality “make-up” water of appropriate salinity or hardness (as we discussed above) will generally avoid this problem. Hardness in fresh water is usually much less of a problem than salinity maintenance in salt waters. Nevertheless, in special cases it can be critical, and the 0.5–1.0% exchange may also be appropriate.

References Evans, D. (1993) Osmotic and ionic regulation. In: The Physiology of Fishes. D. Evans (Ed.). CRC Press, Boca Raton, Florida. Farago, M. E. (2000) Mercury in Marine Environments. In: Chemical Processes in Marine Environments. A. Gianguzza, E. Pelizzetti, and S. Sammartano (Eds). Springer, New York.

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Frausto da Silva, J. and Williams, R. (1991) The Biological Chemistry of the Elements. Oxford University Press, Oxford. Horne, R. (1969) Marine Chemistry. Wiley, New York. Hutchinson, G. E. (1957) A Treatise on Limnology, Vol. 1. Wiley, New York. Hutchinson, G. E. and Edmondson, Y. (1993) A Treatise on Limnology, Vol. IV. Zoobenthos. Wiley, New York. Jobling, M. (1995) Environmental Biology of Fishes. Chapman and Hall, London. Laws, E. A. (1993) Aquatic Pollution, An Introductory Text, 2nd edn. John Wiley and Sons, New York. Millero, F. and Sohn, M. (1992) Chemical Oceanography. CRC Press, Boca Raton, Florida. Moe, M. (1989) The Marine Aquarium Reference. Green Turtle Publications, Plantation, Florida. Pellerito, L., Barbieri, R., DiStefano, R., Scopelliti, M., Pellereito, C., Fiore, T., and Triolo, F. (2002) Toxic Effects of Organometallic Compounds Towards Marine Biota. Ibid.

Preston, M. (2002) Endocrine-disrupting chemicals in the marine environment. In: A. Gianguzza, E. Pelizzeti, and S. Sammartano (Eds). Chemistry of Marine Water and Sediments. Springer, New York. Ragan, M. (1981) Chemical constituents of seaweeds. In: The Biology of Seaweeds. C. Lubban and M. Wynne (Eds). University of California Press, Berkeley, California. Riehl, R. and Baensch, H. A. (1987) Aquarium Atla. Mergus-Verlag, Melle. Spotte, S. (1979) Seawater Aquariums. Wiley-Interscience, New York. Sverdrup, H., Johnson, M., and Fleming, R. (1942) The Oceans, Their Physics, Chemistry and General Biology. Prentice-Hall, Englewood Cliffs, New Jersey. Thurman, H. and Webber, H. (1984) Marine Biology. Merrill, Columbus, Ohio. Turosov, V., Rakitsky, V., and Tomatis, L. (2002) Dichlorodiphenyltrichloroethane (DDT): ubiquity, persistence and risks. National Library of Medicine, Pub. Med. Environ. Health Perspect. 110: 125–128. Van Dover, C.-L. (2000) The Ecology of Deep Sea Hydrothermal Vents. Princeton University Press, Princeton, NJ.

C H A P T E R

5 The Input of Solar Energy Lighting Requirements

In many ways, this is the key chapter in this book. Photosynthesis not only provides virtually all the energy that drives ecosystems, it provides our food and the environment in which humans have evolved. This has not always been so. The early atmosphere and ocean, rich in carbon dioxide, ammonia, and perhaps hydrogen sulfide and without oxygen or ozone, was bombarded with shortwave radiation. Possibly the radiation impacting the elemental soup created a wide variety of physically synthesized simple “organic compounds,” or possibly they “rained in” with comets that also provided the water. The earliest proto “organisms” evolved from chance combinations of these compounds, perhaps with the involvement of the intense energy of lightning strikes. Some researchers think that the structural patterns of clay minerals, which can replicate, may have provided the proto-genetic organization, while the surface tension of water combined with simple “organic” created cellular-like bubbles. These developing “organisms” likely made direct use of simpler, energy-rich compounds, much as many present-day heterotrophic bacteria are able to do, and were able to grow. This pattern of energy supply continued for perhaps a billion years or more and probably could have been effective only in the absence of oxygen.

they are rather rare, requiring an anaerobic environment in conjunction with abundant solar energy, a somewhat unusual situation on today’s Earth (Rheinheimer, 1985). Finally, about a billion years later, the blue-green algae (treated today as cyanobacteria since they lack a well-defined nucleus) developed the ability to use the most abundant compound available in the Earth’s oceans (water) in this same basic process of energy supply (Figure 5.1). Photosynthesis eventually became a highly sophisticated chemical process of two basic steps, the first requiring light and using chlorophyll and associated pigments, as antennae or catalyzers, to capture light energy and to split water to provide electrons and hydrogen ions (and incidentally release oxygen). The second step can take place in the dark. It uses the energy carried by excited electrons from the first step and the hydrogen ions to build simple sugars or alcohols (C6H12O6 or 6CH2O) from carbon dioxide, thereby providing the basic chemical energy supply for the plants, and for the animals that eat them. It is still true that in oceans, at sea floor spreading zones and on anaerobic mud flats, as well as in hot springs on land, some biological sources are chemoautotrophic and probably not even indirectly derived from solar energy. A prime example, discovered in the early 1980s, is provided by the thermal vent communities and their ecosystems, along mid-ocean ridges. These ecosystems are based on energy supplied from the Earth. However, interesting as these systems are, and as interesting as they would be to bring into a microcosm, it is sunlight that drives the vast majority of ecosystems likely to be of interest to the ecologist and the aquarist. Also, in environments such as deep soft bottoms where no light is present, the ecosystem’s driving energy is

PHOTOSYNTHESIS AND ITS ORIGIN About 3 billion years ago, some bacteria developed the ability to absorb sunlight and to split a variety of abundantly available noncarbon compounds with hydrogen and an available electron, such as H2S and H2. The same or similar bacteria still exist today though

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5. The Input of Solar Energy

FIGURE 5.1 Evolution with time of the major groups of organisms, the process of photosynthesis, and the composition of the atmosphere. After Mathews and van Holde (1996). Reprinted by permission of Addison Wesley Longman.

obtained through the rain of organic matter from shallow water or possibly through turbidity or other currents. Tropical jungle streams survive largely through the breakdown of leaves that fall into them or are made available to the community during floods of the adjacent forest floor. In simulating such systems one would perhaps wish to “feed” them with appropriate organic particulates or leaf litter rather than primarily with light through a second model ecosystem. However, the most interesting systems for aquaria, and microcosm models, as well as wild aquatic systems currently needing restoration, are high light systems. Even the source water for blackwater streams might be best “scrubbed” first, as we described at the end of the last chapter, and then acidified to rain level pH with CO2 bubbling. We examine the light-driven reactions of photosynthesis in greater depth, because they provide the keys to the operation of model ecosystems, as well as to the restoration of most damaged ecosystems. The evolution, increasing sophistication and globalization of photosynthesis, and its corollaries, an oxygenated, low carbon atmosphere and mostly low nutrient-shallow waters, provided the basis for the further evolution of higher,

more complex life forms on Earth. Since the dawn of the industrial revolution, human society has been massively extracting energy from fossil fuels and forests (both stored carbon) and simultaneously releasing nutrients to surface waters with little regard for the consequences. To prevent a collapse of human civilization when the fossil oil runs low (see e.g. Diamond, 2005; Lovins et al., 2004) and the Earth overheats, we need to greatly expand our solar energy capture systems (including photosynthesis bioenergy). At the same time we need to de-nutrify and de-toxify our surface waters. In the second edition of this book, we reasoned that while we could build ecosystem models that operated in pre-industrial environments, we could not economically repair the existing damage to our atmosphere and natural waters. The principal focus of the earlier edition was to provide enough public and scientific understanding of the workings of aquatic ecosystems to redouble conservation efforts at preventing further damage. Conservation is essential, but a more pro-active approach is now necessary. In this edition, we replace that more pessimistic, but hopeful view, with one of greater optimism. We describe how our natural ecosystems can be recovered with economic advantage.

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FIGURE 5.2 Electron microscope and diagrammatic view of chloroplast structure. After Keeton and Gould (1986). Reprinted by permission W. W. Norton & Co., Inc.

This optimism is based in an understanding of chlorophyll and photosynthesis, and in an application of that understanding to environmental restoration. Chlorophyll is the basis of photosynthesis. The magnesium-centered chlorophyll molecules, porphyrinring structures (like the iron-centered hemoglobin) were no doubt the end result of hundreds of millions of years of improving the biochemical processes of photosynthesis. The cellular synthesis of the chlorophylls and hemoglobin is part of the same biochemical complex of processes that synthesizes the cytochromes (electrontransferring molecules of photosynthesis), the phycobilins (light capturing accessory pigments of red and brown algae) and cobalt-centered vitamin B12, among many others. Some photosynthetic bacteria have chlorophyll pigments that are zinc-centered porphyrins. These are all molecules configured to easily pick up and lose excited electrons and to bind oxygen. In the algae and higher plants, chlorophyll and photosynthesis occur in chloroplasts, membrane enclosed cellular organelles that contain membrane-bound platelets (granae) (Figure 5.2). Chloroplasts have their own DNA, quite different from the cell’s nuclear DNA, and many researchers think that these represent cyanobacteria, first captured over a billion years ago by algal ancestors (Lee, 1999). Thus, algal (and now higher plant) photosynthesis was the result of a symbiosis similar to the coral symbiosis with zooxanthellae that we describe later. The light capture process occur on the surface of the granae. The so-called dark reactions of the synthesis of sugar (Chapter 7) occur in the intergranae spaces, the stroma. As we will discuss in greater depth in Chapters 19 and 20, stony corals are the primary framework

constructors of most coral reefs. These coelenterates build reef “infrastructure” that is then colonized by the highest diversity of animals and algae in the oceans. This feat of calcification and growth is accomplished by a photosynthesis-enhanced metabolism that accrues from the capture of algal cells (zoothanthellae), and the combining of the physiologies of both animal and alga. There are many animals in coral reefs that are herbivores of free-living algae, and many that hide in the free-living algae that grow on the reef surface, but only the symbiosis of an animal and an alga could create the largest and most diverse ecosystem in the shallow ocean. In algae and higher plants, the chlorophyll molecules are held on the lipid membrane surface of the granae by a convoluted protein and have long hydrocarbon tails embedded in the membrane. As shown in Figure 5.3, chlorophyll “a” (the primary photosynthetic molecule) is tuned to light capture in two different ways. Photosystem II, absorbing light at 680 nm (red), produces excited electrons that escape from the chlorophyll molecules, and then, in a poorly understood process (Pace, 2005; Melis, 2005), replaces those electrons from water molecules resulting in the “splitting” of water and the production of oxygen. In the light, the lipid membrane surface of the granae, which is studded with molecules like cytochrome and ferredoxin, that pick up and lose excited electrons easily, is a “sea” of moving, excited electrons. Some of the cytochrome molecules, as an electron attaches and detaches, use electron energy to pump hydrogen ions into the internal spaces of the granae. Employing the hydrogen ion gradient, enzymes, also embedded in the membrane, function

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FIGURE 5.3 Process of photosynthesis and the sequence and location of light-sensitive phases on the membranes of plant chloroplasts. After Keeton and Gould (1986). Reprinted by permission of W. W. Norton & Co., Inc.

as hydrogen-ion-driven pumps to attach phosphorus ions to ADP to in turn create the energy transporting ATP in the intergranae spaces. The membrane also has chlorophyll “a” molecules that are tuned slightly differently, to 700 nm (Photosystem I), and serve to simply re-excite electrons traveling along the membrane without splitting more water. Finally, ferredoxin molecules, on picking up excited electrons, are able to attach those electrons to NADP to produce the energy carrier NADPH. In the light, activated NADPH and ATP molecules are constantly released from the surface of the granae membranes into the stroma (intergranae spaces) where they are available to drive sugar synthesis (Chapter 6) and then return to the granae surface for reactivation. This process of photosynthesis, evolved over a billion years or more, is highly efficient at solar energy capture and also supplies energy storage in chemical bonds. Solar cells and wind generation also capture energy in the form of moving electrons, albeit far less efficiently than photosynthesis. However, storage of energy acquired with these devices is far more problematical, requiring expensive, inefficient batteries, or more esoteric methods. It is interesting to note that the highly efficient chlorophyll, energy capturing process of algae and higher plants is greatly reduced in its efficiency (as

much as 80%; Melis, 2005) by the chemical storage process. Nevertheless, the overall process of photosynthesis and primary production remains considerably more efficient than current industrial methods of solar energy capture. Many scientists are attempting to find the keys for carrying out photosynthesis industrially, physically independent of algal or plant cells. This is certainly logical. The chemical process of photosynthesis is highly efficient and produces electrons, oxygen, and hydrogen. In the laboratory, some algae have been induced to produce hydrogen gas, which could be used in fuel cells (Melis, 2005). Hopefully, if this can be accomplished without negative side effects (as in atomic energy), then perhaps with a more or less inexhaustible energy source we could concentrate on environmental recovery. However, as we have shown, photosynthesis is a highly complex process, and chlorophyll does not function when it is stripped from its supporting protein molecules and lipid membrane. Perhaps the new science of nanotechnology (the physical manipulation of molecules and atoms) can help us out with this problem. While human understanding of physical and biological processes, and our achievements at engineering that knowledge for practical human use, is phenomenal by any measure, not all natural processes can be reduced to practical

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human use, especially in the time frame we may require. As we discussed in the Introduction, our approaching socio-political collision with the exhaustion of oil energy, coupled with an ever-growing pollution of the Earth’s atmosphere and water, and increasing disruption of natural ecosystems gives us little lead time. We cannot wait on the engineering of photosynthesis to solve these problems. In this book, we describe how we can achieve that “symbiosis” with photosynthesis, not only for the management of aquaria and ecosystem models, but also for the restoration of wild environments and the recovery of our socioeconomic system. However, above all, it requires an understanding of photosynthesis, both in algae and in the higher plants.

SOLAR RADIATION AND WATER Any atom or physical mass, including the sun, radiates electromagnetic energy in accordance with its temperature. Beginning at about 800 K (degrees centigrade plus 273), visible light in the red end of the spectrum begins to be radiated. As the temperature increases, emitted wavelengths (and the amount of energy radiated) increase. An incandescent bulb has a color temperature of 2800 K and is quite red; a cool-white fluorescent bulb radiates at about 4000 K and is strongest in the redorange. Daylight fluorescent bulbs and the sun radiate at about 6000 K. Unfortunately, the magnitude of visible radiation is measured in many ways. Wherever possible, we use an energy measure: microeinsteins per square meter per second (millimoles). For rough comparison, 2000 µE/m2/s is approximately 100 000 lux or 10 000 foot-candles. In the middle of a bright sunny day, early summer at high latitudes and year-round in the tropics, approximately 2000 µE/m2/s of visible or photosynthetically active radiation (PAR) is received at the Earth’s surface. Depending on the clarity of the water in question, this radiation can extend to great depth or be limited to a few meters (Figure 5.4). The total solar radiation received per day over the Earth is shown by month for various latitudes in Figure 5.5. The yearly total is shown in Figure 5.6. Generally, higher latitudes have greater seasonal variability in incoming light. While progressively north and south of latitude 40 total yearly radiation is considerably reduced, in a broad range of mid-latitudes total incoming radiation is mostly a function of cloudiness or atmospheric clarity. Light incoming to the Earth’s outer atmosphere has roughly the spectrum shown by the top curve in Figure 5.7. By the time it passes through the atmosphere and reaches the sea surface through clear sky or clouds, it looks more like the second or third curves. Shaded areas

FIGURE 5.4 Attenuation of PAR in different types of water. After Kirk (1994). Reprinted with permission of Cambridge University Press.

FIGURE 5.5 Change in incoming solar radiation at the top of the atmosphere calculated seasonally and for different latitudes. After Kirk (1994). Reprinted with permission of Cambridge University Press.

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FIGURE 5.6 Mean annual insolation (solar radiation) on the surface of the Earth (calories/cm2/year 103). Note that the greatest yearly totals occur in the horse latitudes rather than in the tropics proper. However, the seasonality is considerably greater in the horse latitudes, with higher levels in summer and considerably lower levels in mid-winter (see also Figure 5.5). After Gates (1980).

FIGURE 5.7 Spectral quality of incoming solar radiation, light reaching the Earth’s surface (through clear and clouded sky), and light transmitted through terrestrial vegetation. After Gates (1980).

Solar Radiation and Water

without significant local reflection and those under green foliage are the fourth and fifth curves. Further, attenuation in lakes or the sea provides a color balance that is even more removed from the original spectrum.

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The resulting attenuation at different wavelengths varies greatly depending on depth and water character. Curves for light distribution with depth for open ocean, clear coastal water, and a lake are shown in Figure 5.8.

FIGURE 5.8 Spectral quality of solar radiation transmitted through natural waters (marine and fresh) of varying character. After Kirk (1994). Reprinted with permission of Cambridge University Press.

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In general, pure water absorbs longer wavelengths above 550–600 nm and thus, given enough depth, will appear green or ultimately blue. Suspended particulates and dissolved substances absorb the shorter wavelengths, and typically as one passes from open ocean to coast, to estuary, and then to river and lake, more of the wavelengths below 500 nm and eventually even 600 nm are absorbed. Thus, depending on the extent of matter in the water, one passes from blue, to green, to yellow, to red or brown in making such a transect. This is also an indication of the kind of light that is available at depth. Further upstream, into mountain lakes and streams (at least when they lack glaciers), the number of particulates usually decreases along with nutrients and planktonic algae. Under these conditions, water clarity and the blue-green character of the water return.

LIGHT ABSORPTION BY WATER PLANTS Plants, including algae, utilize a wide variety of accessory energy-absorbing pigments in addition to the allimportant chlorophyll. Each of these pigments requires specific wavelengths to be photosynthetically efficient. Plants are generally classified into evolutionary groupings, most easily designated by color and therefore by their photosynthetically active pigments. The green plants include the flowering plants such as marsh grasses and all submerged aquatic vegetation as well as green algae including Ulva (sea lettuce) and Enteromorpha. The brown algae, with virtually no fresh water or terrestrial representatives, include large marine plants such as Laminaria (kelp) and Sargassum. The red algae, mostly marine with a few species in fast-running streams, include Chondrus (sea moss) and Rhodymenia (dulce). The blue-green algae (Cyanobacteria) are filamentous or unicellular plants that form slimy crusts, ribbons, or cushions of varying hues (green, red, black, etc.) that are common in most lighted wild environments as well as in many fresh- and saltwater aquariums. Finally, a number of widespread algal groups particularly important as plankton include golden-brown algae (diatoms) and yellow-brown algae (dinoflagellates). The chlorophylls and the accessory pigments used by higher plants, and marine and aquatic algae absorb light for photosynthesis at particular wavelengths or groups of wavelengths. These absorption peaks tend to be in the blue-green and the far-red wavelengths. However, the actual absorbance by plants and the action spectra (or photosynthetic activity) of those plants, including the major phyla of marine algae (Figures 5.9 and 5.10), are more smoothed or spread out. In general for a plant

FIGURE 5.9 Spectral absorption of the freshwater macrophyte (flowering plant) Vallisneria spiralis. After Kirk (1994). Reprinted with permission of Cambridge University Press.

community, particularly an algal community, the photosynthetically active pigments cover the visible spectrum. As stated by Mathews and van Holde (1996) “scarcely a photon can come through that cannot be absorbed by one chromophore (pigment) or another.” Heldt (2005) demonstrates how the red and blue pigments of red algae and cyanobacteria, phycoerythrin, and phycocyanin (structural relatives of chlorophyll) are in effect “extra antennae” that are arranged on the surface of the granae membranes on top of or near chlorophyll “a” Photosystem II reaction centers. Photons are captured by the accessory pigments and subsequently the energy transferred (as a fluorescence process or excitons) to the chlorophyll “a” reaction centers, allowing these algae (and cyanobacteria) to use light thru the middle of the visible light range where the chlorophylls are inactive.

LIGHT INTENSITY AND PLANTS In addition to color balance or spectrum of solar radiation, a major concern in photosynthesis is the total intensity of the radiation. Many plants including marine and aquatic plants are highly adaptive to available light. Plants of a given species grown at high light intensity will perform more poorly under low light than plants raised at low intensity. It is characteristic of many algae that with a major change in solar radiation the plants will die or die back and develop new growth adapted to the new light levels. Terrestrial plants from normal sunny habitats typically show a pattern of photosynthesis with available light similar to that of the bean (Figure 5.11). At cool temperatures leaves of this plant show a more or less direct and strong increase of photosynthesis up to about one-third of full tropical sunlight. Above that

Light Intensity and Plants

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FIGURE 5.10 Action (- - - -) and absorption (—) spectra of photosynthesis in various marine algae. While the two curves usually coincide and light absorbed is utilized in photosynthesis, that is not necessarily the case, particularly at the ends of the spectrum. (A) Ulva (green); (B) Coilodesme (brown); (C) Delesseria (red); (D) Chlorella (green); (E) Skeletonema (diatom). After Kirk (1994). Reprinted with permission of Cambridge University Press.

level up to the strongest natural light possible, photosynthesis continues to increase but at a slower rate. On the other hand, at high midday leaf temperatures photosynthesis considerably increases up to the most intense solar light possible on Earth. Most physiological studies of plants are carried out on small specimens or pieces of those plants. As shown in Figure 5.12, there is a major difference between the photosynthetic performance of whole plants compared to their parts. The relationship between light and photosynthesis for entire trees is almost direct to the full intensity of sunlight. An often quoted pattern of underwater photosynthesis is that of phytoplankton, as shown in Figure 5.13. Here, photosynthesis peaks at about one-quarter of

surface light, and at higher intensities it is actually inhibited. The same results are obtained in more recent, sophisticated computer modeling (Behrenfeld et al., 2002). On the other hand, benthic plants, both flowering plants and algae, do not show an obvious inhibition (Figure 5.14). One might conclude from these data that while many land plants, given no limitation by other factors (e.g. carbon dioxide or temperature), can use all of the possible solar radiation available for photosynthesis, marine and freshwater plants saturate or even lose production at levels of one-quarter to one-half of available surface radiation. However, if one looks at production by entire benthic plant communities in the wild, almost

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FIGURE 5.11 Light response at different temperatures of the bean Phaseolus vulgaris, a tropical plant characteristic of sunny sites. At lower temperatures photosynthesis is limited by molecular and chemical processes controlled by temperature, rather than by light itself. After Gates (1980).

FIGURE 5.13 Photosynthetic rates of Sargasso Sea (•) and Lake Windemere (• • ) phytoplankton as a function of light levels (laboratory experiments). After Kirk (1994). Reprinted with permission of Cambridge University Press.

FIGURE 5.12 Photosynthesis rate for two terrestrial, woody plant species – individual leaves as compared to the entire trees. After Oliver and Larson (1990). Reprinted with permission of John Wiley & Sons, Inc.

invariably primary production (or water purification, if one is thinking in those terms) is limited seasonally and daily by the available solar radiation (Figures 5.15–5.18). Figure 5.15 illustrates the relationships particularly well.

While 50% of production is achieved when 500 µE/m2/s is reached (a few hours after dawn), full production is only achieved at noon, at light intensities close to full tropical sunlight. Below maximum intensity (and down


FIGURE 5.14 Photosynthetic rates of (A) various submerged macrophytes (flowering plants) and (B) algae as a function of light levels. After Kirk (1994). Reprinted with permission of Cambridge University Press.

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FIGURE 5.15 Photosynthesis (day) and respiration (night) as measured on a Caribbean coral reef (Panama): (A) oxygen exchange vs time; (B) oxygen exchange vs light in situ on reef; (C) oxygen exchange vs light for an in situ microcosm of the reef. After Griffith et al. (1987). Reprinted with permission of The American Society of Limnology & Oceanography.

FIGURE 5.16 Photosynthetic rates of kelp as related to light levels (at depth of growth) throughout a 1-year cycle. After Kirk (1994). Reprinted with permission of Cambridge University Press.

to about 500 µE/m2/s) every 10% reduction in intensity causes a 5% reduction in production. Likewise in a coldwater kelp community (Figure 5.16), light and temperature are not in phase. Yet yearly photosynthesis closely follows available light independent of temperature. Factors other than light may also limit plant production. Plankton production in higher latitudes in lakes and oceans, for example, typically rises sharply in the spring, as the light returns and no nutrient limitation exists. There may be dips in production in midsummer, but this is usually due to nutrient limitation or grazing by zooplankton. Phytoplankton production and more rarely benthic plant production can be limited by ultraviolet (UV) radiation near the surface. This limitation is minimal, however, and likely more than made up for


FIGURE 5.17 Diurnal oxygen exchange of a tropical coral reef community by season. After Adey and Steneck (1985).

FIGURE 5.18 Gross primary productivity of four sections across a well-developed shallow-water tropical coral reef community (St. Croix, U.S. Virgin Islands) as a function of light, season, available surface, and biomass. After Adey and Steneck (1985).

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FIGURE 5.19 Generalized spectral characteristics of natural water bodies and the artificial light typically required to provide underwater light in aquarium and mesocosm models of those water bodies.

by increased plant production in deeper water, particularly in benthic communities.

PHOTORESPIRATION As we pointed out above, photosynthesis involves two primary steps: (1) the capture of solar energy in electron excitation, with the electrons derived from the splitting of water molecules (with the release of gaseous oxygen, O2) and (2) the transfer of electrons to NADP and ADP, the energy transfer molecules, on the granae of chloroplasts. The resulting NADPH and ATP are then available in the chloroplast stroma to drive the

Calvin cycle and reduce CO2 to make the sugar phosphoglyceraldehyde and eventually glucose (a process called carbon fixation). The simplest way to determine the magnitude of photosynthesis is to measure oxygen release. All of the measures of photosynthesis diagrammed above were based on determining oxygen release. However, primary production refers to the completion of the process and the net fixation of carbon (from carbon dioxide) in simple carbohydrates. Ribulose 1,5-bisphosphate (RuBP or Rubisco) carboxylase is a critical enzyme in the fixing or incorporation of carbon dioxide in the dark phase of photosynthesis (the Calvin cycle). It has been known for some time that in many higher plants, under some conditions (especially

Light and Model Ecosystems

high temperatures and low carbon dioxide availability) RuBP carboxylase acts as an oxidizer, “respiring” the intermediate products of photosynthesis without providing net energy or biomass to the plant. Some groups of higher plants, particularly the grasses or C4 plants, have developed mechanisms to avoid the effects of photorespiration. Others, with the C3 or standard Calvin cycle, simply perform poorly when matched with C4 plants in intense light at high temperatures. Although all or most algae appear to have C3-like pathways, photorespiration seems to generally be suppressed in algae (Lobban and Harrison, 1994). In algal turfs under coral reef environmental conditions, which we discuss at some length in later chapters, studies have shown no evidence of photorespiration (Hackney and Sze, 1988). It has been assumed that bicarbonate (HCO3) under normal conditions in aqueous environments, especially in the sea, is available to algae as a carbon source and this prevents the significant occurrence of photorespiration. It is unlikely that carbon, as a nutrient, can ever be limiting in marine environments (see coral calcification, Chapter 10). However, this may not be so in highly productive freshwater environments (see Chapter 25).

LIGHT AND MODEL ECOSYSTEMS Until the 1980s, because of the rule of thumb that aquatic plants used only a fraction of available sunlight, model ecosystems tended to be operated with relatively low light levels. In the aquarium world, light was largely considered to be solely for the viewer and perhaps for the activities of fish. Particularly in marine tanks, if algae were present, they were primarily the encrusting blue-greens that could manage the low light levels (and low water quality). Because these algae were often black (and slimy), even such a minimum presence was not desired. Moe (1989) documents this history and provides an excellent review of the changes in attitude among aquarium hobbyists, particularly those specializing in reef tanks. In the reef aquarium world, the approach has shifted radically, and now we find many of the more advanced hobbyists seeking out the various actinic, 10 000 K or even 20 000 K, lamps. These lamps have a spectrum that is shifted far to the blue. If the primary interest is to culture deeper water corals or a deep reef ecosystem, this approach is perhaps warranted. On the other hand, most Acropora, Millepora, and Porites species, among many others, grow most rapidly where they receive greater than 1000 µE/m2/s, at the equivalent of 5000–7000 K (i.e. little shift from the natural spectrum of sunlight), through the middle of the day (Adey,

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1978). Algal turf communities in exposed reef flats reach peak production at midday light intensities of about 1500 µE/m2/s (Adey and Hackney, 1989). Small and Adey (2001) demonstrate system calcification rates equal to the faster growing coral reefs in the wild, as well as the fastest, published Acropora growth rates, using six, 160-W VHO fluorescent lamps on a 130-gallon coral reef system (see Chapter 20). At the distance involved in the formal coral growth studies, light received would have been about 1500 µE/m2/s. When planning light simulation in microcosms, mesocosms, and aquaria, our rule of thumb is to match both light spectrum and light intensity as closely as possible to those of the wild ecosystem being modeled. In general, if desired for reasons of economics, light intensity may be reduced by 20–30% of that in the wild without major effects, but greater reductions would seriously compromise the system biologically and ecologically. Likewise, if there were considerable benefits to be derived, one might omit some of the green-yellow part of the light spectrum, but it is likely that some part of the ecosystem would be compromised. A great number of artificial light sources are now available for use in model ecosystems. Delbeck and Sprung (2005) provide an excellent summary of the more recent lighting developments as they apply to the building of coral reef aquaria. These produce a diverse range of intensity and spectra (Color Plates 7 and 8). Tungstenfilament lamps produce light useful to plants. However, a tungsten lamp produces little green and blue light, whereas it is in the blue-green end of the spectrum that aquatic plants carry out a major part of their photosynthesis. They are also relatively inefficient in terms of PAR produced compared to heat. On the other hand, the gas lamps – fluorescent and metal halide – produce a wide variety of light spectra, much of it within the photosynthetically useful range (Color Plates 7 and 8). In addition, they are quite efficient in terms of power usage. Many spectral types of fluorescent lamps are available and, with appropriate mixing of color types, the spectrum of incoming sunlight to a marine or aquatic community can be reproduced. The intensity of the standard fluorescents is, however, relatively low and, although they are strong enough to supply the light requirements of the deepest-water or heavy-shade communities, they are not generally suitable for most sun-dependent ecosystems, especially those from shallow tropical areas. High-output (HO) and very-high-output (VHO) fluorescent lamps can be found in most of the spectral types of standard fluorescents. The same size as standard lamps, they put out approximately twice and four times as much radiation, respectively. (Output is roughly proportional to wattage.) For most small systems (less than 200 gallons), especially fresh- and cold-water coastal

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microcosms, these lamps are suitable. For coral reef or similar brightly lit communities it is possible to use VHO lamps, particularly if the tank is relatively shallow. However, the light levels of the shallowest coral reefs cannot be effectively produced by this means, and the number of lamps that have to be used require major wiring efforts. For large (deeper) microcosms and mesocosms, and even larger coral reef aquaria, only the high-intensity discharge lamps, which can be obtained from 250 to 1000 W, provide sufficient light to simulate shallow-water intensities. For larger systems, of all commonly available light sources, metal halide lamps have been found to provide the best combination of spectrum and intensity for simulating natural sunlight (Color Plates 7 and 8). These lamps are now available in 2000–6000 K and much higher models, solving the most acute spectrum problems. However, achieving an even distribution of 6000 K light at 1000 µE/m2/s for a shallow reef flat requires a dense aggregation of the highest wattage lamps. In ecosystem models, the intensity and period for which artificial lighting is used can be varied to suit conditions in the native environment of the community being supported. For instance, the microcosms holding the coral reef communities (see Chapter 20) are modeled after areas in the tropical Caribbean between 10° and 25° north latitude. Day length at those localities (photoperiod) ranges from about 11 to 13 h over the year, and incoming light intensity at noon, just beneath the water surface, measures about 1800 µE/m2/s in summer and 1400 µE/m2/s in winter. The “cold tank” (Chapter 21) represents the Maine coast, 2000 miles to the north, where photoperiod and light intensity change significantly with the season. In summer the sunlight is almost as strong as that of the tropics and the day is even longer. However, in the winter, light intensity drops dramatically to about 800 µE/m2/s just below the water surface at noon and there are only 6–7 daylight hours. Lighting for these microcosms was planned with these conditions in mind, and the diagrams of the arrangements that reproduce them are shown in Chapters 20 and 21. Clear 500–1000 W lamps are used to light the tropical tanks, the brighter lamps over the deeper areas. Although output directly beneath individual bulbs exceeds the intensity of natural sunlight in the tropics, the light level decreases rapidly with distance from the center of concentration. The physical size of the light units prevents there being more than one bulb for every 3 square feet of tank surface; thus the mean light intensity per unit surface is lower than that found in the tropics. Peak intensity is, however, stretched out over a longer period each day. On the other hand, lower intensity in midday results in a rapid dwindling of light as it penetrates the water and increases the

effective depth of the microcosm. The light at the bottom of the reef tanks at 6 feet is equal to that measured at 40–60 feet in the natural reef environment. The result is that the microcosm contained in this tank is essentially a scale model, relative to light, and includes 40–60 feet of reef profile (relative to light) in only 6 feet of water. Many opportunities and problems are presented by this compression of depth zones. The cold-water and temperate microcosms, as we have arranged them, are also lighted at least partially by metal halide lamps. The bottom in the Maine tank slopes steeply, and the turbidity is moderate. The community represents a cross section that reaches from the intertidal zone nearly to the limit of the photic zone. While summer radiation in the Maine intertidal zone can be close to that received by an exposed reef, or algal ridge, in the tropics, even during times of strongest sunlight, the energy that reaches the subtidal organisms in the coastal Gulf of Maine is much less than that in the clear water of the tropics. Turbidity is caused by runoff from the land, tidal stirring of sediments, and the bloom of planktonic organisms responding to high nutrients and the seasonal increase in light. A light measurement equivalent to a depth of about 50–60 feet is registered at the bottom of the Maine tank, while the intertidal zone receives light levels close to those found in the wild. As we discuss in Chapter 21, the lights are raised and the daylight period shortened to simulate winter light levels. In the Smithsonian Chesapeake estuarine mesocosm, the shallow and emergent marshes required maximum intensity, and we used four 1000-W metal halides, at a height of about 3 feet above the soil surface, for about 20 square feet of marsh area. It is interesting to note that while radiation of 1200–1800 µE/m2/s is characteristic of the upper third of the marsh plants, many will grow well into the high-intensity cone of light, exceeding 4000 µE/m2/s, with apparent healthy color ceasing only when temperatures finally become too high. On the deeper end of the Chesapeake tank, eight 160-W VHO lamps are used to simulate reduced light in the highly turbid bay analog. Thus, for the marsh, a maximum equivalent intensity of 200 W/ft2 is used whereas in deeper water levels drop to 32 W/ft2 (electrical rating). The period of illumination of each mesocosm, microcosm, and aquarium that we have constructed (i.e. the “day length”) is controlled automatically by timers that open and close the light circuits according to a preset program. However, full intensity is not delivered to the microcosms for the entire period of illumination, but changes gradually to imitate the periods of dawn and dusk. This is accomplished by lighting or extinguishing parts of lights in sequence over a period lasting up to 2 h between each light and dark cycle. This allows

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the tank inhabitants a transition period between day and night activities. Most marine organisms are sensitive to light changes. Some animals are nocturnal, functioning only during dark periods, while others are active in the daytime. In some cases, these transitions are striking. Parrotfish, for instance, rest in a secreted bag of mucous in the dark hours and feed continuously during the day. A reasonable twilight or changeover time is desirable. The total light energy available to a microcosm is a function of period as well as intensity, the length of time as well as the brightness. To a limited extent, a deficiency of light intensity can be compensated for by lengthening the period, but probably with some loss of accuracy in simulation results. Many plant and animal responses are related to day length, especially in populations from higher latitudes where seasonal variation is significant. Often growth and reproductive cycles can be closely connected with light period. As Delbeck and Sprung (2005) discuss, there are a multiplicity of new lighting shapes, sizes, and color temperatures, as well as increasingly sophisticated controlling systems available to the aquarist and modeler. However, the basics have not changed over the last decade. There is great hope for the potential of LED lighting, but the intensities required for coral reefs or most shallow-water ecosystems are not yet available. It is hard to imagine how one could use a metal halide lamp of 10 000 K, except possibly for a very large deepwater ecosystem. Those authors do point out that with the now available lighting, it would be possible to provide harmful UV light to corals and they suggest means for measuring and avoiding the problem. The approach we have shown in Figure 5.19 can be adapted to some of the newer lighting types.

LIGHT AND PHYSIOLOGICAL CONSIDERATIONS The reprocessing of animal and bacterial metabolic wastes and oxygen production occur as natural parts of algal metabolism in well-lighted situations. However, a sufficient biomass of plant material must be maintained to provide the production of plant food needed to accommodate the full requirements of plant-eating animal populations. It is possible to balance this interaction within a single large tank, but usually this requires that the number of animals be limited to their average abundance in the natural environment, especially if herbivorous species that might deplete the algae are included. When the lights go out at night the plants stop producing oxygen and, if the animal population is large, the oxygen supply dissolved in the tank water

can be greatly reduced before morning. Many shallow marine and aquatic environments have relatively dense populations. However, in the wild, during the night, the constant flow of water from less populated areas of the open ocean, lake, or river supplements the supply of oxygen and removes wastes. This situation where one ecosystem supplies the needs of another is common in the wild and can be adopted to preserve the nighttime balance in an aquarium. Rather than using a large reservoir to replenish the water at night, a method of ensuring continuous water conditioning by plants can be utilized. Our microcosm systems are connected to separate units that are reserved for the cultivation of a specialized community of algae. These units are lighted at night when the microcosms are in darkness, and they supply a constant flow of oxygenated, decontaminated water. This process (algal turf scrubbing) and the mechanisms built to support it are described fully in Chapter 11. Light measurement is an important part of microcosm management. It is also one of the most difficult of physical factors to quantify. A number of instruments are available for sensing intensity. Examination of spectral characteristics, while not difficult, requires even more sophisticated instrumentation. In general, if proper light measuring equipment is not available, the guidelines provided above will suffice if the bulbs are replaced on a regular basis (every 6 months).

SUMMARY The light phase of photosynthesis is highly efficient, perhaps more so than any other process in nature (and certainly far more than industrial creations, Barter et al., 2002). However, the second or dark phase is limited in several ways by the basic inefficiencies of the key enzyme Rubisco. The light phase in many planktonic algae is inhibited by high light levels and is therefore reduced in production capability. This may in part be a result of the UV that accompanies the useable part of the light spectrum, but is more likely the result of excess O2 production, and oxidation of the photosynthetic centers. In most benthic algae and the higher plants, it is the dark reactions that are more limiting. In the higher plants, “photorespiration” (basically a chemical “confusion” between CO2 and O2) can be a problem especially when temperatures are high. Some desert and tropical plants (C4 and C5 plants) have developed mechanisms to concentrate CO2 at reaction centers and thereby avoid photorespiration. However, this reduces the efficiencies of those plants under more equable conditions. Benthic algae are at least mostly C3

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plants and rarely have to deal with excessive temperatures and photorespiration. The process of ATS (algae turf scrubbing) that we describe in this book, is a way to optimize photosynthesis for ecosystem modeling and environmental restoration. This solar–algal process removes many of the deficiencies of “wild” photosynthesis, and could well be a critical tool to stabilize the earth’s environments until the scientific community can create a viable artificial photosynthesis without negative side effects. ATS avoids both photorespiration and photo-oxidation/ inhibition. By forcing water/cell contact through surging, it also avoids the additional serious problem of nutrient deficiency that occurs in most benthic and planktonic algae (as well as higher plants). “The same surging motion provides for light flashing on cells, avoiding inhibition due to “over-lighting” and shading. The latter problem is so severe in the more typical algal reactors, that some groups of scientists are working to genetically engineer planktonic cells to both operate at lower light levels and to reduce light absorption (Melis, 2005). ATS is a planar, rather than a volume system, rendering harvest an efficient process of scraping or suction rather than filtering. In the terrestrial plants, primary production has a basic limitation resulting from the coupling of CO2 uptake and water loss. When carbon dioxide uptake and energy production is being considered, water for enhanced terrestrial production (irrigation) is rapidly becoming a serious issue; this is not a factor in large-scale ATS systems.

References Adey, W. (1978) Coral reef morphogenesis: a multidimensional model. Science 202: 831–837. Adey, W. and Hackney, J. (1989) Harvest production of coral reef algal turfs. In: The Biology, Ecology and Mariculture of Mithrax spinosissmus Utilizing Cultured Algal Turfs. W. Adey (Ed.). Mariculture Institute, Washington, DC. Adey, W. and Steneck, R. (1985) Highly productive eastern Caribbean reefs: synergistic effects of biological, chemical, physical and geological factors. In: The Ecology of Coral Reefs. M. Reaka (Ed.). NOAA Symposium Series on Underwater Research, Vol. 3, Washington, DC.

Barter, L., Bianchietti, M., Jeans, C., Schilstra, M., Hankamer, B., Diner, B., Barber, J., Durant, J., and Klug. D. (2002) Biochemistry 40: 4026–4034. Behrenfeld, M., Esaias, W., and Turpie, K. (2002) Assessment of primary production at the global scale. In: Phytoplankton Productivity. P.J. Williams, B. le, D. Thomas, and C. Reynolds (Eds). Blackwell Sci, Oxford. Delbeck, C. and Sprung, J. (2005) The Reef Aquarium, Science Art and Technology, Vol. 3. Ricordea Publishing. Coconut Grove. Diamond, J. (2005) Collapse, How Societies Choose to Fail or Succeed. Penguin. Gates, D. M. (1980) Biophysical Ecology. Springer-Verlag, Berlin. Griffith, P., Cubit, I., Adey, W., and Norris, J. (1987) Computer automated flow respirometry: metabolism measurements on a Caribbean reef flat and in a microcosm. Limnol. Oceanogr. 32: 442–451. GTE/Sylvania (1987) Color Is How You Light It. Catalog. Sylvania Lighting Center, Danvers, Massachusetts. Hackney, J. and Sze, P. (1988) Photorespiration and productivity rates of a coral reef algal turf assemblage. Marine Biol. 98: 483–492. Heldt, H.-W. (2005) Plant Biochemistry. Elsevier, Amsterdam. Keeton, W. T. and Gould, J. L. (1986) Biological Science, 4th edn. Norton, New York. Kirk, J. T. O. (1994) Light and Photosynthesis in Aquatic Ecosystems, 2nd edn. Cambridge University Press, Cambridge. Lee, R. (1999) Phycology, 2nd edn. Cambridge University Press, Cambridge. Lobban, C. and Harrison, P. (1994) Seaweed Ecology and Physiology. Cambridge University Press, Cambridge. Lovins, A., Datta, E. K., Bustnes, O.-E., Kooney J., and Glasgow, N. (2004) Winning the Oil Endgame. Rocky Mountain Inst. Snowmass. CO. Mathews, C. and van Holde, K. (1996) Biochemistry. Benjamin/ Cumming, Menlo Park, California. Melis, A. (2005) Bioengineering of green algae to enhance photosynthesis and hydrogen production. In: Artificial Photosynthesis. A. Collings and C. Critchley (Eds). Wiley-VCH, Weinheim. Moe, M. (1989) The Marine Aquarium Reference. Green Turtle Publications, Plantation, Florida. Oliver, C. and Larson, B. (1990) Forest Stand Dynamics. McGraw-Hill, New York. Pace, R. (2005) An integrated artificial photosynthesis model. In: Artificial Photosynthesis. A. Collings and C. Critchley (Eds). WileyVCH, Weinheim. Rheinheimer, G. (1985) Aquatic Microbiology. Wiley, New York. Small, A. and Adey, W. (2001) Reef corals, zooxanthellae and freeliving algae: a microcosm study that demonstrates synergy between calcification and primary production Ecol. Eng. 16: 443–457.

C H A P T E R

6 The Input of Organic Energy Particulates and Feeding

The treatment of suspended particulates has been largely ignored in most aquatic models used for research and in virtually all aquaria. Unfortunately, in most cases standard filtration methods remove, or at least attempt to remove, the particles, radically altering their size and quality distribution and rarely is this quantified. Traditionally, the filters employed by aquarists have been standard bacterial (biological) types, though more recently trickle filters, protein skimmers, and in some cases resin columns have been used. These devices are designed to trap particulates as well as support biofilms. Less obtrusive “nonfiltration” methods such as rotating drums employing bacterial or algal films have also been employed in aquaculture, though rarely in aquarium or ecosystem models. In this book, we emphasize the use of algal turf scrubbers (ATS) to control water quality (oxygen, pH, nutrients, etc.). Some capture of particulates occurs in these devices (see e.g. Adey et al., 1993); however, relative to particulates, ATS act more like biofilms than filters. Particles, whether of inorganic or organic material, are an integral part of all aquatic ecosystems. In some cases, the use of bacterial or simple physical filtration (or better biofilm capture) might be a valuable component of modeling, for example, to simulate the sinking of plankton and other particulates out of an open, surface-water system. However, when such methods are used, the modeler or aquarist needs to insure that the filters are functioning in the manner intended and are not radically altering the model to a state very different from that desired. Although we have not studied the effects of a variety of filtration systems on a community of plankters (including reproductive stages), we have examined the effects of standard impellor pumps. In general, an impellor pump will select the very small

flagellated microalgae, by removing the larger plankters from the water column. Depending on the exact nature of the filter involved, and the turnover time of the system (all the water in the system passing through a pump or filter several times an hour will have a far greater effect than a turnover of once in several days, particularly on reproductive stages), filters are likely to have far more significant effects than pumps alone. As we describe in Chapter 20, we have had repeated coral larval settlement out of the water column in systems without centrifugal pumps and with very low turnover, and we have not seen significant coral settlement in systems with impellor pumps.

PARTICULATES, ENERGY SUPPLY, AND AQUATIC ECOSYSTEMS All organisms and therefore their ecosystems require energy to function. For most higher plants and algae, that energy source is solar, through the process of photosynthesis. Energy from chemosynthesis, and particularly from volcanic vents along mid-ocean ridges, is quite interesting, but globally is very small as compared to photosynthesis. For many animals and bacteria, the energy source, through food webs, is based directly in higher plants and algae. However, for some very large water ecosystems (e.g. the deep ocean and deeper parts of lakes), most of the direct organic energy supply is derived from particulates originally created by photosynthesis and primary production in shallow water. It is well known that small, planktonic algae, protozoa, and bacteria (which can be considered particulates) are fed on by a wide variety of larger filter feeders, and provide the base of open-water food webs. It is not as

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FIGURE 6.1 Diagrammatic representation of the “mass balance” of particulates in a bottomdominated aquatic ecosystem. Modified after Johnson et al. (1990).

widely recognized, at least in aquatic systems modeling, that the ocean, lake, or river “soup” is in large measure made up of suspended particles, in part inorganic, but in large measure organic but nonliving. This is the detritus of the more obvious organisms and their food webs; it consists of the body parts of animals and higher plants, algal fragments, and fecal material, usually coated with fungal hyphae and/or bacteria, and is called particulate organic material (POM). As it degrades, POM ranges down to the state of dissolved organic material (DOM). These particulates are not, by any means, the end point. They continue to be an energy source in mid-water detrital food webs. Even in the dissolved or extremely small particulate state, these organic materials can be absorbed by bacteria, some animals, and algae, they can aggregate to form larger particulates again, or they can be adsorbed onto larger particles and organic films that have developed on surfaces (Figure 6.1). In addition, ecosystems are rarely closed in the sense that the energy supply is only directly from solar sources. Almost invariably there is an input from an adjacent ecosystem of living or dead organisms and organic particulate materials that are derived from dead organisms, including fecal materials. Coral reefs are among the strongest and most efficient photosynthetic communities on Earth, and yet a significant (⫾10%) part of a typical reef’s energy supply is derived

from the capture of oceanic plankton (Chapter 20). In some very large ecosystems (e.g. the mid-ocean and deep ocean), the only energy supply is through the organic particulates or “marine snow” from surface waters. This particulate transport route is so important to biosphere function that it can determine ocean chemical composition (Stumm, 1987; Boyd et al., 2000; see also Chapter 3). Finally, marine snow is probably the “sink route” for about one-half of the anthropogenic carbon as carbon dioxide that is currently released yearly into the atmosphere. The “sinking” of organic material in the open ocean, after both trophic (food web) and microbial loop reworking, can be quite substantial. Because of this, in the 1990s a plan was developed and eventually tested to increase planktonic photosynthesis in the Southern Ocean (Boyd et al., 2000), hopefully to greatly increase carbon dioxide removal from the atmosphere. In this global-encircling ocean, where land contact is minimum, the potential for iron limitation of photosynthesis (Table 4.4) becomes a reality. The concept was to greatly increase photosynthesis by spraying very fine iron particulates on the ocean surface from freighters. Theoretically, this iron would dissolve and be uptaken by phytoplankters previously limited in production potential. Eventually, the increased organic material developed would form “marine snow” that would fall to the deep ocean, taking carbon out of the atmosphere

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semi-permanently and reducing the effects of global warming. After several trials, this “ocean-seeding” process did not turn out to be as effective as first thought, and because of additional environmental concerns, the idea is on hold. Carbon is often used as a proxy for bioenergy exchange and storage. However, the largest volume of stored carbon near the surface of the Earth lies in inorganic limestones and dolomite, bearing no energy storage. By far the largest proportion of organic (energybearing) carbon on Earth is in coal, oil, gas and kerogen, stored over the last 300–400 million years. Only 1/3000 of the organic carbon on Earth occurs in the biosphere, and only 1/20 000 occurs in the atmosphere. The current scientific evidence strongly indicates that if a fraction of this stored carbon were to be released into the atmosphere, especially considering that human society is continuously reducing the potential for photosynthetic production and accumulation in the biosphere, the Earth would be driven into a super-heated, dead Venus-like state. Why wouldn’t it just return us to the “ocean soup” of billions of years ago? Probably because the Earth’s mantle is out-gassing and continuously producing “new carbon.” While that rate is very small, over the more recent 300–400 million years it has produced much of the organic carbon currently on Earth. In addition, it is generally thought that the sun produces more radiation now than it did during early Earth time (see e.g. Figure 5.1). In short, we cannot go back; we must keep the stored carbon out of the atmosphere, but managing oceanic particulates alone is unlikely to accomplish this need. Assuming that some of the energy supply remains unconverted to organism function and low-level heat, material input to an ecosystem must be balanced by internal storage of organic materials. This will happen by the buildup of nutrients and other elements, by a temporary buildup of living biomass (e.g. a newly set mussel bed), or by equivalent export. We discuss the storage and export equivalents in model ecosystems in Chapters 3, 9, and 11. The form and magnitude of organic particulate input is the primary subject of this chapter.

INORGANIC PARTICULATES In many aquatic environments inorganic particulates are derived from the terrestrial erosion of rocks and the soils produced by the precipitation and atmospheric weathering of rocks. Sand to silt-size particles do not remain suspended for long (Figure 3.8). However, fine clay particles do remain in suspension for long periods and can be carried great distances by

moving waters. Particularly in large and very deep waters, such as the open ocean, clays can provide the primary source of bottom sediment. Ocean sediments are dominated throughout much of the shallow open ocean by calcium carbonate provided by the rain of tests or shells from coccolithophore planktonic algae; at more moderate depths, sediments become dominated by shells of foraminifera and pteropods, and deeper by the siliceous particles derived from diatoms and radiolarians. Both calcium carbonate and siliceous particulates slowly dissolve as they sink. In the deepest ocean waters only the red clays remain. Many groups of animals, particularly some foraminifera (and other protozoans), and many polychaete worms in the sea and chironomids (mayfly larva) and caddisfly larva in fresh water build their external skeleta by “glueing” together primarily inorganic particulates. Although organism-derived, these are mostly inorganic and do not bring an energy component; we treat these particulates in Chapters 3 and 18. To chemists and atomic scientists, all matter including atomic and subatomic materials is particulate, and dissolved inorganic elements and ions we treated in Chapter 4, under water chemistry. This was done, even though we recognize that there is no sharp line, relative to organism function, between dissolved and particulate. Here, as is standard in the field, we use 0.45 µm in diameter as the practically useful boundary between particulate and dissolved. For a greater depth of treatment we recommend the book by Roger Wotten (1990a), The Biology of Particles in Aquatic Systems.

ORGANIC PARTICULATES In terrestrial stream–river systems, large logs can be displaced by bank erosion or beaver activity and eventually carried into the open ocean. In time, these become water logged and sink to the ocean floor, where they continue to be broken down into smaller and smaller pieces. Maser and Sedell (1994) describe this process of mass transfer and degradation of organic materials that encompasses virtually all aquatic environments. The source of a much greater mass of organic particulate and dissolved material is that of wood and leaf fragments that enter streams or lakes as larger particulates, either from soil erosion or simply by being blown in. These fragments are continually reduced through clipping, shredding, masticating, and partial digestion by a host of invertebrates, particularly insect larvae in fresh waters, as they “spiral” through the food webs of freshwater complexes, and finally into estuaries and the sea. Particularly along rocky or coral coasts, algal production adds to the detrital/food-web loops and

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FIGURE 6.2 The movement of particulates (POM) and dissolved organic (DOM) and inorganic (DIM) matter through aquatic systems from the terrestrial realm to the open ocean. Modified after many sources (see especially Kranck, 1984).

the suspended and dissolved supply of particulates. Mud flats and muddy bay bottoms, rich in organic detritus mostly derived from elsewhere, are rich dumps of energy as particulates. A host of invertebrates work these muddy flats and bottoms for their food supply (see Chapter 18).

In larger streams and rivers, as tree shading is reduced and sufficient light reaches the water column, stream banks, and bottoms, phytoplankton populations with zooplankter grazers develop in the water column. In addition, bacterio-algal surface biofilms (epilithon, periphyton, or aufwuchs) begin to form on substrates

Particulates and Aquatic Models

FIGURE 6.3 Relationship of the “microbial loop” to the standard open-water food chain. The reality is far more complex than this diagram. However, it is useful in emphasizing that even at the level of dissolved organics the biochemical energy originally formed in photosynthesis continues to be aggregated and inserted back into the food chain. Dissolved organics in an aquatic ecosystem, wild or modeled, can be an important aspect of function. Modified after Wotten (1990).

(Figure 6.2). Both of these communities can interact with the terrestrially derived organic particulates, degrading them physically and chemically, and can even uptake DOM. Wood and leaf particles are not a high-quality food source. However, as they are worked over, a new and higher quality organic particulate with feces and body parts mixes with the wood and leaf-derived detritus. As the rivers reach estuaries, the flocculating effect of salt ions causes much of the DOM and smaller POM to aggregate into irregular masses and sink to the bottom. At the same time, laterally, sometimes very extensive marshes and mangroves develop that are both trapping river-derived particulates and massively producing woody and leafy detritus of their own. In the extensive tidal channels of marshes and among the prop roots of the mangroves, the same basic organic conversion and cycling occurs as in the rivers that feed the system. Passing out to sea, much of this material is reduced in abundance by sedimentation, incorporation in organisms through the microbial food web (Figure 6.3) of bacteria, ciliates, and plankton, or simple dilution. Further offshore, phyto- and zooplankton come to dominate the organic particulate spectrum.

HUMIC SUBSTANCE Humic substances, in the past called “gelbstoff” or yellow compounds, are the end points of marine,

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freshwater, and soil organic degradation. As polymer compounds, they are highly varying combinations of organic molecules (carbohydrates, amino acids, and fatty acids) and are also highly resistant to further microbial degradation. Terrestrial and freshwater humic substances generally contain recognizable lignin, while marine humic substances do not. Also, marine and terrestrial humic substances differ in isotopic composition, so that it has generally been assumed that terrestrial organics are largely trapped by the estuarine “filter” or at least do not make it across the shelf in any significant proportion (Millero and Sohn, 1992). Although the process is poorly understood, it is widely accepted that humic substances are gradually integrated into sediments and become the kerogen or “oil” of oil shales, probably the largest single reservoir of carbon on Earth. Kerogen, in turn, subject to appropriate geological heating and pressure, is thought to develop into crude petroleum. Kerogen formed in the marine environment is often called algal kerogen. This organic “waste” is largely derived from humic substances originating in phytoplankton production in the ocean, especially along continental shelves and in shallow epicontinental seas.

PARTICULATES AND AQUATIC MODELS Microcosms, mesocosms, and aquarium models have largely ignored the existence of particulates and their relationship to equivalent processes in the wild analogs. Often particulates and unfortunately any plankton, including reproductive states, are removed by a wide variety of filtration processes. Sometimes, particularly in display systems, dissolved organics and humic substances are oxidized or greatly reduced by ozonation or resin column and charcoal treatment. Since very few ecosystems operate exclusively by direct primary production, with degradation up a food web and all particulates exported to another ecosystem (and none imported), an important element of internal recycling is omitted. If bacterial filtration is the reason for the capture of particulates, the filtration system acts like a single large and often very important filter feeder and removes or greatly reduces normal filter-feeding populations and their energy contribution to the model. As Tables 6.1–6.4 demonstrate, many filter feeders are able to extract considerable food value from detritus as well as from dissolved organics. While the food value in leaf and wood fragments and humic (refractory) substances is very low, the food value in mucus, organic films, and some detritus can be as high as that of phytoplankton. As we discussed in Chapter 2, pumps can have a considerable effect on plankters and reproductive

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TABLE 6.1 Assimilation Efficiency (AE) of Freshwater Filter and Deposit Feeders on Organic Particulatesa Taxon Annelida Oligochaete worms

AE (%)

3–6

TABLE 6.3 AE of Freshwater and Marine Shredders Feeding on Organic Materialsa

Food

Particulates in sediments

Insecta Hexagenia Simulium

68 (8) 17–25

Detritus Organic particulates including plankters

Crustacea Cladocera Daphnia Daphnia Ostracoda cypridopsis Ostracoda dolerocypris Ostracoda dolerocypris

(2) 10–30 2–18 50 85 73 27

Detritus Detritus Bacteria Detritus Decomposed blue-greens Decomposed green algae

Taxon

AE (%)

Food

Insecta Pteronarcys

9–16

Detritus

Crustacea Asellus Asellus Gammarus Gammarus Hyalella Hyalella Hyalella Palaeomonetes

23 26–44 10 73–96 22 7–15 14–23 91

Decayed leaves Decomposing leaves Decaying leaves Fungal protein Elm leaf protein Lake sediments Sediment protein Detritus

a

After Wotten (1990b). Reprinted with permission from CRC Press.

a

After Wotton (1990). Note: In this and following tables – repeated citations of a taxon refer to different experimental trials with usually somewhat different results. Reprinted with permission from CRC Press.

TABLE 6.2 AE of Marine Filter and Deposit Feeders on Organic Particulates (Including Dissolved Organics)a Taxon Coelenterata, Gorgonian Coral

AE (%)

Food

22

Coral mucus

Mollusca Geukensia Crassostrea

14

Refractory particulates

1

Refractory particulates

Crustacea Acartia

47

Acartia Mysidium Corophium Echinodermata Stichopus Parastichopus Chordata Pyura

82–92

Mucus and microorganisms Coral mucus Mucus and microorganisms Surface of particles

30

Organic sediments

17 42

Organic sediments Kelp detritus

50 44

a After Wotten (1990b). Reprinted with permission from CRC Press.

stages, drastically altering ecosystem function. While the direct effects of pumping on nonliving or bacterialcoated POM and DOM are probably small, the effect of preventing flocculation (coagulation) and thus the building of organic particulates to a size that is utilizable by many filter feeders is a serious issue for many model ecosystems. Bacterial or algal films (Figure 6.4), in which trapping of particulates is minimal, provide a solution to the need to control water quality and nutrient export in

TABLE 6.4 AE of Freshwater and Marine Browser/Scrapers Feeding on Organic Particulatesa Taxon

AE (%)

Food

Insecta Spaniocerca Pycnocentrodes Helodid beetles

69 18 30–31

Surface organic layer Surface organic layer Surface organic layer

Mollusca Potamopyrgus Potamopyrgus Hydrobia

4 74 5–19

Detritus Surface organic layer Dead green algae

a After Wotten (1990b). Reprinted with permission from CRC Press.

systems of small volume compared to the wild analog. In Chapter 11, we discuss ATS, a process emphasizing primary production that is designed to control nutrients, oxygen, and carbon dioxide/pH without significantly affecting the particulate spectrum. When low-oxygen and low-pH environments are desired, rotating drum units can similarly provide a large bacterial film surface for removing ammonia and DOM. DOM, including humic substances, can probably be controlled for viewing situations, where extreme clarity is necessary, by using ultraviolet light at high oxygen levels. The negative effects of ultraviolet light on plankton can be reduced by limiting application to either a small part of the model or only a small part of the pumped overturn of system volume.

BIOFILMS Bacteria in the environment have generally been regarded as primarily planktonic in nature, free in the water column or attached to organic particulates until those particles are broken down. A newer view regards

Particulates and Aquatic Models

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FIGURE 6.4 The relationship of a river biofilm to dissolved (DOM), colloidal (COM) and particulate (POM) organic matter in the water column. These dynamic interactions apply to all biofilms, to varying degrees, in all ecosystem models. From Lock et al. (1984). Reprinted with permission of Munksgaard International Publishers, Ltd.

bacteria as primarily components of a mini but extremely widespread set of “benthic” ecosystems called biofilms (Harrison et al., 2005). In this latter view, biofilms are diverse communities of bacteria (and protists) in which species are “organized” into consortia to perform different functions in community maintenance, including the releasing of the polysaccharide and protein slime that provides the matrix and protection to the communities. Individual bacterial cells within a biofilm exchange metabolites and even DNA (Figure 6.4). “Reproductive,” free-swimming cells, of bacteria as well as protists, are released into the water column to colonize other surfaces extending the biofilm. In the construction of enclosed marine/aquatic ecosystems, piping and walls add surfaces that do not appear in the wild example or type system. While these surfaces are initially neutral, they soon acquire biofilms. The glass walls of tanks are usually present to provide visibility and are likely constantly cleaned to prevent biofilm formation. However, especially in larger systems, there may well be significant nonglass walls that are not

cleaned. In reef and rocky shore models, this may not matter, and these surfaces can be regarded as additional “bottom” or pore space. However, in many models, these surfaces may well provide a significant biologic/ ecologic presence, with their biofilms, that cannot be ignored. This is also true of the inside surfaces of piping. In general, piping is minimized in the design of any ecosystem model for hydraulic and energy reasons. However, biofilms will form wherever such surfaces exist and these biofilms will capture particulates, organic and inorganic, and become a part of microcosm/aquarium metabolism. Petersen et al. (2003) describing scaling work on mesocosms demonstrate how system volume must be above a certain level so that wall benthic community does not overwhelm a plankton community. However in many systems, the inner surface of piping with its biofilm could easily exceed tank wall surface. If this is to be avoided, piping should be of large diameter and short. In Chapter 25, we discuss a specialized situation of high ammonia loading where biofilms in piping became a very serious issue of water quality control.

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Whether this process is significant or not in any given situation is up to the modeler to determine. In lower-energy environments, even on shallow, well-lighted surfaces that contain photosynthesizing algae, biofilm communities can become very complex autotrophic or subautotrophic ecosystems (Burkholder, 1996). We discuss this issue in many chapters, especially the higher energy variant algal turfs, and the ecologically engineered subset ATS.

Particulate processes in model aquatic systems are poorly understood. We make a plea for more research in this area to test against design concepts. While many of the model systems described in this book have an organic input based on known inputs in wild analogs, none have made a serious effort to develop a reasonable size or quality spectrum for that input.

PARTICULATE IMPORT IN AQUATIC MODELS

In Chapter 3, we discussed the role of inorganic sedimentation in the problems of restoration of damaged aquatic ecosystems. While inorganic and organic sedimentation can occur together, generally the problem of excess organic sedimentation is more likely correlated with excess nutrient loading. These issues we discuss in depth in Chapter 25.

In most ecosystems, particulate import or export to or from external sources (other ecosystems) is normal. It can be at very high levels, as in tidal mud flats, or it may be moderate, as in coral reefs. In a model this provides the opportunity to control organic input by “feeding.” As we discuss in Chapter 20, inputs into coral reef models were based on fine mesh plankton tows upstream (in the trade wind current) of the reef systems in St. Croix, US Virgin Islands. Unfortunately, these tows did not include very fine organic particulates, or DOM, and import to these models at roughly 15% of total organic energy supply may have been low. On the other hand, export from the model systems was in the form of algal filaments from scrubbers (POM in the wild), so DOM was also not exported. Some coral reef microcosms and mesocosms have a faint yellow color at lighting levels less than 5000 K. However, careful microscopic examination has indicated that this coloration is provided by very small suspended algae rather than significant humic substances. The systems that have this coloration are impellor pump-driven units. Even in a situation where waters and organisms are mixed between two separate tanks, one with impellor pumps another with bellows pumps, only the impellor pump unit has the yellow coloration. It is very likely that the impellor pumps select out the small algae by killing off their larger predators and competitors. There is considerable question whether refractory humic substances have any negative effect on system function, though esthetic issues might be of concern. At the Great Barrier Reef Marine Park Authority reef aquarium in Townsville, Australia (see Chapter 20), ozone is used periodically to reduce yellow coloration, solely for esthetic reasons. This is probably having detrimental effects on the microbial and planktonic populations, though no study has been carried out to determine whether ozone is a factor in system function. Large impellor pumps are utilized on this system and since the planktonic microflora and fauna have not been studied, it is quite possible that the coloration observed has the same origin as the systems described above.

AQUATIC ECOSYSTEM RESTORATION

References Adey, W., Luckett, C., and Jensen, K. (1993) Phosphorus removal from natural waters using controlled algal production. Restor. Ecol. 1: 1–11. Boyd, P. W. et al. (2000) A mesoscale phytoplankton bloom in the polar southern ocean stimulated by iron fertilization. Nature 20: 695–702. Burkholder, J. (1996) Interactions of benthic algae with their substrata. In: Algal Ecology, Freshwater Benthic Ecosystems. J.R. Stevenson, M. Bothwell, and R. Lowe (Eds). Academic Press, San Diego, California. Harrison, J. J., Turner, R. J., Margues, L.L.R., and Ceri, H. (2005) Biofilms: a new understanding of these microbial communities is driving a revolution that may transform the science of microbiology. Am. Sci. 93: 508. Johnson, B. D., Kranck, K., and Muschenheim, D. K. (1990) Physicochemical factors in particle aggregation. In: The Biology of Particles in Aquatic Systems. R. S. Wotton (Ed). CRC Press, Boca Raton, Florida. Kranck, K. (1984) The role of flocculation in the filtering of particulate matter in estuaries. In: The Estuary as a Filter. V. Kennedy (Ed). Academic Press, San Diego, California. Lock, M. A., Wallace, R. R., Costerton, J. W., Ventullo, R. M., and Charlton, S. E. (1984) River Apilithon (Biofilm): Toward a Structural Functional Model. Munksgaard International Publishers Ltd., Copenhagen, Denmark. Maser, C. and Sedell, J. (1994) From the Forest to the Sea, the Ecology of Wood in Streams, Rivers, Estuaries and Oceans. St. Lucie Press, Delray Beach, Florida. Millero, F. and Sohn, M. (1992) Chemical Oceanography. CRC Press, Boca Raton, Florida. Peterson, J., Kemp, W. M., Bartleson, R., Boynton, W., Chen, C. C., Cornwell, J., Gardner, R., Hinckle, D., Houde, E., Malone, T., Mowitt, W., Murray, L., Sanford, L., Stevenson, J. C., Sundberg, K., and Suttles, S. (2003) Multiscale experiments in coastal ecology: improving realism and advancing theory. Bioscience 53: 1181–1197. Stumm, W. (1987) Aquatic Surface Chemistry. Wiley, New York. Wotten, R. S. (1990a) The Biology of Particles in Aquatic Systems. CRC Press, Boca Raton, Florida. Wotten, R. S. (1990b) Particulate and dissolved materials as food. In: The Biology of Particles in Aquatic Systems. R. S. Wotten (Ed). CRC Press, Boca Raton, Florida.

P A R T

II BIOCHEMICAL ENVIRONMENT


C H A P T E R

7 Metabolism Respiration, Photosynthesis, and Biological Loading

To maintain a human being or almost any terrestrial mammal or bird, the “hotel” requirements seem relatively simple, at least on the surface. Unfortunately, it is this apparent simplicity that has placed the human race in its present increasingly difficult environmental situation. As long as there were relatively few of us, and our tools and access to the Earth’s great storehouses of short- and long-term “fossil” energy were limited, we took for granted many essentials that the natural ecosystems of the Earth’s surface provided. No longer can we assume that good-quality water and atmosphere will automatically be available or that the products of our daily activities can simply be discarded for “processing” by nature. With our increasing numbers and intense energy use, we are massively changing our planet. With a thorough understanding of organism metabolism at the ecosystem scale, particularly plant metabolism, and the conditions under which solar capture by photosynthesis can be optimized in engineered systems, many of these problems can be solved (Chapter 25). However, with time, if human numbers remain uncontrolled, relative to our large-scale ecosystem management capabilities, our future looks dim indeed. For the hobbyist and scientist the problem of maintaining aquaria, microcosms, and mesocosms is similar on a small scale to the global environmental problem for the environmental restorationist. Several extremely important wild ecosystem-based fisheries have collapsed. We have had a spectacular example in the loss of what was at one time the largest fishery in the world, in the northwest Atlantic. The Atlantic cod fishery is still heavily restricted by the Canadian government 15 years after closure. We can operate aquacultures for a few species, and assuming local aquatic ecosystems

can provide us with a good supply of water, we need to worry only about the temperature, salinity, light, space, and food needs of those few species. But what about good water quality? That is hard to get from most municipally supported taps and many river, lake, and ocean shores these days. When the authors were young, tap water was still mostly drinkable, and, on a hike, one could drink from most streams. Now that is rarely the case, and reverse osmosis (RO) created bottled water is carried by most of us wherever we go. But RO is very expensive at large scale, and many professional production aqua-culturists are increasingly finding themselves in great controversy because of the pollution of natural waters that their intense and massive cultures are producing. In ecosystems, modeled or wild, we do not necessarily want organisms to grow fast, as if we were going to eat them, like a herd of cows in a feedlot or chickens in a coop, but we do want them to behave normally. This is the context in which we have passed more than 99% of our evolution, one in which thousands of species around us behaved “normally” in a mutual environment or biosphere. Water quality is even more important to an aquatic organism than it is to us. When our primary water requirement is for drinking, at least in much of the world we can collect rainwater, use solar stills, or use a variety of filtering and de-ionizing devices. However, the entire bodies of underwater animals are immersed, including their gills and, effectively, their internal vascular or blood transfer systems. So far in this book, we have discussed physical and environmental factors, factors that to a large extent modern humans immediately understand as part of life in an industrial society. Now we approach life in a biochemical context. We also come to a most appropriate

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question that should precede our attempts to re-create or restore living ecosystems based on hundreds of living species. In the introduction to this volume, we asked the question: “How did life originate on planet Earth?” As we discussed, the scientific community is gradually piecing together a “most likely” scenario. However, we did not entertain the question of: “What is life?” A typical dictionary definition would be “a quality that distinguishes a plant or animal from the inanimate such as rocks, earth, or water,” sometimes followed by “especially characterized by reproduction and growth by accreting materials from the surroundings.” To say that something alive is not dead is rather circular reasoning; in any case, many mineral crystals not only reproduce and grow; they often “look alive,” at least in the plant sense. Life, of course, is rich in complex molecules of carbon, hydrogen, and oxygen, but that is also true of the plastics that we now routinely manufacture. Viruses are not alive; they are packets of information that can utilize living cells to make more information. So, what is the state of “alive”? Beginning nearly 40 years ago, the U.S. National Aeronautics and Space Administration began to have this problem when they proposed to find out, as their space probes and landers touched down elsewhere in the solar system, whether life was present. Dr. James Lovelock, the author of Gaia (1979) and The Ages of Gaia (1988), proposed an answer, outlined below, that is still both workable and instructive relative to how we approach life both on Earth and in our mesocosms. In a physical context, the science of thermodynamics tells us that energy is always moving to a lower level of intensity or organization. The disorganization of this energy in the form of the bonding and motion of molecules and atoms (entropy) is always increasing. Thus, in Earth’s time frame, the universe has been running down like a battery, as matter flies out from the big bang. Some billions of years from now this almost inconceivable collection of matter and energy is heading for death close to absolute zero. Perhaps once it has converted all its energy to the gravitational form, it will collapse to another big bang and a rebirth. Our concern here, however, is the running-down process. On the time frame of hours to years rather than a few billion years, life temporarily reverses this apparent process of senescence. It is capable of collecting small amounts of mostly solar energy and chemically organizing, storing, and directing that energy to rather intensive usage. On the scale of the individual, life can literally store and concentrate solar energy, eventually to defy gravity; on the scale of the community, life can store and concentrate energy to be released as heat a few or millions of years later; on the scale of the biosphere, life has been and still is capable of massive alterations of

our planet’s surface. The oxygen-rich atmosphere that allows the rapid time scale of animal life, and has in part given us equitable temperatures for several billion years, the very soil that supports so much terrestrial biomass, and the organic-rich sediments that become an integral part of Earth’s geology (perhaps, as some would have it, even allowing continental drift and the essential features of the Earth’s geology) are all part of the accomplishments of life. These are the unique features of the “living Earth” and probably other living planets scattered through the cosmos. They are contrary to what the physical evolution of the solar system offers when life does not evolve. The ability to reduce entropy and produce highly unlikely levels of organization through energy capture might be the modern physicist’s answer to the nature of the basic entity that we call life. One biologist’s answer seems different (see Mayr, 1988): life is uniquely characterized by information, the information encoded in the genes. If that is so, then a virus is alive, and so is a clay mineral. Also, a cell from which a nucleus has been extracted is already dead, even though it might function as any cell in that state for some time. Perhaps, for now, we should retain the ability to store and process energy definition, recognizing that information from the distant past is required to do this. Several billion years ago life evolved the process of respiration. The information that allows, through energy conversion, the structural and functional elements required to do this has been passed through countless generations of organisms. Every cell in our body has the age-old code for respiration. Hundreds of millions of years ago our distant relatives added another level of respiratory complication. Oxygen and carbon dioxide are exchanged in the lungs from the ambient atmosphere or water to the bloodstream. The blood in turn meets each cell to provide the raw materials for respiration. Every cell in our bodies also “knows” this. Whether a cell acts to “pull its weight” at this level depends on whether it is part of this higherlevel respiratory pathway. Life has what we can call a self-organization capability that occurs at many levels. While we humans may well be very bright as animals go, we still do not fully understand the intricacies of most ecosystems. Yet most of these complex systems preceded us by many millions of years, without the benefit of our brains and powers of organization. Throughout this book we suggest that since we know only vaguely how to internally organize and operate ecosystems in a long-term stable fashion, or even in the short term, we should let those ecosystems be “free” to do what they are more than capable of doing. They “know” because they consist of organisms with information that dates back millions of years,

Metabolism

encoded in their genes. Thus, broadly, but in the context of this book, the modeler or the restorationist should supply the right environment as closely as possible, supply the right genetic material, then sit back and watch or begin the experiment as one’s endeavor directs. It is often necessary, because of the small scale and location of a given mesocosm or wild ecosystem needing restoration, for the human operator to participate to supply energy, to fill the role of missing larger organisms, or to offset patchiness. However, given the right outside parameters (light, temperature, salinity, nutrients, as well as appropriate import and export), the “captured” ecosystem will generally take care of itself. With this statement of philosophy, let us move on to the nitty-gritty of the chapter. A basic understanding of metabolism in living organisms and how it relates to the chemistry of the environment is required to develop a husbandry capability for captured or managed ecosystems, what Adey (2006) called the “operational imperative.” The references will provide the interested reader with a more in-depth treatment of the subject.

METABOLISM Life in the whale, the tree, the alga, or the protist survives by the same very basic process: the chemical “burning” or oxidizing of organic matter (food) at the cellular level. Although it is possible to obtain some energy without oxygen (e.g. by fermentation), cellular respiration using oxygen is the most efficient pathway. The food, a carbon, hydrogen, and oxygen complex, sometimes with nitrogen, phosphorus, sulfur, and minute quantities of other elements, is produced internally (by plants) or is taken from another organism. The energy stored biochemically in the food is directed to the production of chemical compounds that are transferred to specific sites in the cell for release as heat or motion or to the building of structural materials for reproduction or growth. Generally, plants are producers of food and capturers of solar energy. Whether bacteria, algae, or nonvascular or vascular plants, through photosynthesis and acquisition of solar energy, photosynthetic organisms build sugars, starches, and oils. By this means, plants, algae, and photosynthetic bacteria store the captured energy for building the even more complex structural and chemical compounds needed, such as cellulose, lipids, proteins (including the enzymes that drive reactions at biological rates), and the informational nucleic acids. The needs of photosynthetic organisms are great: water, carbon dioxide, nitrogen, phosphorus, and many micronutrients. On the average, growing photosynthetic organisms are also oxygen producers. Photosynthesis

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transfers the energy of sunlight to hydrogen and electrons obtained by the splitting of water and the release of oxygen (see Chapter 5). Thus, in an ecological sense, given light, plants are purifiers: they are constantly removing nutrients, including carbon as carbon dioxide, from their surroundings and adding oxygen. Plants are purifiers in many other ways, such that their use in an environmental sense is now known by the general term phytoremediation. Animals, on the other hand, eat plants or other animals. When they are no longer growing they return all intake materials in reduced form to their environment. Even while growing, food-transfer efficiency is low and therefore a large part of the ingested materials is released to the surroundings for breakdown by bacteria. As long as the delivery rate of animal plus bacterial wastes to the local environment is no faster than the uptake of the plants that require those “wastes,” then a balance is present. An idealized model of animal vs plant requirements is shown in Figure 7.1A. If excess plant production occurs, and direct-feeding animals as well as detritus feeders are not available to consume all of plant production, assuming plenty of water, light, and carbon dioxide from the atmosphere, and some nutrient input, then plant material accumulates. Given the right conditions, as in a swamp, this excess organic material could go into geological storage as coal for tens of thousands to millions of years. As we described in Chapter 6, algal remains, as complex and refractory unreduced organic molecules called humic substances, give rise to the very large quantity of petroleum and kerogen (oil shales) stored in the Earth’s crust. Under natural conditions, excess animals occur only under unusual conditions that do not last long, usually because the food supply runs out or predators arrive to enjoy the excess. In a culture or human-operated environment, as in a human city, where plants do not or cannot balance animals, and food is artificially introduced, something entirely different happens. Here waste products accumulate (carbon dioxide, as well as nitrogenous, phosphorus, and sulfurrich compounds). Bacteria use the excess waste products. However, bacteria, which in most cases metabolically act like miniature animals, when in excess can also radically alter environmental chemistry. In addition, when atmospheric access is slow, in water and muds, for example, oxygen can be used up, creating an anaerobic situation that few higher plants and animals can tolerate. This metabolism, occurring out of environmental context, or organic pollution, is the primary subject of this chapter. The basic picture of metabolism in a generalized plant cell is shown in Figure 7.2. If the segment involving photosynthesis in the lower right is removed, and it

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FIGURE 7.1 (A) Simplified schematic diagram of the movement of essential compounds by organisms in an idealized closed ecosystem. (B) “Unbalanced” community of plants in which excess plant production is being stored (e.g. in sediments). (C) “Unbalanced” community of animals in which food is provided.

is assumed that glucose and basic nitrogen (and other nutrients) are derived from digested food not from the water column, then the diagram also applies to a typical animal cell. Much of the structure of an animal cell is built up from sugars digested from plant or other animal foods. Some amino acids, for protein construction, are derived directly from food; others are synthesized from ammonia derived from the simultaneous bacterial breakdown of food (in a stomach or intestine). In general, the construction or anabolic reactions or steps do not occur at the same site in a cell as the breakdown or catabolic reactions. Also, while most complex

molecules of a cell are stable with time and can even be stored in excess of immediate need, proteins tend to be unstable, constantly breaking down and being replaced by new synthesis.

RESPIRATION Animals come in a wide variety of sizes and complexities. They range from unicellular protozoa (now typically placed in a separate kingdom, the Protista), a fraction of a millimeter long, to elephants and whales

Respiration

107

FIGURE 7.2 Generalized process of metabolism in a living cell. Plant cells normally add the photosynthetic component on the lower right and dispense with the nitrogenous excretory function on the lower left. Modified after Mathews and van Holde (1996). Reprinted with permission of Addison Wesley Longman.

in which tons of complex tissues and multimillions of cells work together. The basic pattern, based on the cell, is the same in all cases. In the more complex animals, individual cells become highly organized parts of tissues and organs specialized in one or a few of the many functions of cells. A generalized animal cell is shown in Figure 7.3. The reader is referred to texts on biology (e.g. Keeton and Gould, 1986) or biochemistry

(Mathews and van Holde, 1996) for a discussion of all cell components. Here we concentrate on the cytoplasm and the mitochondria, because it is in these locales that the basic respiration and glycolysis processes take place. When an animal eats a plant or another animal, a complex digestive process begins. In the stomach and small intestine or their equivalents, digestive acids and

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7. Metabolism

FIGURE 7.3 Idealized animal cell with its multiplicity of internal organelles. After Keeton and Gould (1986). Reprinted by permission of W. W. Norton & Co., Inc.

numerous enzymes break down food particles to their molecular constituents and then the large organic molecules to smaller, simpler molecules. These small molecules can be absorbed through the walls of the intestine and then enter directly into either the blood stream or the lymph system. The blood vessels along the small intestine return directly to the liver where glucose is stored and re-released to manage constant levels in the bloodstream, and amino acids are broken down to

ammonia. The blood stream delivers these basic molecules directly to each cell in the animal body where respiration and the collective anabolic and catabolic processes (as in Figure 7.2) can occur. Within each cell, the basic energy removal is that of the oxidization or “burning” of sugars. Simplistically, this is C6H12O6 ⫹ 6O2 6CO2 ⫹ 6H2O ⫹ 670 kcal/mol of energy: the cell cannot simply burn the sugars. Instead, it uses a small-scale chemical transfer process. Respiration of glucose

Respiration

109

FIGURE 7.4 Simplified diagram showing the process of the complete breakdown of glucose, in respiration, to achieve 36 ATP for energy transfer elsewhere in a cell. After Keeton and Gould (1986). Reprinted by permission of W. W. Norton & Co., Inc.

produces adenosine triphosphate (ATP) and CO2. ATP carries away small packets of energy in chemical bonds (about 1/100 that of an entire glucose molecule) and delivers that energy throughout the cell for many purposes. Figure 7.4 shows a very condensed version of the entire process of breakdown of a simple sugar and conversion of its energy to ATP. Carbon dioxide and water are the by-products. One critical feature to note in this diagram is that some ATP can be produced without oxygen. The amount is small, but this primitive process (glycolysis or fermentation), probably the dominant one in the early eon of life on Earth, allows some organisms

and some tissues within organisms to live in an anaerobic or partially anaerobic environment. When an animal feeds on a plant or another animal, it obtains many organic chemicals more complex than sugars for digestion. Proteins and fats are essential to the animal in many ways, providing vitamins, minerals, and other important compounds. However, much of the protein and fats is also simply digested and respired to produce energy, much as sugars (Figure 7.5). Herein lies a crucial element of the effects of animals on their environment: the production of nitrogenous wastes and, to a lesser extent, phosphorus.

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In more complex organisms, water control and excretion have tended to be joined together. In a sense, the unit of the mammalian kidney, the nephron (Figure 7.8), is an advanced flame cell. Because water loss can be crucial in land animals, the nephron and the kidney came to reabsorb much water, leaving more concentrated nitrogen compounds as urea. In fish, on the other hand, the primary excretory product remains ammonia and, particularly in fresh water, large quantities of water and ammonia are excreted through the kidneys (Bond, 1979). The kidneys are by no means the only site of excretory activity. The liver, in addition to being a digestive organ, excretes waste compounds. Also, the digestive system itself excretes, along with the nondigested wastes of the feces, nonabsorbed nitrogen- and phosphorus-rich compounds that have been broken down both by the animal itself and by bacteria in the gut. In animals with gills, including fish, much ammonia is excreted through the gills, along with carbon dioxide. FIGURE 7.5 Generalized process of breakdown of proteins and fats to achieve introduction of these compounds into the respiration process. After Keeton and Gould (1986). Reprinted by permission of W. W. Norton & Co., Inc.

In many of the tiny protozoans, digestion and excretion can be seen in their basic form. For example, in Figure 7.6, a small plant or animal is shown being captured, engulfed and enclosed in a vacuole (phagocytosis). The golgi apparatus, through the lysosomes, provides digestive enzymes to the food-filled vacuole. After the food is broken down, undigested particles (e.g. a diatom silica wall), along with ammonia and phosphoric acid, are transported to the cell membrane and simply excreted to the exterior of the cell by exocytosis. Sugars, amino acids, and nutrients needed are taken into the cytoplasm through the vacuolar membrane. Also shown in Figure 7.6 is the more general process of recycling of organelles by capture in lysosomes and eventual excretion (B) and even the destruction of a whole cell (D). Pathway (A) refers to the excretion of digestive enzymes to the surroundings, such as would occur in some protists. Early in evolutionary history another process entered into the excretory picture. In any water less than full ocean salinity, outside fresher water continuously moves into the cell by diffusion. The resulting cell dilution is called osmosis, and it often results in a pressurized internal environment. To avoid dilution of the cell to the point of death, some vacuoles (contractile) function to collect this water, eventually expelling it to the exterior. A more advanced form of this process, including a specialized cell, the flame cell, is seen in the simple planarian (Figure 7.7).

BACTERIAL METABOLISM Bacteria are neither plants nor animals and today are placed in a separate kingdom called the Monera. Some bacteria (including the very important cyanobacteria or blue-green algae) are capable of photosynthesis, thereby acting like plants. Most bacteria act like animals and break down dead organisms or are predators acting as parasites in living organisms. Bacteria are very simple cells, filaments, and colonies. They lack a nucleus and other cellular organelles enabling them to carry out the complex cellular digestive/excretion process we discussed above. Bacteria excrete their digestive enzymes into their surroundings and absorb through their cell membranes the simple sugars and reduced nitrogenous and phosphorous compounds that they require. Nitrogenous and other wastes develop at least partly external to the cell. In a sense, when bacteria are abundant, because dead organic material is abundant, the external environment locally becomes like that of the stomach or small intestine. We discuss this in depth later, but excess dead organic material free in a relatively closed space provides an environment like a stomach: acid, rich in carbon dioxide, methane, and ammonia, devoid or nearly devoid of oxygen, and having many enzymes capable of organic breakdown. This is a specialized environment, which in the open world could be the subsurface of an organic-rich mud flat; however, it is not one that many higher organisms can tolerate. It is also an unsatisfactory environment for the open water of most aquaria, microcosms, and many wild ecosystems. And now we briefly return to Figure 7.1 and the basic ecological point of this chapter. Animals and

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FIGURE 7.6 Digestion of food by idealized protozoan cell. After Mathew and van Holde (1996). Reprinted by permission of W. W. Norton & Co., Inc.

most bacteria require complex organic foods, plants, and other animals, dead or alive. The principal requirement is simple sugars for energy. While a small amount of vitamins, amino acids from protein, and many other micronutrients are required, only a small part of the nitrogen, phosphorus, and sulfur in complex compounds is needed. The rest becomes organic waste, some of which is toxic, when concentrated in quantity, to many organisms. On the other hand, these wastes are required by living, photosynthesizing, and growing plants and algae to build their tissues. In a balanced system and in most natural ecosystems, organic wastes do not accumulate; they are used as fast as they are

produced. In the more-or-less restricted localities where wastes do accumulate, in some cases entering into geological storage, they create a special environment in which a few specialized organisms are capable of functioning. The biosphere/lithosphere combination has the means of storing the components of excess organic production – organic-rich sediments and eventually coal and oil, for example. The same basic storage equivalent can be accomplished in a mesocosm, and, with a little more difficulty, in the aquarium. When one is dealing with restoration of an aquatic ecosystem that is receiving excess anthropogenic waste products, the storage option may not be possible without changing

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the entire character of the ecosystem. However, as we discuss in Chapter 25, prevention of organic import may be possible.

PHOTOSYNTHESIS

FIGURE 7.7 Planaria flame cell. A cell specialized for water regulation – a primitive kidney. Keeton and Gould (1986). Reprinted by permission of W. W. Norton & Co., Inc.

FIGURE 7.8 Diagram of the principal cellular element of the human kidney. After Keeton and Gould (1986). Reprinted by permission of W. W. Norton & Co., Inc.

Nearly all the organic energy stored in the Earth’s crust and held as biomass in the biosphere, as well as that used by humans since they have evolved, has been solar energy, captured in the process of photosynthesis. Most of this solar energy has been captured within the chloroplasts of plant cells (Figure 7.9). Nuclear energy remains a miniscule portion of energy used by humans and is likely to also remain problematic. In Chapter 5, we discussed how that energy capture occurs and how, through oxygen release, the process has changed the surface of the Earth, making life possible for more than just microbes. The light reactions of photosynthesis are highly efficient and produce energized electrons and hydrogen ions that end up energizing two transport compounds ATP and NADPH⫹. However, this is just the beginning – the chemical energy built into these compounds has to be efficiently stored and used to build more complex organic compounds and cell structure, plant and eventually animal bodies or it will quickly be lost as heat to the environment. Early in the development of the biosphere, roughly from 2.5 to 3.5 billion years ago, a number of chemical pathways evolved that would allow the anaerobic bacteria of the time to use the energy of ATP, NADPH⫹, and perhaps other energy carriers, to capture, or fix, CO2 (or possibly –HCO3 in some cases) and build organic compounds (Raymond, 2005). Some of these ancient pathways still exist in more or less rare, anaerobic bacteria. However, at about 2.5 billion years ago, cyanobacteria evolved the Calvin cycle (see Heldt, 2005 and Figure 7.10). Probably by symbiotic “capture” of cyanobacteria cells by protists, this has been passed on to all algae and eventually to higher plants. The basic Calvin cycle produces fructose and other sugars in the stroma of chloroplasts (see Figure 5.2), and these sugars, mostly translocated throughout the cells or to other cells in tissues, become the building blocks for more complex compounds. The uptake of CO2 in the Calvin cycle, as shown in Figure 7.10, is catalyzed by the highly abundant but very inefficient enzyme Rubisco. Much as in animal cells, the energy-rich sugars produced by plant cells are respired as needed to produce ATP. The ATP-stored energy derived from photosynthesis is then transferred throughout the cell and used to build walls (cellulose), nucleic acids, proteins, phospholipids (on cell membranes), and more chlorophyll, to name a few. All of these are needed as cells grow and

Photosynthesis

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FIGURE 7.9

Idealized plant cell. To compare essential similarities and differences to an animal cell see Figure 7.3. After Keeton and Gould (1986). Reprinted by permission of W. W. Norton & Co., Inc.

divide. These building processes result in a need for nitrogen, phosphorus, sulfur, and other micronutrients, which are primarily taken up as dissolved salts (phosphate, nitrate, sulfate, etc.). Ammonia, at least in small concentrations, is a preferred source of nitrogen. Often, especially in algae and aquatic plants, higher forms of the most essential requirements, such as urea, can also be taken up. In the aquatic environment removal of these compounds by plants can be crucial, as, in abundance, they are toxic to most animals. If

these compounds are left for bacteria degradation, the result will be lower water quality, perhaps even an anaerobic environment. Plant cells also respire, much as animal cells, and at night generally require oxygen and release carbon dioxide. In some cases, both in the wild and in closed ecosystems, the combination of animal and bacterial respiration in the dark can be crucial to ecosystem function. The practical aspects of this situation are discussed in Chapter 8.

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FIGURE 7.10

Movement of photosynthetic productions in a typical plant cell, including most marine and aquatic plants (C3). After Mathews and van Holde (1996). Reprinted by permission of Addison Wesley Longman. Note that in most algae (other than green algae) the storage products are often not starch, but a wide variety of oils, alcohols, and starch-like compounds.

BIOLOGICAL LOADING As must be very clear from the above discussion, living organisms can radically change the chemistry of their surroundings. From the study of geology and atmospheric chemistry, we know that global-scale changes have been introduced over billions of years by living organisms. In shorter time frames, the same effects are very obvious during a red tide, or near an odiferous mud flat, and become particularly noticeable when one “walls off” a piece of that environment. When scale modeling a living ecosystem, the buffer effect of the larger surroundings is gone and one loses the normal dynamic balances that result from community-level patchiness in the larger ecosystem. Biological loading is the term that we use to describe the effects of the organisms present on the physical and chemical environment. In a simulation system, biological loading can be classified in two general categories: chemical exchange and its requirements, discussed in this chapter and the remainder of Part II, and behavioral requirements and interactions, discussed in Part III. While there is some connection between the two, they are largely independent of each other. Metabolism refers to the complex of chemical reactions that occur inside a living organism. Respiration refers specifically to the basic energy-exchange mechanisms that involve the use of oxygen to “burn” (chemically) the appropriate organic matter to provide energy

for all the various elements of organic function. Carbon dioxide is produced by this process, and a typical measure of respiration is O2 use or CO2 production. Most important in this context is that the use or production of O2 and the use or production of CO2 are among the most critical and obvious ways in which marine or aquatic organisms change the chemistry of their surroundings and the most immediate factors to be dealt with in an enclosed system. In a closed ecosystem, the respiration process is basically no different than that in the wild community, but several factors have to be kept in mind. For example, a high-biomass (and high-metabolic-rate) rocky-bottom community typically relies on constant movement of water from the overlying or off-lying water mass, often a planktonic community, which normally has much lower loading effects. The community in a tank might very well be functioning exactly as in the wild and yet not have sufficient oxygen to survive at night because of lack of contact with the equivalent larger adjacent body of water. Indeed, this basic situation happens naturally in the wild in a mud-flat environment where the oxygen needs of the community as a whole cannot be met because of inadequate oxygen-exchange mechanisms for the large metabolic requirement. A mud-flat community is adapted to this situation. A rich rockybottom community would probably not survive, either in the tank or in the wild, if this need is not met. There are many other metabolic effects of marine and aquatic organisms that lead to changes, buildups, or exhaustion, of elements or compounds in the water in which they live. Chief among these are the variety of compounds that result from nitrogen metabolism. The primary problem in this case is the excretion of ammonia and related products, toxic compounds in large quantity, that results from the constant breakdown of proteins in animal cells and by some bacteria. In a broadly considered wild marine ecosystem, ammonia is very much needed by the photosynthetic organisms, whether phytoplankton, algae, or higher plants that inhabit the community. Thus, it should never be a critically toxic element either in the wild or in a microcosm. However, in both cases potential imbalances exist. On an organic-rich muddy bottom, animal biomass often greatly exceeds plant biomass, which in deeper waters could be totally absent. While bacteria may then take over the role of plants in taking up and utilizing ammonia, the levels of ammonia present are likely to be much higher than those in a community frequented by plants. Thus, in aquarium science, when a bacterial filter is used to break down ammonia, not only is more oxygen used, but the ammonia concentrations are likely to be considerably higher than they would be in a plant-rich

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References

community like a shallow-water coral reef or a rocky shore. Also, dilution plays a major role in potentially transferring toxic ammonia from an animal-rich site of production to a broad area of dilute but more than sufficient plant production. There are many other ways in which use of a bacterial filter can negatively affect many marine organisms and communities, and that relates to a tendency in aquarium science to turn to other methodologies, especially foam fractionation. The same problem applies to wild communities, especially streams, lakes, and bays with large adjacent human communities. Sewage plants are nothing but large bacterial filters, and large bodies of water can be destroyed by the illconsidered use of these systems (e.g. Chesapeake Bay). In some cases, use of a foam fractionator can remove excreted particulates and even large molecules, but they cannot remove ammonia and CO2 already formed and, in addition, remove the plankton and reproductive stages that are key elements of most aquatic ecosystems. Trickle filters, basically water trickling over abundant surfaces with bacterial biofilms, are a great improvement over the more traditional bacterial filters in that atmosphere exchange is greatly improved; however, the same basic problems remain. These matters are discussed in detail in Chapter 9. The basic concept under discussion here can be extended to carbonate metabolism, silica metabolism, and all of the potential water chemistry-altering activities of organisms. When one is considering microcosm or mesocosm simulation of a community, the question should be asked: “How does the wild community in question avoid the problems created by metabolic imbalances?” If they are solved within the community on a daily as well as hourly basis, then faithful reproduction of environment and community in microcosm will produce the same result. However, if the problem of metabolic imbalance in a wild situation is solved by interaction with another community, or effectively by dilution, then either the alternate community or the dilution must be supplied or its effects simulated. Another aspect of biological loading is long- or short-term storage of organism tissues or organic materials derived from those tissues. Some entire ecosystems, such as bogs, are accumulating storage biomass. In these situations, some high-level organic compounds that could be available to organisms are not being used for a variety of reasons. Fossil fuels derive from long-dead ecosystems that functioned in this manner. Other biological communities, such as reef lagoons, mud flats, and temperate forests are characterized by the accumulation of organic detritus in part of the system (e.g. the soil or lagoonal sediment), where it is gradually used by organisms specialized to the environment. A coral reef system stores very little

of its organic production in the reef itself, and there is major loss of plant fragments to lagoons by most reefs. This potential organic loss to a reef is partially made up for by the capturing of zooplankton swept in by currents from the open ocean. Such mass balances need to be carefully considered in microcosm work. For example, in a coral reef microcosm, if 1 g of dried shrimp is fed to the system each day to simulate the planktonic input from the open ocean in the wild, then more than 1 g (dry) of algae or other organics must also be removed from the tank. This may not necessarily be carried out daily or even weekly – the import/export schedule is a function of how much imbalance a system will normally take. There are several ways in which this can be done, as we discuss in depth later: 1. weeding of macroalgae; 2. sediment settling traps that include organic particulates and foam fractionators that remove those particulates as well as large molecules of dissolved organics (see Chapter 3); 3. removal of larger organisms that have grown in the systems (fish, invertebrates); or 4. the use of an algal turf scrubber (Chapter 10). It is also possible to scrape the diatoms or other algae that grow on the walls of the microcosm or aquarium, and to mechanically filter out those scrapings for a short period. However, a major part of the algae removed tends to be diatoms, and the net result after periods of several months can be silica depletion. While this might not be undesirable in some cases, generally it results in considerably reduced numbers of both planktonic and benthic diatoms. In the next three chapters we discuss the primary chemical problems of biological loading, respiration, and nitrogen metabolism, and the generalized means of simulating the required adjacent ecosystem effects. In Chapters 20–23, in discussing the major types of microcosms and mesocosms on which we have worked, other generally less crucial aspects of biological loading are considered further. Finally, in Chapters 24 and 25, we discuss the landscape and global implications of human loading on wild ecosystems and the biosphere, and discuss large-scale methods for dealing with those problems.

References Adey, W. (2006) Lessons learned in the construction and operation of coral reef microcosms and mesocosms. Chapter 17 in: Coral Reef Restoration. Handbook. W. Precht (Ed.). Taylor and Francis Group CRC Press, BocaRaton. Bond, C. E. (1979) The Biology of Fishes. Saunders, Philadelphia.

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Heldt, H.-W. (2005) Plant Biochemistry, 3rd edn. Elsevier, Amsterdam. Keeton, W. T. and Gould, J. L. (1986) Biological Science, 4th edn. Norton, New York. Lovelock, J. (1979) Gaia: A New Look at Life on Earth. Oxford University Press, Oxford. Lovelock, J. (1988) The Ages of Gaia: A Biography of Our Living Earth. Norton, New York.

Mathews, C. and van Holde, K. (1996) Biochemistry. Benjamin/ Cummings, Menlo Park, California. Mayr, E. (1988) Toward a New Philosophy of Biology. Harvard University Press, Cambridge, Massachusets. Raymond, J. (2005) The evolution of biological carbon and nitrogen cycling – a genomic perspective. Rev. Miner. Geochem. 59: 211–231.

C H A P T E R

8 Organisms and Gas Exchange Oxygen, Carbon Dioxide, pH, and Alkalinity

The metabolism of living organisms affects water chemistry in two basic ways: (1) gas exchange (mostly oxygen and carbon dioxide) and (2) exchange of dissolved nutrients (nitrogen, phosphorus, and a variety of micronutrients). However, animals also release undigested food in the form of feces and plants lose or detach parts, which relative to the environment are dead organic materials undergoing further breakdown primarily by microbes. They also excrete organic compounds such as ammonia and urea that undergo further microbe degradation. All of these processes ultimately use oxygen, release carbon dioxide, and produce nutrients. In this chapter and Chapter 9, we discuss gas and nutrient exchange, respectively. In Chapter 10, we examine the issue of biomineralization, the formation of bone and shell, and particularly the crucial subject of calcium carbonate formation by organisms. Calcification is important to the entire biosphere, as well as to many ecosystems and thousands of abundant species, and is inextricably linked to carbon dioxide and its reaction with water. For perspective, we briefly discuss selected wild aquatic and marine environments followed by examples from a variety of captured ecosystems. In Chapter 11, we examine methods of controlling gas, nutrient exchange, and calcification in microcosms, mesocosms, and aquaria. In these model ecosystems, control or compensation is needed because of the small size of the system in a day–night cycle, the presence of an unnaturally large biomass, or the lack of compensating larger adjacent body of water. Finally, in Chapter 25, we show how these same methodologies, at landscape and even global scale, can lead to the repair of ecosystems damaged by human organic overloading. Gases from the atmosphere diffuse into and out of any water body that the atmosphere contacts. If the

water body lacks organisms and organic materials, an equilibrium or saturation is established that is a function of temperature, salinity, and pressure. Nitrogen is the most abundant gas in the Earth’s atmosphere. However, while it is abundantly present as a dissolved gas in water, it is largely inert (as a gas) and is little affected by biological activity. We discuss nitrogen fixation and denitrification (exchange from the gaseous state to the organic or dissolved state and the reverse) in Chapter 9. Here, our concerns are primarily for the next most abundant atmospheric gases, oxygen and carbon dioxide. The concentration of these gases is radically and constantly altered by organic activity in aquatic and marine environments. The carbon dioxide of the Earth’s Northern Hemisphere atmosphere varies seasonally due to the activity of plants (about 5 of almost 380 ppm today, it was 320 in 1965). Indeed, so great is the potential for exchange of these gases by biological activity that the Earth’s atmosphere has been drastically changed (over billions of years) primarily by plants. In addition, a considerable percentage of the rock on the Earth’s surface is limestone or marble (primarily CaCO3), ultimately derived from carbon dioxide through the shell-creating or environment-changing activities of plants and animals. Other rocks, such as shales (derived from muds), can also be very rich in organic carbon derived from the bodies of ancient organisms. Tables 8.1 and 8.2 give the saturation values, that is, concentration at equilibrium, for oxygen and carbon dioxide, respectively, at different temperatures and salinities. These values apply to surface waters, and, for “nonliving” waters, they are good reference points. However, they hardly ever occur in nature because of the constant exchange activities of organisms. In aquatic and marine ecosystems oxygen is generally the

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TABLE 8.1 Saturation Levels of Oxygen Gas Dissolved in Water as a Function of Salinity and Temperaturea Salinity (ppt) Temp. (°C) 0

5

10

15

20

25

30

35

40

5 10 15 20 25 30

14.4 12.6 10.0 9.1 8.3 7.6

13.9 12.2 9.7 8.8 8.0 7.4

13.5 11.8 9.4 8.6 7.8 7.2

13.0 11.4 9.2 8.4 7.6 7.0

12.5 11.0 8.9 8.1 7.4 6.8

12.1 10.6 8.6 7.9 7.2 6.6

11.6 10.2 8.3 7.6 6.9 6.4

11.2 9.8 8.1 7.4 6.7 6.2

14.8 13.0 10.3 9.4 8.5 7.8

a Recalculated from data of Home (1969). Reprinted by permission of John Wiley & Sons, Inc. Values given as mg/liter.

TABLE 8.2 Solubility of Carbon Dioxide in Water as a Function of Salinity and Temperaturea Salinity (ppt) Temp. (°C) 0

5

10

15

20

25

30

35

40

0 6 12 18 24 30

3.31 2.65 2.16 1.80 1.51 1.29

3.22 2.59 2.11 1.75 1.52 1.27

3.15 2.52 2.07 1.72 1.45 1.25

3.07 2.46 2.02 1.67 1.42 1.22

2.99 2.39 1.97 1.64 1.39 1.20

2.90 2.34 1.93 1.60 1.36 1.17

2.83 2.28 1.88 1.57 1.33 1.15

2.75 2.21 1.83 1.53 1.30 1.13

3.39 2.72 2.21 1.83 1.54 1.32

a Recalculated from data of Richards (1965). Values given as g/liter. Note that oxygen (in Table 8.1) is given in mg/liter. Effectively, the solubility of CO2 is hundreds of times greater than that of O2.

most important and straightforward of the two gases. Carbon dioxide reacts with water to form carbonic acid and its ionic forms. It is also involved with both inorganic and organic calcification. We discuss carbon dioxide second. Note that in a water body not significantly affected by the activity of organisms, much more carbon dioxide will be dissolved (including its ionic forms) than oxygen.

OXYGEN EXCHANGE The vast majority of organisms, animals and plants, living on the surface of the Earth and within its waters require an oxygenated environment. While plants produce oxygen, often in great overabundance (to their immediate needs), photosynthesis requires light, which is rarely continuous. Most algae and higher plants cannot store oxygen and must remove some from their environment at night (even if they produced a great overabundance during the day). More complex plants,

such as many submerged aquatic plants and mangroves, are adapted to living on oxygen-deficient soils or substrates and have spaces within their tissues for the storage and transport of oxygen. Nevertheless, an oxygenated water column or atmosphere is required. Some animals and plants can temporarily use nonoxygen-requiring metabolic pathways to derive energy from food. These pathways can be utilized in low-oxygen environments or to carry out “extra” metabolism (e.g. the emergency heavy use of muscles) over and above oxygen transport capabilities. Such pathways are, however, much less efficient than those using oxygen. Unicells, or simple filaments, such as bacteria, protozoa, and fungi, take up oxygen directly from the environment through their cell membranes. Multicellular aquatic animals have evolved a variety of organs called gills to remove oxygen from the water column. They have also evolved a number of blood pigments to carry oxygen in the bloodstream (Table 8.3) so that cells situated deep inside their bodies receive oxygen. In general, it is the microbes, bacteria, yeasts, and some fungi, protozoans, and certain parasites that are adapted to the anaerobic environment. A number of alternate energy, “chemosynthetic,” and nonoxygen-using carbohydrate breakdown pathways exist. Some produce compounds like hydrogen sulfide, which are quite poisonous to most animals. Many organisms are adapted to aqueous environments in which anaerobic sediments are overlain by oxygen-rich water or the atmosphere. However, where oxygen depletion is permanent and extends up into the water column, along with the concomitant H2S, the environment becomes largely “dead” except for anaerobic microbes. This can happen on a very large scale, such as in the Black Sea where deep waters are isolated by the shallow sill at the Bosporus and the rain of organic material to deep water exceeds the diffusion and current transport requirements for oxygen. Unfortunately, today such oxygen depletion is also happening in many lakes, bays, and even coastal waters, ultimately due to human eutrophication. In the surface waters of the open ocean, oxygen is generally supersaturated (Figure 8.1). While extensive surface exchange (wave action) under conditions of low biomass would not allow a large negative difference from saturation values, either seasonally or diurnally, excess plant biomass and photosynthesis in the welllighted zones tend to keep ocean surface waters above saturation levels. The ocean is a major original and continuing source of oxygen to the atmosphere. It can be argued that before humans evolved and utilized oxygen in the burning of forests and fossil fuels, maximum atmospheric oxygen levels had been attained. The use of fire in hunting by Stone Age humans probably already

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TABLE 8.3 Respiratory (Oxygen-Carrying) Pigments in the Animal Kingdoma Hemocyanin: Copper-containing protein, carried in solution. Molecular weight ⫽ 300 000–9 000 000 Mollusks: Chitons, cephalopods, prosobranch, and pulmonate gastropods: not in lamellibranchs. Arthropods: Malacostraca (sole pigment in these): Arachnomorpha: Limulus, Euscorpius Hemerythrin: Iron-containing protein, always in cells, nonporphyrin structure. Molecular weight ⫽ 108 000 Sipunculids: All species examined Polychaetes: Magelona Priapulids: Halicryptus, Priapulus Brachiopods: Lingula Chlorocruorin: Iron-porphyrin protein, carried in solution. Molecular weight ⫽ 2 750 000 Restricted to four families of Polychaetes: Sabellidae, Serpulidae, Chlorhaemidae, Ampharetidae Prosthetic group alone has been found in starfishes, Luidia and Astropecten

FIGURE 8.1 Oxygen saturation levels of the surface waters of the South Atlantic Ocean. After Richards (1965).

Hemoglobin: Most extensively distributed pigment; ironporphyrin protein, carried in solution or in cells. Molecular weight ⫽ 17 000–3 000 000 Vertebrates: Almost all, except leptocephalus larvae and some Antarctic fishes (Chaenichtys, etc.). Echinoderms: Sea cucumbers Mollusks: Planorbis, Pismo clam (Tivella) Arthropods: Insects Chironomus, Gastrophilus. Crustacea Daphnia, Artemis Annelids: Lumbricus, Tubifex, Spirorbis (some species have hemoglobin, some chlorocruorin, others no blood pigment). Serpula, both hemoglobin and chlorocruorin. Nematodes: Ascaris Flatworms: Parasitic trematodes Protozoa: Paramecium, Tetrahymena Plants: Yeast, Neurospora, root nodules of leguminous plants (clover, alfalfa) a

After Schmidt-Nielsen (1975).

significantly lowered oxygen concentration and raised that of carbon dioxide. The domination of Australian forests by eucalyptus and the abundance of parklike grasslands and sedge lands in place of the previously dominant Nothofagus and Araucaria forests were probably caused by the aborigines’ burning activities (Flood, 1983). Atmospheric oxygen levels prior to human influence were in part limited by the natural combustion levels of forests. In short, “the world is (or at least was) green.” Plants probably have the capability to raise atmospheric oxygen concentrations higher than they are, perhaps to 22%. The potential for subspontaneous combustion of forests on land, the release and oxidation of methane from anaerobic deposits, and perhaps the reduction of carbon dioxide to the point where photosynthesis becomes very slow set the limit to atmospheric oxygen levels (see Lovelock, 1979). Although there is much debate on the subject, low CO2 levels could also

FIGURE 8.2 Dissolved oxygen levels in the sea (in ml/liter). After Dietrich (1963).

trigger glacial periods (reverse global warming) and set another kind of limit on photosynthesis. In somewhat deeper water (100–700 meters) in the open ocean, oxygen levels reach their minimum (Figure 8.2). This is below the lighted or photic zone of plant activity. It is also a level at which the rain of algal and animal waste material from the surface provides relatively high animal and bacterial activity. Finally, in the lower half of the deep ocean, oxygen concentrations return to near-surface values. These deep waters are cold and largely derived by deep currents from Arctic and Antarctic zones. At their high-latitude sites of origination, oxygen saturation levels were initially high. Also, at

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cold temperatures plant photosynthesis is relatively more efficient than either plant or animal respiration. Open coastal waters are similar to the open ocean, though fluctuations are greater. Lakes and rivers tend to operate under similar oxygen distributions but, on the average, show a shift to lower oxygen levels. This situation derives from the addition of terrestrial organic matter from the surrounding watershed. There are almost as many oxygen distribution and exchange patterns as there are lakes. For more detail see Chapter 2 and the extensive discussion by Hutchinson (1957) and Dodds (2002). In summary, oxygen concentrations in the surface waters of most lakes are near saturation levels. Relatively clear, unproductive lakes in which a more ordered organic and oxygen exchange occurs can average supersaturated levels of oxygen at the surface and moderate oxygen levels at depth. At the other extreme, in eutrophic or nutrient-rich lakes, variations in oxygen concentration can be very large. Under the right conditions in the spring or summer, such lakes bloom with intensive plant growth. In these cases, oxygen supersaturations of 50% or more are eventually followed by a “crash” in oxygen levels by late summer. Such eutrophic lakes build up biomass to the point where oxygen diffusion at night is not sufficient to prevent anaerobic conditions resulting from the very large oxygen requirements. Extensive fish kills often result. Unlike the oceans, lakes, and rivers acquire significant organic loads from the terrestrial environment. Where depths extend well below the photic zone, mean oxygen deficits can exist, and a lake will use more oxygen than it produces or can diffuse through its surface. Estuaries lie between lakes and rivers and the ocean with regard to mean oxygen concentration and can be more like one or the other depending on the nature of the organic and nutrient input of the fresh waters and the amount of exchange with the ocean. In lakes, rivers, and estuaries, organic and nutrient inputs by humans are crucial to oxygen levels and organic stability. Indeed, oxygen depletion often becomes the most essential element of human degradation of aquatic environments – more on this below. Mesocosms and aquaria are similar. Photosynthesis and respiration are often summed up as CO2 + H2O + energy (light/chemical) ⫽ CH2O + O2. Ecologically, this implies a balance in which all energyrich organic compounds created by the photosynthesis of plants are either metabolized by the plants themselves or metabolized by animals through a food chain. However, this is not the case. Much plant and some animal organic material goes into geological storage, eventually becoming peat, organic-rich shale, coal, gas, and oil. It is estimated that over 14 000 times as much organic material and other carbon of organic origin lies in geological storage as presently exists in the biosphere as

biomass (Stumm and Morgan, 1981). Also, in oxygenpoor environments, glycolysis and fermentation result in the partial breakdown of plant-produced organics without the use of oxygen. This is how oxygen derived from the photosynthetic splitting of molecular water has gradually built up to high levels in the atmosphere. Even if the Earth has now reached a balance (independent of humans) in oxygen production, and levels are no longer building up in the atmosphere, the excess oxygen required by methane, coal, and oil as they are exhumed on the surface of the Earth is not generally recycled by organisms in aquatic environments. Thus, most natural water ecosystems not made eutrophic by humans, particularly shallow-water environments, will tend to be supersaturated or at least rich in oxygen.

OXYGEN, MODEL ECOSYSTEMS, AND ECOSYSTEM RESTORATION In microcosms and mesocosms where one is attempting to simulate all aspects of a particular environment and ecosystem, presumably one provides enough light and the appropriate plant community to simulate wild levels of photosynthesis. If diurnal and season oxygen measurements show oxygen levels below those in the natural community then there is a serious problem that should be corrected. This is often the simplest proxy measurement for the overall model veracity. Assuming that community structure is more or less correct and photosynthetic plant biomass and animal biomass are properly balanced, a problem of low oxygen levels is likely to be caused either by inadequate light or by a failure to simulate water flow from areas of higher oxygen concentration, particularly at night. The first problem was discussed in depth in Chapter 5. We discuss the solution to the second problem in Chapter 11. In microcosms and mesocosms, even if the builder and operator are attempting to maximize equivalences between the wild environment and the aquarium, scaling and inadequate ratios of water surface to water volume can provide great difficulties relative to oxygen concentration. In the aquarium, where display is a primary function and volume is small, animal biomass is likely to be higher than normal, particularly for the marine environment. Also, artificial feeding in excess of wild equivalents is almost invariably provided to an aquarium. Thus, except for the relatively unusual environments normally low in oxygen that one might try to model, it is difficult to simulate a proper oxygen environment by simple aeration. While trickle filters and foam fractionaters may improve oxygen exchange, without using bottled oxygen, they cannot achieve the supersaturation of wild systems.

Carbon Dioxide Exchange

Many lakes and ponds have become hypoxic or anaerobic and unaesthetic and useless for recreation due to nutrient overloading by sewage plant outfalls, farm runoff and runoff from urban/suburban development (Livingston, 2006). This widespread problem has expanded and moved downstream, so that in recent decades one of the largest estuaries in the world (Chesapeake Bay – Blankenship, 2005) and even coastal areas (Gulf of Mexico – USGS, 2005) have developed large “dead” (anaerobic) areas during the summer. In a case of minimum overload (e.g. a pond with human-fed ducks), a water fountain aerator might temporarily solve the problem. Restoration of these large-scale environments can be accomplished, and we discuss the oxygenation and denitrification methodology in Chapter 25.

CARBON DIOXIDE EXCHANGE The other major gas involved in exchange between organisms and their environment is carbon dioxide. The activity of CO2 is, in a sense, the inverse of oxygen, the two being primarily cross-exchanged between plants and animals (Figure 8.3). However, it is also very different from oxygen in that it reacts chemically with water. Also, CO2 is intimately bound to calcification or shell and wall formation in many organisms (bacteria, protists, plants, and animals) and to the chemical precipitation of limestones. Photosynthesis and calcification by organisms are intimately linked through carbon/carbonate chemistry (McConnaughey, 1994; Small and Adey, 2001). In synergistic fashion the two processes enhance each other and have thus given rise to many animals/algal symbioses in the ocean. Unlike oxygen, relative to respiration, the lack of carbon dioxide in special terrestrial and aquatic environments (including greenhouses) may slow

FIGURE 8.3 Chemical and biological movement of carbon dioxide in aquatic and marine ecosystems. After Horne (1969). Reprinted by permission of John Wiley & Sons, Inc.

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down photosynthesis to some degree. However, in most aquatic and virtually all marine environments there is usually a very large supply of this essential compound (as bicarbonate ion, HCO⫺ 3 ) available for all biological activity. On the other hand, excess carbon dioxide tends to increase the acidity of an environment and renders the calcification requirements of an organism more difficult. As shown in Figures 8.3 and 8.4, the proportion of the primary components of the carbonate system (carbon dioxide, bicarbonate, and carbonate and hydrogen ion, pH) present in any given water mass is a function of the interaction of several chemical equilibria dependent on temperature, salinity, and pressure. The status of the entire system under any given set of conditions can be determined by measuring any of two of the following components: pH, total alkalinity, total CO2 (CO32⫺ + HCO3⫺ + CO2), and the partial pressure of CO2 (e.g. Millero and Sohn, 1992). In practice, this is usually done by measuring pH and total alkalinity. Total alkalinity for sea water consists of bicarbonate (HCO⫺3, approximately 89%), carbonate (CO32⫺, approximately 6.7%), borate (B(OH)4, 2.9%), and several minor components (including OH⫺) adding up to less than 0.5%. In most mesocosm work, where great precision is not needed, inexpensive analytical kits are available to measure total alkalinity or carbonate alkalinity. However, pH should be measured with high-quality probes and meters using high-quality buffers for standardization. Calculating the expected changes in the carbonate system of any body of water can be done using the equations discussed in depth by Millero and Sohn (1992). In field work on coral reefs, for example, alkalinity depletion from ocean water pouring over a reef has been used repeatedly to determine rates of community calcification. In practice, in mesocosm and aquarium work, Figure 8.4 can be used to estimate magnitude and direction of change due to biotic effects, and actual measurements of pH and alkalinity can be taken to verify the expected changes. With some minor modification, the nomographs for evaluating bicarbonate and carbonate alkalinity and carbon dioxide given in the seventeenth edition of Standard Methods for the Examination of Water and Wastewater (Cleseri et al., 1989) can be used to quickly and precisely evaluate the status of the carbonate system in both wild and captured systems. Note that while removing carbon dioxide through photosynthesis, in a closed system, raises pH with little effect on alkalinity, calcification lowers both pH and alkalinity. Thus, photosynthesis supports calcification by removing the excess CO2 produced and preventing acidification. Calcification, in turn, supports massive photosynthesis (and oxygen production) by preventing depletion of the carbon supply. We discuss these matters in greater depth in Chapter 10. A specific example

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FIGURE 8.4 The distribution of dissolved compounds in the carbonate/water reaction chain as a function of pH. Note that sea water is buffered and occurs only over a limited pH range, while pure water can range widely. After Home (1969). Reprinted by permission of John Wiley & Sons, Inc.

applied to a coral reef microcosm is given in Chapter 20 and described in depth by Small and Adey (2001), with the primary elements of the carbonate system shown in Figure 8.5. In the CO2–CaCO3 system, the oceanic parallel to high photosynthesis, high levels of oxygen in the surface photic zone, is seen in calcium carbonate saturation (Figure 8.6). In tropical oceans, ultimately due to photosynthesis, there is a great excess of calcium carbonate in crystalline form as shells. However, in deeper water, carbonate concentration rapidly falls and calcite becomes undersaturated (i.e. shells begin to dissolve as they sink). Where the oxygen minimum and the carbon dioxide maximum meet, sea water has only 70% of saturation levels. Finally, below about 4500 meters the rate of supply of calcium carbonate from the surface is exceeded by dissolution and carbonate shells are virtually absent from sediments. Most of the carbon on the surface and in the crust of the Earth does not occur in organisms or in the atmosphere. At any one time, carbon occurs mostly in limestones, in coal and oil, and in other organic rock derivatives (Figure 8.7), mostly deposited in shallow waters. However, the exchange rate, primarily through carbon dioxide, is very large. For example, carbon turnover between the atmosphere and organisms occurs on the order of every 20 years. Also, as large as the reservoir of carbon is in the rocks, on a time scale of about 400 million years, geological processes bring the carbon to

the surface where, partly through the atmosphere, organisms can again turn over that stored carbon. All of the carbon on the surface and in the continental crust, except for a small amount of new carbon arriving from deep in the Earth, mostly through volcanoes, has been cycled through organisms several times. At least prior to the use of fossil fuel by humans, it is likely that the storage of “organically derived” carbon in the Earth’s rocks was continuing to grow slowly as the continents enlarged (Chapter 3).

CARBON DIOXIDE AND GLOBAL AQUATIC RESTORATION Most people are aware of the concept of acid rain and understand that many lakes in largely igneous and metamorphic regions such as New England and Scandinavia, where there is little carbonate buffering, have had their fish populations radically altered by such rain from upwind industrial areas. Carbon dioxide in the atmosphere does make rain acidic, as we describe below; however, in the case of lakes it is excess SOX from coal-fired power plants, effectively sulfuric acid in the rain that is the primary problem. However, the ever-increasing CO2 in the atmosphere, resulting from the burning of all fossil fuels, is also having a serious effect on the pH of natural waters.

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FIGURE 8.6 Factors affecting the distribution of calcium carbonate as calcite, with depth, in the equatorial Pacific Ocean. After Kennett (1982).

FIGURE 8.5 The daily state of the carbonate system and pH in a coral reef microcosm. (A) mean pH levels during a 24-hour cycle for one year; (B) mean Talk (total alkalinity) during a 24-hour cycle for one year; and (C) mean state of daytime carbonate system calculated by nomogram from Talk and pH. From Small and Adey (2001).

Sea water is strongly buffered for pH and generally ranges from 8.00 to 8.40. Because of the ions present, great changes in carbon dioxide are necessary to effect a small change in pH. Nevertheless, most marine organisms are particularly susceptible to small pH changes, and in this respect, environmental status is crucial. Despite the buffering, the pH of sea water can be reduced as a function of the interaction of sea water with the CO2 in the atmosphere as well as photosynthesis and calcification in shallow water. Roughly one half of the anthropogenic CO2 released into the atmosphere does not show up in the many standard measurements taken of the atmosphere. It has generally been thought that this was a good thing, as it has so far saved human civilization from the worse complications of elevating atmosphere CO2. However, researchers have now begun to document drops of pH in oceanic waters. This process is expected to reduce calcification by 14–30% by mid-century (Kleypas et al., 1999; Osmond, 2004). While there is little question that this will have

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FIGURE 8.7 The carbon cycle on Earth showing the approximate quantities of carbon and relative exchange between compartments. Mass exchange rates are given as microgeomoles/year (1014 moles/ year). Carbon mass is given as geomoles (1020 moles). After Stumm and Morgan (1981). Reprinted by permission of John Wiley & Sons, Inc.

disastrous effects on already damaged coral reefs worldwide, the more dangerous effects on biosphere health may be in changing the role of calcifying coccolithores, the dominant phytoplankters in tropical and temperate shallow ocean waters. As we noted above, the exchange rate of carbon dioxide between the biosphere and the atmosphere is very high, overturning on the order of 20 years. This is a good thing, in that it means that the undesirable changes that we have brought about in our atmosphere can be reversed relatively quickly, by reducing fossil carbon export and increasing photosynthesis. We discuss just such a scenario in Chapter 25. Here, we simply note that for a fraction of the cost of going to war we can solve one of our most serious environmental problems.

MANAGING CARBON DIOXIDE AND pH IN MICROCOSMS AND MESOCOSMS Sea Water Within a model system it is possible to increase the buffering effect of sea water using calcium carbonate chips or substrate. Since most shallow marine waters are highly supersaturated with calcium carbonate, this is an essential fail-safe feature for any marine microcosm or aquarium. In small and difficult situations with heavy animal loads or high calcification requirements, the use

of sand- or silt-size aragonite, the least stable form of calcium carbonate, is invaluable. The shells of some calcareous algae (e.g. Halimeda) or crushed coral skeleta can provide the aragonite (when clean of organic material). Oolitic or nearly pure Bahamian aragonitic sand is marketed in bulk in the United States. Spotte (1992) has argued that in an aquarium system, such carbonate (as calcite) has its potential dissolution surfaces “blocked” by magnesium overlays. Organic material can have the same effect. Thus, even though boring and scraping constantly make new surfaces available in a high diversity, properly functioning mesocosm, it is good practice to use a fine aragonite sand or silt and to arrange for frequent delivery of fresh sand. In part, by reducing carbon dioxide production and removing carbon dioxide through “excess” photosynthesis one can achieve a status of the pH/carbonate complex that is equivalent to most shallow sea waters. However, if significant calcification is occurring in a closed system and maintaining the rate of such calcification is a primary feature of the model, it will likely be important to replace alkalinity depletion with an outside source, much as occurs in the wild. This process is discussed in greater depth in Chapters 10 and 20. However, it is important to emphasize that many properly operated shallow water microcosms, especially coral reef systems, will have calcification rates that are so high that both alkalinity and calcium ion need to be monitored and re-supplied, just as in the wild.

Fresh Water Rainwater from an unpolluted atmosphere typically has a pH of less than 5.6 (i.e. moderately acidic due to the interaction of atmospheric carbon dioxide with the water while it cycles through the atmosphere. On limestone and related substrates, this natural acidity can be strongly buffered. In some cases, however, particularly on largely unbuffered granitic rock basements, and with the addition of organic acids from some vegetation, the natural acidity of the rainwater can be significantly increased in the surface and groundwater. Freshwater lakes, ponds, and rivers typically vary from slightly acidic (pH 6) to moderately basic (pH 9). Extremes occur from acid volcanic lakes (near pH 1) to soda lakes (at pH 12), though these would be of concern only to a few aquarists. Because of great concern over the polluting effects of acid rain and the resulting environmental acidification, considerable study has been directed to the negative effects of acidification on flora and fauna (Figure 8.8). The interested reader is referred to Cresser and Edwards (1987). In the modeling of freshwater systems, the aquarist seeks to simulate waters of a given pH. For basic

Gas Exchange and Selected Model Ecosystems

FIGURE 8.8 Lower pH tolerance limit of common molluscs and crustaceans found in Norwegian fresh waters. After Cresser and Edwards (1987). Reprinted with permission of Cambridge University Press.

waters, above pH 8.0, the same rules previously discussed for salt waters apply. On the other hand, if neutral or acidic waters are desired, the situation becomes more complex. Certainly if a high-nutrient, low-pH environment is desired and oxygen levels are not a concern, then bacterial filtration is an ideal approach to system management, preferably using a rotating drum or trickle system instead of a “filter” unit to avoid removing plankters. On the other hand, if a low-nutrient, low-pH (e.g. a black-water stream) environment is needed, the situation becomes considerably more difficult. In mesocosm and microcosm simulations of black-water streams where fish and invertebrate biomass are kept appropriately low and where energy input is derived largely from slowly breaking down leaf litter, minimum mechanical filtration or, preferably, settling traps may be all that is required. For simulating highly acidic natural waters, acidification can be derived from CO2 bubbling.

GAS EXCHANGE AND SELECTED MODEL ECOSYSTEMS The southern bank barrier coral reef on the Caribbean island of St. Croix can be regarded in many ways as a generalized tropical reef. It is mature, well developed

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geologically and biologically, and has been studied in some detail. The water moving onto the reef due to wave and current action typically has an oxygen concentration close to 6.5 mg/liter, a level that varies by only a few tenths day and night (Figure 8.9). This is essentially the saturation point. As this sea water flows in over the reef, driven by the constant trade winds, it picks up extra oxygen, becoming highly supersaturated during the day because of excess photosynthesis, that is, photosynthesis that exceeds respiration. On the other hand, at night the same water loses oxygen, due to the respiration (without photosynthesis) of both plants and animals in the reef. The effect of extensive wave breaking on the exchange of oxygen can also be marked on rough days and causes oxygen loss during the day and oxygen gain at night, the net effect being to smooth out metabolic effects on the gas concentrations. This is not an unusual pattern for a well-developed, open-water coral reef, whether IndoPacific or Caribbean (see Chapter 20). To simulate this typical reef environment in a microcosm system, the aquarist would need to obtain a night-to-day oxygen concentration range from 5.5 to 8.5 mg/liter, 6.3 mg/liter being the approximate saturation level. The traditional marine aquarium, with its heavy animal oxygen requirement, increased by bacterial action in biological filters, cannot achieve supersaturation. Trickle filtering and foam fractionation release oxygen from the water and actually prevent supersaturation, though oxygen rather than or mixed with air might produce the appropriate effect. Even if well lighted, such a system is likely to remain undersaturated for oxygen and may well go below 5 mg/liter at night. The lower limit of oxygen for water overlying a reef community is probably typically about 4 mg/liter under exceptionally calm conditions. Extensive periods lower than this level in the main mass of overlying water would likely be detrimental to reef plants and animals, especially because oxygen concentration would be considerably lower in the interstices of the reef. Intensive air bubbling carried out in well-kept and reasonably loaded traditional tanks could produce minimum oxygen levels at or above 4–5 mg/liter. However, without intense lighting and abundant photosynthetic plants (or an oxygen bottle) it would not be possible to raise oxygen concentrations above 6.5 mg/liter and likely not even to that level. The “dry”-type trickle filter is excellent for raising oxygen levels from the lower potential values. However, it too loses oxygen during the day. A dry trickle filter could be attached to the system at night and separated during the day to overcome this problem. The oxygen concentration in a Smithsonian coral reef microcosm compared to that in the wild reef is shown in Figure 8.9. As described in Chapter 11, by using an algal turf scrubber rather than a bacterial filter, even during

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FIGURE 8.9 Comparison of oxygen levels in the open sea and on a St. Croix coral reef with levels in a coral reef microcosm (see also Chapter 20). After Adey (1983). –, Oxygen saturation.

the dark hours oxygen levels are stabilized just below saturation levels. During the day oxygen levels in this well-lighted reef tank (see Chapter 20) rise well above saturation and in most respects match wild reef values closely. Using an oxygen meter, one can measure the rate of oxygen uptake in a mesocosm or aquarium system during the dark at near saturation levels to determine if the community respiration load is equivalent to that in the environment one wishes to simulate. This measurement must be taken at or near saturation so as not to have to account for exchange with the atmosphere. In one of the early 1800-gallon reef tanks, for example, the dark respiration rate was about 2 g O 2/m2 of reef surface/hour or about 24 g O 2/m2/day. This is only about one-half of the wild St. Croix reef rates, which presumably means that we could have doubled our animal respiratory load, assuming that wave or other exchange keeps oxygen concentrations at a minimum of about 4 mg/liter. Later tanks have had rates of 3–5 g O 2/m2/h, rather closer to rich reef levels. Oxygen is relatively soluble in water and exchanges rapidly with the atmosphere in bubbling or wave action. However, carbon dioxide exchanges more slowly and even though sufficient oxygen may be supplied to a microcosm, CO2 concentration may well increase rapidly,

thereby lowering pH even while oxygen remains at satisfactory levels; therefore both O2 and pH levels throughout the day should be checked at least occasionally. Equally important, as discussed in Chapter 9, nitrogenous exchange between plants and animals is not significantly affected by atmospheric exchange. Even if oxygen is artificially kept above 5 mg/liter by physical atmospheric exchange methods, it does not mean that water quality is not otherwise rapidly degenerating. It is wise to have either adequate water buffer to carry a system through the night or a plant-compensating system. The critically important variable of photosynthesis, or primary production, is treated in several chapters. However, it is so inextricably linked to oxygen, carbon dioxide, pH, and system loading that its role is repeated again here in the context of a coral reef model. Net primary production (in terms of oxygen) for the St. Croix reef is shown in Figure 8.10. If oxygen loss due to respiration, which we presume to be roughly constant at all times, is removed from the data (by dropping the zero line approximately 2.5 g O 2 /day), a curve of approximate total photosynthesis is derived. Several important pieces of information can be derived from this diagram. First, total photosynthesis is very high, at approximately 40 g O 2/m2/day. If this is converted to actual plant production (leaving out what the algae themselves use),

Gas Exchange and Selected Model Ecosystems

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FIGURE 8.10 Mean yearly diurnal oxygen exchange for several reef transects on the island of St. Croix. After Adey and Steneck (1985).

one finds a rate of about 25 g ( dry weight)/m2/day. In the laboratory, measured rates of actual algal production consistently achieve 10–20 g ( dry weight)/m2/day on flat screens. Since a typical reef has several times the mean surface of a flat screen, the reef value measured by oxygen seems not unreasonable. Also production (photosynthesis) continues to increase during the morning, peaking around 12:00 h when sunlight is at its greatest intensity. In summer, it appears that there is a slight drop by noon, but this is probably at least partly due to saturation of metabolites. Unlike what most scientists have thought with regard to other marine algae, the reef plants (primarily algal turfs) can use most of the available sunlight and as a community do not seem to be inhibited by the intense light (see Figure 5.15). The high respiration and biomass levels of a shallow-water reef, and a well-designed and operated reef microcosm, are internally driven by a high level of plant production that needs full sunlight to fully perform. We have based our discussion of oxygen and carbon dioxide exchange to this point on field studies and models of coral reef systems. However, the points made are equally true in other model ecosystems. One tends to think of cold-water northern ecosystems as highly seasonal ones that may reach high levels of

activity for short periods in the summer and essentially shut down for the colder, darker part of the yearly cycle. However, examination of primary production in Gulf of Maine rocky-bottom kelp and rockweed communities shows that this is hardly the case (Figure 8.11). Photosynthetic efficiency, or available light converted to biological use, on a wave-beaten rocky shore is about the same, in proportion to available light, as on a coral reef. Interestingly enough, on the rocky shore itself, grazing rates are relatively low and thus there is an actual excess of production. In the wild, roughly three-quarters of the plant production is eventually lost from the rocky bottom to beach drift and finally delivered by tides and currents to the inshore mud flats. In short this community is a strong net exporter of biological production, and this must be taken into account when designing such a system. In the rocky Maine shore microcosm, oxygen levels averaged higher than on a coral reef, as a reflection of this system as a net producer and exporter of plant biomass. At 8.5–9.5 mg/liter of dissolved O2, average oxygen concentration remains above saturation for most of the year. This occurs in spite of the fact that considerable wave action was present, continuously, in the model (see Chapter 21).

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FIGURE 8.11 Yearly productivity of benthic algae (in wet weight) in rocky intertidal and subtidal zones in the northern Gulf of Maine. After Adey (1982).

References Adey, W. (1982) A resource assessment of Gouldsbaro Bay, Maine. Report to NOAA, Marine Sanctuary Program. NA81AA-D-Cz076. Adey, W. (1983) The microcosm: a new tool for reef research. Coral Reefs 1: 194–201. Adey, W. and Steneck, R. (1985) Highly productive eastern Caribbean reefs: synergistic effects of biological, chemical, physical and geological factors. In: The Ecology of Coral Reefs. M. Reaka (Ed.). NOAA Symposium Series on Underwater Research, Vol. 3, Washington, DC. Blankenship, K. (2005) Bay experiences largest recorded anoxic zone this summer. www.bayjournal.com. Cleseri, L., Greenberg, A., and Prussell, R. R. (Eds) (1989) Standard Methods for the Examination of Water and Wastewater, 17th edn. American Public Health Association, Washington, DC.

Cresser, M. and Edwards, A. (1987) Acidification of Freshwaters. Cambridge University Press, Cambridge. Dietrich, G. (1963) General Oceanography. Wiley-Interscience, New York. Dodds, W. (2002) Freshwater Ecology. Academic Press, San Diego, California. Flood, J. (1983) Archaeology of the Dreamtime. Collins, Sydney. Horne, R. A. (1969) Marine Chemistry. Wiley, New York. Hutchinson, G. E. (1957) A Treatise on Limnology, Vol. 1. Wiley, New York. Kennett, J. (1982) Marine Geology. Prentice Hall, Englewood Cliffs, New Jersey. Kleypas, J., Buddemeier, R., Archer, D., Gattuso, J.-P., Langdon, C., and Opdyke, B. (1999) Geochemical consequences of increased atmospheric carbon dioxide on coral reefs. Science 284: 118–120. Livingston, R. (2006) Restoration of Aquatic Ecosystems. Taylor & Francis, Boca Raton, Florida.

References Lovelock, I. (1979) Gaia: A New Look at Life on Earth. Oxford University Press, Oxford. McConnaughey, T. (1994) Calcification, photosynthesis and global carbon cycles. Bull. l’Inst. Ocean. Monaco 13(Specl.): 137–161. Millero, F. and Sohn, M. (1992) Chemical Oceanography. CRC Press, Boca Raton, Florida. Osmond, B. (2004) Changing the way we think about global change research: scaling up in experimental ecosystem science. Global Change Biol. 10: 393–407. Richards, F. (1965) Dissolved gases. In: Chemical Oceanography. J. Riley and G. Skirrow (Eds). Academic Press, London.

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Schmidt-Nielsen, K. (1975) Animal Physiology. Cambridge University Press, Cambridge. Small, A. and Adey, W. (2001) Reef corals, zooxanthellae and freeliving algae: a microcosm study that demonstrates synergy between calcification and primary production. Ecol. Eng. 16: 443–457. Spotte, S. (1992) Captive Seawater Fishes. Wiley-Interscience, New York. Stumm, W. and Morgan, J. (1981) Aquatic Chemistry. Wiley, New York. USGS. (2005) Resource Data Base for Gulf of Mexico Research. www.gulfbase.org.


C H A P T E R

9 The Primary Nutrients – Nitrogen, Phosphorus, and Silica Limitation and Eutrophication

Open ocean sea water contains about 35 parts per thousand (ppt; 35 000 ppm) by weight salts and other elements, in addition to the hydrogen and oxygen that make up the remaining 965 ppt (mostly as water). Over 99.6% of the “salt” weight is made up, in order of abundance, of chlorine, sodium, magnesium, sulfur, calcium, and potassium. These elements are conservative. They vary little in their proportions over the entire world’s oceans and even into most estuaries. Several gases, nitrogen, oxygen, and carbon dioxide, are also more or less abundant; these we discussed in Chapter 8. Most of the remaining chemical elements occur in sea water, in extremely small quantities. However, there are a number of elements, required by some or all plants, that occur normally at concentrations of a small fraction of a ppm to perhaps as much as 0.2 ppm. The most important of these elements to organisms are nitrogen, phosphorus, and silica. See Table 4.4 for a summary of these relationships. In fresh waters, the conservative elements are generally present in very small quantities with salt lakes in basins without an outflow being striking exceptions. In salt lakes, the dominant salts vary widely, depending on the rocks present in the drainage basin (see Chapter 4). However, the same basic nutrients as in the sea tend to be limiting to plant production in the Earth’s fresh waters. In this chapter we discuss the primary nutrients, nitrogen, phosphorus, and silica. After the basic physical parameters, temperature, light, etc., the abundance of these elements is critical in determining the character and function of an aquatic ecosystem. Other nonconservative elements might be limiting in special cases. Iron has recently been under heavy investigation as a limiter

to primary production in ocean waters far from land. This situation is highly unlikely in model ecosystems and human-controlled aquatic ecosystems because of the abundance of iron in human environments. Carbon (as CO2 and alkalinity) could also be limiting in some community models (e.g. coral reefs). This potential problem is treated in Chapters 8, 10, and 20.

NUTRIENTS IN NATURAL WATERS A typical tropical open ocean distribution pattern of dissolved (reactive) nitrogen and phosphorus with depth is shown in Figure 9.1. Surface values of these essential compounds are typically less than 1 µM (0.014 ppm) nitrogen as nitrite plus nitrate and less than 0.1 µM (0.003 ppm) phosphate. Below the photic zone, and a little below the oxygen minimum and carbon dioxide maximum, where phytoplankton and zooplankton are being eaten or are breaking down without light for recycling, nutrient levels climb to about 20–30 times surface values. In the deepest waters, which are cold with very slow currents derived from Arctic and Antarctic surface waters, nutrient levels are moderate at all times. Largely inaccessible to plants except at unusual points of current upwelling, reactive nitrogen and phosphorus remain in storage for hundreds to thousands of years in the deep ocean. In relatively shallow coastal waters the picture is rather different, especially outside the tropics where surface warming in the summer tends to prevent mixing. The yearly cycles of nitrogen and phosphorus levels for the English Channel are shown in Figure 9.2. Here, the

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9. The Primary Nutrients – Nitrogen, Phosphorus, and Silica

FIGURE 9.1 Distribution with depth of phosphate and nitrate in the tropical and subtropical portions of the oceans. Microgram atoms per liter ⫽ µM; concentrations of N as nitrate with depth are 0.3–0.6 ppm; P as phosphate are 0.06–0.09 ppm. After Sverdrup et al. (1942). Reprinted by permission of Prentice Hall, Englewood Cliffs, New Jersey.

mixing of tides and winter storms accompanied by low light allows moderate levels of nutrients to build up in winter. Note, however, that in the winter at 5–8 µM nitrogen as nitrite plus nitrate, levels are still well below deep ocean levels. Most aquatic animals excrete ammonia. This very toxic compound is metabolized by bacteria to the mildly toxic nitrite and finally to the relatively benign nitrate. Both ammonia and nitrite occur at a fraction of the concentration of nitrate in the water columns of most aquatic ecosystems. Algae and bacteria both compete for these compounds as sources of nitrogen and energy, and if it is possible to measure ammonia and nitrite by any but the most sophisticated of chemical analytical processes, that is, if either is over about 0.5 µM (0.0007 ppm), they are probably much too high, as we discuss in some depth below. The nutrient picture in fresh waters not subject to intensive human activity is similar to that of the ocean, but different in some critical ways. First, nitrogen has many potential sources of atmospheric bacterial fixation on the land. The equivalent process is not available for phosphorus, and thus phosphorus tends to be limiting for plant production, rather than nitrogen. It is phosphorus that operates on a yearly cycle to limit primary production. Figure 9.3 shows typical summer patterns on several lakes with low levels of phosphorus at the surface markedly increasing below the thermocline. On the other hand, near the bottom, additional mechanisms quite different from those applicable to nitrogen are active (Figure 9.4). Under aerobic conditions, phosphate combines with ferrous iron in the sediments. The precipitate that forms remains locked in those sediments until they approach anaerobic conditions. Thus, under stratified and stagnant summer conditions, low

oxygen reverses this reaction and allows reactive phosphorus to escape into the lower water column. However, being generally below the photic zone except in the smallest lakes, it remains largely unavailable for plant growth. Silicon is one step up from carbon in the periodic table of the elements. Thus, chemically it is quite similar to carbon, but is a little over twice as heavy. Forming an enormous number of compounds as minerals in the Earth’s crust, it is to the lithosphere what carbon is to the biosphere. Diatoms are the only primary producers that make an ecologically important use of the element. Diatoms use silicate, instead of cellulose or related compounds, to form cell walls. They are essentially alone in this use, although a few other heterotrophs (secondary producers) such as radiolarians and some sponges make silica skeletons. Radiolarians can be extremely abundant both in the plankton and on the bottom in specialized localities. While silicon (as silicate) is moderately abundant in water environments (about one-tenth of carbon and six times that of reactive nitrogen), it can sometimes be limiting to plant production when that production is dominated by diatoms (see Table 4.4). Today human influence on the biosphere is massive and rapidly growing; thus, it is critical for the modeler, the aquatic restorer, and the hobbyist to keep the above described relationships in mind. Under pre-human conditions, in all aquatic and marine environments, except relatively rare naturally eutrophic situations, the low concentrations of nitrogen, phosphorus, silica, and sometimes iron provided considerable restrictions on the level of plant activity and therefore on the level of total biological activity. An upwelling zone with a prevailing offshore wind, a whale washed up on the shore of a restricted inlet, a marshy basin on a recently burned slope, organic detritus concentrated on a beach or a mud flat by a storm – these were naturally eutrophic or nutrient-rich situations. However, they were restricted in space and time. In the planktonic environment, the flow of nutrients to the algal cells could also be greatly limited by the diffusive boundary layer (DBL); understanding the conditions under which the effect of the DBL is reduced is a science by itself (Riebesell and Wolf-Gladrow, 2002). Much of the practical and operational water quality control measures discussed in this book will deal with ways of reducing the effects of the DBL. Some heterotrophic bacteria, primarily under anaerobic conditions, but as we now know also under some aerobic conditions (Sprent, 1987), utilize nitrate or nitrite and produce the gases nitrous oxide and nitrogen. This process of denitrification removes nitrogen from an aqueous medium or sediments to the atmosphere. In the water column of most lakes and the oceans, this process

Nutrients in Natural Waters

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FIGURE 9.2 Yearly cycles of nutrients in the English Channel. Milligrams per cubic

water ⫽ µg/liter; for nitrate, 100 µg/liter ⬇ 7µM; for phosphate, 30 µg/liter ⫽ 1 µM. After Gross (1982). Reprinted by permission of Prentice Hall, Englewood Cliffs, New Jersey.

is negligible. However, in the anaerobic sediments of eutrophic bodies of water (enriched by human activities) denitrification rates can be considerable, in some cases at the levels of primary production (Seitzinger, 1988). On the other hand, in noneutrophic shallow waters, low in nitrogen, denitrification, mostly from underlying sediments, occurs at rates an order of magnitude or more below primary production, particularly

when that is achieved largely by macrophytes or attached algae. In summary, below about 15–20 µM (N as NO2 ⫹ NO3) (0.2–0.3 ppm) denitrification is negligible. Below about 1–2 µM (N as NO2 ⫹ NO3) (0.014–0.03 ppm) nitrogen fixation from gaseous N2 begins to be a significant factor (Lucid, 1989; Chapter 20). The net effect is that in most modeling and restoring efforts, where achieving

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FIGURE 9.3 Phosphate concentration in several temperature lakes during the summer. ␪, temperature °C; phosphorus: PT, total; PS, soluble; PST, in particulates. After Hutchinson (1957). Reprinted by permission of John Wiley & Sons, Inc.

the original, nondegraded, ecological environment is desired, denitrification (nitrogen loss to the atmosphere) is not a significant factor and a small amount of nitrogen fixation (from the atmosphere) is likely.

EUTROPHICATION AND HYPEREUTROPHICATION OF NATURAL WATERS Excess concentration of organics and nutrients by human activities leads to a variety of problems in wild ecosystems that are not adapted to such excesses. Most critical for marine and freshwater environments is ammonia. When this very toxic nitrogenous excretion of many waterliving organisms (see Chapter 7) is available in abundance, and sufficient plant or microbe activity is not present to remove it, it can become deadly. A number of bacteria and fungi also perform nitrification, or breakdown of ammonia to nitrite and nitrite to nitrate, though they generally require oxygen and release carbon dioxide. Excess organic material without consequent plant return to the stored “fixed” carbon state also leads to a drawdown of oxygen and eventually anaerobic conditions. The combination of anaerobic conditions in the water column and the often-toxic products of anaerobic

bacteria (including H2S) provides environmental conditions that are suitable for very few organisms. As we discuss under Bacteriological Filtration in Chapter 11, it has become customary for modern human societies to avoid the most serious problems of excess concentration of organics (generally sewage) by providing large bacteria-operated industrial plants to break down these organics. A sewage plant releases carbon dioxide to the atmosphere, reducing biochemical oxygen demand (BOD) in the water effluent (but adding to global warming). The bacterial biomass that develops (sludge) is hauled away to environments of less concentration. Ocean dumping is rarely allowed today; however, spreading or spraying sludge on farm fields simply moves the problem to another location. Most of the nutrients in solution, as nitrites, nitrates, and phosphates, are then dumped into estuaries, lakes, and streams. While this process has avoided the most immediate difficulties of mass sewage, namely disease transmittal and local low oxygen, when carried out with large human populations it only extends the basic problem a few years. After a half-century of adding and upgrading sewage plants, as a “half solution,” the nutrients have simply built up downstream in lakes, bays, and now the ocean. Many algae and some aquatic plants are adapted to make use of the temporary mass availability of nutrients

Eutrophication and Hypereutrophication of Natural Waters

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FIGURE 9.4 Seasonal cycling of oxygen, iron as Fe2⫹, and phosphate just over the deepest mud, at 14 meters in an English lake. After Hutchinson (1957). Reprinted by permission of John Wiley & Sons, Inc.

in wild ecosystems (the dead whale, for example, or the school of fish on the beach). The life strategy of these “opportunists” is extremely rapid growth, given adequate light, temperature, and a large peak of nutrients. Given summer long or permanently high nutrients, these plants multiply rapidly, choking bodies of water and eventually reducing oxygen, killing themselves as well as many invertebrates and fish at the same time. Given elevated nutrients and typically higher temperatures some blue-greens (cyanobacteria) in fresh water and dinoflagellates in coastal waters can bloom, produce abundant toxins, and provide mass kills of fish and sometimes birds and humans (e.g. Livingston, 2006). To many humans, it is the fast-growing algae or the equivalent macrophyte such as Hydrilla or water hyacinth that is the problem, not ourselves who have created the unnatural high nutrient situation. Increasing nutrients to

moderate levels increases the growth rates of many plants (other factors being equal) and most animals including corals are not directly affected by this increase. Thus, in human cultured environments, it may be desirable to elevate nutrients (as in farming). However, at the risk of overstatement, we note again that such increases almost always change ecosystem community structure, sometimes radically. Direct control methods (e.g. weeding, light control) can affect these changes; however, this can be very difficult and costly to achieve. It has not been unusual to apply herbicides (to kill off the offending submerged aquatic vegetation (SAV) or algae), but this is a very short-term solution. Also, dredging of eutrophic sediments merely puts the problem off a few years and can rarely return an ecosystem to its original state. In wild ecosystems, this is not simply a matter of esthetics. The loss of major fisheries and their associated

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jobs, and the impending loss of recreational value, in Lake Okeechobee, Pensacola Bay, Chesapeake Bay, and now the northern Gulf of Mexico (to name just a few) is only a prelude of things to come. Serious fish and invertebrate diseases, and red tides that cause human illness and even death, are not far behind. Chemical and bacterial methods of dealing with human-concentrated nutrients have been developed (BNR: biological nutrient removal), and are beginning to be used in the US (Zickefoose, 2004). However, they are difficult, erratic, and costly (Chesapeake Bay Commission, 2004). After roughly 25 years of major effort by governments and NGOs, and billions of invested dollars, Chesapeake Bay, for example, is more eutrophic than when the effort began. Nutrient inputs in the rivers of the Bay have not been reduced, and the dead zone in the Bay in the summer of 2005 (Blankenship, 2005) was larger than ever. Some of this degradation can be put down to increasing population in the watershed, and indeed this cannot go on indefinitely. Mostly, however, it is a failure to recognize basic biology and ecology, and to develop countering methodologies. In Chapter 25, we bring together the rationale and methodology for a full solution to this ever-increasing problem.

problem in traditional aquarium management, and in most model ecosystems for that matter, has been preventing the “pollution” of the system by these excretory compounds. It is primarily to solve this very basic problem that the biological filter was developed. Unfortunately, in many cases reliance on the bacterial or “biological” filter is counterproductive in that the solution to the ammonia problem is accompanied by a number of negative side effects that render natural ecosystem management difficult or impossible to achieve. Marine and freshwater planktonic algae actively photosynthesizing and growing have a continuous and often production-limiting requirement for nitrogen and other nutrients. Approximately 1 nitrogen atom is needed for every 7 carbon atoms built into plant tissue and 1 phosphorus atom for every 100 carbon atoms. Benthic algae, on the other hand, are capable of producing at a considerable deficit when nutrients are low (Figure 9.5). Likewise many fleshy algae are noted for their “luxury” or excess consumption of nutrients when they are available. Most algae accept ammonia as a nitrogen source and are capable of rapidly taking it up. The nitrification products of ammonia, nitrite, and nitrate, as well as more complex nitrogenous excretory products such as

NUTRIENTS AND MODEL ECOSYSTEMS Basically, the organic pollution problems are the same for the aquarist as they are for human society at large. Only the scale is different. It is instructive to compare wild ecosystem nutrients discussed above with those for traditional aquaria. We quote from Spotte (1979): “It is inevitable that seawater aquariums will become eutrophic . . . inorganic nitrogen levels in aquarium water can be staggering.” Great improvements in culture techniques have been made since the first edition of this book was written. However, these improvements apply to a limited set of organisms, in a garden-like environment; in an ecological context, considerable improvement is still needed. As we discussed in Chapter 7, animal tissue that has become food for other animals or for bacteria or fungi undergoes a continuous process of breakdown and assimilation. Carbohydrates and most fats in this breakdown process are metabolized using oxygen and result in the release of carbon dioxide. On the other hand, proteins, nucleic acids, and phospholipids (along with other compounds) provide an excess of nitrogen and phosphorus in addition to the basic carbon, hydrogen, and oxygen of organic tissues. The net result is a requirement for the excretion of nitrogen-rich and phosphorusrich compounds into the ambient water. Chief among these excretory compounds is ammonia. The central

FIGURE 9.5 Carbon, nitrogen, and phosphorus ratios in marine plants. Note that temperate algae were apparently not nutrient deficient, tropical algal turfs were not nitrogen deficient (due to nitrogen fixation) but were slightly phosphorus deficient, and larger tropical algae were deficient in both nutrients. Productivities as measured by biomass increase were approximately equivalent in all groups (Adey, 1987).

Nutrients and Model Ecosystems

urea, can also be used by many algae. In reef tank ecosystems, with dense algal and higher plant communities, nitrogen salts, measured with autoanalyzers, typically occur at a concentration of less than 1–1.5 µM (14–21 ppb). This is equivalent to the situation normally encountered in a wild reef and yet is at great variance with traditional aquarium systems in which nitrogen levels of over 100 ppm are acceptable. The limiting of sensitive organisms in aquarium systems by ammonia, nitrate, and nitrite, as well as the unstable environment these nutrients create in excess, is a major element in the erratic nature of the traditional aquarium. Tropical reef communities in particular are characterized by low nutrient levels. Nitrate levels in incoming ocean water in St. Croix reefs are about 0.4 µM (6 ppb). More open ocean or equatorial current situations (such as Grand Turk, for example) are even lower, on the order of 0.1 µM. Blue-green algae in reef waters are known to fix gaseous nitrogen much as the bacteria of the root nodules of legumes do in the terrestrial environment. However, these blue-greens are either not present or unable to fix nitrogen in any but the most nutrientminimum environment. High nutrient levels cause a shift in algal community structure, a shift that can be very detrimental to an attempt to simulate an ecosystem. It has long been known that perhaps next to siltation, elevated nutrients (or eutrophication) is one of the primary factors causing degeneration of wild reefs. A serious problem for coral reefs as well as most open shallow-water ecosystems is the relationship of such high nutrient levels to the growth capabilities of some species of both planktonic and benthic algae. Solar

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radiation or equivalent light levels can induce disastrous planktonic algal blooms at the nutrient concentrations of traditional aquarium tanks. It has been demonstrated that moderate nutrient levels (⬃5 µM N–NO3, 70 ppb) are not directly damaging to some reef corals (Atkinson et al., 1995). However, experiments have shown calcification disruption in corals by even lower nutrient levels (Marubini and Davies, 1996). At the very least, excess nutrients can allow benthic algae to outcompete corals. Even if grazing levels are greatly increased, this can provide a level of disturbance that is destructive to stony corals. Maine rocky shore and temperate estuarine systems such as the Chesapeake Bay, as well as other communities that have been involved in microcosm or mesocosm simulation, have relatively high concentrations of dissolved or reactive nitrogen (Figures 9.6 and 9.7). Those naturally rich ecosystems, however, at 5–10 µM ⫺ (N–NO⫺ 3 ) for unpolluted waters, and 10–80 µM (NO3 ) for polluted waters, are still far below the older type aquaria at 5000 µM (N–NO⫺ 3 ) or higher. Note that in Figure 9.7, 25 µM (0.38 m/liter) N–(NO2 ⫹ NO⫺ 3 ) and 13 µM (0.38 mg/liter) (total phosphorus as PO3⫺ 4 ) are noted as critical levels, above which algal or aquatic plant blooms occur with disastrous consequences. Both systems are also characterized by having both a sediment sink and an open ocean sink for such nutrients. If rocky shore and estuarine communities are managed properly, with considerable nutrient importation, then a “nutrient sink” is required to prevent eutrophication and radical alteration of the biological communities. Most such coastal marine communities are characterized by runoff from the adjacent land. Without the ocean sink to

FIGURE 9.6 Nitrate concentration as a function of salinity in the Sheepscot estuary (Maine), September 1986. After Fefer and Schettig (1980).

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FIGURE 9.7 Nitrate plus nitrite and total phosphorus as PO43⫺concentrations on the upper Potomac estuary, summer, 1972–1975. After Lippson et al. (1979).

eventually dilute and remove those nutrients, eutrophication would result. The data given in Figure 9.7 shows the Potomac River leading into the upper-mid Chesapeake Bay, as it was in the 1970s – already eutrophic. As we discussed above, this eutrophic character, in 2005, has extended to the entire upper half of this 200-mile-long Bay. In the simulations of Chesapeake Bay and the rocky Maine shore described in Chapters 21 and 22, dissolved nitrogen concentrations are normally maintained in the 1–10 µM range, far below presently existing levels in the wild ecosystem, but probably slightly above pre-human levels.

Some aquarists have advocated using the process of denitrification in special anaerobic traps to remove excess nitrogen from mesocosm and aquarium environments. Indeed, this process probably occurs to a limited extent in virtually all closed systems and in many wild systems. In eutrophic aquaria with rich sediment bottoms, it will certainly be an important process. However, in sediments and their overlying waters that are not enriched far beyond natural levels, denitrification rates are likely to be below 30–50 µM N/m2/h (Seitzinger, 1988). This is one to two orders of magnitude below the removal rates of nitrogen in primary production or

139

Summary

photosynthetic removal of nitrogen. In addition, denitrification does not remove the balanced array of nutrients that are taken up in primary production. A number of schemes have been developed to enhance denitrification (NO⫺ 3 to N2) in coral reef systems, and these have been reviewed by Delbeek and Sprung (2005). Some of these methods add sulfur so as to use sulfur bacteria to drive the process, and they can then work efficiently. However, all of the other criticisms remain, and one is operating a potentially deadly system in tandem with the highly oxygenated system desired. The chance for disaster is always present, and one has to ask: why not stick with the primary production processes that work so well in the wild? In recent years perhaps the most favored methodology for maintenance of high water quality in aquarium systems is foam fractionation, more commonly known in the aquarium trade as protein skimming. This process provides a fine stream of bubbles in a vertical column with a means for collecting the foam generated (Delbeek and Sprung, 2005) and has numerous variations and methods for increasing efficiency. The primary purpose is to remove dissolved organics and thus, unlike denitrification “filters” and similar to algal “filtration” systems, it will remove a cross section of nutrients. Foam fractionation does not directly remove dissolved nutrients and therefore cannot achieve the oligotrophic levels of open ocean waters, although schemes have been developed to enhance water column bacterial action (e.g. by adding alcohol – vodka) to enhance bacterial production and therefore increase skimmer removal of nitrogen and phosphorus. However, most important as a consideration for a technology for operating closed ecosystems, foam fractionation cannot differentiate between dissolved and particulate organics and the planktonic and reproductive flora and fauna. While foam fractionation cannot be used to accurately model most ecosystems, it could have been used where a more limited result of the culture of individual organisms does not directly or indirectly utilize a natural planktonic or particulate community (see Chapters 2, 6, and 17). If a “garden” is desired, this could be an excellent way to go, one for the aquarist and one for the aquarium (i.e. vodka). Ion exchange media, including charcoal and newer resins and plastic materials with great porosity and ion absorption characteristics, can also be used to reduce nutrients as well as dissolved organics. These media all suffer from difficulties of control and balance in the chemical soup that is a “living” water, especially sea water. Also, as in all filtration methods, plankton and larval stages are trapped and mostly destroyed (see also Chapters 6, 11, and 17).

SUMMARY The handling of nitrogenous and phosphorus wastes in aquarium simulations of ecosystems can be summed up by several critical requirements: 1. An animal load that is at least close to that in the wild (an excessive load technically can be managed; however, it makes the system more equivalent to an aquaculture or farming unit and presents numerous ecological balancing problems). 2. A built-in system for rapidly exporting ammonia and other waste compounds. In most aquarium systems this is the bacterial or “biological” filter. In most natural shallow-water ecosystems, and in the examples in this book, this requirement is accomplished directly by plants or by export/mixing with an adjacent community (a larger open body of water). 3. A means of ultimately exporting added nutrients. In the wild this is partly accomplished by oceanic dilution and sinking to deep water, although burial in marshes, sediments, and soils acts as a primary, short-term sink. The first requirement, that of an appropriate animal load for the area and volume involved, is discussed in depth in a number of the following chapters. The second requirement can be met by providing the appropriate photosynthesizers for the system being worked, and the right environmental factors, light, and water motion to enable those plants to function. These elements are discussed primarily in Chapters 12 and 14. Finally, the effects of an open-water sink relative to nutrients can also be provided by plants and algae (MAPS: managed aquatic plant systems), given a proper control mechanism. Several mechanisms, particularly algal turf scrubbing (ATS), have been devised and are discussed at length in Chapter 11. The management and restoration of wild ecosystems subject to human eutrophic degradation differs only as a matter of scale. Sewage plants at cities and towns and buffer strips and best management practices (BMPs) on farms are essential at the primary, particulate level and for disease control. New BNR methods have been developed for nitrogen and phosphorus, but they are batch, one nutrient at a time, processes and are very sensitive to minor environmental changes. Computer control and expert staff are necessary to achieve success. However, only solar-capture, photosynthetic (MAPS) methods can efficiently solve the eutrophication problem at landscape scale. These low cost methods have been demonstrated at large scale (20 mgd modules) and are discussed in Chapter 25.

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References Adey, W. (1987) Food production in low-nutrient seas. Bioscience 37: 340–348. Atkinson, M., Carlson, B., and Crow, G. (1995) Coral growth in high nutrient, low pH seawater: a case study of corals cultured at the Waikiki Aquarium, Honolulu, Hawaii. Coral Reefs 14: 215–223. Blankenship, K. (2005) Bay experiences largest recorded anoxic zone this summer. www.bayjournal.com. Chesapeake Bay Commission (2004) Cost effective strategies for the Bay. www.chesbay.state.va.us. Delbeek, C. and Sprung, J. (2005) The Reef Aquarium: Science, Art, and Technology, Vol. 3. Ricordea Publishing, Coconut Grove, Florida. Fefer, S. I. and Schettig, P. (1980) An Ecological Characterization of Coastal Maine, Vol. 2. US Fish and Wildlife Service, Boston, Massachusetts. Gross, M. C. (1982) Oceanography, 3rd edn. Prentice Hall, Englewood Cliffs, New Jersey. Hutchinson, C. E. (1957) A Treatise on Limnology, Vol. 1. Wiley, New York. Lippson, A. J., Haire, M. S., Holland, A. F., Jacobs, F., Jensen, J., MoranJohnson, R. L., Polgar, T. T., and Richkus, W. A. (1979) Environmental Atlas of the Potomac Estuary. Environmental Center, Martin Marietta Corp., Baltimore, Maryland. Livingston, R. (2006) Restoration of Aquatic Systems. CRC Press, Taylor and Francis, Boca Raton, Florida.

Lucid, D. (1989) Effects of Dissolved Inorganic Nitrogen Concentrations on Primary Productivity, Nitrogen Fixation, and Community Composition of Coral Reef Algal Turf: A Microcosm Study. M.S. Thesis, University of Maryland. Marubini, F. and Davies, P. (1996) Nitrate increases zooxanthellae population density and reduces skeletogenesis in corals. Mar. Biol. 127: 319–328. Riebesell, U. and Wolf-Gladrow, D. A. (2002) Supply and uptake of inorganic nutrients. In: Phytoplankton Productivity. P.J. le B. Williams, D. Thomas, and C. Reynolds (Eds). Blackwell Science, Oxford. Seitzinger, S. (1988) Denitrification in freshwater and coastal marine ecosystems: ecological and geochemical significance. Limnol. Oceanogr. 33: 702–704. Spotte, S. (1979) Sea Water Aquariums: The Captive Environment. Wiley, New York. Sprent, J. (1987) The Ecology of the Nitrogen Cycle. Cambridge University Press, Cambridge. Sverdrup, H., Johnson, M., and Fleming, H. (1942) The Oceans: Their Physics, Chemistry and General Biology. Prentice Hall, Englewood Cliffs, New Jersey. Zickefoose, B. (2004) Improving the Design of the BNR Process in Wastewater Treatment Plants from an Operations Perspective. M.S. Thesis, Engineering Department, Florida State University.

C H A P T E R

10 Biomineralization and Calcification A Key to Biosphere and Ecosystem Function

Under very special circumstances of burial and preservation the soft tissues of animals and their imprints in sediments can be preserved in the fossil record. Woody plants of the last 400 million years have been preserved, especially under swamp conditions. However, the tremendous library of organic evolution of fauna over the last 543 million years, the paleontological record, is primarily written in mineralized skeleta. This is a complex record of comings and goings, of changes in the kinds of organisms that are dominant, that depends, at least in part, on small changes in the chemistry of the sea (Knoll, 2003). For nearly a century, geologists drew the practical line between living and nonliving at the pre-Cambrian/ Cambrian boundary, about 500 million years ago. The principal paleontological question of the first half of this century was: why did a large, complex fauna suddenly show up at the Cambrian? Intensive paleontological work through the middle and later part of the 20th century has demonstrated life over 2 billion years further back, with numerous complex, taxonomic lines at least several hundred million years before the Cambrian. The event that changed apparent life on Earth so radically was the widespread development of an ability on the part of many evolutionary lines to make mineralized hard parts. That these fossils were easily seen in sedimentary rocks, and their predecessors were not, formed the principal character of early paleontology. The development of mineralized hard parts was an inevitable step in evolution. Protection by external skeleta in aqueous environments was an obvious way to lessen predation pressure, though, almost as quickly, predators upped the ante of the arms race (Chapter 16) by developing mineralized teeth and radula. In reef systems, calcification by many organisms also became a competitive device to obtain space and light.

Muscles certainly greatly pre-date the Cambrian as part of multicellular organisms. However, muscles are more efficient, the required distance of movement being less, if they are attached to and pulling against something hard. Thus, whether for capture or escape, mineralized skeleta for muscle attachment provided major advances in evolutionary “races.” Finally, sensing and balance systems gain greater precision, in many cases, if they are not jell-like in texture, and instead are heavier than water and “rock-firm.” Many organisms developed mineralized otoliths or their equivalent. Thus, mineralized hard parts have become an indelible and critical element of many organic lines, both aquatic and terrestrial. The realm of geology is dominated by silicate chemistry. However, except in science fiction, this is the province of geology, the lithosphere, rather than the biosphere, where carbon is the key element. The element silicon is used by many living organisms to form hard parts, and diatoms are a very abundant example in aquatic environments; however, such use is as amorphous silica (SiO2) not as a crystalline silicate. Silica is an important biomineral; however, it follows the carbonates in abundance. Of the hundreds of minerals known, nearly half are not silicates, and about 50 have been developed by many phyla of living organisms as hard parts (skeleta, teeth, and sensory devices). Table 10.1 shows the more important minerals of aquatic systems and the phyla in which they occur. For very good reasons, as we shall see, carbonate minerals overwhelmingly dominate the biominerals. Nevertheless, a dozen phosphatic minerals are also extremely important in the biosphere, for example as vertebrate bone (calcium hydroxyapatite), and iron oxides and calcium oxalates come into play in a few groups (especially as teeth and skeleta, respectively).

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142

10. Biomineralization and Calcification

⫹

⫹

* ⫹ ⫹

Sipuncula

* * ⫹ ⫹

Arthropoda

⫹ ⫹

⫹ ⫹

Chordates (mostly bony fish)

⫹

Echinodermata

⫹ ⫹

Mollusca

⫹

Brachiopoda

⫹ *

Ectoprocta

* ⫹

Platyhelminithes

Ciliophora

* ⫹

Coelenterata

*

Foraminifera

Radiolaria

Heliozoa

Rhizopodea

Charophyta

Zygnematophyta

⫹ *

Annelida

⫹

* * ⫹

Porifera

⫹

Chlorophyta (including Halimeda)

*

Rhodophyta (including Corallines)

⫹

Phaeophyta

Coccolithophores

*

Diatoms

Dinoflagellata

⫹ ⫹

Cyanophyta (Cyanobacteria)

Carbonates Calcite (Ca(Mg)CO3) Aragonite (CaCO3) Vaterite (CaCO3) Monohydrocalcite Amorphous hydrated carbonate Phosphates Dahllite (Ca10(PO4)6(OH)2) Francolite (Ca3Mg3(PO4)4) Brushite Amorphous dahllite Amorphous brushite Amorphous whitlockite Amorphous hydrated ferric phosphate Halides Fluorite Amorphous fluorite Oxalates Whewellite Weddelite Sulfates Gypsum Celestite Barite Silica Opal (SiO2) Fe-oxides Magnetite Goethite Lepidocrocite Ferrihydrite Amorphous ferrihydrates

Bacteria

Phylum

TABLE 10.1 Principal Mineral Formation by Aquatic Organisms

*

⫹ ⫹

⫹ ⫹

⫹

*

⫹

⫹

⫹ ⫹ ⫹

⫹

⫹ ⫹ ⫹ ⫹

⫹ ⫹ ⫹ ⫹

⫹ ⫹ ⫹

⫹

⫹

*

⫹

⫹ ⫹

*

⫹

*

⫹

⫹

⫹

⫹ ⫹

⫹ ⫹

⫹

⫹ ⫹ ⫹ ⫹

⫹

⫹

⫹

⫹ ⫹ ⫹ ⫹ ⫹

Note: *Biomineralization of widespread occurrence and of special significance to mesocosm and aquarium operation. Modified after Simkiss and Wilbur (1989).

Since such a large number of minerals of quite different chemical composition are used in such a large percentage of phyla of living organisms, it seems likely that there are some basic physiological and biochemical

conditions under which biomineralization occurs. Before entering into our principal concern in this chapter, biomineralization that is potentially controlled or limited by the basic parameters of living models and

The Carbonate System and the Formation of Calcite and Aragonite

degrading ecosystems, we examine biomineralization in general. In some species, mineralization occurs simply because of the chemical changes caused in the surrounding waters by the metabolism of the organism. This occurs most often in bacterial and blue-green algae (cyanobacteria) films and can involve the precipitation of sulfides in the first case and carbonates in the second. See also the discussion on the green algae Halimeda below. Mostly, however, biomineralization is under some direct control (and at some energy expenditure) of the organisms involved, as is the case for most skeletal hard parts, such as vertebrate bone, mollusc shells, and a wide variety of tooth-like structures.

THE PROCESS OF BIOMINERALIZATION Control of the production of hard parts by an organism involves two key elements: 1. The enclosure of a very small volume of water by tissues, cells, a membrane-bound vacuole, or a macromolecular sheath produced by the organism. This space can be totally surrounded by organic material or it can be created against a substrate or an already formed mineral base. 2. The capability of bounding cellular membranes to pump ions (typically Mg2⫹, Ca2⫹, Si4⫹, CO32⫺, PO42⫺, H⫹, etc.). The enclosure of the mineralization space allows the membrane-pumping function to build up high concentrations, generally greatly supersaturated, of the appropriate mineral components. The ion pumping capabilities of phospholipid membranes are well known (Figure 10.1) and are typically the subject of whole chapters in modern biochemical texts (e.g. Mathews and van Holde, 1996). Typically, the pore of an ion-channel is formed by a protein, embedded in the phospholipid membrane, and, especially in plants, the structure and rapid function of these channels have been extensively studied (Heldt, 2005). Some ion-channels pump ions to create an electrical gradient (e.g. the strong pH gradient between stroma and thylakoid in photosynthesis; see Chapter 5); however, generally the electrical gradient is avoided by exchanging ions of equivalent valence and this is likely critical in coral calcification (see below). Other components of greater sophistication may or may not be present. The most common of these are nucleation sites created by organic molecules (often acidic glycoproteins) that attract and hold the cation (e.g. Ca2⫹) from which mineralization can initiate. Another component that can provide more control to biomineralization is an organic matrix that provides

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the framework of a more complex hard-part structure (such as a tooth or bone). Thus, the basic principles for the construction of organism hard parts, with minerals both known in the lithosphere and specific to organisms, whether skeletal, sheathing, or sensory, are known. The minerals employed are numerous, with undoubtedly more to be discovered. In general, the process of membrane formation followed by ion pumping requires energy and can therefore work against considerable environmental gradients. In the end, however, a basic ecological trade-off must apply. The survival benefits provided by the skeleta or sensory apparatus must exceed the survival losses inherent in the energy given up. Also, in many cases, behavioral aspects requisite to the use of hard parts can have considerable bearing on survivorship. A very striking example in the aquatic environment is the required molting phase of crustaceans: during the soft intervals, while the skeleta are being “calcified,” individuals of many species are in large measure defenseless and subject to considerable losses due to predation.

THE CARBONATE SYSTEM AND THE FORMATION OF CALCITE AND ARAGONITE The construction of hard parts of silica and phosphate is very important to biosphere function. However, they do not begin to compare in magnitude to the importance of calcium carbonate. The direct or indirect formation of calcite and aragonite by organisms has massively altered the Earth’s atmosphere, hydrosphere, and lithosphere and moved about 70 000 gigatons of carbon from the original atmosphere primarily to the oceans and thence to the lithosphere. Limestones and lime-rich rocks are among the principal elements of the Earth’s crust. Yet, they were virtually absent before the activities and numbers of organisms became significant on a global biochemical basis. The reason for this tremendous biogeochemical processing is more or less obvious: the carbonate ion is oxidized carbon, the basic building block of living organisms. Through carbon dioxide, the basic respiratory product of most of Earth’s organisms, and the primary substrate for the building of biomass in photosynthesis, carbonate mineralization is directly linked to the core chemistry of living organisms. Furthermore, as we discussed in Chapter 8, carbon dioxide does not simply dissolve in water, remaining in its gaseous state (e.g. like nitrogen); it also reacts with water to develop a series of ions linked directly to the acidity/basicity of the aqueous environment, a key element in organism function. Finally, although there are other biological

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FIGURE 10.1 Generalized cell membranes showing pumping organelles and function. (A) Typical cell and membrane; (B) bicarbonate pumping; (C) sodium–potassium pumping. The ␣ and ␤ refer to the specific protein that form the pore (in channel) and with adenosine triphosphate (ATP) energy drive the pumping process. From Mathews and van Holde (1996). Reprinted by permission of Addison Wesley Longman.

carbonates, calcium is abundant in the Earth’s crust and oceans and forms several key crystalline minerals that, under the physical/chemical conditions at the surface of the Earth today, are approximately in equilibrium

with a saturated aqueous solution. Particularly in warm, tropical seas where the surface waters are highly supersaturated with calcium carbonate, calcification would be expected to happen massively sometimes

Halimeda: Photosynthesis-Induced Calcification

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incidentally to the normal functioning of many organisms and their ecosystems. Oolitic (aragonite) sands are abundant on shallow, tropical banks and can be important rock-formers where the environmental conditions are too extreme for corals and calcifying algae. While many attempts have been made to implicate algae (as cyanobacteria) directly in this process, the consensus today is that the warm, calciumsaturated, very high pH conditions of the water over these banks (probably due to phytoplankton) results in aragonite crystallization out of solution without direct biological control. Because an understanding of the calcium carbonate biomineralization process is crucial to the design and operation of many microcosms, mesocosms, and aquaria, we examine two key calcifying organisms of coral reefs: the green alga Halimeda and scleractinian, hermatypic corals in general. Halimeda calcifies almost incidentally to the photosynthesis processes. Stony corals have more direct biotic control over mineralization. However, they also rely not only on their internal symbiotic photosynthetic system with zooxanthellae but also on the reef community of algae in general to provide conditions that are favorable for competitive calcification. Adey (1998) reviews, in depth, the role of algae in coral reef calcification.

HALIMEDA: PHOTOSYNTHESISINDUCED CALCIFICATION Halimeda is a well-known tropical benthic genus of green algae. Fairly large, of centimeter to several decimeter dimensions, species of this genus consist of strings of flattened or sometimes crinkled, calcified discs connected by flexible joints. They are abundant in shallow seas around the tropics especially on “coral” reefs and in their lagoons, although some species range down reef drop-offs to great depths. During the 1950s when large numbers of deep boreholes were drilled into Pacific atolls, geologists found that the dominant element of the carbonate structure of these atolls was not stony coral but rather a lithified sand made up of the lobes of Halimeda. The members of this genus rank as one of the most important calcifiers of the biosphere; it is likely that their CaCO3 production over all tropical seas is considerably greater than that of the stony corals. Halimeda (Figure 10.2) is a member of the green algal order Siphonales and is further described in Chapter 14. In brief, anatomically, members of this genus are constructed of tubules, with very few cross walls. Thus, individual cells are extremely long and narrow. At the surface of the discs or lobes, the “bat-like” surface expression of these tubules (called utricles) is slightly

FIGURE 10.2 Halimeda favulosa, drawn from a 10-inch-high plant collected in the Bahamas. This green alga is constructed of filaments without cross walls (coenocytic). In the segments, the filaments branch and end in swelled-tip utricles that lay down a matrix of aragonite. Between the segments, the filaments are not calcified, giving the plant the flexibility and the capability of withstanding moderate water motion. From Taylor (1960).

swollen to form a continuous surface as a kind of cellular pavement. Just below the surface of the lobe, there are considerable spaces between the utricles (Figure 10.3). The calcification, mostly of aragonite needles, occurs almost entirely in these interutricular spaces. Thus, as we described above, through the anatomy of their utricles, these algae have provided one of the basic requirements for biomineralization, confined spaces in which critical supersaturation can occur. When a Halimeda disc is sectioned (some are soft enough to be cut with a razor blade), it is possible to see under a dissecting microscope that the chloroplasts are

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FIGURE 10.3 Movement of calcium and carbon dioxide and the carbonate cycle in the green alga Halimeda. The calcification is primarily extracellular and does not involve ion pumping by membranes. It is “incidental” to the process of photosynthesis as the small molecule of CO2 is “sucked” out of the interutricular spaces. Modified after Borowitzka (1989). Reprinted with permission of Springer-Verlag.

crowded into the outer parts of the utricles. Most of the cellular remainder of the lobes and joints is colorless or nearly so. Thus, when photosynthesis is proceeding rapidly, CO2 diffuses from the water immediately exterior to the plant and, particularly because this is the largest surface of each utricle, from the interutricular spaces. This strongly raises the pH and the concentration of carbonate ion (CO2⫺ 3 ) in the interutricular spaces. As long as calcium is available to diffuse through the porous cell wall from the exterior, calcium carbonate becomes highly supersaturated in these largely enclosed spaces. The cell membranes lining the utricular wall have macromolecules probably with attached exposed calcium ions that initiate aragonite crystal growth. Once started, with the elevated pH and elevated carbonate

environment, mineralization proceeds rapidly. A strong demonstration of this process can be provided by placing Halimeda discs in sea water buffered to a low pH. The discs will photosynthesize normally but will not calcify. Also, extracts of dead Halimeda utricles dropped into supersaturated but otherwise stable solutions of calcium carbonate will cause initiation and rapid growth of aragonite crystals. Readers interested in the details of this process can consult the article by Borowitzka (1989). An interesting question at this point is, Why is it that all tropical algae do not calcify as they rapidly photosynthesize in tropical sunlight? Many do, in fact, develop a coating of loose aragonite crystals. However, most lack the appropriate intercellular spaces, and the outer cortex where chloroplasts and photosynthesis are concentrated is densely packed with cells. In many cases, where apparently appropriate spaces are present, the initiating (or nucleating) molecules are not present. Finally, many species may even develop chemistry that is inhibitory to calcification. Calcification is only one strategy for life by tropical algae. Another, such as that used by algal turfs, is to grow and reproduce very rapidly. Grazing only removes the larger, slower growing competitors. In general, in shallow, warm, calcium carbonatesaturated tropical seas, algae induce considerable calcification simply as a result of photosynthesis. Some of this calcium carbonate (aragonite or calcite) does dissolve at night, as algal respiration releases CO2 taken up earlier in photosynthesis (algal biomass does not continually build up despite the high level of photosynthesis because of grazing and loss of fragments to lagoon and ocean). Eventually, much of the algal captured carbon, after being grazed, is respired by animals, but a good part of this released CO2 is removed up into the water column, above the algal surface, or off in the adjacent lagoon.

CALCIFICATION IN STONY CORALS Calcification in the stony corals is somewhat different from that in Halimeda, in that it occurs under the basal disc of each polyp. This biomineralization zone is well removed, on the scale of a millimeter to a centimeter, from the photosynthetic region occupied by the zooxanthellae, which is typically located in the upper part of the polyp. It seems highly unlikely that carbon dioxide removal and subsequent pH elevation is a direct driving force in coral calcification, although it is almost certainly an important factor. In recent years, models have been developed (Figure 10.4), particularly by McConnaughey (1989; 1995), that fit what is now known of the physiological

Calcification in Stony Corals

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FIGURE 10.4 Model of calcification in the generalized stony coral. The key elements for calcification are the pumping of calcium and hydrogen ions by the calcifying cells, the reaction of hydrogen ions with ambient bicarbonate, and the uptake of CO2 by zooxanthellae and external algae (see text for details).

performance of many stony corals rather closely. Unlike in Halimeda, it seems that membrane pumping of calcium ions to, and hydrogen ions from, the mostly enclosed spaces between the basal disc of the polyps and the aragonite skeleton is the key to control of calcification by the animal. The carbon dioxide molecules, being small and uncharged, diffuse through membranes and cells easily to the calcification site as a result of respiratory processes of the cells making up the base of the polyp. The removal of hydrogen ions greatly raises pH in the calcification area beneath the polyp, causing the equilibrium in the reaction between water and carbon dioxide to shift to dominance and supersaturation by carbonate ion (CO2⫺ 3 ). With calcium being pumped in, once aragonite crystallization has started, calcification occurs rapidly. Tissues having cells with membranes

bearing macromolecules with projecting and charged calcium ions are probably also a factor in initiating calcification and providing appropriate morphology. However, if hydrogen ions are pumped higher up in the polyps, in the process of raising pH against the aragonite skeleton, these ions begin to create an acidified zone. On the other hand, these ions react with the abundant bicarbonate ion in the water column and the gastroenteron of each polyp to produce CO2. As the equations show, for every one molecule of CO2 taken up and calcium carbonate laid down, two ions of bicarbonate are used and two molecules of CO2 are produced. Since the buildup of acidic conditions and excess carbon dioxide would soon slow the calcification process, if allowed to continue, the removal of carbon dioxide by the coral zooxanthellae (for photosynthesis) is critical

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FIGURE 10.5 Diurnal uptake of calcium and bicarbonate ions in a 130-gallon coral reef system, based on eight sets of data points, taken from 11/96 to 5/97. Note, concentrations are set high, as described in the text, to avoid depletion during a run. Note that removal of both ions is parallel, tending to decrease slightly in rate during the day. There is little or no uptake of the ions at night. See Figure 20.9 for diurnal pH values. These dictate a free carbon dioxide concentration ranging from roughly 2 mg/liter in the morning to 1 mg/liter late in the day.

to continued rapid calcification. While corals and other calcifiers do calcify in the dark, the rates are much slower than when the zooxanthellae are able to photosynthesize (Figure 10.5). Thus, calcification by the described process supports photosynthesis, providing the preferred low energy carbon substrate CO2, which is in very short supply under typical reef conditions of pH. Photosynthesis, in turn, supports calcification, locally removing the acidifying CO2 conditions that would soon greatly slow calcification. Thus, the symbiosis between the animal part of the coral and the zooxanthellae is far more than just an exchange of nutrients and CO2 for sugars; it is likely a key to the rapid calcification that is the dominating factor of life for many corals. Almost certainly species of different genera utilize these elements in a variety of ways (see Chapter 19). More recent work on dissolved inorganic carbon utilization by stony corals (Al-Moghrabi et al., 1996; Goiran et al., 1996) generally supports the model described above. While these articles demonstrate that under some conditions coral zooxanthellae can also directly uptake HCO⫺ 3 (rather than CO2), and this is likely true for algae in general (see Chapter 8), the overriding rule is that most corals, as well as all organisms, do not live in a laboratory flask; they live in a highly competitive world where efficiency matters. It may well be that

an algal cell can pump bicarbonate ion (which is highly abundant) and can provide enzymes to assist conversion to CO2 for use in photosynthesis. However, this requires energy. By symbiotically associating with the coral animal, the algae get CO2 (and nutrients in general) in some abundance at low energy cost. Likewise, corals (and most molluscs) could simply expend energy and pump the required ions to calcify, and indeed some genera lack zooxanthellae. However, genera that lack zooxanthellae calcify quite slowly. By associating with symbiotic algae, the corals receive not only some of the sugars produced by the algae, but also an enhanced production of calcium carbonate skeleta. On a global scale, this is seen in the massive calcium carbonate production of many reef corals, which far outweighs that of mollusc shells. On the ecosystem scale, the photosynthesis of freeliving algae in a coral reef community typically greatly exceeds that of the coral zooxanthellae. This is instrumental in driving the calcification rate of reef ecosystems, and is a critical element of the coral reef calcification process to which we return below (Adey, 1998). In the calcification model we have presented, bicarbonate and carbonate ions are removed in some quantity from the water column as substrate for the entire calcification process. At normal seawater pH, bicarbonate ion is abundant, and with the typical continuous input of oceanic seawater across wild, well-developed reefs, significant depletion of bicarbonate seems highly unlikely. On the other hand, the depletion of total alkalinity across calcifying reefs has been determined and has been used as a direct measure of total calcification (see e.g. Kinsey, 1978; Smith, 1978; Barnes and Devereaux, 1984). Alkalinity depletion (principally as bicarbonate and carbonate) in closed or semiclosed systems thus can be an issue in depressing stony coral calcification, as we discuss in some depth below.

CALCIFICATION, STONY CORALS, CORAL REEFS, AND GLOBAL WARMING Considerable discussion has centered around the growth of stony corals in reef aquaria. Much of it, unfortunately, is unrelated to the reality of calcium carbonate construction in wild ecosystems. While there is certainly some value in centering attention on the tip rate of extension of scleractinian corals in culture systems (Chapter 24), and we discuss these matters below and in Chapter 20, the principal purpose of this book is to develop the parameters for the creation of model reefs and other ecosystems. Thus, some discussion of the larger-scale process, that is, bioherm or coral reef formation, in general, is necessary.

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Calcification, Stony Corals, Coral Reefs, and Global Warming

TABLE 10.2 Net Calcification Rates for Various Coral Reef Communities Location Houtman Abrolhos Island Johnston Atoll Central Kaneohe Bay Rangiroa Atoll Johnston Atoll One Tree Island Johnston Atoll One Tree Island Enewetak Atoll Enewetak Atoll Lizard Island Lizard Island Kaneohe Bay Enewetak Atoll Tulear Barrier Reef Johnston Atoll One Tree Island

Biotopes or communities

Rate (kg CaCO3/m2/year)

Coral bank Back reef, heavy coral Coral zone Encrusting coralline pavement Lagoon, heavy coral cover Reef flat, coral zone Coral/algal pavement Algal pavement Reef flat, coral/algal community Reef flat, algal turf Lagoon reef flat Seaward reef flat Coral/algal ocean reef Windward fore reef Coral/algal reef flat Lagoon, reticulated reefs Reef flat, sand/rubble

12 9.6 8.8 7.5 6.4 4.6 4.4 4.0 4 4 3.1 2.7 2.6 1–2 1.9 1.5 0.4

Note. All results obtained by alkalinity depression. Modified from Pichon (1996).

There are many kinds of tropical, calcium carbonate reef structures or bioherms (Adey, 1978). Some are created primarily by calcifying algae (algal ridges, corallines, atolls, Halimeda). Even nonalgal bioherms, mostly coral reefs, are not areally or physiologically dominated by stony corals (Adey and Steneck, 1985; Kinsey, 1992). Stony corals play an important role in the construction of many reefs by forming an aragonitic framework, the interstices of which are then filled by the activities of other calcifying organisms. As we mentioned above, Halimeda (a green alga) is probably the most important bulk calcifier in reefs worldwide, although coralline red algae, other calcifying greens, molluscs, foraminifera, and numerous other invertebrate groups are significant contributors. Extensive investigations of average calcification rates in coral reefs in the Indo-Pacific (based on alkalinity depletion) have shown that while calcium carbonate accretion rates at reef surfaces can range up to 12 kg/m2/year in some isolated reef segments, mean rates for whole reefs are closer to 1.5 kg/m2/year (Table 10.2). This amounts to a mean whole reef accretion rate of less than 1 mm/year, with a maximum local rate of about 7 mm/year. Yet, in the Caribbean, rates of reef accretion over the past 5000 years as documented by extensive drilling have exceeded 10 mm/year (Adey, 1978; MacIntyre, 1988). The latter situations were so-called bank barrier reefs with extensive Acropora frameworks, but in situations where currents probably were able to maximize the framework infill from broader carbonate banks. The growth rates of coral surfaces and branches (Table 10.3) provide an entirely different perspective.

Some very rapidly growing branching species (Acropora spp.) range up to almost 19 mm/month of tip extension, although the average rate is closer to 10–11 mm/month. If these values are placed in the context of branch cross section, this would be the equivalent of about 0.1 mean (0.2 max) mm/month, less than the rate of accretion of the massive species, 0.8 mean (1.6 max) mm/month. If an entire reef surface were to be made of coral growing at the known mean rates, yearly accretion would be less than 1.0 mm/year. Thus, stony coral accretion could nearly account for whole reef calcification, but since stony corals account for only about 20% of reef surfaces (Adey, 1998; Kinsey, 1992) then numerous other calcifiers must be producing infill carbonate at about the same rate as the stony corals. As we discuss at some length in Chapter 20, species diversity per unit area is higher in coral reefs in general than in any other biological community on Earth (including rain forests). A major factor in this diversity is the spatial heterogeneity or surface complexity created primarily by branching stony corals. Thus, while corals cannot be responsible for more than about 20–30% of total reef calcification (and primary production, see Chapters 5 and 20), they are primarily responsible for the framework and multiplicity of surfaces that give rise to high diversity. As is clear from the above discussion of the calcium carbonate deposition process, and that in Chapter 8, concerning CO2 and pH, there is a strong link between calcification and pH. The calcification process in part results from CO2 removal and pH elevation. While, in general, calcification is driven by photosynthetic activity and energy-driven ion pumping, these processes

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TABLE 10.3 Growth Rates of Scleractinian Corals in Coral Reef Communities Species

Location

Growth rate (cm/year)

Method

Massive species Porites lobata Porites lutea Porites lutea Porites lutea Favia speciosa Favia speciosa Favites flexuosa Montastrea annularis Montastrea annularis Montastrea annularis Montastrea annularis Montastrea annularis

Great Barrier Reef Enewetak Enewetak Enewetak Enewetak Moreton Bay Bikini Barbados Jamaica St. Croix Florida Florida

0.4–0.9 1.35 0.3–1.2 0.9–1.2 0.5 0.6 0.8 1.9 0.2–0.7 0.7–0.9 0.9–1.3 1.7

X-radiography X-radiography X-radiography X-radiography X-radiography X-radiography X-radiography Real time Real time (alizarin) Real time (alizarin) Real time (alizarin) X-radiography

Digitate species Pocillopora damicornis Pocillopora damicornis Pocillopora damicornis Pocillopora damicornis

Hawaii Panama Samoa Great Barrier Reef

0.9–1.5 3.9 2.3 2.5

Real time (alizarin) Real time (alizarin) Real time Real time

Brancing species Acropora palmata Acropora palmata Acropora cervicornis Acropora cervicornis Acropora pulchra Acropora pulchra Acropora formosa Acropora formosa Acropora formosa

Curacao St. Croix Barbados Barbados and St. Croix Philippines Carolines Samoa Great Barrier Reef Phuket

8.8 5.9–10.1 14.4 10.0 18.1 22.6 18.5 8.0–16.6 8.5

Real time Real time (alizarin) Real time Real time Real time Real time Real time Real time Real time

Note. Modified from Pichon (1996).

effectively work against a pH gradient. The human release of CO2 into the atmosphere is resulting in global warming, which in itself is a danger to coral reefs. However, 30–50% of this released CO2 is going into the ocean and has resulted in an average reduction of oceanic pH by 0.1 units. This may be very small, but if CO2 release continues, by the end of the century it is likely to be on the order of 0.4 units (Kleypas et al., 1999; Tedesco et al., 2005). This will certainly reduce calcification in the oceans in general and cause significant changes in community structure, especially in those parts of the open ocean where coccolithophores are dominant. However, in coral reefs, where community existence is connected to calcification, the results could be disastrous indeed. As we describe in Chapter 25, using the techniques and understanding provided in this book, major steps can be taking to help stop this process, reverse CO2 accumulation, thus hopefully providing one of the key elements to restoring coral reef ecosystems worldwide. However, this problem is much larger than ecosystem restoration since it involves a global change in the methodology of human energy acquisition.

CALCIFICATION IN MESOCOSMS AND AQUARIA Unless a specific and massive export mechanism is present in a semiclosed aquatic mesocosm or aquarium used to simulate a wild ecosystem, it is unlikely that any biomineralization, except for calcium carbonate, will be limited by lack of the necessary ions. In Chapter 9, we briefly discussed a case where diatoms were routinely harvested and removed from the glass walls of a large reef microcosm for many years. Eventually, silicon depletion resulted. However, this is the exception that proves the rule. Even in the case of calcium carbonate (or calcium phosphate), as long as an appropriate mineral substrate, such as an oolite, for a reef system, or a shelly sand, for a cold water rocky shore or an estuary, is present, limitation by lack of the appropriate calcification ions for teeth, bone, or shells, in a system with a reasonable community structure, has not been demonstrated. On the other hand, coral reef systems provide a special case in which alkalinity and/or calcium limitation is not only possible but quite likely if such a system

Coral Reef Aquaria and Stony Coral Calcification

includes abundant coral reef calcifiers, including stony corals, and is performing at optimum levels. Some authors have concluded that we do not know enough about coral reef metabolism to rationally build effective living system models (Atkinson and Falter, 2003). Surely we have much to learn about calcification in coral reefs, especially with regard to variation among species and between reefs. However, as we shall describe below, and in greater depth in Chapter 20, the knowledge of coral reef calcification accumulated, especially in the last 20 years, allows us to achieve a truly remarkable veracity in closed system modeling of coral reefs.

CORAL REEF AQUARIA AND STONY CORAL CALCIFICATION The authors have operated a 130-gallon coral reef ecosystem for 10 years with a diverse assemblage of stony corals, calcareous algae (Halimeda (Color Plate 13) and corallines), molluscs, molting crustaceans, and calcifying worms (see Chapter 20 for an extensive description). For the first 8 of that 10 years, other than the presence of an oolite (aragonitic) sand in the base of the system, a small organic throughput (passed through to harvested algal turf) and a less than 5% per month water change (to avoid salt drift), no specific calcium or alkalinity additions were made. Corallines and Halimeda grew abundantly in this system. Also, throughout this 8-year period, several genera of stony corals reproduced sexually, a Tridacna clam introduced in the 2nd year grew from about 5 cm in length to nearly 30 cm, and a rare reef lobster, introduced early in the 2nd year, continued to molt regularly. None of this activity suggests any significant limitation for calcium, carbonate, or phosphate ions. As described by Small and Adey (2001), the stony corals in this microcosm had a pattern of growth that was apparently limiting for some species and genera and not for others (Color Plates 2, 13–15, and 18). Clearly, stony coral survival, whether in the wild or in a model, is dependent in part on the balancing of predation and other damage against growth. A rapidly growing individual coral colony may or may not add significant biomass over time. It is clear that in a wild reef as a whole, unless it is a very young reef or one recovering from significant damage, such as a hurricane, continuous addition of biomass cannot occur. Thus, while “growth” over time occurs as calcification, equivalent biomass increase cannot occur. In some ways many forest trees are similar. After reaching maturity only a small amount of active photosynthesizing, reproductive, or transport tissue is added. For the majority of its life, the tree adds major biomass as cellulose (the

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equivalent of carbonate) but little active tissue. Unlike trees, coral colonies show an even starker contrast because they almost always show tissue die-back at the base or sides, depending on morphology, while the tips or upper surfaces continue to grow. For any given coral colony, if it is “growing” well, that is, adding carbonate, survival against continual predation and competition with other corals, colonial invertebrates, and algae is greatly enhanced. As described by Luckett et al. (1996), growth rates of Porites and Dichocoenia in the model system under discussion were typically 1–2 mm/month, appreciable but not maximal. Other genera remained healthy for the entire period of time, but did not grow significantly (e.g. Diploria spp.). Species of a few genera (e.g. Mussa sp.) slowly shrank and eventually died. During the period under discussion, calcium concentration in the 130-gallon coral reef microcosm remained at a mean level of 380–390 mg/liter. On the other hand, as measured at the end of the period, alkalinity had reduced from the normal level of 2.3–2.5 to about 1.6 meq/liter. During the 9th year, the concentration of calcium in the system was kept at about 420 mg/liter using kalkwasser. No effort was made to adjust alkalinity. During the 10th year, the effects of maintaining calcium concentration at about 7% over normal at 450 mg/ liter were examined (using the neutralized supernatant of acidified oolite), and alkalinity was experimentally maintained at 2.6 meq/liter using potassium or sodium bicarbonate. Additional coral colonies of Indo-Pacific Acropora and Montipora, mounted on plastic cups, were added to the system to provide a comparison with information from Pacific reefs. As shown in Figure 10.6, growth rates were considerably higher than those found in earlier studies. Over many months, total calcification rates of this reef community, based on both calcium and bicarbonate removal (which are approximately equal), ranged from 5 to 7 kg/m2/year of calcium carbonate. This is considerably higher than the mean rate for Indo-Pacific reefs of 1.2 kg CaCO3/m2/year noted above and falls within the range of about the upper 2% of tabulated reef surfaces (Pichon, 1996). Thus, this reef microcosm is operating on the high side for calcification. This is not due to the elevated calcium and bicarbonate concentrations, as demonstrated by Small and Adey (2001). Only part of this total system calcification is due to corals, Halimeda, and coralline algal and molluscs also being present (Color Plates 12, 18, 19, and 22). However, the stony corals occupy 15–20% of the surface of this model reef, about average for wild systems. When individual coral colonies are separated into closed chambers for short periods their uptake rates are such as to provide for the total level of calcification in the

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FIGURE 10.6 Growth of the stony coral Porites astreoides in the 130-gallon reef system from the time of its larval settlement in late 1992 or early 1993 until present. Note that this coral has a head morphology, typically being hemispherical at maturity; thus, mean diameter represents only a small part of total calcification. Prior to mid-1994, growth was moderate based on only aragonite addition and resulting in slightly depressed calcium concentrations (see text). The addition of trace elements and Ca(OH)2 apparently gradually caused a reduction in growth rate, perhaps due to elevated strontium levels (to 14 mg/liter) and interference with calcification. The removal of all trace element additions and the management of calcium and total alkalinity approximately 5–15% above seawater concentrations greatly increased growth rate.

entire system at 100% coverage (Color Plates 13–15). This is very much in agreement with the information presented above and from many sources for wild reefs. If pieces of reef carbonate with their typical surface coverage of algal turf are placed in a similar closed chamber, significant alkalinity depletion (and therefore calcification) occurs. This is not of the magnitude of stony corals or Halimeda (it is about 50% of whole system levels), but it is certainly significant. While some of this background calcification is due to small invertebrates and corallines, much of it results from precipitation in small cavities (micritization), due to removal of CO2 by the highly productive algal turf. A purist aquarist operating a coral microcosm as a closed system might be concerned about the “artificial” need to add alkalinity as bicarbonate. However, in a wild reef this alkalinity is “sucked out” of overflowing ocean waters. Most of the alkalinity is emplaced in those ocean waters far from the reef in localized deep anaerobic waters (such as the Black Sea). To repeat a general

principle, no ecosystem stands alone. Matching inputs with exports is a key to operating microcosms and mesocosms of those ecosystems. In this case, input of alkalinity as sodium or potassium bicarbonate matches that input in the wild ecosystem. In a coral reef microcosm or mesocosm with moderate stony coral coverage and minimum predation, calcium depletion can be prevented by the daily addition of fresh oolitic (aragonitic) sand. Where extensive coverage of calcifiers, including stony corals, and/or excessive coral predation is present, or if rapid growth rates are desired, oolitic sand can be dissolved with reagentgrade hydrochloric acid (HCl), to provide a calciumrich additive. The supernatant of this process should be allowed to nearly neutralize (pH 6.5–6.7) with excess oolite, and should have a concentration of about 30 000 mg/liter. Sufficient supernatant can be added daily to a model system to balance out the calcification that is occurring. This process is equivalent to open ocean input in the wild, where coral colonies remove calcium from overflowing waters to build their structures. The same basic process applies to alkalinity. Wild reefs are scrubbers of carbonate from overflowing ocean waters, as many studies have shown. The addition of bicarbonate provides a process that is close to that working in wild reefs. Unfortunately, that addition must come with a cation. Either sodium or potassium bicarbonate will suffice, but the sodium will have less longterm effect on the water chemistry. The combination of HCl/oolite and NaHCO3 that we have described will add excess sodium chloride to a system. Since these are the most abundant ions in sea water, the effects are likely minimal. For a typical microcosm or mesocosm, waterexchange rates of about 12% per month will keep NaCl concentration at less than 10% over normal. This exchange rate will prevent the drift of conservative salts due to evaporative losses (see Chapter 4). An appropriately designed sea salt mix could greatly reduce the magnitude of exchange water required. Recent research (Small and Adey, 2001) using the 130-gallon aquarium microcosm described in detail in Chapter 20, has shown the McConnaughey (1995) model of bicarbonate uptake and calcification by stony corals to be correct. Thus, removal of the CO2 produced by coral calcification is critical to efficient continued calcification. That same research has shown that, at least in the fastest of reef calcifiers (Acropora), colony zooxanthellae are unable to keep up with CO2 production and that the presence of enough free-living algae to raise pH to the typical daytime levels of reef ecosystems increases coral calcification by over 60% (Figure 10.7). Thus, the optimally calcifying coral reef ecosystem is one in which algae occupy 50–75% of the surface. Similarly, with at least 25% of the surface occupied by calcifying

Coral Reef Aquaria and Stony Coral Calcification

FIGURE 10.7 The effects of free-living, independent algae on coral calcification as indicated by pH, oxygen, and alkalinity depletion in test chamber subsets of a coral reef microcosm. (A, B) The corals alone have little effect on pH during a day run showing the compensation of calcification for photosynthesis, while coral and Chondria (free-living) and Chondria alone rapidly elevate pH; (C, D) Photosynthesis, as demonstrated by O2 release, occurs in all combinations, but is minimal in coral-alone runs; (E, F) Chondria alone does not show alkalinity depletion (thus no calcification); coral samples alone show alkalinity depletion (thus calcification); the combination of corals and free-living, noncalcifying algae provides maximum alkalinity depletion and thus calcification. From Small and Adey (2001).

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FIGURE 10.8 Daytime carbonate and pH cycle in entire coral reef microcosm. Bicarbonate provides virtually all alkalinity depletion. The mean daily rate of calcification in this microcosm is about 8 g/day, or 4.0 kg/m3/year, in the range of the top 2-4% of worldwide coral reefs.

corals, algal production is not likely to be limited by lack of CO2. As Adey (1998) has shown, reef ecosystems optimize both calcification (reef construction) and photosynthesis (primary production) through the mutual interaction of corals and algae at many different scales. This process is shown for a whole microcosm in Figure 10.8.

References Adey, W. (1978) Coral reef morphogenesis: a multidimensional model. Science 202: 831–837. Adey, W. (1998) Coral reefs: algal structured and mediated ecosystems in shallow turbulent waters. J. Phyc. 34: 135–148. Adey, W. and Steneck, R. (1985) Highly productive eastern Caribbean reefs: synergistic effects of biological, chemical, physical and geological factors. In: The Ecology of Coral Reefs. M. Reaka (Ed.). NOAA Symposium Series on Undersea Research, Vol. 3. Washington, DC. Al-Moghrabi, S., Goiran, C., Allemand, D., Speziale, N., and Jaubert, J. (1996) Inorganic carbon uptake for photosynthesis by the symbiotic coral/dinoflagellate association. II. Mechanisms for bicarbonate uptake. J. Exp. Mar. Biol. Ecol. 199: 227–248.

Atkinson, M. and Falter, J. (2003) Coral reefs. In: Biogeochemistry of Marine Systems. K. Black, and G. Shimmield (Eds). Blackwell Publishing and CRC Press, Oxford. Barnes, D. and Devereaux, M. (1984) Productivity and calcification on a coral reef; a survey using pH and oxygen electrode techniques. J. Exp. Mar. Biol. Ecol. 79: 213–231. Borowitzka, M. (1989) Carbonate calcification in algae – initiation and control. In: Biomineralization. S. Mann, J. Webb, and R. Williams (Eds). Springer-Verlag, New York. Goiran, C., Al-Moghrabi, S., Allenmand, D., and Jaubert, J. (1996) Inorganic carbon uptake for photosynthesis by the symbiotic coral/dinoflagellate association. I. Photosynthetic performances of symbionts and dependence on sea water bicarbonate. J. Exp. Mar. Biol. Ecol. 199: 207–225. Heldt, W. (2005) Plant Biochemistry, 3rd edn. Elsevier, Amsterdam. Kinsey, D. (1978) Alkalinity changes and coral reef calcification. Limnol. Oceanogr. 23: 989–991. Kinsey, D. (1992) Foreword. In: The Turf Algal Flora of the Great Barrier Reef. I. Price and F. Scott (Eds). James Cook University, Townsville, Australia. Kleypas, J., Buddemeir, R., Archer, D., Gattuso, J.-P., Lungdon, C., and Opdyke, B. (1999) Geochemical consequences of increased atmospheric carbon dioxide on coral reefs. Science 284: 118–120. Knoll, A. H. (2003) Biomineralization and evolutionary history. Rev. Mineralogy and Geochemistry 54(11): 329–356. Luckett, C., Adey, W., Morrissey, J., and Spoon, D. (1996) Coral reef mesocosms and microcosms – successes, problems and the future of laboratory models. Ecol. Eng. 6: 57–72. MacIntyre, I. (1988) Modern coral reefs of the Western Atlantic: new geological respectives. Bull. Am. Ass. Petrol. Geol. 72: 1360–1369. Mathews, C. and van Holde, K. (1996) Biochemistry, 2nd edn. Benjamin/ Cummings, Menlo Park, California. McConnaughey, T. (1989) Biomineralization mechanisms. In: Origin, Evolution and Modern Aspects of Biomineralization in Plants and Animals, R. Crick (Ed.). Plenum Press, New York. McConnaughey, T. (1995) Ion transport and the generation of biomineral supersaturation. Bull. l’Instit. Ocean. Monaco 14(spec.): 1–18. Pichon, M. (1996) Coral reef ecosystems. In: Encyclopedia of Environmental Biology, Vol. I. W. A. Nierenberg (Ed.). Academic Press, San Diego. Simkiss and Wilbur (1989) Biomineralization. Academic Press, San Diego, California. Small, A. and Adey, W. (2001) Reef corals, zooxanthellae and freeliving algae: a microcosm study that demonstrates synergy between calcification and primary production. Ecol. Eng. 16: 443–447. Smith, S. (1978) Alkalinity depletion to estimate the calcification of coral reefs in flowing waters. In: Coral Reefs Research Methods. D. Stoddard and R. Johannes (Eds). UNESCO, Paris. Taylor, W. R. (1960) Marine Algae of the Eastern Tropical and Subtropical Coasts of the Americas. University of Michigan Press, Ann Arbor, Michigan. Tedesco, K., Feely, R., Sabine, C., and Cosca, C. (2005) Impacts of anthropogenic CO2 on ocean chemistry and biology. NOAA Research Web site http://www.oar.noaa.gov/spotlite/spot_gcc.html

C H A P T E R

11 Control of the Biochemical Environment Filters, Bacteria, and the Algal Turf Scrubber

As a beginning to the modeling and restoring of aquatic ecosystems, in the first set of chapters in this book, we have introduced the role of physical/chemical factors “allowing” life to develop, and in circumscribing the biosphere and its ecosystems. We have also repeatedly emphasized that organism metabolism, since the dawn of life, has radically altered the Earth’s chemical and physical environment. The biosphere today is quite stable, as compared to that in the early eons following the origin of life, and no doubt in the eras following major meteorite or comet impacts. Nevertheless, many species have the potential to quickly develop population explosions, significantly disrupting their environments, even to the extent of multiple population crashes and ecosystem death. The balance of nature generally refers to limits placed on population explosion, and therefore chemical disruption, by resource limitations. As we will discuss in later chapters, the balance can also be in food webs. In the ecosystem context, the nutrients (N, P, C, Fe, etc.) that provide that limitation have long ago been locked up, in the Earth or the deep ocean, providing a natural brake, albeit with fluctuations. In modeling and restoring ecosystems, and in building a display aquarium, we constantly deal with that basic balance between environmental chemistry and organic potential. In this chapter, we entertain the question of how to solve the chemical problems created by placing an ecosystem in an enclosure, whether an aquarium or larger mesocosm, thereby separating it from its normal “sink” for nutrients. Also, when display is contemplated, how do we counteract the effect of purposeful overstocking? Later, in Chapters 24 and 25, we approach the issues of mass culture of organisms for food, pharmaceutical

drugs, and recreation, when disruption of adjacent wild environments (or human environments) will result from the organism concentration that culture requires. The larger human issue of disruption of environments by the concentration of people is different mostly as a matter of scale. In concentrating a human population in a city, and then delivering a steady stream of food with its nutrients to that city, the local stream or river becomes the sink, usually with disastrous consequences. The “nutrient” carbon is a little different in that it goes into the atmosphere as CO2 (even if a sewage plant is added to the loop). As we discussed in Chapter 8, excess CO2 in water environments drives down pH and can be a significant negative factor for many species. However, as long as it was only food that we were dealing with in this context, carbon mattered little, it was mostly cycled through the atmosphere to plants and algae outside the city and in the oceans. However, once the carbon began to be released en masse from geologically stored hydrocarbons, to provide additional energy (beyond food energy) for human heat and transportation, and this release became in excess of the capabilities of the biosphere’s photosynthesizers to take it up and restore it, it began to build up in the atmosphere. This CO2 buildup is causing the Earth to retain more solar heat, with the potentially disastrous consequences that we label as global warming. Thus, while technically CO2 is a nutrient, and indeed can affect plant growth, its uncontrolled release is detrimental to the Earth’s ecosystems and the human race in a global environmental context. In ecosystem modeling, in aquaria, and in organism aquaculture systems, as well as in sewage plants, we

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may well get away with releasing carbon into the atmosphere, but if we do not soon deal with the need to keep it out of the atmosphere, in general, the consequences to the human race will be significant indeed. In microcosm and mesocosm simulations of wild ecosystems, the aquarist is recreating the physical and biological characteristics of the wild ecosystem. In an accurate simulation, filtration or chemical control should be involved only to provide the effects of the missing, larger body of water or, possibly, adjacent ecosystem. Sometimes, when a mesocosm is located adjacent to such a body of water, this can be done simply by pumping or otherwise exchanging with the existing ocean or lake. Some of the most successful public aquaria, such as the Monterey Bay and Waikiki Beach Aquariums, use this approach. Otherwise “filtration” or other control is necessary. The small aquarium situation is generally similar, but the problem is more acute for a variety of reasons: (1) even smaller size, (2) often inaccurate environmental simulation, and (3) the tendency to exaggerate biomass, particularly large animal biomass, for reasons of display. In this chapter we briefly review the current methods of handling excess biomass nutrients and oxygen loss, primarily those that rely on microbe management. We also discuss several recent variations on the traditional approaches as well as higher plant and algal methods of solving the broader issues of nutrient and metabolite recycling, export, and control. Some bottom communities remove chemical elements from overflowing waters. However, typically these are equivalently exported as biomass. Coral reefs are unusual in that they remove calcium and carbonate in large quantities from overflowing waters and deposit them over long periods of time as calcium carbonate in situ, beneath the living veneer. Particularly in this situation, and perhaps in other ecosystem simulations that might be attempted, a means of inputting the lockedup element or ion at the appropriate rate must be developed.

STERILIZATION METHODS An approach often used to keep fish and a relatively few invertebrates in culture is the sterile or “hospital” approach. These methods rely on chemicals, treatments including ozone sterilization, and physical processes such as ultraviolet sterilization. At least for ultraviolet light, it might be argued that these short wavelengths are present in solar radiation, where they have considerable controlling effects. However, when using gas lamps, especially metal halides, for aquatic modeling, radiation roughly equivalent to that in the wild is already present. Certainly using ultraviolet filters is moving

towards sterilization of the water column. Both ozonation and ultraviolet “filtration” are equivalent to greenhouse culture in which a few species are maintained and others are killed using insecticides and herbicides or constant weeding. Such sterile approaches manage only a relatively few species and they are inherently unstable, requiring constant attention to avoid “pests” and environmental collapse. Delbeek and Sprung (2005) provide an excellent discussion of some of the innumerable, chemical treatments available for managing water quality, including GAC (granulated activated carbon). As they point out, one can balance out the negative and positive effects of many chemical treatments, including those for removing phosphorus, by suspending the absorbing media (usually granules) in porous bags near a system water intake to avoid the general “filtration” effects, but careful monitoring is still necessary to avoid chemical imbalances. It is the view of the authors that equivalent methods applied to an ever-increasing area of our biosphere for farming and landscape “beautification,” combined with habitat destruction in cities and industrial zones, are leading to a significant reduction of the ability of the biosphere to support higher animals, including man. Such “hightech” methods, when applied at large scale, as we note in Chapter 25, appear to merely slow degradation, and often lead to totally unanticipated effects.

BACTERIOLOGICAL FILTRATION In the first edition of this book, we reviewed the status of bacteriological filtration in aquarium systems. Spotte (1992), in Captive Sea Water Fishes, had provided an excellent review of the subject. Delbeek and Sprung (2005) bring that discussion up to date. Although bacteriological filtration has been widely used for many wastewater situations and for some heavily loaded aquaculture applications, we feel that its use should be re-evaluated and increasingly restricted. It has only limited use for water quality control in the modeling of ecosystems. Therefore, we refer the interested reader to the above literature and note that Chapters 6 and 22 include sections on the aufwuchs community, the closest ecological equivalent to the bacteriological filter in most ecosystems. Some researchers have argued that there is natural ocean filtration along the Earth’s ocean ridge system. As we noted in Chapter 3, sea water is circulated through cracks along the rifts of sea floor spreading centers. It has been estimated that the entire ocean is overturned in 7–10 million years in this process, as the sea water is heated, its composition is changed, and then it is released in “hot springs” or smokers. Sulfides and other

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Denitrification

mineral deposits are formed on release and interesting chemosynthetic communities of organisms are developed. However, this “filtration” relates primarily to very long-term effects on the conservative elements of sea water, not on the organic or nutrient components. A seven- to ten-million-year turnover is six to seven orders of magnitude too great to affect organism populations. Finally, there are some scientists and engineers that seek to use the bacterial breakdown of sewage and other waste for the direct extraction of electrical energy. Even if this can be developed as an economic tool, as long as nutrients are released to the water column, and CO2 to the atmosphere, the negative side effects of bacterial breakdown will be too great for widespread use. There is more solar energy incoming to planet Earth than we can ever use. Nutrients should be used only to directly and immediately extract solar power and then should be locked up (i.e. stored as plant or algal biomass). In the end, nutrients (including carbon) should be treated as radiation in atomic power, a dangerous by-product not to be released into the environment.

REEF SYSTEMS Beginning in the 1980s a variety of improvements to aquarium standard filtration methods were introduced (Delbeek and Sprung, 1994; Borneman, 2004). Generally, these methods (“reef systems”) increased water flow, aeration, and light, and somewhat reduced dissolved nitrogen concentrations (Figure 11.1). Reef systems have been partly successful in keeping invertebrates, particularly some corals, that previously could not survive in aquaria, although fish loadings must remain minimal. Since many of the invertebrates typically kept in these systems have zooxanthellae algae in their tissues, they are effectively high plant biomass cultures requiring relatively high light intensities. Although reef systems have been a major advance for keeping many invertebrates, and, in some cases of tight water quality control, considerable coral growth has been achieved, reef systems still fall well short of many basic requirements for maintaining aquatic ecosystems. Another similar variant of the bacteriological filter is the rotating drum or screen unit, which provides the bacterial or aufwuchs surface in and out of the water (for aeration) without providing physical filtration of plankton. In this respect, it is similar to the trickle filter of reef systems, though it requires a relatively large space. Although widely used in aquaculture, where space is not so constricting, it is rarely used for aquarium control purposes.

FIGURE 11.1 General layout of modern “reef” system. Not shown is the typically used trickle bed through a calcium carbonate gravel. After Moe (1989).

DENITRIFICATION Beginning in the early 1990s, a new addition to the array of biological (bacterial) filter systems was devised that also included a bacterial denitrification unit. Bacterial denitrification, particularly under anaerobic conditions, is quite capable of removing nitrogen to the atmosphere, and in any ecosystem, microcosm, or aquarium with anaerobic or near anaerobic sediments, this process will be active. Also, unlike CO2, there is no harm in releasing nitrogen to the atmosphere as N2, the gaseous form, as it is highly unreactive. However, at the nutrient levels of most natural situations, denitrification rates are at least an order of magnitude below nitrogen removal in photosynthesis (see Seitzinger, 1988; also see Chapter 9). Standard reef aquarium methods now in use can reduce dissolved nitrogen to less than 1 ppm (Moe,

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1989; Smith and Schuman, 1991). However, this is about 70 µM N, far above that of most natural aquatic ecosystems. Denitrification as a partial process can also lead to chemical inbalances, since only nitrogen is removed. A separate process can then be used to remove phosphorus, but then what about iron or sulfur buildup especially if sulfur is used to enhance denitrification?

FOAM FRACTIONATION (PROTEIN SKIMMING) Foam fractionation, or protein skimming as it is often called in the aquarium industry, uses a stream of bubbles in a wide variety of tower types, some rather elaborate and proprietary, to capture large organic molecules (dissolved organic carbon, DOC) and particulates on bubble films. As an export device for dissolved organics and particulates (and therefore to some degree nutrients), the process has considerable capability. The efficiency of the process has been considerably enhanced in recent years by the addition of sugar formulations or alcohol substrates including vodka, to increase planktonic bacteria production. This can produce cloudiness and instability. More importantly, foam fractionation cannot differentiate between the organics of interest and plankters, reproductive larvae, the food of these organisms, and attached and infaunal filter feeders. While some foam fractionation does occur in some shallow water shore situations, mostly due to wave action, it is a very minor element in most aquatic ecosystems. It would be difficult to model most ecosystems using foam fractionation though the process certainly has uses in some high-density aquaculture situations. Delbeek and Sprung (2005) provide a review of skimmer practice for coral reef aquaria.

PHOTOSYNTHETIC METHODS Photosynthetic organisms, including higher plants as well as marine and freshwater algae, require quantities of nitrogen to build their tissues. Ammonia, nitrite, nitrate, amino acids, and even urea and related compounds are sources of nitrogen for many algae (DeBoer, 1981). Phosphorus is generally taken up by plants as phosphate, though in some cases organic compounds may also be useful to some algae. Algae absorb these substances from the surrounding water, effectively removing them from the environment by locking them in their tissues. Carbon also is required for photosynthesis, and is used to build storage sugars and eventually a wide variety of tissues in plants. It is removed from the water column as carbon dioxide, and at least for many

algae, when that gas is limited, also as bicarbonate ion. Through plant metabolism, these animal wastes become converted to forms that once again can be utilized as food by other animals. Algal metabolism also produces oxygen and a variety of essential vitamins that animals and bacteria alone generally cannot manufacture. A variety of techniques that utilize these attributes of the algae as well as those of their higher plant, freshwater, and marine cousins have been developed. These photosynthesis-based techniques simulate the high water quality of the missing noneutrophic larger body of water when ecosystem modeling in microcosms and mesocosms. They also close the gaps in the natural recycling of organic compounds within a closed aquarium system. Although the concept of employing algae for aquarium water conditioning is not new (see Honn and Chavin, 1975; Spotte, 1979), it was rarely used to any great extent prior to 1985 and certainly had not been developed to its full potential. Encouraging microscopic plant growth within aquaria has become standard practice in recent decades. “Live rock” is primarily a fragment of rock or dead coral with its algal or plant growth included. In some cases, to increase the beneficial effects of algal growth, special culture trays containing stands of larger algae are connected in line with other filtration and purification equipment (Figure 11.2). One of the supposed negative side effects of algae was its “leaky” nature, that is, its tendency to release organic compounds into the water column. To some extent these objections may apply to some of the larger macroalgae. However, many algae, and protists in general, also have the capability of extracting dissolved organics from the water. The use of attached microalgae as a water quality control system has, however, become well known in the last decade, although for many practitioners of the art it remains an “exotic” process. For most aquatic ecosystem restoration, the first question should be: Is the system eutrophic and/or hypoxic? Except for offshore waters, unpopulated coasts without significant rivers and remote mountain streams and lakes, the answer is likely to be: Yes, but is that the dominant degrading factor? In some cases, restoration of plant communities, including marshes and SAVs, can provide a relatively straightforward amelioration of the problem. In other cases, silt loading from land-based development might have to be reduced along with plant community re-establishment. In most cases, involving extensive farming in the watershed or city sewage load, the problems are far beyond natural photosynthetic potential. Often, even when sewage plants have been repeatedly upgraded, and BMPs applied to farming, eutrophic or hypereutrophic conditions remain. The logical answer

Algal Turfs

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FIGURE 11.2 Use of macroalgae for aquarium water conditioning. After Spotte (1979). Reprinted by permission of John Wiley & Sons, Inc.

is: How can extensive photosynthesis be added to the process?

ALGAL TURFS The concept of using turf algae to purify water for microcosm research was conceived during research on shallow tropical coral reefs, home of the Earth’s most productive (photosynthetic) systems. In reefs, where algae are supplied with abundant sunlight, intense wave action, and strong currents, photosynthesis and primary production occur at a great rate, generating more plant material than in almost any other natural or man-made environment. Because of the prolific animal life, however, few plants are apparent on most reefs. The high rate of plant production is accomplished mostly by a small, seemingly insignificant group of algae known collectively as algal turfs (Adey and Hackney, 1989). Some photosynthesis also occurs with symbiotic microalgae inside corals, and in mostly filamentous boring algae in the upper millimeter of any “dead” carbonate, in large algae such as Sargassum, as well as in the higher plant seagrasses. However, most primary production in the typical shallow water reef is performed by algal turfs (Adey, 1998).

Algal turfs are short, moss-like mats of algal filaments commonly covering most hard surfaces in shallow reef zones (Figure 11.3 and Color Plate 16). They are usually no more than several centimeters tall. Their actual tissue production rate in very low-nutrient environments is 5–20 g dry weight per square meter per day, a rate several times that of most terrestrial plants, including carefully tended and fertilized agricultural crops. Algae, in a welldeveloped turf, can absorb typically 0.2–0.6 g N and 30–100 mg P per day per square meter of screen, even in very low-nutrient environments. As we will discuss later, in more mid-level and eutrophic environments, removal rates can be much higher. Algal turfs are communities within themselves. A coral reef surface or an attached meter-square plastic screen in a warm, well-lighted, high-water-quality tropical environment would typically contain 30–40 species of algae, with red algae, blue-greens, and diatoms dominating (Color Plate 27; Adey and Goertemiller, 1987). Of those major groups, diatoms tend to be the early colonizers. Later, blue-greens are most important in very high light, and reds in more shaded environments. Typically, green and brown algae are lesser but omnipresent components. A similar situation in subarctic-temperate waters would provide the same overall floral composition, though small brown algae tend to be more important,

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FIGURE 11.3 (A) Typical tropical algal turf growing on a 1-mm mesh plastic screen. Genera shown: (a) Pilinia, (b) Cladophora, (c) Giffordia, (d) Sphacelaria, (e) Herposiphonia, and (f) Calothrix. (B) Typical, layered algal community on a freshwater scrubber screen. The lower layer is dominated by the blue-green Calothrix, the middle layer by the blue-screen Oscillatoria and the green unicell Gloeocytis. The upper layer consists largely of long strands of the green alga Ulothrix.

The Algal Turf Scrubber (ATS™)

and about one-half the species diversity would be more typical. In fresh waters, green and diatom species provide most of the floral composition although blue-green algae (cyanobacteria) can be dominant with lower water qualities. Brown algae do not appear in freshwater algal turfs, and in higher water qualities a very few specialized reds can be present (e.g. Adey et al., 1993). In waters of lower quality, the number of species is generally much reduced. Algal turfs grown in raw sewage, for example, have a community that tends to be composed of several species of blue-green algae (cyanobacteria) and perhaps one or two species of green algae. Algal turfs are the equivalent of grassland communities. They must be grazed (or harvested) or the community will build up to the point where the basal portions die and the turf sloughs off. If larger algae are available, the community will go through a succession to a lessproductive, higher-biomass macroalgal “forest.” Algal turfs also have their “locusts” (generally amphipods or chironomid insects), which in the wild are kept moderate in numbers by small fish predators. In the presence of these micrograzers and lacking grazing by large organisms, a macroalgal or higher plant community of moderate to low productivity is inevitable with time. The practical aspects of maintaining algal turfs for managing enclosed ecosystems are discussed below. For a more in-depth discussion of this plant community, its definition, composition, and biology, the reader is referred to Adey (1987), Adey and Hackney (1989), and Adey et al. (1993). The wave action and surge-like motion characteristic of reef surfaces are crucial. When turned off, the result is a radical drop in turf photosynthesis because the wave surge boosts the efficiency of the photosynthetic mechanisms, partly by serving as a light “flasher.” Algal turfs do not light-saturate at normal levels of solar energy. They are “sun plants” and can use all the sunlight they can get (Figures 5.15 and 5.17), though there may be a small reduction due to ultraviolet effects at depths less than 20–30 cm under tropical sun (Adey and Goertemiller, 1987). In addition, wave surge also serves as a strong mixing agent, facilitating the exchange of metabolites needed or excreted by the algae. Another reason for the unusually efficient growth of these algae lies in their structure. The algal filaments are to a large extent simple strands, not differentiated into specialized forms or functions. Most cells in the plant mass are photosynthetic, absorbing light, carbon dioxide, and nitrogenous and phosphorus compounds, and producing oxygen and carbohydrates. In contrast, larger, more complex plants reserve much of their body for other functions such as structural support, reproduction, and protection, leaving a smaller proportion for photosynthesis.

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The very survival of turf algae hinges on their rapid growth rate, for in the wild they are subjected to extremely heavy grazing by herbivores. Aided by their capacity to absorb large quantities of sunlight and metabolites in relation to their body mass, algal turf spores settle, grow, and become reproductive within days or weeks on any available surface. Even when their upright portions are eaten by grazers, their basal filaments remain, having penetrated minute irregularities in the substrate. These filaments rapidly regenerate new growth to replace lost material. Algal turfs are common in marine, shallow water environments, where physical energy levels can be quite high. Similar algal species occur in fresh waters where they are typically called periphyton. Where physical energy is low, they become part of biofilms or aufwuchs communities. The mutual interactions between algae, bacteria, protozoans, and some small invertebrates within these biofilms can become very complex (Burkholder, 1996). The algal turf scrubber (ATS) (marine, estuarine, and fresh water) applies defined physical energy to these communities to enhance water column exchange and photosynthetic efficiency while maintaining many of the complex, internal interactions (see also Leigh et al., 1987).

THE ALGAL TURF SCRUBBER (ATS™) Overcoming the oxygen depletion and organic waste and nutrient buildup that occurs in the dark in high-biomass shallow water communities is a necessity, both in closed systems and in the wild. Shore and bottom communities benefit from the open ocean or open lake, which provides a continuous supply of oxygenated and low-nutrient water when photosynthesis stops. But maintaining a large reservoir equivalent to the open ocean or a large lake is usually not feasible in a captive ecosystem. ATSs have been used as water quality control devices by the authors and by the Smithsonian’s Marine Systems Laboratory and its associates on over 25 coral reef, rocky shore, estuary, and stream and pond microcosms and mesocosms, ranging from 30 to nearly 1 million gallons for a total of well over 125 ecosystem-years of operation (see e.g. Adey, 1983; Adey, 1995; Luckett et al., 1996; Table 11.1). Many of these systems have been in continuous operation for over 10 years, with one now approaching 30 years. ATSs are engineered mini-ecosystems, dominated by algal turfs; the high levels of photosynthesis and primary production produced by the algal turfs are utilized to control water quality in the model ecosystems to which they are attached. Such scrubbers are separate from the model systems that they control, being installed

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TABLE 11.1

Mesocosms, Microcosms, and Aquaria Operated with Algal Turf Scrubbers by the Authors and Their Associates and Colleagues

Surface area (m2)

5 26 a 8 17

4.57 11.6 0.85 646

Volume (gallons/liter)

1 0.7 0.3–0.7 0.5

1129

0.3–0.7

14

0.85

14

6.98

2500/10 000

1

1

MH/2/800

800

MH/14/5600

924

1–10b

Estuarine Chesapeake mesocosm

9

44.8

15 000/60 000

3.9c

0.65

MH/8/3200

820

942

0.5–8

Everglades mesocosm

14

130.3

22 000/88 000

3

0.34

3–15b

3

0.85

120/480

0.082

1.7

690 natural light 1700

–

Chesapeake home aquarium

VHO/8/1820 MH/12/800 natural light HO/4/140

VHO/64/ MH/32/42 240 Natural light

VHO/6/960

816

–

Freshwater Florida Everglades stream

12

37.6

4000/16 000

2

1.4

MH/2/800

None

–

2 µM

3

7.7

2500/10 000

1.5

7.7

Natural light

800 natural light –

Natural light

–

0.1–2.3

14 3

0.51 0.51

70/280 70/280

0.085 0.072

3 2.6

MH/1/125 HO/2/70

1200 970

Natural light VHO/2/230

450 450

8–16 1

Including years at Fort Pierce (note some parameters change after move). Nutrient range for research purposes. c Does not include “river input” scrubbers.

3.8

MH/4/1600 800 MH/10/400 MH/13/58 000 828 MH/22/14 800 HO/6/300 1670 VHO/6/960 MH/40/40 000 500 natural Natural light natural light light MH/3/300 1670 VHO/6/960

875 1276 1129

130 reef microcosm

b

0.18

System lighting (type/No./W)

Subarctic Maine rocky shore and marsh

a

2 4.6 3.8 0.26

Scrubber power/area (W/m2)

2500/10 000 3800/15 280 130/500 750 000/ 3 000 000 130/500

Microcosm–blackwater (South American) African pond aquarium Blackwater (South American aquarium)

2 7 0.18 80

Scrubber lighting type/No./W

Operational nutrient System levelb (µM) power/area (W/m2) (NO3 NO2)


Marine Tropical reefs Smithsonian Institution prototype Caribbean exhibit Exhibit-130 microcosm Australian I.P. mesocosm

Years in operation

Ratio Scrubber scrubber area/ area system volume (m2) (cm2/liter)

The Algal Turf Scrubber (ATS™)

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FIGURE 11.4 This battery of 2-m2 ATSs is placed on the Great Barrier Reef Marine Park Authority’s coral reef mesocosm in Townsville, Australia. At time of writing, it had operated as the primary water quality control system on that large model ecosystem for over 20 years. Photo by Great Barrier Reef Marine Park Authority.

FIGURE 11.5 Diagram of standard scrubber showing all essential components.

in the microcosm’s or aquarium’s water-circulation line and typically lighted in a cycle opposite to that of the main ecosystem (Figures 11.4 and 11.5). While the microcosm is in darkness, the algae in the scrubber are photosynthesizing, ensuring a continual supply of oxygenated water and rapidly removing CO2 and nitrogenous waste when it is most abundant. The rate of oxygen production and the uptake of nitrogenous wastes can be easily controlled by changing the length of time the turf algae are lighted. The scrubber duplicates the balancing process found in the wild, and is effective in full-salt, brackish, and freshwater systems from tropical, temperate, and coldwater environments. As we have discovered through

years of research, algal turfs are available in most coastal environments, rocky shores, salt marshes, and estuaries as well as reefs, and need only to be provided with a suitable environment to produce a rich growth. Unlike the bacteriological filter, which, in return for the removal of ammonia and some particulates, returns to an aquarium water depleted in oxygen and plankton, and high in dissolved nutrients and carbon dioxide, the scrubber keeps oxygen near or above the saturation point and effectively removes all classes of dissolved animal wastes in a balanced process. Although the mean relationship of C:N:P is often given in texts as 106:16:1, as we demonstrated in Chapter 9 (text and Figure 9.5), algae easily under- or overcompensate for nutrient concentrations in the water column, thus tending to re-balance the nutrient spectrum. Scrubbers also offer the advantage of not destroying plankton or the larval stages of bottom-dwelling invertebrates that are a natural component of virtually all aquatic systems. The ATS is designed to produce elevated rates of plant production in order to remove a large quantity of pollutants. Figures 20.2, 20.7, and 21.15 show how shallow troughs, separate from but connected to the tank being serviced, create optimal conditions for algal turf growth: (1) maximum light, (2) wave surge, (3) controlled grazing, and (4) exclusion of animals that would offset the effects of the algae. This design also allows coarser and finer tuning of algal functions by varying

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algal area, wave surge, and light levels and periods. Through harvest, algal turf scrubbing also presents an automatic and controllable source of organic export. Table 11.1 shows some of the model ecosystems (microcosms, mesocosms, and aquaria) and the scrubber dimensions and lighting that have been used to successfully manage those closed ecosystems. Turf algae can be grown on a fine-mesh plastic window screen stretched on a frame that fits in the bottom of the trough. A somewhat coarser 2 4-mm black polyethylene screen functions as well and is considerably more durable. The screen can be seeded by suspension in an established microcosm or in the natural environment. An alternative, equally satisfactory, approach is simply to stock the ecosystem first with algal turf substrate and, once the scrubber is operating, add the remainder of the community. Because water in the trough is shallow, the turf-bearing screen is situated at or near the surface, and receives maximum light, which otherwise would be filtered through the water column. For tropical, nonshaded algae, high-intensity metal halide lights or very high-output (VHO) fluorescents are used. For turfs from arctic and temperate regions, one can use high-intensity fluorescent tubes (VHO or high output (HO)) (see Table 11.1 and Chapter 5). Scrubbers are typically lighted for 10–18 h per day; the length of the lighted period can be adjusted to the oxygen cycle desired (Figure 8.9). They are best kept in darkness when the light in the community tank is brightest, that is, when the oxygen level in the tank is at its highest and nutrient levels are low. Pumps deliver water from the primary ecosystems to the scrubber trough at a rate that depends on the size of the system and typically ranges from 3 to 10 gallons per minute depending on the size of the scrubber. At the other end of the trough, water returns to the main tank through gravity drain pipes, or can be used directly to provide wave generation (see Figures 20.2 and 21.15). Assuming adequate light, algal production is limited only by inadequate exchange of metabolites – oxygen, carbon dioxide, and nutrients – between the water and the cells of the attached algae. We have demonstrated a strong correlation between wave surge and improved metabolic interchange. When the wave generators in our main reef tanks are blocked, while maintaining a constant rate of circulation and level of light, there is an immediate 50% reduction in oxygen production. The surge generated by the wave maker produces a back-and-forth motion within the tank, greatly reducing the development of semistagnant boundary layers that occur when a constant flow of liquid passes by a fixed object. A steady current would tend to pin the filaments in an immobile position, and a surface layer of very slow-moving water would develop. Also,

while exposed portions of the algae would derive most of the benefits of light and current, interior portions would be shielded, reducing metabolite exchange and light for photosynthesis. By growing turf communities outside the main body of the model ecosystem, the algae are protected from larger grazers in the ecosystem. The latter would reduce the effectiveness of the algal photosynthesis and growth. However, some small, herbivorous invertebrates can spread to the scrubber trough through the piping and become established. Chief among these are species of amphipods in salt water and chironomid larvae in fresh water. Since the latter organisms are an insect with a flying stage, they are not likely except in the largest, greenhouse-type mesocosms. In that case, the scrubbing system itself can be isolated from the general system atmosphere. These micrograzers attach themselves to hard surfaces and some species construct small, protective nests. Thus, partially protected from the ecosystem’s predators, these invertebrates release larval plankton and young animals, which serve as food for the animals in the main tank, just as they do for larger animals in the wild. However, when these organisms are allowed to proliferate unchecked, they can reduce the efficiency of the scrubber by eating the turf algae and contributing animal wastes to the system. Periodic scraping of all the wetted surfaces of the scrubber unit in addition to the algal screen keeps micrograzers in check, ensuring full efficiency of the scrubber.

Harvesting of ATS Periodic harvesting of algal turfs in scrubbers is essential because these plants are most efficient when young. Harvesting keeps them in the “log phase” of growth. Those adding new growth use greater quantities of animal wastes than those simply supporting existing tissues. The dense, tangled mass of a mature community shades the turf’s interior from light and restricts water circulation, reducing plant production per unit plant biomass. Very heavy algal turf growth also conceals flourishing colonies of amphipods and other invertebrates that consume plant filaments and oxygen and produce more wastes. In small systems, harvesting can be accomplished simply by removing the scrubber’s screen and scraping away excess growth, with a plastic device similar to an automobile windshield ice scraper. However, a shop “wet-vac” is more appropriate for larger ATS screens and allows the harvester to avoid a screen-washing step that maximizes removal efficiency. Very large, acre-size systems are best harvested with a small “street sweeper” with only the vacuum part operating (see Chapter 25). These procedures mimic the grazing that the turfs have

Algal Scrubbers and the Modeling of Ecosystems

evolved to counteract. It also effectively removes nutrients from the entire system by collecting nitrogen, phosphorus, and carbon that have become incorporated into the algal biomass. The basal filaments that remain intertwined in the mesh of the screen after scraping quickly send up new growth to replace that which has been removed. Optimum harvest rates for all systems that we have worked on have ranged from 7 to 20 days. Production rates vary widely from harvest to harvest. A mean standard deviation of a wide variety of microcosm scrubber runs was 26% of the means. If harvest length is extended to visually fit production, total harvest tends to be reduced. Periodic harvest, preferably at a fixed interval, is necessary for optimum scrubbing. For larger systems with multiple scrubbers or floways, harvesting should be spread out over a week, one-fifth or one-seventh per day. Also, the greatest constancy (evenness) of water quality, or export, where that is important is achieved by spreading harvest out over a weekly cycle. Also, 3–9 weeks and several harvests are usually required to bring screens established in the wild to full production. While the time required for laboratory or home aquarium screens to seed and come to full production is typically less (3–6 weeks), significant time is still required to allow succession to occur. In the last half of the succession process, normal harvest procedures should be carried out. In coral reef models, and any microcosm/mesocosm system in which maximum export of nutrients and extremely low nutrient levels and maximum clarity are desired, algal turf screens should be rinsed, under light pressure over a sink. For the purist, a saltwater rinse system with a spray head can be established. We have found in practice that a 1-min spray/rinse with fresh water has little effect on algal composition or regrowth. Most complaints of algal turf weak performance relate to a failure to routinely harvest. This is difficult to understand because for a 100–1000-gallon system, 5–30 min per week is required for harvest. We repeat for emphasis: for maximum performance, screens of algal turf scrubbers must be routinely harvested, typically at 1-week intervals. In addition to producing oxygen and scrubbing nitrogen and phosphorus, algal scrubbers also remove carbon dioxide and increase pH. In all marine systems (which are strongly buffered) pH increase only improves the match of the model to the wild environment. In fresh waters, unless one desires a highly acidic environment, pH increase is normally offset by increasing animal biomass to achieve the desired levels. When a “blackwater” acid environment is desired and strong algal scrubbing is employed, it may be necessary to acidify or bubble the environment with carbon dioxide. Addition of tanninrich top-up water can also be effective (see Chapter 23).

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The size and scrubbing potential of an algal scrubber must be balanced against the community load to achieve the desired results. To some extent the scrubber algal community and production will adjust against the load, though the dimensions given below for a number of systems provide guidelines of approximate size. In underscrubbed systems, nutrients simply rise above desired levels and oxygen falls below desired levels. In our experience negative feedback or crash situations do not develop. At the other extreme, that of overscrubbing, nitrogen can rarely be driven below about 0.5 µM for N as NO 2 NO3 . Below about 1 µM, blue-green algae are dominant on the scrubber screen and nitrogen fixation increases the rate of input of nitrogen into the system (Lucid, 1989). Phosphorus and other micronutrients do not have a natural method of input, except in food or evaporative water input. Once nutrient levels near the lower values found in the wild ecosystem being modeled are achieved, the harvested and dried algae can be returned to the model by a variety of means. We prefer grinding with a mortar and pestle and casting the organic particulates on the water surface. In very large models such return should reflect seasonal cycles, in small systems, daily cycles.

ALGAL SCRUBBERS AND THE MODELING OF ECOSYSTEMS In microcosms and mesocosms, one is seeking environmental and ecological parameters close to those of the wild analog to be modeled. In aquatic ecosystems, nutrient concentrations are extremely critical to system function. While the spectrum of nutrients can become unbalanced, they tend to run in parallel, as we discussed in Chapter 9. For routine monitoring, a single nutrient ion can be followed and in many of our microcosms, we have used nitrogen, N as NO2 plus NO3, with a bimonthly or semi-annual broad spectrum check. For example, from an early 3500-gallon Caribbean coral reef microcosm, a typical plot of nitrate levels for a period of several years is shown in Figure 11.6. These levels were achieved by five scrubbers with an algal turf area of 1.4 m2 each. The nitrite plus nitrate concentration in the water incoming to a scrubber is typically 0.5–0.7 µM, and that in the water exiting, it is typically 0.05–0.1 µM (an 80–90% removal rate). Mean production levels are shown in Figure 11.7. Four of the five scrubbers operated with two 400-W metal halide lamps and the fifth with a single 1000-W lamp. This amount of scrubber area is relatively high per volume of system for research purposes (Table 11.1). The algae typically present on these scrubbers is shown in Table 11.2.

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FIGURE 11.6 Plot of nutrient levels in Smithsonian coral reef microcosm from December 1988 to June 1990 compared to dissolved nitrogen over St. Croix reefs in 1976–1977. The range is similar, although mean levels over the wild reef are about 0.2 µM (0.003 ppm) lower than those in the microcosm. Note that reactive nitrogen is measured as the nitrogen in nitrite plus nitrate, although nitrite is typically a small fraction of nitrate.

FIGURE 11.7 Diagram showing coral reef microcosm scrubber algal turf production for a 6-month period.

Algal Scrubbers and the Modeling of Ecosystems TABLE 11.2 Common, Persistent Components of Coral Reef Algal Turf Assemblage in Microcosm Scrubbers Bacillariophyta Licmophora sp. Navicula sp. Nitzschia sp. Thalassiothrix sp. Cyanophyta Anacystis dimidiata (Kutzing) Drouet and Daily Calothrix crustacea Schousboe and Thuret Entophysalis sp. Microcoleus lyngbyaceus (Kutzing) Crouan Oscillatoria submenbranacea Ardissone and Strafforella Schizothrix sp. Chlorophyta Bryopsis hypnoides Lamouroux Cladophora crystallina (Roth) Kutzing Cladophora delicatula Montagne Derbesia vaucheriaeformis (Harvey) J. Agardh Derbesia sp. Enteromorpha lingulata J. Agardh Enteromorpha prolifera (Muller) J. Agardh Smithsoniella earleae Sears and Brawley Phaeophyta Ectocarpus rhodocortonoides Borgesen Giffordia rallsiae (Vickers) Taylor Sphacelaria tribuloides Meneghini Rhodophyta Acrochaetium sp. Asterocytis ramosa (Thwaites) Gobi Callithamnion sp. Centroceras clavulatum (C. Agardh) Montagne Ceramium corniculatum Montagne Ceramium flaccidum (Kutzing) Ardissone Erythrocladia subintegra Rosenvinge Herposiphonia secunda (Agardh) Ambronm Polysiphonia subtillissima Montagne

In a very different microcosm, a 2500-gallon rocky Maine shore, two scrubbers of 0.5 m2 each were used. Both of these produced at mean levels of 12.0 g (dry weight) per square meter per day. The dominant scrubber algae were species of Ectocarpus, Enteromorpha, Cladophora, Polysiphonia, and Porphyra. Blue-greens and diatoms are also present within the dense algal turf. Nutrient levels were typically maintained at 3–10 µM (NNO2 NO3), though on occasion they were driven below 1 µM. In small home ecosystem-based aquaria, the situation is rather different. Here, although an analog of a type of wild system is attempted, the volume is so small that the accuracy of simulation is more limited. For example, spatial heterogeneity (reef surface per unit area) is lower and fish biomass is higher than that in the wild, feed must be supplied to make up for the lack of forage area, and scrubber-to-volume area must be increased (see Table 11.1). The Australia reef mesocosm at 3 million

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liters operated at 0.3 cm2 of scrubber area per liter of ecosystem water, while our 130-gallon coral reef aquarium operates at 3.3 cm2 per liter (see Chapter 20). In addition, an understanding of export and its relationship to import is crucial. Scrubber algae typically contain 0.3–8% (mean 3%) nitrogen as a fraction of dry weight, the lower percentages characterizing systems operated at very low nutrient concentrations [2 µM (NNO 2 NO3 )]. Most feeds, whether brine shrimp, krill, or flake foods, contain between 8% and 12% nitrogen of dry weight. Thus, export (of algal turf or removed ecosystem plant biomass) should be two to four times feed input (dry weight), depending on the situation. Very low-nutrient systems are typically operated with an export:import ratio of 5–7:1. This results partly from falling nitrogen percentages in the removed algae and partly from nitrogen fixation. While this process might theoretically overscrub some micronutrients (the scrubber algae will compensate in part as they do with nitrogen and phosphorus), the standard 1–2% water change per month should handle this. In some cases, it may be necessary to add micronutrients, though as we describe in Chapters 10 and 20, this has not been our experience. Many extremely low-nutrient situations are nutrient limited in the wild, and this is what blue, high-clarity waters mean. Also, high productivity in nutrient deserts (coral reefs) results from large quantities of water with low nutrient concentrations flowing over a fixed point (Adey, 1987). This results in the availability of large, total quantities of needed nutrients at low concentrations; in models, this is simulated by adding food. Two of the most commonly used small scrubber types for home aquarium systems and microcosms and mesocosms are shown in Figure 11.8A and B, and their management is discussed in detail in Chapters 20–23. A schematic diagram of the typical one-quarter to 5-acre ATS system for landscape scale is shown in Figure 8C. Management practices for these larger systems is discussed in Chapter 25. Human culture has gradually developed an extensive use of metals. Some of these, such as iron, are crucial to many organisms in moderate quantities. Other metals are often required in microquantities. On the other hand, many metals, particularly the heavy metals (lead, mercury, copper, and zinc), can be highly toxic when they occur in appreciable quantities in the water. Indeed, some human water supplies have serious health problems in the form of dissolved heavy metals, and copper is often used as a poison to reduce algal levels in drinking-water reservoirs. It has long been known that growing algae have the capability of taking up and concentrating many heavy metals as well as numerous toxic organic wastes (Green and Bedell, 1989; Adey et al., 1996). The algal scrubber process can maintain model ecosystems at

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FIGURE 11.8 Diagram showing different types of ATSs. The “perpetual-motion” or “dump-bucket” scrubber can also provide wave and surge motion in the aquarium itself. (A, B) aquarium or microcosm/mesocosm units; (C) “floway” set for mesocosms or landscape scale and can range from one-tenth to 5 acres in dimension.

acceptably low levels of heavy metals and toxic organics as long as spike additions are not at levels that are toxic to the algae.

SUMMARY ATS units can manage most aquatic and marine model ecosystems. The data given here for scrubber area and operational procedures provide the background that will enable the aquarist to adapt the concept to different model ecosystems. Every wild ecosystem varies from its “type,” and each microcosm, mesocosm, and aquarium will vary even more from the analog or wild model. These numbers are guidelines developed from decades of working experience. When in doubt in a particular case, add 20–30% to scrubber area. It is a simple task to reduce light period if excess scrubbing is occurring and nutrients are lower than desired. Algal scrubbing serves three primary purposes: (1) oxygen and pH control, (2) nutrient control, and (3) nutrient export. The first function is primarily a diurnal, or at least a short-term, need. The term reverse daylight photosynthesis is sometimes used when algal scrubbing is deployed with nighttime lighting while the model ecosystem is on local daylight. If water volume is very large relative to the area undergoing nighttime respiration, and daytime photosynthesis is adequate, scrubbing might not be needed for this function. This applies

typically to models larger than several hundred thousand gallons. For smaller mesocosms, microcosms, and aquaria, that is, any system less than 50 000–100 000 gallons in volume, the gas-exchange requirement can be used to calculate required scrubber area. For example, if the aquarist can measure and calculate the respiration rate (Chapter 8) of the planned community, then required scrubber area is approximately that needed to supply the oxygen requirements of the model system during the dark period. This method assumes no atmospheric exchange (which for carbon dioxide is likely to be essentially correct) and means that the aquarist must establish a minimum oxygen concentration that is acceptable for the ecosystem in question. Nutrient scrubbing is a longer-term requirement. Depending on system volume relative to feeding, lighting, and other plant or animal export, it is most likely measured in weeks or months for larger model systems. In totally closed systems where no feed is introduced, scrubbers are used to balance seasonal production cycles, or in mesocosm situations where watersheds are included, to return elements to the watershed simulating a geological function. Practically, it is difficult to calculate with precision the nutrient scrubbing requirements of a given system. It is best to use the guidelines of Table 11.1 to determine scrubber area and lighting. These are based on approximately 125 system-years of operation. This can be followed up with monitoring of nutrient concentration as the system matures.

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References

It has been argued by some authors in recent years (summed up by Delbeek and Sprung, 2005) that while ATS systems provide excellent control for estuarine and rocky shore systems, they are marginally successful in operating coral reef systems. The 10-year-old “home” reef aquarium system described in Chapter 20, and appearing numerous times in scientific publications, belies that assertion. That reef model, controlled solely by ATS, shows among the highest rates of calcification known for both whole wild reefs and wild Acropora corals (Small and Adey, 2001). In addition, after 7 years of closure, it showed a species biodiversity of 534–800 spp., proportional in the wild to a pan-to-tropic biodiversity of 2.6–3.2 M species (Small et al., 1998). This biodiversity was extraordinarily broad, the 534 species occurring in 230 families belonging to 96 orders and 27 phyla (Adey, 2006). Some of the early ATS systems did suffer from their very success, in that calcification rates were so high, that the calcium and alkalinity monitoring and replacement were insufficient. Some of the later systems, over which we had no control, became severely depleted of calcium and alkalinity because their calcification potential was so high and replacement was inadequate. To discredit the function of such an ATScontrolled coral reef model is about the same as saying that the fastest car in a race is not a good car when the operators do not put enough gas in to finish. Finally, in referencing the reef system noted above, some authors have attributed that success to bacteria in the abundant sand in the base of the tank. A glance at Figures 8.9 and 5.15 and Table 20.8 shows that nighttime respiration (also daytime) is modest in these systems. Indeed, as shown by Small and Adey (2001) it is less than that for the analog wild reef and could take a heavier fish and invertebrate load. It is not possible to directly measure bacterial relative to animal and plant biomass, so that the proportionality of bacteria to animal and plant respiration can be determined (it might be possible to do it by isotope analysis). However, a glance at the fish and animal biomass in the system, as compared to potential biomass in the sand (which appears quite clean in comparison to the obvious invertebrate biomass) indicates that the free bacterial biomass is very small in this system. A microscopic examination of the sand also shows abundant protozoans but few identifiable uneaten food particles. Undoubtedly, bacterial biomass in animal guts is high and particulates clearly spend more time in animal guts than free, but this respiration is typically allocated as part of animal respiration. Finally, as we discuss in the Bacteria section of Chapter 18, even in fine, organic-rich sediment, bacteria constitute less than 1% of the biomass in the richest, top 5 mm, and have an equivalently low metabolic effect on the ecosystem as a whole. It is likely, in this

coral reef model, that bacteria, in the sandy sediment constitute less than 0.1% of the organic biomass and probably far less in the system as a whole. The effect of bacteria, outside of animal guts, is likely negligible in this system. In summary, it is important to remember that ATS systems are not filters, and on any given microcosm/mesocosm system the ATS size is in practice determined by matching the model O2 curve with that of the wild analog. In highly diverse and well-populated coral reef systems, controlled by ATS, food particles and animal and plant parts are constantly recycled by animals and eventually protists. There is no equivalent of a bacterial filter where food particles are held for slow breakdown by bacteria. Foam fractionation would be a better option for particulate removal, if for any reason an ATS system cannot be used; it can provide the equivalent in a wild analog of export from the ecosystem. However, to a large extent, foam fractionation cannot differentiate between particulate and reproductive stages. The large biodiversity of the “home” coral reef mentioned above, after 7 years of closure, is the result of extensive population maintenance by reproduction, most of which involves reproductive and larval stages spending hours to days suspended or swimming in the water column.

References Adey, W. (1987) Food production in low nutrient seas. Bioscience 37: 340–348. Adey, W. (1983) The microcosm: a new tool for reef research. Coral Reefs 1: 193–201. Adey, W. (1995) Controlled Ecologies. Encyclopedia of Environmental Biology, Vol. 1. Academic Press, San Diego. Adey, W. (1998) Coral reefs: algal structured and mediated ecosystems in shallow turbulent waters. J. Phycol. 34: 135–148. Adey, W. (2006) Lessons learned from the construction and operation of coral reef microcosms and mesocosms. In: Handbook for the Restoration of Coral Reef Ecosystems. W. Precht (Ed.). Taylor and Francis/CRC, Boca Raton. Adey, W. and Goertemiller, T. (1987) Coral reef algal turfs – master producers in nutrient poor seas. Phycologia 26: 374–386. Adey, W. and Hackney, J. (1989) Harvest production of coral reef algal turfs. In: The Biology, Ecology and Mariculture of Mithrox spinosissimus Utilizing Cultured Algal Turfs. W. Adey (Ed.). Mariculture Institute, Washington, DC. Adey, W., Luckett, C., and Jensen, K. (1993) Phosphorus removal from natural waters using controlled algal production. Restor. Ecol. 1: 1–11. Adey, W., Luckett, C., and Smith, M. (1996) Purification of industrially contaminated ground waters using controlled ecologies. Ecol. Eng. 7: 191–212. Borneman, E. (2004) Aquarium Corals: Selection, Husbandry and Natural History. Ricordea Publ., Miami. Burkholder, J.-A. (1996) Interactions of Benthic Algae with their Substrata. In: Algal Ecology: Freshwater Benthic Ecosystems. R.J. Stevenson, M. Bothwell, and R. Low (Eds). Academic Press, San Diego.

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DeBoer, J. A. (1981) Nutrients. In: The Biology of Seaweeds. C. D. Lobban and M. Wynne (Eds). University of California Press, Berkeley. Delbeek, C. and Sprung, J. (1994) The Reef Aquarium. Ricordea Publ., Miami. Delbeek, J. C. and Sprung, J. (2005) The Reef Aquarium, Science, Art and Technology, Vol. 3. Ricordea Publ., Coconut Grove, Florida. Green, B. and Bedell, C. (1989) Algal gels or immobilized algae for metal recovery. In: An Introduction to Applied Phycology. I. Akatsukai (Ed.). S.F.P.B. Academic Publishers, The Hague. Honn, K. and Chavin, W. (1975) Prototype design for a closed marine system employing quarternary water processing. Mar. Biol. 31: 293–298. Leigh, E., Paine, R., Quinn, J., and Suchanek, T. (1987) Wave energy and intertidal productivity. Proc. Natl. Acad. Sci. USA 84(5): 1314–1318. Lucid, D. (1989) Effects of Dissolved Inorganic Nitrogen Concentrations on Primary Productivity, Nitrogen Fixation, and Community Composition of Coral Reef Algal Turf: A Microcosm Study. M.S. Thesis, University of Maryland.

Luckett, C., Adey, W., Morrissey, J., and Spoon, D. (1996) Coral reef mesocosms and microcosms – successes, problems and the future of laboratory models. Ecol. Eng. 6: 171–224. Moe, M. (1989) The Marine Aquarium Reference. Green Turtle Publications, Plantation, Florida. Seitzinger, S. (1988) Denitrification in freshwater and coastal marine ecosystems: ecological and geochemical significance. Limnol. Oceanogr. 33: 702–724. Small, A. and Adey, W. (2001) Reef corals, zooxanthellae and freeliving algae: a microcosm study that demonstrates synergy between calcification and primary production. Ecol. Eng. 16: 443–457. Small, A., Adey, W., and Spoon, D. (1998) Are current estimates of coral reef biodiversity too low? The view through the window of a microcosm. Atoll Res. Bull. 458: 1–20. Smith, T. and Schuman, A. (1991) The denitrator in the reef aquarium. Freshwater Mar. Aquar. 14: 66–67. Spotte, S. (1979) Sea Water Aquariums: The Captive Environment. Wiley Inter-Science, New York. Spotte, S. (1992) Captive Sea Water Fishes. Wiley, New York. Sprung, J. (2002) Algae: A Problem Solver Guide. Ricordea Publ., Miami.

P A R T

III BIOLOGICAL STRUCTURE


C H A P T E R

12 Community Structure Biodiversity in Model Ecosystems

Individual organisms, as part of species populations, in a microcosm or mesocosm, interact with each other, and together with the physical environment, to form an ecosystem. The development of an ecosystem, whether in a newly created environment in the wild or in a model, is called self-organization. Ultimately, the metabolic and behavioral information encoded in the genes of each individual determines how each individual will interact with other individuals of its own and other species and with its environmental parameters. In this chapter, we specifically treat the subject of biodiversity, the number of families, genera and species in an ecosystem, and particularly how those species, as populations, structurally relate to each other in any biological community that we may wish to model. It is widely recognized today that the Earth’s biodiversity is rapidly being reduced due to the numbers of humans and their economic activities (Reaka-Kudla, 1996). To understand what a simple species count in an ecosystem model should be and is, in reality, it is necessary to understand the reasons for biodiversity in wild ecosystems. Although the reasons are complex, enough information has been collected, particularly in the past 10–20 years, to provide the framework for that understanding. In a sense, many of Earth’s ecosystems have become models, increasingly limited by the everexpanding and ever-more intrusive bounds of human society. Understanding how to manage biodiversity in microcosms and mesocosms can provide us with the ability to further understand and manage the biodiversity of the planet at large. Models can be the experimental tools that assist us to develop a rationale for living

with the incredible and incredibly valuable biological diversity that 3–4 billion years of evolution has produced. During the past several centuries, and particularly the 20th century, humans have shuffled decks of species over and over, so that invasive species now blur our view of the reality of communities and ecosystems (Carlton, 1999). Mesocosms, especially, provide the opportunity to test hypotheses of the roles played by invasive species in restructuring natural systems. The same or similar models can be used to educate a willing public as to why they should demand, and be willing to pay for, a human society that lives with and supports the biodiversity of the Earth.

THE FRAMEWORK OF BIODIVERSITY The number of species present at any one time over the past 4 billion years of development of life on Earth is a dynamic. During one several-million-year period, the numbers may grow rapidly, sometimes in one ecosystem at other times in another (Valentine, 1985). There have also been narrow intervals of massive species extinctions, thought by many paleobiologists to be related to cataclysmic events resulting from collisions of extraterrestrial bodies (asteroids, comets, etc.) with the Earth. Nevertheless, the fossil record clearly shows that, while some major groups of plants and animals have appeared and become diverse and abundant, only to later become rare or extinct, in general the total numbers of species on Earth has continued to grow, now reaching tens to hundreds of millions.

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12. Community Structure

FIGURE 12.1 Larger animals are fewer (B) and are represented by fewer species (A). The drop-off in species numbers in the smallest sizes is probably real and is a function of minimum size that can be accommodated by a body plan. Adding protozoa or even bacteria would reduce the position of the peak, but the drop-off would remain. After Bonner (1988, from May, 1984, and Peters, 1983).

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The Biome

Life exists on Earth with several major constraints that directly determine a species’ presence or absence and to some extent numbers. Temperature is one of those constraints. Few organisms can survive where below-freezing conditions are constantly present. Likewise few organisms survive above 60°C and very few above 100°C. Even between the extremes, few species can successfully negotiate a wide temperature range. As we discussed in Chapter 2, long-term patterns of temperate distribution on the Earth’s surface have had a major influence on the development of biogeographic zonation patterns. The availability of water on land and light in the ocean is also critical. Thus, the evolution of species tends to occur within major zones or provinces of similar characteristics that may or may not be physically separated by distinct barriers. A primary characteristic of natural ecosystems is the relationship between organism size and the numbers of that organism (Figure 12.1). Most species are small (Purvis et al., 2003). Even though there are fewer species and fewer numbers of large organisms, they occupy larger home ranges (Bonner, 1988). Some sea birds and marine mammals have ranges reaching tens of thousands of miles. Thus, in modeling an ecosystem, it is clear that the larger animals (though perhaps not plants), depending on the size in question and the model system, have to be accounted for by the intervention of the human manager. This is already true in some of our larger US terrestrial national parks, though there is some question whether this needs to be the case (Chase, 1987), and there are many efforts to introduce higher predators (wolves, lynx, cougars), mostly in the US West, where they had become effectively extinct. The extermination of large predators in the eastern third of the US has left hunters (in turn controlled by state game commissions) the managers of an enormous population of white-tailed deer. In a well-designed and operated model ecosystem, protozoa, amphipods, small fish, and crabs will be “at home” just as much as in the wild. On the other hand, the largest animals will probably have to be simulated. In the largest mesocosms, it is only the adult alligators, sharks, and snapping turtles that have to be omitted. In the microcosm, many predators, for example pickerel, barracuda, whelks, and octopi, may need to be omitted. In the aquarium ecosystem, on the other hand, great care must be taken with any predator that feeds on organisms larger than a centimeter in length. These problems can be handled, but some ecological understanding is required. Since that same understanding is also required for our as-yet feeble attempts to maintain natural ecosystems and communities in the “real” world, the knowledge acquired in building and maintaining model ecosystems by scientists, hobbyists, and

school children alike may well be an important element to our continued well-being on Earth. We start our discussion of biodiversity with an explanation of the larger framework within which biodiversity develops, the community and the biome. Later we return to the numbers issue: Why do some communities have far more species than others?

THE COMMUNITY Community structure is the ecologist’s term for indicating what organisms are present in a given environment, in what numbers, and how they relate to each other. Another way to look at a community is as a collection of niches or slots that organisms can fit into in order to “make a living.” In Chapter 13 on ecosystems and trophic structure, or food chains, we discuss rates of production, of feeding, and of energy and material flow. There is no sharp line between the subject matter of these two chapters. This chapter refers more to static and behavioral aspects, and Chapter 13 to dynamic aspects. The term community is rather arbitrary. Its boundaries can be as wide or as narrow as one chooses to make them. For example, a rocky-shore community could refer to a thousand miles of coastline or to a kelp community in a band tens to hundreds of feet wide on that coast, or the kelp epiphyte community could refer to those organisms growing on single kelp plants. Reasonably sharp community boundaries are required for such a designation, but even that criterion is sometimes rather fuzzy. Traditionally, a biological community is named for a dominant element or elements. An Acropora palmata reef community is conspicuously dominated by that single coral species as a major element of biomass or structure, controlling many other organisms by its presence. A Batis–Distichlis salt marsh community is a salt marsh in which the saltwort Batis and the salt grass Distichlis more or less equally provide the primary vegetation and therefore cover in the marsh.

THE BIOME Biomes are the largest-scale terrestrial communities (Figure 12.2). They are defined primarily by the effect climate (temperature and precipitation) has on the dominant community structure-creating plants. In this context, climate is a matter of altitude as well as latitude, mountain ranges, and geographical position on a continent. A secondary type of biome relates to the special effects of unusual rock and soil type. Since plants,

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FIGURE 12.2 Biomes, the largest scale terrestrial communities, diagrammed in relation to mean annual air temperature and mean annual precipitation. After Ehrlich and Roughgarden (1987, from Odum, 1971, and Whittaker, 1975).

especially forest trees, but even rushes and grasses, greatly modify the environment and establish a physical structure within which animals live, terrestrial biomes and communities are largely defined and often named by the dominant type of plants. In this book on the physical modeling of communities, or synthetic ecology, we concentrate on the marine and aquatic worlds, though often wandering out of the strictly submerged and intertidal habitats and into the transitional wetland communities. The large-scale marine and aquatic parameters that define the underwater equivalent of biomes are rather different from those in the terrestrial world. First, water, instead of being one of the two primary limiting parameters, is in great abundance. The only equivalent to the precipitation limitation is salt in the water, since in a sense it renders water relatively unavailable to organisms adapted to fresh water. Temperature is certainly important. However, because its short- and long-term range is more limited than on land, its influence is considerably more muted. Temperature effects on large-scale structural elements certainly are present, as exemplified by kelp beds in colder waters and coral reefs in the tropics. However,

in the water world the basic factors controlling the development of a community framework are so different from those on land that it is necessary to develop an entirely separate biome classification system. On land, the vast majority of plants must be rooted in the ground to obtain water. Because light is as crucial as water, the terrestrial communities we look at today are the result of 300 million years of competition, natural selection, and evolution directed to building more or less massive cellulose and lignin structures rooted in the ground and reaching to the sky. Plants were the first terrestrial builders, hundreds of millions of years before humans evolved. However, in the same sense as human communities, but much more extensively, plants have built natural community frameworks over most of the Earth’s land. These frameworks have become occupied by a host of animals, not only those feeding on the plants, as we discuss in the next chapter, but those using the plant structures as homes. In this context, home is used in all the ways that humans use that word. Under water, most of this is different. First, a major volume of deep-ocean and deep-lake water is unavailable

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FIGURE 12.3 Distribution of known hydrothermal spring activity on ocean ridges. Vent communities probably occur along a narrow zone on most of these ocean ridges. After Van Dover (2000).

to plants, rather like high-altitude rocky ledge or arctic ice on land. Relative to other biomes, the organisms of these areas are determined primarily by physical factors because of the total lack of plants. Also, unlike in air where few organisms can fly and even those only temporarily, many water plants and animals can float and swim more or less indefinitely. Water characteristics and its three-dimensional space thereby provide parameters that control all aspects of animal structure and their interactions. Thus, we can start by designating two deep water, nonphotic, lightless biomes: nektoplanktonic (swimming and floating) and benthic (bottom). These biomes occupy approximately 50% of the Earth’s surface at all water depths below about 100–200 meters. However, they are not likely subjects of synthetic ecosystems in the near future. Because it is so extraordinary, a primary production community not based on light, and probably oceanwide in a linear respect, the hydrothermal vent community of mid-ocean ridges (Van Dover, 2000) is also worthy of the biome designation (Figure 12.3). In the photic nektoplanktonic zone, plants that are not microscopic are rarely important. Thus, while occupying a critical position in planktonic food webs, the plants themselves do not generally provide a community

framework. It is the characteristic of water itself as a volume – the characteristics of light penetration, mixing, and temperature – that provides the structuring elements. The Sargassum brown alga of the Sargasso Sea is an obvious exception, but being rather limited in extent and probably rather transitory in time and space, it is best left as an interesting community of the photoplanktonic biome. Planktonic mesocosms and enclosures are variants that have been the subject of a considerable amount of scientific research. While we discuss the role of plankton in benthic systems, our focus has been on benthic and wetland communities. For readers interested in the living simulation of planktonic communities we suggest Petersen et al. (2003), as a starting point. Thus, we finally come to the bottom biomes within lighted zones of ocean and fresh water. Even here, while there are some parallels with the terrestrial world, to a large extent the controlling factors remain different. First, on land, wind in the form of tornadoes and hurricanes can cause considerable breaking up of plant structure. However, rarely is the major part of biome or community destroyed. A ship on land would remain until it rotted or rusted away. On the ocean, a ship is only ephemeral. When power and intelligence are

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FIGURE 12.4 Coral reef frameworks forming community structure. (A) Acropora palmata and Acropora cervicornis frameworks in shallow water (⬍20 meters); (B) Montastrea annularis buttresses in deeper water (⬎20 meters); (C) a few of the larger organisms occupying the surface of reef framework – many more are subsurface. (A, B) Illustrations by Tom Prentiss. From Coral and coral reefs by T. J. Goreau. Copyright © 1979 by Scientific American, Inc. All rights reserved. (C) After Thurman and Webber (1984). Copyright © 1985 by Scott, Foresman and Company. Reprinted by permission of HarperCollins Publishers.

not used to move and orient the ship, it is destroyed. The point is that ocean waves are not to be resisted by any structure of cellulose. Mangroves, the only marine equivalent of terrestrial forests, occur only on quiet, protected shorelines. Kelp, rockweed, seagrass, and submerged or floating aquatics are the equivalent of land forests, but they survive by being flexible, not by developing massive structures that resist. As we discuss in Chapter 21, kelp forests are certainly deserving of the name in a community sense. However, kelp plants last only a few years at most before they are on the beach, part of the drift, with their biomass designated for another community. Also, under some conditions or perhaps biogeographic regions urchins are abundant and kelp zones can shift to crustose coralline algae zones. Coral reef and algal ridge communities are true parallels with the forests of the land. In these cases, associations of animals and plants together build calcium carbonate structures that greatly modify the environment and can

mostly withstand the waves (Figure 12.4), although intense hurricanes can be very damaging. The parallel with forest building on land is far-reaching, because it is both directly and indirectly that photosynthesis and the subsequent removal of carbon dioxide make massive construction of calcium carbonate skeletal material possible. Because of the wide variety of new niches created by coral growth, coral reefs and algal ridges together, with worm and bryozoan reefs as a subset, are worthy of biome status. Wherever there is sufficient wave action and sufficient shore relief without abundant sand, rocky-shore communities occur, and they have many features in common worldwide. Kelp, rockweed, and Irish moss beds are characteristic and have important structure-creating features that suggest biome status (Figure 12.5). However, there are other biotic elements that are equally important, namely, barnacles, mussels, and coralline algae. Attached to the hard rock substrate, these organisms also

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FIGURE 12.4 (Continued)

build a low-lying structure that creates habitat and modifies the environment. Thus it seems reasonable that the rocky-shore intertidal and subtidal should be accorded biome status. It is true that these are narrow linear features, a few hundred yards to at most a few miles in width, unlike the thousands of square mile areas accorded some terrestrial biomes. However, it is the nature of light and wave action control, having replaced water as a molding key environmental factor, to occur in narrow coastal bands. The rocky-shore biome extends into the tropics. Subtidally, Sargassum and a variety of reds replace the kelp beds. Intertidally the intense sun and drying effects along with heavier herbivores prohibit any equivalent of the rockweed communities. However, here blue-green algae produce extensive black mats that are fed on by snails. Pleistocene limestones are common in this shoreline zone, having been developed as terraces at the last higher sea-level stand about 130,000 years ago. Between solution and scraping by the snails, these

limestones develop an extremely irregular microkarst or iron shore. This community is part of the worldwide rocky-shore biome. Sandy shores, intertidal as well as subtidal, are also worldwide features in which environmental control, wave action, and an abundant supply of sand from a wide variety of sources create a unique, extremely difficult biome, virtually free of plants. This biome is characterized by a few species of rapidly burrowing filterand detritus-feeding macroinvertebrates of several phyla, mostly bivalves and worms, and many species of very small (⬍1 mm) meiofauna. Many of the meiofauna are from diverse “worm” phyla. Some are tiny arthropods belonging to many crustacean groups as well as other classes. In fresh waters, tiny insects and insect larvae are members of the sand-dwelling meiofauna. Finally, we reach the mud bottom, which may or may not be vegetated. Mangroves, submerged aquatic

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FIGURE 12.5 Rocky intertidal zones. (A) Generalized worldwide relationships; (B) west coast of North America; (C) Maine coast. Revised including data from Stephenson and Stephenson (1972), Rickets et al. (1985), Fefer and Schettig (1980), and Carefoot (1977). Similar zones extend subtidally with typically a kelp zone, a leafy red algae zone, and finally a crustose coralline zone. Plant structured communities end at 10–50 meters depending on turbidity and the sediment supply.

vegetation, marshes, and swamps (tree-dominated wetlands) are dominated by their plants. The plants form the structures within which the animal members live and find their food (Figures 12.6–12.8). Each can be usefully given biome status. Finally, even “bare” mud bottoms in the photic zone usually have a diatom film on the surface. The basic point is that a muddy bottom frequently supports a very rich fauna that is adapted in

many ways to life in this environment (Figure 12.9). It is the physical–chemical characteristic of the soft bottom rich in organics and low in oxygen and with an overlying water mass usually rich in plankton that establishes community structure. Table 12.1 provides a classification for marine and freshwater biomes. It certainly is not perfect anymore than the terrestrial biome classification is. However, in

Features of Communities

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FIGURE 12.6 Organisms living within Florida red mangrove communities. After Drew and Schomer (1984) and Britton and Morton (1989).

accordance with the above discussion, the classification is based on the same principles, and it provides a useful reference system within which to discuss and carry out aquatic ecosystem modeling.

FEATURES OF COMMUNITIES Under a given set of environmental conditions, the development of the structural elements of the community from a “bare” surface to one of seagrass, kelp, coral reef, etc., changes the local environment. This allows new organisms that require the cover, the substrate, the food organisms, and more or less light, to enter a community that they would be excluded from based only on substrate. Thus, a developing community alters its own environment and slowly drifts to a different structure. This process, called succession, finally reaches a substable state, the climax community, which may take many months or many years to attain. Normally, disturbing factors such as storms, ice, floating logs, or larger predatory animals continually “knock” the community back to the pioneer or intermediate stages of succession. However, such disturbances usually happen in a patchy way and give rise to heterogeneity in community structure. A wild community is dynamic in its composition; the aquarist should not expect a model to be greatly different.

A now-classic example of these dynamic processes, succession, and disturbance, was described for the rocky intertidal shore of northwestern North America by Dayton (1971). In that region and many other temperate and boreal rocky intertidal zones, mussels (e.g. Mytilis spp.) can become the primary structure-creating member of a climax community covering enormous areas. However, logs or ice driven by waves and the feeding of seastars (e.g. Pisaster) and gulls on the mussels constantly remove large patches of these attached bivalves, allowing several species of barnacles to colonize. As a general principle, great disturbance reduces the number of species. However, a moderate level of disturbance, physical or biotic, results in the highest species numbers (Figure 12.10). A feature of community and trophic structure not yet discussed is the tendency of more complex communities to be characterized by guilds. A guild is a group of species populations that occupies the same or very similar niches. This feature has been most studied in birds and insects but certainly characterizes marine communities such as coral reefs. An example of a bird guild and the resultant resource partitioning is shown in Figure 12.11. This becomes particularly critical in model systems where scaling does not allow the inclusion of all members of the guild and niche overlap allows the utilization of one or a few members to satisfy the need for the niche without overburdening the limited size of the resource in the model.

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FIGURE 12.7 Dominant macroorganisms of a North American, Gulf of Mexico, freshwater coastal marshland. (A) Cat-tail, Typha latifolia; (B) bullrush, Scirpus maritimus; (C) dwarf surf clam, Mulinia lateralis; (D) common rangia, Rangia cuneata; (E) tube-building amphipod, Corophium sp.; (F) small-mouthed hydrobiid, Texadina sphinctostoma; (G) hydrobiid, Texadina barretti; (H) Probythinella Iouisianae; (I) freshwater shrimp, Macrobrachium acanthurus; (J) redwinged blackbird, Agelaius phoeniceus; (K) snow goose, Chen caerulescens; (L) Canada goose, Branta canadensis; (M) American widgeon, Anas americana; (N) blue-winged teal, Anas discors; (O) green-winged teal, Anas crecca; (P) gadwall, Anas strepera; (Q) mottled duck, Anas fulvigula; (R) northern pintail, Anas acuta; (S) lesser scaup, Aythya affinis; (T) shoveler duck, Anas clypeata; (U) Florida marsh clam, Polymesoda maritima; (V) marsh clam, Polymesoda caroliniana; (W) thead-fin shad, Dorosoma petenense; (X) American eel, Anguilla rostrata; (Y) alligator gar, Lepisosteus spatula; (Z) tarpon, Megalops atlanticus; (A1) big mouth sleeper, Gobiomorus dormitor. From Britton and Morton (1989).

Within the biomes discussed above, many communities can be delimited. Particularly within terrestrial ecology, considerable dispute has been engendered over the past several decades as to whether communities and their boundaries exist. The interested reader is referred to Ehrlich and Roughgarden (1987) and Blackburn and Gaston (2003) for a discussion of these

issues. Regardless of the situation in the terrestrial environment, marine, freshwater, and wetland communities do tend to have sharp boundaries. In part this is because water surface, light, and substrate, which is often wave controlled, are the primary environmental community determiners. These parameters usually have considerably sharper boundaries than the

The Magnitude of Biodiversity

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FIGURE 12.8 Organisms living within the submerged aquatic vegetation communities of Chesapeake Bay. After Lippson and Lippson (1984).

temperature and precipitation boundaries of the terrestrial environment, though there is some parallel where topography and rock type are critical controlling factors. In very extensive sand or mud-bottom biomes, the same difficulty in sharply delimiting communities is encountered.

THE MAGNITUDE OF BIODIVERSITY In natural communities the richness of biodiversity varies by orders of magnitude, for example as between

a tropical sandy beach and a coral reef or between a kelp bed and the uppermost intertidal zone in colder waters. Why is this so, and how important is this species count in measuring the success of a model ecosystem? Diversity has two basic forms of measure, richness and evenness. Richness can be simply species number or an equation that weights a species by its abundance. In the latter case, a community with 12 species of the same abundance will be regarded as more diverse than one with 1 abundant species and 11 rare species. Evenness is a separate measure that shows that disparity. In this book, we treat diversity as simply

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FIGURE 12.9 Organisms living within a nonvegetated sandy-mud bottom. After Lippson and Lippson (1984). (A) Stout razor clam; (B) soft-shelled clam; (C) hard clam; (D) gem clams; (E) Baltic macoma. Worms below the intertidal flats: (1) milky ribbon worm, Cerebratulus lacteus (to 4 feet); (2) common bamboo worm, Clymemella torquata (to 6 inch); (3) clamworm, Nereis succinea (to 6 inch); (4) trumpet worm, Pectinaria gouldii (to 2 inch); (5) freckled paddle worm, Eteone heteropoda (to 4 inch); (6) barred-gilled mud worm, Streblospio benedicti (to 1⁄2 inch); (7) red-gilled mud worm, Scolecolepides viridia (to 4 inch); (8) opal worm, Arabella iricolor (to 2 inch); (9) capitellid thread worm, Heteromastus filiformis (to 4 inch); (10) glassy tube worm, Spiochaetopterus oculatus (to 21⁄2 inch); (11) bloodworm, Glycera species (to 15 inch); (12) lugworm, Arenicola cristata (to 12 inch). After Lippson and Lippson (1984).

the number of species, typically with notes as to qualitative abundance. More quantitative diversity measures can be obtained from any modern biostatistical text. The reasons for the differences in species numbers from one type of community to another have been debated for decades. While just about every community parameter, physical and biotic, has been implicated at one time or another, a few stand out as critical: (1) frequency and magnitude of disturbance (physical or biotic); (2) the magnitude of primary production (available food and controlling factors); (3) competitive interactions (the exceptional capabilities of a few species

for growth); (4) spatial heterogeneity (the numbers of spatial niches, physical or biotic); and temperature. The qualitative basis for the magnitude of biodiversity has been brought together in a synthesis called the dynamic equilibrium model (Huston, 1994). In this book, we expand the dynamic equilibrium model by adding spatial heterogeneity. In our presentation, potential productivity refers to all factors that control production, primary or secondary, and thus food availability. It also includes competitive growth potential in that if a large potential for primary production exists or if large amounts of food are available in an animal

TABLE 12.1 Marine and Freshwater Biomes Photic Planktonic/Nektonic

Aphotic Benthic (intertidal ⫹ subtidal)

Planktonic/Nektonic

High energy

Low energy

Coral reefs including algal ridges, worm reefs Rocky shores Sandy Shores

Swamps Mangroves Marshes (including bogs and fens) Submerged vegetation (aquatic/marine, floating, rooted) Unvegetated muddy bottoms (only if disturbed)

Benthic Muddy bottom Rift valley vents

The Magnitude of Biodiversity

FIGURE 12.10 Control of algal species diversity by disturbance created by the grazing of littorinid snails. After Ehrlich and Roughgarden (1987, from Lubchenco, 1978).

community, then a few species capable of utilizing that resource can rapidly increase their numbers and/or biomass to dominate the community to the exclusion of many other species, at least those of the same guild. The ranges of disturbance can be created physically (wind, wave action, mud slides) or biotically (grazing, trampling, etc.). The same is true of spatial heterogeneity, for example, which can be a result of organic structure (coral structures, forest trees) or physical factors (a rough lava flow with caves and tunnels). How these issues relate specifically to the building of living model ecosystems we discuss further below. Biodiversity also has much larger components, namely geographic area and time. The area relationship is shown in Figure 12.12 as the numbers of bird species as a function of island size. The general result, now well accepted in ecology as S⫽ kAz, where S is species number, A is area, and z is a constant that varies slightly with biome or taxonomic group. We use this equation in Chapter 20 to estimate wild coral reef biodiversity from a coral reef model in Chapter 20. In Chapter 2, we described a temperature, area, time physical model for coastal biogeography that was quite successful in identifying global biogeographic regions previously identified based on organisms. Since that model identifies the area of biogeographic regions, it is also possible to use S⫽ kAz to estimate the diversity of an unknown region based on a known

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FIGURE 12.11 Fruit sizes eaten by different fruit-eating pigeons in the South Pacific. After Ehrlich and Roughgarden (1987, from Diamond, 1975).

FIGURE 12.12 Relationship between area and species number of birds on islands in the vicinity of New Guinea. After Ehrlich and Roughgarden (1987, from Diamond, 1973).

region (Adey, 2005). Thus, for many reasons (shorter period of existence, great physical disturbance, low productivity, etc.), more northerly shores should have fewer species than tropical or temperate regions. However, the North Pacific Subarctic is a large area of coast that has existed for 10–15 million years. According to the biogeographic model and S⫽ kAz,

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this should be an unusually rich area of biodiversity, and indeed Briggs (2003) confirms the region as a rich “center of evolution.” More recently, temperature has been directly implicated as a controller of generation time. Additional theories that seek to explain variations of abundance and biodiversity in space and time are reviewed in Blackburn and Gaston (2003).

COMMUNITY STRUCTURE AND ECOLOGICAL MODELS Every ecosystem has to be studied and modeled on its own terms. Nevertheless, there are some general principles that can be applied to the development of an ecosystem in a microcosm, mesocosm, or aquarium. A successful model ecosystem results from the placing of a community or organisms within its appropriate structure, whether physically or biologically derived, and within the framework of a given set of physical parameters – temperature, salinity, waves, current, etc. Although one would necessarily establish all of the physical parameters of a model before adding the living community, the planning of community structure, and the engineering techniques needed to achieve the proper physical parameters go hand-in-hand. A general approach to establishing community structure within living models is:

must provide the physical structure (e.g. gorgonians), planktonic food may have to be included early on. (5) Carry out structuring in a block-transfer process. That is, do not try to remove small microorganisms, soil, mud, or any small invertebrates associated with the bases of the plants or other substrate. Bring them along with the structuring elements. (6) Repeat the process in as many small units or injections as possible. Each injection will successfully introduce more microspecies or young plants and animals. (7) Begin introduction of the symbionts (e.g. live corals) and the smaller animals and fish, also by a multiinjection process, as the plant or shell communities establish themselves. (8) Finally, tentatively experiment with the larger animals to learn the ecological capacity of the system. When overgrazing or overcropping is apparent, remove the offender, and try another species. Another approach is to allow the larger organism only a short period of time in the model, removing it to a holding system or alternate model (assuming it is easy to catch). (9) Watch for intense competition for limited resources such as space or food and cull when necessary. (10) Compare the model to the analog over as wide a range of physical, chemical, and biotic parameters as possible.

SCALING AND REPRODUCTION (1) Establish the boundaries of the wild analog community or communities. Obtain as much about pre-existing information as possible and add extensive observation. Field guides, especially when provided with an ecological overview, can be extremely helpful, and having a specific wild analog to compare can be a critical element in success. Also, determine the source of the energy (food) that drives the ecosystem. In many cases this energy supply will result from establishing community structure. In other cases it will have to be supplied (see Chapter 6). (2) Develop species lists and determine what species are the structuring elements. Learn what provides primary modification of physical space and supplies habitat – plants, animals, substrate, or physical factors such as breaking waves. (3) Determine the relative numbers of each species. Most important, determine which larger plants or animals are always present in dominating size or numbers. (4) Begin community development by physical structuring with the dominant plants that are present and/or substrate or animal skeletal units. Provided the proper environment is present, these units will normally survive for some time without significant animal interaction. In the few cases where live animals (rather than skeleta)

We have discussed the difficulties of keeping larger organisms, particularly higher predators in model ecosystems. Size is of obvious importance, but so is behavior. The predator or specialized herbivore that requires a large territory to obtain enough food can only be included in a model with special manipulation, if at all. Reproduction is a critical form of behavior. For many small plants and invertebrates, reproductive success occurs abundantly in ecosystem models, though in cases with larger, longer-lived planktonic larvae this can depend on the nature of pumping and filtration. For some fish, particularly those that protect their eggs and hatchlings in some manner, such as cichlids, reproductive success in ecosystem models is likewise ensured. However, for many fish a fairly large territory, in the form of low egg or larval predator density, sometimes the open ocean, is required. If these species are preyed on, or as they eventually age, they must be occasionally added to the model, from the wild or from special hatchery or perhaps refugium environments. In the wild, as we have noted, species diversity is a function of area, in part because of the increase in spatial heterogeneity, and while half the total species of a given biome might exist for centuries in a few tens of

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Model Diversity

acres, the remainder would require hundreds of square miles. Nevertheless, local populations of many species are forever on the verge of extinction due to random or periodic unfavorable events. Small remote island populations live constantly on the verge of extinction, as shown by the devastating effects of the arrival of humans and their animals, both domestic and camp followers (Quammen, 1996). Very large areas, up to the largest continents and oceans, show more species not just because of the variety of habitats but because extinction is unlikely to occur in many local populations at the same time. We have a much better understanding of these matters in the terrestrial world where forest and mammal preservation has become a matter of great concern. Harris (1984) has developed a model for conservation of the biotic diversity of forests that is based on an archipelago of protected habitats or refugia. In the ecosystem modeling described in this book, plant communities are established in accordance with species dominance and abundance in the wild analog. Some changes in model populations occur with time and generally the plant community is allowed to selfadjust. The larger animals, particularly those high on the food chain or with complex life cycles, are manipulated to maintain their role, while the remainder of the animals able to successfully fit the model are allowed to freely develop populations, based on several months of repeated community block or individual injections. While studies of the population ecology of ecosystem models and how they relate to the wild are certainly needed, it is assumed that the basic principles of Harris’ model apply. Thus, after economic constraints have determined the maximum size of the model, then refugia are added with the intention of circumventing obvious population constraints of selected elements of the community. Most of our refugia have been directed toward freeing attached fleshy algae, soft-bottom invertebrate populations, and plankton from severe predation by fish and larger invertebrates (particularly crabs and lobsters). Several of these refugia are described in Chapters 20–23. In general, the semistability that is achieved in community and population structure in the wild over large areas, and at time scales of centuries and millennia, is achieved in microcosms, mesocosms, and aquaria by the manipulation of space (refugia) and, when necessary, the populations themselves. Extensive studies have been undertaken to determine the effects of scale on microcosm/mesocosm modeling. The MEERC (Multiscale Experimental Ecosystem Research Center) group of the University of Maryland extensively studied this phenomenon for Chesapeake Bay models, and anyone attempting serious quantitative research should consult their summary review (Petersen et al., 2003). The basic conclusions are included in the list

given above and can be re-stated as: know the analog ecosystem well; attempt to overcome the more obvious scaling problems, particularly the relationship between planktonic and benthic elements, and re-run the system (for months to years); verify the results (biodiversity and physical–chemical); and adjust the parameters.

MODEL DIVERSITY As we have discussed, a basic principle of the longestablished field of island biogeography is the relationship between area and species number. As we mentioned above, the potential for extinction of local populations of any given species is probably a factor in this relationship. Probably of considerably greater importance is the inevitable increase of spatial heterogeneity, or the number of spatial niches, with increase in area. Finally, the puzzle of rare species remains a mystery: Why are there so many, and how do others continue to exist in the face of formidable competitors and random physically based extinctions? If one continues to sample a habitat for species (as shown in Figure 12.13

FIGURE 12.13 Numbers of species of aquatic vascular plants in the freshwater streams of the Piedmont Province of the Chesapeake Bay Watershed. The streams have been separated into high-quality and low-quality streams based on water chemistry; the biodiversity loss in low-water quality streams is highly significant. Note, however, that repeated samplings at different sites in each stream are necessary to obtain species numbers that approach the actual biodiversity of the whole streams. A single sample from a high-quality stream intended to establish an aquarium-sized model of the whole stream will on the average have nine species. Twenty samples will provide 38 species. Thirty-eight species are not likely to remain in a model of such a stream. However, how does one compare the approximately 20 species that are likely to remain in the model after several years with the wild analog in terms of “success” in modeling? Is 20 species 50% or twice the wild diversity? From Small et al. (1996).

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for the diversity of macrophytes in streams of the North American Central Atlantic Coast area), cumulative curves do not reach saturation. Presumably the search could continue in space and time until all known macrophyte species in eastern North America are eventually tallied. The problem becomes even more difficult in deep-sea sampling for benthic invertebrates where the sampling itself requires a major and costly effort (Gage and Tyler, 1991). It remains questionable whether rare and uncommon species play any significant role in ecosystem function; however, it seems clear that some rare species, difficult to impossible to find in the wild, appear repeatedly in some microcosms and mesocosms, suggesting that these models may act as refugia. Thus, when one creates a small functioning model of a much larger wild ecosystem, in most cases one seeks to model the entire ecosystem (recognizing the extreme flexibility of definition in this term), rather than a wild patch the size of the model itself. Aside from the mobile species that would flit in and out of any modelsized wild area, and would have to be simulated as we discussed above, and with exclusion of the rare and uncommon species, the diversity of a model seeking to recreate species diversity as appropriate for a wild area the size of the model would not be difficult. It would perhaps be an exercise of limited value. A more appropriate approach for a model of 100 square meters of rocky shore, for example, would be to sample many such areas in the wild and create a theoretical mean or composite, based on species numbers. However, just as each of the sample patches in the wild changes with time, so would the model “patch” change, and invariably be reduced in species number if there is no contact with the larger wild ecosystem. This is a conundrum that is best resolved by considering a local island (patch reef, rocky outcrop, etc.) as the minimum for model diversity. This number can be increased to a level that would almost certainly appear as the saturation curves shown in Figure 12.13, by increasing the number of refugia in the model. However, perhaps it will suffice to say that by increasing patchiness and, effectively, spatial heterogeneity, in small scale, appropriate to the model, species diversity is increased much as it is in the wild, but at small scale. While continued introductions to a model might seem to be against “the rules,” this happens constantly in the wild in both islands and patches. A core element of island biogeography theory has been the diversity balance achieved from the relationship between extinction and new immigrants from outside. In Chapter 22, we describe a complex Florida Everglades mesocosm, a greenhouse-size complex of mangroves, coastal, and freshwater communities that was operated for 4 years with a small allowance for

introductions as needed and then for 4 years of virtually total closure (see also Adey et al., 1996). At the end of the first 4 years, self-organization of introduced species had led to a very “recognizable” Everglades with the major structural elements intact in their typical ecologically dominant roles and over 600 counted species (some taxonomic groups not being tallied). After 4 years of closure, of the major plant and animal groups tested, species diversity was moderate, with more than 300 species maintaining populations. Of the common invertebrate and fish species that failed to maintain populations in the mesocosms, most were caused by identifiable omissions in mesocosm structure (mostly absence of an open water refugia for planktonic larvae). Some species absences, or failures to reproduce, were quite puzzling. Although extensive field studies to determine the mean diversity of this size patch in the wild have not been carried out, it seems apparent that the model has at least the relevant number of species. As expected, the species array of the mesocosm is considerably reduced from that of the much larger area of the wild Everglades. A more interesting example is the “home” coral reef microcosm described in Chapter 20. At 532 counted species (with a number of important groups uncounted) and using the widely accepted area/diversity relationship (Reaka-Kudla, 1996), wild coral reefs in comparison should have a diversity of well over 1.5 million species. Yet only about 200 000 have actually been counted. Does this mean that, after many years of virtual closure, this model reef has a much higher diversity per unit area than wild reefs? Or, could it be that rare species in the model are in a refugium, develop larger populations, and are easier to locate? Certainly the diversity of wild reefs is much greater than we now recognize; but how much greater? A major field study currently underway in the western topical Pacific is suggesting a count of 2–3 million macrospecies. With reference to Chapter 20, another feature of complex ecosystems that we need to further appreciate before we can evaluate the diversity of ecosystem models is that of higher-level taxa. This small reef has at least: 4 kingdoms; 27 phyla; 45 classes; 94 orders; 231 families, and 344 genera, to contain the 532 species. Although biodiversity data equivalent to that in Figure 12.13 from the analog coral reef does not exist, it is apparent that higher order diversity does not suffer nearly as much from scale modeling as species diversity. It is likely that we are seeing the equivalent of the “guild effect.” Species of the same family/genus often are similar to each other in behavior function. The model ecosystem will select from a taxonomic “guild” the most “efficient” species; or in other terms, the niche width is expanded for each successful species.

References

Thus, we leave this issue with many questions. However, there is little question that, by any measure, properly constructed model ecosystems can contain very high levels of biological diversity.

SUMMARY There is no fixed answer for what the number of species should be in a successful ecosystem model. If the object is to create a model that is a cross section of a larger ecosystem with more spatial heterogeneity that occurs at model dimensions in the wild, and if the understanding and capability for such modeling that we describe in this book are fully employed, then species numbers will lie somewhere between those of a wild area that equals the model and the full ecosystem. If continual injections of critical species are allowed into the model (as they are to patches in the wild), and considering the likelihood that many rare species are favored in models, species diversity may indeed be higher in a model than in the typical hectare/acre-size wild system that one would typically use as an analog. One of the greatest difficulties in framing a precise statement of species diversity in models is the same as the one that the ecologist faces in the wild. The large number of specialists required to make a fully definitive statement of diversity is generally financially prohibitive and in addition if such an array of specialists were to be available, extreme efforts would have to be employed to keep the disturbance of collecting and analyzing from being the primary defining characteristic of both model and wild system. Depending on the nature of the ecosystem being modeled and the extent to which the principles of ecological engineering have been applied, a microcosm or mesocosm will have hundreds to perhaps thousands of species. However, ultimately, the test of success in a model is not likely to be species diversity, per se, but rather trophic structure – the number of species maintaining populations in food webs that characterize the wild analogs – the subject of Chapter 13.

References Adey, W. (2005) Marine plant diversity. In: Plant Conservation. G. Krupnick and W. J. Kress (Eds). The University of Chicago Press, Chicago. Adey, W., Finn, M., Kangas, P., Lange, L., Luckett, C., and Spoon, D. (1996) A Florida Everglades mesocosm – model veracity after four years of self organization. Ecol. Eng. 6: 171–224. Blackburn, T. and Gaston, K. (2003) Macroecology: Concepts and Consequences. Blackwell Publication, Malden.

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Bonner, J. T. (1988) The Evolution of Complexity. Princeton University Press, Princeton, New Jersey. Briggs, J. (2003) Marine centers of origin as evolutionary engines. J. Biogeogr. 30: 1–13. Britton, J. and Morton, B. (1989) Shore Ecology of the Gulf of Mexico. University of Texas Press, Austin. Carefoot, T. (1977) Pacific Seashores. Douglas Ltd., Vancouver. Carlton, J. (1999) The scale and ecological consequences of biological invasions in the world’s oceans. Chapter 13. In: Invasive Species and Biodiversity Management. T. Sandlund et al. (Eds). Kluwer Academic, Boston. Chase, A. (1987) Playing God in Yellowstone National Park. Harcourt Brace Jovanovich, San Diego. Dayton, P. (1971) Competition, disturbance and community organization: the provision and subsequent utilization of space in a rocky intertidal community. Ecol. Monogr. 41: 351–389. Drew, R. and Schomer, N. (1984) An Ecological Characterization of the Caloosahatchee River/Big Cypress Watershed. US Fish and Wildlife Service FWS/OBS-82/58.2. Ehrlich, P. and Roughgarden, J. (1987) The Science of Ecology. Macmillan, New York. Fefer, S. and Schettig, P. (1980) An Ecological Characterization of Coastal Maine. US Fish and Wildlife Service FWS/OBS-80/29. Gage, J. and Tyler, P. (1991) Deep Sea Biology: A Natural History of Organisms. Cambridge University Press, Cambridge. Goreau, T. F., Goreau, N. I., and Goreau, T. J. (1979) Corals and coral reefs. Sci. Am. 241: 124–136. Harris, L. (1984) The Fragmented Forest: Island Biogeography Theory and the Preservation of Biotic Diversity. University of Chicago Press, Chicago. Huston, M. (1994) Biological Diversity: The Coexistence of Species on Changing Landscapes. Cambridge University Press, Cambridge. Lippson, A. J. and Lippson, R. L. (1984) Life in the Chesapeake Bay. Johns Hopkins University Press, Baltimore, Maryland. [Illustrations by Alice Jane Lippson.] Petersen, J. et al. (2003) Multiscale experiments in coastal ecology: improving realism and advancing theory. Bioscience 53: 1181–1197. Purvis, A., Orme, C. D. L., and Dolphin, K. (2003) Why are most species small-bodied? A phylogenetic view. In: Macroecology: Concepts and Consequences. T. Blackburn and K. Gaston (Eds). Blackwell Publication, Malden. Quammen, D. (1996) The Song of the Dodo. Scribner, New York. Reaka-Kudla, M. (1996) The global biodiversity of coral reefs. A comparison with rainforests. In: Biodiversity II: Understanding and Protecting Our Natural Resources. M. Reaka-Kudla, D. Wilson, and E. O. Wilson (Eds). Joseph Henry/National Academy Press, Washington, DC. Rickets, E., Calvin, J., and Hedgpeth, J. (1985) Between Pacific Tides, 5th edn. Stanford University Press, Stanford, California. Small, A., Adey, W., Lutz, S., Roberts, D., and Reese, E. (1996) A macrophyte-based rapid biosurvey of stream water qualityrestoration at the watershed scale. Restor. Ecol. 4: 124–145. Stephenson, T. and Stephenson, A. (1972) Life Between the Tide Marks on Rocky Shores. W. H. Freeman, San Francisco. Thurman, H. and Webber, H. (1984) Marine Biology. Merrill Publishing, Columbus, Ohio. Valentine, J. (1985) Phanerozoic Diversity Patterns: Profiles in MacroEvolution. Princeton University Press, Princeton, New Jersey. Van Dover, C. L. (2000) The Ecology of Deep Sea Hydrothermal Vents. Princeton University Press, Princeton, New Jersey.


C H A P T E R

13 Trophic Structure Ecosystems and the Dynamics of Food Chains

An ecosystem is a structured relationship of living organisms in a given environmental framework that receives and utilizes a flow of energy. Many chemical elements also flow or are “cycled” through an ecosystem, and system function is usually measured by the flow of carbon, oxygen, nitrogen, or phosphorus. However, energy flow (the creation and degradation of food) is the crucial element. While only a few species might be present in a very simple ecosystem, “complexity of organization seems to be a key ingredient in ecological persistence” (Conrad, 1976). O’Neill et al. (1984) argued “for a correlation between ecosystem stability and the functional redundancy of the system” and cited a microcosm study of van Voris et al. (1980) as proof of the concept. The concept that species diversity provides ecosystem stability has been debated for years; it now tends to be unacceptable to most ecologists (see, however, Waldbusser et al., 2004). However, multiple species at all levels in an ecosystem must be considered for the operation of model ecosystems because species immigration may be limited. While many species are desired, only if a working trophic structure can be established will the model be successful. This in itself is not necessarily difficult. A number of studies of insect community re-establishment have shown that trophic structure (i.e. a food chain or web) is developed regardless of the species involved (O’Neill et al., 1984). In a model, however, the cultured ecosystem must be open to a wide range of immigration for this to happen. In short, the builder or operator must allow the possibility for the introduction and establishment of a high diversity of species at all levels in the food chain or web. Among many ecosystem modelers there seems to be a view that the ideal of achievement is a totally closed system. However, rarely does this happen in the wild,

and when it does, the likely result is the extinction of many species with the evolution of bizarre forms. Management of the import and export of species elements is a more appropriate and dynamic analog. Traditional aquarium science revolves around feeding and managing the waste particulates, nutrients and oxygen reduction that results from that feeding. Aquarium culture has evolved rapidly in the past few decades and the range and types of “feeds” available for aquarium systems has grown accordingly. Delbeck and Sprung (2005) provide an excellent survey of feeding options available for coral reef systems. Most important in the current context, they discuss a wide variety of live (and frozen) plankton feeds and the techniques for their culture. Although microcosm and mesocosm operators will need to consider their specific planktonic feed requirements based on an analog, this is a very useful resource. Traditional bacterial filtration and the more modern skimming or foam fractionation systems remove plankters and reproductive stages and, depending on the system being modeled, this necessitates the continual addition of “extra” feed to account for this. If display, and not modeling, is desired, as long as total export approximately matches import and nutrients do not rise (or oxygen levels fall), the current adaptations of traditional methods can be quite adequate. In modeling an ecosystem, the general approach is very different from the most modern aquarium approaches, and the specific approach can vary widely from one analog ecosystem to another. The question to be asked first is what is the energy input in the wild system being modeled? Second, how is that physical energy converted to chemical energy (if that has not been done before import)? And third, how is that energy, now as “food,” distributed through the ecosystem in the form of a food chain, or more appropriately a food web

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or trophic structure, since the pattern is usually quite complex. Typically in a benthic aquatic ecosystem, there is a planktonic or particulate input, which can be very large and central to the entire modeling effort, or it can be quite small, a minor side issue. In practical modeling, where the model itself, by economic necessity, might be quite small, the situation can become more complex, as higher predators or larger organisms cannot find enough natural food. Thus, one is left feeding the equivalent of import at both the “bottom and the top of the chain.” In human culture, we are a population adapted over millions of years to a variety of wild foods. We are beginning to recognize that in industrializing human nutrition, we are “creating” many modern diseases (such as some cancers, diabetes, and heart disease) by building foods that are efficiently produced for energy supply, are shipped easily, and have minimum spoilage. If we cannot, through modern technology and with the support of a major part of our gross national product, craft a food supply suitable for the human species, how can we hope to artificially supply an ecosystem of many different species with often very different food needs? It is clear that wild and model ecosystems must be operated through a natural food chain of high organism diversity. Out of economic necessity we are often likely to simulate a portion of a model ecosystem food supply with an artificial feed. Where this is done, it is essential to try to simulate the wild food supply as closely as possible. The culture of an ecosystem is rather different in basic concept from the culture of individual organisms. To emphasize this basic point, we quote from Wyatt (1976): Despite all efforts to survive, the natural destiny of almost all animals and plants in the sea is to be eaten before maturity is attained. It is only the few which live long enough to perpetuate their species. The best that most species can do is remain one step ahead of those which prey on them, and so avoid extinction. So eating and being eaten are central to the whole science of ecology, and it is these two topics which are emphasized here.

Although some manipulation will probably be employed to adjust longevity of certain species in a captured or cultured ecosystem, as a whole, an ecosystem will not function without energy flow and the daily pattern of predator eating prey at all levels. Trophic or feeding structure must develop and be maintained or there is no ecosystem. If “eat and be eaten” seems the antithesis of the reason for culture in the first place, before getting into the basic subject of the chapter we remind our readers of several critical elements discussed earlier. The primary purpose of this book is to assist scientists, aquarists, and hobbyists in the re-creation of marine, aquatic, and wetland ecosystems in living models. While

establishing ecosystems in living models may be more or less difficult to accomplish, depending on size and complexity, this is a crucially important endeavor (see Petersen et al., 2003). On the scientific side, microcosms have been used to establish some important ecological principles (Beyers and Odum, 1993; Small and Adey, 2001). Although computer and mathematical modeling of ecosystems has been extensively used in the past several decades, some well-known ecologists have considered the mathematical model of little value (Andrewartha and Birch, 1984). In the realm of public education, a broader, heuristic, day-to-day understanding of ecosystem function by a larger public can be crucial in alerting mankind, not just environmentalists, to the primary problems of the 21st century. Some scientists maintain that “sustained life under present day conditions is the property of an ecological system rather than a single organism or species” (O’Neill et al., 1984). This suggests that while the culture of individual organisms may be important to understanding the intricacies of function of each species, only by working with whole ecosystems will we truly begin to understand the whole as well as the parts. It is highly unlikely that humans can be totally supported by our own monocultures. Since we are dominating the Earth to the point where, increasingly, natural ecosystems do not have the freedom to function on their own, we must quickly learn the techniques of culture of ecosystems. Finally, it is clear that many ecosystems and some biomes (coral reef, e.g.) are likely to disappear (or virtually so) before the inertia of human expansion can slow and take ecosystem function and the human requirement for this function into account. The fossil fuel, carbon release, global warming and sea level rise sequence is just one example of many, and it is important to the thesis of this book that a large mesocosm was used in part to demonstrate the effects of CO2 rise on coral reef function (Osmond et al., 2004). Assuming we come to our senses, there will be ecosystems that we will wish to restore, and, as we noted in the last chapter, hypotheses as to the role of invasive species in trophic structure examined (Carlton, 1999). While surely there is much yet to learn, it is hoped that the understanding in this book will assist in providing the first steps to aquatic restoration.

ENERGY CAPTURE AND FLOW All organisms, and therefore all ecosystems, require a source of energy to operate. Virtually all of the energy of Earth’s ecosystems derives from plant photosynthesis. In the most efficient cases, such as wetlands and coral

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reefs, plants convert about 5–6% of available sunlight to chemical energy. Generally the efficiency of solar energy capture is less, typically 2–3%. In any case, the bodies, parts, or particulates of plants become the food for many animals, sometimes by simple routes, in other cases by complex routes. For other animals, the food energy comes in the form of animal bodies or their parts. Typically, some of the energy in the available food is used for motion, construction of tissues, internal circulation, reproduction, etc., and is then discarded as low level and thus usually unusable heat. The remainder, typically anywhere from 20% to 80% of the supply, is simply passed on, altered in character perhaps, but available for another user. This process is repeated over and over again, and, unless some of the original biomass or “food” is buried in geological storage, such as in a swamp, all of the original energy is either temporarily stored as structural energy in organisms (potentially more food) or is lost as low-level heat to the environment. While this loss might be said to represent a low efficiency of transfer, it must be remembered that most of the loss was used to “drive” the system, to move muscles and carry out the necessary building of required chemistry. Ecologists speak of the transfer efficiency of an organism, which is typically 10–20%. This efficiency is calculated as the new weight or biomass developed, as a percentage of the amount of food eaten. In an adult animal, efficiency could be zero or close to it, but in truth 50% or more may have been used to drive the organism. If one is producing chickens or cows, and weight is money, the transfer efficiency is extremely important. If one is running an ecosystem, it is not of overriding interest. In ecosystem modeling, assuming equivalent energy input by primary production or import, a completely efficient model ecosystem would be one that uses as much energy as the wild analog and processes that energy in as complex a manner. In a scientific modeling endeavor, these numbers can be estimated; in the aquarium effort they will likely never be calculated. Once thought about, however, these concepts will place the modeling effort in proper perspective. A new wild community may grow for a few years, perhaps even a century or two in biomass. This process, called succession, sooner or later must stop (without geological storage or export to another community) and all input energy must be used and converted to low-level heat that escapes. The model ecosystem should be no different from the wild. The time frame for balance is shorter, generally much shorter. Depending on the arbitrary definition of an ecosystem, all such systems must produce their own food (thus energy) through plants or receive it from producer communities. If one is operating a producer community and a consumer community separately (e.g. a kelp bed

and a mud flat), the mechanisms for food transfer and nutrient return must be allowed for. If the producer community is not present, and the aquarist is adding food, then either the food and feces must all be used, and the excess nutrients removed as they would be flushed away by the ocean, for example, or the true equivalent of geological storage is required. If the consumer community is not present when stable biomass maximum is reached, then assuming required food is being added, excess biomass (e.g. leaf fall) must be removed, or again the true equivalent of geological storage must be made available. In Chapters 7–11, we discussed wild and captured ecosystems in terms of the cycling of the major required, and then discarded, elements. In Chapter 12, the ecosystem was treated as a community; we talked about the living organisms themselves, their numbers, and how they behave and react to each other. Here we treat the ecosystem and its modeled counterpart as a functioning machine. We choose to look at this machine from the point of view of how it captures and uses energy or how it produces and then uses food. In a structural sense this is what the ecologist calls trophic structure, a food chain or a food web. The ecologist often measures both incoming solar energy and plant gross primary productivity (typically as daytime released oxygen plus total oxygen used in respiration). Primary productivity (as biomass produced in the absence of grazing) is rarely used to determine actual energy transfer through a food web measured by converting the appropriate food or body tissues to heat (determined as energy with a bomb calorimeter). Most typically, the critical measure is related to carbon in body tissues or exchanged carbon dioxide or oxygen. One gram of dried algae provides about 5.3 kcal, but on the basis of carbon content or carbon moved it is about 15.8 kcal/gC. Although the energy actually available in a gram of food is dependent on the type of food (carbohydrates, fats, proteins), 1 g of dried food provides about 5.5 kcal (1 cal ⫽ 4.19 J) (Valiella, 1984). This is a reasonable approximation for understanding the energetics of something as complex as an ecosystem, and the technique has been applied to some model ecosystems (Beyers and Odum, 1993).

FOOD WEBS In the mid-1950s, H. T. Odum carried out a detailed study of the trophic structure of a freshwater spring and its resulting stream in central Florida. Dividing the organisms in the spring into producers (plants), herbivores, carnivores, top-level carnivores, and decomposers, Odum produced the biomass pyramid shown

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in Figure 13.1. In this case the amount of plankton present was minimal and was ignored. This now classic and often cited study shows a food chain or trophic structure as static. However, it is probably typical for very simple ecosystems and not far from what one would expect to find in well-simulated microcosms and aquaria. In this very simple pyramid one can see one of the problems of all food chains. One can also see part of the reason they are often called food webs and are typically oversimplified. The stumpknocker (redear sunfish, Lepomis microlophus) eats small invertebrates, especially snails, that are in turn feeding on algae. However, it also eats the algae and the mixed small animals (aufwuchs) that coat the stems and leaves of the aquatic higher plants, the macrophytes. Also, the pyramid concept does not really include the decomposers. The decomposer biomass line in this case is simply set off to the side, presumably to indicate that it receives from all other elements of the pyramid. In another diagram, developed for a Georgia salt marsh (Figure 13.2), a slightly different approach to presenting a simple food web is taken. Here the primary decomposers, the bacteria, are included within the web. However, an attempt is made to add the obvious complexity that many “herbivores” also eat bacteria, which are the primary decomposers of organic waste. This system and its food web could easily be simulated in microcosms. However, the place of the birds and the racoon would be taken by the aquarist. A plankton community, brought in by the tide, could also be added and the aquarist could generally simulate this aspect by artificial feeding. In this case, an Algal Turf Scrubber (ATS) would not be required to remove

this imported biomass, since the unused particulates gradual accumulate in the marsh, and is partly used by the infauna. However, if there were not an external source of sea water from the open coast, an ATS could be used in a semi-closed system to simulate the quality of water in that tidal reservoir. A more complex food web for a rocky, subtropical shore is given in Figure 13.3. In this case a large part of the food chain above the producer community is made up of molluscs and finally a top carnivore (TC), a starfish. Fish and birds undoubtedly play a subsidiary role in this web. This ecosystem would also not be difficult to achieve in model. The plankton equivalent would have to be added and the aquarist would harvest and control

FIGURE 13.2 Food chain in a North American East Coast salt marsh. After Levinton (1982, from Teal, 1962). Reprinted by permission of Prentice Hall, Englewood Cliffs, New Jersey.

FIGURE 13.1 Biomass pyramid for Silver Springs, Florida (g/m2 dry biomass). P, primary producers; H, herbivores; C, carnivores; TC, top carnivores; D, decomposers. After Odum (1957).

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FIGURE 13.3 Rocky shore food web from the northern Gulf of California. This web is dominated by the starfish Heliaster. The Columbellidae are the dove shells, algae-eating snails; Hexaplex and Muricanthus are murex snails; Morula and Cantharus are small snails that feed primarily on barnacles; and A. tubeculata and A. angelica are predatory snails of the genus Acanthina. After Levinton (1982, from Paine, 1966). Reprinted by permission of Prentice Hall, Englewood Cliffs, New Jersey.

the top predators. Here, as in the previous example, the modeler could use an ATS to control the quality of the offshore water. An interesting offshore variant is the food web for the North Sea herring shown in Figure 13.4. The web is centered on this single, albeit extremely important, fish, but shows how its feeding habits change as it matures. This web does not indicate the many predators on the herring itself, nor does it complete the cycle by showing the decomposer part of the local ecosystem. It begins to demonstrate how complicated a realistic trophic structure can become for a wild community and why some scientists argue that formal trophic structures are only heuristic devices. While acknowledging that such complexity can be “almost malevolent,” Pimm (2002), in his classic and now reprinted (with updated Foreword) treatment of the theory of food webs, goes on to show how food webs have a strong theoretical basis. In any case, they can only help to provide a better feeling for the dynamic aspects of ecosystems. This herring food web would obviously be very difficult to achieve even in a very large mesocosm. Finally, so as not to neglect fresh waters and to indicate that freshwater food webs can be as complicated as those in the marine world, we provide a web for the upper Nile River in Uganda (Figure 13.5). In this case, the crocodile becomes the top predator, feeding on virtually all organisms in the middle and upper levels of the web. With the aquarist playing the role of the crocodile itself as well as the birds and mammals, this web

and its community probably could be simulated in a mesocosm. A full understanding of energy flow in a model ecosystem is likely to be undertaken only in a mesocosmscale research project. An ecosystem energy flow characterization is a quantification and summary of diagrams like Figures 13.4 and 13.5. In Figure 13.6, for Lake Ontario, the producer community is not shown. This is a benthic community and the total energy input (6856 cal/ m2/day) represents organic detritus from plankton and land runoff. Of this detritus, 1586 cal/m2/day, rich in bacteria, is eaten by a variety of detritivores from which the carnivores and TC derive their food and energy resources. Note in this case, besides the large amount of unutilized and eventually buried energy in the form of subfossil organic material, a small quantity is also exported in the form of emergents (flying insects).

FOOD WEBS IN MODEL ECOSYSTEMS Whether carried out formally or informally, a model food web should be developed for all model ecosystems simply to provide a guide. In Figures 13.7–13.9, we show such simplified webs for a microcosm coral reef, a Maine rocky shore and bay microcosm, and a subtropical Florida Everglades mesocosm, respectively. Particularly note that in two of these systems there is an energy supplement (feeding) intended to simulate primarily the plankton supply from the larger body of

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FIGURE 13.4 Planktonic food web of the North Sea herring. The food utilized by the herring gradually changes as the fish matures. After Cushing and Walsh (1976, from Hardy, 1924).

water that is not possible to present to the model. This is quite acceptable as long as the equivalent nutrients are exported, or possibly sent to a fossil reservoir within the system. As we discussed in Chapter 11, this is the primary function of the ATS, although any full and controllable method of export could perform the same function. One might simply harvest parts of plants from the community itself and remove them, though by that means it would not be possible to smooth out diurnal effects. The primary difficulty with traditional filters is that they do not provide full export of all elements. While carbon may be released as CO2 and if eutrophic enough, some nitrogen as N2, much nitrogen, phosphorus, and other nutrients remain. Also, even if filters were frequently and automatically backwashed to partly overcome this objection, they cannot discriminate between desirable and undesirable particles, including living organisms in the water column. While the use of foam fractionation can provide an export mechanism with captured particulate and dissolved organics, it cannot directly remove nutrients and likewise does not discriminate between particulates and desirable plankters and reproductive stages.

In a massive effort to bring together a generation of research work on laboratory microcosms and mesocosms, Beyers and Odum (1993) applied primarily energy flow models to dozens of these systems. This approach was developed by those authors in a framework of demonstration of ecological principles. For the researcher and hobbyist interested in parallel mathematical and living modeling approaches, their book is an indispensable starting point.

ESTABLISHMENT OF FOOD WEBS Initially, some knowledge of both the feeding capabilities and preferences of organisms and the trophic structure of the community in question is necessary to properly manage a microcosm of a natural community. As we discussed in the previous chapter, it is possible to model, in closed form, any marine or aquatic ecosystem. However, the systems most interesting to the aquarist, and those with which we now have considerable experience, are shallow, benthic communities.

Establishment of Food Webs

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FIGURE 13.5 Food web of the River Nile, Uganda. Varanus is the monitor lizard. The remaining generic names are fish. From Cott (1961).

FIGURE 13.6 Energy flow in an arm of Lake Ontario, Canada. IM, incoming organic matter; NU, not used (geological storage); RCOM, respiratory losses; E, flying insect loss. The boxes represent biomass (in kcal/m2) of microorganisms (M), detritivores (D), carnivores (C), and top carnivores (TC). The width of the arrows represents energy flow as cal/m2/day. From Johnson and Brinkhurst (1971).

When these communities have hard bottoms, the base of the food chain – or web – is formed largely by benthic (attached) algae or by invertebrates with symbiotic algae. On soft bottoms flowering plants are often included with the algae. Many of these benthic systems also have a detrital or particulate component. In some cases, this component provides the dominant energy supply. The problems of handling attached plants and algae in a closed microcosm are relatively straightforward. Managing this lowest or producer level in the microcosm involves four primary factors related to the natural system being modeled: type of substrate, available light, grazing rate (or rate of removal of plant biomass), and the cover and biomass of the plants themselves. Prior to the introduction of the first plant samples, the essential physical ingredients discussed in Chapters 2–6 should be in place, including sufficient light of appropriate quality, proper temperature, and water motion. Some plant species will be immediately successful. Others will require repeated introduction. A sufficient standing crop of plants, algae, or higher plants approximating that in the community being

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FIGURE 13.7 Simplified food web for the Smithsonian coral reef model ecosystem (see also Chapter 20).

modeled should be allowed to develop before the introduction of a significant community of grazers. There are several ways to gauge the correct ratio of the microcosm’s standing crop to that of the wild: visual approximation, plant length, dry or wet weight, and primary production measured by oxygen release (see Chapter 8). Larger grazers such as fish, urchins, and crabs can be added according to their approximate abundance or biomass in the community being modeled. Because this involves guesswork and trial and error, it is advisable to work initially with too few rather than too many of the larger herbivores. If plants become too abundant, grazing can be supplemented with harvesting by hand. Additional grazers can then be added one by one until the desired biomass or standing crop of plants is achieved.

Any system being modeled is likely to contain not only larger grazers, typically fish, urchins, snails, and crabs, but also numerous micrograzers such as amphipods and isopods and, in fresh water, insect larvae. Some element of control of these micrograzers is often necessary. Relative micrograzer/macrograzer abundance often determines plant community structure – specifically, the abundance of fine-turf algae in relation to crustose algae, macroalgae, and higher plants. Micrograzers can be controlled, though often with difficulty, by simply removing them when they become too plentiful. However, micrograzer predators are required if one is attempting to simulate either an analog or synthesized ecosystem. When establishing a new microcosm, usually the first carnivores introduced are predators of the micrograzers – wrasses in a reef system;

Establishment of Food Webs

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FIGURE 13.8 Simplified food web of a Maine coast microcosm (see also Chapter 21).

killifish, tom cod, or sculpins in a cold-water marine system; and a wide variety of shiners, bluegills, tetras, barbs, and mollies, to name a few, in fresh water. Several weeks or months into the stocking process, as plankton begins to build up, especially the swimming reproductive and larval stages of organisms already established, filter and suspension feeders such as sponges, bryozons, worms, and Chromis fish in reefs, and hatchetfish in fresh water, can be added. Finally, as the buildup of their prey warrants, such mid-level predators as butterfly fish, angelfish, and grunts in a reef tank, and discus, larger tetras, and barbs in fresh water can be placed in the growing system. Up to this point, at least for most benthic microcosms, scaling factors are not a major consideration. In any moderate-size tank, it is usually possible to add several

elements of each of the trophic levels that we have discussed so far. However, when dealing with the higher carnivores such as jacks, barracuda, and sharks in a reef, large cods and haddock in marine cold water, pike and bass in cold fresh water, and a wide variety of cichlids in tropical fresh water, scaling difficulties invariably arise even in the largest of systems. These higher predators, especially adults, need a fairly large foraging territory to obtain required food. Using small members of a species will help to alleviate the problem. However, the feeding patterns of the young of a top predator may be quite different from those of the adults. We have generally been successful in keeping barracuda by feeding them supplementary goldfish. When introduced to salt water the goldfish immediately emit distress signals and are attacked by the barracuda within seconds. The feeding

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FIGURE 13.9 Simplified food web of a Florida Everglades mesocosm (see also Chapter 22).

of barracuda is somewhat analogous to that of snakes and larger cats (short feeding periods alternating with long quiescent spells), and is easily managed. However, smaller fish in the system have been subject to attack in the absence of a reasonable control element. For TC management, it is essential to provide prey with the protection of proper cover, reef structure, or abundant plants. We have briefly discussed the benthic (or at least bottom-oriented) elements of trophic structure in some of our microcosms. Except for the TC, these elements are all “within scale” for moderate-size tanks. In the beginning of our trophic discussion we bypassed filter feeding of plankton. This is also primarily a scaling problem in that some filter feeders require an amount of plankton that would normally be derived from water flowing

through the wild system. We have introduced brine shrimp into our reef systems (see Chapter 17) based on our measurements of plankton input into a St. Croix reef. Chromis and numerous coelenterates and worms rely on this input. In our cold-water system, to keep mussels and scallops for long periods especially in the first year it was necessary to periodically introduce a phytoplankter such as Isochrysis. In the second year, in a 3000-gallon tank, this proved unnecessary. Depending on the level of ecosystem simulation being sought, over time such refinements tend to be less required. As the ecosystem matures and many animals become fully adapted, the wide variety of reproductive stages present, as well as particulate organics released by many plants and animals, can fulfill most, if not all, requirements of

Trophic Structure in Aquaria

generalized filter feeders. Some specialized filter feeders may not find the size or kind of plankter they need and have to be fed separately or omitted. Detritus feeders are usually not a problem in models of any size. However, these have to be introduced to the system. Worms and microelements such as protozoans are usually present if the tanks are “seeded” with blocks (rock, sand or mud or larger plants or algal thalli) from equivalent wild environments. Larger detritivores such as sea cucumbers in the sea and catfish in fresh water can be added according to the amount of detrital load. As unused detritus begins to build up in the system, typically several months into stocking, these animals can be added in numbers based on a visual analysis. As we discussed in Chapter 11, the primary function of an ATS is to maintain water quality on a diurnal basis by simulating the large, relatively low-biomass volume of water that lies adjacent to the ecosystem of interest in the wild. However, the scrubber also performs another critical function: the removal of excess nutrients. These nutrients might first be stored as excess biomass or particulates on a marsh or mud flat. Generally excess nutrients are the result of adding food to an aquarium or microcosm to simulate either a larger area of plankton production or a larger area of small invertebrate or insect production (typically fresh water). Excess nutrients can also result from overloading the tank with fish or other higher trophic elements either purely for esthetic reasons or to drive a system faster to carry out scale modeling in a smaller space or lesser time. If the algae removed exceeds added food by 2–5 times (see Chapter 11), the system will remain balanced. However, if the model is that of a highly oligotrophic (low nutrient) wild ecosystem and large volumes of algae must be exported to ensure macronutrient (N, P) balance, then some attention must be paid to the potential for depletion of micronutrients (see Chapters 4 and 10). As we noted in Chapter 10, macronutrients such as calcium can be depleted when systems are extensively calcifying, but this is a side link to energy flow. Among the microfauna, especially the protistan protozoans, there exists a food web in miniature, further complicating the understanding of the trophic structure as a food web. Some of these tiny flagellated and ciliated organisms have photosynthetic pigments and organelles and, like many corals, for example, function partially or wholly as plants. Other protozoans are grazers, primarily of algae and bacteria, and many others, including large amoebas familiar to anyone who has taken a biology course, are predators on the smaller protozoans. All of these protists can be and often are eaten by higher invertebrate micrograzers or micropredators or even by fish.

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There is a rather informal theory among ecologists that says that community structure can be very different when there are even rather than odd numbers of levels in a food chain. As we have discussed, a complex and stable ecosystem should be more appropriately characterized as a web rather than a chain. Nevertheless, the food webs shown in this chapter for several model systems could be idealized as three-level systems. (The fourth level is normally simulated or strongly managed by the aquarist so that it does not overpower the level below.) According to the theory, since the simple carnivore level controls the grazers (and micrograzers), plants are able to maintain biomass and productivity. Indeed, most of the model systems that we have developed have high plant biomass. On the other hand, in our 130-gallon “home reef” (see Chapter 20), the top predator, the rare reef lobster, had been allowed to occasionally remove mid-level fish predators for many years. As a result, there is very heavy grazing pressure in this system, and the plant community (perhaps equivalent to thorn scrub) is strongly dominated by calcified and other tough algae. Thus, there is a high plant biomass and moderate productivity in spite of the heavy grazing.

TROPHIC STRUCTURE IN AQUARIA Even in modest-size aquaria, sufficient plant production is not difficult to manage if light and water motion are adequate. Grazer abundance and standing crop of algae and submerged aquatic vegetation have to be carefully monitored, but manipulation to attain a balance is also not difficult. Likewise, the plankton component is mostly simulated by dried food, brine shrimp or the equivalent, and top predators, which cannot normally be present, must also be simulated by the aquarist. As long as a sufficient number of hideaways within or separate from the primary ecosystem are available as refugia, the smaller grazer and carnivorous and detritivorous invertebrates can typically maintain their numbers in the face of predation. The difficulty usually lies with mid-level fish. A few species can reproduce and maintain their numbers in the face of predation pressure in the community tank – some cichlids are quite amazing in this respect and provide exciting observation. However, most fish cannot achieve successful reproduction in a modest-size aquarium with numerous other species present, although they frequently provide an important feed component with their eggs and/or young. Thus, sooner or later as mid-level fish are either preyed upon or die from old age, they must be replaced. This can be done through wild capture, purchase, or by separately culturing the species desired. This process is another case of simulation to achieve the effect of a much

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larger water volume. In Chapter 23, we discuss an African pond tank of 70 gallons that had been left for many years to come to its own population level. After enough of the oldest fish eventually died, a reproducing pair of cichlids, after many failures due to predation on the young, finally succeeded in getting a few young to a size where they would not be eaten by the adult fish in the tank. Multiple tanks, linked by screened pipes, and functioning as refugia, can greatly increase reproduction for many species. Analyzing, modeling, and predicting ecosystem behavior are difficult for ecologists because of the complexity of even the simplest ecosystems. Modeling by measuring energy flows through an ecosystem – a variant of trophic structure analysis – can be a valuable accounting tool. The process, which goes several steps beyond trophic structure analysis, determines the energy equivalent of food passed from step to step by considering the controls on the amount of energy flow between each step.

THE ORGANISMS The major trophic levels for several types of ecosystems are discussed in Chapters 14–19, along with descriptions of selected organisms. Identification manuals, typical examples of which are given in the references for each chapter, are available for most plants and animals inhabiting coasts, ponds, and lakes likely to be simulated. These manuals often provide feeding information for the very abundant species. For others, inferences can often be made based on the morphology of a close relative. Often, when information is unavailable elsewhere, it can be gained simply from observing the animals themselves. Our understanding of how organisms relate to each other structurally and evolutionarily has been increasing by leaps and bounds in the past 20–30 years. Beyond simply more anatomical work on less wellknown organisms and rapidly improving additions to the repertoire of well-known fossils, the electron microscope and scanning electron microscope have had a very major impact on this process. Also, as we discussed in the Introduction, the techniques of molecular biology have been providing considerable new security to phylogenies, some of which have remained as we have known them for many decades and others changing markedly. No longer are the terms protozoa, algae and even protists evolutionarily meaningful, though in a pre-molecular general sense we use them for ecological discussion in this book. Thus, the references: Five Kingdoms: An Illustrated Guide to the Phyla of Life on

Earth by Lynn Margulis and Karlene Schwartz (1988) and Synopsis and Classification of Living Organisms, edited by Sybil Parker (1982) are valuable, but the purist might wish to modify that stance using Knoll (2003) (see also Chapter 1). It would now appear that we have at least eight kingdoms of eukaryotes.

References Andrewartha, H. and Birch, L. (1984) The Ecological Web. University of Chicago Press, Chicago. Beyers, R. and Odum, H. T. (1993) Ecological Microcosms. SpringerVerlag, New York. Carlton, J. (1999) The scale and ecological consequences of biological invasions in the world’s oceans. Chapter 13. In: Invasive Species and Biodiversity Management. T. Sandlund et al. (Ed.). Kluwer Academic Publishers, Dordrecht. Conrad, M. (1976) Patterns of biological control in ecosystems. In: Systems Analysis and Simulation in Ecology. B. Patten (Ed.). Academic Press, New York. Cott, H. B. (1961) Scientific results of an inquiry into the ecology and economic status of the Nile crocodile (Crocodilus niloticus) in Uganda and northern Rhodesia. Trans. Zool. Soc. Lond. 29(4): 211–391. Cushing, D. and Walsh, J. (Eds) (1976) The Ecology of the Seas. Saunders, Philadelphia, Pennsylvania. Delbeck, J. C. and Sprung, J. (2005) The Reef Aquarium, Science, Art and Technology, Vol. III. Ricordea Publ., Cocoonut Grove, Florida. Johnson, M. S. and Brinkhurst, R. O. (1971) Production of benthic macroinvertebrates of Bay of Qunite and Lake Ontario. J. Fish. Res. Board Can. 28: 1699–1714. Knoll, A. (2003) Biomineralization and evolutionary theory. Rev. Mineral. Geochem. 54: 329–356. Levinton, J. (1982) Marine Ecology. Prentice Hall, Englewood Cliffs, New Jersey. Margulis, L. and Schwartz, K. (1988) Five Kingdoms: An Illustrated Guide to the Phyla of Life on Earth, 2nd edn. Freeman, New York. Odum, H. (1957) Trophic structure and productivity of Silver Springs, Florida. Ecol. Monogr. 27: 55–112. O’Neill, R., DeAngelis, D., Waide, J., and Allen, T. (1984) A Hierarchical Concept of Ecosystems. Princeton University Press, Princeton, New Jersey. Osmond, B. et al. (2004) Changing the way we think about global change research: scaling up in experimental ecosystem science. Global Change Biol. 10: 393–407. Parker, S. (1982) Synopsis and Classification of Living Organisms. McGraw-Hill, New York. Petersen, J. et al. (2003) Multiscale experiments in coastal ecology: improving realism and advancing theory. Bioscience 53: 1181–1197. Pimm, S. (2002) Food Webs: reprinted with updated Foreword. University of Chicago Press. Small, A. and Adey, W. (2001) Reef corals, zooxanthellae and freeliving algae: a microcosm study that demonstrates synergy between calcification and primary production. Ecol. Eng. 16: 443–457. Valiella, I. (1984) Marine Ecological Processes. Springer-Verlag, New York. van Voris, P., O’Neill, R., Emanuel, W., and Shugart, H. (1980) Functional complexity and ecosystem stability. Ecology 61: 1352–1360. Waldbusser, G., Marinelli, R., Whittatch, B., and Visscher, P. (2004) The effects of coastal marine sediments. Limnol. Oceanogr. 49: 1382–1492. Wyatt, T. (1976) Plants and animals of the sea. In: The Ecology of the Seas. D. Cushing and D. Walsh (Eds). Saunders, Philadelphia, Pennsylvania.

C H A P T E R

14 Primary Producers Plants That Grow on the Bottom

The theme of this entire book is that the efficient functioning of photosynthetic organisms is the key to both the building and the restoration of the Earth’s aquatic ecosystems. Clearly, not all aquatic ecosystems are directly dominated by photosynthetic organisms. The deep ocean bottoms and sandy beaches are prime examples. However, the energy to drive the vast majority of the Earth’s wild ecosystems is ultimately derived from plant photosynthesis, and, in many ways, the critical impact of human activities on the planet has been on photosynthetic organisms and their needs and products. As we previously discussed, in a global context, the locking up or storing of the key chemical elements of life (carbon, nitrogen, phosphorus, and other nutrients) first by photosynthesis and later, and more sporadically, by geological burial, has provided a major element of stability to the biosphere. In this chapter, we discuss the plants themselves in their role as providers of habitat and food for animals. Note that for efficiency in writing we use the word plants as being the equivalent of photosynthetic organisms, including higher plants (vascular and nonvascular), algae (protists), and some bacteria (mostly cyanobacteria or blue-green algae). As we shall see, in an evolutionary context, the issues are complex. Probably several different types of photosynthesis in bacteria evolved separately in bacteria; it is the photosynthetic variant of the cyanobacteria, which involved splitting water and releasing oxygen, that radically changed the character and potential of the biosphere, and eventually led to the algal groups and the higher plants. At least several algal and higher plant groups have arisen at very different times during the biosphere’s development. The plankton community, including its algae, is covered separately in Chapter 17 because of the great difference in form and function between phytoplankton

and benthic plants. Also, although the general subject of this book includes living models of swamp wetlands, and Chapter 22 deals with mangrove and Everglades forested “hammocks” or swamps, this is a rather specialized topic that we leave to other chapters. Here, we cover three major areas of interest: (1) benthic algae (of many major groups, divisions, or phyla); (2) submerged aquatic vegetation (SAV; submerged vascular plants); and (3) emergent aquatic vegetation (EAV; mostly marsh plants growing from waterlogged soils into the atmosphere). A rough indication of the importance of the major groups of benthic plants in the primary environments considered in this book is shown in Figure 14.1. As we discussed in Chapter 12 “Community Structure,” plants are often far more than just the primary food or energy source for the biosphere. In most terrestrial ecosystems and in many benthic marine and aquatic ecosystems, plants also provide a major element of habitat structure. The plants provide cover or protection and sometimes surfaces for direct attachment, and often are modifiers of environmental characteristics such as oxygen, carbon dioxide, available light and/or drying and ultraviolet effects, pH, waves, wind, and temperature.

BENTHIC ALGAE To the layman familiar with green trees, shrubs, and herbaceous land plants, marine and aquatic algae may seem to be on the small side and at the same time rather simple in morphology. However, the algae of the sea can be very large, some many tens of feet in length, elaborate in construction, and sometimes reproductively very complex. As one might expect, algae mostly

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14. Primary Producers

FIGURE 14.1 General distribution of the major benthic plant groups from terrestrial environments to the sea.

lack the vascular, water-conducting, and foodconducting tissue of land plants. These structures are not of general use in a watery environment. It is of interest in this context that many vascular plants that have become secondarily adapted to the aqueous environment also have very reduced or even lack conducting tissue. On the other hand, those higher plants that have evolved back into the water environment often have a very special ability that allows many vascular plants to root into anaerobic muds: a secondary gas-exchange system made up of intercellular spaces. Also, among the largest algae, the kelps whose bases of attachment lie heavily shaded in deeper water, an entirely different conducting tissue has evolved to carry sugars from the more productive fronds near the surface to the holdfasts. This is the equivalent of the phloem, or inner

bark, conducting tissue of many land plants. The xylem, the often woody water-conducting tissue, is of course absent. While most algae are anatomically simpler than terrestrial plants, they show great diversity of color, virtually every color of the rainbow. Nevertheless, like terrestrial green plants these underwater relatives (mostly very distant relatives) photosynthesize, using chlorophyll and the energy of sunlight. Generally using the same photosynthetic process, algae bring water, carbon dioxide, and nutrients together to make their own food and build their own tissues. Many algae can also use direct organic sources for nutrients and can uptake bicarbonate ion when carbon dioxide is in low supply (Lobban and Harrison, 1994). In addition, many algae have accessory photosynthetic pigments, which are

Benthic Algae

mostly responsible for the wide range of color characteristics and allow a greater efficiency of light capture in water, where light spectra are often quite different from those on the land (see Chapter 5). In the later 20th century, it had been accepted that there were about 40 000 species of algae in the sea, belonging to a number of major groups and about 10 000 species in fresh waters. However, it is now widely accepted that the numbers of algal species (particularly in the sea) are much higher, perhaps as many as a million. Indeed it has been suggested that there are more than a million diatom species alone (see review by Adey, 2005). It might seem relatively easy to separate technically the “lowly” algae from the higher plants. However, some algae have conducting tissue and structures appearing as roots, stems, and leaves. Even the “pièce de résistance” of the dictionary differentiation, the lack of a special cell layer surrounding the egg cell, does not apply to the Charophytes (freshwater green algae). Indeed, only with careful semantics does it apply to some of the advanced browns and reds. The major groups of algae are differentiated by their photosynthetic pigments, type of storage food, wall structure, type of flagella, and to some extent reproduction (Table 14.1). It is now recognized, from molecular (i.e. DNA) studies, that the eukaryotic, animal and algal, origins are far more complex than earlier thought (see Figure 1.1). Although this is not likely the end of the story, Figure 14.2 shows a recent tree, or molecular phycology of plants and algal protists, showing two major algal origins from bacteria (presumably cyanobacteria). As this tree shows the red and green algae (the latter leading to the higher plants) are on the same line, but the red algae branched off early (1200 Ma), presumably before any of the other protists and animals evolved from separate blue-green roots. The other major groups of algae (browns, diatoms, dinoflagellates) evolved from blue-greens somewhat later (though still in the preCambrian) and perhaps some (e.g. euglenids) not until much later (Paleozoic). The bacterial relationships of the blue-green algae had been suspected for a century or more, and in the third quarter of the 20th century, the electron microscope conclusively demonstrated that the blue-green algae (Cyanophyta or Cyanobacteria) were distinctly bacteria of the Kingdom Monera, and lacked nuclear or plastid membranes. However, we continue to refer to them as algae, algal protists, or plants in this book since they photosynthesize as other algae do, and have chlorophyll and accessory pigments similar to the red algae. Blue-greens exhibit many primitive features, including the lack of a membrane-enclosed nuclei and chromatophores, and other cell organelles. Blue-greens can be any color, including purple, red, and black, but are frequently blue-green. They are almost always

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present in aquaria and can be fairly easily identified with a microscope by their lack of a nucleus or chromatophores, lateral cell walls (between adjacent cells) that are difficult to see, and relatively small cell size. Superficially, they tend to be slimy or silky in appearance, because they tend to have gelatinous outer cell walls. Reproductively, these primitive algae bud off cells or short filaments. As with bacteria, the presence of sexual reproduction is not seen, but can be demonstrated genetically. Blue-greens are ubiquitous in the wild and some species occur in the most extreme of environments, often those too hot, too nutrient rich, too nutrient poor, or too variable for other algae. They are also typically important elements of the algal turf scrubbers (ATS). A variety of blue-greens and their reproduction is shown in Figures 14.3 and 14.4. A now widely accepted theory holds that the numerous cell organelles of more advanced algae (and higher plants and animals) are partly derived through the acquisition of smaller blue-green cells by the larger more “advanced” cells (Margulis and Sagan, 1986). Green algae (Chlorophyta) are physiologically close to the land plants. Relative to other multicolored algal types, especially blue-greens, they are sometimes referred to as grass green. Greens occur more or less abundantly in fresh and estuarine environments; in the benthic marine environment, they tend to be dominated by brown and red algae, except in the tropics, where a single order, the Siphonales, can be quite prominent. In the marine phytoplankton, they are totally dominated by diatoms, dinoflagellates, and coccolithophores. The green algae are the archetypal algae in the minds of laymen, who are more likely to be familiar with small eutrophic streams or ponds. Not as large as many brown algae or as complex structurally as most red and brown algae, green algae are nevertheless ubiquitous if not dominant plants. They show most simpler forms of reproduction known in the algae, most typically with both male and female flagellated cells set free in the water. However, green algae also range up to full oogamy (a large, nonmobile egg on the female plant and small motile sperm from a male plant); in a few cases, direct fusion of cells from adjacent filaments occurs. Figure 14.5 shows a variety of types of green algae. A very early offshoot of the green algae, now usually placed in a separate division, the Charophyta, is notable because it is generally thought to be on or near the green algal evolutionary line to higher plants. Chara and Nitella, common plants of high-quality, calcareous waters, are partly calcified and develop large eggs enclosed in a sheath of protecting cells (Figure 14.6). An unusual structural type of the green algae, well developed in fungi but uncommon in higher plants, is

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14. Primary Producers TABLE 14.1 Summary of Some Algal Divisions and Their More Significant Characteristicsa

Division Cyanophyta

Common name Blue-green algae

Prochlorophyta

Chlorophyta

Green algae

Charophyta

Stoneworts

Euglenophyta

Euglenoids

Phaeophyta

Brown algae

Chrysophyta

Golden and yellowgreen algae (including diatoms)

Pyrrhophyta

Dinoflagellates

Cryptophyta

Cryptomonads

Pigments and plastid organization in photosynthetic species Chlorophyll a; C-phycocyanin, allophycocyanin, C-phycoerythrin; ␤-carotene and several xanthophylls Chlorophyll a,b; seven carotenoids, of which ␤-carotene and zeaxanthin are major Chlorophyll a,b; ␣-, ␤-, and ␥carotenes and several xanthophylls; 2–5 thylakoids/stack

Chlorophyll a,b; ␣-, ␤-, and ␥-carotenes and several xanthophylls; thylakoids variably associated Chlorophyll a,b; ␤-carotene and several xanthophylls; 2–6 thylakoids/stack, sometimes many Chlorophyll a,c; ␤-carotene and fucoxanthin and several other xanthophylls; 2–6 thylakoids/stack Chlorophyll a,c (c lacking in some); ␣-, ␤-, and ⑀-carotenes and several xanthophylls, including absent fucoxanthin in Chrysophyceae, Bacillariophyceae, and Prymnesiophyceae; 2 thylakoids/stack Chlorophyll a,c; ␤-carotene and several xanthophylls; 3 thylakoids/stack Chlorophyll a,c; ␣-, ␤-, and ⑀-carotene; distinctive xanthophylls (alloxanthin, crocoxanthin, monadoxanthin); phycobilins; 2 thylakoids/stack

Storage product

Cell wallb

Flagellar number and insertionc

Habitatd

Cyanophycin granules (arginine and aspartic acid); polyglucose (glycogenlike)

␣- and ␧-diamino pimelic acid, glucoseamine, alanine, etc.

Absent

fw, bw, sw, t

Starchlike

Peptidoglycan

Absent

sw

Starch (amylose and amylopectin) (oil in some)

Cellulose in many (␤-1,4glucopyranoside), hydroxyproline glucosides; xylans and mannans; or wall absent; calcified in somee Cellulose (␤-1,4glucopyranoside); some calcified

One, 2–8 many equal, apical

fw, bw, sw, t

Two, equal, subapical

fw, bw

Starch (amylose and amylopectin)

Paramylon (␤-1,3glucopyranoside), oil

Absent

1–3 (–7) apical, subapical

fw, bw, sw, t

Laminaran (␤-1,3glucopyranoside, predominantly); mannitol

Cellulose, alginic acid, and sulfated mucopolysaccharides (fucoidan)

2, unequalf, lateral

fw (very rare), bw, sw

Chrysolaminaran (␤-1,3-glucopyranoside, predominantly); oil

Cellulose, silica, 1–2 unequal or calcium carbonate, equal, apical mucilaginous substances, and some chitin; or wall

fw, bw, sw, t

Starch, ␣-1,4-glucan (oil in some)

Cellulose or absent; mucilaginous substances

Two, one trailing, one girdling

fw, bw, sw

Starch, ␣-1,4-glucan

Absent

Two, unequal, subapical

fw, bw, sw

(Continued)

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Benthic Algae TABLE 14.1

Division

Common name

Rhodophyta

Red algae

Pigments and plastid organization in photosynthetic species Chlorophyll a (d in some Florideo phyceae); R- and C-phycocyanin, allophycocyanin; R- and Bphycoerythrin. ␣- and ␤-carotenes and several xanthophylls; thylakoids single, not associated

(Continued)

Storage product

Cell wallb

Floridean starch (amylopectinlike)

Cellulose, xylans, several sulfated polysaccharides (galactans) calcification in some; alginate in Corallinaceae

Flagellar number and insertionc Absent

a

Habitatd fw (some), bw, sw (most)

Underlined groups are discussed in text. After Bold and Wynne (1985). In terms of cell wall chemistry, the vegetative cells have received most attention. Spores, akinetes, dormant zygotes, and other resting stages have not been studied, but it is clear that their walls may contain other substances (e.g. waxes and other nonsaponifiable polymers and phenolic substances). c In motile cells, when these are produced. d fw, fresh water; bw, brackish water; sw, sea water; t, terrestrial (soil, rocks, etc.). e Others are wall-less or have xylans, mannans, other glucans, some silica, or protein. Also, nearly all skeletal polysaccharides (cellulose, xylans, mannans) are accompanied by one or more mucilaginous substances (e.g. arabinogalactans and sulfated mucopolysaccharides). f Except the uniflagellate sperms of Dictyotales. b

FIGURE 14.2 Evolution of the two major “kingdoms” of photosynthetic organisms (plants) from the cyanobacteria. Presumably, these major groups derived from different cyanobacteria ancestors. Also, note that all of the prominent groups of photosynthetic organisms had evolved long before the invertebrate phyla began to appear. After Knoll (2003).

208


FIGURE 14.3 Major types of structural organization (anatomy) in blue-green algae: (A) Gloeocpsa, (B) Stigonema, (C) Nostoc, (D) Scytonema, (E) Pleurocapsa, (F) Oscillatoria, (G) Calothrix, (H) Fischerella, and (I) Anabaena. After South and Whittick (1987).

FIGURE 14.4 Major types of asexual reproduction in blue-green algae: (A) Gloeotrichia, (B) Wollea, (C) Calothrix, (D) Chamaesiphon, and (E) Dermocarpa. After South and Whittick (1987).

Benthic Algae

209

FIGURE 14.5 Primary anatomical types of green algae: (A) Chaetomorpha area (marine), (B) Draparnaldia glomerata (fresh water), (C) Cladophora sp. (marine), (D) Anadyomene stellata (marine), (E) Ulva lactuca (marine), (F) Enteromorpha sp., and (G) Oedogonium (fresh water). (A,C,E,F after Taylor (1957); B,G after Prescott (1951); D from Dawes (1981), reprinted by permission of John Wiley & Sons, Inc.)

the siphonaceous or coenocytic body. Based on filaments with rare cell walls between cells and abundant nuclei, some genera of the marine Siphonales become elaborate and often calcified (Figure 14.7). Based on extensive deep-core drillings in Pacific atolls several decades ago it was concluded that a strongly calcified member of this group, Halimeda, and not the corals, was the dominant carbonate contributor to these enormous, organically built, but now geological structures. Other related genera, such as Udotea and Penicillus, along with the flowering seagrasses, form the often dense vegetation of tropical lagoons. These siphonaceous algae, along with some surface-living algal cells

such as diatoms, are competitors with the flowering plants in the sandy or muddy SAV biome. Most other benthic algae are more or less limited to the rockyshore biome and coral reefs. The strictly marine or saltier estuarine brown algae (Phaeophyta) are the giants of the algal world, some being as long as large trees though never of similarly great mass. Although virtually all structural types are represented in the browns (Figure 14.8), the branched filament Ectocarpus, occurring in a wide range of coastal environments, arctic to tropics, is especially ubiquitous, and sometimes covers large, shallow, quiet areas with a brownish cottony coating. The large, complex

210



Benthic Algae


211

212



parenchymatous type of body represented by the kelps and rockweeds dominates many rougher water areas. Although usually thought of as the primary plants creating the rocky-shore communities of colder waters in both the Northern and Southern Hemispheres, the large browns are also well represented in the tropics by Sargassum and Turbinaria. Also, the brown genera Dictyota, Padina, and Lobophora are among the commonest mid-size algae occurring in coral reef environments. Brown algae show virtually all types of sexual reproduction known in the algae. Many of the simpler and smaller types alternate generations between sporeproducing, diploid (double chromosome set) plants and haploid, male and female, plants bearing sexual cells. However, the larger browns such as the rockweeds show a reproductive pattern that is not unlike that of the higher plants and animals. Sperm are produced in conceptacles on diploid male plants, and eggs in similar conceptacles on female plants. The spermatia are released and can swim, and are carried by currents to the releasing eggs, where fertilization takes place (Figure 14.9). After partial division the fertilized egg is released to settle and form a new plant.

The reds (Rhodophyta) are primarily small- to midsize marine algae, although a few genera occur in fresh waters, particularly clear streams. They are usually red in color although under some circumstances can be green or black. One family common on coral reefs, the Champiaceae, is characterized by a brilliant iridescence that often includes shades of blue. The red algae are unusual among algae, and all plants, in several ways. Although sometimes appearing parenchymatous, or built of a mass of cells dividing in all directions, almost all reds can be shown to be built by the elaboration of filaments (Figure 14.10). Many reds are simply branched filaments, though more complex branched fleshy types and leafy forms are not unusual. The red crustose coralline algae, with or without the corals, are capable of building large reefs or algal ridges (Adey, 1978; 1986). Red algae have no motile stages. Even the spermatia (sperm) do not have flagella, but move rather like amoebas. On the other hand, the egg (or carpogonium) is relatively large with a protruding structure, the trichogyne, to “catch” the spermatia. In the more complex types, the eggs are borne in special organs called conceptacles, and in most red algae the result of fertilization is a complex

Benthic Algae

FIGURE 14.6 Charophytes, Chara sp. (F,G,I,J,L) and Nitella sp. (A–E,H,K). A,C,E,J,L, with oogonia. A,E,J,L, with antherida. After Prescott (1951).

213

214


FIGURE 14.7 Three members of the marine green algal order Siphonales, a group anatomically built on a coenocytic plan of few cell walls: (A) uncalcified Caulerpa verticillata; note trabecullae (wall supports), W, (B) weakly calcified Udotea cyathiformis, and (C) heavily calcified Halimeda discoidea; note flexible connection (G) of calcified segments. All after Dawes (1981). Reprinted by permission of John Wiley & Sons, Inc.

Benthic Algae

215

FIGURE 14.8 Primary morphological characteristics of brown algae (Phaeophyta). (A) Filamentous Ectocarpus sp. (a) habit and (b) microscopic view showing gametangia. (B) Pseudoparenchymatous Acrothrix sp. developed by cortication of a single axial filament. (C) Fully parenchymatous Laminaria (kelp) spp. (D) Fucus vesiculosus, a common rockweed. (E) Sargassum filipendula showing stems, bladders, and leaves. All after Taylor (1957).

series of fusions and growths that give rise to large numbers of spores (carpospores). These fertile structures are often seen as distinct knots or cysts (cystocarps) on the female plant (Figure 14.11). While many types of life cycle are found in the red algae, the most common type is an alteration of similar-appearing generations. The diploid generation bears spores, usually tetraspores, sometimes also in conceptacles (Figure 14.12). The haploid or sexual generation generally has both female and male plants producing their respective eggs or sperm. Finally, a crucial and omnipresent group of the goldenbrown algae (Chrysophyta) is the Bacillariophyceae or diatoms. Some writers place diatoms in their own phylum, Bacillariophyta (Margulis and Schwartz, 1988).

Different species of diatoms occur in both fresh and salt waters and can be either benthic or planktonic (see Chapter 17). Primarily unicells, some diatoms are also filaments (Figure 14.13). Sometimes called the “grass of the sea,” primarily for their offshore planktonic abundance, the diatoms are often the first algal colonizers of new surfaces and are usually responsible for the coating that snails graze (and the aquarist must clear) on the glass of a well-lighted, well-run aquarium. There are a number of additional algal phyla or divisions that are primarily microscopic. We refer the interested aquarist to several modern texts for a full treatment of the major groups we briefly discussed above as well as omitted taxa (Bold and Wynne, 1985; Lobban and Harrison, 1994; Van Den Hoek et al., 1995; Lee, 1999; Littler and Littler,

216



Benthic Algae


FIGURE 14.9 Sexual reproductive structures in northern rocky shore Fucus sp. This is a monoecious species (eggs and sperm borne in the same plant and conceptacle). Some Fucus species are dioecious and consist of separate male and female plants. After South and Whittick (1987).

217

218


FIGURE 14.10 Red algae (Rhodophyta) of increasing structural complexity but all based on a filamentous building plan. (A) Acrochaetium zosterae, a branched filament with a filamentous rhizoidal base. (B) Cystoclonium purpureum, a single, heavily corticated filament giving rise to a lax, fleshy macrophyte. (C) Hypoglossum woodwardii, a leafy macrothallus based on the single axial filament structure. (D) Ahnfeltia plicata, a heavily branched thallus. (E) Mesophyllum spp., multiaxial, heavily calcified crusts, a member of the Corallinaceae. (A) After Taylor (1957) and (B–E) after Fritsch (1952; 1956).

Algae in Model Ecosystems

219

2000). A particularly good treatment of the ecology of seaweeds is provided by Luning (1990). In the marine environment, except perhaps where algal biomass is very high, such as in an Irish moss mat, wave, and tidal energy drives contact between the water column and the algae and substrate. In fresh waters, where often less disruptive physical energy is available, benthic surfaces develop biofilms (Chapter 6), and these can become virtually independent ecosystems in which complex, internal chemical and biotic interactions can become as important as the water column interactions (Burkholder, 1996).

ALGAE IN MODEL ECOSYSTEMS


Algae are considered to be the bane of most culture systems. This is primarily because many algae are highly efficient opportunists reproductively, in wild ecosystems, waiting for the more or less unusual spike of nutrients. This very characteristic, used in a controlled manner, is the basis of the highly efficient ATS. A few algae become undesirable as “blooms” in many culture systems partly because nutrients are higher than they should be and, in some cases, partly because water motion and/or grazing are insufficient. Algae, as part of a properly run model ecosystem, only contribute to

FIGURE 14.11 Characteristic sexual reproductive patterns in red algae. (A) Variety of carpogonia (egg cells) with projections (trichogynes). (B) Fertilized carpogonium-producing tube, fusing with auxiliary cells give rise to cystocarps and carpospores. (C) Crustose corallines with male (c,d) and female (a,f,g,h,i) cells being borne in separate sexual organs (conceptacles); (e) carpospore production after fertilization. After Fritsch (1952).

220


FIGURE 14.12 Tetraspores of the diploid generation of red algae. Some are borne at random in the tissue, others in special organs (conceptacles). After Fritsch (1952).

the productivity, food availability, and energy flow, as well as to the overall stability of the system. Sprung (2002), in his Algae, a Problem Solvers Guide discusses many of these issues as they relate to the home aquarist. For the modeler, or the wild ecosystem restorer, if algae are exploding, the microcosm, mesocosm, or macrocosm is not functioning properly. The problem is not the algae; it is most likely excess nutrients, though specific grazers may also be lacking. As we describe throughout this book, for very small systems, it may not be possible to have the “right” grazer, because that grazer needs more territory than is available in the model. In that case the operator (aquarist) must become the grazer, or as we describe elsewhere, the grazer must be kept in a reserve or refugium system and introduced to the model for short periods of time. It is hard to imagine a situation where chemical treatment would be appropriate. It is not possible to provide enough background here for the aquarist to fully understand and identify all the algae in any given synthetic system under development. Indeed, depending upon the ecosystem in question, a

FIGURE 14.13 A variety of diatom frustules: (1) unicells and (2) filamentous types. After Fritsch (1956).

Algae in Model Ecosystems

few to many of the species may never have been described (Adey, 2005). The references in this chapter’s bibliography plus the field guides for the community being modeled can, however, identify and provide some of the natural history information required. Here, we simply provide some notes on our experiences with algae in a variety of mesocosms, microcosms, and aquaria. We also refer the reader to Chapters 20–23. To the casual observer a colder-water rocky shore often has a dense subtidal kelp forest and a thick intertidal carpet of rockweed. These plants are the primary elements structuring many rocky-shore communities and around which the remainder of the flora and fauna are oriented. However, forming a substory or understory under, and in bare spots around, the large browns that form the canopy is a wide variety of much smaller red, brown, and green algae, as well as attached diatoms and generally inconspicuous blue-greens. In some circumstances, particularly when grazing by sea urchins is heavy, calcified crustose red algae (the corallines) can also be widespread dominants below low tide. A typical algal zonation pattern for a moderately exposed shore in the Gulf of Maine is shown in Figure 12.5. Obviously, even to the level of the division, the algae at different elevations on the rocky shore are quite different. Bluegreens (along with some lichens) are most important at the uppermost reaches of the tide. Browns dominate in the intertidal zone and extend below low water typically to 10–30 feet. Reds really come into their own in the deeper water, mostly below 10–30 feet. Although green algae are present, especially in upper levels and tide pools, they are generally not conspicuous except around small streams or freshwater seeps. The algae being considered for a microcosm of this rocky shore can be quite diverse, depending on the vertical and wave energy extent of the community being simulated. Several times in recent years we have modeled subarctic rocky-shore communities (Gulf of Maine) ranging from the highest tide levels to about 50 feet (15 meters in depth (see Chapter 21). Elevation and depth are simulated physically by tide and by variation of light levels in the tank. The larger brown algae (kelp and rockweeds) characteristic of moderately open to protected shores have generally been successful in these microcosms. In the highest intertidal, the blue-greens Oscillatoria, Lyngbya, and Spirulina dominate, with the peculiar green Prasiola also present in abundance. In the mid-intertidal, the rockweeds Ascophyllum nodosum and Fucus species dominate. Large individuals of the rockweeds reproduce and release viable spores that develop into long-lived individuals (probably 3–10 years characterizes wild plants). However, the mature plants introduced typically do not survive longer than 6–8 months. We have found that repeated introduction over several years is

221

required to produce a dense rockweed-dominated intertidal. Beneath the rockweeds in the mid to lower one-third of the intertidal range, Chondrus crispus (Irish moss) forms an extensive low canopy. While this is also true in many places on the Maine coast, in the longest operated microcosm it became more extensive than when the system was stocked 5 years earlier. Perhaps the generally higher humidities in the closed microcosm environment allow Chondrus to broaden its coverage slowly and extend further up the intertidal. The brilliant green filament, Chaetomorpha melagonium, with extraordinarily large cells, is a persistent minor element in the substory along with Chondrus. This is the normal pattern in the wild. Subtidally our largest rocky-shore microcosm always contained the kelp Laminaria longicruris in abundance, and this is typically the most abundant species in the Gulf of Maine. On the other hand, Laminaria digitata, which is particularly abundant on the most exposed areas of wild coast, did not persist in the microcosm. Perhaps, like Fucus distichus in the intertidal and Alaria esculenta at the lowest low-tide mark, it requires more wave action. This model has urchin grazers in abundance. For these low intertidal species, urchin grazing in a quieter environment may be crucial. In the deepest water in the microcosm, the reds Phycodrys and Phyllophora, as well as the small, perforated kelp Agarum clathratum, were quite successful in evading urchin grazing. It is likely that these species are moderately distasteful to urchin and snail grazers. A detailed list of the algae characteristic of the rocky Maine coast microcosm is given in Chapter 21. Shallow-water coral reefs, subarctic rocky shores, and tropical ponds are all highly productive of plant growth, the reef generally being the most productive because of a higher year-round level of incoming solar energy coupled with the driving or continual mixing effects of the constant trade winds and their seas and currents. There is a tendency in the human mind to equate plant mass (biomass or standing crop) with productivity. This is not necessarily the case. Algal turf production on a reef is extremely high. However, it is eaten almost as fast as it grows and rarely shows a high biomass. In an opposite situation, a northern conifer forest can have an enormous plant biomass. However, yearly productivity is less than one-tenth of that on a reef, little of the plant material produced is eaten directly, and breakdown of the plant biomass is very slow. The algal flora of a tropical reef is generally quite different in appearance from that of a northern rocky shore. While Sargassum, a close relative of the rockweeds of northern waters, can be extremely abundant under heavy sea conditions, where grazing is greatly limited, and some larger greens, particularly the calcified Halimeda, which

222


resists grazing can cover large areas, most algae are relatively inconspicuous. A coral reef algal turf, in spite of its diminutive dimensions, can be extraordinarily diverse and can include a wide structural and reproductive variety representing virtually all of the major algal groups. Furthermore, these small algae form a plant community as productive as any on the Earth, both in the wild and in aquaria and microcosms. That turf algae are so important on wild reefs is rarely recognized by the hobbyist and often not recognized by the professional biologist. We refer interested readers to a series of volumes on the turf algae of the Great Barrier Reef in which their key role is discussed (Price and Scott, 1992). The same basic algal patterns occurred in the coral reef microcosm at the Smithsonian Institution as on a reef. In the areas of lesser wave action, larger algae were subject to heavy grazing and did not persist. However, in refugia protected from fish and urchins, many mid-size species survive. They can also be found in small crevices on the reef itself. Halimeda was a persistent algal dominant in the microcosm as long as very large parrotfish were not present. The algal turf community, as on a wild reef, was quite rich. Eighty-five species were tallied, including several diatoms and blue-greens. The greens Cladophora, the browns Ectocarpus and Dictyota, and the reds Hypnea, Laurencia, Acanthophora, and Ceramium, along with several corallines, were all common members of this model reef community, as they are in the wild (see list in Chapter 20). Prior to the 1960s, light levels were extremely low in most home aquaria and nutrients were very high. The only algae that were common were blue-greens, particularly those of reddish or blackish hues. In the 1960s, these were discouraged by most writers (because they were not very esthetic, i.e. they were slimy in appearance), though in fact similarly slimy blue-green colonies are extremely abundant in many wild reef environments. Later, aquarists were encouraged to maintain these algae (any photosynthesis helped). For the home aquarist, Sprung (2002) provides an excellent and balanced approach to algae in reef systems. In our view there are no uniquely beneficial or problem algal groups for aquarium systems. As we have indicated, if cyanobacteria are the only “algae” present, either the aquarium in question has not been adequately provided with “seed” algae or the environment is marginal. Most environments that an aquarist is likely to model should include many different types of algae; the greater the variety, the more viable and stable the tank is likely to be. To many ecologists, abundant green algae indicates eutrophic conditions, although this is by no means an established indicator. We have seen marine ecosystems with unusually low nutrient concentrations with abundant Ulva and

Enteromorpha, the greens most often the subject of this view. For 12 years we operated a small 130-gallon reef aquarium that had most of its algae stocked directly from the exhibit reef microcosm described above. Several pieces of “live rock” were then introduced directly from wild Caribbean reefs before we began the long period of closure described in Chapter 20. Generally the calcified Halimeda and corallines such as Jania and Mesophyllum dominated, though algal turfs were abundant in the crevices and of course on the ATS. It is clear, however, that heavy grazing, particularly as it relates to the wave action present, and cover for the noncalcified algae were the chief factors controlling algal growth. Tough algae such as the green Dictyosphaeria and Valonia were abundant, and the fleshy browns and reds were stunted by constant cropping. On the other hand, when larger grazers, particularly fish, are removed and kept from the system for many months, then larger reds such as Laurencia and Spyridia formed a significant carpet. In this small reef system, diatoms also coated all surfaces, where they were subject to sporadic grazing by snails and limpets. The tank glass had to be scraped with a razor blade to remove this limited “aufwuchs.” When this was done the grazing fish such as tangs and damsels were typically waiting to harvest the scrapings. This is discussed again in Chapters 15 and 20, but clearly the primary energy supply for the aquarium (on the order of 95–98%) is supplied by algae. All of these aquarium reefs were particularly rich in amphipods and mysid shrimp. As in the wild, the algal cover provides protection for these small invertebrates from the predatory activities of angelfish, rock beauties, damsels, and butterflyfish.

SUBMERGED AQUATIC VEGETATION Thirty-three higher plant families with submerged aquatic members, 124 genera, and over 1000 species can be attributed to SAV (Table 14.2). There are two families of seagrasses (see Figure 14.14), both of which also have many freshwater members. Only 48 species and 12 genera of these vascular aquatics have been able to return to the sea from which their ancestors, the green algae, had been derived 700–900 My BP earlier. Seagrasses sometimes occur as enormous beds that probably exceed the rocky-shore biome in area. However, they are included here under the SAV category rather than as a separate marine listing because their ecological parameters are quite similar to the freshwater equivalents and they form taxonomically only about 5% of the total SAV. Unlike our treatment of the algae, we do not provide detailed description of the major groups of SAVs.

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Submerged Aquatic Vegetation TABLE 14.2 Summary of the Major Families and Genera of Submerged Vegetation Showing Pollination Characteristics and Distributionsa

Genera

Species

Genera

Life formb

Spore production (pteridophytes) or pollination (angiosperms)c

2

c. 60

Isoetes

E, S

Heterosporous

2. Ceratopteridaceae (Parkeriaceae) 3. Marsileaceae

1

c. 6

Ceratopteris

E, S, Ff

Homosporous

3

c. 70

E, S, Ff

Heterosporous

4. Azollaceae

1

c. 6

Marsilea Pilularia Regnelidium Azolla

Ff

Heterosporous

5. Salviniaceae

1

c. 12

Salvinia

Ff

Heterosporous

8

c. 60

Fl, E, S

Entomophilous; few autogamous

Cosmopolitan Fresh water

7. Ceratophyllaceae

1

c. 6

Nymphaea Barclaya Brasenia Cabomba Euryale Nelumbo Nuphar Victoria Ceratophyllum

S, Ff

Hydrophilous

8. Elatinaceae

2

c. 30

Elatine Bergia

E, S

Ff

? Entomophilous; many perhaps autogamous Entomophilous

E, S

Anemophilous

Cosmopolitan Fresh water Cosmopolitan (but Elatine mainly temperate, Bergia mainly tropical) Fresh water Palaeotropical and warm temperate Eurasian Fresh water Cosmopolitan (but especially south temperate) Some species semiterrestrial; all aquatic species in fresh water

E, S

Anemophilous

Anemophilous; some hydrophilous Entomophilous

Number of Family A. Pteridophytes 1. Isoetaceae

B. Dicotyledonsd 6. Nymphaeaceae

9. Trapaceae (Hydrocaryaceae) 10. Haloragaceae

1

4

6

c. 100

11. Hippuridaceae

1

1

Trapa Haloragis Laurembergia Loudonia Meziella Myriophyllum Proserpinaca Hippuris

12. Callitrichaceae

1

c. 25

Callitriche

E, Fl, S

13. Menyanthaceae

5

c. 35

Menyanthes Fauria Liparophyllum Nymphoides Villarsia Podostemum Dicraea Griffithella Indotristicha Mniopsis Mourera Tristicha Terniola Willisia, etc.

E, Fl

14. Podostemaceae c. 25 (Podostemonaceae)

c. 120

S

Entomophilous, anemophilous, or autogamous

Geographical and habitat range

Cosmopolitan (but mainly at high altitudes in tropics) Some species terrestrial for at least part of year; all aquatic species in fresh water Pantropical and subtropical Fresh water Cosmopolitan Some species semiterrestrial; all aquatic species in fresh water Tropical and warm temperate Fresh water Tropical and warm temperate Fresh water

North temperate and cool South American Fresh water Cosmopolitan Some species semiterrestrial; all aquatic species in fresh water Cosmopolitan Fresh water

Tropical (rarely subtropical) Flowing (often torrential) fresh water

(Continued)

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14. Primary Producers TABLE 14.2 (Continued) Spore production (pteridophytes) or pollination (angiosperms)c

Number of Family

Species

1

c. 10

Hydrostachys

S

?

Tropical and subtropical African Fresh water

5

c. 10

E, Fl

Entomophilous; some probably autogamous

Temperate and tropical (except Africa south of equator) Fresh water

17. Hydrocharitaceae

14

c. 90

S, Ff

Entomophilous, Cosmopolitan (main in warm anemophilous, regions) – some genera hydroanemophilous, Old, others New World or hydrophilous Fresh and salt water

18. Alismaceae

12

c. 70

E, Fl, S

Entomophilous; ? few anemophilous or autogamous

Cosmopolitan (but especially north temperate) Fresh water

19. Scheuchzeriaceae

1

1

Butomus Hydrocleys Limnocharis Ostenia Tenagocharis Hydrocharis Blyxa Egeria Elodea Enhalus Halophila Hydrilla Lagarosiphon Limnobium Nechamandra Ottelia Stratiotes Thalassia Vallisneria Alisma Baldellia Burnatia Caldesia Damasonium Echinodorus Limnophyton Luromum Machaerocarpus Ranalisma Sagittaria Wiesneria Scheuchzeria

E

Anemophilous

20. Juncaginaceae

4

c. 15

E

Anemophilous

21. Lilaeaceae (Heterostylaceae) 22. Posidoniaceae

1

1

Cycnogeton Maundia Tetroncium Triglochin Lilaea

Cold north temperate Fresh water North and south temperate (few in American tropics) Fresh and brackish water

E

Anemophilous

1

2

Posidonia

S

23. Aponogetonaceae

1

c. 30

Aponogeton

Fl, S

24. Zosteraceae

2

c. 12

Zostera Phyllospadix

S

25. Potamogetonaceae

2

c. 90

Fl, S

26. Ruppiaceae

1

3

Potamogeton Groenlandia Ruppia

27. Zannichelliaceae

6

c. 25

Zannichellia Althenia

S

15. Hydrostachyaceae C. Monocotyledonsd 16. Butomaceae

Genera

Life formb

Genera

S


Pacific North and South American Fresh (alkaline) water Hydrophilous Mediterranean, Southwest. Asiatic and Australasian coasts Salt water Entomophilous Palaeotropical and southern African or autogamous Fresh water Hydrophilous Temperate coasts (except South American and West African) Salt water Anemophilous; few Cosmopolitan hydroanemophilous Fresh (barely brackish) water Hydrophilous Temperate and subtropical Brackish and salt water Hydrophilous Cosmopolitan (but marine genera mainly tropical) (Continued)

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Submerged Aquatic Vegetation TABLE 14.2 (Continued) Number of Family

Genera

Life formb

Spore production (pteridophytes) or pollination (angiosperms)c

Species

Genera

S

Hydrophilous


28. Najadaceae

1

c. 35

Amphibolis Cymodocea Halodule Syringodium Najas

Brackish and salt (rarely fresh) water

29. Mayacaceae

1

c. 10

Mayaca

E, S

Entomophilous

30. Pontederiaceae

7

c. 30

E, S, Ff

Entomophilous (few probably autogamous)

31. Lemnaceae

4

c. 28

Ff

? Unspecialized

Cosmopolitan Fresh water

32. Sparganiaceae

1

c. 15

Pontederia Eichhornia Heteranthera Hydrothrix Monochoria Reussia Scholleropsis Lemma Sirodela Wolffia Wolffiella Sparganium

E, Fl

Anemophilous

33. Typhaceae

1

c. 10

Typha

E

Anemophilous

North temperate and Australasian Fresh water Cosmopolitan Fresh water

Cosmopolitan Fresh (rarely brackish) water Tropical American and West African Fresh water Pantropical and temperate American Fresh water

a

After Sculthorpe (1967). E, emergent; Fl, floating-leaved; Ff, free-floating; S, submerged. c Entomophilous: insect pollinated; hydrophilous: waterborne pollen; anemophilous: windborne pollination; autogamous: self-pollinating. d The order in which the families of angiosperms are arranged in the table corresponds with the relative positions they occupy in the phylogenetic system of classification proposed by Hutchinson (1975). b

The following three references are for those wishing to gain a more in-depth understanding of these plants: Muhlberg (1982), Phillips and Menez (1988), and Sculthorpe (1967). Many local field guides that describe these plants are also available in bookstores specializing in natural history. In the following sections we provide a general description of SAVs and describe some specific experiences, marine and fresh water, that we have encountered in mesocosms, microcosms, and aquaria. SAVs are lower vascular plants (such as ferns) and flowering plants from several dozen families (less than 10% of the total terrestrial plant families) that have acquired the ability to enter the watery world. In this environment, drying out is rarely a problem but oxygen and light are often limited and competition from the algae can be extreme. In this situation many of these species have undergone a great reduction in vascular (transport) and supporting tissues. Concomitantly many SAVs have developed air spaces and passages as a

very simple kind of respiratory system to support rooting tissues buried in oxygen-poor sediments. Most SAVs in fresh water raise their flowers above the water surface. Many are insect pollinated, and a few are wind pollinated (see Table 14.2). In a sense, while vegetatively the tissues have evolved considerably to fit the very different aquatic environment, the reproductive process has remained mostly the same as that of their terrestrial ancestors. It is interesting to note that while very few freshwater aquatics produce underwater flowers and utilize water transport for their pollen, most marine SAVs have totally committed to the water life and keep their flowers submerged. This partly relates to tides and to the higher wave energies in the ocean. Most protected lagoons are more than 6 feet in depth and often have considerable currents and some wave action. (Where they are shallower and less open, they tend to become hypersaline.) This would provide a great structural hurdle for the plant rooted in the bottom and attempting to raise its flowers above the surface.

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FIGURE 14.14 Typical seagrass morphology, anatomy, and flowers. (A) Syringodium isoetifolium: (a) plant habit showing rhizome, roots, and leaf stalks and (b) rounded leaf showing few small vascular bundles and large lacunae (air spaces). (B) Halophila engelmann: (a) habit; (b) leaf cluster; and (c) serrated leaf tip. (C) Thalassia hemprichii: (a) rounded leaf tip and (b) habit. (D) Halophila decipiens: (a) habit with flowers; (b) flower showing anthers and pistil; and (c) mature beaked fruit with seeds. Reprinted with permission from R. C. Phillips and E. Menez. © Smithsonian Institution, Washington, DC 1988.

Submerged Aquatic Vegetation


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C


Marine SAV and Model Ecosystems

As we discussed in Chapter 12, there are many reasons to regard the SAV-dominated bottom as a biome of many communities extending worldwide. The presence of seagrasses and freshwater SAV communities greatly modifies the environment by trapping organic-rich sediments (and therefore nutrients) and by providing substrate (epiphytic algae and animals), cover (for fish and many invertebrates, both surface and infauna), and food (both trapped organics and the primary production of the plants themselves). There is also a very critical environmental and cultural reason to have a special interest in SAV communities. Algae can be highly productive and indeed respond quickly to the availability of light and nutrients in the water column. Algae also provide a generally highquality food to many waterfowl, fish, and invertebrates. However, algae mostly lack the tough supportive tissues of terrestrial plants, and when they die, they break down almost as quickly as they produce tissue when they are alive and growing. Thus, an algal-dominated environment can be a very erratic one, moving quickly with environmental changes. The stable type of algal community occurs in high-energy, low-light, or low-organic supply situations. SAVs are slower growing and the plant tissues are slow to break down. SAVs are able to oxygenate the organic-rich substrate (which they have trapped) and to extract the nutrients through their rhizomes and root hairs. Low turbidities, moderate organic sediment supply, and moderate energy levels in bays and protected areas lead to stable, species-rich SAV ecosystems. Even when storm or winter conditions produce windrows of seagrasses on the beach, breakdown is slow and nutrient return to the water column is stretched out over a long period of time. Human activities in semiprotected coastal bays and estuaries, particularly in increasing both nutrients and turbidities, have resulted in sometimes disastrous losses of SAV communities. This provides unstable ecosystems with more limited productivities and a reduction in effective use of the available energy supply. Although SAV biomass levels may be high as herbaceous land plants go, they do not match the biomass levels of woody land plants or even kelp or rockweed beds. Nevertheless, SAVs can be among the most productive of plant communities (Table 14.3). It is particularly interesting that seagrasses in a generally poorer nutrient environment are more productive on an areal basis than freshwater aquatics. Although whether the availability of carbon dioxide (or bicarbonate) is relatively limiting in fresh waters has been debated (see Chapter 8), it seems more likely that a generally higher physical energy level (Chapter 2) and greater light availability (because of lower turbidity) are the primary factors. As we have discussed, higher freshwater

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nutrients may actually favor attached algae (as aufwuchs) and limit aquatic plant production. Much of the SAV nutrient supply is probably derived from the sediments. Seagrasses generally have a higher root to shoot ratio (⬎1) than their freshwater counterparts. This probably relates to the lower nutrient levels and higher wave and current energies in the ocean. Seagrass beds can be heavily grazed, although exactly how much has been hotly debated (Stevenson, 1988). It seems clear that, at least in the temperate environment, much of the SAV production goes to detritus rather than grazers. However, much of algae production in the temperate and colder environment also goes to detritus rather than grazers. Certainly in tropical lakes and rivers there are many fish grazers, and this has great importance to the aquarist. We discuss these matters in Chapter 15. The microcosm or aquarium is often operated in a similar way to the very troubled and unstable farm pond, bay, or estuary: excess higher food chain animals supported by artificial feeding and high nutrient levels, low-light intensities, and limited invertebrate fauna, especially filter feeders. In semiclosed ecosystems, whether fresh or salt water, it is crucial to maintain a moderate to low nutrient environment rich in stabilizing SAVs where appropriate. In Chapter 11, we discussed methods for maintaining normal nutrient levels. Even without sophisticated nutrient measurements, one can easily determine when nutrient levels are normal by noting the balance between epiphytic algae and the SAVs. Most SAVs receive a major portion of their nutrients and carbon dioxide as HCO3 from their root systems. Thus, if the water column has low to moderate levels of nutrients, the algae are unable to grow so rapidly that the young growing tips and mid-aged leaves of SAV become heavily coated with an aufwuchs of algae, sediment, and small invertebrates. As we discuss in Chapter 15, a moderate level of grazing (both algae and SAV) is important in this equation. However, low nutrients provide the critical starting point.

MARINE SAV AND MODEL ECOSYSTEMS Only two families of higher plants, the Potamogetonaceae and the Hydrocharitaceae, both with fresh water species, have given rise to marine SAV. Marine SAVs or “seagrasses” occur on coasts over the entire world’s oceans except for the strictly Arctic and Antarctic zones. Only a few species are pantropic (Halophila decipiens) or pantemperate (Zostera marina). Most species occur throughout their respective ocean temperature zones (Indo-Pacific, Tropical Atlantic, etc.), though a few regions are unusually rich in endemic species (South Australia, Japan). Almost all marine

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14. Primary Producers TABLE 14.3 Comparison of Biomass and Productivity of Selected Fresh Water, Brackish, and Marine Macrophytes Rates of productivity Peak biomass (g dw/m2) Species/location

Fresh water and brackish Vallisneria spiralis L. Merrimajeal, Australia Vallisneria americana New York State Wisconsin Mississippi River Maryland Myriophyllum spicatum Wisconsin Wisconsin Wisconsin New York State New York State Maryland Hydrilla verticillata Florida Florida Maryland Ruppia maritima Chesapeake Bay, Virginia Redfish Bay, Texas Borax Lake, California Caimanero Lagoon, Mexico Marine Posidonia oceanica Mediterranean, Italy Posidonia australis Port Hacking, Australia NSW, Australia Spencer Gulf, Australia Syringodium filiforme Tague Bay, St. Croix Thalassia testudinum Texas Cuba Puerto Rico Laguna de Terminos, Mexico Jamaica Tague Bay, St. Croix Barbados Bimini Harbor, Bahamas Zostera marina L. Grevelingen, The Netherlands Oresund, Denmark Vellerup Vig, Denmark Brittany Coast, France Rhode Island Chesapeake Bay, Virginia North Carolina Nabeta Bay, Japan Netarts Bay, Oregon Izembek Lagoon, Alaska Heterozostera tasmananica Australia Amphibolis antarctica Shark Bay, Australia

(mg O2/h1/g1 leaf)

(g/C/m2/ day1)

NPP (g/m2/ 2 day)

Above

Below

Total

463

66

529

2.1

50 344 180 53

13 64 38 38

63 408 218 91

1.5

407 220

39

446

3.2 3.8–10.6

2–17 387 878

3.35 2–4 1.2–1.8 4.44

8.0 161.4 280 322 80–150 160 64

4

326

50

210

2.8–5.4 0.92 0.98

1000

0.9–9.7

600–1700 80 137–453 616

0.8–4.4 195

275 847–25 550 2457

1.9 1.9–5.2 5.5

6

0.3

60–250 76–517 564

1–16

880

2800 1444

8.0 1.6–2.2 0.7–1.4 1.9–3.0

77 200 75–94 290 226 260 65 150–225 180 222 84–256 500

1.8–2.4 35–50 160 217 314

110–144 450 443 470

1.7 2.9 5.9 4.4 6.7 2.02 1.1

71 56–214 900

292 140–470 1400

83–218 300–850

2.7 1.3–7.9 2.6–3.9

4.8

7.2 2.8 7.2–10.3 1.3–3.6

300–1150

600–2000

2–17

Freshwater SAV and Model Ecosystems

SAVs occur on weakly disturbed muddy to sandy bottoms. A few may grow over rock or coral from their sediment base. One genus of several species in temperate waters (Phyllospadix) prefers a rock substrate. The morphology or growth form of seagrasses is rather uniform: a rhizome with a primary growing tip, growing parallel to the substrate surface at shallow depth, and nodes that bear leaves, leaf stalks, and/or roots, depending on the genus. The roots bear abundant root hairs, and the leaf stalks may or may not be short shoots with abundant leaves. In some genera, secondary rhizomes may form at some nodes. Most seagrass leaves are flattened and straplike (Figure 14.14). Syringodium leaves are rounded, and Halophila has ovate leaves. In the late 1970s we established several tropical Atlantic seagrass beds in small aquaria (40–200 gallons) attached to coral reef microcosms. These were more or less successful for Thalassia, Halodule, and several siphonaceous greens. They were kept in operation only for a year or two. In 1980, we established a relatively large seagrass/lagoon community (500 gallons) attached to the Smithsonian coral reef. Williams and Adey (1983) describe the process in detail, and the entire microcosm is described in Chapter 20. Although the Halodule did not survive the first year and the Syringodium eventually died out (these may very well be successional effects), the Thalassia community remained densely developed over 20 years. Rich in small- and moderate-sized invertebrates, this community had fluctuated in blade length and density according to the size and type of fish grazers that were kept in the system. More recently we have attempted to establish Zostera marina and Ruppia maritima in a Chesapeake Bay mesocosm (Chapter 22) and Zostera in a Maine coast microcosm (Chapter 21). The constant “rooting activities” of crabs and fish in both of these systems, during more than a year in some cases, has thwarted our efforts. This may well have been a scaling problem: too many root-grubbing species perhaps without higher predator control in small systems. However, in a larger mesocosm system (Florida Everglades, Chapter 22), with a richer invertebrate and fish fauna and better wave action (sandy mud rather than mud), we were quite successful with establishment of the dominant Florida seagrasses. Nine years after stocking, Thalassia with lesser amounts of Halodule and Syringodium formed a dense grass bed, in spite of the considerable number of rooting crabs and fish. Our suggestion to aquarists seeking to construct seagrass systems is simply to stock with both block transfers and seedlings. Both survived in our system. If seedlings are not available, it is important to collect rhizome tips. When collecting and transporting seagrasses sufficient undisturbed sediment must be brought with them, at

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least 6 or more inches thick; the rhizomes should not be allowed to wash out during transportation.

FRESHWATER SAV AND MODEL ECOSYSTEMS Plants, having established a foothold on the land and finally, some 100 million years ago, having evolved flowers as an effective means of reproduction, underwent an enormous adaptive radiation, eventually producing tens of thousands of species in hundreds of major lines or families. In addition to the ferns and fern allies, who were never far removed from the water environment, members of many flowering plant families have returned to the freshwater environment. It is striking that only a limited number of morphologies work in the aquatic situation, and these can be arranged approximately in order of reduction or adaptation to the generally less-demanding conditions (Figure 14.15). The end points of this reduction are: (1) the tiny duckweeds, more like the generally simpler algae except for the miniature telltale flowers, and (2) the totally submerged naiads with their waterborne pollen. Also, note the Type 8 SAV, some of which have returned to the marine environment, as we discussed above. Selected examples of this morphological array are shown in Figures 14.16–14.23. On a typical lake with moderate erosion and slope, SAV vegetation occurs lakeward of a more or less narrow band of emergent vegetation or marsh (Figure 14.24). Depending on the depth and turbidity, the morphological forms occur in an irregular zonate pattern: partly emerged, floating, and totally submerged, followed by algae at the greatest depth that plants are found. We have developed several freshwater mesocosms and aquaria that have included SAVs. These are described more fully in later chapters. Here, we simply make some general points. We have never used undergravel filters and we have rarely used a substrate other than that from which the plants were collected. In common with all of our benthic establishment techniques, the requisite bottom was collected with its plants and invertebrates as intact as could be managed in often difficult collecting situations. Our attempt was always to stock initially with every member of the analog community and to let our particular ecosystem variant “select” the appropriate species. Often multiple insertion of key SAV species was carried out before success was achieved. In some cases in the first year of operation, a bloom of one or two species developed. This can be controlled by selective weeding or disturbance. We have tried several aquarium simulations using a variety of SAVs. As long as the water column itself was

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FIGURE 14.15 Hypothetical patterns of evolution of morphological forms of submerged aquatic vegetation (SAV) from emergent aquatic ancestors. Type forms shown in Figures 14.16–14.23.

233

Freshwater SAV and Model Ecosystems

Gentianaceae Nymphaeoides spp. Primulaceae Samolus floribundus Daucaceae Hydrocotyle vulgaris Nymphaeaceae Barclaya longifolia Brasenia schreberi Nuphar spp. Nymphaea spp. Butomaceae Hydrocleis nymphacoides Aponogetonaceae A. distachyus Araceae Orontium aquaticum

FIGURE 14.16 Type 2 SAV. Plants rooted in the bottom but having long petioles that bring floating leaves to the surface and stalks that float or elevate flowers. Drawing (Nymphaea elegans) after Godfrey and Wooten (1981); plant list after Stodola (1967).

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aquarium, with a small ATS for water quality control, was stocked with several inches of barnyard soil and cow manure overlain by several inches of gravel. SAV growth was particularly successful in this case over several years of operation. This demonstrates the principle of sub “geological storage” with only very slow transfer of nutrients to plant tissue and ultimately to the water column, where they are exported by the ATS unit. The primary problem with freshwater SAV maintenance is that of SAV grazing fish. To some extent this problem can be controlled by using particularly tough species of SAV and periodically “feeding” a preferred softer species. However, even a small headstander, silver dollar, or to a lesser extent Tilapia, for example, can raise havoc with the plant standing crop. These matters are discussed further in Chapter 15.

EMERGENT AQUATIC VEGETATION

FIGURE 14.17 Type 3 SAV. Plants roots in the bottom, a rosette of submerged leaves, sometimes with aerial leaves little modified, flowers aerial, usually insect pollinated. Drawing (Sagittaria graminea) after Godfrey and Wooten (copyright 1979 by the University of Georgia Press, used by permission); plant list after Stodola (1967).

scrubbed to moderate nutrient levels, even with heavy fish and artificial feed loadings, no serious problems have been encountered with aufwuchs coatings or plant loss. Inclusion of a few algae eaters, such as snails and stick-cats (Farlowiella), ensures the minimizing of aufwuchs. In one test case, the base of a 70-gallon

In the transition from land to open water, a band often narrow but sometimes extraordinarily wide, there exists a zone of soil or substrate that is generally waterlogged. This band is flooded periodically either twice daily by tides or seasonally by variations in rainfall. If wave energy is high, the band is occupied by rock or moving sand and the appropriate algal vegetation or no vegetation at all (on sand). On the other hand, if wave energy is low, fine, relatively stable sediment can collect. Often this sediment becomes vegetated, dominantly by flowering plants but usually with an understory or plant coating (aufwuchs or periphyton) of algae. The community that occupies this zone is called a marsh if low and mostly herbaceous, or a swamp if dominantly occupied by woody plants. Although it might seem that this dominantly higher plant community should be heavily occupied by relatives of the same plants that have adapted to the submerged environment, in fact this is only rarely the case. The dominant herbaceous plants in the marsh are grasses, sedges, rushes, and cattails, families with very few submerged relatives. While the woody plants of swamps came from a wide variety of flowering plant families, and cypress, an extremely important swamp component in North America, is a conifer, virtually none of the woody members or their relatives have made it under water. We do not discuss woody swamp plants in any depth in this chapter. Mangroves and cypress, along with a few other groups, however, are treated in Chapter 22 on the Everglades mesocosm. We have placed SAV, including seagrasses, as a biome, separate from EAV. Although sometimes with very sharp boundaries, and formed by very different plant groups, these biomes often grade into each other over a linear

Emergent Aquatic Vegetation

FIGURE 14.18 Type 4 SAV. Plants rooted in the bottom, often very elongate stems, some aerial leaves, often strikingly different from submerged leaves, flowers elevated, usually insect, wind, or, rarely, water pollinated. Drawing (Proserpinaca pectinata) after Godfrey and Wooten (1981); plant list after Stodola (1967).

235

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FIGURE 14.19 Type 5 SAV. Plants fully floating, with roots usually not reaching to the substrate, flowers aerial, mostly insect pollinated. Drawing (Eichhornia crassipes) after Godfrey and Wooten (copyright 1979 by the University of Georgia Press, used by permission); plant list after Stodola (1967).


FIGURE 14.20 Type 6 SAV. Plants fully floating, greatly reduced and “thalloid” in form. Form of pollination uncertain. Drawing (Spirodela polyrhiza) after Godfrey and Wooten (copyright 1979 by the University of Georgia Press, used by permission); list after Stodola (1967).

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FIGURE 14.21 Type 7 SAV. Plants rooted in bottom, leaves typically strap-shaped, elongate, flowers raised to surface, many water pollinated. Drawing (Vallisneria americana) after Godfrey and Wooten (1981); plant list after Stodola (1967).


FIGURE 14.22 Type 8 SAV. Plants rooted, generally rhizomatous, leaves mostly elongate, strap-shaped, flowers submerged, water pollinated. Drawing (Thalassia testudinum) after Godfrey and Wooten. Copyright 1979 by the University of Georgia Press, used by permission.

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FIGURE 14.23 Type 9 SAV. Unrooted, totally submerged with water-pollinated submerged flowers. Drawing (Najas minor) after Godfrey and Wooten (copyright 1979 by the University of Georgia Press, used by permission); plant list after Stodola (1967).


zone, sometimes tens of feet wide. While this gradation might seem excessive to allow biome differentiation, especially considering the linear character, it is helpful to remember that terrestrial biomes intergrade over tens, sometimes hundreds, of miles. Also, marshes, even if of great length, typically range from tens of feet to several miles wide. This relative narrowness results from the sharp change of the environmentally determining conditions in the transition from land to open water. In Florida, for example, where the terrain is of very low relief,

FIGURE 14.24 Section across exposed eastern shore of Lake Kisajno, Poland. An emergent vegetation on the beach terrace of Phragmites australis is succeeded on the dropoff by Ranunculus circinatus, Elodea canadensis, and Charophytes. After Hutchinson (1975). Reprinted by permission of John Wiley & Sons, Inc.

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marsh, with its characteristic plants, covers thousands of square miles. Likewise, in the shallow offshore, seagrasses occupy even greater areas. Within the largely marshy fresh and salt Everglades complex, patches of open water, sometimes richly endowed with SAV, do exist. However, this mosaic of SAV biome within a much larger emergent vegetation biome reflects the fact that water abundance, light, and substrate, as the primary determiners of biome nature in the water world, have a very different character of distribution than do temperature and precipitation on land. Marshes are among the most productive communities on Earth (Figure 14.25). Normally endowed with an overabundance of water, light, nutrients, and carbon dioxide, it is only the very basic physiological and biochemical limitations of plant structure that put bounds on photosynthesis. Many marsh plants are sun plants in that they do not saturate for photosynthesis but rather show higher and higher rates to the highest light intensities. We have added ATS (see Chapter 11), our primary water quality control device, to Figure 14.25 to demonstrate the functional relationship to other aquatic plants. ATS algae are technically submerged, though because of the thin water layer, photosynthetically they function as emergent plants. Their productivity is roughly twice as high as their emergent distant relatives, in part because of the surge energy that provides water mixing and light flashing. While grazers of the higher plants of marshes are numerous in kind (deer,

FIGURE 14.25 Net primary productivity (biomass developed) of submergent and EAV compared to phytoplankton and major terrestrial communities. After Leith and Whittaker (1975).

242


muskrat, birds, insects, and snails, to name a few), rarely is a major portion of the primary production removed by grazing. In freshwater marshes, except in patchy muskrat “eat-outs,” typically no more than 10% or 20% of the net primary production is consumed by grazers. In marine and estuarine marshes, the figure is even lower. Most of the production eventually either degenerates in place or is removed by currents and tides to basins or beaches where gradual breakdown produces a bacteria-rich detritus. This marsh plant production thus eventually becomes a critical, largely seasonal, food and nutrient source for the adjacent lake or estuary (see Chapter 18). The dominating marsh plants, fresh and salt water, whether grasses (Figure 14.26), sedges (Figure 14.27), rushes (Figure 14.28), or cattails (Figure 14.29), have a number of characteristics in common that address the requirements for success in this very rich but in some ways difficult environment. All are monocots with long, thin, or even rounded leaves. Basically the leaves are mounted on rhizomes, which, once established, provide an enormous colonizing potential. Also, all of these plants are wind pollinated, an important feature in environments adjacent to large lakes or the ocean, areas that are often windswept. Similar to SAVs, EAV often has lacunae or air spaces that allow the movement of oxygen from leaves to rhizomes and roots. Some have been shown to oxygenate the generally oxygen-deficient soil in which they grow. The dense growth of emergent aquatics, the resultant tendency to accumulate often organic-rich silt, and a general lack of grazing with accumulation of detrital biomass all lead to a rather extreme environment in the marsh (Figure 14.30). Such conditions are exacerbated in a salt marsh, where landward and away from channels, salinities can become very high to the point of causing species zonation and sharply reduced growth (Figure 14.31). Some salt marsh plants have salt-excreting glands and, lacking rain or wind, the excreted salt can be seen on the blades (Phleger, 1977). In dry climates, the zone of flooding at the highest tides becomes a salt flat or barren, devoid of plant life. In lakes, the location of the EAV, or reed beds as they are sometimes called, lies in the transition zone between land and water. However, the extent of development ranges widely depending on wave exposure and steepness of the shore (Figure 14.32). Under some conditions of extremely rapid and matted growth, the “reed bed” can develop into a floating platform. Aquatic vegetation, emergent and submergent, has been treated as largely the province of higher plants that have returned to the watery environment. Especially in the emergent environment, very little of the higher plant production is available to grazers, and this is where algae

play a critical roll. As the often structural element of the aufwuchs, or periphyton, community that coats all submerged objects (Figure 14.33), algae become an important primary producer, often the major direct plant food supply to fish and invertebrates (see Figure 13.1).

EAV AND MODEL ECOSYSTEMS We have established a number of microcosms and mesocosms with emergent vegetation. The first was a very small and simple salt marsh attached to the rocky Maine shore system. It included both Spartina alterniflora and Spartina patens, smooth cordgrass and salt hay, the primary elements of Maine coastal marshes. The collections were taken using the block transfer system. The tide on the Maine coast where samples were collected has a spring range of about 12 feet. The microcosm has a 38-cm spring tide range, with a neap to spring high tide difference of 9 cm. S. alterniflora was established in the upper half of the neap range and S. patens in the spring tide zone above neap highs. Both species established easily and functioned well in this system for 15 years. The second set of marshes, including linked but separate full-salt, brackish, and tidal fresh marshes, was established in an artificially lighted Chesapeake Bay mesocosm in 1987. Transfer was also entirely by block methods, and during the early 1990s, the system had a mature diversity of about 50 species of emerged aquatics. Most of the dominants, including S. alterniflora, S. patens, Distichlis picata, Juncus roemerianus, Iva frutescens, Limonium sp., Scirpus spp., Carex sp., and Pontederia cordata, were present in this model estuary (see Chapter 22). Typha angustifolia remained present in the tidal fresh water part of this system, following its original stocking; however, it was never dominant, probably because of the small space and interference by other species. This mesocosm had a maximum tide range of 6 inches, as compared to 1–2 feet throughout most of Chesapeake Bay. Establishment of block surfaces was directly proportional to tide levels. S. alterniflora did not survive the first and second winters in the polyhaline zone but did survive in the marine zone. It is possible that insect predation is involved, a problem we had not encountered in earlier mesocosms. Otherwise, no significant difficulties were encountered. A miniature, 70-gallon version of a Chesapeake Bay salt marsh at 26 ppt was later established separately. In this aquarium, also with a 6-inch semidiurnal tide, the two Spartina species, Distichlis spicata, Limonium sp., and Salicornia sp. were similarly established with ease. Here, the difficulty lay with a small J. roemerianus colony that provided virtually no growth in about a year of operation. Since

EAV and Model Ecosystems

FIGURE 14.26 Emergent marine and aquatic grasses. (A) Salt marsh Puccinellia spp. from northern Europe. Fresh water: (B) Glyceria borealis, (C) Leersia oryzoides, and (D) Zizania aquatica from New England. (A) After Fitter et al. (1984) and (B–D) after Hutchinson (1975), reprinted by permission of John Wiley & Sons, Inc.

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FIGURE 14.27 Emergent sedges of the genus Scirpus from British streams and ponds. Note triangular format and “cones.” After Fitter et al. (1984).

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FIGURE 14.28 Emergent rushes of the genus Juncus (A) from British salt marshes and (B) New York lake margins. (A) After Fitter et al. (1984) and (B) after Hutchinson (1975), reprinted by permission of John Wiley & Sons, Inc.


FIGURE 14.29 Freshwater EAV of the genera: (A,B) Typha (cattails) and (C) Sparganium (bur-reed). After Hutchinson (1975). Reprinted by permission of John Wiley & Sons, Inc.

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FIGURE 14.30 Change of major chemical characteristics of the water column on passing from open tropical lake into a submerged aquatic zone and finally into an emergent aquatic zone of sedges (Papyrus). After Carter (1955).


FIGURE 14.31 (A) Zonation by dominating species in a New England salt marsh. (B) Cross section of a midAtlantic coast salt marsh showing species zonation, biomass, and soil salinity. (A) After Chapman (1960) and (B) after Haines and Dunn (1985).

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FIGURE 14.32 Vegetation profiles along various types of lake shores. (A) High-energy, eroding steep shore with emergent vegetation lacking and submergent vegetation minimum. (B) Moderate-energy, steep shore with emergent vegetation lacking, but strongly developed submergent vegetation. (C) Moderate-energy, low-slope shore with a narrow, partly protective emergent vegetation zone and submergent aquatics on both protected shelf and the lake slope. (D) Protected, low-sloping lake shore with a rich development of emergent and submergent vegetation. (E) Very-low-energy, low-sloping shore developing a floating shelf of emergent vegetation and with a floating leaf bed of submerged aquatics. After Hutchinson (1975). Reprinted by permission of John Wiley & Sons, Inc.

J. roemerianus grew extensively in the large system, flowering frequently, this may indicate a negative interaction of one species on another in such a small system. Peak light levels are about 800 µE/m2/s in the aquarium compared to about 1600 µE/m2/s in the mesocosm, which could also be a factor. Finally, in 1988, an Everglades mesocosm with both salt and fresh marshes was established in a greenhouse in Washington, DC. This system, with its salt marsh and mangrove communities, operated for over 10 years and was the subject of detailed status analyses after 4 and 8 years of operation and is described in depth in Chapter 22.

PLANT COMMUNITIES AND THE RESTORATION OF WILD ECOSYSTEMS All types of plant communities in wild ecosystems can be affected by human activities. Fishing can directly

or indirectly affect benthic algae, or even plankton, and direct physical destruction can reduce marshland, swamps, and shorelines to a fraction of their preColumbian levels. For the ecosystem restorer, these are the more obvious problems requiring physical biological intervention and numerous studies have been undertaken to establish procedures for restoration (Lewis, 1982; Berger, 1990). However, an almost universal problem in fresh, estuarine, and coastal marine situations alike is eutrophication. Elevated nutrient levels primarily from farming and sewage plants can be devastating both to the SAV communities of coastal areas and to the stability of phytoplankton (see Chapter 17). In some places, large public organizations, using considerable financial resources, have been devoted to nutrient reduction. However, even if the publicly organized processes of amelioration (mostly BMPs, best management practices, for farming areas, and BNR, biological nutrient removal, for sewage system upgrades for cities) achieves some success, rarely does it keep up

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References

nonpoint-source amelioration. Also, the 1–2 mg/liter nitrogen and phosphorus effluent levels of the newer BNR sewage systems are not adequate to prevent eutrophication downstream. Lower concentrations can be achieved by BNR, but the cost is so high that rarely, if ever, is it likely to be achieved. Here again, low cost ATS systems can usefully be employed, with solar energy capture as a side benefit. Nutrient reduction can allow reclamation of plant communities damaged or destroyed by eutrophication.

References


FIGURE 14.33 Floating pipe from a European lake showing the algal communities that typically develop the “aufwuchs” or periphyton that coats emergent and submergent aquatic vegetation. After Hutchinson (1975). Reprinted by permission of John Wiley & Sons, Inc.

with population growth. Population growth needs to be controlled. However, until that can be accomplished, the large-scale application of ATS systems (see Chapter 25) could assist other efforts to provide the largely missing

Adey, W. (1978) Algal ridges of the Caribbean Sea and West Indies. Phycologia 17: 361–367. Adey, W. (1986) Coralline algae as indicators of sea level. In: Sea Level Research: A Model for the Collection and Evaluation of Data. O. van de Plassche (Ed.). Geo Books, Norwich, Connecticut. Adey, W. (2005) Plant conservation, a natural history approach. In: Marine Plant Diversity. G. Krupnick and W. J. Kress (Eds). University Chicago Press, Chicago. Berger, J. (1990) Environmental Restoration. Island Press, Washington, DC. Bold, H. and Wynne, M. (1985) Introduction to the Algae, 2nd edn. Prentice Hall, Englewood Cliffs, New Jersey. Burkholder, J.-A. (1996) Interactions of benthic algae with their substrata. In: Algal Ecology, Freshwater Benthic Ecosystems. R. J. Stevenson, M. Bothwell, and R. Lowe (Eds). Academic Press, San Diego, California. Carter, G. S. (1955) The Papyrus Swamps of Uganda. Heffer, Cambridge. Chapman, V. (1960) Salt Marshes and Salt Deserts of the World. Interscience, New York. Dawes, C. (1981) Marine Botany. Wiley-Interscience, New York. Fitter, R., Fitter, A., and Farrar, A. (1984) Collins Guide to the Grasses, Sedges, Rushes and Ferns of Britain and Northern Europe. Collins, London. Fritsch, F. E. (1952) The Structure and Reproduction of the Algae, Vol. II. Cambridge University Press, Cambridge. Fritsch, F. E. (1956) The Structure and Reproduction of the Algae, Vol. I. Cambridge University Press, Cambridge. Godfrey, R. and Wooten, J. (1979) Aquatic and Wetland Plants of the Southeastern US: Monocotyledons. University of Georgia Press, Athens. Godfrey, R. and Wooten, J. (1981) Aquatic and Wetland Plants of the Southeastern US: Dicotyledons. University of Georgia Press, Athens. Haines, B. and Dunn, E. (1985) Coastal marshes. In: Physiological Ecology of North American Plant Communities. B. Chabot and H. Mooney (Eds). Chapman and Hall, New York. Hutchinson, G. E. (1975) A Treatise on Limnology, Vol. III. Limnological Botany. Wiley, New York. Knoll, A. (2003). Biomineralization and evolutionary history. Rev. Mineral. Geochem. 54: 329–356. Lee, R. (1999) Phycology, 3rd edn. Cambridge University Press, Boca Raton. Leith, H. and Whittaker, R. L. (1975) Primary productivity of the biosphere. In: Ecological Studies. Springer-Verlag, New York. Lewis, R. (1982) Creation and Restoration of Coastal Plant Communities. CRC Press, Boca Raton. Littler, M. and Littler, D. (2000) Caribbean Reef Plants. Off-Shore Graphics, Inc., Washington, DC. Lobban, C. and Harrison, P. (1994) Seaweed Ecology and Physiology. Cambridge University Press, Cambridge.

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Luning, K. (1990) Seaweeds: Their Environment, Biogeography and Ecophysiology. Wiley-Interscience, New York. Margulis, L. and Sagan, D. (1986) Microcosms. Summit Books, New York. Margulis, L. and Schwartz, K. (1988) Five Kingdoms: An Illustrated Guide to the Phyla of Life on Earth, 2nd edn. Freeman, New York. Muhlberg, H. (1982) The Complete Guide to Water Plants. EP Publishing Ltd., German Democratic Republic. Phillips, R. C. and Menez, E. (1988) Sea grasses. Smithson. Contrib. Mar. Sci. 34: 1–104. Phleger, F. B. (1977) Soils of marine marshes. In: Ecosystems of the World – Wet Coastal Ecosystems. V. J. Chapman (Ed.). Elsevier, Amsterdam. Prescott, G. (1951) Algae of the Western Great Lakes Area. Reprint 1982. Cranbrook Institute of Science, Koeltz. Price, I. and Scott, F. (1992) The Turf Algal Flora of the Great Barrier Reef. Part I, Rhodophyta. James Cook University, Townsville, Australia. Sculthorpe, C. (1967) The Biology of Aquatic Vascular Plants. Reprint 1985. Arnold, Koeltz.

South, R. and Whittick, A. (1987). Introduction to Phycology. Blackwell Science Publishers, Oxford. Sprung, J. (2002) Algae, a Problem Solvers Guide. Ricordea Publishing, Coconut Grove, Florida. Stevenson, J. C. (1988) Comparative ecology of submerged grass beds in freshwater, estuarine and marine environments. Limnol. Oceanogr. 33: 867–893. Stodola, J. (1967) Encyclopedia of Water Plants. T. F. H. Publications, Neptune City, New Jersey. Taylor, W. R. (1957) Marine Algae of the Northeastern Coast of North America. University of Michigan Press, Ann Arbor, Michigan. Van Den Hoek, C., Mann, D., and Jahns, H. (1995) An Introduction to Phycology. Cambridge University Press, Cambridge. Williams, S. and Adey, W. (1983). Thalassia testudinum Banks ex Konig. Seedling success in a coral reef microcosm. Aquat. Bot. 16: 181–188.

C H A P T E R

15 Herbivores Predators of Plants and Omnivores, Predators of Plants and Animals

With the exception of a few interesting, but globally very minor ecosystems, virtually all energy required to drive the Earth’s biosphere is derived from the sun. The result of this energy capture by plants (including algae) is primary production, the building of plant biomass, or to put it in other terms, the chemical conversion and storage of energy. The food value of plant bodies provides the energy to operate the remainder of the biosphere. Depending on the ecosystem, some of this plant production becomes detritus after the demise or partial demise of the plant. In some cases, the percentage of the plant biomass that becomes detritus is very large (see Chapter 18). However, in other ecosystems large amounts of plant production are eaten directly by herbivores such as grazers, browsers, suckers, and seed or fruit eaters. Most people are generally aware of the phenomenon of overgrazing. When there are too many plant-eating animals, whether in a pasture or on a range or countryside, without natural or human limitation, the plants are eaten faster than they can grow. The net result is a relatively barren landscape, or one minimally occupied by inedible plants. Total plant production is then far below potential and the grazers are food limited. In the dry terrestrial environment, deserts may result, and a feedback loop is often present. The presence of vegetation encourages rain. Once it is gone, in the marginal situation, rainfall, and plant productivity are greatly reduced. In another situation, a reduction of higher predators, such as grizzly bears and mountain lions, can lead to overpopulation by deer or elk. This also results in overgrazing and a panoply of negative ecological effects (see Chase, 1987). In a synthetic ecosystem that models a well-lighted aquatic ecosystem, plants will likely be present, as will herbivory. While the desertification process is

not a consideration in the aquatic environment, reduced plant production because of overgrazing often results in a degradation of environmental quality. With few plants, oxygen levels are lower, pH values are more acid, nutrient levels are higher, cover and substrate are reduced, sedimentation is slower (thereby reducing light), wave and current action are increased, and of course potential food is reduced. Thus, a balance of plant growth and herbivory is crucial to wild ecosystems and to the modeling of mesocosms and microcosms as well as aquarium management. Returning that balance can also be a crucial part of the restoration of degraded ecosystems. Grazing fish can significantly reduce algal vegetation. For example, Power et al. (1985) describe how a grazing minnow (Compostoma anomolum) is capable of causing considerable reduction of algal biomass as well as changing algal community structure in a freshwater stream. Significantly, those same authors were also able to show that where the algal turf was reduced, the addition of predator bass caused the minnows to decline and the algal biomass to increase again. Any aquarist who has kept headstanders, parrotfish, or tangs with plants, including algae, has experienced the same basic phenomenon, though not usually with a fish predator present to control the grazer. Many situations have been described in shallow marine environments in which sea urchins, in particular, have devastated highly productive algal communities, such as kelp forests, when their predators were removed, particularly by human fishing or hunting. Cyclic patterns of several years, similar to the classic terrestrial cycles of owls and lemmings, and lynx and hares, but alternating between “urchin–coralline barrens” and kelp forests have been described. However, as Lobban and Harrison

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FIGURE 15.1 Model of the relationship of algal morphology (at the community scale) and community standing crop and productivity to the intensity of grazing by larger animals. The model, modified after Hackney et al. (1989), was specifically developed for coral reef ecosystems.

(1994) point out, it can rarely be demonstrated that a simple asynchrony between predator (herbivore) and prey (plant) is responsible for the complex cycling. While extremely difficult to demonstrate, it seems likely that other factors – temperature, weather, parasites, disease – play a role in mediating these events. Figure 15.1 shows a diagrammatic and idealized grazing continuum model specifically developed for coral reefs but generally applicable to all benthic communities. The grazing pressure level can be established by many factors, including wave action, limiting of grazing, and predator control. The model also assumes the moderate availability of algal requirements, specifically light and nutrients, and the lack of a direct physical control of algae (drying, ice, etc.). It is significant that the highest levels of productivity occur not with very limited grazing but with moderate grazing. In light of the diversity discussion presented in Chapter 12, such grazing limits algal species primarily to those that grow and reproduce quickly (in the case of coral reef algal turf species), while species that must invest energy in building structures to compete for space, or in defensive skeleta or toxic compounds, cannot generally compete. Algae and macrophytes are not necessarily helpless victims to grazers. On the contrary, some plants are actually helped by grazing, for example prairie grasses and reef algal turfs (Owen, D., 1980; Adey and Hackney, 1989). These plants are adapted to being eaten – they grow fast from their base, reproduce quickly, and are resistant to environmental factors (wind and waves) that

may damage other plants. Most important, their larger plant competitors do not do well when constantly snipped off at small size. Also, many plants attract specialized predators of pollen, fruit, or seeds to gain fertilization or distribution of seeds, forming a symbiotic relationship. However, even beyond these predatoradapted plants, except where human effects have unbalanced ecosystems, or where seasonal effects of cold or dry conditions or other weather anomalies have considerably affected plants, only 10–50% of net plant production is normally eaten (Owen, J., 1980). In some cases, such as salt marshes, the amount directly eaten by grazers can be extremely small (Parsons and de La Cruz, 1980). Plants, including many algae, have also developed many direct defenses. Woody plant tissue, as well as much coarse greenery, is generally inedible by animals. As most people know, in the forest one can get very hungry with abundant potential plant food all around. While herbivores abound, plants protect themselves in many ways. Particularly in the marine environment some algae develop tough, cellulosic or even calcium carbonate walls, making grazers pay a high price for their meals. An overgrazed situation in warm, calcium carbonaterich waters is likely to show reduced photosynthesis. However, because of the abundance of fast-growing algal turfs and those resistant algae with tough walls, the reduction is likely to be small. Meanwhile the herbivores must constantly guard against their own predators. Thus, as a whole “the world is green” (or brown or red in the algal world). Under water, in most shallow zones, plant growth exceeds animal growth, as it must, except where food input from another community is important. However, in the aquatic, estuarine, and marine coastal environments, the human factor enters into the plant-herbivore equation. Human building and farming activities on the land release enormous quantities of silt from eroded soils into natural waters. These sediments produce elevated turbidities, which reduce light and therefore aquatic plant photosynthesis. Excess nutrients cause blooms of planktonic algae that further reduce light for submerged aquatic vegetations (SAVs), can favor toxic blue-greens or dinoflagellates, and can even produce hypoxic or anoxic conditions. Along with lower light levels, water quality degeneration, resulting from herbicides and numerous other chemicals, can also hinder balanced plant growth. Under these conditions, herbivores, particularly fish and waterfowl, often overgraze and then become strongly limited themselves.

TYPES OF HERBIVORES Table 15.1 lists the major orders of animals with herbivorous members and indicates what form the

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Types of Herbivores TABLE 15.1 Major Orders of Marine and Aquatic Animals with Herbivorous Members*

Phylum

Class or order

Frequency of herbivores within group

Name

Example

Example of tissue eaten

Mode of feeding

Invertebrate herbivores Protozoa Several

Many

Amoeba

Amoeba dubia

Diatoms

Nematoda Echinodermata

Several Echinoidea

Many Many

Nematodes Sea urchins

Algae Seaweeds

Mollusca

Gasteropoda

Most

Slugs, snails

Leaves, fruits

Rasping

Amphineura

Virtually all

Chitons Bear animalcules

Algal turfs, corallines Sphagum moss

Rasping

All

Dorylaimida Echinus esculentus Deroceras reticulum Ischnochiton ruber Macrobiotus macronyx

Cytoplasmic engulfing Sucking cell contents Rasping

Many Most

Water fleas Copepods

Daphnia pulex Calanus

Diatoms Phytoplankton

Selective filtering Selective filtering

Some Some

Slaters Gammarids

Seaweed Microalgae

Chewing Browsing

Most

Krill

Phytoplankton

Selective filtering

Decapoda Plecoptera

Few Few

Crabs, lobsters Stoneflies

Ligia oceanica Gatmmarus neglectus Euphausia superba Birgus latro Isoperla

Fruits, etc. Algae

Ephemeroptera

Most

Mayflies

Ephemerella

Turf grazers

Trichoptera

Few

Caddis flies

Neophylax

Algae

Coleoptera

Few

Crawling water beetles

Haliplus

Algae

Chewing Browsing or filter feeding by larval stages Browsings or filter feeding by larval stages Browsing or filter feeding by larval stages Browsing or filter feeding by larval stages

Diptera

Many

Midges

Microtendipes

Algae

Browsing or filter feeding by larval stages

Some Few Few Some

Bony fishes Lung fishes Frogs, toads Sea turtles

Water weed Stoneworts Water weed Seagrasses

Browsing Browsing Browsing Browsing

Squamata Anseriformes Passeriformes

Few Many Few

Snakes, lizards Ducks, geese Many marsh birds

Carp Protopterus Rana tadpoles Chelonia myolas Giant iguana Anas Agelaius

Lagomorpha Rodentia

Few Some

Sirenia

All

Marsh rabbits Muscrat, marsh rats Sea cows

Tardigrada Arthropoda

Crustacea Subclass Branchiopoda Copepoda Malacostraca Order Isopoda Amphipoda Euphausiacea

Insecta

Vertebrate herbivores Actinopterygiia Several Sarcopterygia Dipnoi Amphibia Reptilia Chelonia

Aves

Mammalia

*Modified after Crawley (1983).

Sucking cell contents

Silvilagu Ondatia

Seaweeds Water weeds Marsh and wetland seed eaters Marsh plants Marsh plants

Browsing

Trichechus

Seagrasses

Browsing

Seed eaters

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herbivory takes. Many phyla have at least a few herbivores, and a large number of orders have all or most of their members at that trophic level. In orders primarily characterized by aquatic and marine members, an even higher percentage is characterized by all or most of their members being herbivorous. In the terrestrial environment, because of the special adaptations of plants required to stand up in a dry atmosphere and carry out sexual reproduction, the range of types of herbivory is very broad, including grazing, browsing, rasping of bark or stems, sucking of plant juices, predation on flowers (nectar or pollen), and feeding on fruit and seeds as well as plant roots. Virtually all of the same types of herbivory occur in wetlands, marshes, and swamps. However, in the truly submerged environment, although all these same types can be identified in a few special cases, herbivory is largely restricted to grazing and browsing. Because submerged plants generally lack the strengthening requirements of land plants (lignin and massive cellulose), the adaptations for grazing and browsing are not as extensive as they are in land plants. On the other hand, a major form of plant defense under water is calcification, and some animals (e.g. chitons, limpets, and parrotfish) are adapted, sometimes extensively, to overcome these defenses to varying degrees. And, as we now have come to recognize, some of these calcified algae develop accommodations to such grazing in the form of specialized structures. These species give up some tissue in return for protection from faster-growing algae that would out-compete the crust. This is a simpler form of co-evolution, much as the more complex relationship between pollinating insects and the flowers of higher plants.

PLANT DEFENSES As mentioned above, some plants (all are algae) have developed “rock-hard” skeleta of calcium carbonate, in large measure to reduce grazing. There are few of these plants in freshwater environments, where calcification is generally more difficult and where long-term stable evolutionary pressure to develop calcification is not usually present. The Charophytes (Chara, Nitella) are prime examples, though even these plants are more characteristic of hard waters. Sinter or calcium deposits, primarily by blue-green algae in mineral and hot springs, probably are the direct result of pH effects rather than an adaptation for defense against grazing. Even in the marine environment where calcification can happen simply as a result of photosynthesis, relatively few major groups have developed calcification as a defense. However, where this has happened, primarily

in the red algal family Corallinaceae and related groups and the green order Siphonales (e.g. Halimeda, Udotea), the genera and species involved are quite widespread and ecologically very important. Skeleta of Halimeda are generally recognized to be the major contributor to tropical limestone structures such as atolls, and corallines are builders of large reefs (algal ridges). In general, even where they do not dominate, coralline algae are important contributors to coral reef structures and often extensively encrust shallow bottoms well into the Arctic and Antarctic. Particularly in ecological situations where urchins or fish grazers are highly abundant, corallines can develop bottom environments that are the equivalent of thorn scrub in sheep country. They are often called “coralline/urchin barrens,” even though the resulting porous coralline bottom is like a mini coral reef and can support very high biodiversity. The most obvious chemicals providing protection for terrestrial plants are the lignins and tannins that are present in many vascular plants. So important are these in the terrestrial environment that at least one author (Swain, 1979) has stated, “it seems doubtful whether plants, and hence life as we know it, could have developed on land without the acquisition of the ability to synthesize these two classes of phenolic compounds.” Lignins and tannins are also heavily involved in the protection of many marsh and wetland plants and lead to the great resistance to breakdown of marsh plants. Both are usually thought of as providing protection against fungal degradation. However, they also provide an amazingly effective general protection against animal herbivores. Tannins are so resistant to breakdown that they “wash out” to color bogs, swamps, some streams (black waters), and even coastal waters. In addition to providing a measure of direct protection from herbivores, lignin greatly increases the strength of woody plants, allowing them to “stand erect,” particularly in the nonaqueous environment. There is, however, another whole class of defense by plants against herbivores and even against parasites and other plants. These are direct chemical defenses. The chemicals themselves are called secondary compounds because generally no day-to-day metabolic use other than as poisons is known. A wide variety of chemicals are involved, including cyanide derivatives, alkaloids, and terpenoids. Most higher plants and many algae develop such protective toxic chemicals to varying degrees. Curiously, however, virtually every defensive toxin has led to detoxification mechanisms in some herbivores. Because all living organisms share the same basic chemistry, it is unlikely that a plant could develop an ultimate chemical defense against all herbivores. Although a few secondary compounds are deadly, most operate on a more subtle basis, reducing

Modifications of Marine and Freshwater Herbivores

an animal’s efficiency. It is more a matter of protection to a certain degree. The energetic and therefore growth or reproduction costs to a plant of significant amounts of secondary compounds are considerable and in the end are weighed, by natural selection, against percentage of reduction in grazing. Likewise, for a herbivore to develop a strategy to manage the effects of a toxin is costly. The evolutionary selection process sometimes leads to coevolution of a plant and a specific grazer. Secondary compounds have been identified in algae as well as in the flowering plants. It has also been demonstrated that the effects of these compounds, mostly terpenoids, on grazers can be lethal (Norris and Fenical, 1982). Plants rich in secondary compounds are avoided by grazers. In Chapter 21, we describe how a whole biogeographic region of rocky bottom has become characterized primarily by the relationship between a very abundant grazing sea urchin and a number of secondary compound protected and unprotected species. On the other hand, some grazers have come to tolerate the secondary compounds of algae. A few even concentrate these compounds for their own defense. Norris and Fenical (1985) discuss methods for isolation and identification of these mostly lipid-soluble chemicals. However, as we discuss below, in practice, in model ecosystem development and operation, each situation requires the adjustment of herbivore/plant relationships by the human operators. Theoretically, in the confines of small model ecosystems, secondary toxic compounds could provide serious problems to the general community. However, in our experience this has not been the case. The epiphytic and benthic dinoflagellate Gambierdiscus toxicus has been widely regarded as the source of a compound that, when concentrated in higher predators, gives rise to ciguatera, a form of severe fish food poisoning that affects the central nervous system of fish-eating humans and is common in the tropics. G. toxicus has been identified in at least one coral reef microcosm where only under certain conditions of heavy blue-green algal growth has the substrate for the dinoflagellate been present and fish distress occurred. In another case of a reef microcosm, damage to the toxic sea cucumber Stichopus nigricians caused some fish distress and death (see Chapter 20). However, of the many invertebrates known to be present, none was affected. Thus, the toxin was apparently specific to vertebrates. Littler et al. (as reported by Luning, 1990) have described fish kills in aquaria having the highly toxic brown alga Stypopodium zonale. However, we have introduced this species into complex reef models controlled by algal scrubbers many times, with no such losses. In general, given an active ecosystem, particularly one in which plants play their wild-equivalent roles,

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oxygen concentrations are high, and no unusual concentrations of toxic organisms are present, the effects of secondary compounds at the ecosystem level are not likely to be a problem in model systems.

MODIFICATIONS OF MARINE AND FRESHWATER HERBIVORES Herbivores become better adapted to their mode of feeding through a variety of morphological and physiological modifications. These adaptations allow them to forage for food more effectively in the face of plant defenses and the ever-present danger of predators. The modifications for herbivory are almost as numerous as the species involved. Nevertheless, there are types or guilds of herbivores that make understanding the process easier and below we examine several fairly welldefined types. Cellulose, in a variety of forms, is the major constituent of the cell walls of most plants including algae (Chapter 7). Cellulose itself, however, can be broken down or digested by animals only with difficulty and generally only with the help of microbes or protists. In most marine and aquatic plants, the very thick and lignified walls of woody plants are absent. Nevertheless, the walls of emergent marsh plants do possess lignin and break down very slowly. Even submerged aquatics and algae are difficult to digest compared to animal cells. Some herbivores make do by simply crushing the cells and digesting the cell contents. Others, like many land herbivores, have specially modified digestive tracts to allow for the activity of microbes in breaking down cellulose. In the marine environment, calcified surfaces laid down by algae or in which algae grow or bore provide the need for rasping or scraping mouthparts. Calcium carbonate itself provides no organic energy and is not chemically broken down further. However, when dissolved by digestive tract acidity, calcified structures provide calcium in solution, which can be useful for some metabolic processes as well as shell construction by the herbivore itself. In the following pages, we briefly describe several types of marine and freshwater herbivores to provide a general understanding of the difficulties they face and their adaptations to overcome those problems.

Parrotfish (Scarids) Parrotfish (Figure 15.2 and Color Plate 20) are full grazers in every sense of the word as it is applied to terrestrial mammals. They develop a strongly calcified beak of fused teeth that is used to scrape calcified algae and other calcified surfaces that have plants growing

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15. Herbivores

FIGURE 15.2 Jaws (f) and “teeth” (a–e) of the pharyngeal mill, grinding complex of a terminal male western Atlantic stoplight parrotfish, Sparisoma viride. After Gygi (1975). Reprinted with permission of Birkhäuser Verlag, AG.


in pores. Depending on the species and the location, some parrotfish also scrape coral. While to some degree this makes them carnivores, it must be remembered that coral is richly endowed with an algal symbiont (Chapter 19). Most parrotfish also browse to some extent, and some species spend much of their time in this mode of feeding. However, when this is the case, the plant involved is typically a tough seagrass or calcified alga. As with most marine and aquatic grazers, presented with the opportunity to capture small invertebrates, parrotfish will also take animal food. In addition to the obvious rasping/scraping apparatus, parrotfish also possess a pharyngeal mill consisting of internal molar-like teeth that are used to grind up the mixture of carbonate and algae or coral tissue delivered to it from the beak. The effectiveness of the beak/mill combination is such that parrotfish are one of the major degraders of reef hard structure as well as being important suppliers of the resultant fine carbonate silt. In a model system, without sufficient wave and current or settling traps that are the equivalent of lagoons, the supply of fine sediment defecated by parrotfish can be a serious problem for corals, which must expend considerable energy to constantly slough off the sediment. Many parrotfish also develop behavioral patterns that adapt them to a grazing mode of life in reef environments. Most species operate in schools and graze in roaming “herds.” The herds consist mostly of females and different-colored secondary males and have a hierarchical social structure that includes a dominant female and a single brightly colored terminal or “super male.” Social grazing tends to confuse and disperse territorial reef species like damselfish, allowing the parrots access to plants they would otherwise be denied. Likewise, as with a terrestrial herd, the schooling behavior makes predation by larger fish more difficult.

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FIGURE 15.3 Digestive tract of a tang, Acanthurus caeruleus. PH, pharynx; ES, esophagus; ST, stomoch (muscular gizzard); PY, pylorus; PYC, pyloric ceca; I, intestine; A, anus. After Breder and Clark (1947).

tangs. Tangs have unique tail spines for defense; hence the name surgeonfish. These remind one of the horns of some hoofed grazing animals, the spines of porcupines, and the tail spikes of some famous dinosaurs. Tangs, particularly when young, have a stringent requirement to feed almost continuously, undoubtedly because of a relatively poor utilization of their algal food (Thresher, 1980). While the long thin-walled intestine is probably well adapted to absorbing the cell contents of crushed cells, it is probably poorly suited to handling cellulose. This has considerable bearing on their survival in model ecosystems, since they must have an algal lawn and brush that allows almost continuous foraging. Also, given a small area previously occupied by other herbivore fishes, tangs may be kept in a corner to the point of starvation.

Tangs (Surgeonfishes)

Damselfish (Pomacentrids)

The Acanthurids, tangs or surgeonfish, are extremely abundant tropical and subtropical marine fish of a few genera and species (Color Plate 22). Along with parrotfish and damselfish, these animals are mostly herbivores, and together they form the largest part of the fish biomass of most reefs (Thresher, 1980). Tangs are browsers, with lips and dentition for snipping off the tips and branches of algae. They also have long thinwalled digestive tracts and some species have a sandfilled, muscular gizzard-like fore-intestine (Figure 15.3). These are all adaptations for foraging on relatively soft algal filaments and blades, though the thorough processing of cellulose seems unlikely. Like parrotfish, tangs are generally strongly schooling, at least as adults. Often they are part of mixed herds of parrotfish and

The pomacentrids fill a wide variety of environments in tropical waters. Some are planktivores (Chromis); others are small invertebrate eaters strongly associated with anenomies (clownfish). The majority, however, are benthic algal browsers (Color Plate 23) with the occasional small invertebrate added to their diet. What is especially interesting about damselfish is their very strong territoriality and an apparent “farming” behavior. Many damsels vigorously defend their territories against larger organisms, including scuba divers, but particularly tend to vent their ire on other grazers. They also clear or weed their “farms” of undesirable algae and other objects and have been described as killing off coral within their farms to create surfaces for algal growth.

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15. Herbivores

Damselfish are ideal animals for model ecosystems since they occupy small territories. However, their very strong territoriality can also make developing community structure in a small tank difficult. For larger microcosms and mesocosms, if one adds the damselfish of the community last, and does not crowd the system, there is usually no problem.

Headstanders (Abramites, Anastomus) The headstanders are voracious freshwater feeders of softer submerged aquatic plants such as Vallisneria, Potamogeton, and Egeria. An adult fish will quickly strip the latter to a bare stalk, leaving numerous floating fragments. Tougher plants, perhaps with some secondary compounds such as Echinodorus and Sagittaria, are usually left untouched. There are apparently no detailed anatomical data for the headstanders. However, one suspects that their primary adaptation to browsing lies in their mode of operation in the water, which is headstanding. Judging by their voraciousness and restriction to soft plants, it seems likely that a long gut, perhaps with numerous pyloric ceca to assist in digestion, is present. Properly handled, headstanders are excellent higher plant grazers in freshwater models. In a small tank one may have to add Elodea or Egeria to provide sufficient forage or to reduce predation on desired plant species.

Herbivorous Crab (Mithrax) Many crabs are herbivorous. The tropical western Atlantic, Caribbean king crab, Mithrax spinosissimus (Figure 15.4), is strongly adapted to herbivory, somewhere between grazing and browsing (Adey, 1989). This species, as well as the other members of the genus, provides an excellent example of a marine plant eater among the arthropods, having many special features that fit the animals for a grazing/browsing niche (Figure 15.5). The scooped and serrated tips of the chelae or claws of Mithrax are particularly well adapted to clipping off turf and small macroalgae as well as to pulling out larger macroalgae. Numerous mouthparts handle the algal food and present it to a set of cutting or clipping mandibles. Just inside the mouth is a large buccal cavity or forestomach that serves to store the roughage. At the back of the forestomach is a muscular gastric mill with well-developed molar-like teeth that serve to finely crush and grind the plant material, now thoroughly mixed with digestive enzymes. The forestomach acts as the equivalent of the rumen in a cow. Finally, although the intestine is relatively short and more or less straight, numerous digestive ceca exist at the beginning of the tract to provide a very large digestive volume.

FIGURE 15.4 Mithrax spinosissimus, a grazing/browsing crab from tropical western Atlantic waters. This large nocturnal crab (Caribbean king crab) occurs abundantly in deeper reef waters when large grazing surfaces and small-to-mid-size caverns are in close proximity.

Mithrax species, which are numerous and mostly smaller than the large M. spinosissimus, are excellent grazer candidates for the model ecosystem. Largely nocturnal, they tend to forage from a protective cave or crevice base. They also tend to have a harem-type social structure and a minimum territory as adults. Although these crabs have a swimming larval stage, it is short, and as long as nondestructive pumps are used, reproductive maintenance of populations is likely. Even though juveniles can be quite territorial, and in chance encounters one animal will often dismember and sometimes eat another, the numbers of individuals from a clutch of eggs is quite large. Adults will occasionally take animal food, disemboweling an urchin, for example, to get it. However, the majority of the food eaten is plant material (Adey, 1989).

Chitons (Polyplacophorans, Amphineura) Chitons are the quintessential grazers of algal turfs and crustose algae. Except in shell morphology, they have probably not evolved far from the ancestral molluscs (Yonge and Thompson, 1976). These “coat-of-mail” shells (Figure 15.6), with their eight calcareous plates and leathery girdle, often embedded with calcareous spines and small plates, are adapted to remaining on the grazing grounds. Their multiplate flexibility allows extraordinary adhesion to a rough substrate without loss of the protection provided by their shells against predators. Like many snails, the chitons feed with a scraping radula consisting of many rows of 17 teeth tipped with the iron


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FIGURE 15.5

Characteristic adaptations of Mithrax spinosissimus to the herbivorous mode of life. (A) Spoonshaped, serrated chelae for removing and clipping algae, especially algal turfs. (B) Mandibles (single of a pair) for clipping algae into short fragments, a cutting edge. (C) Centerline section of carapace showing digestive tract: large gastric mill, midgut (numerous ceca not shown), and hindgut. (D) Gastric mill ossicles (teeth) – center ossicle and one side shown. Drawings by Charlotte Johnson and Gustavo Hormiger. After Adey (1989).

mineral magnetite (Figure 15.6). The large esophagus has well-developed salivary glands and special starchdigesting “sugar glands.” The intestine is very long, filling much of the body cavity, as an adaptation to the requirements of plant digestion. Between the two intestines lies a special sphincter that forms the feces into pellets. Since the chiton must excrete into the semiclosed space created by adhesion of the animal to its substrate, the same space with gills and mouth, this probably provides an isolating disposal mechanism. Although the more advanced types of molluscs, such as many of the gastropods, can be voracious predators, many of the more primitive gastropods are grazers. Having an adult shell and body plan very different from the chitons, many snails have undergone a twisting process called torsion when very young (Brusca and Brusca, 2003). Nevertheless, many of these snails possess the same basic grazing adaptations (Figure 15.7).

Sea Urchins (Echinoderms) Like the chitons, but mostly grazing or browsing on larger algae (the seaweeds), a wide variety of echinoid

species are the principle grazers on rocky or reef bottoms from the tropics to Arctic waters. In many cases, echinoid grazers are keystone species, and without a higher predator will be the primary determiners of community structure. In Chapter 21, we discuss at some length the green sea urchin, Strongylocentrotus drobachiensis, and its role in structuring North Atlantic Subarctic rocky bottoms. We refer interested readers to that chapter.

Micrograzers Many small crustacea (especially amphipods and copepods) as well as polychaetes and nematodes are herbivores on algae. In fresh waters, larval midges of the family Chironomidae are particularly important algal grazers (Armitage et al., 1995). In this book, we refer to these animals as micrograzers, while other authors (e.g. Lobban and Harrison, 1994) prefer the term mesograzers on the assumption that the term micrograzers best applies to protozoan feeders of algal cells. Whatever the terminology, these small animals are capable of extensively removing algal turfs and other small algae. Whether they can significantly

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FIGURE 15.6 Feeding and digestive systems in algal turf and crust-eating chitons. (A,B) Diagrammatic views of radula action. (C) Longitudinal section through feeding area and foregut of a chiton. (D) Bottom view of chiton. (E) Dorsal view of entire digestive tract of Lepidochiton cinera. All after Barnes (1980).

reduce the primary productivity of a community or not depends on other factors, particularly the abundance of predators. In utilizing an algal scrubber for water quality control in modeling, care has to be taken to harvest more or less frequently, depending on the circumstances, to avoid losing the primary control mechanism to large, tougher, and less productive algae.

Omnivores Anyone who has spent time under water observing benthic habitats, or more easily, similarly observing organism activity on the surface of coral or rock substrate in a model ecosystem, is well aware that most algal (or macrophyte) grazers will ingest small animals routinely. However, there are numerous true omnivores

(including humans) that will switch from a typical plant food source to an animal when possible. As described by Eubanks (2005), this changes the whole relationship between predator and prey in many ways and further complicates food webs. The 21st century has brought an enormous change of viewpoint in the home aquarium hobby with regard to the role of algae and their grazers in coral reef aquaria. From a general practice in the earlier 1970s of low light and no algae (except the blue-greens that had to be fought continuously) to books especially on algae (Sprung, 2002) and finally to sections in aquarium books on grazers and their relationship to algae (Calfo and Fenner, 2003) there is a major change that is extremely important in the context of public understanding of ecological science.

Herbivores and Model Ecosystems


HERBIVORES AND MODEL ECOSYSTEMS In a properly designed model ecosystem where direct physical/chemical parameters are operating as in the wild and sufficient species diversity over a broad trophic range is present, a balance of herbivores and plants is the key element to long-term stability. This is particularly true as model size gets smaller and becomes critical at aquarium dimensions. Unless one is working on a specific analog model that is poor in plants and primary production, the maximizing of plant productivity in the model is often the key to model veracity. This is the case for most microcosms and aquaria. First one determines that there is sufficient light (Chapter 5) and water motion (Chapter 2). Then the objective becomes the maximizing of plant surface and the reduction of grazing to the level where grazable plant production roughly equals that used. Since there is much room for imbalance, it is important to have a reasonable amount of plant biomass that is defended by a tough skeleton or chemicals. The productivity of the grazable plant material that remains is then what one will balance against utilization. Algal turfs that support heavy grazing can be very important in this respect. However, in small artificial systems, particularly those in which

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large, abundant, or voracious herbivores have been placed, it may be necessary to populate the tank largely with inedible plants and artificially feed the browsers with added plant material at the desired level. This added plant material must then be balanced by scrubbed algae (Chapter 11) or some other form of export. Another approach is to establish refugia, as part of the overall system, from which larger grazers are excluded. Equally important in this process is the distribution of grazing types so that all types of vegetation can be utilized, assuming enough surface is present to fully support the grazer biomass. Usually this is not a severe problem in mesocosms where one gradually adds grazers after the vegetation is established. It can become considerably more difficult in systems of smaller dimensions. One particular problem that needs careful observation is that of stocking with young grazers. Young animals generally withstand transport and reestablish better than adults. Thus, they are often used in the establishment of new systems. However, if the grazer and browser biomass increases considerably with time, particularly in the absence of higher predators, a well-balanced young ecosystem can become heavily overgrazed at maturity. In some moderate to small-sized model ecosystems, grazing is easily balanced against plant productivity. However, the system is not large enough to support higher predators that will keep grazer reproduction in check. This situation, often encountered with snails in both fresh and salt water, requires the operator to assume the role of the higher predator in periodically cropping the grazers. Another situation often encountered in the refugia of both fresh and saltwater models is where micrograzers (mostly amphipods or chironomids) totally consume the smaller filamentous algae, the most productive elements of the ecosystems. This rarely happens in a primary system because of the presence of many fish predators of small invertebrates but may be a problem in a refugium free from larger organisms. The insertion of a small wrasse will usually solve this problem, though to some extent this defeats the purpose of the refugium. Ideally every ecosystem model would have a series of refugia, each treated a little differently to provide a refuge for a different component, and thereby simulating a larger area. Although normally spatially separated from the model ecosystem itself, algal turf scrubbers, both fresh and salt water, can also suffer from an explosion of micrograzers (see Chapter 11). In fresh water, these grazers are usually the larvae of midges (the chironomids), though in enclosed systems not open to the flying adults, this is not a problem. In marine systems, the

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FIGURE 15.7 Feeding regions, radula, and digestive tracts of primitive, herbivorous gastropods. Note in (B) the large cecum in which much digestion takes place as well as the process of pellet formation at the end of the tract. After Barnes (1980).

References

problem is usually herbivorous amphipods. This kind of overgrazing is generally easy to solve by simply cleaning the scrubber walls when the screens are scraped. If the problem extends to auxiliary tanks or settling traps, a wrasse (or bluegill in fresh water) will quickly reduce the problem.

Ecosystem Restoration In wild ecosystems affected by human activity, disruption of plant growth, trophic structure, including grazers, or both, is likely. However, it is often the difficult task of the restoration ecologist to determine the level of importance of the various factors in order to devise a path to restoration. As we describe in Chapter 21, the issues can be quite complex, and this may only be a guess; however, the use of test model ecosystems, as well as field manipulations can be very valuable in this respect.

References Adey, W. (Ed.) (1989) The Biology, Ecology and Mariculture of Mithrax spinosissimus Using Cultured Algal Turfs. Mariculture Institute, Washington, DC. Adey, W. and Hackney, J. (1989) Harvest production of coral reef algal turfs. In: The Biology, Ecology, and Mariculture of Mithrax spinosissimus Using Cultured Algal Turfs. W. Adey (Ed.). Mariculture Institute, Washington, DC. Armitage, P., Cranston, P., and Pinder, L. (1995) The Chironomidae: The Biology and Ecology of Non-Biting Midges. Chapman and Hall, London. Barnes, R. (1980) Invertebrate Zoology. Saunders College, Philadelphia. Breder, C. and Clark, E. (1947) A contribution to the visceral anatomy, development and relationships of the Plectognathi. Bull. Am. Mus. Nat. Hist. 88: 291–319. Brusca, R. and Brusca, G. (2003) Invertebrates, 2nd edn. Sinauer Associates, Inc., Sunderland. Calfo, A. and Fenner, R. (2003) Reef invertebrates, and essential guide to selection, care and compatibility. In: Reading Trees and Wet Web Media Publs. Monroeville, Pennsylvania.

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Chase, A. (1987) Playing God in Yellowstone National Park. Harcourt Brace Jovanovich, San Diego, California. Crawley, M. (1983) Herbivory: The Dynamics of Animal–Plant Interactions. University of California Press, Berkeley, California. Eubanks, M. (2005) Predaceous herbivores and herbivorous omnivores: the biology of omnivores and the ecology of omnivore–prey interactions. In: Ecology of Predator–Prey Interactions. P. Barbosa and I. Castellanos (Eds). Oxford University Press, Oxford. Gygi, R. (1975) Sparisoma viride (Bonnaterre). The stoplight parrotfish, a major sediment producer on the coral reefs of Bermuda. Eclogue Geol. Helv. 68: 327–359. Hackney, J., Carpenter, R., and Adey, W. (1989) Characteristic adaptations to grazing algal turfs on a Caribbean coral reef. Phycologia 28: 109–119. Lobban, C. and Harrison P. (1994) Seaweed Ecology and Physiology. Cambridge University Press, Cambridge. Luning, K. (1990) Seaweeds, Their Environment, Biogeography and Ecophysiology. Wiley-Interscience, New York. Norris, J. and Fenical, W. (1982) Chemical defense in tropical marine algae. Smithsonian Contrib. Mar. Sci. 12: 417–431. Norris, J. and Fenical, W. (1985) Natural products chemistry: uses in ecology and systematics. In: Handbook of Phycological Methods. Vol. 4. Ecological Field Methods. M. Littler and D. Littler (Eds). Cambridge University Press, Cambridge. Owen, D. (1980) How plants may benefit from the animals that eat them. Oikos 35: 230–235. Owen, J. (1980) Feeding Strategy. Oxford University Press, Oxford. Parsons, K. and de La Cruz, A. (1980) Energy flow and grazing behavior of canocephaline grasshoppers in a Juncus roemerianus marsh. Ecology 61: 1045–1050. Power, M., Matthews, W., and Stewart, A. (1985) Grazing minnows, piscivorous bass, and stream algae: dynamics of a strong interaction. Ecology 66: 1448–1456. Sprung, J. (2002) Algae, a Problem Solver Guide. Ricordea Publishing. Coconut Grove, Florida. Swain, T. (1979) Tannins and lignins. In: Herbivores, Their Interaction with Secondary Plant Metabolites. G. Rosenthal and D. Janzen (Eds). Academic Press, New York. Thresher, R. (1980) Reef Fish. Behavior and Ecology in the Reef and in the Aquarium. Palmetto Publishing, St. Petersburg, Florida. Yonge, C. and Thompson, T. (1976) Living Marine Molluscs. Collins, London.


C H A P T E R

16 Carnivores Predators of Animals

Predators and parasites, differing primarily in their size, are organisms that humans perceive with fear or loathing. However, once energy has been captured, from the sun, and is stored as chemical energy, it becomes valuable to living organisms that need energy to survive. Indeed, as omnivores, we are predators on both plants and other animals ourselves. Any organic material is a potential food or energy source for a living organism. Animal flesh in general is easily digestible, provides a balance of needed compounds and elements, and is a rich source of energy. It seems likely that 3–4 billion years ago, as soon as the earliest bacteria developed the ability to utilize a nonorganic energy source, a line of evolving offspring became predatory on these primary producers. Likewise, it seems clear that there are very strong selection pressures that lead most evolving lines of organisms to produce some members that are predatory on other living organisms. To most people, the word predator brings to mind a voracious, fast, and large-clawed and fanged lion or tiger on land and a sharp-toothed shark or piranha in the water. However, the range of predators is enormous and includes tiny protozoans that feed on bacteria and other protozoans as well as the sponge that gently filters plankton from the water column. There are even a few plants, such as the Venus flytrap, that are predators of animals, and many plants are predators (i.e. parasites) of other plants. Most animals predatory on plants are called herbivores, and those were treated separately in Chapter 15. In this book, because they are so different from carnivores when handled in model ecosystems, plankton predators, parasites, and predators that are also partly symbiotic with algae are treated in separate chapters (17 and 19). Even so, the range of predator structure

and ancestry as well as how they are handled in model ecosystems is enormous. The first thought of the aquarist when asked about predators is that they are difficult to handle in the model ecosystem because of its relatively small size and need for a large foraging territory. Indeed, a barracuda would normally patrol several thousand square meters or more of coral reef, making inclusion in a model system without supplementary feeding virtually impossible. On the other hand, many voracious predators exist among the protozoa, and these little protists can be easily present in the smallest of ecosystem models. Also, the majority of fish, fresh and salt water, that are handled in the aquarium trade are mid-level predators normally feeding on insects in fresh water and small crustacea, worms, and other invertebrates in salt water. In the balanced aquarium or model ecosystem, the average predator might be a little more difficult to accommodate to the small ecosystem dimensions than the average herbivore, but in practice animal size is the most crucial factor. In this chapter, we first briefly discuss some general characteristics of predators that will perhaps help with the concept of handling these organisms in models. We then discuss a range of the types of predators that occur in marine and freshwater environments. Finally, we try to impart some of our experience in dealing with predators in actual model systems.

THE CARNIVORE PREDATOR Herbivores generally greatly outnumber carnivores in terms of individuals and biomass (Owen, 1980). On the other hand, carnivores occur in a wider variety of forms (species). This is partly because each herbivore is

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subject to more than one form of predation. However, “everybody is eaten by somebody,” and a tremendous complexity is generated in any food web by predators feeding on other predators. There are general patterns of operation that characterize most predation. These can be reduced to finding, catching, and eating. Predators either inherit the recognition of or quickly learn to visit the right kind of environment in which their prey are likely to be. Once in the vicinity of appropriate living food, a wide variety of sensory apparatus, some highly specialized, is used to pinpoint the prey for capture. Smell or other chemical sensing, visual sharpness, and the utilization of sound or electrical signals are the typical tools of the hunter. Each species hones these down to the particular combination that works. Once located, the prey must be caught and secured. This step provides a tremendous range of adaptations for evolutionary success that include ambush, stealth, attraction, traps, special weapons (chemical, electrical, or physical), speed, and strength. The killing and/ or holding step has its own set of weapons, whether teeth, claws, venom, or pure muscular ability. In general, the last step, eating, is typically the least difficult for the predator. Nevertheless, even here some organisms have had to develop special methods for avoiding toxic parts or wholes and even for the more mundane separation of inedible bones, scales, and feathers. In the competitive evolutionary race in which not only other organisms but also sometimes difficult environmental conditions are present, each predatory individual becomes “a computer with a program” that analyzes the availability, palatability, accessibility, and profitability of its prey. Energy and time cannot be continually expended in hunting without a food return that not only allows compensation of the energy expended in the hunting itself but also allows enough excess food for reproduction, migration, and the ability to ward off other predators and parasites. The problems and choices faced by organisms can be analyzed mathematically. For example, an interesting analysis of the feeding/ predation options of a bluegill is discussed by Stephens and Krebs (1986). Because of the necessity for a predator to optimize its predatory actions, it is often the sick, the old, the injured, and the young of its chosen species that are preyed on first and most successfully. Predators can be highly specialized to feed on a single species, in some cases even to a single phase in the life cycle of a single species. While such specialization usually increases the rate of success of the individual predator, it is often an evolutionary dead end. If the environment changes and the prey is greatly reduced in numbers, extinction of the predator may be the net result. Prey populations fluctuate often due to weather and disease and to their source of food. To a large extent

the highly specialized predator is doomed to follow with its own population fluctuations. Population cycles are inevitable features of food webs (Berryman, 2002), and as we describe in Chapters 20–23, are also features of high veracity models. Top predators can be “keystone species” and often play a major role in structuring ecosystems and in maintaining biodiversity. Yet, these species are often the first to be lost as a result of anthropogenic disturbance of an ecosystem. In modeling, the full time existence of a large predator is often not possible, and in several places in this book, we discuss how to simulate top predators. Whether modeling or restoring an ecosystem (and bringing the top predators back), the role of the predator needs to be understood (Gittleman and Gompper, 2005).

THE PREY Animal prey are rarely greatly diminished by a predator. Great reduction could mean disaster for predator and prey alike. Such prey usually have an enormous range of defenses, including defensive behavior, defensive organs, and the chemicals they produce, social support, and camouflage or mimicry. The relationship between predators and prey has been called a “gigantic biological chess game” (Whitfield, 1978). As described by Edmunds (1974), the elements of prey defense consist of avoidance (primary defense) followed by a variety of direct active and inactive measures (secondary defense) when simply staying hidden fails. Many animals stay out of sight within a substrate, reef rock, or muddy bottom, for example. A whole host of worms, crustaceans, molluscs (and insects in fresh water) utilize this mode. An examination of the hundreds or even thousands of individuals of these animals that can be sieved from a square-meter grab of muddy bottom shows how effective this strategy is. Nevertheless, organisms as different as fish (such as grunts) and certain diving ducks simply scoop up mouthfuls of this bottom, sieving out the animals hiding therein. Also, there are predators within their midst. Annelid worms (e.g. Nereids) are a characteristic feature of the fauna of muddy coastal bottoms; these polychaetes have large pincers adapted for harvesting their mud-dwelling mates. Other organisms remain above the bottom but rely on a wide variety of camouflage. Many flatfish, for example, not only look like the bottom they are lying on, but change colors from place to place as required. Other fish and invertebrates use a military type of camouflage to break up the outline that would identify the organism to a predator. Finally, decorator crabs take the

Marine and Freshwater Predators

most direct and effective route of “gluing” algae to their carapace to provide a living, traveling plant cover. The most obvious defenses are sharp spines, sometimes poisonous, such as the long-spined sea urchin (Diadema) or the easily recognizable and potent sting of Millepora (the fire coral). Finally, there are numerous indirect defensive mechanisms, for example those that mimic a dangerous organism such as the “big eye” on the butterfly fish. Once identified, the prey usually still has more active options of defense. While there is a myriad of forms of protection from predation, we note just a few here. Many fish and even clams survive by lightning-fast movement. Razor clams are famous in this respect. A more obvious and seemingly impenetrable method is to build a rockhard shell of calcium carbonate or chitin. Many molluscs and snails have taken this route. However, as with most forms of defense, in spite of the hard shell, many animals (e.g. boring snails and straddling starfish with extensible stomachs) have circumvented this means of protection. Sea gulls take advantage of their flight capabilities and lift clams and snails to a height from which they will break open when dropped on a hard surface. Indeed, the birds soon develop a sense of the minimum height needed for breakage so as to avoid excess energy expenditure. A defense method common among fish and similar to many grazing land animals is schooling behavior. Large numbers of fish swimming in formation can confuse a larger predator, and while some members of the school are lost to the predators, as a whole the method is quite effective (Krause and Ruxton, 2002). Human netting counter behavior is often devastating to schooling and a principal factor in overfishing. Associations of animals, anenomes growing on hermit crab shells, for example, provide an even more complex method of defense that can provide considerable protection. Crabs demonstrate how many modes of defense can be utilized. These animals have several defensive tactics against fish. The chitinous shell and often numerous spines are obvious in their protective effects. However, many crabs take a very aggressive “attack” stance and with their sharp or crushing chelae can severely damage a striking fish. In addition, crabs can autotomize appendages, leaving a leg to the predator while the animal escapes. The leg can usually be grown back after several molts. The defense of releasing camouflage “ink” into the water column is well known for the octopus in the marine environment. Less well known is the behavior of nymphs of the stonefly Pteronarcys in fresh water. In responding to attack by a crayfish, the nymph autohemorrhages, bleeding so extensively that the crayfishes sensory appendages become covered with a viscous

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film, causing it to drop the insect and retreat (Williams and Feltmate, 1992). Finally, a form of defense particularly characteristic of plants and colonial animals, but occurring virtually everywhere in the animal world, is that of toxic compounds. Sometimes the transfer of the toxins is accomplished by a sting, the injection of some cone shells being fatal to fish and potentially even fatal to humans. Other groups, algae, gorgonians, and some sponges, for example, possess toxic or distasteful chemicals throughout the animal body. Thus, the toxin is transferred only if and when the animal is eaten. Even in this case, angelfish, for example, typically eat toxic sponges, and gorgonions are subject to predation by specialized snails (Cyphoma). Thus, as mentioned earlier, predation evolutionarily often develops into an “arms race.” As prey develop defenses by natural selection, the predators slowly evolve strategies to circumvent the defenses.

THE DYNAMICS OF PREDATION A considerable amount of research has been devoted to understanding the complex dynamics of predator– prey interactions; this was collated in a review by Michael Crawley (1992) and then updated by Lima (2002). We now better understand the cost–benefit tradeoffs. For example, researchers now refer to the value of increased food resources compared to the danger from larger predators that obtaining such resources occasions: for example, the difficulties of a crab opening a given-sized bivalve for the food benefit to be derived from the mass of meat inside. Optimal foraging and the concepts of the continual coevolution that the arms race between predator and prey often occasions are extremely complex subjects when placed in the context of a real ecosystem rather than an extremely simplified computer model. It is now recognized that hardly ever can the on-going status of predator–prey interaction be simply described as the result of the meeting of two individuals or even two populations. The roles of environmental factors (temperature, wave action, precipitation, etc.) and incidently related populations of plants and animals are usually critical. This is a field of natural science for which the microcosm/mesocosm approach, with its ability to provide much higher levels of biotic complexity within a framework of easily controlled environmental parameters, could be extremely productive.

MARINE AND FRESHWATER PREDATORS In this section we briefly discuss a selection of predatory animals. There are thousands of modifications that

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allow organisms to be successful predators; we discuss only a few. Examples that are likely to be present or that could be used in a model ecosystem are given.

Micropredators As we have discussed, protozoa, or protists if the algal divisions are included, are now recognized as having developed many times on different branches of organic evolution. In this text for simplicity we continue to lump them as protozoa, including all those single-cell adaptations to all of the complex activities embodied in multicellular plants and animals. Some biologists call them acellular since all functions are accomplished by a single unit rather than by aggregations of specialized units as in the cellular organisms. The protozoan has numerous organelles rather than organs to accomplish all the complex needs of life including motion, food capture, digestion, and reproduction. Virtually every known type of plant and animal activity is also carried out by protozoans at the microscale. There are plants, grazers, decomposers, planktivores, and, of course, predators. What is particularly interesting in the context of this book is that these predators, some quite voracious, are tens of micrometers to at the most a few millimeters in longest dimension. Rarely would they be limited by the size of the model ecosystem and indeed they might be quite at home in a liter-sized microcosm. Figure 16.1 shows two of these micropredators. Since the Peranema is eating a Euglena, which some biologists would call a plant, perhaps it should be termed a herbivore. However, Euglena has a flagellum and is motile. Thus, it seems more appropriate to regard this situation as carnivory. The rod organ at the anterior end of the Peranema functions as both a proboscis and a hook. Once the Peranema has oriented for the attack, the rod organ snaps into the prey and is used either to “suck out” the cell contents of the prey or to pull the prey into a developing in-pocketing, which eventually becomes a large food vacuole. Suctorians are rather specialized protozoa that are normally sedentary, being motile only in reproductive or sporulation states. Figure 16.2 shows the suctorian mode of predation, which is similar to that seen in many coelenterates on a larger scale. The spines or tentacles have organelles (haptocysts), which apparently bear a potent toxin. When prey protozoa contact the tentacle, the haptocysts inject the poison into the prey cell, immediately causing immobilization. Then the tentacle becomes a tube or proboscis, which is capable of sucking up the cell contents of the captured organism.

FIGURE 16.1 The protozoan Peranema “swallowing” a captured Euglena, a photosynthetic flagellate. After Barnes (1980). Reproduced by permission of Saunders College Publishing.

A Worm Predator – The Bloodworm Glycera, the bloodworm, is a common intertidal or subtidal marine polychaete worm. Often sought out as fish bait by worm diggers, it provides an important bait industry in some areas. Glycera possess four sharp jaws in an extendable proboscis (Figure 16.3). The jaws in themselves are potent armament, but they also inject a poison as strong as a bee sting. The animal forms a series of burrows from which it lies in wait for the numerous primarily detritivorous worms and small crustaceans that are common in its rich mud habitat. Glycera, along with its worm and crustacean prey, is also sought out by numerous mud-browsing fish and crabs. While it is thus a potent mid-scale predator, it is also prey for many larger predators. Since in some localities digging for bloodworms has become a major industry, obviously the hiding defenses of the bloodworm were quite adequate. On the other hand, human’s ever more voracious appetite for the worms as bait and their digging and hunting capabilities could lead to “overfishing.” As long as the process is not extended subtidally with more efficient mechanized apparatus driven by fossil fuels, and broad areas of estuarine and coastal habitat


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FIGURE 16. 2 Suctorian weapons of immobilization and capture and mode of feeding. (A) Acineta; (B) suctorian tentacle showing haptocyst armament and means of sucking up the cell contents of its prey; (C) disc-like Heliophyra capturing and ingesting Paramecium. After Barnes (1980).

do not become polluted, bloodworm populations are likely to be maintained in the subtidal region.

A Poisonous Predator Of the two major groups of molluscs, one tends to think of the clams as being filter feeders and the snails, with their rasping radulae, as grazers of algae and other plants. While the clams are not far removed from the stereotype, with some being deposit feeders and virtually no predators (except for a few parasites), the snails or gastropods are far more varied. Indeed, many snails,

such as Buccinum (Figure 16.4A) and Busycon, are rather voracious predators on their relatives, the clams. In some of these cases, the snail radula is modified as an organ for rasping a hole in the clam shell. However, there is one family of snails that can be regarded as very highlevel predators. Theoretically, some species of the family might be predators, even at times killers, of humans. Such snails are often beautiful cone shells (Figure 16.5) (Yonge and Thompson, 1976). The family Conidae has about 500 species, most of which prey on polychaete worms and other snails. A few, however, in spite of their quite characteristic “snail’s

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FIGURE 16.3 (A) The bloodworm, Glycera americana; (B) head region with retracted proboscis; (C) extended proboscis showing four jaws with their poison glands. (A) After Gosner, (1978); copyright © 1978 by Kenneth L. Gosner. Reprinted by permission of Houghton Mifflin Company. All rights reserved. (B,C) After Barnes (1980).

FIGURE 16.4 Methods of predation of some gastropods. (A) Buccinum prying open a cockle shell; (B) cowie feeding on tunicates. After Barnes (1980).

pace,” are predators of fish. The catching of fish is accomplished with a rapidly extensible proboscis armed with poison barbs. While the barbs are modifications of the radula teeth of the other snails, members of this family

also possess poison glands and ducts as well as a sac in which to bathe the poison darts. After paralyzing and killing small fish, the snail’s proboscis, remaining extended, can engulf and partially digest the fish. Thus


273

FIGURE 16.5 Feeding structures of cones. (A) Pharynx, mouth, and poison apparatus of Conus striatus; (B) cone swallowing a paralyzed fish. After Barnes (1980).

armed, the “lowly” snail becomes in turn a predator on some of the more advanced predators of the sea.

Top Invertebrate Predators Molluscs as a whole are very slow if not virtually sedentary. As we have discussed, even the highly predaceous and sometimes dangerous cone shell is adapted to catching motile prey by its evolution of poison barbs. The cephalopods, particularly the squids, however, show many of the features that characterize aquatic and marine vertebrate evolution. The cuttlefish and squids, with their streamlined bodies, a combination of lateral fins and a jet-propulsion funnel, and a highly developed nervous

system known for its giant axon nerve cells, are particularly adapted for rapid mid-water propulsion. Also, their eight tentacles and double-suckered arms and, most of all, their highly developed image-forming eyes render them formidable predators (Figure 16.6). Indeed, the giant squids are nearly the equals of the top predators in the sea, the sperm whales. Once prey is captured by squids and cuttlefish, as if their expertise at stalking, pursuit, and capture were not enough, they have powerful and razor-sharp beaks finally capped by a paralyzing toxin to reduce energy-draining prey struggle. Recognizing the “eat and be eaten” status of even highly adapted predators, cuttlefish and squids also have a uniquely variable and complex ability to change skin

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FIGURE 16.6 Primary hunting characteristics of squids and cuttlefish. (A) The cuttlefish Sepia capturing a shrimp; (B) basic body plan of the squid Loligo; (C) diagrammatic view of the “jet propulsion” and ventilating system of a cuttlefish. After Barnes (1980). Reproduced by permission of Saunders College Publishing.

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colors and pattern for disruptive displays and mimicry. Finally, unique in the entire animal kingdom, along with their closer cephalopod cousins, these super-invertebrates possess camouflaging smoke screens in the form of their “ink.” In the world of predators, we must truly reach the vertebrates to see even marginal improvements in the archetypic characteristics of the cephalopod predator. It is among the reptiles and mammals that the top carnivores of watery environments are to be found. However, since realistically these are not the common top predators in synthetic ecosystems, at least not in microcosms and aquaria, we finish our brief discussion with two fish.

A Lower Level Fish Predator The evolution in the more primitive chordates and early vertebrates of the muscular-ensheathed notochord and eventually vertebrae led to a bilaterally symmetrical, head–tail body plan that is ideal for rapid movement through water. Finally, with a brain and spinal cord forming a well-developed central nervous system, image-forming eyes, and a wide variety of sensory apparatus including the lateral line “sonar system,” it is hard to improve on the basic construction of fish for a watery predaceous life (Bond, 1979). This has obviously been elaborated on, evolutionarily, in a tremendous variety of ways (Migdalski and Fichter, 1976). Although a wide variety of possibilities exist, for this very brief discussion with synthetic ecosystems and aquaria in mind, we choose the family Poecilidae. These fish include the mollies, swordtails, guppies, and mosquito fish. Poecilids have relatively recently evolved in fresh waters of the tropical to temperate Americas, and because of their use in the aquarium trade and their abilities as eaters of mosquitoes, some have become virtually worldwide in distribution. These small fish are capable of withstanding a wide range of environmental conditions, even high salinities, making them highly adaptable to wet–dry season regimes in which water bodies dry down to virtual puddles. Many can also move into estuaries and take advantage of the hunting territory offered by enormous marsh-mangrove areas that may be flooded only on spring tides. The poecilids are live-bearing, thus circumventing the free-egg mass and planktonic larval stages, which would likely be less successful in semi-ephemeral, small water bodies. A glance at any poecilid shows the primary trophic adaptation of these fish: their mouths have evolved to make them particularly effective at surface feeding. While their highly generalized characteristics also suggest animals capable of feeding on almost anything organic including algae, they are especially adapted to feeding surface-floating or alighting insects. An enormous food

source is potentially available in the form of filterfeeding mosquito larvae. Indeed, it is these fishes and their cousins the killifishes that perform a major part of mosquito control. In some areas of the world marshes were drained to reduce mosquitoes. Since that method was not particularly successful, a more modern approach is to build ditches not for draining but to allow fish such as poecilids and killifish access. It is usually only in stagnant waters inaccessible to these fish that mosquitoes do exceptionally well. As we discuss later, we have had great difficulty in achieving even a low level of mosquito production in our Everglades mesocosm, in part because it was designed such that the mollies and killifish have access to every part of the system, at least at high spring tides and seasonal high waters.

A Top Predator Finally we come to the archetype top-level aquatic predators, which are without doubt the most difficult problem for synthetic systems. We have chosen to discuss the barracuda. For a variety of reasons these streamlined fish work to a degree in a relatively small system. The barracuda in the tropical coral reef environment is generally similar in design to the pickerel or pike in fresh waters. Adapted for quiet cruising or lying in wait for most of the time, its elongate highly muscular body is capable of lightning strikes at other fish. Most important, its dentation is unmistakable. Long, razorsharp teeth slightly inclined inward prevent the escape of larger fish once they are caught. Smaller or elongate fish are often cut in two on the first pass, the pieces then retrieved at leisure. Like many top predators, marine or terrestrial, these fish particularly hone in on weak or struggling prey. Since it would be an unusually large mesocosm that could truly support such fish beyond the juvenile stage, this characteristic can be used for artificial support, as we discuss below.

PREDATORS AND SYNTHETIC ECOSYSTEMS We have placed all animals from the upper levels of food webs under the general heading of “carnivores.” It is likely that the higher they rank the more likely it is that they will pose an increasingly broad range of difficulties for managers of aquaria or microcosm ecosystems. However, while we lump all free-living, nonplanktonic or detritivorous animal-eating vertebrates and invertebrates in this category, it is necessary to remember that size is at least as important as mode of nutrition. A carnivorous amoeba, worm, or copepod, or even a tetrafish, is unlikely to create serious problems in a model ecosystem, but a large grazing fish, as we noted in Chapter 15,

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requires considerable foraging territory. In many ways it is more important to prevent overgrazing than overpredation. Not only is excess carnivory more apparent and more easily guarded against, but it also does not directly damage the energy supply of the system. As we have stressed repeatedly, these are primarily scaling problems due to limited microcosm size. Top carnivores are few and they usually forage over a relatively large territory. It is possible to reduce this territorial difficulty in models somewhat by using younger members of a species with reduced food size requirements as compared to the adults. On the other hand, young animals may require a larger total mass of food to support more rapid growth. Another approach is to introduce special feeding stocks to simulate a larger foraging territory for the particular species in question. Selected carnivores of different sizes and positions in the food webs of the Smithsonian coral reef and Maine coast microcosms are shown in Figures 16.7 and 16.8. The food webs are shown in Figures 13.7 and 13.8. Among the mid-level carnivores in the reef systems we have developed are fish, such as grunts, wrasses, butterflies, squirrels, and angels (Color Plate 24), and invertebrates such as various worms, lobsters, and predatory snails (Color Plate 19). Although some of these organisms feed on the reproductive stages of a variety of small animals, most feed on small- to moderate-sized grazers, filter feeders, or detritivores. As long as the model is not overloaded with low-level carnivores and sufficient primary production, particularly algal growth, is present, little difficulty can be expected. However, we note two special cases created by the typically nocturnal migratory habits of grunts and lobsters; both frequently migrate into associated reef lagoons to feed. Depending on the number of these animals, a large amount of lagoon or equivalent territory can be necessary for foraging. In some of our reef tanks we were able to supply a lagoon area that was about half the size of the reef itself, and this worked quite well. Another approach, that of providing artificial nighttime feeding (see Chapter 20), requires sufficient algal turf scrubbers (ATS) or other equivalent methods of export of nutrients. It is possible to estimate animal biomass at different trophic levels in natural reefs and to use these data to adjust the number of lower carnivores in a reef microcosm. In practice, however, both the natural reef estimate and the microcosm measurement are difficult to make. Generally it is possible to determine whether sufficient food is present at this level simply by looking at the external physical appearance of the fish. In some cases involving daytime feeding of mid-level predators such as butterflies and angels, food availability on a reef is primarily determined by filter feeders such as sponges,

worms, and corals. We have rarely experienced problems with these groups, perhaps because reproduction in a large number of invertebrates and algae is continuously supplying small planktonic stages. In some cases we have artificially maintained plankton levels in our reef microcosms and treated this as ocean import. This is discussed further in Chapter 17. Higher-level carnivores in our reef systems have included barracuda and snappers. These high-speed pouncers rely entirely on smaller fish and, except for the smallest sizes, require a larger foraging area than is likely to be available in the small to moderate-sized microcosm. Left to their own devices, these fish will soon deplete a tank of all but the largest fish. A continuous supply of small reef fish added to a reef microcosm can make up for losses to these higher-level carnivores. This is likely to be overly expensive and inconvenient. We have found that goldfish, which are cheap or easily raised, not only provide adequate feeding for barracuda but also get eaten first because of their immediate distress upon entering sea water. Thus, although reef fish occasionally are lost to a barracuda, as in the natural environment, the problem is not serious. Snappers, on the other hand, tend to be voracious and to tackle any other residents from their own size downward. They make poor higher predators for a relatively small system. The basic conclusion from this discussion is that there is no fixed formula for dealing with upper-level carnivores; the size of the model, the nature of the ecosystem, and the behavior of the available higher predators, all have to be considered. When supplementary feeding is used for higher carnivores, an equivalent export can be achieved with ATS. As long as the size and mode of operation of the scrubber is matched to the load, the overall result in water quality should not be too different from that on a wild reef. On most wild, shallow-water reefs, flow from the open ocean constantly supplies juvenile fish ready to drop from the plankton. Most of these juveniles are eaten immediately. Also, scrubber action in the model is a simulation of the inefficient grazing of algal turfs in the wild, which results in a constant loss of algal fragments from the reef. These kinds of exchanges at moderate levels probably make little difference, either in the appearance of a model ecosystem or in its biological function. In the end, while the principles can be “stretched” using algal scrubbers if ecosystem simulation is desired, community scaling is the primary problem. Either microcosm size must be relatively large, or mid-level carnivore number and higher carnivore size must be kept to a minimum, in keeping with the natural situation in the wild. The cold-water, rocky-benthic ecosystem of the Maine coast (Chapter 21) is considerably less complex than a

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FIGURE 16.7 Selected carnivores in the food web of the Smithsonian coral reef microcosm (see Chapter 20). Drawing by Alice Jane Lippson.

reef ecosystem. It is younger (evolutionarily), and therefore has had less time to develop diversity and trophic complexity, and, in the case of the North Atlantic Subarctic Boreal, is rather depauperate due to its pattern of biogeographic development with time. We have kept a number of medium-size carnivores in our cold-water systems, including Cancer irroratus,

the rock crab; Carcinus maenus, the green crab; Asterias vulgaris, the common sea star (Color Plate 29); and Buccinum undatum, the waved whelk. Asterias is one of the major mid-level animal predators both on the Maine coast and in our microcosm. Its primary prey is the edible mussel Mytilis edulis, although a wide variety of bivalves, gastropods, and barnacles are also potential

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FIGURE 16.8 Selected carnivores in the food web of the Smithsonian Maine coast microcosm (see Chapter 21). Drawing by Alice Jane Lippson.

food sources. As we discuss below, the success of Mytilis as a filter feeder in a closed microcosm is determined by how much plankton and organic particulates is available. Because this calls for a relatively large volume of water, it may be necessary to add artificial plankton, particularly early in tank development. Large quantities of Mytilis are readily available from the wild or commercially, as the blue mussel is now a common restaurant food. Thus overpredation by starfish in a microcosm system is seldom a serious problem, if artificial feeding

is acceptable and export managed. In our 15-year-old Maine coast system Asterias was able to feed on most exposed Mytilis, but it cannot negotiate beneath rocks and in crevices that harbor a large population of mostly smaller animals, which again shows the important role adequate cover plays in predator–prey relationships even in aquaria and microcosms. Along the Maine subtidal region and in our coldwater microcosm, crabs (particularly rock crabs on rocky shores and green crabs on the mud flats) were

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References

the primary predators of herbivores and detritivores. These animals preyed especially heavily on the urchin Strongylocentrotus, as well as on a wide variety of molluscs and small invertebrates, particularly worms. Because rock crabs normally foraged over many square meters of bottom, scaling problems in terms of prey reduction were introduced into the small cold-water microcosm just as into the reef model. The solution to the problem was basically the same: crabs were limited to moderate size and/or grazer populations were boosted by adding grazers either from a natural community or from supplementary “nursery” tanks. The lobsters, Homarus americanus in the Maine microcosm and Panulirus argus in several of the reef microcosms, are generalized scavengers and mid- to upper-level predators. While they were particularly successful in many of our systems, typically within a year, if added as juveniles, they grew too large for the ecosystems. At large size, they caused excessive physical damage due to lack of sufficient foraging territory. About once a year we removed the larger animals and replaced them with juveniles of the same species. Higher predators most associated with freshwater ecosystems include pike and bass in cold water and piranha in tropical waters. All of these fish are in the same category as the reef and rocky-shore higher predators described above. They all can be kept in wellmaintained community tanks operated as ecosystems, but unless the tanks are quite large it is likely that feeding will have to be supplemented and that the tanks will require careful balancing with properly operated ATS units. On the other hand, mid-level carnivores that feed on insects, worms, and small crustacea in the wild are highly diverse in fresh waters and form the backbone of the aquarium trade. They include many of the tetras, barbs, toothcarps, some cichlids, and angelfish. At a somewhat higher level in the food webs, and a little more difficult level in model ecosystems, are many of the cichlids and labyrinth fishes. It is interesting to note that while a wide variety of invertebrates are mid-level carnivores in both cold and tropical salt waters, the vast majority of mid- and upper-level carnivores in fresh water are fish, reptiles, birds, and mammals. While some of the more specialized of these fish can certainly cause problems because of their food requirements, the same basic principles generally apply: the larger the predator and the further its food source from the plant/producer level, the larger the tank should be and the more difficult its management is likely to become. Foraging territory can be simulated, but when live food must constantly be added, ecological balance becomes more difficult to achieve. Through algal

scrubbing or truly equivalent technologies, we now have the means to achieve this balance, so that we can concentrate on the more interesting aspects of model ecosystems, community structure, and behavior. Foam fractionation can be an excellent alternate export device, but likely it will greatly reduce system reproduction and population maintenance. Because of the small size of aquaria, carnivores are generally more difficult to maintain in aquarium-sized models than in microcosms and mesocosms. On the other hand, perhaps the most successful continuous longterm management of a higher predator in any of our systems has been that of Enoplometopus occidentalis, the rare reef lobster, in a 130-gallon coral reef (see Chapter 20, especially Figure 20.10). This animal grew to maturity in the aquarium, and served for over 10 years, in a very stable manner, as the top predator of the system. Old fish, as they become slower and less active, sooner or later fell prey to this very aggressive lobster (or shrimp as some taxonomists might say), though always at night. Likewise, newly added fish, off balance in a new system and frequently harassed by other territorial fish, also fall prey to the lobster. If a new fish survives the first night or two, almost invariably it becomes a longterm addition to the system. A reasonable balance is maintained by providing the lobster with an oyster or mussel once a week.

References Barnes, R. (1980) Invertebrate Zoology, 4th edn. Saunders College, Philadelphia. Berryman, A. (2002) Population Cycles: The Case for Trophic Interactions. Oxford University Press. Crawley, M. J. (Ed.). (1992) Natural Enemies: The Population Biology of Predators, Parasites and Diseases. Blackwell Science, London. Edmunds, M. (1974) Defense in Animals. Longman, New York. Gittleman, J. and Gompper, M. (2005) Plight of predators: the importance of carnivores for understanding patterns of biodiversity and extinction risk. In: Ecology of Predator–Prey Interactions. P. Barbosa and I. Castellanos (Eds). Oxford University Press. Gosner, K. (1978) A Field Guide to the Atlantic Seashore. Peterson Field Guide Series, Houghton Mifflin, Boston. Krause, J. and Ruxton, G. (2002) Living in Groups. Oxford University Press. Lima, S. (2002) Putting predators back into behavioral predator–prey interactions. Trends Ecol. Evol. 17: 70–75. Migdalski, E. and Fichter, G. (1976) The Fresh and Salt Water Fishes of the World. Bay Books, London. Owen, J. (1980) Feeding Strategy. Oxford University Press, Oxford. Stephens, D. and Krebs, J. (1986) Foraging Theory. Princeton University Press, Princeton, New Jersey. Whitfield, P. (1978) The Hunters. Simon and Schuster, New York. Williams, D. and Feltmate, B. (1992) Aquatic Insects. CAB International, Oxon, UK. Yonge, C. and Thompson, T. (1976) Living Marine Molluscs. Collins, London.


C H A P T E R

17 Plankton and Planktivores Floating Plants and Animals and Their Predators

Seventy percent of the Earth is covered with water and most of that is open ocean. That open ocean is mostly blue, not green, so it might appear that the phrase “the world is green” does not apply. However, fortunately for the human race, the photosynthesis is there, even if there is continuing debate of exactly how much and just how to measure it (e.g. Marra, 2002). Roughly half of the carbon dioxide released by modern society does not appear in the atmosphere or in terrestrial plants (where it is in large measure re-cycled back to the atmosphere). That “missing” half goes to support photosynthesis by phytoplankton, and fortunately for us, the largest part of the carbon dioxide taken up by phytoplankton gets transferred (by sedimentation) as particulates to the deep ocean. Per unit area, open ocean photosynthesis is less than it is on land, in coastal waters and on coral reefs. Part of the reason for this difference is reduced mixing and metabolite exchange, and to some extent cell shading; however, a major part of the reason for lower primary production is a paucity of nutrients, with iron becoming important along with nitrogen and phosphorus (Chapter 4). So important is this limitation that some scientists have seriously suggested seeding the open ocean with the missing nutrients (see e.g. Boyd et al., 2000). The purpose of this endeavor is to remove significantly more carbon dioxide from the atmosphere, and hopefully to save us from our continued folly in creating global warming. Unfortunately, as we noted earlier, the seeding experiments have not been entirely successful. The open ocean is dominated by plankton, floating or weakly swimming plants and animals that are more or less passively carried by ocean currents. There is no sharp line dividing the plankton from the nekton, the midwater swimmers. However, jellyfish and flagellated or ciliated organisms that have only minimum

control over their position in the water are usually regarded as plankton. Plankters occur in virtually all natural bodies of water. In the open ocean and in large lakes, collectively the plankton totally dominates in plant primary productivity and biomass. Even in the smallest bodies of water, including those made by humans and some that are quite ephemeral, some plankters are normally present. It is perhaps useful to point out that the larvae of most mosquito species feed primarily on floating plants and animals, even when the quantity of water in their “pool” is extremely small. In the open ocean and within large lakes, phytoplankton replaces the trees, herbaceous vegetation, and grasses that on land provide most photosynthesis. Offshore, minute plants become the base of the entire food chain. As we have noted, this environment usually does not appear green, or if it does, it is normally only weakly so. We noted the nutrient and mixing issues, but, in addition, turnover or grazing is high, and plankton biomass does not build up to the levels seen in plants and algae on land or in coastal waters. Nevertheless, productivity can be moderate even with a low standing crop. Many types of plankton, particularly phytoplankton, have been cultured, and some microcosms and mesocosms have been dedicated primarily to the open-water column and its floating organisms (see especially Oviatt et al., 1981; Nixon et al., 1984; Petersen et al., 2003). On the other hand, in benthic mesocosms and aquaria, the primary subject of this book, plankton have largely been ignored. In traditional aquarium technology, physical and/or bacterial filtration was employed, and more recently trickle filtering and foam fractionation have become dominant. Except for rotating film bacterial reactors, these methods effectively trap all of the mid to large sizes of floating plants and animals, including planktonic

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larvae. Depending on the filtration system employed, only the smallest plankters escape in this very artificial world. In Chapter 2 we discussed the same problem in relation to the type of pumps used to move water, and the basic issues of using any filtration system are treated in Chapter 11. In modeling an aquatic ecosystem, the basic question to be asked is: can true plankters and perhaps more importantly reproductive plankters carry out their cycle before being filtered out? If not, the system will be a “garden” and not a self-sustaining ecosystem. Even in benthic microcosms and mesocosms, plankters cannot be ignored. A very large percentage of the species in marine benthic ecosystems, including coral reefs, have planktonic larvae. Some cooler water and estuarine benthic ecosystems are rich in organic detritus, and organisms that filter out or feed directly on that detritus are abundant. Such systems cannot be realistically modeled without considering the role of plankton and its relationship to the bottom. Most of the energy supply of coral reefs is derived by in situ photosynthesis. However, as we describe in depth, in Chapter 20, long-term biodiversity in reef models will depend on allowing the numerous swimming or floating reproductive stages and larvae to survive and settle.

TABLE 17.1 Size Classification of Planktona Size class

Mean diameter ⬎5 mm 2–5 mm 0.2–2.0 mm 20–200 µm 2–20 µm 0.2–2 µm

Megaplankton Macroplankton Mesoplankton Microplankton Nanoplankton Picoplankton

a Note that most bacteria fit in the picoplankton range. However, a large percentage of the suspended bacterial flora is attached to larger organic particles. After Cushing and Walsh (1976) and Stockner (1988).

Whether to the scientist with his or her nets or filters trying to retrieve a sample of a planktonic plant or its predator, or to a floating predator attempting to feed, the size of a plankter is crucial. The floating organism can be caught only if the apparatus is the right size. While terminology has varied widely, the terms and size ranges shown in Table 17.1 are typical of those currently in use. The plankton, whether fresh water or marine, is made up of two general types of organisms. The holoplankton, or true plankton, consists of those plants and animals that normally spend most or all of their life cycle solely within the water column. Meroplankton, on the other hand, consists of the reproductive stages of plants, invertebrates, and fish that are normally either bottom dwelling or included in the fast-moving or neritic community of midwater. The holoplankton also consists of abundant bacteria and protozoa, which are often attached to organic particulates, as well as free-living phytoplankton and zooplankton.

to bacterial breakdown (see Chapters 7–9). It seems likely that the same species of bacteria or at least strains of the same or similar species can carry out the same processes in both fresh and marine waters. However, many marine bacteria when placed in fresher waters appear to be limited by a sodium requirement (Hobbie, 1988). In the open ocean, there are few refractory organic particulates (i.e. those particulates that bacteria find difficult to break down), whereas in fresh or coastal waters, compounds such as lignins and tannins derived from higher plants are more abundant and last for longer periods in the water column. Nevertheless, in all waters, bacteria are present on suspended organic particulates or are truly free living, using dissolved organics as their food source. As we discuss below, a wide variety of organisms from marine and fresh waters feed on these bacteria. This is the end of the detrital food chain in midwater and is also the base of a secondary food web. In a sense, the bacteria plankton keep bouncing the organic energy supply back up the food web until it is finally fully degraded (Figure 17.1). There is still considerable debate as to how much of the energy remaining in organic particulates and dissolved organic material is sent back up an aquatic food web through this “microbial loop” (Wotton, 1990). In low-nutrient, high-quality waters, it is probably a very substantial percentage of initial primary production. Because of their lack of a membrane-bound nucleus and other similarly delimited cell organelles, cyanobacteria (blue-green algae) are now generally accepted, evolutionarily, as bacteria. However, functionally and to a large extent morphologically the blue-greens act more like algae, and we treat them that way in this chapter.

THE BACTERIA

PHYTOPLANKTON

Virtually all organic wastes, plant and animal, occurring suspended in fresh or salt waters or delivered to those waters from the terrestrial environment, are subject

The floating plants of open waters, fresh, brackish, and salt, are primarily those of a dozen or so alga phyla or divisions, from two major lines of evolution (see

PLANKTON SIZE AND COMPOSITION

Phytoplankton

283

FIGURE 17.1 Generalized planktonic food web in shallow waters showing the position of the bacterio-plankton.

Figure 1.1 and Figure 14.2). For an introductory treatment of these groups, the reader is referred to Bold and Wynne (1985); Williams et al. (2002) provide a review of plankton production. Some algal groups are almost entirely planktonic, although many have both planktonic and benthic members. As a whole, in both fresh and salt waters, the diatoms (class Bacillariophyceae in the division Chrysophyta, the golden-brown algae) form the dominant plant components of the plankton (Figures 17.2 and 17.3). Diatoms have cell walls of silica and are often highly ornamented. Occurring in two main groups, centric (radially organized) and pennate (bilaterally organized), diatom shells or frustules consist of two interlocking halves or valves.

While many genera are unicellular, others are filamentous and a few are complexly branched. Some of the pennate diatoms have an elongate groove or rhaphe, which is used to provide a gliding type of mobility to the cell. Diatoms can sexually reproduce by forming motile or nonmotile gametes. While some are fully planktonic, many are dominantly benthic and enter the plankton only in reproduction or when disturbance of the bottom temporarily introduces them to the water column. Any well-lighted and naturally operated model ecosystem that has had nonsterilized introductions from the wild will have a diatom community. However, if filtered, skimmed, or richly bubbled, the midwater diatom population is likely to be minimal or virtually absent.

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FIGURE 17.2 Marine diatoms: (A) pennate diatom Thalassionema nitzschiodes (⫻500); (B) diagram of frustule construction in a pennate diatom (r, rhaphe; pn, cn, polar and central nodules); (C) valve of centric diatom, Actinoptychul senarius (⫻1300); (D) colonial centric diatom Bacteriastrum furcatum (⫻700). After Dawes (1981). Reprinted by permission of John Wiley & Sons, Inc.

In general, diatoms prefer cooler and less nutrient-rich waters. Higher temperatures, higher or extremely low nutrients, or other extremes will usually lead to replacement of the diatoms by dinoflagellates or blue-greens. Dinoflagellates of the division Pyrrophyta are abundant in the oceans, particularly in the tropics. A number of genera and species also occur in fresh and brackish waters, although they tend to be less important than in the oceans. Dinoflagellates are relatively primitive algae with a tendency toward a single distinctive organization and wall. Although some benthic unicells and filaments occur in this group and most algae symbiotic in animals (Chapter 19) are derived from the group, most genera are planktonic. Whether marine or fresh water,

dinoflagellates, as the name suggests, are characterized by a plantlike and often sculptured cellulosic cell wall or “armor” of two hemispheres (Figures 17.4 and 17.5). Lying in the groove or girdle between the hemispheres are two flagellae, one extending around the groove and the other projecting downward along another groove, the sulcus, which extends down the face of the lower hemisphere. This provides the great motility characteristic of the group. Many coastal and freshwater genera also have resistant resting spores that serve to carry them through unfavorable environmental conditions, usually resting on the bottom. Dinoflagellates are characteristic of warmer, often more nutrient-rich conditions. Some genera are able to

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FIGURE 17.4 Marine dinoflagellates: (A) Gonyaulax; (B) Ceratium; (C) Gymnodinium; (D) Peridinium.

FIGURE 17.3 Freshwater diatoms: (A) pennate types (⫻137 to

⫻930); (B) centric types (⫻375 to ⫻750). After Hutchinson (1967). Reprinted by permission of John Wiley & Sons, Inc.

take in particulate organics as food or are even predatory in addition to being photosynthetic. Other genera excrete toxic compounds. Sometimes, under warmer conditions, perhaps additionally supplemented by organics derived from land runoff, these species form “red tides” that can

kill fish and/or invertebrates. Food-chain concentrating of dinoflagellate toxins can also render them fatal to humans (shellfish poisoning and ciguatera; tropical fish poisoning). Nevertheless, these important phytoplankters are generally desirable members of model ecosystems. In our experience, only two cases of mesocosm/microcosm operation have exhibited red tide problems (during over 100 system-years of operation). This occurred in our early years of developing coral reef systems, when several fish were lost and a number exhibited neural distress, tending to lose control over swimming and orientation. The large dinoflagellate Gambierdiscus, known as a source of ciguatera, was shown to be responsible for the situation. However, gradually over several months, the symptoms disappeared from the mesocosms although the presence of Gambierdiscus could be demonstrated for years thereafter. Cyanobacteria, or blue-green algae (Figure 17.6), can be important elements of both freshwater and marine phytoplankton communities. Often considered to be indicators of rather advanced eutrophic or nutrient-rich

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FIGURE 17.5 A variety of freshwater dinoflagellates ranging from primitive (A) to more advanced (E–J). Most forms shown are fully photosynthetic; (C) and (F) feed on other small animals or phytoplankton (⫻375 to ⫻1500). After Hutchinson (1967). Reprinted by permission of John Wiley & Sons, Inc.

conditions in lakes and streams, blue-greens can produce toxins that are deadly to fish and animals. However, they can also be dominant in the extremely low-nutrient conditions of tropical, oceanic waters. Although rarely mentioned in the literature, blue-green-dominated communities can also characterize the waters of pure mountain lakes (Hutchinson, 1967). Certainly the ability of many blue-greens to fix nitrogen from the gaseous state, readily available dissolved in all waters, is partly responsible for their success in situations poor in dissolved nitrogen. Blue-greens tend to fare well in mesocosms if light levels are low, water quality poor, and physical variations common. For the traditional aquarium excessively

rich in nutrients and with relatively low light levels, this makes sense. However, even for ecologically more “normal” conditions, blue-green presence does not necessarily carry negative connotations. The rich algal turf communities of high-quality wild coral reefs are usually rich in blue-green algae as are their normally functioning model analogs. Perhaps the answer partially lies in the minimum tolerance of the primary, “advance” algae for extreme conditions. Given moderate environments the more advanced algae out-compete the bluegreens. For the remaining algal groups, marine and freshwater plankton communities begin to greatly diverge in their composition. Another major group of the Chrysophytes (golden-brown algae) that often dominates in tropical and temperate oceanic situations is the coccolithophores. These phytoplankters, geologically well known because of their armor-plated, calcareous discs (coccoliths) attached to their outer cell walls (Figure 17.7), are motile, typically with a pair of flagella. While abundant enough in the ocean to create geological deposits under certain conditions, only a few coccolithophore genera occur in fresh water, and these are relatively rare. The freshwater equivalents of these coccolith-bearing unicells are a variety of flagellated and nonmotile freshwater green algae (Chlorophyta) (Figures 17.8 and 17.9). The desmids, many species of which can be benthic, are particularly interesting members of the freshwater plankton. Generally characterizing more moderately acid waters as compared to the high-pH waters of the coccolithophores, the desmids have strongly structured cellulosic walls consisting of two symmetrical semicells (Figure 17.10). Most of the photosynthesis occurring in the photic or well-lighted zone of open waters is accomplished by the algal groups described above. These algae also form the base of the midwater food webs and support the underlying filter-feeding benthic fauna. For many decades it has been thought that most phytoplankton production was grazed and passed up through a relatively simple but long food chain. Now it is recognized that, similar to many shore and terrestrial communities, much of the production of offshore phytoplankton is not directly eaten by grazers but after death is degraded by bacteria. Some of this detritus “loop” is then passed up a food web by filter feeders and their predators.

THE PLANKTONIC FOOD WEB Filter or suspension feeding is not as simple as copepods eating phytoplankton and then being fed upon by larger invertebrates or small fish. Especially if one includes free bacteria and organic particulates with their

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FIGURE 17.6 Common planktonic blue-green algae (cyanobacteria) from saltwater (top) and freshwater (bottom) environments. (Top) (A) Trichodesmium; (B) Oscillatoria; and (C) Lyngbya. (Bottom) (A,B) Anacystis; (C–F) Agmenellum and Gomphosphaeria spp., (G) Aphanizomenon; (H) Oscillatoria; (I) Lyngbya; (J,K) Anabaena; (L) Gloeotrichia. (Top) After Thurman and Webber (1984), copyright © 1984 by Scott, Foresman and Company. Reprinted by permission of Harper Collins Publishers. (Bottom) After Hutchinson (1967). Reprinted by permission of John Wiley & Sons, Inc.

bacterial flora, a total spectrum of size from fractions of a micrometer to millimeters and of greatly varying food quality typically exists in a plankton community. Often omitted from the more generalized open-water

food web are the animal protists, or protozoans, that provide a link to the smallest of plankton or particulates. Also, one generally thinks of the planktonic food web, especially in its lower segments, as being one of filtering

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MECHANISMS OF FILTER FEEDING Generally, three basic processes of food capture are utilized by all filter feeders: netting or more straightforward filtering devices, entangling or flowing mucus threads or trails, and cilia trains. None of these are mutually exclusive. In many cases, various combinations or even all three are used together. The number of types of filtering mechanisms are almost as numerous as the number of filtering genera. Also, even among the plankton, prey are often not passive. Motility and the presence of spines, unmanageable shapes, and even toxins, some extremely potent, are utilized to avoid capture. As in the benthic world, plankton can be arranged along a socalled r–k spectrum, which consists of organisms at one end that do not waste energy on protection and put everything into rapid reproduction (accepting great losses), and organisms at the other extreme that place considerable energy into construction of skeleta, spines, toxins, etc., and a long life that emphasizes the quality rather than quantity of reproduction. FIGURE 17.7 Coccoliths on the surface of coccolithophores: (A) Emiliania huxleyi; (B) Umbilicosphaera sibogae; both bars 1 µm; (C) Calcidiseus (⫻2800). After Bold and Wynne (1985).

or filter feeding. However, in addition to the abundant and highly varied filtering processes, at all levels raptorial or “grasping” feeding is also important. Because we technically covered raptorial feeding in Chapter 16 for ease of discussion we concentrate on a more narrowly defined process of filter feeding in this chapter.

Some Protozoans Two widespread and geologically important protozoan groups are abundant herbivores and carnivores at the lower levels of the planktonic food web: the radiolaria and foraminifera (Figure 17.11), which are dominantly marine though with close freshwater relatives. They sometimes secrete incredibly complex shells of silica and calcium carbonate, respectively. In common with their distant relatives, the amoebae, these animals extend numerous sticky tube-like pseudopodia into the surrounding water. The pseudopodia trap small plankters and organic particulates, ingesting them into food vacuoles.

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FIGURE 17.8 (A) Freshwater planktonic unicellular green algae of the order Volvocales. Chlamydomonas (⫻500); (B) colonial motile members of the same order, Volvox (⫻177). After Hutchinson (1967). Reprinted by permission of John Wiley & Sons, Inc.

Filter-Feeding Arthropod Plankters Many midwater crustaceans are filter feeders. Prominent, for example, are most cladocerans such as the wellknown Daphnia (Figure 17.12), which primarily occurs

in fresh waters, as well as many of the abundant marine and freshwater copepods (Figure 17.13). These animals establish water currents for feeding by movement of their numerous appendages, and the filtering

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FIGURE 17.9 Freshwater planktonic green algae: (Top) colonial chlorococcales, (A) Coelastrum; (B–F) Pediastrum (⫻167). (Bottom) Miscellaneous genera, (A) Dictyosphaerium; (B–H) Oocystis; (I) Spherocystis; (J) Gloeocystis; (K) Kirchnoriella; (L) Tetraedron; (M) Elaktothrix; (N) Scenedesmus (⫻500). After Hutchinson (1967). Reprinted by permission of John Wiley & Sons, Inc.

is accomplished by “fans” of setae or small spines located on the bases of the appendages. Water is forced through the setal filters, in some cases, such as Daphnia, using the “bivalved” shell cavity. The collected planktonic cells are wiped off the setae and delivered to the mouth parts by

specialized appendages. Mucus secretions from glands located at the bases of some appendages assist in forming the collected particulates or algal cells into more easily handled “food balls.” Other appendages and the mouth parts are capable of rejecting particles that are

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too large, unpalatable, or perhaps even toxic. Figures 17.14 and 17.15 graphically illustrate the difficulties of discrimination based on size and shape alone faced by these planktonic herbivores. Many of these animals and related species are also capable of raptorial feeding if the prey is too large for the filtering system. Some scientists have suggested that the physical characteristics of water at small scale would force considerably more raptorial response for success (Levinton, 1995). However, the efficiency of capture is reduced if the prey must be individually handled. In spite of the difficulties of capture and ingestion, populations of cladocerans and copepods are capable of overgrazing phytoplankton blooms. It is typical of northern waters, marine and fresh, that the spring phytoplankton bloom, often of a few particularly welladapted, and rapidly growing algal species, is rapidly depleted by zooplankton as the populations of the herbivores quickly develop in response to the presence of abundant plant cells. A group of very small filter feeders that are almost exclusively fresh water is the rotifers. These animals are equally important in the benthic environment and are discussed in Chapter 18.

FIGURE 17.10 Planktonic green algae belonging to the desmids: (A) Spirtaenia; (B–F) Staurodesmus; (G) Cosmarium; (H–J) Staurastrum; all (⫻300–400). After Hutchinson (1967). Reprinted by permission of John Wiley & Sons, Inc.

animals, a good proportion is truly planktonic. Sponges appear to be the archetype filter feeders at the level of the organism (Figures 17.16 and 17.17). Here, both pumping and filtering are accomplished by individual specialized cells called choanocytes. The remainder of the sponge body provides the walls of the pumping channels, structural strength, protection, and reproductive capabilities. However, virtually all feeding activity is concentrated in individual choanocyte cells, which function “raptorially.”

Sponges

Chaetopteris – A Mucus Bag Filter Feeder

Many benthic organisms are planktivorous. While much of the food for these animals is stirred off the bottom by wave action, currents, or the activities of

Many aquatic and marine invertebrates secrete net bags of mucus to filter out plankton from the water column. These are the equivalent of spider webs in the

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FIGURE 17.11 Marine radiolarians: (A) living animal with numerous, spinelike pseudopodia and a captured protozoan (⫻ 150); (B–C) siliceous tests or shells of a variety of genera; (B) is 300 µm in length. After Thurman and Webber (1984). Copyright © 1984 by Scott, Foresman and Company. Reprinted by permission of Harper Collins Publishers; and (D) foraminifera, courtesy of Brian Huber.

terrestrial world, though in many filter feeders using this method, the mucus bag is often eventually ingested along with its trapped particles. Chaetopteris, the parchment worm (Figure 17.18), is cosmopolitan on muddy bottoms in tropical to temperate seas. Using modified legs to “fan” water through its U-shaped burrow, it continuously secretes a mucus bag, which is collected with its entrained food particles by cilia in a central groove. There it is formed into food/ mucus balls, which are eventually passed upward to the mouth in a ciliated groove. A more web-like example is the feeding system used by vermetid gastropods, calcareous, wormlike, attached snails that are colonial and build small reefs or steplike projections on rocky shores. These animals, which adapt quite well to microcosm systems, secrete a spider-like web that is eventually retrieved and eaten along with whatever particles have become entangled. In fresh waters, the larvae of caddis flies are famous for their silk nets (Williams and Feltmate, 1992).

Bivalves – The Master Filter Feeders Primitive bivalves have featherlike ctenidia or gills that function primarily as devices for gaseous exchange. In more advanced species the gills are developed into elaborate folded lamellae that serve a dual purpose: food


gathering as well as respiration (Figure. 17.19). The advanced bivalve gill is richly endowed with cilia as well as groups of cilia that function together. Mucus sheets are also secreted by cells of the gill. Together, the

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mucus and sometimes highly coordinated patterns of beating cilia move water in intricate patterns over the surface of the gills. This motion collects or rejects particles and eventually transports them to the mouth area. So sophisticated is the typical bivalve gill feeding system that in many cases, organic particles or living organisms larger than 4 µm are routinely removed with very high efficiency. In some cases, particles as small as 1 µm are removed, while the bivalve retains a highly discriminatory apparatus for rejecting undesirable particles.

Fish Planktivores Many fish snatch small individual plankters (or nekton) from the water column. Both fresh and marine waters abound in Chromis, killifish, and tetralike fish that feed in this more directly predatory fashion. On the other hand, some fish, for example, those in the herring family, are much more elaborately endowed for direct water-column filtering of plankton. Most herrings are marine or estuarine but some are anadromous, swimming up rivers and streams from the ocean when reproductively mature to breed in fresh water. A few herring are landlocked or occur exclusively in fresh water. In all fish, water is taken in through the mouth and passed laterally over fine, capillary-rich gills for gas exchange. Inside the often blood-red gaseous exchange part of the gills lie a series of sieves or gill rakers (Figure 17.20). In the herring the gill rakers are specialized to sieve out large or smaller plankton depending on the species. While zooplankton are undoubtedly the dominant food acquired in this fashion, in some species the gill rakers are fine enough to capture phytoplankton.

PLANKTON, PARTICULATES, AND MODEL ECOSYSTEMS In most model aquatic ecosystems, except for the few that have been particularly directed toward simulation of plankton-dominated systems, the plankton have been given minimum attention. In the more traditional aquarium work, whether by home hobbyists or professional aquarists, not only have plankton been ignored but the methods employed for water quality control are such that these organisms are largely if not totally destroyed. It has been a major goal of our efforts at ecosystem simulation to avoid any methods that artificially reduce or destroy floating or suspended plants, animals, protists, and microbes. Suspended organic particulates not only are an integral part of the microbe community but also are critical for filter feeders, and this provides additional impetus to avoid physical filtration. In a typical synthesized marine or freshwater ecosystem, emphasizing benthic communities, the plankton populations are minimal because of the relatively small volume of water compared to that typically present in the wild. Note that Petersen et al. (2003) have provided size relationships that allow the modeler to estimate the minimum volume required to prevent dominance by the wall (benthic) communities. However, in smaller systems, just as the chemical and physical effects of the larger body of water must be simulated with scrubbers and other devices, it is also necessary to simulate the presence of the plankton that would normally be present in that larger body of water. In this chapter we primarily discuss the planktonic elements required by benthic communities in microcosms.

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FIGURE 17.12 Several genera of cladocerans including Daphnia, the common planktonic filter feeder from lakes and rivers. From Parker (1982). Reproduced with permission of The McGraw-Hill Companies.


FIGURE 17.13 The marine copepod Calanus showing (A) vortex of water movement and (B) feeding currents through filtering setae on the ventral side. After Barrington (1979).

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FIGURE 17.14 Planktonic copepods and the variety and sizes of phytoplankton on which they would feed: (A) Oithona similis (adult); (B) O. similis (nauplius); (C) Temora longicornis (nauplius). After Jorgenson (1966).

Just as tropical lagoon tanks have been attached to our coral reefs and a mud flat and salt marsh tank is attached to the cold-water rocky shore, open-ocean microcosms could be developed and attached to either a reef or a rocky shore. However, these would require a very large volume of water, and unless an open, highquality natural body of water is available adjacent to the model it would probably generally be impractical. Our approach has been to limit destruction of plankton as reproductive stages of benthic organisms and to import true planktonic biomass in quantity and, to a more limited extent, in quality, into benthic microcosms. Of course, an equivalent nutrient export is required to

use this approach. The algal scrubber (Chapter 11) fulfills this requirement along with managing gas exchange, although other plant systems could be used in the same way with less efficiency. In the model systems described in Chapters 20–23, filtration is not used, the functions of filtration being performed by algal scrubbers and settling traps. These systems have moderate planktonic flora and fauna. The Everglades mesocosm, which used an Archimedes’ screw for saltwater circulation in the early years and then was switched to a disc-flow pump, is particularly rich in plankton, including reproductive stages of the


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FIGURE 17.15 Planktonic copepod and the relative size and abundance of its principal algal prey. After Barnes (1980). Reprinted by permission of Saunders College Publishing.

numerous invertebrates and algae that reproductively maintain their populations. In a typical coral reef community, a major part of the water mass that overlies the reef has been driven there recently, usually from the open ocean, by waves or tides. Studies have shown that while the planktonic biomass that arrives over the reef from the ocean is similar in weight to what is lost from the reef to the lagoon, the composition of the plankton arriving is quite different from that departing the reef. In the water mass coming into the reef, the plankton is dominated by fully planktonic elements, those animals and plants that primarily float in open tropical waters; however, numerous larval fish and numerous invertebrate larvae from distant coral reefs are often also present. Leaving the reef, the planktonic biomass is dominated by fragments of benthic algae lost from the reef’s surface. In the Caribbean windward reef models that we have operated at the Smithsonian, a constant flow of open-ocean water is driven across the reef by the pumping arrangement. The simulated loss of plant material from the reef is easily managed within the framework of the normal algal turf scrubbing harvest. However, while the scrubber system can simulate the effects of “high-quality” incoming ocean water chemically and physically, it cannot supply the holoplankton. Brine shrimp, Artemia salina, are easily hatched from cysts and as 48-h hatchlings; they provide an excellent

mid-sized plankton supply. One can grow or purchase brine shrimp larger in size, thereby providing a spectrum of mid to larger plankton input. However, we have found this approach time consuming, and therefore use dried krill to simulate the larger sized plankton input. It is desirable for more accurate system function to provide a wide range of both species and size input. A holoplankton import of about 2 g/m2/day (dry weight) was found in a well-developed St. Croix reef, and for lack of suitable additional information, that is the rate that we have used for our 3000-gallon reef system. For 4 m2 of reef surface our rate of input was about 8–10 g (dry)/day. It is important to note that this is a relatively small part of the equivalent of approximately 60–70 g (dry)/day input through photosynthesis on the model reef surface, as determined by oxygen measurement. In the Smithsonian Maine coast model system, we have also used live planktonic input. Because they are so easily grown, we have used the flagellate Isochrysis, although Dunaliella or a wide variety of diatoms would do equally well. These algal species are considerably smaller than a brine shrimp or krill. A wide variety of mostly dried artificial foods is now available on the aquarium market (see Delbeek and Sprung, 2006). Many of these have been carefully structured as a balanced food source for aquarium fish. While dried foods are more limiting than live foods, since

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some planktivores may not sense and capture dead material, they nevertheless provide a very convenient simulated planktonic input. When dried foods are used, it is a good idea to widely vary the type and size to maximize availability to a variety of filter feeders. In the many home-size aquaria that we have constructed using the methods described in this book, we have almost exclusively followed this technique. In an open ocean reef, arriving plankton is not restricted by the time of day. The composition often varies markedly from day to night primarily due to vertical migrations, but the standing crop or biomass remains more or less constant throughout the 24-h day. Fish, in particular, easily modify their behavior patterns with the adoption of fixed “feeding” schedules. It is advisable to approach a pattern of continuous introduction as closely as possible to more closely simulate the natural environment and avoid heavy cropping by fish. A wide variety of mechanical devices, timed pumps as well as aliquot-metering systems for dried foods, are now commercially available so continuous plankton introduction is no longer a difficult problem. Planktivores of a wide variety of animal phyla occur in virtually all benthic systems, both hard and soft bottoms. It would be impossible to construct a benthic community with any degree of realism without this element. A large percentage of coral reef organisms in particular use planktonic food sources, either true plankton or reproductive stages of benthic species. Sponge, filter-feeding worms, and vermetid gastropods as well as bivalves fall in this category. Most coelenterates, including stony corals, gorgonians, and anemones, also are included, though strictly speaking, the capture method is more actively predatory. Reef fish of moderate to small size will capture a moderate-sized plankter if the opportunity presents itself. However, a few species such as Chromis and Apogon are largely plankton eating. Of the organisms present in such reef models (see list in Chapter 20), fully one-quarter can be classified as at least partially planktivorous. This percentage is probably low, as the worm phyla have not been carefully studied and many of those species are also plankton eaters. Cold-water coastal systems such as the Maine coast are richly provided with nutrients from runoff and from the constant exhuming and mixing of organic materials from the bottom by tides. The midwater communities are thus proportionally very rich in plankton. The Maine mesocosm that we describe in Chapter 21, although having a reduced holoplankton, nevertheless successfully supports a plethora of filter-feeding colonial animals such as sponges (Leucolenia), hydrozoans (Hydractinla), anemones (Metridium senile), molluscs (Modiolus modiolus, Mytilis edulis, Placopectin magellanicus,

FIGURE 17.16

(A) Simple and (B–D) more complex types of sponges showing the “pumping” cells (choanocytes) and the increasing complexity of organization of pumping and flow chambers. After Barnes (1980).

Aequipectin irradiata, Mya arenaria, Yoldia limatula, Macoma balthica), barnacles (Balanus balanoides), and worms (Spirorbis species, Polydora ligni). Some of these organisms undoubtedly feed on suspended particulate organics, along with their bacterial and protozoan associates. Most, however, feed on the plant and animal plankton, much of it undoubtedly as reproductive stages of the benthic community. Insufficient information is available to determine rocky-shore community consumption of open-water plankton. Scrubbers on the cold-water tanks have been used simply to adjust nutrients or water clarity to the desired level rather than to achieve a specific algal export. Plankton is important to normal ecosystems. While plankton can bloom or “explode” even in the wild, in most cases this is because of human interference or an unusual meteorological event. Given good water quality and careful nutrient management, plankton can be highly beneficial elements to simulating benthic communities in aquaria. The stability provided by an appropriate level of algal scrubbing as described in Chapter 11


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is such that while phytoplankton blooms can occur when import exceeds export for some period, the change is slow, over weeks or months. Also, it is relatively easy to stabilize an aquarium at moderate plankton densities. The primary question the home aquarist need ask is what turbidity level is desired. Using algal scrubbing for control, no apparent negative effects have resulted from this practice even in cases where intense green or yellow blooms have been allowed to persist for several days to several weeks. Generally, a healthy system with good water quality relative to oxygen and pH should carry a small to moderate load of phytoplankton and zooplankton. Filter feeders such as clams can actually be used to maintain moderate levels. If, when experimenting, plankton levels become too high for desired visibility, foam fractionation can be used to reduce plankton concentration. However, if this “plankton scrubbing” is used, the plankton concentration should be monitored closely and foam fractionation removed immediately when desirable levels are achieved.

In our view, the primary area of synthetic ecosystem development needing further technical improvement is that of pumping. As we discussed in Chapter 2, centrifugal pumps are damaging to plankton and defeat efforts to achieve much of what we have discussed in this chapter. While centrifugal pumps are relatively inexpensive, highly reliable, and available in a very wide variety of types commercially, bellows pumps, Archimedes’ screws, and vacuum pumps are rare to nonexistent in small sizes. Disc-flow and screw pumps used in the food technology industry for pumping food items like cooked whole asparagus will pump live fish and clearly can produce the required low plankton damage. At this time they tend to be available only in larger sizes and are expensive. As we discuss in depth in Chapter 20, the use of bellows pumps, as well as an algal turf scrubber (without filtration), has allowed us to sustain, for many years, populations of over 500 species in a home aquarium size reef system. A major proportion of the species in this system have planktonic reproductive stages.

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FIGURE 17.17 Pumping and filtering cells (choanocytes) of sponges. (A) Group of choanocytes in chamber; (B) ultrastructure of a choanocyte in longitudinal section. After Barnes (1980).

WILD ECOSYSTEM RESTORATION In considering the restoration of anthropogenically damaged wild freshwater or coastal marine systems, the issue of the planktonic community is usually directly associated with high nutrient levels, and phytoplankton blooms and crashes. While it may be possible in some cases to approach remediation by replacing failed filter-feeding communities (top-down approaches, such as oysters in Chesapeake Bay), without significantly reducing nutrients, it is more likely that the planktonic community under eutrophic conditions bears little resemblance to its pre-damaged state. The trophic cascade, or top-down control on food webs, has been

extensively researched as a restoration tool for lakes. As we describe earlier, if eutrophication is minimal and the particular situation is relatively simple, some success may be achieved. However, as Dodds (2002) describes, the issues can be extremely complex, with many possible end points. An approach more likely to bring success in such cases is to reduce nutrients first, with large-scale algal turf scrubbing, and then to follow that effort up with attempts to replace the original communities. In restoring wild systems that have been over-fished, but are not seriously eutrophic and have not acquired serious disease problems, restoring filterfeeding communities may well be a viable option.

Wild Ecosystem Restoration

FIGURE 17.18 Longitudinal section of the parchment worm, Chaetopteris, in its burrow, showing the “fanning” parapodia and filtering mucus bag. After Barnes (1980). Reprinted by permission of Saunders College Publishing.

FIGURE 17.19 Internal anatomy of Ostrea edulis (oyster) with right shell removed. Arrows show current created by cilia on the gills (g). After Barrington (1979).

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FIGURE 17.20 Gills of filter-feeding bony fish showing the gill rakers used to sieve out planktonic food. After Barnes (1980). Reprinted by permission of Saunders College Publishing.

References Barnes, R. (1980) Invertebrate Zoology. Saunders College, Philadelphia, Pennsylvania. Barrington, E. (1979) Invertebrate Structure and Function. Wiley, New York. Bold, H. and Wynne, M. (1985) Introduction to the Algae, 2nd edn. Prentice Hall, Englewood Cliffs, New Jersey. Boyd, P. W. et al. (2000) A mesoscale phytoplankton bloom in the polar southern ocean stimulated by iron fertilization. Nature 207: 695–702. Cushing, D. and Walsh, J. (1976) The Ecology of the Seas. Saunders College, Philadelphia, Pennsylvania. Dawes, C. (1981) Marine Botany. Wiley, New York. Delbeek, C. and Sprung, J. (2006) The Reef Aquarium: Science, Art and Technology. Ricordea Publishing, Coconut Grove, Florida. Dodds, W. (2002) Freshwater Ecology. Academic Press, San Diego. Hobbie, J. (1988) A comparison of the ecology of plankton bacteria in fresh and salt water. Limnol. Oceanogr. 33: 750–764. Hutchinson, G. E. (1967) A Treatise on Limnology, Vol. 2. Wiley, New York. Jorgenson, C. B. (1966) Biology of Suspension Feeding. Pergamon Press, Oxford. Levinton, J. (1995) Marine Biology: Function, Biodiversity, Ecology. Oxford University Press, Oxford. Marra, J. (2002) Approaches to the measurement of plankton production. In: Phytoplankton Productivity. P.J. leB. Williams, D. Thomas, and C. Reynolds (Eds). Blackwell Science, Oxford.

Nixon, S., Pilson, M., Oviatt, C., Danaghy, P., Sullivan, B., Seitzinger, S., Rudnick, D., and Frithsen, J. (1984) Eutrophication of a coastal marine ecosystem: an experimental study using the MERL mircocosms. In: Flows of Energy and Materials in Marine Ecosystems. M. Fasham (Ed.). Plenum Press, New York. Oviatt, C., Buckley, B., and Nixon, S. (1981) Annual phytoplankton metabolism in Narragansett Bay calculated from survey field measurements and microcosm observations. Estuaries 4: 167–175. Parker, S. (Ed.) (1982) Synopsis and Classification of Living Organisms. McGraw-Hill, New York. Petersen, J. et al. (2003) Multiscale experiments in coastal ecology: improving realism and advancing theory. Bioscience 53: 1181–1197. Stockner, J. (1988) Phototrophic picoplankton: an overview from marine and freshwater ecosystems. Limnol. Oceanogr. 33: 765–775. Thurman, H. and Webber, H. (1984) Marine Biology. Merrill Publishing, Columbus, Ohio. Williams, D. and Feltmate, B. (1992) Aquatic Insects. CAB International, Wallingford, UK. Williams, P. J. leB., Thomas, D., and Reynolds, C. (2002) Phytoplankton Productivity: Carbon Assimilation in Marine and Freshwater Ecosystems. Blackwell Science, Oxford. Wotton, R. (1990) Particulate and dissolved organic material as food. In: The Biology of Particles in Aquatic Systems. R. Wotton (Ed.). CRC Press, Boca Raton, Florida.

C H A P T E R

18 Detritus and Detritivores The Dynamics of Muddy Bottoms

In the idealized food chain, plants (including algae) capture solar energy and build energy-rich biomass; herbivores then eat plants, and with the materials and energy derived from this food they power their movements and build their body tissues. These grazers or browsers are in turn eaten by carnivores. While the herbivores may require bacteria or protozoans in their digestive tracts to accomplish digestion of some of the plant materials, this is internal, a kind of symbiosis, and conceptually the simple food chain remains. For perhaps half of the primary plant production in the biosphere as a whole, the photosynthetic energy accumulated by plants is passed to the remainder of their communities in this more or less idealized food chain or web. In offshore marine and larger freshwater ecosystems, much of the planktonic and benthonic algae eaten by fish and invertebrates is internally digested by those grazers. However, due to the inefficiencies of handling the plant food, a major part of the food ultimately passes through the gut and into suspended detritus (Figure 18.1). Also, not all phytoplankton is eaten; some live at their life cycle and die “in situ.” As we discussed in Chapter 17, some of the resulting detritus is ecologically treated as additional plankton and, with its bacterial and fungal flora, is grazed or filtered accordingly. Finally, a small portion (in this case 10%) of the energy-bearing detritus settles out of the water to become available for use by a bottom community. A coral reef is similar to this offshore plankton community, except that approximately 3–5% is ocean introduced plankton and the equivalent, mostly as attached algal fragments, with some feces, is passed on to the reef lagoon.

FIGURE 18.1 Energy flow (as carbon) in an idealized planktonic food chain. Note that while a majority of phytoplankton production is eaten by herbivores only about 50% is utilized either in respiration or biomass building. The remaining 50% is transferred to the midwater detrital cycle. C: herbivore consumption; R: respiration; P: growth production; F: feces production; oxidized carbon is that which has passed through detritus. After Newell (1984).

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18. Detritus and Detritivores

On the other hand, in many coastal and freshwater ecosystems, larger, tougher benthic algae such as kelp and Sargassum, as well as higher plants such as submerged aquatic vegetation, seagrasses, marsh grasses, mangroves, and virtually all land plants washed into the water as leaves, branches, and fruits, are the major source of primary production. The tough stalks, leaves, and woody parts of these plants are not readily digestible by most grazers, although the cell contents may be digested as they pass through their guts. Fragmented by grazers or physical degradation, the cellular contents can be exuded or leached as dissolved organic material or particulates to be used by bacteria, fungi, and protozoa or even directly by other plants. However, the cellulosic and lignic cell wall components become larger debris. Then gradually, as physical and organic processes work them over further, they become a finer and finer detritus. These waste plant materials are attacked over and over again, primarily by bacteria, fungi, and protozoans, until they are fully broken down and their energy and minerals redistributed through detritivores to the community. Figure 18.2 shows the trophic dynamics of a kelp bed, in terms of energy flow, as a simplified example of a detrital-dominated ecosystem in which the algal particulates, heavily occupied by bacteria, are fed on by filter feeders. In most lakes and coastal ecosystems with protected bays, as well as in deeper water on open coasts, fine sediment delivered by streams or eroded from shorelines is deposited in zones of low wave energy. Organic particulates derived from rocky shores or marshes of great plant production are often deposited along with the muds, sands, and clays. A major portion of lake and coastal

marine inshore production is delivered as plant detritus and reworked animal feces to such organic-rich soft bottoms. While organic content can be as high as 10%, typically the percentage of organic materials in these sediments is low, less than 5%. Yet the supply is large and tends to be smoothed, so there are not great seasonal or other periodicities that leave gaps in the food supply. An example of such a detrital-dominated system, a Maine coastal bay where much of the organic particulates is delivered by waves and tides to sandy–muddy flats and bay bottoms, is shown in Figure 18.3. The epifauna and infauna of these soft-bottom communities can be taxonomically rich and diverse in species. For the example cited, probably a relatively impoverished case, over 60 species of macroinfauna larger than 2 mm and consisting of worms, bivalves, and crustaceans are present (Table 18.1). The uncounted smaller meiofauna provide many additional species. These bottoms can also be relatively high in animal biomass (Figure 2.10). It is particularly interesting that the marine and estuarine soft bottoms, on average, have an order of magnitude higher faunal biomass than fresh waters. This has been attributed primarily to the driving or mixing effect of tides in the marine and estuarine environments (Nixon, 1989). Larger waves in general are almost certainly an additional factor. This chapter examines the abundant organisms of fine sediments where the included organic detritus has collected from the overlying waters and from adjacent shore and land areas. When these fine sediments also lie in shallow, well-lighted waters and can support a diatom or blue-green growth, plant-derived organic materials

FIGURE 18.2 Basic energy flow diagram for a kelp bed in South Africa. POM: particulate organic matter; DOM: dissolved organic matter. Numbers in kJ/m2/year; P: produced; C: consumed. After Mann (1988).

Detritus and Detritivores

FIGURE 18.3 Distribution of sedimentary bottoms on a portion of the open rocky coast in eastern Maine. Note that while this is a rocky coast with very rich rockweed and kelp beds, areally soft-bottom communities dominate. After Shipp et al. (1985).

305

306

18. Detritus and Detritivores TABLE 18.1 Common Invertebrate Macrobenthos (⬎2 mm) in the Muddy Bottoms of Gouldsboro Bay, Maine, and Its Off-Lying Waters (No./m2)a

Range

Genus/species

Phylum

Offshore

Nearshore

Outer Bay

Upper Bay

Intertidal

Wide range

Nucula proxima Ninoe nigripes Unidentified species Nepthys incisa

Mollusc/bivalve Annelid/polychaete Nemertean Annelid/polychaete

590/100% 250/80% 39/60% 57/80%

14 348/100% 645/100% 89/83% 25/50%

8045/100% 75/62% 15/37% 19/75%

137/22% 2/22% 17/11% 2/11%

0 0 0 0

Intermediate range

Scolopus acutus Ophelina acuminata Prionospio steenstrupi Unidentified clam species Nucula delphinodonta Edotea montosa Unidentified worm species Ampelisca abdita Tharyx acutus Nephtys ciliata Aglaophamus neotens Phoxocephalus holbolli

Annelid/polychaete Annelid/polychaete Annelid/polychaete Mollusc/bivalve Mollusc/bivalve Arthropod/isopod` Annelid/polychaete Arthropod/amphipod Annelid/polychaete Annelid/polychaete Annelid/polychaete Arthropod/amphipod

0 0 0 163/100% 0 0 23/100% 0 0 23/20% 0 0

267/62% 114/50% 44/33% 58/83% 11/33% 62/83% 58/50% 0 0 0 0 0

167/67% 206/75% 242/87% 12/37% 148/62% 4/25% 0 50/62% 15/66% 10/25% 15/37% 31/75%

235/66% 33/56% G/11% 0 65/44% 0 0 167/89% 95/66% 48/78% 31/66% 6/11%

0 0 0 0 0 0 0 0 0 0 0 8/17%

Narrow range

Dentalium entale Diastylis cornufer Sternapsis scutata Yoldia sapotilla Harpinia propingua Diastylis sculpta Eudorella pusilla Cyclocardia borealis Orchomonella minuta Anaitides mucosa Ampharete acutifrons Lumbrinereis tenuis Saccoglossus kowaleski Scoloplos fragilis Corophium volutator Unidentified worm species

Mollusc/scaphopod Arthropod/cumacean Annelid/polychaete Mollusc/bivalve Arthropod/amphipod Arthropod/cumacean Arthropod/cumacean Mollusc/bivalve Arthropod/amphipod Annelid/polychaete Annelid/polychaete Annelid/polychaete Hemichordate Annelid/polychaete Arthropod/amphipod Annelids/oligochaete

30/100% 14/80% 23/80% 74/100% 0 0 0 0 0 0 0 0 0 0 0 0

0 0 0 6/33% 0 0 0 0 0 0 0 0 0 0 0 0

0 0 0 10/25% 77/87% 667/62% 471/100% 73/66% 54/75% 23/62% 33/75% 25/62% 0 0 0 0

0 0 0 0 0 0 7/33% 2/11% 0 2/11% 6/11% 4/11% 0 0 25/11% 6/12%

0 0 0 0 0 0 0 0 0 0 0 0 86/83% 150/83% 278/66% 580/66%

Number of species Mean incl./m Number of stations

68

64

74

32

16

2916

17 564

10 440

749

1447

5

6

8

9

6

a Numbers given (250/80%) are mean numbers of individual animals per station and the percentage of the stations at which the species was found. Only species occurring at greater than 60% of the stations within any one region are included (about one-third of total). The strongly zonate character of the bottom fauna results from a variety of interacting factors including depth, sediment coarseness, and water climate (the inner bay is strongly subarctic in character with overlying ice and temperatures below 0°C in winter, and summer temperatures of 15–20°C; offshore winter temperatures are in the 0–2°C range, while summer temperatures are rarely over 12°C).

can even originate directly from the sediment surface. It is in these sediments, if they are not so rapidly buried as to become geological deposits, that the last traces of organic energy are wrung from organic particles, further supporting the activities of animals. The size ranges typically in use by biologists and ecologists to define this benthic flora and fauna are given in Table 18.2. To a large extent, microbenthos include larger protozoans and a very wide diversity of tiny invertebrates from all phyla. Although most meiobenthos

groups have macrobenthos representatives, a few, such as nematodes, kinorhynchs, and gastrotrichs, are primarily members only of the meiobenthos or of soils. The marine macrobenthos is the domain of a large percentage of known invertebrates. In freshwater sediments, numerous insect larvae join some of the other invertebrate phyla that occur in both salt and fresh water. In general, microbenthos feed on small organic particulates, meiobenthos feed on larger organic particulates (and their host of attached microbenthos), and

307

Fungi TABLE 18.2 Size Ranges of Benthic Faunaa ⬎0.5 mm 0.1–0.5 mm ⬎0.1 mm

Macrobenthos Meiobenthos Microbenthos

a In practice this usually refers to what will pass through a screen of that mesh size. Thus, the dimensions are generally minimum dimensions: a worm 0.2 mm in diameter, 2 mm long is treated as meiobenthos. After Levinton (1982).

macrobenthos feed on meiobenthos. However, as always in biology and ecology, organisms and their activities are not easily categorized. The food chain is more accurately described as a web, and some macrofauna are capable of feeding on small organic particulates. Also, there are no sharp lines among planktonic (suspension) feeders lying within the sediment and feeding on waterborne organisms, those organisms feeding off detritus stirred off the bottom, filter feeders on interstitial water between the sediment grains, and true deposit feeders eating organic particulates that form part of the sediment. Our separation between Chapters 17 and 18 is as much a convenience as a sharp line of demarcation.

THE DEEP OCEAN The largest nonplanktonic ecosystem on Earth is the detrital-based deep ocean floor. Most of this dark, cold region has a layer, and sometimes thick layers, of sediment, produced primarily by calcareous or siliceous plankton shells (mostly from the shallow sunlit regions) or by clays derived largely from continental erosions and finally settled to the deepest sea floors (Seibold and Berger, 1993). Except for scattered cold seeps and hydrothermal vents, which are tectonically created features, with a chemosynthetically based energy supply (Van Dover, 2000), the energy supply of this community is based on the rain of organic materials from shallow water. It is now known that much of the deep ocean has a rich fauna. In accordance with the dynamic equilibrium model that we described in Chapter 12, species diversity rises progressively from the shallow continental shelves down the continental slope, peaks at high levels on the continental rise, and falls again passing further into abyssal zones (Gage and Tyler, 1991). Although as far as we are aware no one has attempted microcosm or mesocosm systems of the deep ocean, this would surely be a valuable, albeit very expensive, endeavor. The various vent systems with many unique organisms, discovered and elaborated on only during

TABLE 18.3 Mean Numbers and Wet Biomass of Organisms in a Silt Sample of 1 m2 in the Top 5 mma Organism group

Numbers

Biomass (g)

Large macrobenthos Small macrobenthos Meiobenthos Protozoa Diatoms Bacteria

2.8 230 146 ⫻ 103 283 ⫻ 106 590 ⫻ 109 335 ⫻ 109

3.75 3.30 1.15 0.02 0.07 0.07

a From Rheinheimer (1985). Reproduced with permission of John Wiley & Sons, Ltd.

the past several decades, would provide a particularly rich vehicle for experimentation.

BACTERIA Bacteria are abundant in all sediments, fresh water, and marine, although generally the finer and more organic-rich muds and clays have a much larger number of cells. Typically, half of the bacterial flora is attached to sediment particles and half occurs in the interstitial water. As we discussed in previous chapters, virtually all organic compounds can be broken down by some bacteria species. Bacterial numbers, especially those of the more generalized decomposers, can be enormous (on the order of 106 to 109 cells per cm3) in fine, organicrich sediments. However, as compared to macro- and meiobenthos, the resulting biomass (and therefore effect on organic processes) is usually relatively low. Rheinheimer (1985) discusses a case of a fine, organicrich marine sediment in which the bacteria constitute less than 1% of the biomass although numbering 355 ⫻ 109 cells in the top 5 mm of the sediment (Table 18.3). Numbers are generally highest near the surface, or around the tubes and burrows of macrofauna, where oxygen is abundant. Within a number of centimeters from the surface, where oxygen becomes depleted, bacterial numbers are lower and sulfur and methane species are dominant. Here, breakdown of organic materials is incomplete, although constant bioturbation or mixing by the fauna repeatedly brings buried material to the oxygen-rich surface and oxygen to greater depths.

FUNGI Fungi, as well as being important parasites, are ubiquitous decomposers of organic materials, particularly plant materials, in virtually all of the Earth’s marine as well as terrestrial environments. Although generally requiring a rich supply of oxygen, a wide variety of

308


FIGURE 18.4 Aquatic phycomycetes showing nonseptate mycelium and fruiting bodies releasing flagellated zoospores: (A) Phythophora, (B) Pythium, and (C) Blastocladia. From Freshwater Biology by L. G. Willoughby (1976), reproduced by kind permission of Kluwer Academic Publishers.

Meiobenthos: Protozoans

fungi are characteristic of freshwater and marine sediments and the organic materials that are in the process of being incorporated into those sediments. Fewer species of fungi are present in the marine and estuarine environment, some being invaders from fresh water. However, a number of genera and species of fungi carry out their full life cycle in marine waters (Dix and Webster, 1995). Except for some yeasts, the primary life form of fungi is a mycelium of branching, ramifying, colorless hyphae, 10–30 µm in diameter (Figure 18.4). It is the branch or rhizoidal tips of these hyphae reaching into the interstices of cellular or multicellular organic material and releasing digestive enzymes that results in the breakdown of those materials. In the terrestrial environment the relatively large fruiting bodies of the basidiomycetes and ascomycetes form the familiar mushrooms and bracket fungi. These fruiting bodies are based on decomposition of mostly dead plant materials by characteristic, septate hyphae. Some ascomycetes and basidiomycetes occur in the marine and freshwater environments (Figure 18.5), though here they tend to lack the familiar macroscopic fruiting bodies. However, they still possess the characteristic sporebearing asci and basidia that allows them to be identified. The unicellular yeasts, which are thought to be very reduced ascomycetes, are abundant in both marine and fresh waters. The dominant fungi of the freshwater environment are phycomycetes (water molds) and Fungi imperfecti. The former possess nonseptate hyphae and generally have flagellate zoospores or gametes at some point in their life cycle (Figure 18.4). The latter are higher fungi with septate hyphae but no known sexual reproduction. Many phycomycetes are parasites, but the majority are either decomposers or are capable of following either a parasitic or a decomposer mode of life. In the marine environment, the ascomycetes are dominant, though the other major groups are still present. Figure 18.6 shows a greatly idealized decomposer food chain based on the fungal breakdown of leaves on the surface of a sediment bottom. It is still functioning when the leaf has been degraded to fine detritus. The feeding path of natural ecosystems is typically much more complex.

PROTOZOA Some protozoan protists are large enough to be members of the meiobenthos. A few, such as the giant amoeba, many foraminifera, and even some ciliates, can technically qualify as macrobenthos. However, many protozoans are less than 100 µm in largest dimension and are

309

regarded as microbenthos. Some protists function as plants. Others are tiny but voracious predators, as we discussed in Chapter 17. However, large numbers of protistan microbenthos are detritus and bacteria feeders within aquatic sediments and wet soils. A typical feeding and digestion process for particulates or bacteria is shown in Figure 18.7. Since protozoans are a food source for many meio- and macrobenthos and an important link in the detrital food chain, we briefly discuss a few characteristic types. (See also Chapter 6.) Mastigophorans are protozoans with typically one or two, but sometimes many, flagella. Some animals placed here are photosynthetic and often included in algal groups, and some are parasitic on a wide variety of animals including humans and domestic animals. However, many flagellates are feeders on detritus either within or on the surface of sediments. A few of these genera characteristic of the Smithsonian Chesapeake mesocosm, described in Chapter 22, are shown in Figure 18.8. All of the major protozoan groups have small bacteria- and particulate-feeding members that are technically members of the microbenthos. However, the remaining nonflagellate types are mostly larger and strictly speaking are members of the meiofauna though they are often deposit feeders on particulates.

MEIOBENTHOS: PROTOZOANS Sarcodines are closely related to the flagellates, even though generally motion and feeding are accomplished by pseudopodia and amoeboid actions. The familiar amoeba is a sarcodine. Many have flagellated reproductive states, and a few are both amoeboid and flagellate. Some sarcodines with well-developed calcareous and siliceous shells and some foraminifera and radiolarians primarily in marine environments and heliozoans in fresh water are primarily planktonic. Others, particularly among the forams, have many benthic members. Along with some naked amoebas, amoebas that build shells, and the forams, these typically meioto macrobenthic-sized animals can be extremely important feeders on bacterial coated particulates as well as on diatoms and flagellates within and on the surface of sediments (Figure 18.9). The ciliophorans, the majority of which lie in the meiofaunal range, are the most advanced of the protozoa (Figure 18.10). This group includes the Paramecium, which nearly every one has seen either in high school biology or in films. Here, the unicellular condition, through the development of a wide variety of cell organelles, becomes as complex in function as many multicellular

310


FIGURE 18.5 Aquatic ascomycete (Anguillospora) showing nonsexual spore production (A) and the “reduced” fruiting body (B) resulting from sexual reproduction. From Freshwater Biology by L. G. Willoughby (1976).

FIGURE 18.6 Basic process of breakdown of plant material in aquatic environment. C: cellulose; L: lignin; P: protein. The microbial intermediate stage is characterized by abundant fungal hyphae. From Freshwater Biology by L. G. Willoughby (1976).

Meiofauna: The Multicellular Invertebrates

311

FIGURE 18.7 Basic feeding process in a single-celled protozoan. After Barnes (1987).

invertebrates. The cell surface of a ciliophoran is typically fixed in form, being characterized by a complex pellicular structure. In primitive genera, the cilia, which are part of a subpellicular infraciliary system, occur in simple rows. In more advanced forms the cilia can group to perform complex feeding or locomotion tasks. In some cases they are grouped in tufts as cirri; in others they work together to form a well-defined, undulating membrane. Different species of ciliophorans can engage in a wide variety of feeding modes. Many are bacterial, detrital, or microalgal feeders in either the deposit or filtering mode. These tend to have complex mouth, buccal cavity, and ciliary relationships. Others are raptorial in feeding style (Chapter 16), preying on small multicellular invertebrates as well as other protozoans. Many of the raptors have specialized stinging organelles or toxicists that function like the stinging cells of jellyfish. It is difficult to overrate the importance of the protozoan community in a normally functioning wild ecosystem, mesocosm, or aquarium. In a brief survey of the 15 000-gallon Chesapeake mesocosm (Chapter 22), 11 genera of flagellates, 14 genera of sarcodines, and 41 genera of ciliates were counted. Most of these were found in aufwuchs communities and most likely also occur in the dominating benthic soft bottoms in this system. A similar survey of a much smaller coral reef (130 gallon; see Chapter 20) produced more than twice as many species: 18 flagellates; 44 sarcodines; 75 ciliates.

FIGURE 18.8 Several flagellated (mastigophoran) protozoa of the Smithsonian Chesapeake mesocosm: (A) Monas, 5–16 µm, (B) Chilomonas, 15 µm, (C) Anisonema, 15–60 µm, and (D) Monosiga, 5–15 µm. After Pennak (1953). Reprinted by permission of John Wiley & Sons, Inc.

MEIOFAUNA: THE MULTICELLULAR INVERTEBRATES Many invertebrate phyla (22 out of 39) have at least a few meiobenthic representatives as adults. Many groups are temporarily present as larvae. However, the major groups occurring only in this fauna of tiny organisms are five peculiar phyla that are almost totally meiobenthic: the Loricifera, Kinorhyncha, Tardigrada,

312


FIGURE 18.9 Protozoans in the meiofauna size range. Shelled amoebas (A–D) and foraminifera “shells” (E–J) (sarcodines). (A,B) Arcella, (C) Euglypha, (D) Difflugia, (E) Bulimina, (F,G) Elphidium, and (H–J) Ammonia. Scale 200 µ. (A–D) After Barnes (1987); (E–J) after Pennak (1953), reprinted by permission of John Wiley & Sons, Inc.

313

Macrobenthos

FIGURE 18.10 Freshwater ciliates characteristic of the Chesapeake mesocosm. (A) Chilodonella, 50–300 µm, (B) Vorticella, 35–160 µm, (C) Paramecium, 60–300 µm, and (D,E) Stylonychia, 50–300 µm. (E is a lateral view.) After Pennak (1953). Reprinted by permission of John Wiley & Sons, Inc.

Gastrotricha, and Gnathostomulida (Figure 18.11). Some members of the major invertebrate phyla, Arthropoda and Turbellaria, are also represented here (Figure 18.12). Because they are so important and are not discussed elsewhere in this book, the nematodes and rotifers that are ubiquitous meiofaunal denizens deserve special mention. Many nematode genera are parasites (the roundworms) on animals and plants and include some of human’s most serious parasitic infections. Other genera are herbivorous or carnivorous in a wide variety of environments. Both parasites and herbivores can be moderately large, many on the order of several centimeters. Most nematodes, however, are nonparasitic denizens of sediments and soils. In these environments

they are generally quite small, less than 2 mm long and often less than 0.5 mm. The nematodes can be extremely abundant in both marine and terrestrial soils and sediments, often millions per square meter of bottom. Nematodes living in sediments are typically round and smooth with a faint indication of annulations on an elastic and rather tough cuticle. The anatomical layout is simple but still fairly complex for such small animals (Figure 18.13). Nematodes move through the interstitial spaces of sediments by undulatory motions. Many species feed on diatoms, fungi, bacteria, and organic particles coated with bacteria and diatoms. Others are carnivorous on other nematodes and protozoans and can have complex dentition (Figure 18.14). Some carnivores have mouthparts with spears or stylets and are able to produce poisonous injections into their prey. Nematodes are extremely important low- to mid-level members of detrital food webs. While relatively difficult for the nonspecialist to identify, their presence should be encouraged in synthetic ecosystems as they are strong contributors to detrital recycling and to the stability of marine and freshwater ecosystems. Finally, since they are ubiquitous elements of freshwater meiobenthos, we briefly discuss the rotifers or rotatoria. These distinctive little animals, with many species occurring in pond and lake zooplankton, are familiar to anyone who has looked at drops of pond water through a microscope (Figure 18.15). The typical paired “whirling” corona of cilia at the head bring food to the mouth. The food is generally organic particulates, bacteria, or algal cells, but some species are predatory on other small invertebrates. The mastax, just interior of the mouth, is a food processing center, often muscular and with toothlike structures for the grinding or tearing of food particles. In some cases locomotion is derived from the coronal cilia; however, in sediment dwellers, bending motions, contractions, and extension of the body and “foot” are equally likely to provide movement.

MACROBENTHOS Virtually all invertebrate phyla have members that occur on or within aquatic sediments. Soft bottoms are often extremely rich in species and are critical feeding grounds for many fish and some diving and wading birds. In addition to predator species, soft bottoms have a broad spectrum of invertebrate types ranging from deposit feeders to suspension feeders. As we mentioned in Chapter 17, there is no sharp dividing line between the soft bottom and the immediately overlying water column. Many species of fish that live primarily in the water column feed on the bottom. Many clams and worms that live within soft bottoms feed on plankton from the overlying water. Since we

314


FIGURE 18.11 Invertebrate phyla occurring primarily in the meiofauna. (A) Tardigrada, marine and fresh (water bears), bars ⫽ 50 µm, (B) Loricifera, marine with extrusible mouth and a chitinous skeleton, bar ⫽ 100 µm, (C) Kinorhyncha, marine/estuarine, extrusible head, strongly segmented, bar ⫽ 100 µm, (D) Gastrotricha, marine and fresh, move by cilia, bar ⫽ 100 µm, and (E) Gnathostomulida, marine of low oxygen sediments, ciliary motion, and distinctive jaws, longer bar ⫽ 100 µm, shorter bar ⫽ 10 µm. All after R.P. Higgins and Theil (1988).

Macrobenthos

FIGURE 18.12 (A) Benthic meiofaunal elements of some major invertebrate phyla. (A) Typical harpacticoid cope-

pods: (a) nauplius larva, (b) copepodid larva, and (c) adult, bar ⫽ 300 µm; (B) polychaetes: (a) Pusillotrocha, (b) Saccocirrus, and (c) Nerilla; (C) turbellarians, bars: (a) ⫽ 1 mm and (b) ⫽ 200 µm; (D) ostracods, bar ⫽ 200 µm. After R.P. Higgins and Theil (1988).

315

316


FIGURE 18.13 (A) Longitudinal section of a female nematode, Pseudocella; (B) cross section of generalized nematode through pharynx. After Barnes (1987).

Deposit Feeding in Saltwater Soft Bottoms

317

FIGURE 18.14 Structural variety in nematodes. (A) Wilsonema with elaborate mouth parts, (B) abundantly setate Trichotheristus, (C) Placodira with armored caticle, (D) Monopisthia with spiny cutide, and (E) cross section through head of Enoplus showing jaws. After Barnes (1987).

touched on filter or suspension feeders in the last chapter, we concentrate here on a few examples of invertebrate deposit feeders.

DEPOSIT FEEDING IN SALTWATER SOFT BOTTOMS As an illustration of the richness and complexity of soft-bottom communities, we use the relatively

well-studied, estuarine Delaware Bay (Table 18.4). Of 174 macrobenthic species tallied during a bottom survey, 84 were deposit feeders, 37 suspension feeders, 15 omnivores, and 38 carnivores. In terms of species numbers, the great majority of deposit feeders were about equally divided between polychaete worms and amphipods. However, of the three bivalve mollusc species, two were highly abundant. Thus, in a biomass sense, the fauna is about equally divided between

318


FIGURE 18.15 Structure of rotatoria: (A) Philodina and (B) Notommata. After Barnes (1987).

polychaete worms, amphipod crustaceans, and bivalve molluscs. Annelids are strongly segmented, highly developed worms. Polychaetes in particular have two lateral “feet” or parapodia on most segments, are often rich with spines or setae, and have a well-developed head region with a wide variety of sensory and feeding structures. The role of polychaete worms in deposit feeding has been well studied and two general feeding types have been identified: the burrower and the surface or selective feeder (Whitlach, 1980). These two types, from the dominant forms of Delaware Bay, are shown in Figure 18.16. Generally, the burrowers are adapted in a variety of ways for simply taking up mouthfuls of raw sediment, digesting the organic material, bacteria, and any contained meiofauna, and

ejecting large quantities of the remaining fecal material. The surface feeders, on the other hand, use ciliated tentacles or palps and mucus to select organic particles from the surface of the sediment and transport them to the mouth. In some cases, the tentacles can be numerous and quite long (many centimeters). Some of the most primitive but abundant bivalve molluscs, including the nut shells, the Nuculidae, and the Nuculanidae, are adapted for deposit feeding (Figure 18.17). The mechanism is similar to that in the worm groups using selective deposit feeding with ciliated and mucus-rich tentacles or palps. Unlike the selective-feeding polychaetes, the deposit-feeding bivalves feed within the sediment rather than on the surface. However, the European Scrobicularia clam has a long siphon that sweeps in a radial fashion around its

319

Deposit Feeding in Freshwater Soft Bottoms TABLE 18.4 Macroinvertebrate Deposit Feeders in a 10 Square Mile Area of Southwestern Delaware Baya All samples number of species

Summary deposit feeders

Abundant species Asabellides oculatus Heteromastis filiformis Scoloplos fragilis Polydora socialis Spio setosa Spiophanes bombyx Streblospio benedicti

37 Suspension (filter) feeders

Annelid worms Polychaetes 33 spp., 8 abd.

38 Carnivores

Oligochaetes 2 spp., 1 abd. Spunculids 1 sp

Oligochaete unidentified

84 Deposit feeders

Molluscs Bivalves 3 spp., 2 very abd. Pycnogonids 1sp.

Nuculla proxima Tellina agilis

15 Omnivores 174 spp

Anthropods Cumaceans 3 spp., 1 abd.

Oxyurostylis smithi

Isopods 2 spp., 1 abd. Average density of macroinvertebrates per m2: 722

Edotea triloba Ampelisca verrilli Unicola serrata Parahaustorius longimerous Protohaustorius wigleyi

Amphipods 30 spp., 4 abd. Callianasids 2 spp. Echinoderms

a

Data derived from 150 quantitative samples. After Maurer et al. (1979).

burrow, thus functioning much like the long-tentacled polychaetes. Of the major groups of detritivores in Delaware Bay, the isopods and amphipods (Figure 18.18) need little detailed discussion. These little pill buglike and shrimplike crustaceans are richly endowed with feeding apparatus in terms of legs and mouth parts and are well equipped to handle organic particulates. As with the worms, some amphipods are tube builders, some are normally shaped burrowers that do not construct tubes, and still others are elongate and quite narrow, allowing movement interstitially between sand grains. Although not conspicuous in the sediments of Delaware Bay, the echinoderms have several major groups that are richly endowed with detritivorous abilities. The brittle stars, sand dollars, heart urchins, and sea cucumbers are often conspicuous on soft bottoms and have basic feeding patterns that are similar to those described for the polychaetes (Figure 18.19).

DEPOSIT FEEDING IN FRESHWATER SOFT BOTTOMS The sandy and muddy sediments of fresh water have either the same or functionally similar groups of organisms that feed and perform as do their counterparts in the sea and in brackish waters (Lopez, 1988). However, among the detritivores themselves, there are two major taxonomic differences. The polychaete worms, largely restricted to the sea, are replaced by oligochaete worms in fresh water. Oligochaetes, which do occur in the sea but to a lesser degree, are segmented and richly setate. However, they lack the lateral “feet” or parapodia of the polychaetes and generally have simpler head and feeding structures (Figure 18.20). Earthworms and the tubifex worms of the aquarium trade are well-known oligochaetes. Typical tubifex worms are burrowers feeding on bacteria and organic particles in the sediment. However,

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FIGURE 18.16 Two main types of marine polycheate worm deposit feeders. Selective surface feeders: (A) Cirratulus, (B) Amphitrite, in burrow, (C) ciliated tentacle, (D) with food transported, (E) tentacle bringing food to mouth, of Terebella, (F) Spio with two tentacles, and (G,H) Arenicola, burrower with extensible pharynx for nonselective feeding. All after Barnes (1987).

their posterior extremities, which are red due to an excess of respiratory pigment in the blood, extend up into the water from the often oxygen-poor bottom sediments. Insects, virtually absent from fully marine environments, are major elements in most fresh waters. Very conspicuous and abundant organisms of freshwater muddy bottoms, replacing many polychaete and bivalve members of marine soft bottoms, are chironomids, the midges or Tendipedidae (Figure 3.15). Flying adult midges form large mating clouds over ponds and lakes and do not feed. The eggs are laid in water and the larvae (Figure 18.21) can be directly herbivorous or filter feeding, depending on the species. However, many

chironomid larvae are deposit feeders. Some form tubes like many polychaetes in the marine environment, and others are naked. These typically highly abundant and diverse forms are an important food source for other aquatic insects and for fish. A freshwater microcosm or aquarium that is open even occasionally to the outdoors will certainly develop a midge fauna, and modelers of freshwater systems should be familiar with The Chironomidae by Armitage et al. (1995). In our Chesapeake Bay and Everglades mesocosms, the chironomids are permanent and important members of the fauna. Like amphipods in salt and brackish waters, they also are nuisance micrograzers on algal scrubbers, as we discussed in Chapter 11.

Detritus and its Role in Model Ecosystems

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CARNIVORES AND THE DETRITIVORE COMMUNITY Like any complete community, the detritivore-based soft bottom has its higher level predators. Of course, animals basically external to the community, such as bottom-feeding fish, birds, and large roving crustacea such as crabs and lobsters, easily come to mind. However, there are also many carnivores at all levels from protozoa to arthropods that are integral elements of the soft bottom. Note that almost one quarter of the Delaware Bay soft-bottom community discussed above (Table 18.4) consisted of carnivores. These generally smaller predators also become prey to the top carnivores that are

external to the community. Carnivores in general were discussed in Chapter 16.

DETRITUS AND ITS ROLE IN MODEL ECOSYSTEMS In all of our microcosms, mesocosms, and aquaria we have included moderate-sized soft-bottom communities; some of these systems have been dominated by soft bottoms. It has been assumed in the past, based on whole system function, that these greatly increase the diversity and the stability of the ecosystem being modeled. More recent research, some with microcosms,

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FIGURE 18.17 Deposit-feeding bivalves. Here, respiration with water flow over gills and feeding are separate. Ciliated palps or tentacles carry out the feeding function. (A) Nucula, (B) generalized feeding, respiration process, (C) Yoldia, and (D) Nuculana; ciliary action on palp. All after Barnes (1987).


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FIGURE 18.18 Deposit-feeding crustacea: (A) isopods, Cyathura and Idotea, (B) burrowing amphipods, Haustorius and Gammarus, and (C) tube-building amphipods, Leptocheiris and Jassa. From A Field Guide to the Atlantic Seashore by Kenneth L. Gosner. Copyright © 1978 by Kenneth L. Gosner. Reprinted by permission of Houghton Mifflin Co., all rights reserved.

has shown that there is indeed a positive relationship between biogeochemical exchange (between the sediment and the water column) and biodiversity (Waldbusser et al., 2004). In addition, the often assumed homogeneity of detrital bottoms, is simply not correct, a wide range of physical and biological factors leading to bottom heterogeneity and therefore increased biodiversity, are in play and these must be

considered in the modeling process (Zajac et al., 2003). While a variety of these systems are described in detail in Chapters 20–23, we briefly refer here to the detrital aspects of several of these model communities. Finally, we discuss in depth the more traditional approaches to the handling of fine organic sediment in aquaria, and we relate these to the methods that we describe below.

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FIGURE 18.20 Freshwater oligochaete annelid worm, Aeolosoma. Note relatively simple head and structure, lack of parapodia but abundant setae. After Barnes (1987).

FIGURE 18.19 Deposit-feeding echinoderms: (A) heart urchins and (B) sea cucumbers. After Campbell (1976).

Detritus and Coral Reef Microcosms A large part of the waste organic material of reef communities is repeatedly captured and utilized in midwater by fish and on the reef surface by many invertebrates including corals. Much of what is not utilized on a short time scale, along with the fine carbonate sediment generated by the boring and scraping of organisms, is carried either into deeper water on the fore reef or into the lagoon. Lagoons in particular as detrital ecosystems are rich food areas for some reef fish, such as grunts. In this case, the fish typically ingests a mouthful of sediment and works the sediments over its gills as a sieve to extract worms and other macrofauna, then “spits out” the remaining sediment through its mouth or gill slits. Often, to avoid predators such as jacks and barracuda, grunts in large schools “file off” a reef at night to work lagoon sediments. Some scientists feel that by this process, grunts can be critical in returning nutrients to the reef ecosystem. Since the normal processes of distant removal (down the drop off or into a broad lagoon) are not as effective in a microcosm or

aquarium situation, a rich macrofauna of worms, constantly reworked by fish like grunts, is an essential component of the living reef aquarium. In addition to grunts, most reef fish that are mid- to low-level invertebrate predators will search the surface of available sediment for the occasional worm or crustacean that exposes itself at the wrong time. With a very small lagoon in proportion to reef it is difficult to avoid overpredation of the detrital community. Isolated and partially isolated lagoons as refugia have provided partial solutions to this problem. As can be seen in Figure 20.1, and in Color Plate 31, a dense Thalassia bed has developed in the Smithsonian’s coral reef lagoon. This “grass” bed effectively traps further fine sediment, the surface of which is occupied by dozens of detritivore species, primarily crustaceans and polychaetes (Color Plate 32). One particularly conspicuous component of this model lagoon is the mysid shrimp that appear in clouds within a centimeter or two from the sediment surface. The fish and a spiny lobster constantly rework the detrital fauna. In reef microcosm and aquarium environments, where extremely low nutrient levels are generally needed, a newly stocked lagoon community may “out-well” at a higher rate than an established lagoon ecosystem. Thus, higher algal scrubbing capability may be required during stocking and early operation to avoid excess nutrients.


FIGURE 18.21 Larval stage of Chironomus (Tedipes): a: proleg; b: abdominal gills; and c: anal gills. After Pennak (1953). Reprinted by permission of John Wiley & Sons, Inc.

Generally, we have had few community structure difficulties in operating coral reef communities together with their soft-bottom lagoon counterparts. However, large parrot fish or tangs and some sea urchins, in the absence of higher predator controls, need to be avoided if a successful seagrass community is to be maintained. In the wild situation, lagoons are generally quite large in size in proportion to their reefs and are heavily patrolled by barracuda, jacks, and large trigger fish. Thus, heavy grazing is typically avoided, except perhaps occasionally by sea turtles. Just as for predators of detritivores, a semi-isolated lagoon (that is to say one with controlled access from the reef) will solve this scaling problem to some degree.

Detritus and Cold-Water Microcosms In the wild Maine coast ecosystem, a relatively small part of the rich kelp and rockweed production is grazed or browsed in place (on the order of 10–20%). In many areas, it builds up to a large biomass and then is torn

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off by winter storms and deposited as bermlike drifts along the upper shore. This algal food becomes a continuing store of energy for the entire ecosystem. It is gradually broken down by a variety of crustaceans (such as the amphipods Orchestia and Talorchestia), by protozoans, and by bacteria and fungi. Eventually, as fine organic particulates, this organic drift, now as part of the seawater soup, finds its way back into the quieter, more protected, inner coastal waters, from which it either settles out in deeper water or is delivered by the incoming tide to the mud flats and salt marshes at the heads of bays. These muddy areas, rich in organic sediment, provide food for a large diversity of deposit- and filter-feeding animals, which in turn become the feed for a wide variety of fish and other invertebrates. It is particularly interesting in Gouldsboro Bay, Maine, that even though the abundance of organic particulates in the silt to clay sediment gradually decrease in abundance seaward, away from the source, species diversity of the infauna increases. These inverse gradients are likely related to the extreme range of weather conditions. Landward the waters are relatively fresh in spring, quite warm in summer, rather saline in the fall, and intensely cold in winter. In any case, large numbers (hundreds to thousands per square meter) of individuals of these fewer species able to withstand the extreme conditions are available to constantly rework the rich energy source. We have built and operated a number of rocky Maine shore microcosms that included muddy deep bottoms and small mud flats. The largest of these is described in Chapter 21. This system has provisions for the equivalent of algal drift accumulation and breakdown. However, the fine particulates eventually collect at the base of the rocky shore, in the tidal reservoir, and in the semiseparated mud-flat tank. Although not as rich as the mud bottom of a Maine bay, these sediments contain numerous mollusc species (Hydrobia minuta, two Nucula species, Yoldia, and Macoma), several worms (Scoloplos fragilis, Ninoe nigripes, Cirratulus sp., Nereis sp., Lepidonotus sp., and Thelepus sp.), and a few amphipods (Corophium volutator and Ampelisca abdita). A rich fauna of protozoa and meiofaunal worms is also present (Table 21.10) to fill in the lower portions of the detrital food chain. At the other end of the food chain, a single green crab and several killifish constantly rework the sediment for the larger detritivores. It is particularly of note that although the muddy bottom in this model was stocked from the wild at a thickness of 40–60 cm, the relatively small scrubber is capable of driving nutrients (as N–NO2 ⫹ NO3) to levels below 1 µM. Nutrient levels can be raised for experimental purposes by manually disturbing the sediment, but otherwise, even with the extensive

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surface reworking by killifish, the green crab, and polychaete worms, nutrient release remains at an easily controllable level.

in all of these cases ambient nutrient concentrations in the water column remain at or below levels characteristic of the wild analogs.

Detritus and Estuarine Mesocosms

Detritus and the Aquarium

In the Chesapeake mesocosm (Chapter 22), just as in the Chesapeake Bay itself, large areas of fresh to salt marshes were present. Productivity in the marshes and other shallow-water areas of the system is very high and produces a dense growth of vascular plants and a surface coating of algae (aufwuchs or periphyton). A reduced seasonal cycle of light and temperature is operated in this system and in maturity, the yearly plant production was mostly allowed to break down within the mesocosm (10–20% is exported). Virtually all of this plant biomass was eventually deposited on the five sediment bottoms that dominate the unit. The deeper areas of the system, as well as in the tidal reservoirs, have detrital bottoms. The resulting sediments were richly organic, with a diversity of surface and infauna (not including bacteria) that exceeds 150 species including 66 protozoa, 7 rotifers, 22 annelids, 32 crustaceans, 24 molluscs, and 15 species from miscellaneous invertebrate phyla (see Table 22.3). Anaerobic conditions can be found with the probe of a finger into the fine sediment of this model, and the constant release of nutrients into the tank water would seem assured. Yet the waters of this mesocosm are constantly saturated or near saturated with oxygen, and the moderately high levels of nutrients entering the model with fresh tap water (simulating river input) are progressively reduced as this water works its way through the estuary. The Everglades mesocosm is similar in many ways to the Chesapeake model. Perhaps the most interesting additional characteristic of this subtropical system is the presence of mangrove communities, and the very dense and relatively diverse “grass bed” of the high salinity areas. The estuarine swamp building mangroves efficiently trap sediment and have their distinctive invertebrate elements, particularly the fiddler crabs (Uca species) and the coffee snail (Melampus coffeus). The mangroves themselves provide a constant rain of leaves, which along with the ubiquitous mat of algae provide the primary energy supply. Most important for all of the systems described above, fine particulates, organic and inorganic, are not filtered out. They are allowed to collect in the appropriate low-energy parts of the models, where they support, in some cases, macrophyte beds in addition to a rich microbe, protist, and invertebrate fauna. This protist and invertebrate fauna utilizes the energy in organic particulates to drive complex detrital communities. Yet,

The traditional bacteria filters of aquaria are being rapidly replaced by a wide variety of foam fractionating devices. These simple to complex units remove fine organic particulates and even some dissolved organics. As we have noted, they also remove reproductive stages and generally act like large filter feeders. They allow the aquarist the ability to place a much heavier organism load on the aquarium, since they function as a filter feeder passing thru and not leaving a metabolic load. Many aquarium procedures developed over the past several decades also include increased oxygenation and pH control by a variety of trickling filters, increased light for photosynthesis, and possibly even a denitrification filter. In these cases whether a foam fractionation device is included or not, organic particulates are still delivered to a wide variety of trapping (filtering) devices where primarily bacteria and to a lesser extent fungi and protozoans are expected to process all organics to carbon dioxide, water, and nutrients. Thus, the filter is equivalent to the detrital communities of wild ecosystems. However, as we discussed above, free-living bacteria, while extremely abundant in numbers, typically are a minor biomass element on most active and fully viable soft bottoms. The filter process prevents the development of a full detrital-based food web with its host of invertebrates. It also prevents the “kicking upstairs” of a considerable part of the energy supply to the fish and larger invertebrates that would normally feed on the community and continually rework the organics to full degradation. Also, as we discussed in depth in Chapter 11, complete bacterial processing of detrital organics in the aquatic environment without full return to plant biomass (the algal turf scrubber or similar system) reduces water quality and does not allow the export of nutrients to match food input. For many communities to be simulated in microcosms and aquaria, it can be inconvenient to maintain a detritus-based soft-bottom community of proper proportion to the bottom feeders in the primary system of interest. When this is the case, the sediment is overworked and the detritus-based community of invertebrates is likely to be kept too low to properly process the organics. At the same time the sediment tends to be excessively thrown up into the water column without the extensive mucal binding that is characteristic of such communities when occupied by a myriad of invertebrates. The problem can be solved to some extent by including sediment

References

traps, with a detrital community refugia, within the piping system. This procedure allows the full development of a detrital community without the predation of larger organisms; the detrital community will then provide larval stages for the main system. While it is preferable to provide an appropriate interaction between the communities, this approach avoids an all-or-nothing situation and simulates a distant detrital bottom.

References Armitage, P., Cranston, P., and Pinder, L. (1995) The Chironomidae: The Biology and Ecology of Non-Biting Midges. Chapman and Hall, London. Barnes, H. (1987). Invertebrate Zoology, 5th edn. Saunders, Philadelphia. Campbell, A. (1976). The Seashore and Shallow Seas of Britain and Europe. Country Life Books, Feitham, England. Dix, N. and Webster, J. (1995) Fungal Ecology. Chapman and Hall, London. Gage, J. and Tyler, P. (1991) Deep Sea Biology: A Natural History of Organisms at the Deep Sea Floor. Cambridge University Press, Cambridge. Gosner, K. (1978) A Field Guide to the Atlantic Seashore. Peterson Field Guide Series, Houghton Mifflin, Boston. Higgins, H. P. and Thiel, H. (1988) Introduction to the Study of Meiofauna. Smithsonian Press, Washington, DC. Levinton, J. (1982) Marine Ecology. Prentice-Hall, Englewood Cliffs, New Jersey. Lopez, C. (1988) Comparative ecology of the macro fauna of freshwater and marine muds. Limnol. Oceanogr. 33: 946–962.

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Mann, K. (1988) Production and use of detritus in various freshwater, estuarine and coastal marine ecosystems. Limnol. Oceanogr. 33: 910–930. Maurer, D., Watling, L., Leathan, W., and Kinner, P. (1979) Seasonal changes in feeding types of estuarine benthic invertebrates from Delaware Bay. J Exp. Marine Biol. Ecol. 36: 125–155. Newell, H. (1984) The biological role of detritus in the marine environment. In: Flows of Energy and Materials in Marine Ecosystems: Theory and Practice. NATO Conference Series 4, Marine Science 13. Plenum Press, New York. Nixon, S. (1989) Physical energy inputs and the comparative ecology of lake and marine ecosystems. Limnol. Oceanogr. 33: 1005–1025. Pennak, H. (1953) Fresh Water Invertebrates of the United States. Ronald Press, New York. Rheinheimer, C. (1985) Aquatic Microbiology, 3rd edn. Wiley, New York. Seibold, E. and Berger, W. (1993) The Sea Floor: An Introduction to Marine Geology. Springer–Verlag, Berlin. Shipp, C., Staples, S., and Adey, W. (1985) Geomorphic trends in a glaciated coastal bay: a model for the Maine coast. Smithsonian Contrib. Marine Sci. 25: 1–76. Van Dover, C-L. (2000) The Ecology of Deep-Sea Hydrothermal Vents. Princeton University Press, Princeton, New Jersey. Waldbusser, G., Marinelli, R., Whitlatch, R., and Visscher, P. (2004) The effect of biodiversity on biogeochemistry of coastal marine sediments. Limnol. Oceanogr. 49: 1482–1492. Whitlach, R. (1980) Patterns of resource utilization and coexistence in marine intertidal deposit-feeding communities. J. Marine. Res. 38: 743–765. Willoughby, L. (1976) Freshwater Biology. Kluwer Academic Publishers, Norwell, Massachusetts. Zajac, R., Lewis, R., Poppe, L. P., Twichell, D., Vozarik, J., and DiGiacomo-Cohen, M. (2003) Responses of infaunal populations to benthoscape structure and the potential importance of transition zones. Limnol. Oceanogr. 48: 829–842.


C H A P T E R

19 Symbionts and Other Feeders

All eukaryotes appear to be derived from the same root-set of bacteria and thus genetically are from the same stock (or at least two closely related stocks). Eukaryote cells have a variety of membrane-based organelles, including plastids and mitochondria, with their own DNA or RNA, and it is thought that these represent the “capture” or possibly originally the parasitism, of bacteria by more advanced cells. We now know that genes are mobile, flowing frequently between bacteria, but can even be transferred between higher animals by bacteria and viruses. Thus, it should be no surprise that innumerable intimate relations have developed between members of different species of plants and animals. These relationships can be as occasional as the grapsis crab that frequently finds protection from marauding fish by hiding beneath the long-spined sea urchin Diadema. They can be a whole way of independent life such as the cleaner wrasse that removes parasites from many different species of willing fish. Or they can be as fixed and complex as the parasite that must have several specific hosts to complete its life cycle. Symbiosis is a term meant to include all of these, as well as mutualism, where both parties benefit; commensalism, where one species benefits and the relationship is of no consequence to the other species; and parasitism, where one species benefits and the other is harmed. Parasitism is arbitrarily and with some difficulty separated from predation. It is generally accepted that a parasite is smaller and more numerous than its host. Also, the parasite consumes only a small part of the host. However, if that part is critical, or if other predators or parasites are introduced as a result, the death of the host can result. Until recently, symbiosis was regarded as a biological curiosity (mutualism) or a serious and sometimes correctable problem (parasitism), but not a centerline factor of organic evolution. In recent years, it has come to be recognized that symbiosis, or the joining together of

separate organic lines, is a major factor in evolution (see e.g. Smith and Douglas, 1987). Many cellular organelles, even the plastids that allow algae and the green plants that dominate the Earth to carry out their principal functions, were probably originally acquired through symbiosis. Of the thousands of interspecies relationships that can be called symbiotic, many do not involve feeding directly (Figure 19.1). Since the focus of our biological discussion for ecosystem modeling is based on feeding or trophic structure, we do not discuss nonfeeding symbioses in depth. However, nonfeeding symbiotic behavior can be extremely important to the structuring and efficient operation of model ecosystems. It is worthwhile for the aquarist to collect as much natural history information as possible for each species of moderate to larger size so that such adaptations can be allowed. Also, tremendously varied basic feeding symbiotic relations are described in the literature and would be of interest in specific modeling situations. The many cases of anemones and hydrozoans that inhabit the surfaces of snail shells are an example. However, our primary interests in this chapter, because they are so directly important to living ecosystem modeling, are plant–animal mutualism directly involving photosynthesis and parasitism.

ZOOXANTHELLAE AND THEIR ANIMAL HOSTS Cells from a number of major algal groups are known to occur symbiotically in the tissues of animal hosts. By far the most common are dinoflagellates, which occur in a wide variety of invertebrate phyla in the sea and are called zooxanthellae. The dinoflagellates have generally been placed in a “super genus and species” Symbiodinium microadriaticum, though probably several taxa

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19. Symbionts and Other Feeders

FIGURE 19.1 Commensal organisms living within the burrow of the echiurid (annelid) worm Urechis caupo. After Thurman and Webber (1984). Copyright © 1984 by Scott, Foresman and Company. Reprinted by permission of HarperCollins Publishers.

are involved. Cultured algal cells taken from coral hosts have been repeatedly seen to develop the unique dinoflagellate, double flagella, and girdlelike sulcus form that unmistakably place them in this group. Presumably it is also in this form that they migrate from host to host, although most vegetative biomass production occurs in the host by cell division. Flagellated zooxanthellae obtain access to their host through the mouth and stomach cavity, from which they enter the tissue lining the stomach. From there, they move to the cells of the tissues allocated for photosynthesis, dividing vegetatively until they reach a density tolerated by the host. Other phyla, genera, and species of algal protists can perform this same role for other invertebrate hosts (Figure 19.2). The host is capable of ejecting the algae in some situations, usually those involving stressful conditions. Over the last decade, this process has been occurring widely around tropical seas, usually associated with excess water temperatures (Knowlton, 2001). Unfortunately, while sometimes corals re-acquire the zooxanthellae, often they die when the zooxanthellae are lost; great concern exists that we may be seeing the early states of extinction of some coral species because of this process. A major part of the chemical production of zooxanthellae photosynthesis, often greater than 50%, is released to the host typically in the form of glycerol (SpencerDavies, 1984) (Figure 19.3). It has been shown that this same release of glycerol to the medium can be also

achieved in algal culture, but only when some of the host’s tissues are present (Bold and Wynne, 1985). The proportion of energy acquired by the host from their zooxanthellae varies widely. In some cases the mutualism pair is functioning basically as a plant, with the host carrying out some small but critical predation providing nutrient needs; this is similar to what happens with carnivorous land plants such as the Venus flytrap. Also, as we discuss below, photosynthesis and calcification are mutually supporting processes. To an animal whose ability to rapidly lay down a calcium carbonate skeleton is critical to survival, a symbiotic association with an alga, provided with light and nutrients for rapid photosynthesis, can be greatly supportive of success and survival. In addition, it is clear from Figure 19.3, and from consideration of the ecology of coral reefs (see Adey, 1998) that continual addition of biomass (as different from calcification) is not possible. Thus, there are major losses of chemical energy in the form of slime of mucilage production. This probably serves an additional and significant protective function. It is clear what the invertebrate host gains from this symbiotic arrangement: food, easier calcification, protection by slime release or all three. The benefit to the alga is a little less obvious. Such relationships are considerably more common in nutrient-poor tropical seas, and the driving process from the algal point of view is generally ascribed to the elevated nutrient supply, gained

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Zooxanthellae and their Animal Hosts

FIGURE 19.2 Algal cells (Chlorella) growing within the cells of the freshwater hydrozoan Hydra. From Smith and Douglas (1987). TABLE 19.1 Tabulation of Data on Productivity of Primary Types of Plants Growing on Coral Reefs* Plant community

FIGURE 19.3 Twenty-four-hour energy budget of a stony coral; energy equivalents in joules (J). The dashed line represents transferring of chemical energy from algae to coral. After Spencer-Davies (1984).

from animals captured and digested by the host. Protection from grazers and ultraviolet (UV) light is perhaps an additional incentive. While some scientists have suggested that these algae would be unable to make it in the typically high-UV, nutrient-poor reef environment, most coral reefs are rich in an algal turf that provides on the order of half to three-quarters of reef plant production (Table 19.1). Also, Gambierdiscus toxicus, an epiphytic dinoflagellate, is often abundant enough in reef environments to effectively poison the upper levels of the food chain with its toxins (Lobel et al., 1988). Perhaps the zooxanthellae can be regarded as being

Benthic macroalgae Benthic turf algae Zooxanthellae Sand algae Phytoplankton Seagrasses Total

Range cover Productivity on reef (g/cm2/day) communities (%)

Typical contribution to productivity (%)

0.1–4 (2)

0.1–5

4

1–6 (5)

10–50

45

0.6 (0.6) 0.1–0.5 (0.2) 0.1–0.5 (0.3) 1–7 (5)

10–50 10–50 10–50 0–40

4 0.7 0.5 45 99.2

*Note that on the average, the productivity of zooxanthellae in corals and other animals is not the major component, and turf algae and seagrasses are both dominant. After Larkum (1983).

related to their hosts in the same way that cows and pigs relate to humans. The price can be high for the individual, but as far as the genome is concerned reproduction is consistently successful. In the end that is the key element for the success of all biological systems.

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FIGURE 19.4 Longitudinal section of a stony coral showing the polyps, connecting tissue, and carbonate skeleton (black). After Barnes (1987).

FIGURE 19.5 Nematocysts of coelenterates (in this case the freshwater hydroid Hydra): (A) undischarged (within a coelenterate ectoderm); (B,C) discharged. After Borradaile and Potts (1958).

BIOLOGY AND ECOLOGY OF CORALS Corals are coelenterates or cnidarians that are often predators, particularly on plankton and small fish and invertebrates. These animals were not discussed in Chapter 16 or 17 because so many have zooxanthellae

and are thus a plant–animal symbiotic mix. Coelenterates are simple, radially oriented animals with tentacles, a mouth, and only a single entrance to the gut (Figure 19.4). They are also characterized by stinging cells, or cnidoblasts (Figure 19.5), that are used to stun prey and provide protection. Coelenterates include three major

Biology and Ecology of Corals

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FIGURE 19.6 Polyps and flexible proteinaceous skeleton of a generalized octocoral. After Barnes (1987).

groups: the hydrozoans, the scyphozoans, and the anthozoans. The hydrozoans have only a few calcareous members that have zooxanthellae, the fire coral, for example, and the scyphozoans are primarily jellyfish. It is the last group that concerns us here as it includes sea anenomes, gorgonians, soft corals, and the stony corals, most of which have zooxanthellae. The basic structure of the gorgonians is shown in Figure 19.6. While these animals are mostly colonial and have carbonate and proteinaceous skeleta, the individual polyps are little different from their coral and anemone cousins. It has been demonstrated that some octocorals do not feed and lack stinging cells. They rely totally on their zooxanthellae for their energy supply. Most stony corals require their zooxanthellae for continuous calcification, and it has been shown that calcification in sunlight exceeds that in the dark by 3–25 times (Goreau, 1961; see also Chapters 10 and 20). Indeed, it is well known that little coral growth and calcification occurs below 50 meters in depth and peak growth occurs at less than 20 meters in depth, primarily

due to the availability of light. Stony corals are major carbonate framework producers in reefs, with numerous other organisms providing the fill between the framework (see Smith, 1983). On the other hand, corals are probably only minor providers of photosynthetic energy to most reef ecosystems (Larkum, 1983; Adey and Steneck, 1985; Adey, 1998). Stony or scleractinian corals and the reef structure they create require low-nutrient, low-turbidity, warm tropical seas for their success. The extremely low-nutrient concentration normally associated with active, coraldominated reefs more typically relates to space competition with algae, which can easily outgrow corals given nutrients and freedom from intense grazing pressure. Relatively small disturbances, whether by hurricanes or humans, or diseases of keystone species, provide sediment and nutrients that smother corals and allow the more productive algae to grow over them (Hughes, 1989; McField, 2002). Given time, coral reefs may or may not recover from these destructive events (Cho and Woodley, 2002). Scleractinian corals live a precarious

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existence in nutrient-poor seas, balanced between grazing levels that keep their free-living algal competitors at low levels, and predation levels by reef fish and other invertebrates that are moderate. Stony corals have long been shown to be voracious predators themselves, particularly of plankton (Goreau et al., 1979). Although in many cases their need for food in terms of volume is probably low, it seems likely that many species are highly specialized in their planktonic food requirements. It is not only the stony corals (scleractinians) that harbor zooxanthellae and are important on coral reefs. Some clams, most notably the very large Tridacna, anemones, and a scattering of genera in many phyla, also keep algal “farms.” Gorgonians and soft corals, perhaps with calcareous spines but with a largely proteinaceous skeleton, are especially crucial ecologically. While these octocorals mostly provide little in the way of calcareous skeletal materials to a reef structure, they often provide a large element of surface heterogeneity and habitat for other organisms. Usually, octocorals are much more tolerant than stony corals of adverse environmental conditions, particularly including lower temperatures and light, increased turbidity, and nutrient levels. Also, most octocorals have developed chemical protection in the form of noxious compounds in their tissue, which make them unpalatable to all but the most specialized of animals, such as the flamingo tongue snail.

THE POSITIVE FEEDBACK LOOP BETWEEN PHOTOSYNTHESIS AND CALCIFICATION Many green algae calcify as well as photosynthesize, and in the well-known and abundant coral-atoll-forming genus Halimeda photosynthesis and calcification have been directly linked (Borowitzka, 1987). In the intercellular spaces created by the chloroplast-filled utricles, near the surface of the lobes, CO2 is rapidly removed during photosynthesis, creating abundant carbonate (CO32) ions and (see Figure 10.3) shifting the pH to higher levels and raising the concentration of carbonate. With calcium nucleation sites present on the outside of the utricles, and abundant available calcium, rapid formation of calcium carbonate crystals, as aragonite, occurs. Although reef-forming stony corals have zooxanthellae and are capable of photosynthesis, the sites of calcification and photosynthesis are separated anatomically. Thus it seems that the simple, photosynthetically mediated calcification mechanism described for Halimeda cannot be a significant generator of calcium carbonate. McConnaughey (1994) proposed a related mechanism called transcalcification in which the cells on the basal disc of stony corals “pump” calcium ions onto the

skeletal surface and concurrently remove protons (hydrogen ions, H). As shown in Figure 10.4, this raises the pH in the aqueous solution adjacent to the skeleton, uptaking CO2 and producing CO32. The concentrated calcium and carbonate ion combine on the surface of the elongate aragonite crystals to extend the crystals and effectively “lift up” the living coral polyp. CO2 migrates from the polyp’s tissues where it is continuously created by cellular respiration of sugars translocated from the zoothanthellae (as discussed above). The pumping of protons (H ions) into the intracellular spaces and the coral coelenteron lowers pH, producing CO2 from the abundantly available biocarbonate ion. Thus, the net effect above the calcification tissue is a continuous production of excess CO2. Allowed to accumulate, this would soon slow down calcification. The removal of CO2 from the coelenteron by the abundant zooxanthellae in the upper gut wall accelerates the process of calcification. Ultimately, as calcium and bicarbonate continuously migrate into the polyp, excess CO2 is created by the process of calcification. Thus, the presence of corals in a highly photosynthetic reef environment, where freeliving algae are rapidly removing CO2-producing tissue and continually losing carbon-rich fragments to the lagoon, prevents the damping of calcification by accumulation of the products of the reaction. Thus, the algal symbiosis in stony corals is not just an evolutionary device that internalizes energy and nutrient cycling, it also enhances both community calcification and photosynthesis. Effectively, stony corals capture calcium and bicarbonate (alkalinity) from the overflowing ocean water and convert it into accumulating calcium carbonate skeleta, releasing carbon dioxide. The released carbon dioxide is then taken up by the freeliving algae that are typically abundant on coral reefs. There is no net accumulation of biomass, by algae or corals, as this is lost by grazing and predation with subsequent outwash to the lagoon or deep ocean (Adey, 1998). Small and Adey (2001) and McConnaughey et al. (2000) demonstrate this process in a relatively small coral reef microcosm (see also Chapter 20). The process described refers primarily to the more rapidly growing reef-building corals, such as the acroporids, with a strategy of space competition. Similar to trees in a forest, they elect to continuously build supporting structures to compete for light with little if any accumulated biomass after maturity. There are certainly many species of stony corals with a more animal-oriented strategy for the capture of small invertebrates and plankton. For these species, algal symbiosis may relate more to their capability of producing abundant carbon-rich mucilage, primarily as a protective device.

Anthozoans and Microcosms, Mesocosms, and Aquaria

ANTHOZOANS AND MICROCOSMS, MESOCOSMS, AND AQUARIA The animals that we are considering here mostly have zooxanthellae and thus require light for photosynthesis. Kept in the dark, many corals and their cousins eject their zooxanthellae, turn white, and often do not survive. Species and individuals have zooxanthellae species that are adapted to certain light levels. Changing that light level, even in the wild, can place an animal under considerable stress, at least until it re-adapts perhaps even acquiring new zooxanthellae. When establishing a living ecosystem, it is important to know the approximate light level from which a colony was derived so that equivalent values can be simulated. Generally, if it is not possible to determine this, light-colored corals are usually from high light situations, less than 20 feet and greater than 700 µE/m2/s. Darker corals are usually found under less intense light. The spectrum of the light in most cases probably is not crucial, as long as it is a reasonably broad band. The accessory pigments of the zooxanthellae allow a broad range of light use, though certainly light in the yellow-orange band is of limited use (see Chapter 5 for detailed discussion). Some anemones are characteristic of highly turbid, high-nutrient waters, and provide little management difficulty in that respect. On the other hand, most gorgonians, soft corals, and stony corals require high-quality waters. It is our experience that gorgonians and soft corals have only moderate requirements. Some stony corals similarly have minimal requirements. For example, the small Astrangia danae occurs from Florida north on the east coast of North America to Cape Cod. It can even be found in the highly turbid lower reaches of Chesapeake Bay and is generally successful in our estuarine models. Although Astrangia calcifies and can make colonies as large as a football under the right conditions, it lacks zooxanthellae. On the other hand, most tropical stony corals are extremely sensitive to poor water quality in all respects, both in the wild and in model ecosystems. One rule of thumb, assuming light and turbidity levels are reasonable, is that nutrient levels, as measured by nitrite plus nitrate, must be below 2 µM for some species and below 1 µM for many species. It has been suggested that this low nutrient restriction does not apply to the stony corals themselves but rather relates to their competitive ability relative to free-living algae (Atkinson et al., 1995). It is well known that very rich wild reefs strongly disturbed by hurricanes can become densely algal coated, losing much of their live coral surface at least for many years. More recent, experimental work has shown a direct reduction of calcification by slightly elevated nutrients (Marubini and Davies, 1996). Extensive field work has also demonstrated a

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negative impact of elevated nutrients (Koop et al., 2001). Although long-term, large-geographic-scale synoptic evidence is lacking, there is concern among reef scientists that the stony corals of many wild reefs, particularly those in the Caribbean, are in a pattern of general degradation. However, there is no consensus as to whether this results from elevated temperatures, due to a greenhouse effect; greater UV, due to ozone degradation; lowered pH, due to increased carbon dioxide in the atmosphere, increased fishing pressure, or other factors such as organic pollutants. There is a tendency today to accept rising temperatures as the key issue in wild reef degradation (Hoegh-Guldberg, 2002) and as we describe in Chapter 20, we have seen that problem in our microcosms’ simulations. Using modern microcosm and mesocosm management techniques for high-quality waters, stony corals require the same basic ecological manipulation as other seashore invertebrates. They certainly have their predators and can be out-competed by algae in the absence of sufficient grazing or because of elevated nutrients. In some cases, particularly involving larger, fleshy polyps, plankton feeding can be critical and may have to be achieved by human intervention. Even if plankton-friendly pumps and Algal Turf Scrubber (ATS™) control systems are employed on a coral reef model, it is still necessary to provide the equivalent of open ocean plankton input. Many filter feeders will rely on this external source. For example, many reef fish have larvae that enter into the ocean plankton, often for many weeks. When they do reach a coral reef and settle, a large proportion are probably caught by corals. Most important, however, most stony corals must calcify (grow) and in some cases add some biomass to “stay ahead” of predators and competitors. Growth in stony corals requires some concern for temperature, salinity, light, etc., as we discuss in depth in Chapter 20. However, attention to calcium and alkalinity is also important, since these ions are continuously removed in the process of coral calcification. In addition, in a well-balanced reef aquarium, many organisms will be calcifying and a mean layer of 2–6 kg per year per square meter of calcium carbonate should be continuously laid on the bottom of the tank if it is to simulate a wild reef. In an appropriately calcifying 130-gallon reef tank, the water column calcium will need to be replaced about 7 times per year and the carbonate/ biocarbonate 60 times. Of course, neither will go to zero because of recycling from internal calcium and internal and external carbon (CO2). However, it does mean that carbonate can become seriously depleted, as can calcium (to a lesser extent) if it is not imported to balance (internal) calcification export to “geological storage” (Chapters 10 and 20).

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PARASITISM It is the nature of organic evolution that any opportunities to “make a living” will be followed. The potential availability of food energy in the form of a living organism will inevitably lead to predation and parasitism by other organisms, and in this discussion of parasitism in closed aquatic systems, we include pathogenic bacteria and protists. That is, not to say that macroparasites (a wide variety of worm species) are not important at the population level. While they are more likely to be sluggish “nuisance” factors rather than populationaltering elements, they can actually control population cycles (e.g. a nematode in British grouse, Thomas et al., 2005). In the broadest ecological sense, parasitism is not “bad.” That connotation is certainly a human addition to the biological equation. When a particular organism makes an evolutionary advance that allows its populations to greatly increase, the increase in numbers (because it makes the infection step easier) also renders the organism more susceptible to parasite expansion. Ecologically, the alternative is controlled by starvation or a runaway population increase of prey or host, which in the end is destructive of stable community structure. Humans have seen this process many times as we have transported organisms to places lacking their natural controls, such as rabbits and cactus to Australia. In both cases parasites had to be imported to keep the organisms from massively disrupting their new environments. Indeed, with the advance of modern medicine, in part removing or avoiding human parasites, we are witnessing an uncontrolled explosion of populations of Homo sapiens. This could be an ecological disaster, or on the other hand perhaps the balance has not been fully tipped and a series of human global epidemics are inevitable (Garrett, 1994; see Renaud et al., in Thomas et al., 2005). To further try to dispel the human tendency to regard parasites in a very negative light, perhaps even as “unnatural,” we point out that parasitism has played a very important role in evolution. Much of the complexity and abilities of higher plant and animal cells have derived from the “capture” of parasites, or a détente between parasite and host, and the use of these initially foreign bodies as organelles. Also, at the tissue and organism level, much of the complexity now seen has derived from adaptations and evolution in response to the incursions of parasites. One of the most brilliant of scholarly environmentalists, Rene Dubos, spent the early part of his career as a bacteriologist, searching for means of germ control and “tempt(ing) humanity with an edenic vision of a sanitized world” (Nash, 1989). Yet, he eventually concluded that “people and germs should coexist just like people and wolves.”

Thus, predators and parasites alike are important to balanced organic evolution. Parasites, by their nature, are closely associated with their hosts. The concomitant to an organism taking up the parasitic life, particularly an internal parasite, is the difficulty of meeting a sexual partner and then passing the results of reproduction on to another host. Pure distance and relative isolation of host make this process of infection more difficult. Unlike the more classical views of the role of at least microparasites in populations, it is now generally accepted that parasites can control population levels and can, perhaps incidentally, drive a population to extinction (Grenfell and Dobson, 1995). It is another conundrum of biological/ecological systems that large areas support large populations, high diversity, and long-term rapid evolution, concomitantly with abundant parasites. Small isolated areas support small, low-diversity populations, and relatively few parasites. Evolution can be rapid when introductions are made, and when those introductions are parasites the isolated ecosystem can be thrown into chaos for a short term (for an extensive human-based discussion of these matters, see McNeill, 1976). Model systems, by their relatively small nature, increase the likelihood of infection and of epidemics of parasites once a parasite has gained access. On the other hand, it is well known that in small isolated wild populations, parasites can fade out due to the even smaller genetic diversity and/or chance events. Also, most model ecosystems are isolated or semi-isolated from plant and animal populations of wild ecosystems. The operator potentially possesses the ability to prevent the initial access of parasites more definitively than is possible in the wild. Thus, either as an important modeling concern to achieve natural levels of parasitic loading, or as an esthetic concern as parasitized organisms may look or act poorly or even die, control of parasites becomes an important endeavor of the manager of model ecosystems. Whether human, animal, or plant health is at stake, reduction of disease in ecosystem models, which is in large part parasitism, is achieved by four general approaches: 1. Provision of a high-quality environment and balanced food that allow organisms to function in an unstressed state (some diseases result from poor physical or chemical environment or lack of proper nutrition and do not involve other organisms). Even where a parasite is involved, both the successful invasion of the host and a potential host/parasite détente relate to physical and chemical health and a fully intact immune system. 2. Provide each model ecosystem with the highest biodiversity possible concomitant with the wild system

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being modeled and the size of the model (S kAz ). Biodiversity and parasitism are negatively correlated, though in complex ways (Thomas et al., 2005). 3. Prevention of disease transmission. 4. Cure of the disease. Although we discuss all four approaches to disease control, it is the first two that we emphasize in this chapter. In general, as long as the basic issues discussed above are well understood, disease is normally only a minor issue in model ecosystem operation. That is not necessarily so in aquaculture (see Chapter 25) where individual species populations can be very high – but that is a reason for aquaculture water quality to be high and for systems to be closed.

ENVIRONMENT, GENERAL HEALTH, AND DISEASE Organisms are adapted in various ways to a wide variety of physical, chemical, and biological factors. Generally speaking, these parameters can be determined from the wild environment within which the organism is successful, remembering that the extremes of that environment are likely to be marginal for many species. Establishing an organism under conditions of relatively high or low temperature, salinity, pH, oxygen, etc. in unusual habitats, such as no cover or improper substrate, or under unusual biotic conditions, will place an organism under stress. Under these conditions, parasites that are only rarely successful in gaining entrance to the host, or perhaps are established but under equilibrium conditions with the host’s defenses, will become dangerous and perhaps lethal to the host. Likewise, any organism, plant or animal, has certain food or nutrient requirements. Poor health can result from inadequate diet or nutrient supply that will allow a parasite success where normal immune system defenses might otherwise be adequate. Providing an environment biotically and physically as close as possible to the wild will most likely avoid this problem as well (Yeaman, 1987). The imported productivity or food supply to simulate that from adjacent ecosystems in the wild necessarily leads to the need for a careful consideration of adequate artificial food supply in small model systems (see Chapters 5 and 6). The above points are crucial to operating ecosystems that are not controlled by parasites and pathogens. In summary, it is essential to maintain an environment more than just adequate for the organisms. If oxygen levels for a particular community are supersaturated in the wild for 8 hours per day, the bubbling of air in a model of that community cannot maintain a proper

environment. While bubbling of oxygen might suffice in this case, controlled plant photosynthesis offers a logical solution to this need as well as several concomitant requirements. In this context, our attempts to achieve environmental accuracy for a number of model ecosystems are described in Chapters 20–23.

BIODIVERSITY The primary focus of this book is veracity in the modeling of living ecosystems, and in the restoration, of damaged wild analog systems. While precision in physical and chemical parameters, often in synergy with the development of organism populations, provides the starting and developmental strategy, the end result is a maximizing of biodiversity within food webs. In Chapters 12 and 13, we present the rationale for determining what that biodiversity should be, and particularly in Chapters 20–23 and in summary in Chapter 26, we describe particular methodologies for achieving maximum biodiversity. By maximizing biodiversity, not only is ecosystem stability assured, when disease invades one or two species, but relative population numbers for any one species are kept low or moderate, thereby reducing chances for transmission. This inverse relationship between disease and biodiversity may be partly theoretical and complex (see Thomas et al., 2005), but in our experience, it is quite real.

QUARANTINE (PREVENTION OF TRANSMISSION) The transport and temporary storage of organisms destined for model ecosystems are highly stressful. If at all possible every effort should be taken to reduce the transportation stress by limiting damage in collection and by providing a proper environment en route. Nevertheless, the immune systems of all introduced organisms, particularly intermediate- and larger-sized organisms, are frequently in the process of collapse. Control of parasite injection into a model ecosystem can be handled by quarantine of the organisms in a separate quarantine tank for several weeks until diseases can become apparent. Since the transport is environmentally such a crucial time, it is essential, however, that the quarantine system be operated at a water quality that equals or exceeds that in the full model being attempted. Otherwise the quarantine process becomes a severe limitation instead of an advantage. We have found that no matter how high the water quality of freshwater systems, general quarantine is

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essential if outbreaks of disease are to be avoided. While this process is desirable for seawater ecosystems, considerable experience, on the part of the authors, in situations where quarantine could not be used for practical reasons suggests that this step can be omitted for saltwater systems with greater impurity. The reason for the apparent relative lack of parasite and pathogen effects in saltwater models is not known.

DISEASE TREATMENT IN MODEL ECOSYSTEMS Serious or epidemic disease in model ecosystems is best avoided by maintaining high-quality environments and by appropriate quarantine. Occasional nonepidemic disease probably cannot and should not be avoided. In some cases where considerable efforts to manage epidemic disease involving a particular species in an ecosystem model are not successful, it is best to allow both the species and its parasite to run to extinction. This happens in the wild and may be inevitable in a given environmental situation and in ecological patches. In a properly designed and diverse ecosystem, this should cause little problem with regard to overall operation. Diseases that do not result from deficiencies in the basic requirements of an organism can result from the effects of bacteria, fungi, viruses, protozoans, certain worms, particularly flatworms, nematodes, and some arthropods. Parasite species are especially common among the isopods, amphipods, and insects (in fresh water). Parasites occur in virtually all animal and plant groups, though those mentioned above have some taxa that are particularly successful in this mode of life. Transmission from host to host is a crucial problem for a parasite. In many cases, the host-to-host transmission is direct, with infectious stages airborne or with swimming stages in water. Penetration of the host can be direct, through body openings, gills, feeding, reproductive tract, etc. In many cases the life cycle is more complex, involving intermediate hosts. Elaborate double- or triple-stage life cycles involving transfer through several hosts also occur. These are usually tied to feeding patterns, with parasites such as mosquitoes introducing smaller parasites such as protozoans and worms that have already gone through a phase in the mosquito body. In many cases the infection is acquired through the digestive tract through feeding on an intermediate host such as a snail or worm. Almost all larger parasites can effectively and inadvertently introduce bacteria, fungi, and viruses to form secondary infections. We do not do an in-depth treatment of disease; the interested reader is referred to Olsen (1974) and Grenfell and Dobson (1995).

Diseases of Fish Humans have kept fish in culture for many centuries, and methods of treatment have developed for some of the most serious problems that are likely to be encountered. We refer the interested reader to several books: Spotte (1995) and Noga (2000). However, we add a note of caution to all planned treatment of organisms in living ecosystems. It may be extremely important to the aquarist to save a favored fish or group of fish that have contracted a disease. However, if treatment cannot be handled by isolation or physical removal, and chemical methods must by resorted to, rarely is a chemical specific to a single species of parasite. Protists and small invertebrates, in most cases, are critical elements of the model ecosystem and are likely to be negatively affected. Likewise, most bacteria and fungi, are essential to ecosystem function. Most chemical treatments especially antibiotics, copper, and formaldehyde must be scrupulously kept from the ecosystem itself. It is valuable to recall that the widespread human use of insecticides and herbicides in the wild environment has placed natural ecosystems and specific organisms in jeopardy numerous times. The classic story of DDT is a prime example, and it is suspected that we will see many more chronic examples of this kind of pollution of wild ecosystems. The recent worldwide concern for a potential catastrophic loss of amphibians probably lies with insecticides or herbicides. Diseases apparently are becoming widespread in the ocean. Fire in the Turtle House (Davidson, 2003) describes a good example of the problem in relation to sea turtles. The problem in that case could be global warming, eutrophication leading to red tides, man-made chemicals finding their way into the ocean or even just a moment in time that a specific disease vector (a virus) has exploded. However, the latter possibility seems unlikely given the widespread occurrence of similar phenomena, widely spread among taxa. This is probably an environmental issue, and until we can clean up our waters (which is still possible – see Chapter 25), it may be necessary to bring some species into protective culture. However, this must be done with “pristine” environments, and we can now accomplish that, even in a large enough scale to do sea turtles. Where parasitism must be dealt with in model ecosystems, biological methods should be used wherever possible. Use of cleaner fish or shrimp is helpful for ectoparasites in marine systems. Human removal of a pest by physical processes, using hand, needles, water jets, etc., can be valuable, though often time-consuming. As we describe in upcoming chapters, we have found that in wetlands ecosystems, control of insects on vegetation can be achieved by appropriate use of jets of

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References

water. It would appear that in the wild swamps, marshes, and mangroves of the Everglades or Chesapeake Bay, wind and rain are major limiters of insect depredations. The simple approach of simulating a thunderstorm every week or so avoids serious insect predation. This is all the more interesting in that in the production greenhouse adjacent to the Everglades mesocosm (Chapter 22), extensive and repeated applications of highly toxic insecticides are employed as a routine element of management. Although we have lost relatively few plant species in the adjacent Everglades mesocosm, a high level of survival, especially that of key species, has been achieved without resort to insecticides.

Diseases of Stony Corals In recent years, ecologists have begun to notice numerous stony coral diseases in wild reefs. Whether these are just being recognized as scientists are able to study reef ecosystems in greater depth or whether disease incidence is expanding due to increasing reef stress is unknown. Black band disease (BBD, Phormidiumcoralyticum, a blue-green alga or cyanobacterium) has been a subject of considerable recent research, although some studies have suggested that BBD is not a single taxon but rather several different but related species (Frias-Lopez et al., 2003). Other studies have shown the additional involvement of other bacteria (Richardson and Aronson, 2002). Other studies on wild reefs have indicated a statistically significant linkage to higher water temperature and to elevated nutrient concentrations (Kuta and Richardson, 2002; Jones et al., 2004). Depth may be a complicating factor. More recent work strongly links BBD with proximity to sewage effluent (Kaczmarsky et al., 2005). On wild coral reefs, BBD causes die back at the bases of colonies, especially those of head corals. This coral tissue loses its zooxanthellae and then is colonized or parasitized by the black-appearing cyanobacteria, creating the “black band.” It can “cause” the death of entire colonies or can come and go, its extended presence usually being associated with higher temperatures or nutrient levels. BBD has been present in some of our reef models over the years. Generally occurring on only a few colonies of many in a microcosm or mesocosm, its resulting effects often relate to growth (i.e. calcification) rates of the colonies. When growth rates are rapid, die back at the base balances or does not keep up with growth at the tip, creating a tissue to skeleton ratio that is typical for the wild. In some cases, we have noted that where the effects of BBD on a single colony appear to be slowly diminishing the living tissue (and this is almost

always when most or all other colonies in the system show no presence of BBD) simply scraping off the “black band” and moving the colony elsewhere in the system reverses or apparently “removes” the disease. However, it is likely to return at some future time. The microcosm systems in which BBD has been most prevalent have been those units most afflicted with high-temperature events, spiking above 29–30°C (Chapter 20). We treat BBD as an endemic element (see e.g. McNeill, 1976), similar to the common cold, mumps, or chicken pox in modern human populations. It is part of the natural function of a coral reef system, to be of concern and adjusted only if it is epidemic and in the long term significantly reducing coral biomass tissue. When it appears in any abundance in a model system, we suggest looking at the possibility of temperature spikes at some unattended part of the day and examining calcium concentration and alkalinity. As Adey (1998) and Small and Adey (2001) discuss, continuous long-term calcification is necessary for corals in a reef ecosystem, even though long-term increasing biomass is not possible or desirable. To some extent, basal die back of coral tissue must be a normal response to low nutrients and nutrient transfer. Much black band “disease” may be an incidental bacterial occupation of naturally necrotic tissue. Another coral disease (WBD, white band disease), more specifically related to Acropora species of corals, is more mysterious. Some authors have linked it to the bacterium Vibrio carchariae (Richardson and Aronson, 2002). However, it could be that the bacteria become involved, in a saprophytic fashion after the tissue has become necrotic. It may be that more basic multifactorial environmental problems disrupting growth and nutrient transfer produce the initial tissue necrosis. In any case, it is generally recognized to be, along with bleaching, a very serious problem leading to broad-scale decline of coral reefs (Bruckner and Hourigan, 2002).

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Larkum, A. (1983) The primary productivity of plant communities on coral reefs. In: Perspectives on Coral Reefs. D. Barnes (Ed.). Australian Institute of Marine Sciences, Manuka, Australia. Lobel, P., Anderson, O., and Durand-Clement, M. (1988) Assessment of ciguatera dinoflagellate populations: sample variability and algal substrate selections. Biol. Bull. 175: 94–101. Marubini, F. and Davis, P. (1996) Nitrate increases zooanthellae population density and reduces skeletogenesis in corals. Mar. Biol. 127: 319–328. McConnaughey, T. (1994) Calcification, photosynthesis and global carbon cycles. Bull. I’lnstit. Ocean. Monaco 13(spec.): 137–161. McConnaughey, T., Adey, W., and Small, A. (2000) Community and environmental influences on coral reef calcification. Limnol. Oceanogr. 45: 1667–1671. McField, M. (2002) Influence of disturbance on coral reef community structure in Belize. Proc. 9th Int. Coral Reef Sym. 2000 (1): 63–68. McNeill, W. (1976) Plagues and Peoples. Doubleday, New York. Nash, R. F. (1989) The Rights of Nature. University of Wisconsin Press, Madison. Noga, E. (2000) Fish Diseases: Diagnosis and Treatment. Blackwell Prof. Publ. Olsen, O. W. (1974) Animal Parasites: Their Life Cycles and Ecology. University Park Press, Baltimore. Richardson, L. and Aronson, R. (2002) Infectious diseases of reef corals. Proc. 9th Int. Coral Reef Sym. 1: 1225–1230. Small, A. and Adey, W. (2001) Reef corals, zooxanthellae and freeliving algae: a microcosm study that demonstrates synergy between. Ecol. Eng. 16: 443–447. Smith, D. C. and Douglas, A. E. (1987) The Biology of Symbiosis. Edward Arnold, Baltimore. Smith, S. (1983) Coral reef calcification. In: Perspectives on Coral Reefs. O. Barnes (Ed.). Australian Institute of Marine Sciences, Manuka, Australia. Spencer-Davies, P. (1984) The role of zooxanthellae in the nutritional energy requirements of Pocillopora eydouxi. Coral Reef. 2: 181–186. Spotte, S. (1995) Marine Aquarium Keeping: The Science, Animals and Art. Wiley, New York. Thomas, F., Renaud, F., and Guegan, J.-F. (2005) Parasitism and Ecosytems. Oxford University Press. Thurman, H. and Webber, H. (1984) Marine Biology. Merrill Publishing, Columbus, Ohio. Yeaman, M. (1987) Aquarium microbiology. Freshwater Mar. Aquarium 10(9): 37–43.

P A R T

IV ECOLOGICAL SYSTEMS IN MICROCOSMS, MESOCOSMS, AND AQUARIA


C H A P T E R

20 Models of Coral Reef Ecosystems

Coral reefs are large, generally spatially complex, calcium and magnesium carbonate structures formed by tropical, shallow-water communities of plants and animals. They occur in clear, very-low nutrient, highsalinity waters of moderate to intense wave action, and they are dominated and built primarily by stony corals and/or calcareous algae (Birkeland, 1997; Adey, 1998), though other invertebrates can also provide some calcium carbonate (see Chapter 10). Where such reefs are algal-dominated (by crustose corallines) and extend near or above the water surface, especially on shores with strong and constant wave action, they are sometimes called algal ridges (Adey, 1978a,b; Littler et al., 1996). Seen in section, as demonstrated by many core drillings, only a narrow vertical wall consists of coral or coralline framework. Much of a typical reef structure consists of carbonate debris provided by framework destruction and by algal and foraminiferal carbonate granules. Large-scale calcareous reef structures, such as atolls and barrier reefs, are constructed in large part by the calcified discs of species of the calcareous green alga Halimeda growing on back reefs and in lagoons. Coral reefs and their lagoons are typically highly productive communities, due to the photosynthesis of abundant small algae (algal turfs), calcareous algae, seagrasses (in the lagoons), and the zooxanthellae algae of corals and other sedentary invertebrates (Adey and Steneck, 1985; Hatcher, 1997; Adey, 1998). Coral reefs are the most diverse ecosystems in the sea. Older estimates of species numbers in reefs of all tropical seas provided a total of about 1 million species, about 90% remaining undescribed (Reaka-Kudla, 1996). More recently, Small et al. (1998) and Small and Adey (2001), using the coral reef microcosm system described later in this chapter, derived an estimate of 2.6–3.0 M

species for pan-tropic coral reefs. A number of field studies currently under way further suggest that this estimate is conservative. While these numbers may seem a small fraction of the 10 million species sometimes cited for tropical rain forests, in terms of number per unit area (e.g. species per square kilometer), coral reefs are certainly the most diverse ecosystems on Earth. Unfortunately, the coral reef literature of the last decade has been dominated by descriptions of degradation and apparent impending coral reef ecosystem collapse (e.g. Knowlton, 2001); the last International Coral Reef Symposium, in 2000, provided numerous papers on the problem (e.g. Hoegh-Guldberg, 2002). The current scientific consensus appears to be that a threshold of stony coral tolerance to many, both global and local, negative factors, introduced by human activity, was passed in the 1980s. The coral reef literature of the 21st century, to the time of this writing, has been dominated by studies of the many interrelated factors contributing to ecosystem degradation: thermal and UV stress and coral bleaching due to climate and atmospheric change (Hoegh-Guldberg, 1999; Fitt et al., 2001); CO2 elevation and oceanic pH reduction (Pelejero et al., 2005); stony coral diseases (Jones et al., 2004); eutrophication (Koop et al., 2001; Kuta and Richardson, 2002); hurricanes (McField, 2002; Cho and Woodley, 2002); and trophic disruption due to overfishing and other factors (Szmant, 2001). What some scientists have predicted to be the first biome level extinction by human activity appears to be under way, and this is the framework in which this chapter has been revised from earlier editions. Some scientists feel that coral reefs can be restored, and a recent volume (Precht, 2006) is dedicated to that attempt. However, some of the major problems – temperature, pH, and probably disease – apply at the level of global

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restoration. Our approach is to first demonstrate that coral reef ecosystems can be constructed as microcosms and mesocosms and then used as research tools to better understand coral reef function in terms of restoration; they can also be used as culture holding systems to manipulate organisms in the restoration process. In Chapter 24, we also discuss the pharmaceutical value of coral reef mesocosms, a significant factor that might provide social and financial support to both local and global restoration. Secondly, we feel that the global environmental problems leading to coral reef degradation can be corrected, and we discuss that process at length in Chapter 25.

MODELING CORAL REEF ECOSYSTEMS Although coral reefs were long considered to be very difficult to maintain in semi-closed culture systems, considerable progress has been made in the late decades of the 20th century in maintaining some species characteristic of coral reefs in aquaria. Bruce Carlson (1987) and Moe (1989) described the history of the various technologies involved. More recently, Delbeek and Sprung (1994; 2004) have described home and public aquarium systems with coral reef communities, and discussed the techniques required to maintain them. Strong lighting (metal halide or fluorescent lamps), often with actinic fluorescents to provide an esthetically desired blue color, are universal employed in the newer reef aquaria, and the water-quality control apparatus is a complex array of filters, the number and type of which varies from system to system. Perhaps the central methodology most in favor in reef aquaria at this writing is foam fractionation (protein skimming). A paper presented at the 1996 International Coral Reef Symposium in Panama described the “Scleractinian Challenge” (Brown, 1996), in which numerous coral fragments were shipped to a wide variety of aquarists for comparison of survivorship and growth. The extensive mortality (83%) and generally poor growth (though a few grew extensively) described in that paper suggest that at that time culture methodologies left room for considerable improvement. Delbeek and Sprung (2006) suggest that considerable improvement has been achieved, including the successful culture of some additional reef invertebrates and many fish. Indeed, there is a large scientific literature in the general field of marine biology in which many marine species, including coral reef species, have been brought through reproductive culture in the laboratory. Also, several hundred coral reef species (mostly fish) have received aquaculture level treatment, at least implying the possibility of routine production for ornamental (aquarium) use. This we

discuss further in Chapter 24. However, it is a vast leap from the laboratory culture, or even aquaculture production, of several hundred species to the construction of a functioning ecosystem. It is important to note that many of these aquarium systems, perhaps most (ecosystem descriptions were lacking), were established as “gardens” not ecosystems. Trophic balance was often lacking, and predation or algal overgrowth due to high nutrient levels and low grazing cannot be ruled out as major factors. Furthermore, virtually all were operated with filtration systems that remove most if not all of the key reproductive, planktonic components. As we will describe below, our efforts have been directed at modeling coral reef ecosystems, usually with a particular analog wild system as an example to work against. Many environmental factors are considered, monitored and managed, but our larger scale measure of success has been threefold: whole system calcification rate, the calcification rates of individual key species and whole system biodiversity. Calcification rates are central to coral reef modeling because this is what structures coral reef ecosystems. It is possible to have a coral reef community without a significant carbonate framework, but until that framework has developed, the ecosystem will be minimal because habitat is minimal. In this chapter we describe four different model coral reefs that we have been involved in constructing and maintaining at various times over the past 26 years. The first, a Caribbean reef ecosystem, is the 3000-gallon exhibit in the Smithsonian’s National Museum of Natural History and subsequently the Smithsonian’s Marine Laboratory at Fort Pierce, Florida. The Museum unit followed a series of smaller prototypes, and is the system from which many of the basic modeling techniques that we discuss in this book have evolved (Adey, 1983). The second is a very large, 800 000-gallon, IndoPacific reef built in 1986–1988 at Townsville, Australia, for the Great Barrier Reef Marine Park Authority. Finally, we describe in considerable detail a 130-gallon generalized reef ecosystem that we initially started in 1988 and then moved in the early 1990s to large quarters in a sun-room on the back of our garage, where it operated until 2000. This system had been maintained to tight physical/chemical tolerances for most of its life. Most important, it was never operated with impellor pumps for circulation, nor had it ever had filtration or foam fractionation. Except for a very few test stony corals, added to obtain calcification standards, this unit had remained closed to outside biotic introductions for over 7 years prior to the year-long, multi-disciplinary study of its function and biodiversity that we describe below. Though relatively small, this unit was an ecosystem by any measure; it contained well over 530 species that reproductively maintained their populations.

Caribbean Coral Reef Microcosm at the Museum of Natural History

CARIBBEAN CORAL REEF MICROCOSM AT THE MUSEUM OF NATURAL HISTORY In this section we describe the 3000-gallon (7 kiloliters) exhibit/research microcosm that was in operation at the Smithsonian Institution’s National Museum of Natural History for nearly 20 years. In 2000, it was moved to the Smithsonian’s Fort Pierce Laboratory in Florida, where it is still functioning today. It was the fourth closed reef system developed at the Marine Systems Laboratory. The earlier units were smaller prototypes. Its physical dimensions, arrangement, and morphology are shown in Figures 20.1 and 20.2. In this discussion we treat the unit as it operated from 1980 to about 1986, as that is when we had staff and students to collect data. The exhibit was rebuilt and reopened in 1991 using the same basic control systems, including the algal turf scrubbers (ATSs) (Luckett et al., 1996). It was possible to operate this system closer to physical/ temperature tolerances after its reopening.

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The shape and community structure of this microcosm reef were scaled after a typical Caribbean bank barrier reef, as were the light, wave energy, and current conditions. The critical physical/chemical variables and their relationship to an actual reef in St. Croix, Virgin Islands, are discussed below. The reef substructure contained within the Smithsonian microcosm was built from dead reef carbonate material (derived from storm berms behind Caribbean reefs) to simulate characteristic barrier reef configuration. This “reef” structure begins in deeper water in the fore reef, crests near the water surface, and drops to a shallow sandy lagoon behind. Considerable fine carbonate sediment was produced by boring and rasping of organisms on this reef. Both the seagrass-rich lagoon and the interstices of the rubblebuilt reef itself continuously collect this sediment. Thus, these two areas acted as geological storage systems (see Chapters 2 and 18) for both carbonate sediment and entrained organic particulates. This structure and process provided a basal framework to the model that is

FIGURE 20.1 Schematic diagram of the Caribbean coral reef and lagoon model opened at the Smithsonian Institution in October 1980. Scrubbers and refugia overlie the primary tanks; the wave generator appears at the far left. Drawing by Charlotte Roland.

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FIGURE 20.2 Plumbing/flow diagram of the Smithsonian coral reef model. This particular diagram is that of the last prototype system. It is quite similar to the exhibit model except that scrubbers and refugia were added.

very much the same as that found in the wild (Adey, 1978a). The rich benthic infauna occurring in this sediment (Color Plate 32) and the obvious bioturbation it produces, demonstrate the effectiveness of this sedimentation system. In this microcosm, the refugia (Figures 20.1 and 20.2) also contain sediment traps. Exchange water is removed from the traps along with entrained sediment and this allowed “geological export” from the model. In the prototypes, the sandy back-reef area developed the overgrazed and reworked aspect known as a reef halo. Thus, in the exhibit system described here, the lagoon was physically isolated by a pair of 5-inch pipes with 1/2-inch mesh screen. This separation was designed to simulate distance from the reef, an approach that allows controlled grazing and successful development of a lagoon community while maintaining the normal water flow and sediment relations between the reef and its lagoon. The microcosm described here would be more properly considered to be two attached ecosystems: reef and lagoon. The ocean or shelf ecosystem was not present but it was simulated by a wave generator and a bank of ATSs, as we discuss below. Living material to be transplanted to this microcosm was collected in the field and returned to the laboratory by air in insulated containers containing aeration equipment. This operation averaged 6–10 h from ocean to tank. The water contained within the tank microcosm was initially prepared with artificial sea salts but then exchanged with natural sea water at a rate of about 2 gallons/day (2% per month). During most of the operating time of this system, the sea water used for exchange was obtained from the outer coast of Virginia or Delaware. It was coarse-filtered in batch culture, and an algal culture was allowed to bloom; after several days,

each batch was diatom-filtered to scrub nutrients, but otherwise it was untreated. During later years, the tendency was to use commercial sea salts for the makeup media, since we no longer felt that near shore water was of adequate quality. On several occasions when we had access to appropriate research vessels, we were able to go 50 miles offshore to get our exchange water. The primary reason for this small water exchange is to avoid drift of salt composition. Salt loss occurs with evaporation, such salt being evident around the laboratory, particularly on the overhead beams, and was one of the primary reasons for the 1990–1991 reconstruction (along with delaminating glass and lack of temperature control). The wave action and current flow necessary for reef function were induced by eight centrifugal pumps totaling 140 gpm. These pumps removed water from the back reef and lagoon end of the tank and delivered it to a double-bucket “wave generator” in deeper water at the fore reef (Figure 20.2). The wave generator overturned every 10–15 s, spilling the contents into the tank. This flow, combined with that of several additional pumps that did not cycle through the wave generator, produced a mean current across the reef flat of approximately 3 cm/s. This was low compared to the mean flow rate of 10 cm/s found on the windward reef flats off St. Croix, but it is within the range of the more protected sections of that reef. The wave-induced flow is irregular and surgelike, back and forth (Chapter 2), and functioned to enhance organism/water contact, much as happens in an ATS (see Chapter 11). Wave reflection at the downstream (back reef) end of the reef tank was prevented by a boxlike “wave catcher” (Figure 20.3), which was a separate reservoir containing the intakes for the pumps supplying the


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FIGURE 20.3 Diagram of wave catcher and water-level damping and sensing systems on the Smithsonian coral reef.

wave maker. As the water was pumped from this enclosure, the level dropped, to be filled again as the next wave rolls across the tank and spilled into the open top. This mechanism was also a critical element in salinity control, since water level in the catcher was amplified in proportion to tank levels. The wide level of fluctuation with wave fall in the catcher was smoothed by a small siphon/reservoir device and the level was monitored by an electronic capacitance sensor that activated a peristaltic pump delivering distilled water to the tank. With this device, detection and replacement of as little as 50–100 milliliters of evaporated water at one time is possible. The procedure maintained salinity over a very narrow range on an hour-to-hour basis. Generally, it was maintained at 35.5–36.5 ppt, to match eastern Caribbean reef water, although on occasion it was allowed to fall as low as 34.8 ppt or to climb as high as 37.0 ppt for several weeks. Approximately 20 gallons/ day (80 liters) was evaporated from the entire reef/ lagoon system. Since such large volumes of replacement water are required, and Washington, DC, tap water at that time ranged from 120 to 180 µM for dissolved nitrogen (nitrite plus nitrate), high-quality deionized water was used for evaporative replacement. Clear, metal–halide vapor lamps (General Electric and Sylvania) proved satisfactory in intensity and spectral quality. Ten 1000-W lamps provided an irradiance over the 4.5 m2 area of the reef tank, which was approximately that measured in the field (Figure 20.4). In the back-reef section of the microcosm, light energy measured 500–900 µE/m2/s compared to 1100 µE/m2/s

recorded in the late spring at a depth of 1 meter on the reef flat at St. Croix. To compensate for the somewhat lower instantaneous energy, the light periods were expanded to bring total light energy input to comparable levels in the microcosm (Figure 20.5). In the reconstructed system, the newer 6000-K metal halide lamps were used, and this provided a significant improvement to the light spectrum and the color balance. Lamps lighting the main reef tanks were controlled by five separate circuits, and the illumination periods vary for each. Activation of circuits was sequential, operating over approximately a 2-h period, simulating in steplike fashion a changing intensity from dawn to midmorning and then again from late afternoon to dark. The crest area experienced the longest light period (16 h in summer), and the deepest areas experienced the shortest (14 h in summer). This effectively increased the depth-scaling factor. A summer–winter temperature cycle approximating that on St. Croix reefs was followed partly by adjusting the level of air conditioning in the tank room. A heat exchanger/refrigeration system was also used, particularly in late spring or during fluctuations in building air conditioning. Summer temperatures in the tank were between 27°C and 29°C, and usually followed a daily range of less than 1–1.5°C. The museum building is very old, and the temperature control often malfunctioned, especially when visitor density was very high. No mechanical or bacterial (“biological”) filtration, air bubbling, or chemical conditioning was incorporated into this system, nor has it ever been necessary to

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FIGURE 20.4 Light levels measured in ␮E/m2/s on the reef surface of the Smithsonian coral reef compared to light levels on a Bahamian reef at 14:00 h on a clear day in May.

FIGURE 20.5 Typical timing of the main tank lighting system on the Smithsonian coral reef.

use such methodology. During the daylight hours no conditioning was needed as extensive photosynthesis on the reef surface rendered ammonia unmeasurable by standard techniques and maintained oxygen at supersaturated levels. A bank of two to eight “ATSs” (see Chapter 11) maintained water quality during the dark hours. In this system, during the interval described, the number varied primarily in accordance with research projects that were under way. Dissolved oxygen concentrations as measured with a water-quality analyzer ranged from a minimum of 5.5–6.2 mg/liter in the early morning to a maximum of 7.5–8.3 mg/liter in the late afternoon. This diurnal pattern was close to that measured on a St. Croix reef flat with moderate wave action (Figure 8.9). The rate of change of oxygen concentration at morning and evening times of saturation was measured to determine utilization


at night and production during full illumination. This avoided the complex problem of oxygen exchange with the atmosphere. This approach indicated a gross primary productivity of 32.5 g O 2 /m2/day, which compared to 20–80 g O 2 /m2/day for back reefs and 18–20 g O 2 /m2/day for fore reefs as measured in St. Croix. Community respiration for the entire system is 0.9 g O 2 /m2/h. This compares to an average rate of 2.6 g O 2 /m2/h for St. Croix back-reef zones, and 0.7 g O 2 /m2/h for fore reefs. The tank measurements were taken without the ATSs attached. The pH was monitored primarily as a measure of the state of the carbonate system, particularly the concentration of CO2 in the tank water. The relationships among pH, photosynthesis, and calcification to some degree affects all calcifying reef organisms and is critical in the microcosm. The microcosm pH range was between 8.05 and 8.25, in accordance with a daily cycle that peaked at about 19:00 h from a minimum at 08:00 h. A bank of five to eight ATSs as described in detail in Chapter 11 was utilized to regulate nutrients, pH, and oxygen. Nutrient levels in the tank varied according to the import–export regime employed (i.e. the amount of algae removed compared to feed added). The primary variables measured were ammonia (NH3), nitrite (NO2⫺), nitrate (NO 23 ), and phosphate (PO 34), all of which showed diurnal cycles when levels were relatively high. At low 2⫺ concentrations, only N⫺NO⫺ 2 ⫹ NO3 showed a clear diurnal cycle, correlated with primary production. Nutrient levels typically ranged from 0.6 µM (0.008 ppm) to 1.5 µM (0.02 ppm) for dissolved nitrogen as nitrite plus nitrate. These are slightly above the average found in St. Croix, although well within its upper limits (see Figure 11.6). Plankton supplied to a wild reef system from the open ocean can account for only a small part of the energy utilized in the reef food web. The estimate for a St. Croix reef is less than 10%. Nevertheless, it is probably an important component for some filter-feeding animals. Live brine shrimp (Artemia salina) and dried krill are added to the microcosm to simulate this input. Approximately 0.5 g C /m2/day (9 g dry weight of feed) is introduced by this means compared to about 17 g C / m2/day from primary productivity (plant photosynthesis). This was gradually increased over the years and reached about 11 g (dry weight) of feed in later operation. In the original system, several additional sanctuary or refugium tanks were placed in the reef circulation (Figure 20.2). Due to reduced levels of predation on some species within the refugia, species diversity can thus be increased to levels equivalent to much larger areas under natural conditions. A number of plants and animals that cannot currently be kept in the main

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tank in any numbers due to predation function quite well in refugium tanks. The anemone Aiptasia pallida is a striking example, being virtually absent in the reef tank due to predation; it flourished in some refugia. During the period described (1980–1986), seasonal sampling in the fore- and back-reef areas in St. Croix yielded from 35 to 50 larger benthic algae. The reef microcosm contained at least 35 species identifiable at any one time (Table 20.1). The algal species that characterized the ATSs of this microcosm were shown in Table 11.2. A dense population of the turtle grass Thalassia testudinum had functioned in the associated reef lagoon throughout the life of this system (Williams and Adey, 1983). The community was moved as several blocks to the lagoon in the reconstructed system (when it was moved to Florida, it was about 17 years old). Flowering was first found toward the end of the first year and was a yearly feature in this lagoon. Mature blade length varied with time and the intensity of fish grazing and was generally well within the range encountered in the field. Under minimum grazing conditions, the blade length often greatly exceeded that typical for field conditions. Blade length, lifespan, and colonization rate increased markedly when browsing fish were introduced to remove epiphytes. The animal and protist community structure in the microcosm is perhaps not as complex as that found on a large natural reef. However, many major elements are present in the microcosm. Those tallied during the later 1980s are given in Tables 20.2–20.4. The vertebrate species (fish) of this system were subject to routine management. Disease was not significant, and fish that have suffered injury through accident or territorial defense often returned to health spontaneously if further predation did not occur. No quarantine procedures were used for the introduction of new fish, and on a number of occasions, fish apparently diseased when introduced returned to good health without medication. This disease-free pattern for fish did not carry over to the Fort Pierce system, where some problems have been encountered. There, however, exchange water has been derived from near shore coastal sea water and we suspect that is the source of pathogens. Behavior patterns for fish were quite similar to those in the wild. Feeding, territorial responses, and, at least in some cases, reproductive responses of fish paralleled those observed in the wild. The population included common grazers, scavengers, and invertebrate predators. In the system described here, higher vertebrate predators were largely excluded because of the depletion that would result in the absence of a large reef surface for feeding and an open-ocean pool for recruitment. However, for over 2 years a 12–15-inch-long barracuda was maintained

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TABLE 20.1 Plants Present in the Smithsonian Coral Reef and Lagoon Microcosma Kingdom Monera Cyanophycota Calothrix crustacea Oscillatoria submembranacea Schizothrix sp. Spirulina subsalsa Kingdom Plantae Subkingdom Thallobionta Division Rhodophycota Asterocytis ramosa Goniotrichum alsidii Acanthophora spicifera Bryothamnion seaforthii Centroceras clavulatum Ceramium corniculatum Ceramium fastigiatum Heterosiphonia secunda Laurencia papillosa Polysiphonia havanensis Spyridia sp. Botryocladia occidentalis Coelothrix irregularis Halymenia floresia Halymenia pseudofloresia Porolithon pachydermum Neogoniolithan solubile Lithothamnium ruptile Jania adherens Peysonnellia rubra Gelidiella trinitatensis Gracilaria cylindrica Gracilaria domingensis Gracilaria sp. Hypnea spinella Neoagardhiella ramosissima Soleria tenera Division Chromophycota (browns) Ectocarpus elachistaeformis Giffordia rallsiae Sphacelaria tribuloides

Chromophycota (continued) (diatoms) Nitzschia closterum Nitzschia dissipata Nitzschia leutzingiana Nitzschia longissima Nitzschia 2 spp. Opephora schwartzii Plagiogramma 2 spp. Surirella fastuosa Amphora 5 spp. Cocconeis placentula Cocconeis trachyderma Cocconeis sp. Fragillaria sp. Navicula varians Striatella sp. (dinoflagellates) Gymnodinium sp. Polykrikos schwartzii Division Chlorophycota Chaetomorpha geniculata Chaetmorpha gracilis Chaetomorpha fascicularis Chaetmorpha fuliginosa Valonia ventricosa Enteromorpha prolifera Pringsheimiella sp. Penicillus capitatus Udotea flabellum Bryopsis hypnoides Caulerpa cupressoides Caulerpo mexicana Derbesia vaucheriaeformis Halimeda incrassata Halimeda monile Halimeda opuntia Halimeda tuna Subkingdom Eumetazoa Thalassia testudinum (turtle grass)

a This survey was undertaken during the years 1985 and 1986. The system was about 5 years old at that time.

in the lagoon without significant predation on other fish. This higher predator was fed small goldfish daily, a basic procedure that has been used in several other reef microcosms. For example, by using appropriate added prey it was possible to maintain a rare reef lobster for nearly 10 years (see below), and, in another case, a banded tulip (carnivorous snail) for more than 5 years, in systems that otherwise function as largely closed ecosystems. Of particular interest was a school of striped parrot fish, Scarus inserti. Early in the development of the system, these fish were introduced as small juveniles and matured to assume the social structure characteristic of the species, including a single brightly colored terminal

TABLE 20.2 Benthic Protists Occurring in the Smithsonian Coral Reefa Subkingdom Protozoa Mastigophora (flagellates) Stephanopogon mobilensis Sarcodina (amoeboid types) Acanthamoeba sp. Allogromia sp. Gromia sp. Hyalodiscus sp. Mayorella sp. Actinophrys sp. Ameoba 2 spp. Hartmannela sp. Limax sp. Rotaliella sp. Ciliophora (ciliates) Acineta sp. Ascobius sp. Chilodonella sp. Cinetochilum marinum Condylosoma patens Diophyrus 3 spp. Euplotes 3 spp. Lagotia sp.

Ciliophora (continued) Loxophylum xp. Pleuronema sp. Sonderia sp. Strombidium 2 spp. Tracheloraphis sp. Urosoma sp. Vorticella sp. Actinotricha 3 spp. Aspidisca 3 spp. Ciliofaurea sp. Cohnilembus sp. Cyclidium sp. Dysteria 4 spp. Keranopsis rubra Lionotus 2 spp. Metafolliculina producta Prorodon sp. Stichotricha gracilis Trachelocerca sp. Uronychia transfuga Vorticella marina

a This survey was undertaken during the years 1985 and 1986. The system was about 5 years old at that time. Courtesy D. Spoon.

male and two heavily contrasted black-and-white dominant females, one dominating the fore reef and one the back reef. Also, several species of damselfish, including the beaugregory and the three-spot, had, at times, laid and fertilized egg clutches. These eggs were tended by the males and apparently hatched normally. After each clutch hatched, the larval stages could be found in the tank plankton for 12–24 h. No attempt was made to raise these larvae, and all were lost to either predation or the centrifugal pumps. The most conspicuous sessile animals of this exhibit system were the stony corals, gorgonians, and anemones. Of the 40–45 common hermatypic scleractinia of the Caribbean–West Indian area, 24 were originally introduced into the tank. Virtually all species survived for at least several months. Some species showed little or no growth and eventually shrank marginally. The relatively high density of damselfish may place extra stress on the slower growing species, which are often overgrown by dense filamentous algal growth propagated within the damsel territories. In most cases, this marginal pattern of shrinkage was prevented in the reconstructed system (the second half of the 20 years of operation) by preventing depletion of calcium and bicarbonate (see discussion below) and largely preventing high temperatures. Individual colonies of Acropora palmata, the dominant shallow-water reef builder in the eastern Caribbean,


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TABLE 20.3 Invertebrates Present in the Smithsonian Coral Reef and Lagoon Microcosma Kingdom Animalia Subkingdom Placozoa Trichoplax adherens Subkingdom Parazoa (porifera) Callyspongia sp. Chondrosia collectrix Clathria sp. Tethya sp. Chondrilla nucula Chondrosia sp. Monanchora barbadensis Subkingdom Eumetazoa Phylum Cnidaria (coelentrates) Class Anthozoa Aiptasia tagetes Condylactis gigantea Stoichactis helianthus Rhodactis sanctithomae Briareum abestinum Gorgonia flabellum Muricea sp. Plexaura flexuosa Pseudopterogorgia sp. Acropora palmatab Dendrogyra cylindricus Diploria clivosa Diploria strigosa Isophyllia sinuosa Montastrea annularis Mussa angulosa Porties asteroides Palythoa caribaeorum Bartholomea annulata Phymanthus crucifer Ricordea florida Eunicea mammosa Gorgonia ventalina

Phylum Cnidaria (continued) Muriceopsis sp. Plexaura homomalla Colpophyllia natans Dichocoenia stokesi Diploria labyrinthiformisb Eusmilia fastigiata Madracis mirabilis Montastrea cavernosa Mycetophyllia lamarckianab Porites porites Zoanthus sociatus Class Hydrozoa Staurocladia sp. Millepora alcicornis Millepora complanata Phylum Platyhelminthes Anaperus sp. Plagiostomum sp. Phylum Gastrotricha Macrodasys sp. Phylum Mollusca Class Gastropoda Astraea tecta Cittarium pica Coralliophila caribaea Murex sp. Bulla occidentalis Coraliophila abbreviata Cyphoma gibbosum Strombus gigas Class Pelecypoda Diodora sp. Lima scabra Isognomon sp.

Class Polyplacophora Chiton tuberculatus Phylum Annelida Class Polychaeta Eupolymnia nebulosa Sebellastarte magnifica Hermodice carunculata Spirobranchus giganteus Phylum Arthropoda Class Crustacea Artemia salinas unidentified demersal and harpacticoid sp. and larvae Amphithoe ramondi Alpheus armatus Mithrax sculptus Panulirus argus Stenopus hispidus unidentified gammaridean sp. Calcinus tibicen Mithrax spinosissimus Petrochirus diogenes Synalpheus brevicarpus Phylum Echinodermata Diadema antillarum (long-spined urchin) Eucidaris tribuloides (slate pencil urchin) Ophiuroid spp. Echinometra lucunter (red rock urchin) Astichopus multifidus (furry Sea Cucumber) Phylum Chordata Ascidiacean spp.

Planktonic invertebrates and protists Wave-breaking zone (fore reef) Zoomastiginids (flagellates) Abundant Hymenostomatid ciliates Common Vestibuliferid ciliates Common Cyclopoid copepods (some bearing Occasional eggs) Nematodes Occasional Copepod larvae (nauplii) Occasional Harpacticoid copepods Rare Over Thalassia bed (lagoon) Artemia larvae (nauplii) Abundant Nematodes (several spp.) Abundant Hymenostomatid ciliates (several spp.) Common Harpacticoid copepods Occasional Chaetonotid gastrotrichs Rare Foraminifera (several spp.) Rare Peritrich ciliates Rare a b

This survey was undertaken during the years 1985 and 1986. The system was about 5 years old at that time. Long-term element not present at the time of survey.

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TABLE 20.4 Fish Typically Present in the Smithsonian Coral Reef and Lagoon Microcosma Kingdom Animalia Subkingdom Eumetazoa Phylum Chordata Vertebrata Acanthurus bahianus (ocean surgeon fish) Acanthurus chirurgus (doctor fish) Acanthurus coeruleus (blue tang) Apogon maculatus (flamefish) Chaetodon capistratus (foureye butterflyfish) Amblycirrhitus pinos (red-spotted hawkfish) Thalassoma bifasciatum (bluehead wrasse) Acanthostracion polygonius (honeycomb cowfish) Holocanthus bermudensis (blue angelfish) Holocanthus ciliaris (queen angelfish) Chromis cyanea (blue chromis) Microspathodon chrysurus (yellowtail damselfish) Stegastes dorsopunicans (dusky damselfish) Stegastes planifrons (yellow damselfish) Eupomacentrus leucostictus (beau gregory) Haemulon flavolineatum (French grunt) Haemulon sciurus (bluestriped grunt) Sparisoma viride (spotlight parrotfish) Pareques acuminatus (cubbyu) a This survey was undertaken during the years 1985 and 1986. The system was about 5 years old at that time.

were kept in the system for more than 3 years at a time, growing at a rate of about 0.7 cm/month in spite of occasional predation by the crab Mithrax spinosissimus. This compares with 0.3–0.8 cm/month found by Gladfelter et al. (1977). The morphology of the new growth, however, resembled the short, bushy branches of Acropora prolifera, even though the original specimens had the typical bladelike appearance of A. palmata. Eventually, portions of colonies died suddenly after months or years of apparent good health, exhibiting symptoms of what has been called “white band” disease (Gladfelter et al., 1977). The true nature of this rapid death, a feature often present in natural reefs, is not known. Bacteria are present in the tissue after the zooxanthellae either die or are expelled. However, whether the bacteria cause tissue death or follow death has not been established (see also Chapter 19). However, “white band disease” has the appearances of a deficiency disease. In the 130-gallon coral reef system, discussed in depth below, this syndrome has been avoided by preventing calcium and bicarbonate depletion on a daily basis (rather than weekly or monthly). Damselfish, butterfly fish, bristle worm (Hermodice carunculata), and snail (Coralliophila; Brawley and Adey, 1982) predation with resultant algal colonization were recurrent problems for the stony corals in the earlier systems. In the later reefs these were not a significant issue.

As we discuss below for a 130-gallon system (and also specifically treat for calcification chemistry in Chapter 10), whole reefs and individual corals operate in a dynamic steady state of growth with calcification balanced against predation and bioerosion. Although living coral biomass (flesh) on any given wild or model reef may vary with time, long-term continued increase is not possible. Thus, over the long term, while biomass may remain more or less constant, buildup of calcium carbonate skeleta beneath the coral polyps continues (producing the coral reef structure). However, this general pattern implies a continual die back (or prey back) of coral margins, which is seen everywhere in healthy wild reefs. Thus, parasitism (see Chapter 19) and predation of stony corals is a normal feature of wild reefs and should be characteristic of captured (model) reefs. The key to long-term stability of coral reefs and coral colonies is coral calcification beneath the growing tips or surfaces. Several species of the hydrozoan Millepora were present in this exhibit system and were generally long lived, with considerable but sporadic growth. Octocorals, including species of Gorgonia, Eunicea, Pseudopterogorgia, Plexaura, and Briareum, as well as the zoanthid soft corals Zoanthus and Palythoa, were successful in the system and showed moderate growth. Many filter feeders and detritivores, including numerous sponges, mysid shrimps, amphipods, foraminifera, and worms, were abundant in cryptic environments, within the reef. Larger invertebrates that were successful in the microcosm were the lobster Panulirus argus and a variety of crabs, including Mithrax spp., Calcinus tibicen, Petrochirus diogenes, and the cleaner shrimp Stenopus hispidus. Young specimens of Panulirus grew rapidly and after molting four to five times eventually cause physical damage, particularly in the “uprooting” of uncemented carbonate. They were introduced as small specimens and then removed as adults a year or so later. The stomatopod Pseudosquilla was present since the earliest stages of tank development. Probably because of its predation, it was not possible to keep limpets in the reef tank for periods longer than a few months. The grazing gastropods Cittarium pica, generally in high-energy situations, especially on the reef crest and in the wave box, and Strombus gigas, the queen conch, in the lagoon, were particularly successful over many years. Numerous echinoids, including Eucidaris tribuloides, the slate pencil urchin, and particularly Diadema antillarum, were conspicuous nocturnal grazers. Like the lobster, the Diadema were placed in the system as young and removed after 1–2 years when overgrazing tended to become a problem. In the second decade of operation of this system, the same Diadema were not removed and never contracted the disease that ravished populations throughout the Caribbean. In addition, a wide variety of small annelids, copepods, isopods,

Great Barrier Reef Mesocosm

mysid shrimp, and ophiurid brittle stars could be found on close examination, particularly at night. Fish diversity of the microcosm seemed limited in relation to normal reef conditions: 21 species compared to a predicted 200 for the 23-mile-long St. Croix reef. However, in a study of patch reefs behind the Buck Island barrier in St. Croix, only 22 species were found to be consistently present. Chief elements of fish community structure in our microcosms were the same as those on the patch reefs, the primary missing elements being the higher predators, which normally patrol larger territories than contained within the tank microcosm. Although figures as to the size of the patch reefs were not available, they are probably considerably larger than the microcosm surface. In this microcosm many hundreds of species of algae and invertebrates were successful in terms of reproduction, settling, and growth to maturity. A few fish spawn successfully but hatchlings failed to reach maturity, in part the result of predation. However, it should be expected that a few individuals would have developed to maturity. Most reef fish have planktonic larvae that escape into the open ocean, returning to coastal reefs at a later stage of development. However, this reef and its prototypes were all operated with multiple impellor pumps. In some ATS-operated systems, fish hatchlings have been moved to refugia that are operated so that they do not pass through pumps. Several species have been brought to maturity by this means (see Chapter 24). Intensive study of this microcosm/exhibit tank microfauna by protozoologist Donald Spoon and his students demonstrated more than 80 species of protozoans and micrometazoans in the benthos. However, a close examination of the planktonic community of the unit at different periods over several years showed a quite depauperate biota. Scattered meroplankton (reproductive stages from the benthos) and especially scattered diatoms also out of the benthos shared the water column with abundant, very small (2–4 µm) yellowish, apparently uniflagellated phytoplankters. Technically, these are members of the ultra- or picoplankton, presumably Chrysophytes, and they provided a slight, barely visible yellowish cast to the water. A careful study of the 130-gallon reef system that lacked impellor pumps, described at the end of this chapter by the same specialist, showed none of these ultraplankters, and instead a considerably broader spectrum of diatoms, dinoflagellates and meroplankters. The water column lacked a yellow coloration. Our interpretation was that the impellor pumps were minimizing the larger plankters that would otherwise graze on these tiny Chrysophytes, which in turn were largely unaffected by passage through the pumps. At the time of these investigations we lacked access to an SEM and no further studies of

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the small flagellate were carried out. This is an example of top-down control of trophic structure; however, in this case it is the pumps that are acting as a predator.

CORAL REEF MICROCOSM AT THE SMITHSONIAN MARINE STATION For the move of this system to the Smithsonian Marine Station at Fort Pierce, it was necessary to store much of the carbonate and biomass in a holding system at the Museum of Natural History, while new facilities were being constructed. In mid-2001, the organisms were shipped to the new facility along with the organisms from the 130-gallon reef described later in this chapter. The new unit is similar to the Museum of Natural History system in most parameters. However, the large dump bucket wave-generating system was replaced with a fore-reef, back-reef surging device created by a switching valve in the ATS return line on a 20-s timer. Although this system has been primarily controlled by ATSs, impellor pumps have been used since inception; thus, part time granular activated carbon service is used to increase clarity for exhibit. No whole system calcification studies have been carried out on this system. However, in a survey carried out in mid-2003, after almost 2 years of stabilization, considerable calcification was found in a number of head corals and in Acropora cervicornis (Color Plate 25). Also several stony corals, which had not been successful long term in the earlier system, had adapted well (Table 20.5). In addition a number of new fish species were successfully introduced (Table 20.6). Delbeek and Sprung (2006) briefly describe this unit after it was fully established.

GREAT BARRIER REEF MESOCOSM The Australian Great Barrier Reef is the largest single coral reef system in the world. Lying near the center of maximum shallow-water diversity in the East Indian Archipelago, the Indo-Pacific Biogeographic Province, the Barrier Reef also has a very high diversity of organisms. In the 1970s, the Australian government designated the entire Barrier Reef Province a national park. Later it was also designated a World Heritage Site. Most of the Great Barrier Reef is 10–50 miles offshore and often difficult to reach from the Australian mainland. Thus, the Marine Park Authority, needing a public display and educational tool to implement park policies, decided in the early 1980s to establish a large aquarium system on the mainland.

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TABLE 20.5 Invertebrate Species New to the Smithsonian Coral Reef Marine Ecosystems Exhibit after Establishment at Fort Pierce, August 2003. See also Table 20.3 Acropora cervicornis Arbacia punctulata Asterina sp. Bispira brunnea Clibanarius tricolor Clibanarius vittatus Convolutriloba retrogemma Erythropodium caribaeorum Holothuria grisea Holothuria impatiens Lithopoma tectum Lysmata wurdemanni Lytechinus variegatus Montastrea cavernosa Paguristes cadenati Palythoa grandis Percnon gibbesi Pseudoplexaura sp. Pterogorgia sp.

Staghorn coral Common Arbacia urchin Sea star Social feather-duster worm Tricolor hermit crab Striped hermit crab Red flatworm Encrusting gorgonian Gray sea cucumber Slender sea cucumber West Indian starsnail Peppermint shrimp Variegated urchin Great star coral Red reef hermit crab Sun zoanthid Nimble spray crab Porous sea rod Sea whip

TABLE 20.6 Fish Species New to the Smithsonian Marine Ecosystems Exhibit after Establishment at Fort Pierce, August 2003. See also Table 20.4 Anisotremus saxatilis Bodianus pulchellus Centropyge argi Coryphopterus personatus Gobiosoma oceanops Malacoctenus traingulatus Opistognathus aurifrons Parablennius marmoreus Scartella cristata Scarus croicensis

Porkfish Spotfin hogfish Cherubfish Masked goby Neon goby Saddled blenny Yellowhead jawfish Seaweed blenny Molly miller Striped parrotfish

The Great Barrier Reef Wonderland Aquarium, opened in 1987, is basically a 250 times larger version of the Smithsonian model reef. It is considerably more sophisticated in design, and along with its larger size is a major improvement in reef simulation over earlier systems (Harriott, 1991). The following discussion of the Great Barrier Reef Aquarium does not include the predator tank, a separate, smaller, and adjacent unit also run with algal scrubbers but at higher nutrient levels. This separate system is for maintenance of large sharks and other reef predators, which, even at the large scale of the Australian reef model, could not be included in the main reef. The Townsville reef aquarium is 38 meters long and 17 meters wide (Figure 20.6). Its depth varies with the tide from 3.8 to 4.5 meters. A separate unlighted tidal reservoir with 350 000 liters at high tide and 750 000

liters at low tide in the reef tank handles the tidal volume. The reef tank includes 200 m3 of coral sand and 700 metric tons of carbonate rock. The nominal water volume of this large model reef is 2 500 000 liters (625 000 gallons). Natural sunlight is used for the Great Barrier Reef Aquarium (Figure 20.6). To provide a greater light range in summer and reduce heat loading some shading (shade cloth-plastic screen) is applied for several months in mid-summer. On the other hand, shading on the sides of the reef from the aquarium walls is such that some species appropriate for the actual depths in that area cannot be maintained there. The Great Barrier Reef Aquarium tank uses three large impellor pumps that remove 1 000 000 liters/h (4200 gpm) from the downstream (lagoon) end of the tank and return it to the fore reef end. In addition to the current created by this flow, an air–pressure-driven wave generator (Chapter 2) develops a 0.5- to 0.75meter wave every 2–8 s to create a marked wave surge motion throughout the reef. During most if its nearly 20-year history, water quality in this reef model was managed primarily by a bank of 40 algal scrubbers (80 m2). These scrubbers (Figure 11.4) were driven largely by natural light, though 6 h of night lighting with 1000-W metal halide lamps is also provided. When stabilized and harvested every 10–14 days, these scrubbers produced 5–7 g (dry)/m2/day (Morrissey et al., 1988). This value was generally lower than the 8–12 g (dry)/m2/day produced in other lownutrient saltwater scrubbers. The difference was perhaps to be ascribed to the largely daytime operation, which put the scrubber algae in competition with the reef algae for nutrients and carbon dioxide. Salinity in the Great Barrier Reef Aquarium is maintained at about 34.5–35.5 ppt to match that characteristic of the Barrier Reef Province. Temperature is maintained at 20–29°C. Some cooling is required at the upper end of the range, since it is well established in the wild that coral bleaching and other negative effects are initiated at about 30°C. It is noteworthy that in most ecosystems, optimum temperature levels at the upper end of the range are often close to lethal values. Operational care is needed in most models in this regard, and in the case of the Great Barrier Reef Aquarium, some mortality has resulted from inadvertent short periods of operation above 30°C. In the earlier configuration of the Smithsonian model described above, high temperatures had also become serious. This same problem has now become widespread in wild reefs due to global warming. In the Townsville model reef, several metals, mostly stainless steel but some galvanized (zinc) iron, occurred throughout the system’s plumbing. In the early months of operation, rising levels of dissolved heavy metals threatened to be a serious problem. Most of this metal

Great Barrier Reef Mesocosm

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FIGURE 20.6 Schematic diagram of the layout of the Australian Great Barrier Reef Aquarium.

was eventually replaced by plastics. Heavy-metal concentrations in the water after about a year were moderate but within acceptable limits. The ATSs gradually removed these metal contaminants once the basic source of the metals was removed (Morrissey and Jones, 1988). In recent years, it has been shown that degradation of the plastic on the scrubbers by sunlight has released an organic compound into the water column. This can be prevented either by using different materials for the scrubbers (e.g. glass) or possibly by adding the same coating that prevents this UV-driven breakdown on boat plastics. The original design of this very large reef system included sediment traps on the downstream end of each algal scrubber. For a variety of reasons these were omitted. Although not noticeably affecting the reef community, the net result of moderate turbidity for the long public viewing line across the aquarium was felt to be unacceptable. In spite of having to accept some plankton losses, this situation was brought under control with

the partial operation of sand filters. The slight yellow coloration perceived (Gelbstoff) was managed by very low levels of ozone treatment. Species counts had not been extensively developed for this system during the first decade, although they are clearly far above the smaller models that we have discussed. By late 1995, the Townsville system had approximately 800 colonies of hard and soft corals representing 100 species. Over 200 species of fish were represented (Luckett et al., 1996). The benthic or emergent zooplankton of the sandy areas of the tank had a community structure similar to that of the Great Barrier Reef lagoon but less than one-tenth of the density. The sand filter, low-level ozone, and the impellor pumps are probably responsible. While no deleterious ecological effects could be attributed to the pre-existing turbidity or to turbidity levels in other models, visitor expectations necessitated this level of treatment of the water. After 16 years of operation this large mesocosm was extremely depleted of both calcium and alkalinity

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and was performing poorly. As we demonstrate experimentally below, because algae (in wild reefs and in ATS units) accelerate CO2 removal of calcium and alkalinity and increase reef calcification (to wild reef levels), significant additions of calcium and bicarbonate are necessary (as happens in wild reefs from the open ocean). Unfortunately, these additions were not provided. Subsequently, the ATS system was removed and replaced with an array of protein-skimmers and large water exchanges were made with wild sea water (Michanek-Wagner, 2004). As we described in Chapter 11 and discuss in greater depth for a specific situation later in this chapter, coral reef systems operated with sufficient light and within the normal parameters of wild reefs will deplete calcium and alkalinity rapidly. If depletion occurs, eventually, many of the numerous reef calcifiers will shut down growth and perhaps show general calcium deficiency as well. Schleractinian corals, especially, need to grow to compete with algal turfs and macroalgae and to stay ahead of predation. These deficiencies were very likely responsible for most of the problems encountered in the large system. The ozonation employed for several years was also not likely conducive to system success. In this particular system, the cascade to poor performance was apparently initiated by a desire for the ultra-clarity supposedly required by public viewing.

In most wild reef systems, such clarity is restricted to the outer fore reef. Across the breaker zone and over the back reef under average conditions, water column typically has abundant algal fragments, fine carbonate silt thrown up from water turbulence, and numerous bubbles from both breaking waves and photosynthesis. Nevertheless, the ATS systems were described as producing particulates as well as dissolved organics from scraped algae. There is no question that for high quantity visibility, scrupulous technique in scraping and washing screens is necessary. As we describe in Chapter 25, the use of vacuum harvesters (wet shop vacs) avoids much of the algal losses, when both maximum algal biomass recovery is required and minimum suspended particulates are desired. As we describe next, using manual harvest on an ATS-controlled system for over 13 years, we continued to achieve the highest calcification rates and biodiversity levels reported for any microcosm or mesocosm coral reef system.

A 130-GALLON REEF MICROCOSM Physical/Chemical Parameters In October 1987, this 130-gallon microcosm home reef aquarium system (400 liters water volume) shown in Figure 20.7A and Color Plate 1 was placed in operation.

FIGURE 20.7 (A) Longitudinal section through the 139-gallon coral reef microcosm system (also shown in Color Plates 1 and 9). Not shown are the VHO tank lights. The lights indicated are the scrubber lights used in the first 6 years of operation. (B) Experimental and organism manipulation (large refugium) arrangement for the 130-gallon coral reef microcosm. From Small et al. (1998).

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A 130-Gallon Reef Microcosm

Originally it was stocked entirely with Caribbean organisms, except for the Indo-Pacific fish which were purchased at aquarium stores. However, when specific organisms were needed for experimental purposes they were also usually obtained from aquarium stores, and thus were mostly Indo-Pacific in origin. The last general introduction (of Caribbean live rock) was placed in the tank in June 1991. At that time the separate, auxiliary, “live rock” tank of 320 gallons was put into operation primarily as a refugium for organisms being manipulated. Except for two species of Indo-Pacific stony corals introduced in August 1996 for calcification measurements, and comparison with the literature (Chapter 10), and replacement of a few fish lost to predation, the system and its refugium had been closed to outside organisms for nearly 7 years at the time of the experiments and biodiversity analysis described below. This relatively small reef system model was illuminated by six 72-inch very-high-output (VHO) daylight fluorescent lamps having a total of 960 W or 1129 W/m2. This is slightly lower than the Smithsonian reef exhibit at 1280 W/m2 and might be limiting for some sun-adapted corals. However, the system also receives about 30% of its total mean light from natural daylight, mostly filtered by leaves and a double thermopane glass. This lighting provides daytime oxygen levels exceeding 7.0 mg/liter (and sometimes 9.0 mg/liter), well above saturation for the operational temperature and salinity. In spite of the pumping and wave mixing, early in the afternoon the algal community becomes densely covered with oxygen bubbles that break off and float to the surface. The ATS system as shown in Figure 20.7 and Color Plate 9 is of the screen/dump bucket type. Originally, this scrubber utilized six 36-inch HO lamps having a combined power of 300 W. In 1994, these bulbs were replaced by two 150-W metal halide lamps. On a 7-day harvest schedule this provides 3–12 g (dry)/m2/day of export and maintains minimum night levels of dissolved oxygen in the system at about 5.7 mg/liter. The scrubber algae are dominated by Polysiphonia, Herposiphonia, Cladophora, and Derbesia (Table 20.7), though bluegreen algae are abundant, as one might expect in such a low-nutrient reef model. The daily range of oxygen concentration produced, as a combination of system photosynthesis (day) and ATS (night) (Figure 20.8), is well within the envelope for typical, wild, back-reef communities (Adey and Steneck, 1985). In this coral reef model, the ATS maintains nutrient levels (N-nitrite plus nitrate) at 0.3–0.6 µM (0.004– 0.009 ppm) in this system (Table 20.8). Since the tank is so small, and fish and invertebrate biomass are relatively high, 0.43 g (dry) of mixed commercial flake food is added to the system each day. In the early years, about one-third of this addition was added at 22:00–24:00 h

TABLE 20.7 Algae Occurring on the Scrubber of the 130-Gallon Reef System shown in Figure 20.7 (1996–1997) Kingdom Monera Division Cyanophycota (blue-greens) Anacystic aeruginosa Gomphosphaeria aponica Porphyrosiphon kurzii* Microcoleus lyngbyaceous Shizothrix mexicana Schizothrix calcicola* Kingdom Plantae Subkingdom Thallobionta Division Rhodophycota (red algae) Goniotrichum alsidii Erythrotrichia carnii Acrochatium sagraeanum Hypnea spinella

Spirulina subsalsa Spirulina major Scytonema hofmanni Arthrospira sp. Calothrix crustacea

Spyridia filamentosa Polysiphonia subtillissima* Herposiphonia secunda Lophosiphonia cristata

Division Chlorophycota (green algae) Cladophora crystallina* Derbesia vaucheriaeformis* Cladophora delicatula Derbesia marina Enteromorpha compressa Derbesia lamarouxii Division Chromophycota (brown algae) Giffordia mitchellae* Many uncataloged diatoms (see Table 20.9) *Dominant species (note that Polysiphonia subtillissima is a primary structuring element).

each night, specifically intended for coral feeding. In the several years before and up through the experimental and analysis year, approximately 3 g (wet)/week of mussel meat was added to feed the higher predator lobster (see below), and an additional 1.5 g (wet) of oyster meat is chopped and given to actively feeding corals and anemones. This food import was balanced by export from the ATS and by occasional hand weeding during intervals when grazing tangs were not present in the tank. The total daily import of approximately 0.69 (dry)/day (0.75 g/m2/day) is smaller than the amount of planktonic import estimated on the St. Croix reef (2 g (dry)/m2/day see Chapter 17). Also, the export from the ATS, at approximately 1.6 g (dry)/day, would seem to assure nutrient depletion. However, at the concentration of nitrogen in this system (slightly above that in the wild, Figure 11.6), the nutrients in the algae harvested from the scrubber are also likely depleted enough to bring the system in balance (Figure 9.5). We started this smaller system with lower input than the exhibit coral reef first described in this chapter in the hope of achieving nutrient concentrations closer to those in the wild. However, at 0.56 µm (N⫺NO2 ⫹ NO3), that is about 8 ppbN, we were probably still a tenth or two of a µM above wild (St. Croix) levels. At no time in the 13 years’ total operation of this microcosm was there a suggestion of depletion, and probably scrubber export was well balanced with import. Primary productivity

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FIGURE 20.8 Diurnal oxygen concentration (A) and pH (B) in the 130-gallon coral reef model. Although light addition is stepwise and oxygen concentration tends to level off for each light level (1st set of tank lights; second set of tank lights; solar radiation through glass, but controlled in morning and evening by tree cover), the resulting curve is more or less smooth and quite similar to wild reef cycles The night concentration is maintained by the ATS. The curve is a mean of five diurnal cycles taken over a period of about 6 months. The pH curve is similar to oxygen, but follows oxygen curve by several hours: oxygen peaks at 12:00 (in some cases 13:00), while pH typically peaks at 16:00 or later. From Small and Adey (2001).

in this tank was very close to that measured in the wild. However, as we discuss further below, respiration, about average for worldwide coral reefs, was about 24% low for the St. Croix analog. It is possible that a roughly 30% increase of both feeding rate and scrubber size would provide a better veracity with the St. Croix analog wild reef. There are likely other factors that are involved in this matter of proportionally low respiration rate. Also, in energy terms, planktonic input, in the wild reef and

in all of the system discussed here, provides less than 10% of the energy required by the entire system. Most of the energy derives from in-situ photosynthesis. It should be noted again, as we have discussed in Chapters 9 and 11, that low nutrients are essential in a reef ecosystem if dominance of stony corals and algal turfs is to be maintained (Szmant, 2001). Littler et al. (1991) discuss this relative dominance paradigm, wherein the reef community dominance (algae vs corals) relates to a combination of nutrients and grazing. The pH of this coral reef microcosm ranged from a minimum of 7.95 in the early morning to a maximum of 8.35 in the afternoon. Values of 8.20–8.25 occurred through most of the middle of the day, and were associated with particularly high calcification rates in the model (Chapter 10). Although the scrubber area employed was only 0.18 m2, per unit volume (3.8 cm2/ liter, scrubber area to tank volume) and wattage (1670 W/m2), this is one of the most effective scrubber units that we have employed, having maintained constantly low nutrients in this model throughout its 14-year life. The pumping utilized in this model reef system was that of two bellows pumps. These modified, fully plastic, hand bilge pumps, converted to geared electric motor drive, provided a flow rate of about 6 gpm for a tank overturn period of about 30 min. As shown in Figure 20.7, the scrubber bucket also provided wave surge, producing a wave every 8–12 s. This was quite adequate for the upstream third of the tank and provided a quiet, more lagoon-like environment for the lower two-thirds of the tank. Salinity was maintained in this system between 34.5 and 36.0 ppt. An automatic water leveling system was used. While this tends to maintain very stable salinity levels (⫾0.2 ppt) on a day-to-day basis, gradual salt loss to the atmosphere and the sides of the tank and scrubber unit (which is wiped off periodically when the unit is cleaned) causes a very slow downward drift of salinity. For many years salt balance had been maintained by exchanging Chesapeake Bay water (18–19 ppt brought up to 50 ppt with commercial sea salts and then diluted to correct salinity at 2 liters/day). This process prevented any organisms (except perhaps bacteria) from being introduced from Chesapeake water. A commercial sea salt mix was used for making exchange water in the last several years. Temperature in the 130-gallon tank was maintained from 25°C to 29°C. At the lower end, no additional heating over a room temperature of 6570°F was required to keep a stable level in winter. At the upper end, in summer, room temperature had been kept below about 74°F. During the experimental period, we initiated room controls for 72°F to keep tank temperatures below 28.1°C.

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A 130-Gallon Reef Microcosm TABLE 20.8 Comparisons Between Microcosm and St. Croix Reefs (Annual Mean or Mean Daily Range with Standard Error)

Temperature (°C) (a.m.–p.m.) Salinities (ppt) pH (a.m.–p.m.) Oxygen concentration (mg/1) (a.m.–p.m.) GPP (g O 2 /m2/day); (mmol O2/m2/day) Daytime NPP (g O2/m2/day); (mmol O2/m2/day) Respiration (g O2/m2/h); (mmol O2/m2/h) N–NO⫺2 ⫹NO23 (µmol) Calcium (mg/l1); (mmol/l1) Alkalinity (meq/l1) Lighte (Langleys/day1)

Microcosm

St. Croix Reefs (fore reef)a

26.5 ⫾ 0.03 (n ⫽ 365)⫺27.4 ⫾ 0.02 (n ⫽ 362) 35.8 ⫾ 0.02 (n ⫽ 365) 7.96 ⫾ 0.01 (n ⫽ 62)⫺8.29 ⫾ 0.02 (n ⫽ 39) 5.7 ⫾ 0.1 (n ⫽ 14)⫺ 8.7 ⫾ 0.2 (n ⫽ 11) 14.2 ⫾ 1.0 (n ⫽ 4); 444 ⫾ 3 (n ⫽ 4) 7.3 ⫾ 0.3 (n ⫽ 4); 228 ⫾ 9 (n ⫽ 4) 0.49 ⫾ 0.04 (n ⫽ 4); 15.3 ⫾ 1.3 (n ⫽ 4) 0.56 ⫾ 0.07 (n ⫽ 6) 491 ⫾ 6 (n ⫽ 33); 12.3 ⫾ 0.2 (n ⫽ 33) 2.88 ⫾ 0.04 (n ⫽ 59) 220

24.0⫺28.5 35.5b 8.05–8.35c 5.8–8.5 15.7; 491 8.9; 278 0.67; 20.9 0.28 417.2d; 10.4 2.47b 430 (surface); 220 (5-m deep in fore reef)

From Small and Adey (2001).

Black band “disease,” which was a stable/endemic in the system, is unimportant at temperatures below about 28°C (Chapter 19).

Microcosm Metabolism To a large degree, the metabolic state of a semiclosed aquatic ecosystem, like this reef microcosm, can be determined from its oxygen concentration curves with time (Figure 20.8). When operating near oxygen saturation conditions (typically 6.4–6.5 mg/liter in this system), there is little or no oxygen exchange with the atmosphere. Respiration and gross primary production (GPP) (measured photosynthesis plus respiration) can be determined (Table 20.8) by the rate of change of oxygen concentration in full light and in the dark during these near saturation periods. In this system, the primary metabolic parameters, respiration, and photosynthesis, were very close to that of appropriate light levels (upper fore reef) on St. Croix reefs (Adey and Steneck, 1985; Hatcher, 1997). As shown in Figure 20.9, they are well within the mid to upper range of reefs worldwide. Primary production is quite close to that on the St. Croix fore reef; respiration is about 24% low, but right on the regression for reefs worldwide. Perhaps as we noted above, raising planktonic import and ATS export might well “drive the system harder.” On the other hand, part of the reason for the difference probably lies in spatial heterogeneity rather than in community metabolism. The real macro surface area (as determined by the chain method) in the St. Croix reefs mostly lies between 2 and 3 m2/ horizontal m2. The smaller the model, the less spatial

FIGURE 20.9 GPP as a function of respiration in the 130-gallon microcosm and the analog wild coral reef on St. Croix. The other points are well-developed wild coral reefs scattered around tropic seas. From Small and Adey (2001); background data from Gattuso et al. (1998).

heterogeneity is possible. This relationship is thus a part of scaling effect. In modeling research the question becomes: do we drive the system harder (i.e. increase respiration by greater food import, probably thereby slightly raising nutrients levels) to solve the scaling problem? The answer probably depends on the purpose of the research. Perhaps the system should be larger so the appropriate spatial heterogeneity can be included.

Microcosm Calcification Throughout 1997, a series of analyses of the state of the carbonate system and a number of its calcifying elements, including several stony corals, were carried out. As we noted above, the entire system had been operating a total of about 10 years at that point and,

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FIGURE 20.10 Carbonate system in the 130-gallon microcosm: (A) whole microcosm, n ⫽ 11; (B), A. palmata colony in

isolation chamber, n ⫽ 6; (C), Chondria (red algal) plant in isolation chamber, n ⫽ 5; and (D) combined A. palmata plus Chondria plant in isolation chamber, n ⫽ 5. See Figure 20.7 for diagram of system and Small and Adey (2001) for experimental protocol.

except for a few experimental specimens, and 130-gallon reef and refugium exchanges, had been largely closed to import organisms for about 4 years. The diurnal pH and alkalinity of the 130-gallon coral reef as a unit was examined several times in week-long analyses over four seasons. Also, individual component organisms where isolated in chamber sub-sets for series of daily runs scattered through the entire period. For details of experimental protocol, consult Small and Adey (2001). In this long-term, microcosm reef, calcium concentrations and alkalinity, during every run, continually fell during the day and were stable or rose slightly at night. To prevent depletion, calcium was added as a solution of aragonite dissolved in hydrochloric acid. The mean concentration of the solution used was approximately 24 000 mg/liter Ca⫹⫹ (pH ⫽ 6.7), and additions typically averaged 150 ml/day. In an effort to keep microcosm levels above 420 mg/liter, even after a

full day of calcification, the mean concentration of the calcium in the system was maintained at about 490 mg/ liter. Bicarbonate was added daily as either sodium bicarbonate (typically 11.0 g/day) or potassium bicarbonate (typically 14.0 g/day) dissolved in distilled water. The mean alkalinity was 2.88 meq/liter in order to maintain levels above 2.40 meq/liter. To examine the dynamics of the entire carbonate system for the principal components, bicarbonate ion, carbonate ion, and dissolved carbon dioxide were calculated from total alkalinity and pH using monographs. This was done for the whole microcosm, as well as each of the component organisms examined. The daily decrease in alkalinity for the entire microcosm, from January to October, 1997, produced highly repeatable results (Figure 20.10). Alkalinity reduction occurred from 0800 to 2000; ⌬Talk ⫽ 0.41 meg/liter. At night, there was little change in alkalinity;


⌬T ⫽ 0.01 meq/liter. As calculated from total alkalinity depletion, the mean calcification rate of the microcosm was 4.0 kg CaCO3/m2/year. For comparison, the calcification rate for the microcosm based on the amount of calcium added in order to maintain desired concentrations is 4.4 g CaCO3 /m2/year. These calcification rates are quite comparable to the mean calcification rates of reefs in the wild (Pichon, 1995). Considering an entire reef system (lagoon to fore reef), the worldwide means show that 1–2% of reefs will calcify at 10 kg CaCO3 /m2/year, 2–4% at 4 kg CaCO3 /m2/year, and 90–95% at 0.8 kg CaCO 3 / year. Since our microcosm is calcifying at 4.0 kg CaCO3/ m2/year, it is comparable to the top 2–4% portion of pan-tropic coral reefs. There are several key conclusions to be drawn from this data. First, at the current rate of calcification in this system all calcium in the water column should be removed in 50–60 days and alkalinity in 3–4 days. However, failure to add calcium and carbonate or bicarbonate (to maintain alkalinity) for long periods (many years) does not bring those concentrations to zero, nor does it stop calcification. Thus, there is internal cycling within the system. Allowed to deplete for several years, calcium concentration reaches a dynamic balance of about 10% below oceanic levels, with alkalinity about 32% below oceanic levels. As we have noted above, longer periods of depleted operation can apparently have serious effects. While throughout this book we have stated a reef system input requirement for calcium and alkalinity, it seems likely that only alkalinity is truly critical. The constant boring of many organisms in this reef model can undoubtedly return adequate calcium to the water column. However, the carbonate from this interaction is almost certainly released as CO2, which in the high-pH water environment of the model is unlikely to be returned to alkalinity. Kempe and Kazmierczak (1994) consider the problem of alkalinity formation in recent world oceans. They conclude that coral reefs and open-ocean carbonate formation removes alkalinity, while alkalinity formation occurs in stagnant oxygen-depleted basins (e.g. the Black Sea). They call these systems alkalinity pumps. We suggest that deep in the oolitic sand of this reef model, where anaerobic conditions exist, that under conditions of no alkalinity input and resulting depletion, alkalinity (as HCO3–) is produced in a quantity that is sufficient to support a low calcification rate.

Organism Calcification There are numerous species of organisms partly responsible for the calcification in the microcosm. These species span 84 families of green algae, coralline red

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FIGURE 20.11 Calcification rate of the entire 130-gallon coral reef microcosm (Figure 20.7) in comparison with its principal components. The data for the components were obtained by placing the components in an isolation chamber within the larger microcosm. See Small and Adey (2001) for experimental protocol.

algae, foraminifera, sponges, stony corals, mollusks, polychaetes, and arthropods. However, the primary calcifying components in the microcosm are: reef framework with an algal turf community (by micritization within the carbonate), coralline red algae, foraminifera (abundant in the microcosm at the time of data collection), Tridacna clams, Halimeda, and stony corals. The calcification rates, as determined by chamber runs, for all of the microcosm components are compared in Figure 20.11. The algal turf, corallines, and foraminifera have been combined in a category called “background” since they were very close in magnitude and indeed each specimen had small components of the other two. It was not possible to measure the calcification rate of the Tridacna derasa or Tridacna maxima in the system using the chambers because of their large size. The calcification rate of a smaller specimen of T. derasa from the refugium was then used to estimate by area coverage

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the rates of the larger Tridacna in the microcosm. Likewise, the calcification rate of Halimeda tuna was used to represent the calcification rate of all Halimeda spp. in the system. Several stony coral species were run individually in the chambers to determine the calcification rate of each species. Acropora sp., Montipora digitata and Diploria labyrinthiformis calcified at the fastest rates with rates of 8.1, 7.5, and 6.4 kg CaCO 3 /m2/year. Note that rates for Acropora and Montipora had apparently increased slightly when run several months later in Figure 20.11 (stippled bars); they were larger in living biomass but had not changed in their horizontally projected surface area (the unit used in all measurements, including the wild comparisons). The principal elements of the carbonate system of the microcosm (bicarbonate ion, carbonate ion, and dissolved carbon dioxide) are plotted as a function of pH, total alkalinity and time of day, in Figure 20.10. While there is a minor shift of bicarbonate to carbonate with the daily photosynthetic removal of carbon dioxide and subsequent pH rise, roughly 90% of the alkalinity depletion from the water column occurs as bicarbonate removal. Equivalent plots made for the stony coral Acropora, the free-living algae Chondria and for Acropora plus Chondria are also shown in Figure 20.10. In the Acropora chamber runs, there is little net CO2 removal, and thus little pH and carbonate rise, though considerable alkalinity reduction (calcification). Conversely, in the Chondria (free-living algae) chamber, where intensive carbon dioxide removal and rising pH is accompanied by a large carbonate rise, there is virtually no alkalinity depletion. In the combined Acropora plus Chondria chamber, even though carbonate rise is about the same as in the Chondria alone chamber, alkalinity and bicarbonate depletion increased nearly 70% above that for Acropora alone. At the community/ecosystem level, photosynthesis and calcification are mutually supportive. Coral calcification is enhanced by algal removal of carbon dioxide, and, as we have shown, zooxanthellae photosynthesis is insufficient to support calcification potential. In most reefs free-living algae greatly dominate zooxanthellae in biomass and photosynthesis (see Adey, 1998). Corals (and likely most animal calcifiers in coral reefs) provide free-living algae with both substrate and carbon dioxide. Algal turfs cannot normally overgrow corals, but with internal nutrient cycling and nitrogen fixation they can maintain high primary production even with heavy grazing. However, as Szmant (2001) has reviewed, disturbance of the algal/herbivore status of typical reef ecosystems (elevated nutrients, herbivore reduction, etc.) can allow macroalgal overgrowth of stony corals. Many macroalgae released from nutrient/herbivore

control can overgrow stony corals and cause a “phase shift” of reef community structure that greatly reduces net calcification, even though photosynthesis remains high (Hughes, 1994). Excess nutrients may also similarly upset the internal balance between the animal coral and its zooxanthellae (Marubin and Davies, 1996), further limiting calcification rate.

Microcosm Biodiversity As described in detail by Small et al. (1998), this microcosm and its refugium had its last significant collections introduced in 1991. Following that time, only a few fish, as individuals and specific test organisms, were brought into the unit, mostly in the last 2 years before the year-long study of system metabolism and biodiversity were initiated in late 1997. Throughout that nearly 7 years of “semi-closure,” environmental conditions were rather tightly maintained in accordance with the description earlier in this chapter and in Chapter 10. The biodiversity sampling took place over the entire year with one of the authors (WHA) responsible for algal identification, the protozoan specialist Don Spoon working on-site on the wide array of protozoans, dinoflagellates and micrometazoans and Allegra Small responsible for collecting, sorting, and preparing invertebrates for distribution to the array of 22 specialists that had agreed to provide identifications (see Small et al., 1998). It was not possible to find a specialist to work with nematodes, fungi, bacteria, viruses, primarily parasitic invertebrate groups, and several minor phyla, so these were omitted from the survey. Work was carried out over a long period primarily to avoid any significant disturbance of the system. Preliminary investigations were always carried out in the larger refugium tank and once familiarity was achieved with any one group, presence was tested in the primary microcosm with the intention of least disturbance It was because of the consensus of the three primary and direct workers on the system that we were able to tally roughly 70% of the species in the system. In this microcosm, with its refugium, 534 species were tallied (Table 20.9) with our joint estimate of 800 species total. Using the generally accepted formula relating area and species diversity (S ⫽ kAz), this would provide a pan-tropic coral reef diversity of about three million species. This is several times higher than previous estimates (Small et al., 1998), and, per unit area, makes coral reefs more diverse than tropical rain forests. Even more interesting, however, the biodiversity of this model, the vast majority of which had to be supplied by reproductive maintenance of populations, is very broadly based. It is spread out over greater than 230

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A 130-Gallon Reef Microcosm TABLE 20.9 Families (6/5) Species and Genera of Identified Organisms in the 130-Gallon Coral Reef Microcosm and its Refugium PLANTS, ALGAE, AND CYANOBACTERIA Division Cyanophota Chroococcaceae 6/5 Pleurocapsaceae 4/2 UID Family 4/4 Oscillatoriaceae 8/6 Rivulariaceae 4/1 Scytonemataceae 1/1 Phylum Rhodophyta Goniotrichaceae 2/2 Acrochaetiaceae 2/2 Gelidiaceae 1/1 Wurdemanniaceae 1/1 Peysonneliaceae 3/1 Corallinaceae 11/8 Hypneaceae 1/1 Rhodymeniaceae 3/2

Phylum Percolozoa Vahlkampfiidae 2/1 UID Family 2/2 Stephanopogonidae 2/1 Phylum Euglenozoa UID Family 4/3 Bondonidae 7/1 Phylum Choanozoa Codosigidae 2/2 Salpingoecidae 1/1 Phylum Rhizopoda Acanthamoebidae 1/1 Hartmannellidae 1/1 Hyalodiscidae 1/1 Mayorellidae 2/2 Reticulosidae 2/2 Saccamoebidae 1/1 Thecamoebidae 1/1 Trichosphaeridae 1/1 Vampyrellidae 1/1 Allogromiidae 1/1 Ammodiscidae 1/1 Astrorhizidae 1/1 Ataxophragmiidae 1/1 Bolivinitidae 3/1 Cibicidiidae 1/1 Cymbaloporidae 1/1 Discorbidae 5/2 Homotremidae 1/1 Peneroplidae 1/1 Miliolidae 10/2

Phylum Cnidaria UID Family 3/? Eudendridae 1/1 Olindiiae 1/1 Plexauridae 1/1 Anthothelidae 1/1 Briareidae 1/1 Alcyoniidae 2/2

Champiaceae 1/1 Ceramiaceae 3/3 Delesseriaceae 1/1 Rhodomelaceae 7/6 Phylum Chromophycota Cryptomonadaceae 2/2 Hemidiscaceae 1/1 Diatomaceae 6/4 Naviculaceae 9/4 Cymbellaceae 3/1 Entomoneidaceae 1/1 Nitzchiaceae 6/4 Epithemiaceae 3/1 Mastogloiaceae 1/1 Achnanthaceae 9/3

Gymnodiniaceae 6/4 or 5 Gonyaulacaceae 1/1 Prorocentraceae 2/1 Zooxanthellaceae 1/1 Ectocarpaceae 2/2 Phylum Chlorophycota Ulvaceae 1/1 Cladophoraceae 4/2 Valoniaceae 2/2 Derbesiaceae 3/1 Caulerpaceae 3/1 Codiaceae 6/2 Colochaetaceae 1/1 Phylum Magnoliophyta Hydrocharitaceae 1/1

PROTISTA Planorbulinidae 2/2 Siphonidae 1/1 Soritidae 4/4 Textulariidae 1/1 Phylum Ciliophora Kentrophoridae 1/1 Blepharismidae 2/2 Condylostomatidae 1/1 Folliculinidae 4/3 Peritromidae 2/1 Protocruziidae 2/1 Aspidiscidae 7/1 Chaetospiridae 1/1 Discocephalidae 1/1 Euplotidae 11/3 Keronidae 7/2 Oxytrichidae 1/1 Psilotrichidae 1/1 Ptycocyclidae 2/1 Spirofilidae 1/1 Strombidiidae 1/1 Uronychiidae 2/1 Urostylidae 4/2 Cinetochilidae 1/1 Cyclidiidae 3/1 Pleuronematidae 3/1 Uronematidae 1/1 Vaginicolidae 1/1 Vorticellidae 2/1 Parameciidae 1/1

Colepidae 2/1 Metacystidae 3/2 Prorodontidae 1/1 Amphileptidae 3/3 Enchelyidae 1/1 Lacrymariidae 4/1 Phylum Heliozoa Actinophyridae 2/1 Phylum Placozoa Family UID 5 Phylum Porifera Plakinidae 2/1 Geodiidae 5/2 Pachastrellidae 1/1 Tetillidae 1/1 Suberitidae 1/1 Spirastrellidae 2/2 Clionidae 4/2 Tethyidae 2/1 Chondrosiidae 1/1 Axinellidae 1/1 Agelasidae 1/1 Haliclonidae 4/1 Oceanapiidae 1/1 Mycalidae 1/1 Dexmoxyidae 1/1 Halichondridae 2/1 Clathrinidae 1/1 Leucettidae 1/1 UID Family 2/?

EUMETAZOA Vermetidae 1/1 Phyramidellidae 1/1 Fasciolariidae 2/2 Olividae 1/1 Marginellidae 1/1 Mitridae 1/1 Bullidae 1/1

Cyprididae 2/2 Bairdiiaae 1/1 Paradoxostomatidae 1/1 Pseudocyclopidae 1/1 Ridgewayiidae 2/1 Ambunguipedidae 1/1 Argestidae 1/1

(Continued)

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20. Models of Coral Reef Ecosystems TABLE 20.9

Actiniidae 3/2 Aiptasiidae 1/1 Stichodactylidae 1/1 Actinodiscidae 4/3 Corallimorphidae 3/2 Acroporidae 2/2 Caryophylliidae 1/1 Faviidae 3/2 Mussidae 1/1 Poritidae 3/1 Zoanthidae 3/2 Cerianthidae 1/1 Phylum Platyhelminthes UID Family 1/1 Anaperidae 3/2 Nemertodermatidae 1/1 Kalyptorychidae 1/1 Phylum Nemertea UID Family 2/2 Micruridae 1/1 Lineidae 1/1 Phylum Gastrotricha Chaetonotidae 3/1 Phylum Rotifera UID Family 2/? Phylum Tardigrada Batillipedidae 1/1 Phylum Nemata Draconematidae 3/1 Phylum Mollusca Acanthochitonidae 1/1 Fissurellidae 2/2 Acmaeidae 1/1 Trochidae 1/1 Turbinidae 1/1 Phasianellidae 1/1 Neritidae 1/1 Rissoidae 1/1 Rissoellidae 1/1 Vitrinellidae 1/1

(Continued)

UID Family 4/? Mytilidae 2/1 Arcidae 2/1 Glycymerididae 1/1 Isognomonidae 1/1 Limidae 1/1 Pectinidae 1/1 Chamidae 1/1 Lucinidae 2/2 Carditidae 1/1 Tridacnidae 2/1 Tellinidae 1/1 Phylum Annelida Syllidae 3/2 Amphinomidae 1/1 Eunicidae 3/1 Lumbrineridae 1/1 Dorvilleidae 1/1 Orbiniidae 1/1 Spionidae 1/1 Chaetopteridae 1/1 Paraonidae 1/1 Cirratulidae 4/3 Ctenodrilidae 4/3 Capitellidae 3/3 Muldanidae 1/1 Oweniidae 1/1 Terebellidae 2/1 Sabellidae 14/4 Serpulidae 6/6 Spirorbidae 2/2 Dinophilidae 1/1 Phylum Sipuncula Golfingiidae 1/1 Phascolosomatidae 3/2 Phascolionidae 1/1 Aspidosiphonidae 3/2 Phylum Arthropoda Halacaridae 1/1 UID Family 2/?

Diosaccidae 1/1 Harpacticidae 1/1 Louriniidae 1/1 Thalestridae 1/1 Tisbidae 1/1 Mysidae 1/1 Apseudidae 2/1 Paratanaidae 1/1 Tanaidae 1/1 Paranthuridae 1/1 Sphaeromatidae 1/1 Stenetriidae 1/1 Juniridae 1/1 Lysianassidae 1/1 Gammaridae 4/4 Leucothoidae 1/1 Anamixidae 1/1 Corophiidae 1/1 Amphithoidae 2/2 Alpheridae 2/2 Hippolytidae 2/1 Nephropidae 1/1 Diogenidae 1/1 Xanthidae 2/? Phylum Echinodermata Ophiocomidae 1/1 Ophiactidae 1/1 Cidaroidae 1/1 Toxopneustidae 1/1 Holothuriidae 1/1 Chirotidae 1/1 Phylum Chordata Ascidiacea UID Family 1/1 Grammidae 1/1 Chaetodontidae 1/1 Pomacentridae 5/4 Acanthuridae 1/1

See Adey and Loveland (1998) or Small et al. (1998) for Species and Genera Names.

families (Adey, 2006); 60% of these families have only a single species; 32% have two species. This strongly suggests that community and trophic structure of this microcosm is formed primarily from a relatively few species selected from the major structural and physiological plans of the host reefs. It further implies that microcosm models can have a high veracity of function as patches of fully operational reef systems. As a mean, any random patch of a wild reef is fully functioning with a fraction of the species of a whole reef. This we saw earlier in this book as a collecting paradigm (Figure 12.13). As long as the ecosystem modeler persists in obtaining the physical–chemical parameters of the wild ecosystem and provides broad access to species from the wild (multiple block collecting), the species in

the model will self organize to form the same ecosystem as the wild at the scale of a patch. The size of the model (microcosm or mesocosm) is likely to depend largely on the size of the structuring members of the community. Coral reefs can be more or less easily modeled in microcosm because individual coral colonies are not large; mangrove swamps require large mesocosms because individual mangrove trees are much larger on average than individual coral heads.

Ecological Notes As we have discussed above, this coral reef model was highly successful in terms of calcification, metabolism, and biodiversity. It was also the most successful


microcosm or aquarium system of the authors or the Marine Systems Laboratory in terms of repeatedly and successfully spawning and recruiting stony coral colonies (Table 20.9; Color Plates 5 and 6) along with an extensive array of algae and many invertebrates (note that two of the largest systems that we have worked on have also spawned and successfully set scleractinian colonies). Reproductive maintenance of key species populations is an important element of success in modeling any living ecosystem, and that is clearly the case in this small tank for at least 500 species. Food webs and population structure in this microcosm are in a dynamic steady state dependent on human manipulation at weekly to monthly intervals. Algae such as Laurencia papillosa, Spyridia filamentosa, Halimeda discoidea, Chaetomorpha linum, and Oscillatoria submembranacea have gone through cycles of increased abundance only to retreat to a long-term, low-level presence determined by some combination of altered grazing intensity and reproductive success. This phenomenon is directly analogous to the innate tendency of the wild ecosystem to form patches of heterogeneous species. Other algae in this microcosm, with resistance to grazing, such as Valonia macrophysa, Amphiroa fragillissima, and Halimeda opuntia, can form 70–80% of the dense standing crop in the generally intensely grazed environment, and yet apparently disappear beneath the Laurencia and Spyridia when grazing pressure is reduced. Diatoms (microscopic algae) are highly abundant and diverse in this system (Figure 20.12). The primary fish grazer in this model in the grazed mode is the tang, Zebrasoma flavescens. A young pair can keep the surface in a “thorn scrub” of Valonia, Halimeda, Amphiroa, and a constantly grazed turf. After a year or two and predation by the lobster Enoplometopus (see below), the system is sometimes allowed to run for 3–6 months without a fish grazer. When this happens, a patchy, but dense brush of Laurencia and Spyridia develops that requires occasional hand grazing. A rare reef lobster/shrimp (Enoplometopus occidentalis) was the higher predator over most of the life of this system; it was fed 2–3 g (wet)/week of mussels (Geukensia demissus). Every 3–6 months, a fish would fall prey to the lobster, a rate that was higher if the manual feed rate was lowered. When the fish population fell, fish (Amphiprion sp., Chromis sp., and other damselfish) were replaced from external sources (e.g. in 1991, 1993, and 1996). This primarily nocturnal lobster functioned as both scavenger and predator. Growing (and molting) rapidly for the first year and a half, it then remained at about the same dimensions for the remainder of its approximately 11 years of life (Figure 20.13). Its molts were less frequent after the first 2 years (about every 6 months); it died, for unknown reasons, perhaps age, in 1999.

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FIGURE 20.12 Synedra species (400 ␮m long). Several Synedra species along with over 40 species of diatoms from some 20 genera occur in the 130-gallon coral reef aquarium. Several appear to be new to science. Diatoms have siliceous frustules (shells) of intricate morphology and form numerous microcommunities of different species for each microhabitat in the tank. Photo by Ginny Spoon.

Crustose coralline algae, including Mesophyllum mesomorphum and Neogoniolithon spp., are important creators of structure in this system. Although their growth rates have not been measured, they are, by observation, on the order of the millimeters per month levels seen by Adey and Vassar (1975) on Caribbean reefs. The system has 10-stony coral species belonging to seven genera. As described by Luckett et al. (1996), stony coral individuals of two species were measured in 1994–1995 to provide the following expansion rates: Porites astreoides, eight individuals (radial crust expansion: 1.2 mm/month) and Dichocoenia stokesii, two individuals (lateral expansion of column: 0.8 mm/month). Three species of stony coral have sexually reproduced and recruited viable colonies in this system. These species are D. stokesii (one colony); Porites porites (one colony); P. astreoides (seven colonies). In this regard, it is noteworthy that this

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FIGURE 20.13 Molt dimensions and growth of rare reef lobster, Enoplometopus occidentalis.

system has bellows pumps rather than impellor pumps. Six stony coral colonies died before 1997: three Dichocoenia stokesii and three Porites astreoides. The origin of this mortality was not always clear. Sometimes obvious predation is involved. In other cases, one colony of a species was shrinking with white or black band “disease,” while another, 20 cm away, was growing rapidly. These kinds of growth and mortality in the several years before formal experimentation was started were achieved in a system that had calcium maintained only by occasional additions of fresh oolite and without control of alkalinity (bicarbonate). Calcium ranged from

365 to 420 mg/liter and alkalinity (mostly bicarbonate) was typically below 2.0 meq/liter. As we described in depth above and in Chapter 10, when calcium and alkalinity were kept at or slightly above 420 mg/liter and 2.4 meg/liter growth and calcification considerably increased and mortality reduced. As we noted for the Australian system above, long-term failure to main calcium and alkalinity removed in the rapid calcification occurring in these systems can lead to decreased function and biodiversity. The back wall of this microcosm, receiving outside solar light, was often left unscraped for long periods. This surface develops a calcifying aufwuchs, or thick


FIGURE 20.14 Typical polychaete annelid worm. Over 50 species of annelid worms (mostly polychaetes) occur in the 130-gallon coral reef system. It forms the second largest single phylum of invertebrates in this system, although each of the major invertebrate groups (sponges, cnidarians, and molluscs) has numbers in the upper 30s of species; arthropods are represented by well over 50 species. Photo by Dr. Donald M. Spoon.

surface film, heavily dominated by the blue-green Anacystis sp. The film also contained a sprinkling of other blue-greens and red and green algal filaments as well as numerous protozoans, including forams, nematodes, and an occasional small polychaete (Figure 20.14). In a wild coral reef, this kind of a film appearing in patches on the reef itself is referred to as stromatolite development. In some cases, stromatolitic crusts are an important large-scale element of calcification in wild coral reefs. Single individuals of Tridacna gigas and Tridacna maxima have been present in this system for about 10 years and grew considerably, eventually being moved to the refugium (Color Plate 18). Reproductively sustained populations of molluscs, along with abundant fan worms and sponges, also demonstrate a considerable filter-feeding capability in this system. Many

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FIGURE 20.15 Schizothrix mexicana (left center), a common cyanophyte (blue-green alga; cyanobacterium) of the 130-gallon coral reef system. This short filament is a hormogone, a reproductive fragment of what are usually long filaments about 20 µm in diameter. The organism to the right is an ameboid colonial bacterium. A complex series of these organisms was first found in the Marine Systems Laboratory microcosm and later some were searched for and found in wild reefs. They probably represent a new phylum of organisms, although the level of new kingdom is also being considered. Photo by Dr. Donald M. Spoon.

invertebrate larvae are too small to be preyed on by the fish, enter the plankton only at night, or are fully benthic, and as a result are reproductively successful. Two species of small planktonic, big-eyed shrimp enter the water column to feed at night and 13 species (from 10 different families) of copepods have been identified. As can be seen from Table 20.8, numerous species of sponges, of a wide variety of genera, and filter-feeding annelid worms are long-term residents. The sponge Tethya is particularly abundant in spite of the presence of the rock beauty. This genus, common in Caribbean reefs, is known for its toxicity and is avoided by predators. Another notable reproductive success is Petaloconchus, a reef-forming vermetid gastropod that “spins

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Besides the stony corals, numerous alcyonarian soft corals and gorgonians as well as coralliomorphs and anemones are long-term residents of this home aquarium. The two gorgonians, Eunicea sp. and Plexaura homomalla, date from the original stocking, and several Eunicia sp. colonies have spawned, giving rise to young colonies that survive and continue to grow to adult size. Finally, at least in part because of the lack of impellor pumps, the meiofaunal and larger microfaunal elements are particularly abundant (Figures 20.15 and 20.16). Nearly 100 species of protozoans were tallied in a short search (Color Plate 30) and these were accompanied by numerous rotifers and gastrotrichs. Both common reefencrusting foraminifera, Homotrema rubrum and Gypsina sp., as well as the rare Haliphysema sp. (which builds a test of several centimeters length with silicious sponge spicules) are also successful in this system.

SUMMARY

FIGURE 20.16 Chaetonotus sp. at least two species of which occur in the 130-gallon coral reef system. This “lower,” worm-like invertebrate is placed in the Phylum Gastrotricha, most common in the meiofauna, living between sand grains. This animal is multicellular with tissues and organs, but it is only 100 µm long. Photo by Dr. Donald M. Spoon.

a web” and then eats the entrapped plankton and organic particulates. Two of the fish present in this tank were primarily grazers (Zebrasoma flavescens and Pomacentrus coeruleana). The remainder were predators of the abundant small grazing (amphipods, isopods), filtering (sabellids), and deposit-feeding invertebrates. All but the rock beauty (Holacanthus tricolor) fed on both added flake food, which simulated net incoming zooplankton in the wild analog, and internal plankton. The rock beauty preyed heavily on the “weedy” anemone, Aiptasia pallida, which in turn can seriously compete with stony corals for space. It was cycled out to the refugium periodically when anemones become scarce and predation on stony corals was initiated. None of the fish were reproductively successful. The anemone fish produce repeated clutches of eggs that hatch, and the larvae were abundant during the night of hatching, but do not survive to settlement.

The extraordinary essence of wild coral reef ecosystems lies in four principal interrelated components: elevated photosynthesis, complex food webs, high rates of net calcification, and extreme diversity density. It is clearly possible to build reliable, long-lived microcosms that exhibit all of these features. Many secondary elements – schools of brightly colored fish, large marauding fish, and abundant larger invertebrate predators – require large-size mesocosms for their accomplishment.

References Adey, W. (1978a) Coral reef morphogenesis: a multidimensional model. Science 202: 831–837. Adey, W. (1978b) Algal ridges in the Caribbean Sea and West Indies. Phycologia 17: 361–367. Adey, W. (1983) The microcosm: a new tool for reef research. Coral Reefs 14: 193–201. Adey, W. (1998) Coral reefs: algal structured and mediated ecosystems in shallow, turbulent, alkaline waters. J. Phycol. June, 1998. Adey, W. (2006) Lessons learned in the construction and operation of coral reef microcosms. Chapter 17 in: Handbook of Coral Reef Restoration. W. Precht (Ed.). CRC Press, Boca Raton (In press). Adey, W. and Steneck, R. (1985) Highly productive Eastern Caribbean reefs: synergistic effects of biological, chemical, physical and geological factors. In: The Ecology of Coral Reefs, Vol. 3. M. Reaka (Ed.). NOAA Symposium Series on Underwater Research, Washington, DC. Adey, W. and Vassar, J. M. (1975) Colonization, succession, and growth rates of Caribbean crustose corallines. Phycologia 14: 55–69. Birkeland, C. (Ed.) (1997) Life and Death of Coral Reefs. Chapman and Hall, New York. Brawley, S. and Adey, W. (1982) Coralliophila abbreviata: a significant corallivore. Bull. Marine Sci. 32: 595–599.

References Brown, S. D. (1996) Captive Propagation of Scleractinian Corals in Closed Systems. 7th International Coral Reef Congress, Panama. Carlson, B. (1987) Aquarium systems for living corals. Int. Zoo. Yb. 26: 1–9. Cho, L. and Woodley, J. (2002) Recovery of reefs at Discovery Bay, Jamaica and the role of Diadema antillarum. Proceedings of the 9th International Coral Reef Symposium, 2000. Delbeek, C. and Sprung, J. (1994) The Reef Aquarium. Ricordea Publishing, Coconut Grove, Florida. Delbeek, C. and Sprung, J. (1996) The Reef Aquarium, Vol. II. Ricordea Publishing, Coconut Grove, Florida. Delbeek, C. and Sprung, J. (2005) The Reef Aquarium, Science Art and Technology, Vol. III. Ricordea Publishing, Coconut Grove, Florida. Fitt, W., Brown, B., Warner, M., and Dunne, R. (2001) Coral bleaching: interpretation of thermal tolerance limits and thermal thresholds in tropical corals. Coral Reefs 20: 51–65. Gattuso, J.-P., Frankignoulle, M., and Wollast, R. (1998) Carbon and carbonate metabolism in coastal aquatic systems. Ann. Rev. Ecol. Syst. 29: 405–433. Gladfelter, W., Gladfelter, E., Monahan, E., Ogden, J., and Dill, R. (1977) Environmental Studies of Buck Island Reef National Monument, St. Croix, U.S.V.I. West Indies Laboratory, St. Croix. Harriott, V. (1991) Macro-reef system. Freshwater Mar. Aquar. 14(5): 8–10. Hatcher, B. (1997). Organic production and decomposition. In: Life and Death of Coral Reefs. C. Birkeland (Ed.). Chapman and Hall, New York. Hoegh-Guldberg, O. (1999) Climate control, coral bleaching and the future of the world’s coral reefs. Mar. Freshwater Res. 50: 839–866. Hoegh-Guldberg, O. (2002) The future of coral reefs: integrating climate model projections and the recent behavior of corals and their dinoflagellates. Proceedings of the 9th International Coral Reef Symposium, 2000. Hughes, T. (1994) Catastrophes, phase shifts, and large-scale degradation of a Caribbean coral reef. Science 265: 15474–1551. Jones, R., Bowyer, J., Hoegh-Guldberg, O., and Blackall, L. (2004) Dynamics of a temperature-related coral disease outbreak. Mar. Ecol. Prog. Ser. 281: 63–77. Kempe, S. and Kazmierczak, J. (1994) The role of alkalinity in the evolution of ocean chemistry, organization of living systems, and biocalcification processes. Bull. l’Inst. Ocean., Monaco SP13: 61–117. Knowlton, N. (2001) The future of coral reefs. Proc. Nat. Acad. Sci 98: 5419–5425. Koop, K. et al. (2001) ENCORE: the effect of nutrient enrichment on coral reefs. Synthesis of results and conclusions. Mar. Pollution Bull. 42: 91–120. Kuta, K. and Richardson, L. (2002) Ecological aspects of black band disease of corals: relationships between disease incidence and environmental factors. Coral Reefs 21: 393–398.

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Littler, M., Littler, D., and Titlyanov, E. (1991) Comparisons of N- and P-limited productivity between high granitic islands versus low carbonate atolls in the Seychelles Archipelago: a test of the relative dominance paradigm. Coral Reefs 10: 199–209. Littler, M., Littler, D., and Taylor, P. (1996) Selective herbivore increases biomass of its prey: a chiton coralline reef-building association. Ecology 76: 1666–1681. Luckett, C., Adey, W., Morrissey, J., and Spoon, D. (1996) Coral reef mesocosms and microcosms – successes, problems, and the future of laboratory models. Ecol. Eng. 6: 57–72. Marubini, F. and Davies, P. (1996) Nitrate increases zooxanthellae population density and reduces skeletogenesis in corals. Mar. Biol. 127: 319–328. McField, M. (2002) Influence of disturbance on coral reef community structure in Belize. Proceedings of the 9th International Coral Reef Symposium, 2000. Michanek-Wagner, K. (2004) Coral interviews. Coral 1(6): 4, 6–7. Moe, M. (1989) The Marine Aquarium Reference. Green Turtle Publications, Plantation, Florida. Morrissey, J. and Jones, M. (1988) Water – clean, clear and warm. Austr. Sci. Mag. 3: 33–41. Morrissey, J., Jones, M., and Harriott, V. (1988) Nutrient cycling in the Great Barrier Reef Aquarium. Proceedings of the 6th International Coral Reef Symposium. Pelejero, C., Calvo, E., McCulloch, M., Marshal, J., Gaygan, M., Lough, J., and Opdyke, B. (2005) Preindustrial to modern interdecadal variability in coral reef pH. Science 309: 2204–2207. Pichon, M. (1995) Coral reef ecosystems. In: Encyclopedia of Environmental Biology, Vol. 1. W. A. Nierenberg (Ed.). Academic Press, San Diego. Precht, W. (2006) (Ed.) Handbook of Coral Reef Restoration. CRC Press, Boca Raton (In press). Reaka-Kudla, M. (1996) The global biodiversity of coral reefs. In: Biodiversity II: Understanding and Protecting our Natural Resources. M. Reaka-Kudla, D. Wilson, and E. O. Wilson (Eds). Joseph Henry/National Academic Press, Washington, DC. Small, A. and Adey, W. (2001) Reef corals, zooxanthellae and freeliving algae: A microcosm study that demonstrates synergy between calcification and primary production. Ecol. Eng. 16: 443–457. Small, A., Adey, W., and Spoon, D. (1998) Are current estimates of coral reef biodiversity too low? The view through the window of a microcosm. Atoll Res. Bull. 458: 1–20. Szmant, A. (2001) Why are coral reefs world-wide becoming overgrown by algae? Algae, algae everywhere and nowhere a bite to eat? Coral Reefs 19: 299–302. Williams, S. and Adey, W. (1983) Thalassia testudinum Banks ex Konig. Seedling success in a coral reef microcosm. Aquat. Bot. 16: 181–188.


C H A P T E R

21 A Subarctic/Boreal Microcosm Test of a Biogeographic Model

Including its prototype, a 2600-gallon, 6-square meter microcosm/exhibit of a rocky Maine shore and marsh was operated successfully for 17 years in the Smithsonian’s National Museum of Natural History in Washington, DC. Later in this chapter, that model ecosystem is described and compared with the wild ecosystem. In 2000, the “Whale Hall,” in which the cold-water microcosm had resided, was closed for re-development of the entire Hall. The coral reef exhibit was moved to the Smithsonian’s Laboratory at Fort Pierce, Florida, but unfortunately the Maine shore exhibit was not re-built. In the years following the field research that led to the exhibit and the execution of the rocky shore microcosms, Adey and Steneck (2001) published their theoretical biogeographic model of the world’s ocean coasts (a brief review of that paper and the A/S Model, is given in Chapter 3). The A/S Model has very much changed our view of the potential application of the cold-water microcosm systems described in this chapter. As we show in Figure 21.1 and Color Plate 33, the subtidal biota of the Gulf of Maine would lie not in the core Subarctic region of the biogeographic model, but rather in the 50–70% Subarctic transition zone, with northeast Atlantic Boreal species providing the remaining 30–50% of the biota. In this case, the contours shown are that of crustose coralline cover in the subtidal zones. As we will demonstrate later, the intertidal and infralittoral zones (between spring and neap low tides) of the Gulf of Maine (and Nova Scotia) are even more strongly Boreal in their biota. The initial purpose of this chapter is to briefly describe the rather similar structural habitat of the northwestern Atlantic rocky coast that results from a common geological history, especially the glaciation of the last several million years. However, we will then demonstrate the

strikingly different biotic character of the western Atlantic core Subarctic (northern Gulf of St. Lawrence, NE Newfoundland and Labrador) as compared to the mixed Subarctic/Boreal to the southwest (Nova Scotia and Gulf of Maine). This difference we attribute primarily to a geological history that creates lengthy coastlines and a Pleistocene long-temperature control of the biota (as circumscribed by the A/S Model). Thus, the patterns we describe are attributed to “bottom-up” factors. Many other scientists feel that “top-down” factors, or a trophic cascade created by the intensive fisheries of the region and the role of the green sea urchin (as controlled by those fisheries) are more important (see review, Steneck and Carlton, 2000). A mesocosm analysis of this basic problem would provide methodology for understanding and perhaps resolving an apparently intractable issue (Steneck, 1998); we have developed this presentation to encourage just such an approach. At the end of the chapter, we will describe the 17-year-old Maine “living model” system. A minor revision and preferably enlargement of this system we feel would provide secure answers to these questions. At the very least, such an endeavor would provide a considerably deeper understanding of the shore ecology of this region.

THE ROCKY, EMBAYED COAST OF THE NORTHWESTERN ATLANTIC GEOLOGICAL HISTORY As permanent bodies of water in essentially their present configuration, the Gulfs of Maine and St. Lawrence are only 10–12 000 years old. However, they have been basin-like features of the western Atlantic/ North American landscape for at least 3–5 million

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21. A Subarctic/Boreal Microcosm

FIGURE 21.1 Northwestern North Atlantic coast from Cape Cod to Labrador, showing the relative abundance (bottom cover) of Subarctic crustose coralline algal species. The contours represent greater than 90%, 95%, and 98% Subarctic cover and define the core Subarctic as we treat it in this book (see Adey and Steneck, 2001). The additional coralline cover (to reach 100%) consists of Boreal species in the south and Arctic species in the north.

years. When not filled with glacial ice, they have been basins and sometimes embayments or gulfs similar to their present shape for much of that time. The basic ecological character of the Gulfs and the open Atlantic coast is determined in many ways by its geology. The composition and orientation of its rocks and the sediments derived from those rocks are clearly crucial in their effects on communities of organisms and on

ecosystem function. Rocky shores dominate much of this coast, but bays, mud flats, and marshes are conspicuous, and in deeper-water muddy to gravelly/ shelly bottoms cover very large areas. Here we will concentrate on the rocky shores. The northwest North Atlantic coast sits astride the Appalachian Mountain chain built mostly by a complex of plate tectonic motions from 600 to 250 million years

The Rocky, Embayed Coast of the Northwestern Atlantic Geological History

ago (Chapter 3). The primary basement rocks on much of the coast are granitic or moderately metamorphosed sedimentary rocks, although in Newfoundland uplifted and tilted sedimentary rocks provide for spectacular sea cliffs and an array of island/bay topography. When the proto Atlantic Ocean began to split open about 200 million years ago (see Figure 3.4), dead-end “side splits” or rifts occurred that were filled largely with volcanics or terrestrial sands eroded off the sides of the rift valleys. This is the origin of the Gulf of Maine, and although some of the lava layers are resistant to erosion and in places can be important in present-day shorelines (Bay of Fundy), mostly these softer rocks are more easily weathered-out. The Gulf of St. Lawrence basin similarly formed during an earlier “Atlantic” opening (several hundred million years earlier) that later became filled with flat-lying limestones, remnants of which remain as the island of Anticosti and as fringes in the northern and eastern Gulf. The same basic types of bedrock or basement rock that form the Gulfs and Newfoundland and Nova Scotia are abundantly present from the Hudson River southwest to about the Savanna River, between South Carolina and Georgia. Even the elongate side rift valleys, filled with volcanics and sands, are scattered along the entire east coast. However, beginning 50–150 miles inland from the coastline to well offshore, these older rocks were gradually buried under what is now hundreds to thousands of feet of younger sediments washed off the Appalachian Mountains and accumulated since the opening of the Atlantic Ocean. These Cretaceous and Tertiary sediments, to about 150 million years old, are the same kinds of soft “rocks” that originally buried the now rocky coast to the northeast. Northeast of Long Island, Cape Cod, and the array of larger and smaller islands that make up the huge ridge of glacial boulders, gravel, and sand that provides the dividing line between the southwest Atlantic coast and the northeast coast, these sediments are largely missing. Some tertiary sediment layers can be found as patches in the Gulf of Maine (and consolidated, but largely flatlying mid-Paleozoic limestones and sandstones occur in the Gulf of St. Lawrence). However, most of the sediment washed off the Appalachian Mountains and laid down along the coast since the Atlantic Ocean opened, has been bulldozed off the coast. The sediments were pushed to the south and east, repeatedly, over 1–3 million years, by huge masses of moving Pleistocene glacial ice (Figure 21.2). The dynamic interaction of a bedrock geology formed hundreds of millions of years ago with Pleistocene continental glaciation thus produced the physical environment that circumscribes the biogeography that we seek to model.

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Oceanography Unlike most coastal basins, in the Gulf of Maine, the rivers are short and relatively small. The freshwater runoff into the Gulf is minimum, and the Gulf of Maine is not an estuary. Furthermore, a deep, submerged valley (Northeast Channel) was created by plumes of glacial ice, as shown in Figure 21.2. This allows deeper continental slope water access into the Gulf (Figure 21.3). The latter is a relatively warm and salty, nutrientand oxygen-rich water that largely prevents nutrient depletion and is ideal for enhancing primary production. The prevailing and often stiff northwest winds of winter repeatedly blow the surface waters out of the Gulf, resulting in overturn of Gulf of Maine waters with slope waters about once a year (Figure 21.4). The prevailing westerly winds and coriolus forces then drive a constant counter-clockwise gyre in the Gulf as deep, nutrient-rich waters work their way up into the water column and are finally driven offshore. In its general pattern of circulation and yearly overturn, the Gulf of St. Lawrence is similar to the Gulf of Maine (Figure 21.5). However, it differs in four very important ways: (1) the St. Lawrence River is the 16th largest in the world, by mean yearly volume; however, its outflow is largely restricted to the south side of the Gulf of St. Lawrence as the Gaspe Current, and having been thoroughly mixed with salty Gulf water in the big tides of the inner estuary, provides a strong, coastal salinity outflow in the southern part of Cabot Strait. From there it flows as a coastal current along the Nova Scotia coast to become the SSV inflow to the Gulf of Maine shown in Figure 21.3. (2) The deep water flows up the Laurential channel (equivalent to Northeast Channel current in the Gulf of Maine) is similar to the Maine Bottom Water in salinity, though a little cooler and denser. However, overlying the deep water is a midlayer of fresher and very cold water, near or below 0°C, that is the lower end of the highly chilled winter water mass in the Gulf. (3) Together these cold-water masses upwell in the outer St. Lawrence estuary, in the area of Pt. des Monts, due to tidal effects and internal waves in the Gulf against the sharp shallowing of the Laurential channel in that area. (4) While a large tidal range exists in the innermost estuary that assists in rapidly mixing the river fresh water with that of the relatively highsalinity deep and mid-water, it is effective only over a small area of the Gulf of St. Lawrence. Most of the Gulf has a microtide, less than 1 meter in range, and like the Gulf of Maine, most of the Gulf of St. Lawrence is an epicontinental sea and not an estuary. In the Gulf of Maine tectonic forces followed by glaciation have done more than just create a swirling basin that is constantly refilled with offshore water.

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FIGURE 21.2 The Laurentide Ice Sheet at its point of maximum extension; note at 18 000–22 000 years BP, the last or Wisconsinian glaciation, the ice extent may have been a little more limited on the eastern coasts than what is shown here. Preglaciation stream valleys had focused repeated glacial erosion during the 1–3-million year Pleistocene. The net result was the carving of broad depressions in softer rocks, ultimately giving rise to the Gulfs of Maine and St. Lawrence. Plumes of the ice sheet carved out the deep channel entrances to both Gulfs. From Denton and Hughes (1981). Reprinted by permission of John Wiley & Sons, Inc.

The water mass of the Bay of Fundy is just about the right size to match the oceanic tidal wave and allow very large tides (Chapter 2). This, in turn, creates additional tidal mixing that further limits nutrient depletion and prevents the extremes of temperature and winter sea ice formation that characterize the Gulf of St. Lawrence and many other continental embayments at high latitude. Furthermore, although the winter

northeaster storms may be fearsome, the fetches are short, the Gulf coasts relatively protected, and giant waves are not nearly the stringent ecological factor that they are on many rocky coasts (e.g. the western shores of the British Isles). The northern shore of the Gulf of St. Lawrence, with west-flowing currents, is largely removed from the more dynamic mixing of the inner and southern Gulf. In part,

The Rocky, Embayed Coast of the Northwestern Atlantic Geological History

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FIGURE 21.3 Idealized diagram of the Gulf of Maine with its off-lying banks and entrance channels. ⇐ Deep currents; ⇐ shallow currents,

⇐ winter “blowoff” over George’s Bank. Sv (Sverdrups)⫽106 m3/s. Modified after an original diagram by Brown and Beardsley (1978) with flow rates from various sources.

the surface water masses are derived from the Labrador current (from inflow on the north side of Cabot Strait) and in a smaller way through the Strait of Belle Isle. There is also a tendency for shore upwelling of deeper and colder winter water due to the prevailing westerlies. The summer maximum temperatures on this coast are 8–10°C, similar to that in northeastern Newfoundland. Southern Labrador is a little cooler at 6–10°C. However, the temperatures of all of these shores lie within the peak of a large coastal area indicated for the entire Pleistocene by the A/S Model. This is called the North Atlantic Subarctic Region and it is an offshoot of the much larger North Pacific Subarctic. The

western Newfoundland shore is affected by the sunwarmed onshore westerlies in summer; the southern Gulf is shallow and being warmed by the winds off the land in summer is the warmest body of sea-water north of Cape Cod. With the Scotian Shore current derived from the warm southern Gulf in summer and with a moderate tide range, the Nova Scotia Atlantic coast is mostly 14–16°C in the late summer. The Gulf of Maine lacks coastal winter sea ice and would be quite warm in summer except for the extensive tidal mixing (see Chapter 2) that prevents surface waters from warming too steeply. Except for an area around the mouth of the Bay of Fundy, where mixing is extreme and summer

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FIGURE 21.4 Temperature and salinity (thus density) characteristics of the major water masses in the Gulf of Maine as they pass through their yearly cycle of modification. Introduced as lower slope water in the deep Northeast Channel, passing through bottom and intermediate levels, finally to reach the surface, only to be largely blown out of the Gulf in winter northwesterlies, a given water mass changes in temperature and salinity (and thus density) as it passes through its Gulf of Maine cycle. The salinity/temperature characteristics of the equivalent Gulf of St. Lawrence and Newfoundland water masses are also shown (see Figure 21.5). From Hopkins and Garfield (1979).

temperatures are near 10°C, most of the Gulf of Maine shore is 12–16°C in late summer. These parameters are illustrated graphically in Color Plate 33.

THE GULF OF MAINE A Mixed Subarctic/Boreal Biota The shore model ecosystem we describe below was built to match a moderately protected bay with a ledgy

or cobbly shore either in the Casco Bay region or on locally cobbly shores anywhere along the Maine coast (see Figure 18.3; also the profiles shown in Figures 21.6 and 21.7). In the subtidal zone, the limitation to rocky bottom, not covered with glacial sand and silt, is very much dependent on exposure, with its waves and currents. The limit to significant vegetation provided by light penetration, limited in turn by water turbidity, due to plankton and suspended clays and silts, is close to that of the bottom sediment. Far

The Gulf of Maine

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FIGURE 21.5 Movement of the major water masses in the Gulf of St. Lawrence. As Figure 21.4 shows, deep water in this epicontinental sea is a few degrees colder and thus denser than Gulf of Maine Bottom Water. Also, mid-water, a leftover from the very chilled winter water of the Gulf of St. Lawrence is on average a little lighter than deep water and is brought to the surface as a very cold upwelling in the St. Lawrence estuary, where large tides provide for extensive mixing. The resultant light water mass (mixed mid-, deep, and river water) flows out of the Gulf over the heavier, deeper water, but because of coriolus forces is kept on the south side of the Gulf. This warms extensively in summer while the surface waters in the northern Gulf and in Labrador and much of Newfoundland remain cold.

offshore, at Cashes Ledge, the limit of rocky bottom, and its appropriate algal vegetation extends to 50 meters compared to the 20–30 meters characterizing the outer Maine coast and progressively less in bay environments. Although wind, waves, and tides provide a “drive” for shore ecological processes (with new nutrients mostly coming from elsewhere with the water), the essential energy requirements of the rocky shore systems of the Gulf of Maine are derived from solar

energy through higher plant and algal photosynthesis. In this environment, benthic production rates can be many times higher than that of planktonic algae, and thus, primary production along the long and often convoluted shore of the Maine coast is an important element in the overall ecology of the Gulf. Benthic primary production in the coastal Gulf of Maine is accomplished in three quite different habitats (rocky shores, salt marshes, and shallow muddy bottoms) by quite different biological groups. Rocky shores

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FIGURE 21.6 Section across idealized mid-bay from the central coast of Maine (see Figure 21.1).

, bedrock;

, glacial till;

, clay from postglacial high sea level at 13 000–12 000 years BP, subsequently weathered at low sea levels from 10 000 to 6000 years BP;

, recent fine silts.

FIGURE 21.7 Idealized section off the outer coast of the central coast of Maine. Strong wave action has largely removed the postglacial sediments characterizing more protected areas.

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The Gulf of Maine

in the Gulf of Maine are heavily dominated by algae with many species from all of the major algal groups. The ancestors of these algae evolved in the oceans over a billion years ago and preceded life on the land. Those in the intertidal have simply developed the means of withstanding a wide temperature range and in some cases an element of drying. Having optimized the rather opposing requirements of all plants for light and water, rocky shore algae can be highly productive. Salt marshes on the other hand are dominated by terrestrially derived flowering grasses and rushes, although species of other groups of flowering plants and many, mostly smaller, algae are also present (Chapter 14). Salt marshes can also be highly productive. A few species of flowering higher plants, from widely separate families, which are characteristically submerged in freshwater habitats on land, have moved into the fully marine environments on soft, mostly subtidal bottoms. Only a single species, Zostera marina (eelgrass), extensively occupies this habitat in the Gulf of Maine. However, it is widespread on protected shores to perhaps 5 meters below low water. Finally, on the soft mud of flats and shallow bay bottoms, unicellular algae, mostly diatoms, form an extensive golden-brown mat. While the productivity of this diatom mat is well below that of the marsh grasses, eelgrass, and rocky shore macroalgae, the areas involved are large and the contributions to overall primary production are significant. The uppermost fringe of rocky intertidal zones tends to be characterized by lichens or highly resistant bluegreen algae (cyanobacteria), while the sandy or muddy upper and lower fringes of rocky shores in protected bays, particularly in coves or along pocket beaches, harbor marsh species, and Zostera marina, respectively. However, most rocky shores in the Gulf of Maine are dominated by macroalgae (this may be changing now due to human eutrophication). Many unicellular and small filamentous species are present in these environments. However, it is the large brown algae, one-half to many meters long and 5–15 years old at maturity that are most conspicuous. Many red algae, particularly in the lower intertidal and subtidal, along with scattered greens, in the few to 10–20 cm size range, are ubiquitous. However, these algae tend to form a lower, encrusting, and bushy understory with the browns providing the canopy. The general relationship between tide range and depth, and the principal algal species, is shown in Figure 21.8, and the mean biomass of standing crop from many stations in the Casco Bay area is given in Figure 21.9. In general, the description of Gulf of Maine shores that we provide is that of the latter half of the 20th century. It is likely that anthropogenic-driven changes are now under way.

There are approximately 400 species of benthic algae in the Gulf of Maine. Identification of most of these species can be accomplished with Sears (2002), NEAS Keys to the Marine Algae, and with the backup of the drawings in Taylor (1957). Luning’s (1990) volume Seaweeds provides a background on algal ecology and biogeography. Additional references that can assist with algal and animal identification for Gulf of Maine and North Atlantic rocky shores in general are Gosner (1978) and Morton (1991). Hayward (2004), Hawkins and Jones (1992), and Raffaelli and Hawkins (1996) provide excellent modern ecological treatments of rocky shores in general. Intertidal Ascophyllum nodosum (knotted wrack) is the single most important benthic or attached algal species in most of the Gulf of Maine. Achieving mean wet standing crops of over 30 kg/m2 on protected shores (Figure 21.10), with over 50 kg/m2 maximum, and over 12 kg/m2 on exposed shores, A. nodosum is a crucial community-structuring element (Color Plate 34). In addition, with a mean net primary production of typically 8–25 kg/m2/year (wet weight), A. nodosum also provides over 50% of the intertidal primary production of the Gulf of Maine and a significant part of the entire near shore primary productivity. After A. nodosum, Fucus vesiculosus (bladder wrack) is the next most abundant alga in the extensive midintertidal bands of the Gulf of Maine. As a rather flattened fucoid, up to a meter long but more typically one-third to one-half meter, and with a prominent midrib and roughly dichotomous branching, F. vesiculosus is the chief competitor of, Ascophyllum on more exposed shores in the Gulf of Maine. Its paired vesicles (or float bladders) are quite distinctive and usually diagnostic to species. Several other rockweeds are abundant locally, for example Fucus spiralis at the upper fringe of the eulittoral and Fucus distichus (along with the kelp Alaria esculenta) at the other extreme, on very exposed infralittoral zones (Figure 21.10). The small, bushy reds Chondrus crispus and Mastophora stellata also occur under the rockweeds in the lower intertidal and in the infralittoral fringe where they can form extensive dense, red carpets (Color Plate 34). They become denser with exposure and can rise well up into the eulittoral on the outer coast, where wave action is constant. Many groups of invertebrates, and a very few coastal fish, have bottom grazing members. However, dominant grazers of the intertidal regions of the Gulf of Maine are gastropod snails and crustacea. The snails, or periwinkles in this case, are most important. Two Littorinid snails, Littorina littorea and Littorina

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FIGURE 21.8 Major benthic organisms on the rocky shores of the Gulf of Maine and Nova Scotia (modified from Mathieson et al., 1991). Note the Semibalanus zone is generally not as marked as shown here.

The Gulf of Maine

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FIGURE 21.9 Algal standing crop (summer) of rocky bottoms in the Casco Bay Region of the Gulf of Maine (kg dry weight/m2). Data points are the means of many stations of five 1/10 m2 quadrats. The subtidal at protected stations is largely muddy bottom with few algae, except for diatom mats or sometimes in summer, locally dense filamentous floating species. Zostera marina (eelgrass), a flowering plant, can be locally abundant at a few meters depth. At more exposed localities, algal standing crop (mostly kelps, shallower, and reds, deeper increases), though rarely to the levels of most intertidal areas.

obtusata (Figure 21.11) are the primary algae eaters in Gulf of Maine intertidals. They can play a primary role in determining the nature of the shore. Littorina saxatilis, a more subarctic species, occurs in the supratidal in a very patchy kind of way and can be hard to find. While gastropods can also fill a very wide variety of predatory roles, with their scraping radula, they are by nature well suited for a grazing or browsing role (see Chapter 15). L. littorea is a typical grazer, scraping turfs

and crusts off rocks, while L. obtusata generally eats pieces out of Ascophyllum stalks and is more appropriately termed a browser. While the two dominant littorinid species occur together almost everywhere in the intertidal, their local abundance varies considerably and in different ways. The distribution of obtusata is clearly directly related to the abundance of its favored host Ascophyllum nodosum. The abundance of L. littorea, on the other hand, does

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FIGURE 21.10 Standing crop (wet biomass) of dominant macroalgae in the upper, middle, and lower eulittoral (interdal) of protected, middle exposure, and exposed shores in the Gulf of Maine. For statistical analysis see Adey and Hayek (2005).

The Gulf of Maine

FIGURE 21.11 Numbers of individuals of three species of Littorinid snails from rocky shores in the Gulf of Maine, eastern Newfoundland and the Labrador Straits (the Core

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Subarctic centered on the Strait of Belle Isle) areas. The extraordinary shift of depth and exposure abundance of Littorina obtusata in the core Subarctic (right/center diagram) is accompanied by a marked change in shell morphology. From Adey and Hayek (2005).

384


not directly relate to rockweed cover, but apparently to physical factors, tidal exposure, and wave action. This snail does not graze when not covered with water, and tends to move to the subtidal in winter, so feeding rate is a function of elevation on the shore. It would also appear that the snails suffer some mortality in heavy wave action. Subtidal The algal scenery changes in a remarkable way below the level of low water spring tides. On rocky shores, the brown algae still dominate in shallow water, and the reds deeper, with only scattered greens to be seen. However, the algal groups, for the most part, are entirely different from those in the intertidal, and the diversity of species increases markedly. Wave action is the great mediator between the algae, their grazers, and their predators in turn. On the other hand, as one reaches deep water, 30 meters below mean low water offshore and increasingly less in more protected water, the lack of wave action allows sediments to accumulate and eventually bury the rocky bottom. When this happens, the potential for living space for most algae other than diatoms disappears, though the flowering “sea grass” Zostera marina can be abundant in bays. As shown in Figure 21.9, in bays and other protected areas, the algal standing crop or biomass is concentrated in the intertidal and is virtually absent in the mostly muddy subtidal. On more exposed shores, and particularly the outermost ledges and islands, the subtidal biomass increases to moderately high levels. On an idealized, exposed shore of consistent slope and surficial heterogeneity (surface roughness), the width of algalcovered bottom is roughly 5–10 times the intertidal width (Figure 21.12). Nevertheless, for the entire coast, the total subtidal algal biomass is typically only about twice that in the adjacent intertidal, while the yearly production is about equal. The limits to subtidal production, provided by the shading of plankton and sediment, both suspended and lying on the bottom, are thus critical to overall productivity of the near shore environment. The important species of kelps in the Gulf of Maine are perennials, and are deciduous in a sense. They tend to lose some or all of their blades in winter storms (Color Plate 35) and replace them by new growth in the spring and summer. Especially during winter northeasters, it is not only the blades that are torn off and delivered to the algal berms on the beach, but sometimes the whole plants, particularly those attached to mussels and smaller stones, find themselves on the beach in the process of being recycled. In general, the primary kelp bands of outer bays and exposed regions are characterized by yearly mean

production rates of 15–40 g (wet)/m2/day. However, these numbers obscure a dynamic process in which standing crops at the end of winter of 1–4 kg/m2 are built during the late spring and summer at rates of up to 60 g (wet)/m2/day to standing crops of 5–10 kg/m2 by the end of September (the lack of biomass to equal mean summer production is taken primarily by the sea urchins Strongylocentrotus drobachiensis at 1–30 g/m2/ day). The winter loss of roughly 4–6 kg/m2 is the biomass that is senesced, or torn up by storm waves, and delivered to the beach (Color Plate 35). The kelp species Laminaria longicruris and Laminaria saccharina form a major part of the subtidal algal biomass at most exposed and moderately exposed stations (Color Plate 38). They tend to occur a little deeper than Laminaria digitata and typically will form over 90% of the kelp biomass and more than 70% of the entire algal biomass at 5-meter depth. In these species, during the summer months, blade elongation rates from the meristem at the base of the blade are 0.5–1.2 cm/day. Productivity rates reach 10–15 kg/m2/ year (wet weight), exceeded only by the rockweed Ascophyllum nodosum, a species that spends roughly half of the time exposed, with no overlying turbid water to reduce incoming solar energy. Agarum cribrosum can be found at any depth in the subtidal zone, and is the only western Atlantic kelp with a mid-ribbed blade that, also, in most cases bears numerous, self-generated perforations. Typically, in the kelp zone, it occurs scattered beneath the larger canopy-creating kelps, though it can be the only kelp remaining where this zone has been heavily grazed by green sea urchins. Below the kelp zone, A. cribrosum is typically the largest alga to be seen, conspicuously rising above the low mass of red algae. More rarely it forms a low, but more or less continuous, canopy. In laboratory “taste tests,” it is the kelp least preferred by sea urchins, and it has been shown to possess distasteful and defensive chemical compounds. This diminutive kelp grows at half or less the rates of competing kelps, suggesting that it devotes a considerable part of its photosynthetic production to the building of noxious secondary compounds. On the outer coast, extending from under the kelp forest as it begins to thin from 5 to 10 meters depth, a halo of filamentous, shrubby, and foliaceous red algae, loosely coating boulders and cobbles, reaches down to 10, 15, or even 25 meters depth. With the standing crops of individual species almost always less than 500 g/m2 and often less than 100 g/m2, the 10–15 species of upright red algae that dominate in this zone are generally diminutive (less than 5–20 cm long) and often delicate. In many cases, they are beautifully textured and colored, though as with the kelps, they

The Gulf of Maine

385

FIGURE 21.12 Areal extent of significant subtidal standing crop of algae in the Gouldsboro Bay area of the eastern Maine coast. From Brittsan (1989).

become ragged and tattered due to grazing and wave action. Some species become extensively coated, or virtually “buried,” by encrusting colonial animals, especially bryozoans and hydroids. Phyllophora pseudoceranoides is primarily Boreal in its distribution. In the Gulf of Maine, it is one of the most abundant species of the red algal zone occurring at

virtually every station with a well-developed red algal zone. It averages about 20% of the subtidal red algal biomass. More so than any other red alga, all parts of the plant, except the upper few centimeters, become encrusted with bryozoans and encumbered with red algal epiphytes. In ecosystem models, with minimum grazing and with few bryozoans, it becomes a large,

386


bushy plant, lasting for many years, clearly being photosynthetic right to the base. Phycodrys rubens is a delicate, leafy 10- to 20-cm-long, bright pink/red alga, with a well-defined mid-rib and a strong “veined” pattern (similar to a higher plant leaf). Widely distributed through the colder North Atlantic and Arctic Oceans, both attached to rock and shell and as an epiphyte, particularly on Phyllophora pseudoceranoides, P. rubens is one of the most common alga of the red algae zone in the Gulf of Maine; due to its delicate nature and tendency, it tends to become tattered by grazing and wave action in the summer and fall. Beneath the canopy of kelps and the red algal brush, directly and usually tightly attached to the rock surface and to mussel shells, lies a layer typically 1–10 mm thick of red algal crusts. A few of these crusts are feltlike to leatherlike and more or less easily scraped with a fingernail; many to species of the widespread, crustose genus Peyssonnelia, though some are alternate stages for brushy red algae. In the Gulf of Maine the dominant elements of the crustose layer are calcified and members of the very large red algal family Corallinaceae. Coralline crusts grow very slowly in cold waters, marginally less than a few millimeters a month and in thickness less than a millimeter per year. They often structure the bottom and determine what other algal species can settle. Corallines continually slough off an outer layer of cells, like the bark of trees, and therefore greatly limit settling by other algae that would otherwise bury the coralline crusts with their holdfasts. Sea urchin explosions resulting in the intensive grazing of fleshy algae sometimes provide a “barren”-appearing “coralline–urchin” bottom. Even during times of minimum sea urchins, large bays, such as Penobscot, Blue Hill, and Frenchmans, with moderate locally created waves that limit silt and yet are not a serious limitation to sea urchins, can show extensive coralline–sea urchin bottoms. As we discuss below, the core Subarctic Region is characterized by coralline sea urchin bottoms. As in the terrestrial forest that lines most of the shores of the Gulf of Maine, relatively little of this considerable rocky shore algal production (as well as that of the marsh grasses that often occur at the heads of bays) is directly eaten by grazers (on the order of 25–35%). Some of the remainder is buried in marshes or in soft muddy bay bottoms, rather temporarily in a geological sense. Most, however, becomes detritus that lines the shores and makes up part of the “soup” that characterizes Gulf waters and is used and reused by the numerous filter feeders that are the subject of Chapter 17. In the living systems modeling context, over 60% of the energy supply for this kind of system is processed through the water column. In spite of dominant detrital processes, grazers are still important to the coastal

ecology of the Gulf of Maine. Not only do they transfer the energy captured, from mostly algae in this case, up a complex food web, but also they frequently are decisive factors in community structure. Algae would appear to be defenseless against the depredations of grazers and, indeed, sometimes they are, as the occurrence of urchin barrens attests. However, some algae develop resistant skeleta, such as the calcium magnesium carbonate of corallines, and indeed sea urchin barrens are more appropriately called coralline–sea urchin bottoms, because, like mini-coral reefs, they are hardly barren. Others develop toxic or distasteful compounds, such as the deep kelp Agarum, the bush brown alga Desmarestia viridis and the brush red Ptilota serrata. Many have evolved to produce abundant spores, and, once settled, to grow very fast. The algae that develop direct defense mechanisms give up some energy supplies to produce the defenses, and, in so doing, they lose their ability to grow fast. In a sense, algae are competing against each other for space and light, while they participate in a defense “race” with grazers. When grazers remove or limit the undefended fast-growing algal species, less competitive species dominate a shore. When grazers are absent or rare, because they have been removed by wave action or a predator, typically, a few fast-growing species totally dominate a shore. All of these effects occur on the Gulf of Maine coast, and the result is, in a broad view, well-defined patterns of community structure, but in detail, an often very patchy, mosaic-like bottom. The “normal” state of the rocky, upper subtidal is as described briefly above, with a wet biomass or standing crop, of perhaps 5000–10 000 g/m2 in the kelp zone. In the bushy red algal zone, the biomass reduces to 1000–2000 g/m2. Finally, algal biomass becomes negligible (best described by aerial coverage) in the crust zone. Under these conditions, none to a few adult green urchins are found per square meter. The alternate “overgrazed” state is that in which many tens of urchins occur per square meter, there are a ragged few kelps, if any, and the bushy reds are much reduced. This produces a coralline–sea urchin bottom of greatly reduced productivity. There is little question that strong wave action reduces the effects of urchins, and typically bays more commonly have coralline–urchin bottoms while exposed coasts are rich in kelp beds. Numerous species of higher predators are often abundant on rocky shores. The Maine intertidal region is relatively free of higher predators, and that certainly is a prime reason for grazing organisms to live there. However, sea gulls browse for snails, or any invertebrate that moves for that matter, and green crabs, starfish, and the dogwinkle (Nucella) enjoy limited success, depending on the amount of algae for cover, the weather,

The Core Subarctic

and the state of the tides. Indeed the starfish Asterias, feeding on mussels (in the lower intertidal), and the dogwinkle, feeding on barnacles, can locally determine the abundance of these filter feeders. Certainly this is a factor in the near exclusion of fucoids from smooth granite domes where barnacles often dominate and cover for dog winkle is minimal. It also seems likely that the increasing availability of anthropogenic nutrients is increasing the abundance of plankton and therefore the barnacles that feed on the plankton. Subtidally, mid to upper levels of food webs are complex. Lobster, rock and green crabs, the waved whelk, and the sea star are the largest and most abundant of many, generalized predators at mid-levels. Fish, particularly the pollack, tom cod, cunners, and wolffish are the higher-level predators today, though prior to intensive trawler fishing numerous other species including young cod and haddock were probably present. Today the river otter is an occasional top predator. Introductions are also likely a factor particularly in that key species such as Littorina littorea and the green crab are both thought to be introductions from Europe. As we shall describe below, many species in the Gulf of Maine are derived from European Boreal shores, and the numbers are probably increasing, aided by human transport in the bilges and on the bottoms of ships.

THE CORE SUBARCTIC The N. Gulf St. Lawrence, NE Newfoundland, S. Labrador These coasts of the western North Atlantic are shown by the A/S Biogeographic Model to form a core Subarctic Region (Figure 21.1, Color Plate 33); a continuous region in which a considerable area of coast exists at summer temperatures of 5–10°C and winter temperatures near 0°. This is an area dominated by species that are less abundant to the north and south and in which species from outside regions (in this case the Arctic and the Atlantic Boreal) are absent or reduced in their occurrence. We will briefly examine the abundance of seaweeds and the principal grazers and predators at the center of the Subarctic Region, the Labrador Straits area, in comparison with that previously described for the Gulf of Maine, which as Figure 21.1 shows is on the fringe of the Subarctic. Intertidal The Core Subarctic Region is characterized by winter sea ice. When ice is moved by waves against exposed shores, most algae and invertebrates can be scoured off

387

the rock substrate in the intertidal and uppermost subtidal. However, where rock ledges, islands or an early formed ice foot protects the shore, fucoid buildup can be considerable (Color Plate 39). Figure 21.13 shows the biomass of the fucoids and a highly branched, stringy brown algae Chordaria on these shores. As compared to the Gulf of Maine (Figure 21.10) and the outer coast of Nova Scotia, the overall algal biomass on Subarctic shores is reduced by one-half to one-third, but the patterns of abundance distribution with height on the shore and exposure are generally similar. However, Ascophyllum nodosum, the overall dominant in Maine and Nova Scotia, becomes a very minor element in the core Subarctic. The two Fucus species, F. vesiculosus, higher and more protected, and F. distichus, lower and more exposed, totally dominate the shore. In the lower third of the intertidal, and continuing into the infralittoral, the Gulf of Maine and Nova Scotia dominants, Chondrus crispus and Mastophora stellata, virtually disappear. Chordaria flagelliformis, and several associates (Color Plate 39), occasionals in the Gulf of Maine, become abundant (sometimes dense in the infralittoral). The grazing snail populations, shown in Figure 21.11, change radically. The highly abundant, and dominant Littorina littorea in Maine becomes a minor element, except in inner bays and Littorina saxatilis, an occasional supratidal species in Maine becomes the dominant grazer on Subarctic shores; Littorina obtusata appears to change in both morphology and ecology, this is so marked that some scientists have called it an entirely different species. Finally, the barnacle Semibalanus balanoides becomes much less abundant in the Subarctic while the abundant predatory dogwinkle Nucella lapillus of the Gulf of Maine virtually disappears. As we have discussed above, the infralittoral zone, between low water neaps and low water springs, in Nova Scotia and the Gulf of Maine is characterized by a very distinctive and often dense band of mostly Irish moss (Chondrus crispus) (Color Plate 34). While this species can sometimes be found with a search in the core Subarctic, it is mostly replaced by Chordaria flagelliformis. This is not simply a matter of ice scraping, since in northeastern Nova Scotia, which is frequently scoured by winter sea ice, Chondrus crispus although more patchy remains an infralittoral dominant. As shown in Table 21.1, which compares the dominant seaweed species in the infralittoral and uppermost sublittoral between Cornwall, England (the center of the Atlantic Boreal) and the center of the Subarctic, the Gulf of Maine is 78% Boreal species and the Atlantic Nova Scotia coast 99% Boreal species. On the same basis, from two independent studies, the core Subarctic, the lower parts of Figure 21.13, is 96–98% Subarctic in species composition.

388


FIGURE 21.13 Standing crop (wet biomass) of dominant macroalgae in the upper, middle, and lower eulittoral (intertidal) of protected, middle exposure and exposed shores in the Labrador Straits area (the Core Subarctic centered on the Strait of Belle Isle). For statistical analysis see Adey and Hayek (2005).

389

The Core Subarctic TABLE 21.1 Regional Comparison of Macroalgal Biomass Exposed and Intermediate Stations (0–2 m) 5 years. Ice/no ice Conception Bay Keats et al. (1985)

(⫹0.2/2⫻0.5/2.5 m) 12 Stations, 47 quadrats Core Subarctic (this study)

Alaria esculenta Chordaria flagelliformis Dictyosiphon foeniculaceus Agarum clathratum Desmarestia viridis Fucus distichus Saccorhiza dermatodea Devaleraea ramentaceum Pilayella littoralis Acrosiphonia arcta Polysiphonia urceolata Laminaria longicruris

3418 (82) 240 (6) 21 (0.5) – 4 (Tr.) – 257 (6) 58 (1.4) 2 (Tr.) 51 (1.2) 33 (0.8) –

1430 (36) 1017 (26) 297 (8) 267 (7) 242 (7) 178 (5) 144 (4) 85 (2) 41 (1.0) 41 (1.0) Tr. –

429 (8) – – 44 (0.8) Tr. Tr. 19 (0.4) 2 (Tr.) – Tr. – 695 (13)

37 (0.4) 7 (Tr.) Tr. – 4 (Tr.) 26 (0.2) 35 (0.4) Tr. Tr. 1 (Tr.) – –

– – – 0 – 0 0 0 0 0 0 0

% Subarctic

98

97

22

1

T

Laminaria digitata Palmaria palmata Laminaria saccharina Chondrus crispus ⫹ Mastophora stellata Phyllophora pseudoc. Corallina officinalis Fucus serratus Rhodomela confervoides Himanthalia elongata Laurencia spp. Leathesia difformis Lomentaria articulata

65 (1.6) 18 (0.4) – –

119 (3) 28 (0.7) 8 (0.1) –

620 (11) 17 (0.3) 635 (12) 2758 (52)

3623 (39.5) 4 (Tr.) 2686 (29) 2628 (24)

21% 1% – 19%

– – – – 0 0 0 0

– Tr. – Tr. 0 0 0 0

57 (1) 25 (0.5) – – 0 0 0 0

– 100 (0.1) 16 (Tr.) 5 (Tr.) 0 0 Tr. 0

– 19% 4% – 19% 12% 4% 1%

% Boreal Mean total biomass (g/m2)

2 4167

4 3897

77 5301

98 9172

100

Biomass g (wet)/m2 (% of total) (Tr ⫽ trace)

Subtidal In the core Subarctic sublittoral, something structurally very different happens. A glance at Figure 21.8, the “standard” for the Gulf of Maine and Nova Scotia as compared to Figure 21.14, clearly shows this difference. “Sea urchin barrens” occur sporadically in the larger inner bays in Maine and in certain years of sea urchin “explosions” in Nova Scotia. However, the pattern shown in Figure 21.14 (and Color Plates 41 and 42) appears “permanent.” Some authors have argued that the keystone species, the sea urchin Strongylocentrotus drobachiensis, has exploded because it has lost its controlling predators, probably mostly the codfish (Steneck and Carlton, 2000). However, one of us (WHA) covered virtually the entire area of core Subarctic in 1964 by SCUBA, and coralline bottoms, as shown in Color Plate 41, were highly dominant. Furthermore, it was not unusual to find a thickness of 5–10 cm of coralline crust over rock substrate. Considering clam and worm boring, occasional wave breakout and surface grazing,

(⫹0.5/0.5/2.5 m) 8 Stations, 40 quadrats Gulf of Maine (this study)

(⫹0.2/0.5) 16 Stations, 61 quadrats Nova Scotia (this study)

(0–2 m) Devon and Cornwall Lewis (1964)

and the well-known, low growth rates of coralline, these crusts would have represented a minimum of 15–30 years’ growth. Although a coralline crust occurs under dense kelp, it tends to be more patchy in that situation, and rarely develops to great thickness. It seems likely that coralline/urchin bottoms that were abundant in the core Subarctic in 1964 had existed at least as far back as the Second World War and before. At that time, fishing pressure was far below the effort that eventually drove the northwest Atlantic cod to commercial extinction. Except for species chemically protected against sea urchin grazing (like Agarum clathratum, Desmarestia viridis, and Ptilota serrata), in the core Subarctic, large macrophytes (kelps) only exist in scattered patches or in refugia. On exposed shores, subject to heavy wave action, the Alaria esculenta zone (with scattered Laminaria digitata and Saccorhiza dermatodea) is a refugium. Here, sea urchins tend to be removed by wave scour. Also, sea urchin larvae settling from the plankton seem to prefer coralline bottoms, or at least are unable to settle on

390


FIGURE 21.14 Major benthic organisms on the rocky shores of the northern Gulf of St. Lawrence, southern Labrador and northeastern Newfoundland. The “mound” off muddy/gravelly bottoms on the low-energy side of the diagram represents rock bottoms, isolated in mud, sand, or gravelly bottoms within bays. These are kelp “refugia” from intense urchin ( ⫽ S. droebachiensis). Diagram modified after Himmelman (1991).

unstable sediment bottoms or even directly on kelp (probably because of their extensive mucous production). Thus, there are additionally in-bay refugia for kelp, where they can be locally abundant on rocky projections because they are inaccessible to sea urchins. The urchins apparently lack the inability to move across sediment bottoms in any quantity. In contrast, sea urchins in Nova Scotia and the Gulf of Maine are near their temperature limits. They become subject to protozoan disease over 10–12°C, and do not have a continuous presence over those temperatures. Thus, in these areas, kelps are more widespread and the coralline/urchin “barrens” more patchy in space and time. In recent decades, extensive harvest of urchins for a roe fishery has been a secondary factor, mostly in the Gulf of Maine, and this has tended to increase algal biomass or standing crop. Tables 21.3 and 21.4 show the comparative abundance of seaweeds for more exposed stations in the Gulf of Maine and the core Subarctic. Table 21.2 covers the Alaria zone and Table 21.3 the deeper Agarum/ Desmarestia zone (see Figure 21.14). The core Subarctic, at 96–98% Subarctic species, and the Gulf of Maine at 60–62% Subarctic species, provides a pattern that is close to that shown for the previously published crustose corallines in Figure 21.1. In the Subarctic, the

shallow subtidal is highly dominated by Alaria esculenta, with several other kelps occurring occasionally and with no significant underlying turf of brushy reds. This contrasts sharply with the Gulf of Maine shore, where the kelps Laminaria longicruris, Laminaria digitata, and Laminaria saccharina are more or less equally abundant and Chondrus crispus forms a significant underlying turf. In Maine, Alaria is more scattered, occurring (like Fucus distichus shallower) mostly at the most highly exposed stations. Deeper in the subtidal, Agarum cribosum is the dominant kelp in the core Subarctic, followed by the often large, very bushy Desmarestia vividis. The underlying red turf includes Ptilota serrata, Phycodrys rubens, and Callophyllis cristata, none very abundant on the extensive coralline crust of mostly Clathromorphum and Lithothamnion spp. At the deepest algal zones, the Arctic species Turnerella pennyi is also common, though it rarely produces significant biomass. In the same situation in the Gulf of Maine, there is a broad array of kelp species though biomass is a third of that shallower; Agarum cribosum occurs scattered in moderate abundance. The underlying red turf is dominated by Phyllophora pseudoceranoides with lesser amounts of Chondrus crispus, Phycodrys rubens and a diversity of minor species.

391

The Core Subarctic TABLE 21.2 Seaweeds Commonly Occurring in Manually Harvested Square Meter Quadrats at 0.5 m and 2.5 m Depth (see Text), at High and Medium Exposure Sites Exposed and mid-exposure stations

No. of stations

No. of quadrats

X (g/m2)

%

31

1 1 4 5

2 4 4 13

4 3 5 4

24 17 15 14

11 2

22 2

⫺

Chordaria flagelliformis Petalonia fascia Pilayella littoralis Antithamnion borealis Rhodomela confervoides Ectocarpus spp. Dictyosiphon foeniculaceus Fucus distichus Desmarestia aculeate Spongomorpha arcta Ptilota serrata

184 Tr. 1.9 1.4 0.8 3.1 1.1 17.6 1.4 Tr. Tr.

4.0 Tr. Tr. Tr. Tr. Tr. Tr. 0.4 Tr. Tr. Tr.

9 5 4 7 2 5 3 3 2 2 2

14 6 8 8 2 10 3 4 2 2 4

⫺ ⫺ ⫺ ⫺ ⫺ ⫺ ⫺ ⫺ ⫺ ⫺ ⫺

Devaleraea ramentaceum Desmarestia viridis Saccorhiza dermatodea Agarum clathratum Alaria esculenta

2.8 245 138 218 2964

Tr. 5.3 3.0 4.8 64.6

3 7 4 6 9

4 10 6 9 17

⫺ Tr. 37.5 88 857

Laminaria saccharina Laminaria longicruris Callophyllis cristata Phycodrys rubens Stilophora rhizodes Polysiphonia spp. Ceramium spp.

325 334 0.5 0.7 Tr. 1.1 Tr.

7.1 7.3 Tr. Tr. Tr. Tr. Tr.

3 1 4 5 1 5 2

9 5 4 8 1 8 2

1200 1389 60 22.5 ⫺ 40.3 134

0.7 2.2

4 3

12 14

Laminaria digitata Palmaria palmate Corallina officinalis Chaetomorpha spp. (⫹ Rhizoclonium/Cladophora) Cystoclonium purpureum

96.3 47 1.5 Tr.

2.1 1.0 Tr. Tr.

5 2 6 1

6 2 6 2

1193 34 48.8 20

19.5 0.6 0.8 0.3

5 3 5 4

24 10 24 18

⫺

⫺

10.3

0.2

2

Chondrus crispus (⫹ Mastocarpus stellatus) Agardhiella tenera Phyllophora pseudoceranoides Ahnfeltia plicata Polyides caprinus Asparagopsis hamifera Callithamnion corymbosum Porphyra spp.

Tr.

Tr.

847

13.9

5

24

⫺ ⫺ ⫺ ⫺ ⫺ ⫺ ⫺ 4582.2

⫺ ⫺ ⫺ ⫺ ⫺ ⫺ ⫺

14 114.5 1.5 Tr. 2.3 Tr. Tr. 6113.7

0.2 1.9 Tr. Tr. Tr. Tr. Tr.

4 4 2 2 2 1 1

10 13 5 5 13 1 2

19.6 22.7 1.0 0.4

46.5% 21.4%

2

Tr. 0.6 1.4 14.0

16%

1

0%

Tr.

3.2%

Tr.

14.4%

7

0.5 and 2.5 m Turnerella pennyi

77.7%

No. of quadrats

4.4%

No. of stations

16%

Tr.

Species ranked according to coldest (top) to warmest (bottom) based on ranges from Luning (1990), Sears (2002), and Taylor (1957). The Boreal/Subarctic break is a hypothesis for testing abundance in the core Subarctic (see Figure 21.1) as compared to the southern British Isles (core Boreal). Tr ⫽ trace amount.

Subarctic

%

Boreal

X (g/m2)

Gulf of Maine

Arctic

Subarctic (NE Newfoundland and Labrador)

392

21. A Subarctic/Boreal Microcosm TABLE 21.3 Seaweeds Commonly Occurring in Manually Harvested Square Meter Quadrats at 5 and 10 m Depth (See Text), at High and Medium Exposure Sites Exposed and mid-exposure stations

No. of stations

No. of quadrats 28 9

Petalonia fascia Pilayella littoralis Antithamnion borealis Rhodomela confervoides Ectocarpus spp.

Tr. Tr. Tr. Tr. 2.0

Tr. Tr. Tr. Tr. 0.1

1 2 8 1 2

Ptilota serrata Membranoptera alata Desmarestia aculeata Alaria esculenta Desmarestia viridis Agarum cribosum Saccorhiza dermatodea Devaleraea rementacea

5.5 Tr. 0.5 125 601 1242 14.8 Tr.

0.3 Tr. Tr. 6.2 29.8 61.5 0.7 Tr.

Laminaria saccharina Laminaria longicruris Callophyllis cristata Phycodrys rubens Ceramium spp. Polysiphonia spp.

18.3 ⫺ 0.3 3.4 ⫺ 1.2

0.9 ⫺ Tr. 0.2 ⫺ Tr.

8

49

⫺

Tr.

Tr.

1

1

1.1%

8 3 2 5 7 11 1 1

16 5 2 6 13 24 1 1

12.8 ⫺ 12.5 19 12 276 20 ⫺

0.5

2

13

0.5 0.8 0.5 11.4 0.8 ⫺

1 2 3 8 2

6 3 3 38 2

1

2

5 7

10 11

4

4

634 272 46.6 75.5 18.2 46.6

26.3 11.3 1.9 3.1 0.8 1.9

7 4 6 7 3 6

32 10 19 37 12 14

1 4

1 5

636 7 1 39.6

26.4 0.3 Tr. 1.6

5 5 4 5

12 19 16 27

14.5%

98.2%

˚

2 2 11 1 3

No. of quadrats

28.3%

13 4

No. of stations

45.3%

Tr.

%

Tr.

1.1

0.1%

5 and 10 m Turnerella pennyi

X (g/m2)

0.2 Tr. ⫺ ⫺

Chondrus crispus Callithamnion corymbosum Phyllophora pseudoceranoides & membranifolia. Polyides rotundus Agardhiella tenera Antithamnion cruciatum Lomentaria orcadensis Chaetomorpha spp. Porphyra spp Ulva & Monostroma spp.

⫺ ⫺ ⫺

⫺ ⫺ ⫺

49 Tr. 214.5

2.0 Tr. 8.9

6 1 5

26 1 33

⫺ ⫺ ⫺ ⫺ ⫺ ⫺ ⫺ 2020

⫺ ⫺ ⫺ ⫺ ⫺ ⫺ ⫺

Tr. Tr. Tr. Tr. 3.5 3.8 13 2412.6

Tr. Tr. Tr. Tr. 0.1 0.2 0.5

2 2 1 1 3 2 3

3 6 2 1 11 8 14

0%.

11.7%

5 Tr. ⫺ ⫺

0.2%

Laminaria digitata Corallina officinalis Palmaria palmata Cystoclonium purpureum

Subarctic

%

Boreal

X (g/m2)

Gulf of Maine

Arctic

Subarctic (NE Newfoundland and Labrador)


Table 21.4 shows the shallow and deeper subtidal algal biomass on isolated rock refugia from five bays or harbors scattered across the core Subarctic. These communities are highly dominated by Laminaria longicruris, followed by Laminaria saccharina, with a scattering of other kelps and red turfs. Laminaria longicruris is an

endemic in the North Atlantic core Subarctic, occurring as well on fringing Nova Scotia and Gulf of Maine shores. However, in-bay refugia appear to be the primary habitat in the core Subarctic Region. In summary, in the upper subtidal, the core Subarctic appears to have a highly distinctive community as well

393

Core Subarctic vs Mixed Subarctic/Boreal TABLE 21.4A Seaweeds Commonly Occurring in Manually Harvested Square Meter Quadrats at (a) Combined and 0.5 ⫹ 2.5 m (See Text), at Wave Protected Sites

No. of quadrats

7 2 1 2 2 2 2

9 2 1 2 3 3 2

2 1 3 3 4

2 1 3 3 4

50%

2 2 1 2 1 2

2 2 1 3 2 3

7.0%

1 1 1 1

1 1 1 1

Infralittoral 0.5 and 2.5 m Chordaria flagelliformis Petalonia fascia Pilayella littoralis Antithamnion borealis Ectocarpus sp. Rhodomela confervoides

43 Tr. Tr. 0.7 0.6 34

1.2 Tr. Tr. Tr. Tr. 1.0

Fucus distichus Spongomorpha arcta Devaleraea ramentacea Desmarestia spp. Alaria esculenta

247 0.5 274 434 164

7.2 Tr. 8.0 12.7 4.8

Laminaria saccharina Laminaria longicruris Saccorhiza dermatodea Agarum cribosum Phycodrys rubens Polysiphonia spp.

627 1082 182 86 Tr. Tr.

18.3 31.7 5.3 2.5 Tr. Tr.

Palmaria palmata Chaetomorpha spp. Porphyra spp. Ulva lactuca

160 77 Tr. Tr. 3412

4.7 2.3 Tr. Tr.

Boreal

No. of stations

2.2%

%

40.5%

X (g/m2)

Subarctic

Subarctic Protected Stations Subarctic (NE Newfoundland and Labrador)


as physical structure, strongly dominated by the kelp Alaria esculenta in zones of high wave energy and by the western Atlantic endemic Laminaria longicruris in protected waters with sediment-encircled rock refugia. In the mid to lower subtidal, a rich, sea urchin/coralline encrusted bottom, with abundant often colorful and distinctive invertebrates (Color Plates 41 and 42), appears to provide a long-term, stable ecosystem, seen only occasionally in the mixed Boreal/Subarctic Gulf of Maine (and Nova Scotia).

CORE SUBARCTIC VS MIXED SUBARCTIC/BOREAL As Table 21.5 shows, if one accepts the patterns of the A/S Biogeographic Model, there are many core Subarctic endemic species of macroalgae; these species

together form 80% of the algal biomass, with most of the remainder being colder water, more cosmopolitan species like Desmarestia viridis. The invertebrates, on the other hand, provide a large number of endemic genera and even a few families. A few of the families provide keystone species, such as Strongylocentrotus drobachiensis (green sea urchin) and Solaster endeca (purple sunstar), to the fauna. The most abundant invertebrates on shallow, rocky, core Subarctic bottoms: Buccinum undatum (waved whelk); Hiatella arctica (boring clam); the two Hyas spp. (toad crabs); Halocynthia pyriformis (sea peach); the two Psolus spp. (scarlet psolids); and Cucumaria frondosa (orangefooted sea cucumber) also appear to belong to primarily Subarctic endemic genera. In the gravelly shell beds often directly associated with coralline/urchin bottoms, additional keystone species from endemic families (Echinarachnius parma – sand dollar) and genera

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21. A Subarctic/Boreal Microcosm TABLE 21.4B Seaweeds Commonly Occurring in Manually Harvested Square Meter Quadrats at (a) Combined and 5 ⫹ 10 m (See Text), at Wave Protected Sites

%

No. of stations

No. of quadrats

5 m and 10 m Turnerella pennyi Neodilsia integra Coccotylus truncata

1.1 Tr. 0.4

Tr. Tr. Tr.

Tr.

5 3 1 1

15 4 1 1

Pilayella littoralis Antithamnion borealis Rhodomela confervoides Ectocarpus spp. Ptilota serrata Membranoptera alata

0.1 Tr. Tr. 4 1.6 Tr.

Tr. Tr. Tr. 0.3 Tr. Tr.

0.3%

1 3 2 2 3 1

1 9 2 4 5 2

Desmarestia viridis Agarum clathratum

104 565

6.2 32.3

38.5%

3 4

9 10

Laminaria saccharina Laminaria longicruris Callophyllis cristata Phycodrys rubens Ceramium spp. Polysiphonia spp.

2.9 1065 Tr. 1 Tr. Tr.

0.2 60.9 Tr. Tr. Tr. Tr.

61.1%

2 2 2 2 2 4

3 2 4 5 2 6

Subarctic

Corallina officinalis Chaetomorphasp Ulva and Monostroma Delamarea sp. Sticyosiphon tortilis

Tr. Tr. Tr. Tr. Tr. 1750

Tr. Tr. Tr. Tr. Tr.

Tr.

1 1 1 1 1

2 1 1 1 1

Arctic

X (g/m2)

Boreal

Subarctic protected stations Subarctic (NE Newfoundland and Labrador)


(Placopecten mogellanicus – deep sea scallop) provide dominant biotic elements. In contrast, in the Gulf of Maine and Nova Scotia, new arrivals from the European Boreal (during historic times) such as Carcinus maenas (the green crab) and Littorina littorea (common periwinkle) have become primary elements (if not keystone species) of these mixed Subarctic/Boreal coasts. Fucus serratus a relatively new arrival, has an infralittoral dominant in the southern Gulf of St. Lawrence and made inroads on the Atlantic Nova Scotian coast, suggesting that it too in turn will spread further. However, none of these species or the likely prehistoric, Holocene arrivals are likely to significantly encroach on the core Subarctic (without the effects of global warming). Unfortunately, there is not space here to further document the biotic and ecosystem relationship of the core Subarctic to the mixed Subarctic/Boreal of Nova Scotia

and Maine and the Boreal European coast. The literature information alone seems overwhelming, but quantitative field data are essential. The Subarctic ecosystem and its primary species, including the keystone Strongylocentrotus sea urchin, probably derive from the North Pacific Subarctic, as opposed to the interfingering eastern Atlantic Boreal species and ecosystem (Adey and Moller, in press). This hypothesis can be tested, in part, using microcosms or mesocosms, ideally one Subarctic, one Boreal, and a mixed Subarctic/Boreal system that can be experimentally adjusted to demonstrate the effects of temperature on community and ecosystem structure. Unfortunately, when we built the microcosm we describe below, neither we nor the benthic research community fully understood the biogeographic patterns we have described (Mathieson et al., 1991). With this chapter, we strongly urge researchers to enter into this modeling endeavor.

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A Maine Shore Microcosm TABLE 21.5 Abundant Subarctic Endemic Taxa (Including N. Pacific Subarctic) (Allowing Diminishing Occurrence in Atlantic Boreal to a Southern Limit of the English Channel) Macroalgae Atlantic Subarctic only Acrosiphonia (Spongomorpha) arcta Saccorhiza dermatodea Laminaria longicruris Rhodomela confervoides Phycodrys rubens Occurs also in Pacific Subarctic Fucus distichus Chordaria flagelliformis Alaria esculenta Agarum clathratum Ptilota serrata Callophyllis cristata

Lithothamnion lemoineae

Clathromorphum compactum Clathromorphum circumscriptum Lithothamnion glaciale Leptophytum laeve

Invertebrate groups (Of shallow water (less than 50 m): Actinaria, Ceriantipatharia, Amphineura (Chitons), Prosobranchia (Limpets and Topshells), Mesogastropods, Pelecypods, Decapods (Crabs), Tunicates, Echinoids, Asteroids, Ophiuroids and Holothuroids) For 60 families tallied, approximately 10% endemic (notable taxa: Metridiidae, Strongylocentrotidae, Echinarachniidae, Pterasteriidae, Solasteriidae) of 80 genera tallied, 36 endemic – 45% 94 species endemic

A MAINE SHORE MICROCOSM Physical Layout The Maine shore microcosm was configured as shown in Figure 21.15. The entire system included a larger stepped tank with wave action, in this case a rocky shore, and a smaller, calmer tank (the mud flat and marsh) connected by piping. In concept, these are two different model ecosystems linked together to provide the primary interactions that occur between the same two ecosystems in the wild. The internal structure of the rocky shore was built like a stone wall with granitic and metamorphic cobbles and small boulders. This structure (and the available wave energy in the microcosm) is typical for the shores of many large, semi-protected bays in Maine, where the fine to pebble-sized fraction of the glacial till has been worked out by wave action leaving a cobble to boulder shore of great spatial heterogeneity. The base of the rocky shore tank has enough energy to hold a pebbly shell-hash, which would characterize large bay shores or moderately exposed outer shores at 25–45 feet in the wild (Figure 21.9). Light levels are equivalent to about the same depth (see below). The protected basal sections, deep inside the boulder/cobble bottom, along

FIGURE 21.15 Physical layout and plumbing of the 2700-gallon Maine coast exhibit at the Smithsonian’s Museum of Natural History. Drawing by Charlotte Roland.

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with the attached mud flat/marsh tanks serve as sediment traps and “ecological storage” for fine organic particulates, as we have previously discussed.

Environmental Parameters The Maine microcosm had a maximum water temperature of about 15°C (60°F) and a minimum of about 4°C (40°F). This provided a rather warm winter for the eastern Maine coast, which would typically be 1–2°C on outer shores in February. Otherwise, temperatures were close to those experienced in the wild from Penobscot Bay to Casco Bay. The cooling system consisted of a glass-tube heat exchanger in a fiberglass box with a light brine and three, 1-ton, immersion-type cooling units (Frigid Unit). The ecosystem’s salt water was passed through the chilled brine in a set of 1-inchdiameter glass tubes. During the winter minimum,

several additional cooling units were used to achieve the desired low temperatures for periods of up to about 8 weeks. Since this was an exhibit and summer humidity levels were relatively high in the public viewing areas, especially when crowds were present, the tank and its scrubbers were also contained in an air-conditioned room with acrylic viewing panels. In addition to temperature, the distinctive feature of the Maine coast that differentiates it from many coastal environments is a large tide range, roughly 8–20 feet at spring tides, depending on location. The range used in the microcosm was only 1 foot at spring tides and 8 inches at neaps. An insulated fiberglass box placed on the floor above the system served as a tidal reservoir. Water was pumped to the reservoir and returns to the main tank by gravity through a level-controlled hose. Two geared and timed stepping motors, one rotating 360 degrees every 12 hours and 20 minutes, the other

FIGURE 21.16 Diurnal oxygen concentration in the Maine coast microcosm as a function of tidal cycle. While oxygen concentration is within a few percent of saturation at all times, the exact values are very much a function of time in the tidal cycle as well. Data collected and analyzed by R. Santas.

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A Maine Shore Microcosm

rotating 360 degrees every 14 days, set the outflow hose level. The tidal control unit is pictured in Figure 2.28, and a typical tidal curve is shown in Figure 21.16. Salinity was maintained between 31 and 34 ppt in the Maine system on a seasonal basis, low in spring and high in autumn. Since a moderate amount of salinity variation occurs in the natural environment, a simple top-up method, to a mark, was used to replace evaporated water, rather than the more sophisticated control system used for reef models. Such control systems could, however, be used to reduce labor. The yearly cycling can be provided by manual adjustments on a seasonal basis. The metal halide tank lighting consisted of ten 400-W units. Time clocks were used to set the day length as well as dawn and dusk times. The light cycle in winter was greatly shortened, and winter light intensities are reduced by raising the metal halide lights on vertical slides with small boat winches. Light levels on the surface of the rocky shore and on the mud flat and salt marsh for summer and winter are shown in Table 21.6. The irradiance levels at midday on the microcosm were 100–700 µE/m2/s in summer and 30–450 µE/m2/s in winter. These compare to 130–625 µE/m2/s measured in July in outer Gouldsboro Bay, Maine, at 2.5–5 meters, and 45–280 µE/m2/s measured at the same depths and conditions in March and April. Due to the lack of cloudiness and fog in the model, total light received on the microcosm was probably somewhat higher than in the wild. Wave action in this microcosm was created by a pair of dump buckets of 24 and 18 liters, through which most of the pumped water was recycled (Figure 21.15). Depending on the wave action desired, seven 10-gpm

pumps were used to provide a wave period of 5–10 seconds. The current velocity halfway between the dump buckets and the rocky shore reached 10–19 cm/s. The pumps are standard impellor-driven units, and unfortunately, this caused a major limitation to the success of both holoplankton and microplankton in this system. It is essential for future efforts to test the biogeographic concept that we have proposed that a pumping system should be provided that is not destructive of plankton (see Chapter 2).

Principal Chemical Factors The chemical environment in this cold-water ecosystem was generated as a balance between the functioning of the ecosystem itself and a bank of algal turf scrubbers, as shown in Figures 21.15 and 21.16 and Table 21.7. The scrubbers were two relatively small 0.5-meter standard units described in Chapter 11. Each scrubber had a single 400-W metal halide lamp. The scrubber lights were operated for 8–14 hours during the night (dark) period on the main system; this simulated the night-buffering effect of offshore water entering the immediate coast environment with the tidal currents. These scrubber units were sufficient to drive nutrient levels in the system to less than the normal minimum for the wild system, which is about 1 µM (N as 2⫺ NO⫺ 2 ⫹ NO3 , 0.014 ppm). Through disturbance of the mud flat or excess feeding, it was possible to elevate nutrient levels to greater than 15–20 µM (N as 2⫺ NO⫺ 2 ⫹ NO3 , 0.21–0.28 ppm). This is near maximum for the wild environment. Except for periods when experimental work was being carried out, the wild

TABLE 21.6 Dimensions and Physical Parameters of the Maine Coast Microcosm Tank dimensions (meters) Community Rocky shore Marshland mud flat Total Principal operating characteristics

L 3.65 1.21

W ⫻ ⫻

1.21 1.21

D ⫻ ⫻

Summer

1.82 1.21

Tank volume (liters)

Substrate surface area (m2)

9100 1800 10 900

3.98 2.00 5.98

Winter

Lighting (metal halides); 12–400 W Photoperiod Temperature

100–700 µE/m2/s surface to 1.6 m (simulated depth 10 m) 14 hours (maximum) 15°C (maximum)

30–450 µE/m2/s surface to 1.6 m (simulated depth 10 m) 8 hours (minimum) 4°C (minimum)

Tide semidiurnal Wave action

Spring 38 cm Neap 20 cm Current velocity 10–19 cm/s; irregular with two dump buckets of 24 and 18 liters driven by 70–100 gpm of centrifugal pumps; seasonal

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TABLE 21.7 Basic Operational Chemical Parameters of the Maine Coast Microcosm Minimum

Maximum

Salinity 31 ppt (spring) 34 ppt (fall) Dissolved oxygen 8.5 mg/liter 9.5 mg/liter Dissolved nitrogen 2⫺ (NO⫺ 1 µM Na 10 (40) µM Nb 2 ⫹ NO3 ) Dissolved phosphorus 0.15 µM P 0.57 µM P Ocean (coastal) simulation Algal turf scrubber of 1 square meter lighted nightly with two 400-W metal halides for 8–14 hours depending on seasonal scrubber productivity rate: 1.9–11.4 g (dry)/m2/day Principal algal species Ectocarpus, Enteromorpha, Cladophora, Polysiphonia, Porphyra a

Typical 1–10 µM N. For research purposes.

b

pattern of low nutrients (and high visibility) during the winter and high nutrients (and low visibility) in the summer was followed. In Gouldsboro Bay, eastern Maine, in the mid-1980s, dissolved inorganic nitrogen ranged from about 5 µM offshore in late winter to 16 µM on the inner bay in late summer. Although the experimental range used on this tank has been wide, from 1 to 2⫺ 40 µM (N as NO⫺ 2 ⫹ NO3 ), typical microcosm operation has ranged from about 3 to 10 µM (Table 21.7). While this might be a little on the low side for current Gouldsboro Bay conditions, it is probably close to prehistoric values. Current observations of increasing barnacle abundance along the Maine coast even in bay environments suggest that nutrient concentrations are generally rising. Scrubber harvest intervals varied from 7 to 14 days and produced from 2 to 18 g dry weight of algae per

TABLE 21.8 Plants Occurring as Long-Term Residents of the Smithsonian Maine Coast Microcosm Kingdom Plantae Subkingdom Thallobionta Division Rhodophycota (red algae) Porphyra umbilicalis Palmaria palmate Chondrus crispus Rhodophyllis dichotoma Euthora cristata Hildenbrandtia prototypes Corallina officinalis Clathromorphum circumscriptum Lithothamnium glaciale Lithothamnium lemoineae Phycodrys rubens Ptilota serrata Antithamnionella floccose Phyllophora truncata Gigartina stellata Halosaccion ramentaceum Petrocelis middendorfii Phymatolithon laevigatum Phymatolithon rugulosum Phymatolithon lenormandi Polysiphonia sp. Ceramium sp. Division Chromophycophyta (brown algae, golden-brown algae) (browns) Ectocarpus fasciculatus Punctaria sp. Petalonia sp. Laminaria longicruris Agarum cribosum Pylaiella curta Chordaria flagelliformis Ralfsia verrucosa Fucus vesiculosus Fucus spiralis Ascophyllum nodosum Division Chromophycophyta (diatoms) Rhizosolenia sp. Cyclotella sp.

Diatoma sp. Mitzschia sp. Licmophora sp. Fragillaria sp. Navicula sp. Pleurosigma sp. Division Chlorophycota (green algae) Chaetomorpha linum Rhizoclonium riparium Ulothrix sp. Spongomorpha sp. Ulva lactuca Enteromorpha linza Derbesia sp. Chaetomorpha melagonium Cladophora rupestris Cladophora serica Monostroma sp. Enteromorpha intestinalis Subkingdom Embryobionta Division Magnoliophyta (flowering plants) Spartina alterniflora (smooth cordgrass) Spartina patens (salt hay) Juncus gerardi (black rush) Suaeda linearis (sea blight) Solidago sempervirens (goldenrod) Salicornia virginica (saltwort) Limonium carolinianum (sea lavender) Atriplex patula (spearscale) Kingdom Monera Division Cyanophycota (blue-green algae) Lyngbya sp. Oscillatoria spp. 3 spp. unicells Division Bacteria many species not tallied


day. The mean rate of production under normal operation and over a 6-month period was found to be 12 g (dry)/m2/day. A wide variety of algae could be found on the scrubbers, including young sporophytic kelp fronds. However, the dominant genera were the greens Enteromorpha and Cladophora, the brown Ectocarpus, and the reds Polysiphonia and Porphyra. These algae, which are relatively small at reproductive maturity, are the plants that would be expected in the wild in heavily grazed environments. A typical oxygen concentration curve for the water column of the Maine coastal model (with the marsh/ mud flat system temporarily closed off) is shown in Figure 21.16. It is clear that the concentration at any one time was a function of tide level as well as the state of the lighting. As shown in Figure 21.16, at high tide, when the intertidal community was under water and the lights went off, to begin the night cycle, oxygen dropped rapidly from supersaturated levels to a balance point well below saturation (about 8.56 mg/liter). However, as the tide fell and the respiration load of the intertidal was removed from the water column, the oxygen concentration rose (in this case to about 8.69 mg/liter). During the day, as can be seen from the right-hand side of Figure 21.16, the reverse occurred. The tide in this determination was set up to determine rate of fall of oxygen across the saturation point in the dark and the rate of climb back up across saturation in the light (during high tides) allowing the determination of the metabolism of the entire system. Based on the rates of change of oxygen across saturation in the dark and the light, the mean respiration rate for the entire rocky shore system was 0.88 g O 2 /m2/h and the net production rate (during full summer light) was 0.57 g O 2 /m2/h. For a 12 hour lighted day, the gross primary production was thus 17.4 g O 2 /m2/day or about the equivalent of 18.6 g (dry)/m2/day. This compares with a mean summer production rate of algae (intertidal and subtidal) from the wild system (see discussion above) of about 14.5 g (dry)/m2/day. As we have noted, the microcosm is operated without a cloudiness factor; with somewhat more light than is probably average for a Maine shore, primary production in this microcosm is probably a little higher than the wild systems. All in all, the numbers for respiration and primary production make sense, and suggest that metabolically the model system was operating close to its wild counterpart.

The Organisms The Maine coast exhibit microcosm was established primarily by the process of ecosystem block transfer described earlier. In the rocky shore community the “blocks” were individual rocks (pebbles, cobbles,

399

boulders) and fragments of ledge pried or chiseled from the wild. The primary organic-structuring elements were algae (blue-greens, rockweeds, Irish moss, kelps, small reds) or in some cases barnacles or mussels attached to the rocks. These rock/algae invertebrate units were moved in coolers as rapidly as possible from the Maine coast to the microcosm in Washington, DC. They were initially placed in their equivalent microcosm zones with algae and whatever encrusting attached fauna were present. Many smaller mobile molluscs, worms, and crustaceans also accompanied the blocks. Following the initial mass transport, relatively small “block injections” were repeated over the next 2 years. Fish and larger invertebrates were trapped or netted and introduced separately. On the mud flat, marsh, and subtidal mud bottoms, the “blocks” consisted of small ecosystem units of mud substrate with their marsh grass, seagrass, or algal communities intact, carefully shoveled into coolers, and similarly introduced. Since the original stocking, small collections, primarily of species that have suffered overpredation, were added about once per year. As we discussed above, on the Maine coast, except for the deeper, muddy bottoms in bays, plants are the primary determiners of community structure. This is also definitively the case in the microcosm. The plants with their associated communities of organisms were established initially in the microcosm and by and large have been naturally maintained. It is interesting to note that although Fucus and Ascophyllum had shown good growth in this system and have repeatedly reproduced, the original adult stalks established from the wild demonstrated a very slow die back process. Young plants of both genera gradually established in the system, in part from the original hold fasts. Chondrus crispus (Irish moss) did extraordinarily well in this model, generally creeping to shallower levels in the intertidal than where it is found, in abundance, in the wild. This probably relates to the high humidity and moderate temperature levels of the microcosm. In the wild, Irish moss is likely sharply limited by high temperatures and relative dryness in summer as well as very cold temperatures and icing conditions in winter. Although the dominant algal species that characterize the protected portions of the Maine rocky coast were present in the model and were easily maintained, as long as urchin (Strongylocentrotus drobachiensis) populations are controlled, some species that were important in the wild are conspicuously absent or poorly developed in this system. Alaria esculenta and Fucus distichus are the most conspicuous of these. However, as we discussed above, we maintained temperature conditions in this microcosm that would be marginal for both of these Subarctic species. In addition, these macroalgae tend to be characteristic of highly exposed shores even under transitional Subarctic/Boreal conditions. Perhaps, in

400


part, these conditions would provide habitat that would avoid the occasional summer temperature spikes. In a model system designed to be Subarctic in character (i.e. lower summer and winter temperatures than in the model), it is likely that both of these species would also be successful. The muddy subtidal of many Maine bays has a richly developed eelgrass (Zostera marina) community. Although it had been established in the muddy subtidal of the model several times, Zostera gradually died out, each time, over 6–12 months. The intensive burrowing activities of green crabs (Carcinus maenas) may be partly responsible. These crabs did exceptionally well in this system and without larger fish predators, and the lower temperatures of the core Subarctic, may require frequent human intervention.

The plants that were permanent long-term community elements of the Maine coast microcosm are listed in Table 21.8. Although not specifically mentioned above, note that the understory of red, pink, and yellow calcified coralline algae prevalent in the wild, including Clathromorphum, Phymatolithon, and Lithothamniom species, were also characteristic understory elements in the model. The encrusting and attached fauna so characteristic of rocky Maine shores is also present in the Maine microcosm. Barnacles, blue mussels, horse mussels (Color Plate 37), and the calcified worm Spirorbis are subject to heavy predation by Nucella lapillus (dogwinkle) and Buccinum undatum (waved welk) as well as by crabs (Cancer, rock crab; and Carcinus, green crab). Nevertheless, all of these attached animals manage to

TABLE 21.9 Macroinvertebrates Occurring as Long-Term Elements of the Smithsonian Maine Coast Microcosm Kingdom Animalia Subkingdom Protozoa (see Table 21.5) Subkingdom Parazoa (sponges) Halichondria panicea (crumb of bread sponge) Leucosolenia sp. (organ pipe sponge) Subkingdom Eumetazoa Phylum Cnidaria (coelenterates) Bunadactis stella (silver-spotted anemone) Metridium senile (frilled anemone) Tealia felina (northern red anemone) Hydroid sp. Phylum Mollusca Ishnochiton ruber (red chiton) Acmaea testudinalis (tortoise shell limpet) Buccinum undatum (waved whelk) Crepidula fornicata (common slipper) Nassarius obsoletus (mad dog whelk) Neptunea decemcostata (ten-ridged periwinkle) Thais lapillus (dogwinkle) Aequipecten irradinas (bay scallop) Nucula delphinodonta (nutshell) Nucula proxima (nutshell) Placopecten magellanicus (deep sea scallop) Yoldia limatula (yoldia) Hydrobia minuta (swamp hydrobia) Littorina littorea (common periwinkle) Littorina obtusata (smooth periwinkle) Littorina saxatilis (rough periwinkle) Lacuna vincta (chink whelk) Coryphella sp. (nudibranch) Macoma balthica (baltic macoma) Modiolus modiolus (horse mussel) Mya arenaria (soft clam) Mytilis edulis (blue mussel) Phylum Annelida Cirratulus sp. (fringed worm) Haploscoloplos fragilis (obiniid worm) Lepidonotus sp. (12-scale worm) Nereis sp. (clam worm) Ninoe sp. (thread worm)

Polydora ligni (mud worm) Spirorbis sp. (hard-tube worm) Thelepus sp. (terebellid worm) Phylum Bryozoa (moss animals) Alcyonidium sp. Phylum Platyhelminthes (flatworms) Macrostomum sp. Plagiostomum sp. Phylum Arthropoda Class Crustacea (barnacles) Balanus balanoides (northern rock barnacle) Balanus balanus (rough barnacle) (amphipods) Ampelisca abdita Caprella sp. Corophium volutator Gammarus oceanicus Gammarus sp. Orchestia sp. (copepods) America longipes Tisbe sp. (isopod) Idotea sp. (decapods) Cancer borealis (Jonah crab) Cancer irroratus (rock crab) Homarus americanus (northern lobster) Crangon septemspinosa (sand shrimp) Carcinus maenas (green crab) Hyas areneus (toad crab) Pagurus sp. (hermit crab) Phylum Echinodermata Asterius vulgaris (seastar) Ophiopholis aculeata (daisy brittlestar) Strongylocentrotus drobachiensis (green sea urchin) Henricia sp. (bloodstar) Ophiuroid spp. (brittlestars) Echinarachnius parma (sand dollar)

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survive over the long term in the upper intertidal or in crevices where they cannot be easily reached. It was estimated that the diversity of this tank complex was close to 250 species, about one-third that of the similarly sized coral reef microcosm (Tables 21.9–21.11). The open-water volume available for mid-water fish in the Maine shore microcosm was relatively small. Thus, we have emphasized bottom or near-bottom fish and have kept biomass small. Of the large variety of fish placed in the system, relatively few (Table 21.11) became permanently established. These fish tended to grow very large over several years, when they were removed and replaced with younger animals. Although invertebrate and plant reproduction is abundant and successful for many species, in this very limited volume, especially with centrifugal impellor pumps, fish reproduction was not successful. The Maine coast microcosm did not have a refugium from larger fish and invertebrates with the same environmental characteristics of the main system. The tidal tank was effectively a large refugium for some species. However, it was in effect on intertidal mud flat, with hard walls, and totally dark. Nevertheless, in the Maine coast system as a whole, the algae and the smaller encrusting invertebrates appeared to be quite successful while the fish were relatively limited. Probably the greatest needs of the microcosm were simply a larger volume of open water treated as a refugium, higher wave energies and tides, and the installation of disc-flow pumps to

reduce destruction of plankter species. Most critical for a full Subarctic system would be the necessity for lower temperatures.

Kelp Growth In the coral reef systems, we used coral calcification and growth as a measure of biotic physiological performance. In this cold-water system, we use kelp growth TABLE 21.11 Fish and Lower Chordates Occurring as Long-Term Elements in the Smithsonian Maine Coast Microcosm 1 Year After Establishment in 1984 Kingdom Animalia Phylum Chordata Vertebrata Class Osteicthyes (bony fish) Menidia menidia (Atlantic silversides) Myoxocephalus octodecemspinosus (longhorn sculpin) Fundulus heteroclitus (mummichog) Pollachius virens (pollock) Pungitius pungitius (ninespine stickleback) Tautogolabrus adspersus (cunner) Pseudopleuronectes americanus (winter flounder) Stenotemus chrysops (scup) Sygnathus fuscus (northern pipefish) Tunicata Botryllus schlosseri (golden star tunicate) Halocynthia pyriformis (sea peach)

TABLE 21.10 Protists Identified in the Smithsonian Maine Coast Microcosma Kingdom Animalia Subkingdom Protozoa Class Mastigophora (flagellates) Bodo saltans Monosiga sp. Eutreptia sp. Euglena sulcata Class Sarcodina (amoeboid types) Amoeba 8 spp. Flabellula sp. Hyalodiscus sp. Limah hartmanella Mayorella sp. Pontifeh maximus Rhixoamoeba sp. Class Ciliophora (ciliates) Amphileptus sp. Cinetochilum marinum Coleps sp. Dysteria sp. Hemiophrys sp. Lacrymaria sp. Lembus sp. a

Courtesy D. Spoon.

Lionotus spp. Actinotricha sp. Aspidisca crenata Aspidisca 5 spp. Diophrys appendiculata Cothurnia sp. Epistylis sp. Vaginicola sp. Vorticella marina Vorticella microstoma Zoothamnium sp. Loxophyllum sp. Mesodinium sp. Nassula sp. Protocruzia sp. Scuticociliate sp. Trachelophyllum sp. Trochilia sp. Euplotes spp. Deranopsis sp. Uroleptus 2 spp. Acineta sp. Metacineta sp. Podophyra sp.

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FIGURE 21.17 Elongation rates of the kelp Laminaria longicruris as a function of light and temperature in the Maine coast microcosm described in this chapter; *represents similarly derived data from wild, bottom-attached kelp in the eastern Gulf of Maine off Gouldsboro Bay; Winter lighting; low wave action; low nutrients. Data from Brittsan (1989).

and reproduction. In the microcosm, the mature sporophyte fronds produced spores during both simulated spring and fall, just as in the wild. However, this was not quantified. On the other hand, frond elongation, in the meristem, was extensively measured both in the field and in the wild. These data are plotted in Figure 21.17, and they show a remarkable similarity in both the magnitude and timing of kelp elongation. Both in the microcosm and in the wild, there is a strong dependence of growth on solar radiation, increasing consistently with light in the spring but falling sharply in late summer and early fall as light decreases (turbidity, low in the spring, and high in the late summer, probably plays a role also, but this was not quantified); see also Figure 5.16.

Operation and Maintenance The Maine coast microcosm was rather simple to operate mechanically. Evaporation rates are low and

the requirements of makeup water quality are not as sensitive as they are for the coral reef. The plumbing and piping concerns are little different from those in any model ecosystem. However, the unique operational aspect is temperature. A sudden breakdown of cooling apparatus, particularly in summer, could be quickly disastrous for this system. Because of this we maintained several standby cooling units. The Maine coast microcosm was certainly dynamic, but events tend to be much slower paced than they were in the warmer microcosms and mesocosms. Without top fish predators to manage urchin, crab, and lobster numbers naturally, human intervention is needed to help smooth predator–prey cycles. However, the intervention process was relatively easy to accomplish. For example, impending problems with green crab or urchin predation were detectable many months before they became serious. Such overpredation is quite common in the wild on the Maine coast. However, with many hundreds of miles of irregular coast, the net result

An Opportunity to Test Biogeographic Theory

is a community structure that is highly patchy rather than depauperate of many species. The rocky Maine shore microcosm had a relatively large wave generator, the effects of which have been the object of some research. There is little question that wave action is as crucial to algal production in the microcosm as it is in the wild ecosystem. Although difficult to research in the sense of a comparison between wild and model, wave action is certainly a very major factor in determining the character of the entire model community. It is likely that minimum wave action combined with the very limited tide range in the model was a primary factor limiting veracity. A model 5–10 times larger with at least one-half of the wild tidal range would greatly increase the success of secondary species and therefore the veracity of the entire model. As we pointed out above, a major part of the energy processed in the Maine coastal ecosystem was through the filter feeding of particulates. Plankton and some benthic larvae are certainly key elements in this process, but unfortunately this system used impellor pumps. The use of disc-flow pumps, Archimedes screws or lift pumps on such a system would provide a major improvement in veracity. Unfortunately, the design of the microcosm as it is currently laid out, with access between open coast and bay waters lying through the “rock mesh” of the lower rocky shore (see Figure 21.15), does not allow larger rocky shore fish to extend to the mud flat. Fundulus (killifish), Crangon septemspinosa (sand shrimp), and blue crabs all work the very limited surface of muddy shore. It would be far more effective if a larger mud surface was available and the fish of the rocky shore could also browse in that habitat. Like the Everglades mesocosm (Chapter 22), the tidal reservoir could be operated as a mud flat, in this case, to achieve this need. Predation by larger fish might also naturally assist the establishment of a subtidal Zostera marina (eelgrass) community. Perhaps because of the necessarily lowered wave energies in the microcosm, urchin and snail grazing of kelp (44% of production for urchins) exceeded that typically found in the field (Brittsan, 1989). Unlike in the reef communities discussed in Chapter 20, on coldwater rocky shores, the amount of algal production consumed by herbivores is typically low to moderate (10–40%). In the wild, the remaining production is removed by wave action and ice and is deposited at the high tide line as shore drift. As detritus, this plant biomass is reduced to organic fragments by small crustaceans (particularly the amphipods Orchestia and Talorchestia, bacteria, and fungi). Returned to the water column on spring tides, by heavy rains, and in storms, this organic detritus becomes part of the large suspended

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organic load in the water that is available to filter feeders, and the detritivores on quiet muddy bottoms. In the microcosm some algae break free due to snail and urchin grazing. Also, when plant growth is excessive, human intervention is used to remove plants, thus simulating storms. This “drift” algae is placed in the microcosm supratidal where it breaks down and returns to the system, much as in the wild. This is another example of the need for creative human intervention to simulate required physical or biotic processes that would be impractical to simulate precisely in a model.

AN OPPORTUNITY TO TEST BIOGEOGRAPHIC THEORY During Pleistocene glaciations, the northwestern North Atlantic probably had small and scattered refugia for cold water, rocky shore biota. These refugia would have occurred at glacial, low sea level on the shelf edge and probably in rocky patches across the shelf. During interglacials, other Subarctic species may have been re-introduced from the “home territory” in the North Pacific. However, it is unlikely that significant refugia existed for Boreal species in the shores of the western North Atlantic (Adey and Steneck, 2001). The eastern Atlantic Boreal Region continuously exists because both during glaciations and interglacials, a large coastal area exists of the same winter and summer temperatures, it simply slides north and south along the western European, and northeastern African and western Mediterranean coasts. It seems likely that at the end of each glaciation, the coast north of Cape Cod to the Arctic was mostly Subarctic in species composition. Gradually, with accelerating pace as human European visitors and immigrants to North America increased the possibilities for organism transport, Boreal species reached the coast from Long Island to the southern Gulf of St. Lawrence. In those areas, particularly in the intertidal and very shallow water, physical conditions were more suitable for Boreal than Subarctic species, and they would have gradually become established. However, most Boreal species (without global warming) are incapable of penetrating the core Subarctic, where maximum summer temperatures are generally less than 10°C and sea ice is prevalent in later winter and spring. Within the core Subarctic, there are a large number of endemic species, and a considerable number of endemic genera and a few families. Some of these species are keystone ecological elements, and many are structurally important, and well-adapted members of the widespread, apparently permanent coralline/sea urchin rocky bottom. On the other hand, some scientists

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feel that the coralline/urchin bottom is secondary: overgrazing resulting from the overfishing of top predator fish (Steneck, 1998; Steneck and Carlton, 2000). Does the coralline/sea urchin bottom (not barren) represent the effects of biogeographic organization in the oscillating climate of the Pleistocene, or is it a trophic cascade (large predatory fish having been removed)? This is an excellent topic for investigation with both living system modeling tools (microcosms) as well as with the tools of molecular biology. Hopefully, we have demonstrated that this is a practical endeavor that could provide a valid answer to this question.

References Adey, W. and Hayek, L. A. (2005) The biogeographic structure of the western North Atlantic rocky Intertidal. Cryptogamie Algolgigue 26: 35–66. Adey, W. and Moller, K. (in press) The biogeographic origin of Arctic endemic seaweeds: no paradox here. J. Phycol. Adey, W. and Steneck, R. (2001) Thermogeography over time creates biogeographic regions: a temperature/space/time-integrated model and an abundance weighted test for benthic marine algae. J. Phycol. 37: 677–698. Brittsan, J. M. (1989) Regulation of Kelp (Laminaria longicruris) Growth in a Subarctic Marine Microcosm and the Rocky Coast of Maine, USA. M.S. Thesis, University of Maryland. Brown, W. and Beardsley, R. (1978) Winter circulation in the western Gulf of Maine. Pt. 1, Cooling and water mass formation. J. Phys. Ocean. 8: 265–277. Denton, G. and Hughes, T. (1981) The Last Great Ice Sheets. John Wiley and Sons, New York. Gosner, K. (1978) A Field Guide to the Atlantic Seashore. The Peterson Field Guide Series, Houghton Mifflin, Boston. Hawkins, S. and Jones, H. (1992) Rocky Shores: Marine Field Course Guide, Vol. 1. Marine Conservation Society, London.

Hayward, P. (2004) A Natural History of the Seashore. Collins, London. Himmelman, J. (1991) Diving observations of subtidal communities in the Northern Gulf of St. Lawrence. In: The Gulf of St. Lawrence: Small Ocean or Big Estuary? J.-C. Therriault (Ed.). Can. Spec. Publ. Fish Aquat. Sci. 113: 319–332. Hopkins, T. and Garfield, N. (1979) Gulf of Maine intermediate waters. J. Mar. Res. 37: 103–139. Keats, D. W., South, G. R., and Steele, D. H. (1985) Ecology of juvenile green sea urchins (Strongylocentrotus droebachiensis) at an urchin dominated sublittoral site in eastern Newfoundland. Proc. Int. Echinoderm Conf. 1: 295–302. Lewis, J. R. (1964) The Ecology of Rocky Shores. English Universities Press, London. Luning, K. (1990) Seaweeds: Their Environment, Biogeography and Ecophysiology. Wiley-Interscience, New York. Mathieson, A., Penuiman, C., and Harris, L. (1991) Northwest North Atlantic rocky shore ecology. In: Intertidal and Littoral Ecosystems. A. Mathieson and P. Nienhuis (Eds). Elsevier, Amsterdam. Morton, J. (1991) Shore Life between Fundy Tides. Canadian Scholars Press, University of Guelph, Guelph, Ontario. Raffaelli, D. and Hawkins, S. (1996) Intertidal Ecology. Chapman and Hall, London. Schiebling, R. and Hatcher, B. (2001) The ecology of Strongylocentrotus drobachiensis. In: Edible Sea Urchins: Biology and Ecology. J. Lawrence (Ed.). Elsevier, Amsterdam. Sears, J. (2002) NEAS Keys to the Benthic Marine Algae of the Northeastern Coast of North America from Long Island Sound to the Strait of Belle Isle. 161 pp. NEAS Contribution No. 2, 2nd ed. NE Algal Society, Dartmouth, MA. Steneck, R. (1998) Human influences on coastal ecosystems: does overfishing create trophic cascades. TREE 13: 429–430. Steneck, R. and Carlton, J. (2000) Human alterations of marine communities, students beware! In: Marine Community Ecology. M. Bertness, S. Gaines, and M. Hay. Sinauer Associates. Taylor, R. (1957) Marine Algae of the Northeastern Coast of North America, revised edition. University of Michigan Press, Ann Arbor.

C H A P T E R

22 Estuaries Ecosystem Modeling and Restoration

recycle needed elements to the estuarine communities of organisms. Ocean tides in the narrow confines of an estuary provide relatively strong currents. As we pointed out in Chapters 6 and 18, coastal waters tend to be considerably more productive than fresh waters. Tidal currents, with their mixing action, help to drive this production. Also, we have described the process of evolution as an “arms race.” Prey and predator evolve together, each developing more effective ways to defend themselves or to outsmart their prey. Accommodating to higher and, more particularly, lower salinities is a difficult step for many aquatic organisms. A marine organism, for example the oyster, having developed the ability to function at salinities much lower than ocean water, achieves considerable respite from its many predators. In many cases such an animal becomes highly abundant. Young marine fish of many species are hatched in the upper reaches of estuaries where they find not only abundant food for rapid growth but also a measure of protection from voracious larger fish that find the very shallow waters difficult to negotiate. In tight quarters, the larger fish are also exposed to a higher risk of predation from even larger animals such as birds and otters. For this reason, estuaries are often referred to as nurseries. Stable, well-developed estuaries typically range from tens to hundreds of miles in length. Simulating the dynamics of estuaries would seem an almost impossible task in the confines of microcosms and mesocosms. In this chapter, we describe our experiences over the past several years in simulating such systems. We briefly describe a mesocosm of a very large temperate estuary, the Chesapeake Bay. Then, we examine in greater depth the performance of a 10-year-old Florida Everglades

WHERE FRESH AND SALT WATERS INTERACT Estuaries are arms of the sea, partly enclosed by land and with freshwater river input sufficient to provide a significant fresh- to saltwater gradient. During the past 10 thousand years, the Earth’s coastal waters have become relatively rich in large estuaries. The Earth’s climate is at a warm point in the glacial–interglacial cycle, and sea level is high. As a result, the lowermost reaches of many river valleys are flooded, creating elongate bodies of water grading from salt to fresh. The rich food source provided by large numbers of fish, shrimp, crabs, bivalves, and aquatic birds has made estuaries a favored place of habitation for humans. In addition, estuaries have provided a haven for boats of commerce plying ocean waters. Through the estuarine rivers, these same boats or their coastal counterparts have found easy access to the interiors of continents. Many large cities have developed on estuaries, where they function as the gateways to continents. Thus, in modern times these highly productive bodies of water have also become the focus of human disturbance and pollution. We continue to need a greatly extended understanding and appreciation of the ecological nature of estuaries, or we are in great danger of creating extensive abiotic zones of the most useful and beautiful of coastal waters. Estuaries tend to be very rich in organisms. Rivers, before they are diluted by the enormous body of ocean water, have generally high concentrations of many chemical elements needed by plants and animals to build their tissues. Organic particulates draining from the land tend to be sedimented out in the estuary. Their breakdown on the often muddy bottoms tends to

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estuarine mesocosm. The fresh waters of the Florida Everglades where they meet the Gulf of Mexico produce the subtropical estuarine complex that we used as our wild analog. The Chesapeake mesocosm was completed at the National Museum of Natural History in 1986 and operated until 1994 when it had to be dismantled to make space for a major construction project. Because the basic techniques used were highly successful for such a large, complex estuary, it is to be hoped that such a mesocosm can be constructed again with this system providing the lessons for even greater success. We present an abbreviated version here, so that we can devote more space to the results of follow-up studies in the Florida Everglades mesocosm. Day et al. (1989) provide basic background on the ecology of estuaries. Most of the organisms specifically discussed in this chapter can be located in the following field guides: Audubon Society (1983), Godfrey and Wooten (1979), Gosner (1978), Kaplan (1988), and Odum et al. (1984). Local area citations are given below in the appropriate sections. The interest in using mesocosms for research associated with restoration of systems ranging from landscape to global scales in growing in proportion to our need to solve ecological problems, not just study them (Petersen et al., 2003; Osmund et al., 2004). The primary issue has always been: are the results of such work applicable to wild ecosystems (i.e. macrocosms)? In this regard, the work of Petersen et al. (2003), describing the 10-year MEERC scaling work at the University of Maryland, is particularly valuable. They examined many aspects of scale (size, spatial heterogeneity, time, complexity, water exchange, exchange between habitats and the role of nutrients and energy in all of these). Generally, there are thresholds beyond which veracity sharply improves. The systems we have described in this chapter are larger, two orders of magnitude more diverse, and were operated longer than the MEERC systems; in those regards, they are well above the thresholds that they identify. One particularly interesting issue is the role of nutrients in controlling trophic structure. At low nutrient levels, there is a tendency for bottom-up control; at higher nutrients that can switch to top-down. We have consistently maintained throughout this book that low nutrients and bottom-up controlled trophic structure is key, with top-down management applying primarily to managing top predators and large grazers where even the scales at which we are working are below thresholds. Nevertheless, it is clear to us that these estuarine systems should have an order of magnitude larger volume to accommodate plankton dynamics and need a biotic dimension to oceanic simulation.

CHESAPEAKE BAY IN MESOCOSM About 180 miles long and 5–30 miles wide, Chesapeake Bay is one of the largest estuaries in the world. Although depths can reach over 150 feet, it is a relatively shallow body of water, the average depth, including tributaries, being only about 22 feet. The freshwater flow of Chesapeake Bay, which is received from a number of rivers (the Susquehanna, Potomac, and James being the largest), derives from a watershed of about 64 000 square miles. Although there is a peak of flow in the spring and a minimum in the autumn, freshwater input and tidal exchange into this large bay are consistent enough to maintain salinity levels at any one point in open water at a yearly range of usually less than 4–7 ppt (Figure 22.1). Tides in Chesapeake Bay are relatively small, 1–4 feet maximum. Nevertheless, even though saltier water from the ocean does tend to work its way up the bay on the bottom as a heavier “salt wedge,” and lighter fresh water from the rivers tends to flow over the top, mixing keeps surface to bottom salinity differences to less than 2–3 ppt. A very large body of scientific literature exists for the Chesapeake Bay. A description of the bay and its organisms can be obtained from Humm (1979), Lippson and Lippson (1997), Lippson et al. (1979), and Wass (1972). A particularly good introductory reference to the bay is Life in the Chesapeake Bay by Alice Jane Lippson and Robert L. Lippson (1984). The Chesapeake Bay mesocosm model was designed to accomplish a requirement for stable salinity within a series of interconnected segments (Figure 22.2). The model consisted of a large, relatively flat and stepped fiberglass tank (40 ⫻ 12 ⫻ 5 feet) with a total volume of about 15 000 gallons. Fiberglass and acrylic walls separated the large tank into eight segments of about 1900 gallons each. Each section had separate salinities about 4.5 ppt higher or lower than the adjacent section. The salinity separation and gradient were maintained dynamically with free access for organisms from salinity segment to segment, as we describe below. Each section of this estuarine model was connected to the adjacent section by hinged, circular, 4-inch-diameter gates or flapper valves. These pneumatically operated gates (Figure 22.3) were manually or computer controlled to allow fresh water to move on the surface from the freshwater segments to the adjacent more saline segments and to allow the saltier water to flow in the other direction in the deeper parts of the system. Conductivitytype sensors were used to provide the computer with the salinity-level information needed for the decision to open the gate. Since the surface water was heated by the lamps and the water injected into the base of the higher salinity tank was chilled (see below), the denser

Chesapeake Bay in Mesocosm

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FIGURE 22.1 Typical surface salinity distribution in Chesapeake Bay during spring minimum and fall maximum. After Lippson (1973).

bottom water mixed relatively slowly with the surface and gradually moved through the deep gates, up the system toward fresh water. The net result was the flow and salinity pattern shown in Figure 22.4. Normal drift in sensor settings provided a variation in each tank of about 2 ppt. As configured, the Chesapeake mesocosm maintained stable salinity levels even when the gates were operated manually several times a day. Perhaps the only problem with manual operation was that the frequency and random access of organisms from one salinity to the next was more difficult to maintain. Since the salinity gates had an aperture of 4 inches and remained open for 1 min whenever required by the

salinity sensors and computer, mobile organisms such as crabs and fish could easily move throughout the mesocosm. Generally, this salinity gradient system was quite successful. However, since rapid closure of the gates occasionally trapped and killed fish and sometimes tore up the plastic fittings, a slower-acting system would be preferable. Also, in practice the lowest salinity gate on the shallow side between tanks 1 and 2 was not used since salt found its way into the deeper parts of the tidal fresh tank and could only be flushed out with difficulty. To solve this problem, the freshwater tank was kept at a slightly higher level than tank 2, and downstream flow was through a 1/2-inch hole

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FIGURE 22.2 Layout (A) and primary functional elements (B) of the Smithsonian’s Chesapeake Bay mesocosm. Individual tidal reservoirs not shown in (B).

between the two tanks. In the last several years of operation, a shallow sluiceway, like a dam fish ladder, was added to allow estuarine organisms greater access to fully fresh water. However, we were not able to study the effects of this unit on the biota. The gates described maintained stable salinity and allowed organism movement throughout the mesocosm, effectively simulating a distance of almost 200 miles in the wild. The model estuary was not designed for fully tight gates and, thus, the Chesapeake model was

dynamic and had to be driven on both ends to maintain a salinity gradient. A metering pump from scrubbed tap water simulated river input. While mean river flow into Chesapeake Bay relative to bay volume is the equivalent of about 1 gallon/h, in this model we used 2–3 gallons/h to maintain salinity distribution. Tighter gates would reduce this requirement. The ocean high-salinity end had to simulate the effects of the ocean on the bay. The devices used to accomplish this were collectively called the ocean simulator

Chesapeake Bay in Mesocosm

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FIGURE 22.3 Photograph of salinity control gate. In the initial version the flapper valve in the mixing chamber was 4 inches in diameter. On being activated by the computer, a solenoid valve delivers compressed air to the pneumatic piston, which drives the gate through plastic linkages. In the new and tighter unit pictured the gate slides between Teflon bearings. Photo by Nick Caloyianis.

FIGURE 22.4 Flow and mean salinity distribution through the Chesapeake mesocosm.

(Figure 22.2). Just as in the coral reef and Maine microcosms, algal scrubbers were used to simulate an ocean sink for nutrients as well as to provide higher quality, ocean-equivalent water. A small, 4-gpm pump was

used to deliver water from the high-salinity section of the mesocosm to the scrubber complex. This small flow provided a turnover rate for the high-salinity tank alone of about 8 h. This reduced the number of plankton

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per day that had to pass through another centrifugal pump. However, to properly drive the scrubbers each unit was provided with a 10-gpm internal recycling pump to obtain sufficient flow and surge. A sediment trap was used to constantly “sink” fine sediment “out to sea.” Also, as in the other mesocosms, a proportion of “new” salt water, in this case about 10 gallons/day or about 0.05% of system volume, was continuously added with a metering pump to the highest-salinity tank and periodically removed to drain. This procedure provided the equivalent of tidally added ocean water in the wild Chesapeake Bay. In the model, its chief function was to prevent “salt drift” or a change in salt composition due to “evaporated” salts. For an estuarine model, the ocean simulator must accomplish one additional critical element: the removal (scrubbing or sinking) of the fresh water introduced at the river end. By the time the fresh water introduced reaches the lower end of the estuarine complex, it is totally mixed with the salt water and either it must be separated from the salt or the salt water must be removed and the salt replaced in the mesocosm. In the model described, roughly 60 gallons of fresh water per day was removed from the ocean end with a reverse osmosis (RO) ship’s water maker to balance out “river” input and maintain a proper salinity gradient. Unfortunately, removal of fresh water from the system with an RO or evaporator also removes plankton. This problem is discussed in depth in Chapters 2 and 17. In general, turnover time through the RO system should be less than plankton production volume on a daily basis. In our case turnover time through the RO was 3–4 days for tank 8. Finally, as we mentioned above, the saltier effluent from the ocean simulator was also cooled several degrees centigrade to ensure that its density on reinjection into the estuary provided an adequate salt wedge. Rain was simulated in the Chesapeake mesocosm with a polyvinyl chloride (PVC) greenhouse and pipe– sprayer system. In this case, rain was simulated twice each day using about 25 gallons of water. This precipitation roughly balances out evaporation and plant transpiration. Since rain is produced only in the marsh and beach ridge, the needed proportion provides a rainfall of about 0.2 inches/day. An additional element added to the beaches and marshes of the Chesapeake model was wind. Simple oscillating household fans provided enough air movement to move the grasses gently. With grasses and other wind-pollinated plants, wind is important for regular seed set. Also, many halophytes are salt excretors and, along with rain, wind likely removes salt from the surface of the plants. Wind and rain together, in the wild and in these mesocosms, also reduce the effects of insect predation on the plants. There may also

be other important physiological values to wind, including increased production due to oxygen and carbon dioxide exchange as well as light flashing. Lighting, tide control, and wave action in the Chesapeake mesocosm were accomplished essentially as in the coral reef and Maine coast systems. Very high output (VHO) lamps were used rather than metal halides in the deeper areas of the mesocosm. Acrylic dump buckets were used to provide waves in each section. Because of the typical pattern of reduction in open-water areas with reduced salinity in Chesapeake Bay, as well as on most estuaries, the largest dump buckets were placed on the saltier end of the system and gradually reduced in size upstream. The 6-inch tide was created by 10-gpm pumps leading to a separate, elevated tidal reservoir for each salinity segment. Timed stepping motors determined the quantity of water that remained in the reservoir and therefore the tidal cycle (see Chapter 21). In the model, unlike in Chesapeake Bay, the tide is synchronous in all salinity segments. It is possible to develop the 24-h time interval that it takes for the tidal wave to sweep up the Bay in the model. However, it would be necessary to operate with tighter gates, as discussed above, or it would be difficult to maintain the necessary salinity gradient. The physical–chemical characteristics of the Chesapeake mesocosm are shown in Table 22.1. Typical patterns of nutrient distribution (nitrite plus nitrate) for the system are shown in Figure 22.5. It is apparent that the algal turf scrubber portion of the ocean simulator was quite successful as a sink for nitrogen. Only in the earlier stages of operation, in tanks 1 and 2, where dissolved nitrogen levels were higher than they should be to simulate prehistoric wild conditions (as a result of the eutrophic tap water injected), does it seem likely that significant denitrification occurred. We discuss this matter in greater depth below in conjunction with our description of nutrient dynamics in the Everglades mesocosm. If we were to reconstruct a new Chesapeake model at this time, we would use plastic-lined block or concrete for a more permanent, less troublesome installation. Also, artificial light is expensive and hard to maintain at these dimensions – a greenhouse or external environment would be preferred if at all possible. For all of the reasons repeatedly described in this book, we would use disc-flow, or equivalent pumps and a greater tide. The computer we used for salinity gate control was an industrial model. Nevertheless, it did not continue to perform satisfactorily in the mesocosm environment; it should have been housed separately. Today there are many marine hardened computers that could handle both monitoring and control functions. Finally, the salinity sensors would preferably be of the inductive type to avoid corrosion and drift. Where

Chesapeake Bay in Mesocosm TABLE 22.1 Primary Physical–Chemical Parameters of the Smithsonian Chesapeake Bay Mesocosm Lighting, each unit

Three 1000-W metal halides; eight 160-W VHO fluorescents

Seasonal Photoperiod (h light) Temperature (water) (°C)

Summer 14 20–28°C

Semidiurnal Tide Oxygen

Winter 8 4–6°C

Range 6 inches Morning 6.5–7.8 mg/liter; evening 6.5–8.1 mg/liter (tidal fresh: 7.8–8.1 mg/liter; marine 6.5 mg /liter)

Varied for research or normal gradients Salinity Marine 30–35 ppt gradient to tidal fresh in steps of 4–6 ppt; vertical gradient 1–2 ppt Dissolved nitrogen Marine ⬍1 µM; polyhaline and mesohaline 3–5 µM; oligohaline 5–10 µM; tidal fresh 5–10 µM Fixed Wave action Wind

Dump buckets, 1 each, 6–15 s period; 10 gpm pump Four 12-inch rotating fans, approximately 0–10 knots

Ocean (coastal) simulation Four algal turf scrubbers of 0.97 m2 each lighted with eight 400-W metal halides nightly for 15 h Principal algal genera Enteromorpha, Bryopsis, Polysiphonia, Spermothamnion, Cladophora Production (scrubbing) rate 6–14 g (dry)/m2/day Reverse osmosis unit of 50 gallons fresh water/h capacity Freshwater removal rate 35–75 gallons/day Two sediment traps Cooling unit Scrubbed, cooled, more saline water injected into the base of the marine unit Freshwater input control Tap water, treated with RO for chlorine and suspended material; scrubbed to desirable nutrient level with two algal turf scrubbers of 0.58 m2; two 1000-W metal halides Rain on marshes of 0.1–0.15 inch/day Salinity gradient and species mobility control Deep and shallow gates of 6-inch diameter sensed by Honeywell conductivity probes and controlled by a Reliance Automate 30 E computer

appropriate these improvements have been applied to the Everglades system described later in this chapter.

The Biota of the Chesapeake Mesocosm Chesapeake Bay has a wide range of environments and habitats. In this project, an attempt was made to reproduce each of the major communities present in each salinity segment (Figure 22.2, Color Plates 49–51). Open waters with soft mud bottoms were characteristic

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of every salinity zone. Marshes, salt and brackish to fresh, were also major elements, perhaps 20% of the total area of open water. Including the water surface areas of the tide reservoirs in the mesocosm, marshes occupied about 10% of the surface area of the model. Thus, the model has about twice the proportional area of marsh than it should have. Clearly the model is more of a benthic system than the wild Chesapeake Bay, which, having a larger volume of water compared to bottom, is dominated by planktonic communities. The system was stocked direct from the wild analogs, first with underlying sediment or peat as blocks and then by the structuring elements (e.g. oyster shell or marsh grasses). The surface communities were installed by multiple small injections over a year or so. Considering the small areas involved, approximately 12 square feet in each segment, the marshes in the Chesapeake simulation were generally successful. Most of the dominant plants are present, as well as many of the subdominants. Also, the character of the marshes changes appropriately from Spartina alterniflora and Spartina patens (Color Plate 49) domination at the high-salinity end through abundant Distichlis spicata and Juncus roemerianus in the middle brackish zones, and finally shifting to Scirpus americana and Atriplex patula at the low-salinity end (Color Plate 51). Near the end of operation when maintenance was degrading, the system lost its Spartina spp. in the higher salinities to Distichlis. Whether this indicates a long-term trend in such a model is unknown. Spartina cynosuroides, although abundantly present at oligohaline salinities (1–5 ppt) in the wild, never became dominant in this system. This is probably because of the relatively large size of this grass (4–8-feet high). Finally, in the tidal fresh segment, a rich array of nearly 50 species of monocots and dicots produced the rank growth characteristic of these communities in the wild. Table 22.2 lists the higher plants that occurred in the Chesapeake complex along with the less abundant but important periphyton algal species that coated virtually all submerged surfaces in the system. The marsh surfaces and tidal channels were occupied by a variety of animals, varying with salinity levels. Fiddler crabs and wharf and marsh crabs of a half dozen different species dominated the marsh surfaces, which were often pockmarked with their tunnels. Mussels, particularly Geukensia (the ribbed mussel), occurred on the channel sides. The snails Littorina irrorata, at upper salinities, and Melampus bidentata, through the middle of the system, were abundant on the marsh grass itself. Subtidally in the marsh channels several killifish species, the blue crab, and the shrimp Palaeomonetes were conspicuous (Table 22.3). Neither beach ridges nor sandy beaches were successful in this system. The length of each unit was too

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22. Estuaries

FIGURE 22.5 Levels of dissolved nitrogen (as nitrite plus nitrate) over 31⁄2 years in the Smithsonian Chesapeake Bay mesocosm.

short to allow a sand beach profile with the wave energy required to prevent siltation. The problem was solved in the Everglades system (see below) by creating a shell beach that would maintain the steep profile required. Subtidally, both Zostera marina and Ruppia maritima were present for extended periods; however, neither was consistently successful. It seems likely that the constant burrowing activities of crabs in this small

system, without the benefit of larger predator fish that provide a major element of control in the wild, results in physical removal of these species of submerged aquatic vegetation (SAV). The relatively steep gradients in the rather short tank segments also produce sediment movement that is not conducive to SAV survival. Most of these problems could probably be solved with a model of larger dimension.

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Chesapeake Bay in Mesocosm TABLE 22.2 Kingdom Monera Division Cyanophycota (blue-green algae) Anacystis sp. (3,5,6) Microcoleus lyngbyaceous (1,2,3,4,5,6,7,8) Anabaina oscillarioides (3) Oscillatoria 3 spp. (1,3,4,5,6,8) Spirulina subsalsa (2,3,4,5,7,8) Microcoleus vaginatus (2,3,6,8) Schizothrix arenaria (2) Oscillatoria submembranacea (3) Kingdom Plantae Subkingdom Thallobionta Division Rhodophycota (red algae) Erythrotrichia carnea (8) Hypnea musciformis (6,7,8) Callithamnion byssoides (8) Dasya pedicillata (5) Antihamnion cruciatum (8) Gracilaria verrucosa (6,7,8) Polysiphonia harveyae (8) Division Chromophycota (diatoms) Bacillaria paradoxa (1,2,5) Surirella sp. (1,2,3) Nitzschia closterium (2,3,5,6,7) Synedra sp. (2) Navicula sp. (2,3,6,7) Diatoma sp. (1,8) Gomphonema sp. (1) Caloneis sp. (2) Cocconeis sp. (2) Stauroneis sp. (7) (brown algae) Ectocarpus confervoides (2,3) Ectocarpus subcorymbosus (8) Pylaiella littoralis (8) (golden browns) Vaucheria piloboloides (2,3,4) (dinoflagellates) Amphidium operculatum (4,5,6,7,8) Division Chlorophycota (green algae) Cladophora gracilis (3,4,5) Rhizoclonium crassipellitum (1) Rhizoclonium tortuosum (8) Ulothrix implexa (2,8) Spirogyra dubia (1,2) Enteromorpha clathrata (2) Enteromorpha marginata (3,4) Enteromorpha prolifera (8) Ulva lactuca (3,4,6,7,8) Chara fragilis (1) Chaetomorpha linum (4,5) Rhizoclonium fontanum (1) Rhizoclonium riparium (8) Ulothrix sp. (1) Monostroma leptoderma (3) Enteromorpha erecta (2,5) Enteromorpha intestinalis (6,7,8)

Plants Occurring in the Smithsonian Chesapeake Bay Mesocosma Percursaria percursa (4) Derbesia marina (8) Subkingdom Embryobionta Division Pinophyta (gymnosperms) Pinus taeda (loblolly) (4) Division Magnoliophyta (flowering plants) (monocots) Sagittaria stagnorum (wapato) (1) Sagittaria subulata (arrowhead) (1) Sagittaria latifolia (arrowhead) (1) Cyperus niger (flat sedge) (8) Cyperus esculentus (chufa) (1) Carex spp. (sedges) (1,2,5) Fimbristylis spadicea (cone grass) (6,7) Scirpus americanus (common three square) (2) Murdannia keisak (spiderwart) (1) Elodea canadense (water weed) (1) Sisyrinchium atlanticum (blue eye grass) (8) Iris virginica (blue flag) (1) Ruppia maritima (widgeon grass) (3,4,5,7,8) Zostera marina (eelgrass) (5,6,7) Lemna minor (duckweed) (1) Spirodela polyrhiza (water flax) (1) Elymus viginicus (virginia rye) (2) Sparganium eucarpum (burreed) (1) Wolfia sp. (water meal) (1) Distichilis spicata (salt grass) (2,4,5,6,7,8) Panicum sp. (panic grass) (2,6) Ammophila breviligulata (beach grass) (3,6,8) Polypogon monspeliensis (fox grass) (7) Panicum amarum (dune grass) (8) Acorus calamus (sweetflag) (1) Peltandra virginica (arrow arum) (1) Orotium aquaticum (golden club) (1) Eleocharis obtusa (spike rush) (1) Eleocharis parvula (spike rush) (1,2,3) Rhynchospora sp. (beak rush) (3) Scirpus olneyi (olney three square) (2,3) Hydrilla verticillata (1) Vallisneria americana (tape grass) (1) Juncus effusus (soft rush) (1) Juncus roemerianus (black needle) (4,5,6) Juncus acuminatus (rush) (1,7) Juncus megacephalus (rush) (8) Juncus gentianoides (rush) (8) Najas quadalupensis (naiad) (1)

Pontederia cordata (pickerel weed) (1) Potomogeton crispus (curled pond weed) (1) Zannichellia palustris (horned pond weed) (1) Spartina cynosuroides (big cord grass) (2) Spartina alterniflora (smooth cord grass) (2,4,5,6,7,8) Spartina patens (salt hay) (2,3,4,6,7,8) Phragmites australis (reed) (3) Setaria geniculata (foxtail grass) (7) (dicots) Amaranthus cannabinus (water hemp) (1,2) Callitriche heterophyla (water starwort) (1) Hypericum boreale (St. John’s wort) (1) Ultricularia 3 sp. (bladderworts) (1) Hybiscus moscheutos (rosemallow) (1) Kosteletzkya virginica (marsh mallow) (1) Ranunculus pusillus (buttercup) (1) Rumex crispus (sour dock) (1) Rumex verticillata (water dock) (2) Ceratophyllum demersus (coontail) (2) Polygonum asifolium (tearthumb) (1) Polygonum hydropiper (smartweed) (1) Lonicera japonica (honeysuckle) (2) Limonium carolinianum (sea lavender) (3,4,5,6,7) Hypericum virginicum (St. John’s wort) (4) Linularia canadensis (toad flax) (5,7) Mikania scandens (hempweed) (1) Iva frutescens (marsh elder) (2,3,4,5,6) Borrichia frutescens (sea oxeye) (3,4,5,6,7) Baccharis halimifolia (salt bush) (4,5) Aster sp. (5,7) Chenopodium album (lambs quarters) (5) Salicornia virginica (glasswort) (5,6,7) Atriplex patula (spearscale) (1,2,3,4,5,6,7) Impatiens capensis (1) Myriophyllum spicatum (1) Nuphar luteum (spatter dock) (1) Rosa palustris (swamp rose) (1) Galium brevipes (bed straw) (1) (Continued)

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22. Estuaries TABLE 22.2 Hydrocotyle umbellate (pennywort) (8) Hydrocotyle ranunculoides (pennywort) (1) Calystegia sepium (hedge bind weed) (2)

(Continued)

Samolus parviflora (water pimpernel) (2,3) Myrica cerifera (wax myrtle) (4) Sesuvium maritimum (sea purslane) (5) Cakile edentula (sea rocket) (5,7)

Teucrium canadense (germander) (7) Aster dumosus (aster) (1) Solidago fistulosa (golden rod) (2) Solidago stricta (golden rod) (2) Solidago sempervirens (golden rod) (3,7)

a The numbers following each species indicate the salinity levels in which it occurs (see Figure 22.2; 1, tidal fresh; 8, coastal full salinity). Except for cyanobacteria (Cyanophycota), bacteria have not been included.

TABLE 22.3 Protists and Animals in the Smithsonian Chesapeake Bay Mesocosma Kingdom Animalia Subkingdom Protozoa (flagellates) Euglena gracilis (1,2) Paranema trichoporum (1,8) Paranemopsis inflexum (1,2) Anisonema prosgeobium (1,2) Monosiga sp. (1,2,5) Stephanopogon mobilensis (5,7) Euplenid sp. (8) Anthophysa vegetans (1) Bodo saltans (7,8) Chilomonas sp. (1,3,8) Codosiga sp. (1,5) Trachelocerca sp. (2) Monas sp. (5,6) (sarcodines) Vahlkamphia sp. (1,4,6,8) Thecamoeba trichophorum (1) Centropyxis ciculeata (1,2) Arcella discoides (1,2,4,5) Arcella dentata (2) Cochliopodium sp. (5) Actinophorys sp. (1,2) Pelomyxa sp. (5) Qinqueloculina 2 spp. (5,8) Acanthamoeba sp. (2) Astroamoeba sp. (2) Flabellula sp. (2,8) Hyalodiscus sp. (2,3) Labrinthula sp. (5) Nuclearia sp. (2,4) Mayorella sp. (2) Mayorella spumosa (5,6) Amoeba sp. (7) Spiroloculina sp. (8) (ciliates) Kentrophorus sp. (1,8) Litonotus spp. (1,2,5,7,8) Loxophyllum sp. (1,2,3,7,8) Chilodonella uncinata (1) Chilodonella sp. (3,4) Amphileptus sp. (1) Lembus sp. (1) Protocruzia sp. (5) Metacineta mystacina (1) Dysteria sp. (5) Vaginicola sp. (3,4,5)

Vorticella nubulifera (1,4) Vorticella microstoma (1) Pyxicola sp. (2) Cothumia crystallina (3) Platycola sp. (4) Aspidisca costata (1,2,3) Aspidisca sulcata (6) Aspidisca spp. (1,2,3,4,7,8) Euplotes eurystoma (3,4,5) Stylonichia mytilis (1,2) Stylonchia sp. (1) Urostyla sp. (1,7) Stichotricha sp. (4,5) Certesia sp. (5) Keranopsis sp. (7) Cinetochilum marinum (8) Cinetochilum marginatatum (2,3) Cyclidium sp. (2) Frontonia sp. (2) Frontonia leucas (3,5) Pleuronema (2,4) Protospathidium sp. (2) Laurymania olar (3,4) Acineta tuberosa (2,5) Trochilia sp. (3) Parafolliculina sp. (8) Vorticella picta (1) Vorticella campanulata (1) Vorticella marina (3,7,8) Stentor finlayi (3,4,5) Epistylis sp. (4) Actinotricha sp. (1,2,4,5,7) Diophyrys sp. (3,4) Euplotes spp. (2,6,7,8) Holosticha spp. (2) Uronychia transfuga (4,6,8) Subkingdom Parazoa (sponges) Cliona truitti (borer) (4) Cliona celata (borer) (6,7,8) Halichondria bowerbanki (5,6,7,8) Microciona prolifera (red beard) (5,6) Subkingdom Eumetazoa Phylum Cnidaria (coelenterates) Diadumene leucolena (white anemone) (2,3,4) Haliplanella luciae (green striped anemone) (3,4,5,6,7,8)

Hydractinia echinata (snail fur) (6,7,8) Obelia commisuralis (8) Astrangia danae (northern coral) (7,8) Eudendrium ramosa (hydroid) (8) Phylum Platyhelminthes (flatworms) Dugesia tigrina (mottled triclad) (1) Anaperus sp. (7,8) Plagiostomum sp. (7,8) Stylochus ellipticus (oyster flatworm) (4,5,6) Macrostomum sp. (7,8) Gyrotrix sp. (5) Phylum Nemertea (ribbon worms) Micrura leidyi (4,5,6,8) Tetrastemma elegans (four-eyed nemertean) (5) Amphiporus ocraceus (red nemertean) (5,6) Phylum Gastrotricha Chaetonotus sp. (1,7) Phylum Nemata (nematodes) Adonchaimus sp. (7,8) Metacholaimus sp. (7,8) Chromadorid sp. (7,8) Tripyla sp. (1,8) Belbolla sp. (7,8) Thesistus sp. (8) Mesacanthion sp. (5) Sobatierid sp. (8) Phylum Rotifera (rotifers) Cepholodella 2 sp. (1,2,3,7) Lophocharis 2 sp. (1,3,5,6,7) Philodina sp. (1) Testudinella sp. (2,4,6,7,8) Monostylla sp. (1) Lecane sp. (1) Euchlamys sp. (2) Lapadella sp. (2) Phylum Mollusca Chaetopleura apiculata (bee chiton) (7,8) Amnicola limosa (1) Ferrissia sp. (slipper shell) (1) Gyraulis circumstriatus (flat snail) (1) (Continued)

Chesapeake Bay in Mesocosm TABLE 22.3 Littorina irrorata (southern periwinkle) (1,2,3,5,6,7,8) Pseundsuccinea columnella (1) Melampus bidentata (salt marsh snail) (2,3,4,5,6,7,8) Eupleura caudata (oyster drill) (5,6,7) Mitrella lunata (cresentic mitrella) (5) Ellptio complanata (mussel) (1) Polymesoda carolinianum (marsh clam) (1) phaerium sp. (1) Corbicula manilensis (3) Macoma balthica (3,4,5) Geukensia demissus (ribbed mussel) (4,5,6,7,8) Clappia sp. (1) Goniobasis sp. (horn snail) (1) Goniobasis virginica (1) Physa gyrina (pouch snail) (1) Hydrobia sp. (marsh snail) (2) Crepidula fornicata (slipper snail) (4,5,6,7) Nassarius obsoletus (mud dog whelk) (5,6,7) Simnia uniplicata (single toothed simnia) (8) Lampsilis sp. (mussel) (1) Pisidium sp. (1,3) Brachiodontes recurvus (bent mussel) (2,3,4,5,6,7,8) Crassostrea virginica (oyster) (4,5,6,7,8) Mya arenaria (soft shell clam) (4,5,6) Mytilis edulis (blue mussel) (6,7,8) Nuculana sp. (8) Phylum Annelida (oligochaetes) Nais communis (1,2) Chaetogaster diastrophus (1,2) Chaetogaster diaphanus (2) (polychaetes) Heteromastis filiformis (thread worm) (2,3,4,5) Platynereis dumerilli (clam worm) (2,4,5,6,7,8) Glycera dibranchiata (blood worm) (3,4,5,6,7,8) Sabella micropthalmia (fan worm) (4,5) Amphitrite ornata (terebellid) (5) Hydroides dianthus (hard tube worm) (5,6,7,8) Sabellaria vulgaris (fanworm) (6,7,8) Filograna implexa (cluster tube worm) (8) a

415

(Continued)

Marphysa sanguinea (red gilled marphysa) (8) Nereis succinea (clam worm) (2,3,4,5,6,7,8) Nereis virens (clam worm) (5,6,7) Polydora ligni (mud whip worm) (2,3,4,5,6,7,8) Polydora websteri (oyster whip worm) (2,4,5,6,7) Scolecolopides viridis (mud worm) (3) Scoloplos acutus (orbinid) (3) Diopatra cupraea (parchment tube worm) (5,6,7) Lepidonotus variabilis (12-scab worm) (6) Arabella iricolor (thread worm) (8) Phylum Arthropoda Class Insecta Oniscus asellus (terrestrial pill bug) (1) numerous unidentified flying insects and ants (all) Class Crustacea (branchipods-cladocera) several unidentified cladocerans (ostracods) Cypridopsis vidua (1) Candona sp. (1) (copepods) several cyclopoid spp. (barnacles) Balanus eburneus (ivory barnacle) (3,5,6,7,8) Balanus balanoides Balanus improvisus (bay barnacle) (3) (isopods) Asellus militaris (1) Edotea triloba (5) Erichsonella attenuata (3,4,5) (amphipods) Gammarus fasciatus (1) Gammarus mucronatus (2,3,4,5,6,7) Gammarus oceanicus (scud) (7,8) Leptocheiris penguis (3) Leptocheiris plumosus (5) Corophium spp. (4,5,6,7,8) Ampelisca abdita (four-eye) (5) Elasmopus levis (5) (decapods-shrimp, crabs, lobsters) Orconectes limosus (crayfish) (1) Rhithropanopeus harrisii (mud crab) (2,5,6,7 8) Uca pugnax (mud fiddler) (2,3,4,5,6,7,8) Uca pugilator (sand fiddler) (5,6,7,8)

Callinectes sapidus (blue crab) (3,4,5,6,7,8) Hexapanopeus angustifrons (mud crab) (4) Eurypanopeus depressus (mud crab) (4,5,6,7,8) Sesarma cinereum (wharf crab) (2,3,4,5,6) Palaemonetes vulgaris (shore shrimp) (2,3,4,5,6,7,8) Neopanopeus sayi (mud crab) (4,5,6,7,8) Libinia dubia (spider crab) (5,6,7,8) Pagurus longicarpus (hermit crab) (5,7,8) (tanaids) Tanais cavolini (5,6,7) Phylum Bryozoa (moss animals) Membranipora tenuis (3,5,7) Schizoporella unicornis (7,8) Membranipora membranacea (4) Alcyonidium verrilli (6,7,8) Phylum Echinodermata Asterias forbesi (sea star) (6,7,8) Thyone briareus (hairy cucumber) (6,7,8) Arbacia punctata (purple urchin) (7,8) Leptosynapta tenuis (white sea cucumber) (4,5) Phylum Chordata (tunicates) Molgula manhattensis (sea squirt) (8) (vertebrates) Fundulus diaphnus (banded killifish) (3) Lepomis macrochirus (blue gill) (1) Fundulus majalis (killifish) (2,3,4,5,6,7,8) Cyprinodon variegatus (sheepshead minnow) (2,3,4,5) Menidia menidia (Atlantic silversides) (4,5,6,7) Tautoga onitis (tautog) (7) Urophycus regia (spotted hake) (8) Lepomis gibbosus (pumpkin seed) (1) Gambusia affinis (mosquito fish (1) Fundulus heteroclitus (mumichog) (2,3,4,5,6,7,8) Trinectes maculatus (hog-choker) (3,4,5,6) Gobiesox strumosus (skillet fish) (4,5,6) Gobiosoma bosci (naked gobi) (6) Mugil cephalus (striped mullet) (8)

The numbers following each species indicate the salinity levels in which it occurs (see Figure 22.2; 1, tidal fresh; 8, coastal full salinity). Protists courtesy D. Spoon.

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Continuing seaward, each of the main bay segments from 2 through 7 had an oyster bar characteristically with Crassostrea virginica, Ischadium recurvus, Crepidula fornicata, Balanus eburneus, and the annelid worms Nereis succinee and Polydora lignii, as well as several mud crabs and the anemone Diadamena leucolena. Although these bars appeared to function quite well in the short term, predation by oyster drills, blue crabs, and human activity limited their diversity in the long term. In a system of this dimension, it is essential that human investigation and management do not in themselves become major disturbance factors. The block construction of the Everglades system allows internal sampling activity without the intensity of disturbance that characterized the Chesapeake mesocosm. Of all the major groups of invertebrates, the bivalve molluscs had the greatest difficulty in the Chesapeake model. In spite of the conspicuously successful reproductive performance and population buildup of Corbicula in fresh water and Geukensia in brackish water, many bivalves did not survive in the long term. Although a quantitative study of plankton was not carried out in the Chesapeake mesocosm, a careful qualitative study showed a water column rich in diatoms, flagellates, and ciliates, with a few copepods and ostracods but very few invertebrate larvae compared to the Everglades model described below. Since most bivalves probably feed on planktonic algae and organic particulates, the answer to the bivalve problem would not seem to lie in the available feed. Bivalve molluscs often suffer heavy predation in the wild, which is generally overcome by recruitment of new larval stocks. Each of the salinity segments in the Chesapeake system was driven by a 10-gpm-impellor pump that provided a flow to the tidal chamber and simulated tidal currents. The use of disc-flow or other nontraumatic pumps would probably improve this situation though, as we discuss below, oysters continue to be a problem in the Everglades system, where disc-flow pumps are used. In addition, a primary need of a system like the Chesapeake model which must be divided into small volumes to simulate a salinity gradient, is a variety of refugia from fish and larger crabs. Beyond the oyster bars, the tanks dropped off to their greatest depth of about 5 feet. Ramps leading down to this muddy bottom allowed all animals easy access between shallow and deep bottoms and provided dark areas, completing the entire range of depth (on a light basis) in the wild Bay. This deep muddy bottom was populated by a variety of small bivalves and worms. Many important invertebrate species reproduced repeatedly in the Chesapeake mesocosm. In addition to the bivalves mentioned above, many snails, anemones, amphipods, copepods, and a wide variety of annelid

worms were conspicuously successful. Perhaps the most striking example, because of its complex behavior and food web position of higher predator and scavenger, was that of the blue crab, Callinectes sapidus (Color Plate 52). Both males and females bury themselves in deep muds in the winter. However, in the wild the females migrate to the mouth of the bay to do so. In the mesocosm, a similar migratory pattern was followed (to segment 8), and young crabs appeared in the spring in several years. Because of the large size of the older generations of blue crabs and the damage they cause to the system, we harvested these animals in the spring and early summer. Many fish are long-term individual members of the Chesapeake model (Table 22.3). Indeed, some of the mid- to top-level predators, such as tautog, red drum, and chain pickerel, were quite successful in achieving large size (10–12 inches) after being introduced as small fry and eventually had to be removed. However, only the cyprinodonts (Fundulus and Cyprinodon spp.) showed consistent reproductive success. These are small fish with considerable breeding populations, difficult to achieve in a system this small with drum or croaker, for example. On the other hand, even silversides and anchovies did not show long-term success in the model. These matters we discuss in greater depth below. It would be particularly valuable at this time to construct a new Chesapeake or equivalent model utilizing the lessons learned. The use of nontraumatic pumps and the construction of a somewhat larger system (2–5 times larger), with a corresponding larger tide, would likely provide the largest contribution to species diversity increase. A greenhouse situation with no height restriction would also raise biodiversity and greatly assist in management. It is nevertheless encouraging for the modeling of complex estuarine systems that the biogeographic distribution was so similar to the expected wild distribution (Figure 22.6).

A FLORIDA ESTUARY IN MESOCOSM Including the area called the Big Cypress Swamp, the Florida Everglades is a large subtropical wetland of about 5000 square miles. In pre-industrial times, the principal freshwater movement in this wet savanna was sheet flow out of the Kissimmee River complex and Lake Okeechobee and Big Cypress areas south and west to Florida Bay and the Gulf of Mexico. Flow patterns became highly modified during the 20th century by the construction of canals and controlled-flow gates and the diking of Lake Okeechobee. For purposes of developing a reasonably well-known subtropical estuarine model, we chose an area near

A Florida Estuary in Mesocosm

417

FIGURE 22.6 Biogeographic patterns in the Smithsonian Chesapeake mesocosm from a species tally

carried out in 1988. 䉱 number of species in tank 1 (fresh water) and the number of those species that occur elsewhere in the estuary; 䊉 species in tank 8 (full salinity) and their occurrence “up” the estuary; 䊐 species in tank 4 (mesohaline salinity) and the number that occur “up” and “down” the estuary.

Everglades City in the Ten Thousand Islands region. Here, the gradient of the Big Cypress Watershed is relatively steep and all zones from high salinity and sand beach, seagrass beds, and worm reefs, through mangrove and salt marsh, to fresh marsh and forest hammocks are well developed along a band about 30 miles wide. Readers interested in a review of the natural history of the Florida Everglades and its coastal waters can consult Douglass (1988), Drew and Schomer (1984), Schomer and Drew (1982), Britton and Morton (1989), and Davis and Ogden (1994). At 22 000 gallons and 1400 square feet, the Everglades estuarine mesocosm was planned to be somewhat larger than the Chesapeake model. Instead of artificial lighting, which would have been quite costly, a greenhouse system was built. Because of the often heavy cloud cover in the South Florida region, the difference in yearly incoming light between Washington, DC, and South Florida (see Figure 5.6) was relatively small, and we felt that natural, unshaded greenhouse light would be adequate as long as artificially lit scrubbers were used to simulate the Gulf of Mexico interaction with the coastal waters. Also,

in this case, we decided that a cement and butyl-rubberlined concrete block basin would provide the simplest and cheapest method of construction. The physical layout of the system constructed is shown in Figure 22.7. Many modern estuaries are geologically sited such that they lie within thick basins of sediment delivered by their own rivers and the adjacent coastal currents. That is certainly true of the Chesapeake ecosystem. In the Florida Everglades, however, relatively flat limestones mostly with a microkarst topography lie at shallow depth. Under the estuarine portion, these limestones are deep enough so that in our modeling we were able to simulate underlying structure simply with the oyster shell or silty/peaty sediments characteristic of each zone. Since the yearly and even weekly salinity range at any one site is considerably larger for the Ten Thousand Islands estuarine region than the Chesapeake Bay, the computer-controlled gate system between salinity units was not used. Instead, narrow passes with adjustable weir gates and progressively lower tides upstream were employed (Figure 22.8). This system has been quite successful, and the weir sliders have not been used except

418

22. Estuaries

FIGURE 22.7 Layout of the Smithsonian Florida Everglades mesocosm as configured from 1991 to 1997. The longest dimension, including tanks 1, 2, 4, and 5, as shown is 21.5 meters long. The freshwater part of the system is treated separately in Chapter 23.

FIGURE 22.8 Longitudinal and vertical section of the Florida Everglades mesocosm, showing water levels, weir gates, and water management and control systems.

to raise rainy season water levels in the fresher sections. The physical parameters and salinity gradient achieved are shown in Table 22.4. Tides are an extremely important element of the estuarine Everglades. As in other microcosms and mesocosms, stepping motor control of water level in a tidal

reservoir was employed (Color Plate 48). However, here, the complex diurnal–semidiurnal tide of the Ten Thousand Islands area required three stepping motors (Figure 22.9). Also, to save space in the fixed size of the greenhouse, the estuary proper (tanks 2–6) was used as the tidal reservoir for the Everglades coast (tank 1) (see

419

A Florida Estuary in Mesocosm TABLE 22.4

Primary Physical–Chemical Parameters of the Smithsonian Florida Everglades Mesocosm Tank dimensions (inches, feet)

Community Marine (Gulf of Mexico) seagrass bed, sandy beach, and beach ridge Red mangrove and tidal channel Oyster bay and mangrove Black mangrove and tidal channel Salt marsh Oligohaline marsh Freshwater pond Savanna with hammocks and stream Total

D

W

L

Tank volume (liters)

Surface area, feet2 (m2)

Normal salinity range (%)

22 600

450 (42.1)

28–35

21 200 4440 5165 3978 4320 8375 18 146

250 (23.4) 81 (7.6) 86 (8.0) 84 (7.9) 79 (7.4) 84 (7.9) 280 (26.2)

26–32 24–30 18–28 5–25 0–10 0 0

43⬙ ⫻ 18’9⬙ ⫻ 36’

34⬙ 22⬙ 24⬙ 19⬙ 22⬙ 40⬙ 26⬙

⫻ ⫻ ⫻ ⫻ ⫻ ⫻ ⫻

13’4⬙ 8’9⬙ 9’4⬙ 9’4⬙ 8’9⬙ 9’4⬙ 9’4⬙

⫻ ⫻ ⫻ ⫻ ⫻ ⫻ ⫻

18’9⬙ 9’3⬙ 9’ 9’ 9’ 9’ 30’

(22 000 gal) 88 224 liters

1394 feet2 (130.3 m2)

Principal operating characteristics Seasonal Summer Winter Lighting In greenhouse, natural light, Washington, DC Temperature Air (°C) 20–40 10–20 Water (°C) 25–29 15–20 Rain Wet season 0.3 inch/day Dry season 0.1 inch/day Daily Wind Afternoon, to 10 knots Tide Mixed diurnal/semidiurnal, 1 foot marine and red mangrove, decreasing to 3 inch salt marsh Wave action 3–4 inch wave height, marine only

Figure 22.7). At spring high tide on the coast and therefore low spring tide in the estuary, a large gate valve was opened to allow larger animals direct access between estuary and coast. Other environmental needs such as wind and rain are achieved by large fans (Color Plate 48) and a standard sprinkling system. The latter provides 0.1 inch/day in the January through May dry season and 0.3 inch/day in the June through December wet season. RO-treated tap water is used for rain and all evaporative “top-up” requirements. During the summer, windy/rainy afternoons are initiated to simulate the afternoon thunderstorm cycle. The RO water maker process of removing fresh water from the Everglades coast tank and delivering it to the upper estuary is also an important element in simulating the evaporation–precipitation cycle and the salinity gradient. However, since this wind/rain pattern is quite mild relative to the typically intense thunderstorm of the wild Everglades, occasionally a hose is used to spray directly on the vegetation with some force. We have found this to be a major control device for insect pests, and it is the only control method that we have found to be both ecologically sound and effective. The ocean simulator process and unit size employed on the Everglades tank in the system are the same as we

used on the Chesapeake mesocosm. We will not repeat the discussion in detail except to note a few critical points. On these estuarine scrubbers, scrubbing rates of 15–18 g (dry algae)/m2/day can be produced; however, in month-to-month practice with levels of maintenance varying considerably, only 10–12 g (dry)/m2/day was routinely achieved. Micrograzer (amphipod) grazing can be intense on these scrubbers. If amphipod populations in the absence of predation are allowed to explode, this can seriously reduce the efficiency of the scrubbers. Routine scraping every 7–12 days, with attention to the cleaning off of amphipods in the scrubber trays, is essential to adequate nutrient control. Note that here, as well as on the Chesapeake scrubbers, internal recycling of 10 gpm was used on each scrubber to achieve adequate scrubber flow and surge while minimizing turnover volume from the Everglades coast tank. Generally, 2–4 hours of RO operation per day (averaging 80–160 gallons of fresh water per day) along with 50–150 gallons of rain (replacing evaporation) was adequate to maintain the desired salinity gradient. A nutrient dynamics section follows our discussion of the biota of the Everglades model. Three propane heaters, with a total capacity of 385 000 BTU, are used to keep the Everglades greenhouse air at a

420

22. Estuaries

FIGURE 22.9 Tidal control system for the Everglades estuary. The bottom stepping motor has a diurnal cycle (one rotation per 24 h 40 min), the middle motor has a semidiurnal cycle (12 h 20 min), and the topmost motor simulating neaps and springs rotates once every 2 weeks. At every spring tide the system is readjusted to match the times of spring highs on the southwest outer coast of Florida.

minimum of 45°F on the coldest winter nights. Two sets of 1000-W water heaters were used to keep the Everglades coast and savanna streams at greater than 18°C under the same conditions. The estuary is allowed to follow, being

heated at both ends, and has never gone below 15°C under this regime. A similar practice is followed in summer for cooling. The greenhouse atmosphere, with large wall-mounted fans pulling outside air through the


house, is allowed to follow ambient temperature plus greenhouse effect. Occasionally the air in the greenhouse reaches 40°C (110°F). On the other hand, the waters of the saltier and fresher ends of the model are chilled using titanium heat exchangers, allowing a maximum temperature of 30°C in the coast and savanna stream waters. The estuary waters seldom rise significantly above this. Wave action is not used on the Everglades estuary and stream. In the wild, these areas generally consist of narrow channels and only rarely do significant waves develop. The Everglades coast, on the other hand, has moderate wave energy, at least occasionally, in the wild. The required simulation of wave action in the model was achieved with a single large dump bucket. As we discussed in the first edition, we experimented with a wide variety of nontraumatic pump types on this system, including a large Archimedes’ screw. Most of these could have been successful with appropriate design and construction. For the past 5 years we have used disc-flow pumps as a compromise between pump trauma and ease of maintainance.

Communities, Biota, and Food Webs of the Florida Everglades Mesocosm The Ten Thousand Islands area, which the mesocosm models, has a particularly strong estuarine gradient ranging from full coastal salinity to full fresh water over about 50 km. We begin our description of the mesocosm with a look at the distribution of the dominant species of all the major groups studied along that estuarine gradient. After that we discuss the communities that have formed along that salinity gradient and wherever possible we point out the nature of the food webs. Figure 22.10 shows the distribution in late 1995, by percentage of individual plants, of the dominant vascular plant species in the Everglades mesocosm. The species are arranged to show their community relationships. All of the species shown here maintained their populations through either vegetative propagation or flowering and seed production. Many of the minor species also maintained their populations reproductively, though a significant number were lost, mostly during the early years. The minor and more open mangrove community of the Gulf shore (No. 1), with its ground cover of the succulent Sesuvium portulacastum gave way to dense mangroves and their limited understory species in the lower estuary units (2, 3, and 4). By the upper estuary salt marsh (No. 5), the mangrove swamp community was beginning to give way to a small area of marsh, and this trend continued into the oligohaline unit (6). The dominant organisms in the freshwater system are given in these diagrams for continuity. However, in this book that system is discussed separately in Chapter 23.

421

In all parts of the Everglades mesocosm, including the Gulf shore, vascular plant stems, roots, prop roots, pneumatophores, and detritus provided physical structure to many of the individual communities, both terrestrial and aquatic (Color Plates 43–49). A major section of the Gulf shore (No. 1) was dominated by a seagrass bed, which provided a primary habitat addition to the sandy bottom environment. In addition to providing habitat, primarily as woody surface, and spatial heterogeneity, the vascular plants also provided a major element of organic energy supply, some as fruits, but mostly as leaves, bark, and twigs. These materials are broken down as litter in the aquatic system. This process occurs on the scale of weeks to months, in part by fungal and bacterial action, but also by invertebrate and vertebrate reworking of the vegetative fragments with their saprophytic components. Considerable hard substrate for attached algal colonization, including vascular plant parts, occurred in both the wild Everglades systems and in the mesocosm. In the Gulf shore (No. 1), a worm reef of vermetid gastropods extended across the entire tank in the high-energy lower intertidal and subtidal, and to a lesser degree extends over the sandy bottom. A bivalve shell bed occupies much of the shallower intertidal shore. The tank wall structures and water movement systems, including the algal turf scrubber water control system, provide additional benthic algal substrate. Finally, some species that are adapted, at least in part, to living on sand or mud substrate were common in these environments. The distribution of the dominant benthic algal species, based on both relative frequency of occurrence and abundance in each sample, is given in Figure 22.11. A very strong and consistent estuarine gradient was present, and was sharply defined only at the oligohaline/fresh (No. 6/No. 7) boundary. In general, algal biomass (and probably productivity) was very high in the Gulf coast system (No. 1) and decreased significantly in the strongly shaded lower and mid-estuaries (Nos. 2–5). There was very little algal primary production (due to intense shading) in the oligohaline unit (6). After 9 years of operation and 4 years of virtual isolation, the Gulf shore system (No. 1) had a rich array of macroinvertebrate species (42 species) from many of the major phyla (Figure 22.12), with nearly 1 species for each square meter of surface. This number fell rapidly into the Lower Estuary (29 species) where the 1 abundant sipunculid of the Gulf shore did not occur and molluscs in general were sharply reduced in abundance. Only the annelids and arthropods maintained their abundance into the lower estuary. In the upper part of the lower estuary and in the upper estuary, the annelids and sponges were lost, the molluscs greatly reduced, and both the diversity and the abundance of

422

22. Estuaries

FIGURE 22.10 Relative abundance, based on numbers of individual plants, of the dominant vascular plants in the Florida Everglades mesocosm. The species (or genera, as appropriate) are grouped by subcommunity relationships. Modified from Adey et al. (1996).

invertebrates continued to fall sharply. In tank 6, the invertebrate communities were quite depauperate and represented only by a few ostracods and copepods. In the Gulf shore system, the protists showed a similarly wide diversity of species derived from many taxa and feeding types (Table 22.5). The grazing ciliates and amoebae dominated in this microcommunity, primarily preying on bacteria and the rich diatom flora. While there is a sharp drop in diatoms into the strongly shaded estuary, and especially into the upper estuary, there was only a moderate reduction in the array of protozoans. Although a number of taxa of diatoms were restricted to either the Gulf shore and lower estuary or fresh water, there are also a number of genera that

ranged through the entire system. Differentiated at the species level, a strong separation appeared across the salinity gradient. Probably the base of this microfood web shifts from diatoms to detritus into the estuary. The grazing ciliates and the surface-scrubbing amoebas in the aquatic systems of the mesocosm occurred at high diversity and are arrayed, by and large, by species over narrow salinity ranges. Although the species diversity of both ciliate grazers and amoebas dropped from the Gulf shore into the estuary, in abundance units, those species that remain increased. The sessile, ciliate filter feeders maintained their diversity into the estuary and yet showed a drop in abundance units. The general upstream decline in species diversity and abundance


423

FIGURE 22.11 Relative biomass of the dominant algal species in the Florida Everglades mesocosm. The most abundant species are also shown pictorially. Although there are some abrupt cutoffs from one ecological unit to the next (a number of reds and browns do not enter the estuary), most species occur over gradients and peak in definitive parts of the estuary. This demonstrates the creation of a gradient that in the wild occurs over many kilometers. Modified after Adey et al. (1996).

seen in the macroinvertebrates also occurred in the protist groups. However, unexpectedly, protist abundance recovered to some degree in the oligohaline unit (6), and the small, acoelous/pseudocoelous micrometazoans

(nematodes, gastrotrichs, rotifers, etc.) reached their peak of species abundance. As might be expected, the protozoan predators of other protozoans and small metazoans were not nearly

424

22. Estuaries

FIGURE 22.12 Relative abundance of the principal invertebrate species in the Florida Everglades mesocosm. Forty-two invertebrate species were tallied in the Gulf coast unit (this is not an exhaustive count and several groups were omitted from analysis). Many of these extend into the lower estuary, though most do not extend further into the upper estuary. Modified after Adey et al. (1996).

as diverse or as abundant as the grazers, including the amoebas and the filter feeders (Table 22.5). However, the uppermost estuary (No. 6) was disproportionately rich in protozoan predators. The fish community of the Everglades mesocosm was dominated overwhelmingly by two major groups, the Cyprinodontidae (killifish) and the Poeciliidae (live

bearers), both of which are keystone groups in wild Florida Everglades environments (Odum et al., 1982). The killifish ranged from about 80% of all individuals (eight species) in the Gulf shore system (No. 1) to less than 30% in fresh water (Figure 22.13). The success of these two families can be attributed to their reproductive strategies. Poeciliids are viviparous (live bearers)

425

A Florida Estuary in Mesocosm TABLE 22.5 Protists (Diatoms and Protozoa) in the Aufwuchs or Surface Film Communities of the Florida Everlades Mesocosma Unit 1 Gulf shore 1989 Diatoms (all autotropic) (centralean unicells) Coscinodiscus sp. Cyclotella sp. (centralean filaments) Biddulphia Melosira spp. (pennalean unicells) Nitzschia sp. Caloneis sp. Licmophora sp. Amphiprora sp. Nitzschia closterium Nitzschia longissima Cymbella sp. Cocconeis 5⫹ spp. Navicula 2⫹ spp. Pleurosigma spp. Synedra 2⫹ spp. Tabellaria 2⫹ spp. Amphora 2⫹ spp. Fragilaria 2⫹ spp. Bacterial and particulate browsers Bodo sp. Stephanopogon sp. Anisonema sp. Peranema trichophora Peranemopsis sp. (flagellates) choanoflagellate Codonocladium cymosum (amoebas) Nuclearia sp. Cochliopodium sp. Euhyperamoeba sp. Hyalodiscus sp. Vahlkampfia sp. Vahlkampfia avara Flabellula sp. Acanthamoeba sp. Arcella 2⫹ spp. Actinophrys sol Arcella vulgaris Arcella dentata Centropyxis sp. Cochliopodium sp. (foraminifera) Ammodiscus sp. Quinculoculinas sp. Grazing ciliates Chlamydodon sp. Diophrys scutum Diophrys appendiculata Peritromus sp. Urostyla sp. Psammomitra sp. Protocruzia Holosticha 2⫹ spp.

III

II II II

IV

1995

Units 2, 3, 4 Lower estuary 1989

1995

II II

II II

II

I II

Unit 5 Upper estuary 1989

1995


1995

I II

III II II III III II III II III II

I II

II III II II I III

I

II II II

II III II

II

II I

I II

II

II

I I I

II II III I III II I I

IV

II

II

IV

IV

II I II

I

II II I

II

III II

II II II III II II I

II I II II

I I

II

IV II I

II (Continued)

426

22. Estuaries (Continued)

TABLE 22.5 Unit 1 Gulf shore 1989 Frontonia spp. Euplotes sp. Euplotes crassus Keronopsis sp. Epiclintes ambiguum Atopochilodon distichum Aspidiscus 4 spp. Actinotricha sp. Dysteria sp. Haplosticha Orthodonella sp. Nassula sp. Prorodon sp. Trochilia 2 sp. Euplotes eurystoma Stylonychia mytilis Stylonychia sp. Chilodonella sp. Cinetochilum magaritaceum Aspidisca costata Frontonia sp. Holosticha sp. (filter-feeding ciliates) Vorticella sp. Metafolliculina producta Vorticella marina Vaginicola 2 sp. Vaginicola grandea Parafolliculina sp. Chaetospira sp. Vorticella microstoma Lagotia sp. Platycola sp. Platycola longicollis Stentor igneus Vorticella convallaria (omnivorous ciliate) Uronychia tranfuga Predators of protozoans and small metazoans (amoeba) Mayorella 2 spp. (ciliates) Loxophyllum 2⫹ spp. (free-swimming ciliates) Coleps hirtus Paramecium trichium Strombidium sp. Urocentrum turbo Hilteria grandinella Kentrophorus sp. Amphilptus spp. Litonotus 2 spp. Lacrymaria sp. Lacrymaria olor Tracheophysllum sp. Hemiophyrs sp. a

1995

II II II

II

Units 2, 3, 4 Lower estuary 1989 I I I I I I II I I

Unit 5 Upper estuary

1995

1989

I II

II I

1995


1995

II

II I

I I II

II III II II II I

II II I II

I II II II

II

II

II I

II II I II II II I

II III I II I

II

II

II II II I II II II

II II II

II I II

II

II I II

I

II

I

I

II

III

I

I I I I

I

I I I I

I I II I

II I II

II I

Abundance scale: I, rare, 1 individual; II, scarce, 2–10 individual; III, moderate, 11–100 individuals; IV abundant, 101–1000 individuals; on standard settling plates. From the research of Dr. Donald Spoon (see Adey et al., 1996).


427

FIGURE 22.13 Principal fish of the Florida Everglades mesocosm. With the possible exception of the pinfish (see text), all of these species maintain their populations by sexual reproduction. Modified after Adey et al. (1996).

while cyprinodonts are oviparous (egg layers). The advantage of vivipary is clear in that the offspring are fully developed. The oviparous cyprinodonts breed frequently under optimal conditions and have rapidly developing, advanced larvae. These characteristics

give them a significant advantage over other families. (Note that the least killi is a poeciliid.) The eight species of killifish that occurred in the Everglades mesocosm are more or less evenly distributed along the estuarine gradient with two to three

428

22. Estuaries

species per unit. However, the lower estuary has four reproductively successful species. These species were all more or less omnivorous but with a strong tendency to feed on small invertebrates. The sailfin molly (Poecilia latipinna), primarily an herbivore on algae, occurred through the entire Everglades mesocosm (full salinity to fresh water) at a level of 10–30% of all fish individuals. In the freshwater unit (7), the molly was joined by the omnivores, the guppy (Poecilia reticulata), and the mosquitofish (Gambusia affinis), as well as by the least killi (Heterandria formosa). Several small groups of currently nonreproducing species occurred in the Gulf shore system, the lower estuary, and the freshwater units. One of these fish in the Gulf shore system, the blue tang (Acanthurus coeruleus), is primarily herbivorous on algae and seagrasses. The other species are largely carnivorous with a strong tendency to prey on invertebrates and smaller fish. These species undoubtedly occupied a higher trophic level in the system food webs than the killifish and poeciliids, and thus may be food limited. However, the key element in their long-term reproductive failure likely lies in their planktonic larval stage. This is discussed further below.

Community Structure The main structural element of the shell community in the Gulf shore unit was a substrate of shells of Mercenaria campechiensis and other bivalves. The dried Mercenaria shells, within a year or two, developed a conspicuous bluish-green calciferous mat of the cyanobacteria (bluish-green algae) Calothrix crustacea and Microcoleus sp. The dominant grazer on the blue-greens in this high intertidal area was the snail Cerithium lutosum which, in spite of the granular carbonate, heavily grazed the shells and keeps algal biomass at low levels. Abundant small invertebrates, mostly grazers, also occurred in this community, including the isopod, Cyathura polita, ostracods, Cypridina sp., and unidentified harpacticoid and cyclopoid copepods. Several killifish foraged on these small invertebrates at high tide. The main structural element of the conspicuous worm reef community was cobble-sized slabs of the cemented shells of the vermetid mollusc Petaloconchus nigricans lying on sand and shell fragments. These worm reefs are subfossil, as in the wild, and had few, if any, living worms in the system. Primary producers on subtidal and lower intertidal portions of the reef were the greens Caulerpa verticillata and Ulva lactuca as well as the fleshy red Hypnea musciformis. In the mid-intertidal, on flat-lying portions, dark green mats of Oscillatoria sp. covered the surface. The dense algal cover on the worm reef supported large populations of isopods (Erichsonella attenuata,

Cyathura polita), amphipods (Ampithoe sp. and Corophium sp.), and myriad copepods, ostracods, nematodes, flatworms, ciliates, and other protozoans. Other invertebrates dominant in the worm reef were bristle worms (Eurythoe complanata), isopods (Paracerceis caudata), and the grazing cerith (Cerithium lutosum). Sponges, especially two species of Haliclona, were abundant, and thus this community had a considerable capacity to filter suspended organic material from the Gulf shore water column. Omnivorous killifish and the sailfin molly constantly browsed the worm reef surface. The primary structural element of this community was a shallow layer of sand and shell fragments lying on the partially exposed tank floor. On the bottom, a tightly woven mat of the red alga Acanthophora spicifera had developed, intermixed with a number of lesser abundant red algal species. The symbiotically photosynthetic anemone Aiptasia pallida was also very abundant in the mat of A. spicifera. On the margins of the stream, in the intertidal, but under a dense canopy of the flowering plant Sesuvium portulacastrum, subcommunities rich in the filamentous green Cladophora crispula and the red Murreyella periclados had developed high biomass mats. As with the intertidal worm reef and shell beach, omnivorous killifish (at high tides) and numerous gammarid amphipods (at all times) graze the stream flat. A primary element of the Gulf shore system, as in the wild analog, was a dense community of seagrasses in a carbonate sand poor in organic particulates. While all three dominant flowering plants of the wild systems were present (Thalassia testudinum (turtle grass), Syringodium filiforme (manatee grass), and Halodule wrightii (cuban shoal grass)) and all three occupied the central portions of the bed, H. wrightii dominated in the shallow portion and S. filiforme dominated along the deeper fringe. The seagrass blades seasonally supported a diverse flora of algal epiphytes. During the late summer, the blades virtually disappeared under a heavy load of epiphytes, indicating a dynamic production versus browsing balance. Blue tangs (Acanthurus coeruleus) were added in 1994 to reduce this late season epiphyte load, and they were quite successful in reducing epiphytes. As in the wild ecosystem, numerous epifaunal invertebrates characterized the seagrass bed, including the turtle grass anenome Viatrix globulifera; polychaetes, Spirorbus spp.; the tanaid Tanais cavolini; and various ostracods. In the sediments polychaete worms have proliferated. The dominant burrower was Nephtys bucera, a carnivore known to feed on small bivalves, other worms, and crustaceans. Small pieces of hard substrate supported sabellid fan worms and spirorbids. Common deposit-feeding worms were Aricidea fragilis, Melinna maculata, and Cirriformia filigera. The filter-feeding bivalve mollusc Codakia orbiculata was extremely abundant


especially in the sediments of the deeper end of the Gulf shore system, where its densities sometimes exceeded 50 individuals per liter of sediment. At the sediment–water interface the deposit-feeding sipunculid Phascolion strombi occupied about 75% of the available empty cerith shells that were over 6 mm long. Besides the grazing blue tangs, noted above, and various omnivorous killifish, also found in the seagrass bed, there were several carnivorous pinfish, Lagodon rhomboides; a single gulf toadfish, Opsanus beta; and the Spanish grunt, Haemulon macrostomum. In earlier years, the pinfish reproduced and individuals were often removed to reduce predation on young killifish and mollies. The carnivorous fishes primarily ingested amphipods as well as various ostracods and copepods and an occasional young killifish. Based on in situ observations, the toadfish supplemented its diet with the sipunculid Phascolion strombi, while the spanish grunt additionally ingested the polychaetes Nephtys bucera and Ninoe nigripes and the tanaid Tanais cavolini. The lower estuary (Nos. 2–4) was structured and strongly dominated by the mangroves Rhizophora mangle and Avicennia geminans. These two species exported leaves to the aquatic environments of the estuary, where they formed a dense litter over the fine sediment. The red mangroves flowered more or less continuously and abundantly release viable propagules, while black mangroves flowered seasonally and were only rarely successful in releasing viable propagules. Along with the algae that coated the upper surface of the leaves, the prop roots, and the pneumatophores of the mangroves, the propagules provided the primary base of the detrital food web. Above the water line, the mangrove crab (Aratus pisoni) existed in small numbers. The dominant primary producers on the prop mangrove roots of the lower estuary were the black, feathery red algae Bostrychia montagnei, the filamentous red Murreyella periclados, and the rhizomatous green Caulerpa verticillata. The latter two species were often found forming a mat extending across the leaf litter from prop root to prop root. Approximately 80% of the submerged sediment surface of the lower estuary was occupied by a complex algal mat. In addition to the mat of algae, the submerged and lower intertidal portions of the mangrove prop roots supported a reduced community of herbivores and invertebrates, notably the archaeogastropod Scissurella cingulata and a microcrustacean assemblage similar to that in the Gulf shore. Cyprinodon variegatus, a small but abundant omnivorous fish, appeared to have a diet predominantly of the algae Caulerpa verticillata and Murreyella periclados as well as the microcrustaceans associated with them. These algae were also intensively grazed by the sailfin mollies, Poecilia latipinna.

429

The principal hard substrate in these tanks consisted of “reef patches” of the shells of dead oysters, Crassostrea virginica. The primary producers growing on these shells were mostly the same algae that occurred on the mangrove prop roots, except that Bostrychia montagnei was conspicuously absent. The algae were primarily grazed by Poecilia latipinna and copepods, while the dominant predators of the grazers were the fish Eucinostomus gula and the crab Panopeus herbstii. This community was conspicuously characterized by abundant organic-rich silt, in large measure derived from mangrove leaf litter; the principal detrital/deposit feeders reworking this organic-rich fine sediment were the polychaetes Melinna maculata and Cirriformia filigera. The surface sediment in the lower estuary was largely made up of the fallen and rapidly decaying leaves of Rhizophora mangle, Avicennia germinans, and Laguncularia racemosa. Leaf litter degradation was performed by bacterial and fungal action, as well as invertebrate and vertebrate browsing. Only 6 months was required for reduction to less than 1-mm-size detritus. In Avicennia leaf litter, in the high intertidal region, the bacterial and fungal-grazing snail Truncatella pulchella was common. The majority of the accompanying benthic individuals subtidally are filter and deposit feeders; these organisms were working the bacterial-covered organic silt from leaf degradation and included the bivalve Codakia orbiculata and the polychaetes Capitella sp., Melinna maculata, and Cirriformia filigera. The dominant grazers of the overlying algal mat were Poecilia latipinna, Cyprinodon variegatus, and copepods, and the principal higher predators were the fish Eucinostomus gula and the crab Panopeus herbstii. The tanaid Tanais cavolini feeds largely on copepods. When constructed, the upper estuary tank 5 was dominated by salt marsh grasses and rushes. Over time, however, this community had become dominated by a red mangrove and three very large, rapidly growing, white mangroves (Laguncularia racemosa). The white mangroves flowered seasonally and repeatedly set seed. The expanding swamp forest crowded out and shaded the sedges and grasses, and secondarily changed and reduced the invertebrate community that originally occupied the system. The structural elements that remained in this system were the pneumatophores and prop roots of the mangroves; these supported a dense mass of the green algae Cladophora repens, Chaetomorpha gracilis, and Boodleopsis pusilla. B. pusilla dominates in the supratidal, forming domed cushions, and C. repens, having a similar form, occurred somewhat lower in elevation. The algal mat cover that was quite extensive in the lower estuary decreased farther up the estuary, reaching about 40% cover in this tank and becoming reduced to virtually

430

22. Estuaries

zero in tank 6. The dominant grazers were Poecilia latipinna, transient killifish, and numerous copepods. The invertebrate community in the tidal channel of tank 5 was composed of very small herbivores, the largest of which is the snail Littoridinops tenuipes. Occasionally, more freshwater snails occurred there as well (physids and planorbids). The dominant predatory fish in this system was the mangrove rivulus Rivulus marmoratus, whose diet consisted of algae and detritus, copepods, ostracods, and the tanaid Leptochelia savignyi. The oligohaline marsh (No. 6) was a transition zone from the preceding estuarine sections to the adjacent freshwater stream and pond. This system had four fern species: two leather ferns (Achrostichum spp.) and the more transient floating ferns Azolla caroliniana (mosquito fern) and Salvinia rotundifolia (water velvet). Typha domingensis was an important element of this system in the early years and has slowly reduced in standing crop. This was probably a result of the stresses of high soil salinity and the lack of large-scale seasonal flushing, accompanied by insect predation. T. domingensis remained dominant in the freshwater system, a short distance away (see Chapter 23). Numerous monocots were abundant in the understory of tank 6, including Cladium jamaicensis (saw grass), Fimbristylis spathacea (cone grass), and Eleocharis robbinsii (spike rush). The dicot population was dominated by three large individuals; two relatively large trees of Conocarpus (buttonwood), a white mangrove, and a large Myrica cerifera (wax myrtle). Below the water line the primary structural elements were macrophyte stalks, mostly Cladium jamaicensis, and the detritus that these plants release. The dominant algal primary producer was the green algal filament Rhizoclonium riparium, attached as periphyton to the macrophyte stalks and the floating ferns. The mean surface salinity of the tank 6 system was less than 1 ppt. However, the channel was about 50 cm deep and bottom salinities were typically 9–10 ppt. The macroinvertebrate community is depauperate as in the wild analog, some snails more common to freshwater marshes (hydrobiids, planorbellids, physids) occurred periodically. The primary fish predators were Rivulus marmoratus and the least killi Heterandria formosa. Both species were likely consuming small bits of algae and detritus, as well as resident copepods and ostracods. As we mentioned above, the microinvertebrate and protozoan fauna, especially endemic rotifers, were diverse and abundant.

Biotic Variation of the Everglades Mesocosm Over Time The Everglades system was sampled for most of its species elements shortly after its completion in 1987.

Depending on the group, it was periodically examined for species composition over the intervening years, with a general survey again in 1994/1995. There were a few minor additions of species populations during the first few years. However, for 4 years prior to the 1995 survey there were no biotic additions to the system. Tables 22.6–22.9 depict species changes over the life of the system and we discuss them below. In 1995, the shells on the intertidal beach in the Gulf shore tank were covered with a fine mat of calcifying cyanobacteria. This community (and the intertidal tank walls) while moderately productive had much of its biomass tied up in the second trophic layer of grazing snails. The result was a trophic structure akin to many Caribbean rocky intertidal shorelines and corresponding to the worldwide, upper intertidal black zone. This community was not selected or emplaced on construction, but rather arose de nova: a response of the available pool of organisms to a tropical, intertidal environment. The calcification occurring here, as well as on the intertidal walls, the uppermost mangrove pneumatophores in the estuary, and around the subaerial rim of the algal scrubbers, was derived from a strongly elevated pH, resulting from photosynthesis in an environment of tidally limiting water volumes. In the Ten Thousand Islands region of southwest Florida, the intertidal worm reefs formed by colonies of vermetid molluscs are largely subfossil structures. Nevertheless, the wild worm reef structure hosts an extensive community of algae, filter feeders, and predators. In the 1989 census, 19 species of macroalgae (not including diatoms) were recorded from the Gulf shore, many from the worm reef. In the 1994–1995 census, nearly 50% more have been tallied. This does not imply undocumented introductions, but rather that many macroalgae can exist either as spores or buried basal filaments, not likely to be recognized in a standard survey. In the system as a whole, a large part of the substrate supporting the algal communities we discuss was not present or habitable at the time of the original construction and survey. Most algal individuals, certainly all of those treated in this study, have limited life spans, a year or two at most. Since all algae that we discuss in this study must reproduce adequately to maintain populations in the face of grazing and varying physical conditions, these species have been through many generations since installation. The patterns of community structure that we see here have developed with time in the physical, chemical, and biotic framework of this model. In the early years, the seagrass community of the Everglades mesocosm had a history of seasonal biomass variation. This pattern was induced through artificial winter shading due to the presence of large refugia against the south wall of the greenhouse. The

431

A Florida Estuary in Mesocosm TABLE 22.6

Change of Dominant Macroalgae from 1989 to 1994 in the Florida Everglades Mesocosma

1989

Rhodophyta

Chlorophyta

Gulf shore, unit 1 (19 species) (29 species) Goniotrichum alsidii Erythrotrichea carnea Peyssonnelia sp. Gracilaria sp Gigartina sp. Hypnea musciformis Callithmnion cordatum Callithamnion halliae Callithmnion uraguayense Ceramium nitens Centroceras clavulatum Centroceras clavulatum Spyridia filamentosa Polysiphonia subtillissima Pterosiphonia pennata Murreyella periclados Heterosiphonia gibbesii Acanthophora muscoides Acanthophora spicifera

Enteromorpha prolifera Enteromorpha intestinalis Ulva lactuca Monostroma oxyspermum

Bryopsis ramulosa

Bryopsis hypnoides Caulerpa crassifolia

Phaeophyta

Ectocarpus confervoides

Cyanobacteria Spirulina subsalsa Schizothrix sp. Calothrix crustacea

a

1994

Enteromorpha ramulosa

1989

1994

Lower estuary, units 2, 3, 4 (16 species) (14 species) Rhodophyta Peyssonnelia sp. Ceramiun nitens Spyridia filamentosa Caloglossa leprieurii Caloglossa leprieurii Polysiphonia gorgoniae Polysiphonia foetidissima Murryella sp. Murreyella periclados Bostrychia sp. Bostrychia montagnei Chlorophyta Enteromorpha prolifera Chaetomorpha sp. Chaetomorpha minima Chaetomorphora nodosa Chidophora sp. Cladophora repens Rhizoclonium hookeri Derbesia vaucherieformis Bryopsis ramulosa Caulerpa verticillata Caulerpa fastigiata Cyanobacteria Anacystis sp. Anacystis marina Schizothrix mexicana Oscillatoria submembranacea Oscillatoria submembrnacea Scytonema sp. Entophysalis conferva Calothrix crustacea

Ulva lactuca Chaetomorpha gracilis Cladophora crispula Cladophora howeii Bryopsis plumosa Derbesia marina Derbesia vaucheriaformis

Chlorophyta

Caulerpa fastigiata Caulerpa verticillata Caulerpa sertularioides Giffordia mitchellae Sphacelaria furcigera Chroococcus minutus Chroococcus turgidus Oscillatoria submembranacea

Chlorophyta

Calothrix crustacea Anabaina oscillarioides

Charophyta

Upper estuary unit 5 (2 species) (4 species) Enteromorpha prolifera Chaetomorpha sp. Chaetomorpha gracilis Chaetomorpha minima Cladophora repens Boodleopsis pusilla Oligohaline, unit 6 (3 species) (4 species) Chaetomorpha gracilis Chaetomorpha minima Cladophora repens Rhizoclonium riparium Oedogonium sp. Spirogyra sp. Chara sp.

From Adey et al. (1996). Reprinted with permission from Elsevier Science.

shading structures were removed in 1993 and the seasonal variation in seagrass biomass was greatly reduced. Nevertheless, both in the wild and in the mesocosm, considerable seasonal variation in the abundance of seagrass epiphytes is obvious as mentioned above. The communities of this mesocosm were dynamic and self-organized in response to cyclic as well as long-term environmental factors. Much of the model’s invertebrate diversity resided in the seagrass bed. As in the wild (Zieman, 1982), this

community housed a greater abundance and diversity of amphipods and isopods than any other invertebrates. Still, as might be expected based on proportional area alone, the system differed from wild turtle grass beds in Florida Bay by the absence of many species (Tabb and Manning, 1961; Turney and Perkins, 1972). The Florida grass shrimp (Palaemon floridana) and the turtle grass sea slug (Elysia catula) were stocked and reproduced in the early years, but were not present in 1995. They depend on the turtle grass community

432

22. Estuaries

TABLE 22.7 Change of Primary, Established Macroinvertebrate Species, with Time in the Florida Everglades Mesocosma Species

1987

1988

1989

1992

1995

x x x

x x x

x x x

M A R

x x x

x x x

x xnd

A A

xnd

M

x xnd

M

xnd

A

xnd x xnd x x x x xnd x x x xnd x x

U A A

Tank 1: Gulf shores Porifera Haliclona permollis Haliclona loosanoffi Chondrilla nucula Coelenterata Aiptasia pallida Bundosoma cavernata Condylactis gigantea Viatrix globulifera Bryozoa Alcyonidium verilli Bugula neritina Sipunculida Phascolion strombi Mollusca Acteocina canaliculata Cerithium lutosum Codakia orbiculata Crassostrea virginica Crepidula fornicata Crepidula plana Elysia catula Ischonochiton papillosus Littorina angulifera Nassarium vibex Petaloconchus varians Petaloconchus sp. Pisania cancellaria Seila adamsi Strombus alatus Annelida Arenicola cristata Aricidea fragilis Cirriformia filigera Eunica pennata Eupomatus dianthus Eurythoe complanata Filogranna implexa Hesione sp.? Hypiscomus elegans Marphysa belli Melinna maculata Nephtys bucera Nereis succinea Ninoe nigripes Onuphis ermita oculata Onuphis magna Platynereis dumerilii Sabella micropthalma Sabella melanostigma Spirobus sp. Syllis sp. Arthropoda Alpheus armatus Ampithoe sp. Aratus pisoni Balanus amphitrite

x

x x

x

x

?

x

?

x

x x x x

x

x x

x x x

x

x x x

x x x

x

x

x

x x

x x

x x

x

x x

x x

x

x x

x

x x

x

x x

x

x

x

x

x x

x x

M

M

xnd xnd xnd xnd

U M M R

x xnd x

A U

xnd xnd xnd x xnd xnd x x x x xnd xnd

R M A

x xnd x x

M U

A A A R

A

(Continued)

433

A Florida Estuary in Mesocosm TABLE 22.7 Species Balanus eburneus Batea catherinenis Callinectes marginatus Callinectes sapidus Caprella equilibra Corophium sp. Cypridina sp. Erichsonella attenuata Erichsonella filigormis Gammarus sp. Ligia exotica Menippe mercenaria Oniscus asellus Pagurus longicarpus Palaemon floridana Panopeus herbstii Panopeus herbstii Paracerceis caudata Penaeus duorarum Petrolisthes armatus Petrolisthes politus Porcellana sayana Stenocianops furcata Tanais cavolini Cyclopoid copepods 1-3 spp. Haprpacticoid copepod spp. Echinodermata Asterias forbesii Ophiactis sp. Ophioderma brevispina Chordata Amaroucium stellatrim Botryllus planus Ecteinascidia sp. Styella partitia

(Continued)

1987

1988

1989

1992

x

x x x x x x

x x x x x x

x x

x

x x x

x

x x x x x

x x x x x x x x x x

x x xnd xnd xnd x x x x x x x x x x x x x x xnd x xnd

x x x x x

x x x x x

x x

x

x

x

x

x

x xnd x

x x x x

x x x x

1995

A A M M A R

R A A

A A A

R

Tanks 2, 3, 4: Lower estuary Porifera Haliclona loosanoffi Haliclona permollis Lissodendoryx isodictyalis Haliclona loosanoffi Coelenterata Hypolytus sp.? Mollusca Assiminea succinea Cerithidea scalariformis Codakia orbiculata Crassostrea virginica Crepidula plana Detracia bullaoides Geukensia demissus Ischadium recurous Littorina angulifera Melampus bidentatus Melampus coeffeus Scissurella cingulata Truncatella pulchella

xnd xnd x

x x

x x

x xnd

x

x

x x

x x

x x

x x

x x x

x x x

x

x

x

x

R R

x x xnd x x xnd x x x x xnd xnd

A

M

U

R

M A (Continued)

434

22. Estuaries TABLE 22.7 Species

Annelida Capitella sp. Cirriformia filigera Eupomatatus dianthus Eurythoe complanata Hesione sp.? Hydroides dianthus Melinna maculata Spirobus 2 sp. Arthropoda Ampithoe sp. Aratus pisonii Balanus amphitrite Balanus eburneus Caprella equilibra Corophium sp. Cypridina sp. Eriphia gonagra Eurypanopeus depressus Eurytium limosum Leptochelia savignyi Leptodium floridanus Ligia exotica Megalobrachium poiyi Menippe mercenaria Panopeus herbstii Paracerceis caudata Petrolisthes armatus Porcelanna sayana Rhithropanopeus harrisii Sesarma cinerea Sesarma curacaoense Sphaeroma terebrans Talorchestia longicornia Tanais cavolini Uca pugilator Uca pugnax rapax Cyclopoid copepods 2 spp. Harpacticoid copepod sp. Gammarid amphipod sp. Ostracods (2⫹ spp.)

1987

x

x x x

(Continued)

1988

x x x

x x

x

1989

x x x

x x x x x

x

x

x

x x

x x x x x x

x x x x x x x

x

x x

x x

x

x x x

x x x x

x x x x x

x x x x x

x x

1992

1995

xnd xnd x x x xnd xnd xnd

M A

x x x x x xnd xnd x xnd x x x x

A R

x x x x x xnd x x x x xnd x x x x xnd

M A A

A A R M

R A

R

A

A A A

Tank 5: Salt marsh Mollusca Detracia bullaoides Littoridinops tenuipes Melampus bidentatus Melampus coffeus Physid snail Planorbid snail Truncatella pulchella Arthropoda Leptochelia savignyi Ligia exotica Talorchestia longicornis Uca mordax Cyclopoid copepod spp. Ostracod sp.

x x

x

x x

x x x

xnd xnd x x x x xnd

U M R

x x x x xnd x

A

x x x x x

A A

x

x

M

x x x x

M

Tank 6: Oligohaline marsh Coelenterata Hydra sp.

x

(Continued)

435

A Florida Estuary in Mesocosm TABLE 22.7 Species Mollusca Physa spp. Pseudosuccinea columnella Arthropoda Cypridopsis vidua Chirononomid larvae Cyclopoid copepod spp. Ostracod sp.

(Continued)

1987

1988

1989

1992

x x x

x x

x

x x x x x x

x x x

x x x xnd

1995

M A A

a Smaller invertebrate phyla and insects were not tallied. Considering the number of species that appear in abundance in later years but not in early or intermediate years, variations in intensity of collecting were clearly a factor that will have to be considered in future analysis. Modified after Adey et al. (1996) from data collected by C. Luckett. x: present; xnd: present, not documented; A: abundant; M: moderate; U: uncommon; R: rare. Reprinted with permission from Elsevier Science.

TABLE 22.8 Species Tank 1 Acanthurus coeruleus Bathygobius soporator Cyprinodon variegatus Eucinostomus argenteus Eucinostomus gula Floridichthys carpio Fundulus confluentus Fundulus similis Fundulus grandis Gambusia affinis Haemulon macrostomum Haemulon plumieri Hypsoblennius hentzi Lagodon rhomboides Mugil cephalus Opsanus beta Poecilia latipinna Serraniculus pumilio Trachinotus carolinus Tank 2 Cyprinodon variegatus Eucinostomus gula Floridichthys carpio Fundulus confluentus Fundulus grandis Fundulus similis Gambusia affinis Hypsoblennius hentzi Lagodon rhomboides Poecilia latipinna Tank 3 Adinia xenica Cyprinodon variegatus Floridchthys carpis Fundulus confluentus

Populations of Established Fish Species with Time in the Florida Everglades Mesocosm 1987

1988

1989

1992

x x x x x x

x x x x x x

x x x x x x

x x x x x

x x x x x x x x x x

x x x x x x x x x x

x x x x x x x x x xnd x x x x

x x x x

x x x x x x x x

x x x

x x x x

x x x x x x x x x

x x x x

x x

1995

No. individuals in 1995

No. of adults in 1995

Reproducing

U

2

2

No

A M

⫹50 ⫹20

⫹20 ⫹8

Yes Yes

U

⫹8

8

Possible

R

1

1

No

R

3

3

No

R U

1 ⫹10

1 ⫹3

No No

⫹25 1

Yes No

⫹5 ⫹5 ⫹5

Yes Yes Yes

⫹15

Yes

(No. and status in entire estuary) x A ⫹55 x R 1 x x U ⫹10 x U ⫹10 x U ⫹10 x x x x A ⫹35

x x

A

x

U (Continued)

436

22. Estuaries TABLE 22.8 Species

Fundulus grandisd Fundulus similis Gambusia affinis Poecilia latipinna Tank 4 Adinia xenica Cyprinodon variegatus Floridichthys carpio Fundulus confluentus Fundulus grandis Fundulus similis Gambusia affinis Poecilla latipinna Tank 5 Adinia xenica Cyprinodon variegatus Floridichthys carpio Fundulus confluentus Fundulus grandis Gambusia affinis Poecilia latipinna Rivulus marmoratus Tank 6 Gambusia affinis Heterandria formosa Rivulus marmoratus

(Continued)

1987

1988

1989

1992

1995

x x x x

x x x x

x x x x

x

U U

x x

A

x x x

x x x x

x x x x

x x

M

x x x

x x x

x x x

x x x

x x x

x x x x

x x x x

x x

x x

x x

x x

x x

x

x

x

for cover and food production. With the recent greater seasonal stability of the seagrass bed, these invertebrates, and perhaps many others, would have had high probabilities of being reestablished had they been reintroduced. This is an example of bottom-up control of stable population and community structure. Until the plant community can be established and stabilized relative to the physical environment, the complex consumer communities of the wild occur in a more limited state in the model. Some keystone predator invertebrates in the wild analog were introduced into the mesocosm as individuals, or in some cases as very small populations. They mostly died of old age, or remain as only one or a few old adults. A small level of introduction was requisite for these species as they require a large foraging territory, and it was assumed that introduction was necessary to provide an element of top-down control. The banded tulip (Fasciolaria tulipa), two whelk species (Busycon spp.), the Florida fighting conch (Strombus alatus), several species of larger crabs (e.g. the stone crab Menippe mercenaria), and starfish become greatly

x

No. individuals in 1995

No. of adults in 1995

Reproducing

10

Yes

10

Yes

U U U A

M R R

x x

U A

A M

reduced in time or disappeared in just this way. This is why, in part, after several years, the mesocosm is rather different today, in terms of overall diversity, than it was in its initial years. As the largest invertebrates, purposely stocked at low populations, died off, some species that were able to reproduce successfully faced less competition and predation and eventually formed more stable high-density populations; they have selforganized to a similar environment of much smaller area. When comparing fish population of the Gulf shores system to its natural counterpart, the most obvious difference over time is reduction in species diversity. Zieman (1982) and Schomer and Drew (1982) refer to three categories of fishes that occupy bay areas: permanent residents, seasonal residents, and occasional migrants. During the initial stocking, an attempt was made to represent all three categories. Over time, however, the system self-organized into the existing community. This community is typical of a South Florida bay area; however, it is seasonally unchanging, with regard to fish, due to the lack of migration potential.

437

A Florida Estuary in Mesocosm TABLE 22.9 Abundance of Established Higher Plant Species with Time in the Florida Everglades Mesocosma

TABLE 22.9

(Continued)

Species name (common name) Species name (common name)

1987

Tank 1: Gulf of Mexico, beach ridge Agave sp. (agava) U Alternanthera maritima (alligator weed) M Bidens pilosa (Spanish needles) M Catharanthus roseus (Madagascar periwinkle) M Chamaesyce mesembryanthemifolia (spurge) M Chloris glauca (finger grass) A Chloris petraea (finger grass) M Coccoloba uvifera (sea grape) U Cyperus odoratus (umbrella plant) U Dalbergia ecastophyllum 1 (coin wine) R Halodule wrightii (Cuban shoal grass) U Hymenocallis crassifolia (spider lily) M Impomoea alba (moonflower) U Impomoea pescaprae (beach morning glory) M Opuntia compressa (prickly pear) M Physalis angustifolia (ground cherry) M Poinsettia heterophylla (painted leaf) M Poinsettia pinetorum (painted leaf) U Rhizophora mangle (red mangrove) R Sesuvium portulacastrum (sea purslane) A Spartina patens (saltmeadow cordgrass) U Sporobolus virginicus (costal dropseed) U Suriana maritima (bay cedar) R Syringodium filiformis (manatee grass) U Thalassia testudinum (turtle grass) U Thespia populnea (seaside mahjoe) U Uniola paniculata (sea oats) U

1991

U U M U U M U R U U M M U M M U U U U A U U R U M U U

U 0 0 0 0 0 0 0 0 U A U 0 0 U 0 0 0 U A U A R U A R 0

Tanks 2, 3, 4: Red and black mangrove zones Avicennia germinans (black mangrove) A A Batis maritima (saltwort) M U Borrichia frutescens (sea daisy) M M Distichlis spicata (alkali grass) A M Laguncularia racemosa (white mangrove) M M Limonium nashii (marsh rosemary) M M Lycium carolinianum (christmas berry) U U Philoxerus vermicularis (silverhead) M U Rhizophora mangle (red mangrove) A A Salicornia perennis (glasswort) M U Sesuvium portulacastrum (sea purslane) A A

A 0 M A M M 0 0 A 0 A

Tank 5: Salt marsh, white mangrove zone Achrostichum aureaum (leather fern) U Achrostichum danaeifolium (inland leather fern) 0 Avicennia germinans (black mangrove) U Batis maritima (saltwort) M Conocarpus erectus (buttonwood) R Distichlis spicata (alkali grass) A Fimbristylis castanea (cone grass) M Juncus roemerianus (black needle rush) 0 Laguncularia racemosa (white mangrove) U Lycium carolinianum (Christmas berry) U Philoxerus vermicularis (silverhead) A Pluchea camphorata (stinkweed) R Rhizophora mangle (red mangrove) U Salicornia perennis (glasswort) A

M U U R ? R R U A M M 0 M 0

M 0 U U R U U U M U A R U M

1987

1991

1995

Sesuvium portulacastrum (sea purslane) Spartina spartinae (gulf cordgrass) Triglochin striata (arrow grass)

A A 0

A U A

U R A

Tank 6: Olgohaline marsh Achrostichum aureum (leather fern) Achrostichum danaeifolium (inland leather fern) Ampelopsis arborea (pepper vine) Azolla caroliniana (mosquito fern) Bacopa monnieri (water hyssop) Boehmeria cylindrica (false nettle) Borrichia frutescens (sea daisy) Centella asiatica (centella) Cladium jamaicensis (sawgrass) Conocarpus erectus (buttonwood) Crinum americanum (swamp lily) Distichlis spicata (alkali grass) Eclipta alba (eclipta) Eleocharis robbinsii (spikerush) Fimbristylis spathaceae (dwarf cone grass) Ipomoea sagittata (marsh creeper) Juncus effusus (soft rush) Laguncularia racemosa (white mangrove) Mikania scandens (climbing hemp weed) Myrica cerifera (wax myrtle)

R R U 0 A 0 A M A R M M A A M U A R M R

R U U M M M U M A R M U M A M U A R U R

R U 0 M 0 M 0 0 A M M 0 0 A M R A U 0 U

1995

(Continued)

a A: abundant; M: moderately abundant; U: uncommon; R: rare; 0: not found. Modified after Adey et al. (1996) from data collected by M. Finn.

Among the fish populations in the Gulf shore system, there was a striking correlation between long-term reproductive failure and the possession of planktonic larvae. Although every effort was made to install pumps (piston pumps, Archimedes’ screws, disc-flow pumps) that would not damage swimming larvae, there have been periods in which large impellor pumps were in service on the Gulf shore. For a number of years, the internal circulators within the lower estuary were also of the impellor type. The problems, however, may go far beyond direct mechanical destruction. Successful larvae of the common lower estuarine fish may well go through a major part of their development outside the estuary, or offshore, where they cannot be preyed upon by the killifish (the very fish that will become their prey as adults). Lagodon rhomboides (pinfish), for example, was successfully reproductive in the early years of system operation when the primary pump was an Archimedes’ screw. The disc-flow pump, used in later years, would probably have allowed success in additional fish species, if they had been introduced. In the vascular-plant-dominated environments of the mesocosm, nearly all the plants that are important contributors to the physical structures and the food webs of

438

22. Estuaries

the wild ecosystem flourished. In the Gulf shore system the seagrasses, always very difficult to transplant and usually successful for only a few individuals at best, grew into a dense meadow. In the estuary proper, the mangroves, started mostly with small saplings and a few seedlings, established a mature canopy, sexually propagated themselves, and contributed extensive structure and leaf litter as a food source. The greatest problem in the red mangrove community was the proliferation, after several years of operation, of pest insects due to the lack of extreme weather conditions in the greenhouse (and the proximity of horticultural greenhouses). Winter chilling to 5–10°C, a typical winter event in the wild Everglades, became an established feature of operation in later years, and as a result, we had no further epidemic problems with insect pests. The black mangrove forest, once established, has grown vigorously. This mangrove actively excretes salt through glands on its leaves, which kept this species virtually free of insect pests even during the peak of insect predation on the red and white mangroves. Although there is good seasonal flowering in this species, as in the white mangrove, only a few viable propagules have fully developed, possibly due to a paucity of insect pollinators. In wild mangrove communities, the well-developed prop roots and pneumatophores also provide an ideal environment for a select group of algal genera that are adapted to this rather specialized pantropic environment (the Bostnjchia–Caloglossa association). If shading is not extreme, the mangrove root algal community can be more productive than the mangroves themselves (Burkholder and Almodovar, 1973). In the mesocosm mangrove root community, the keystone species Bostrychia montagnei and Caulerpa verticillata dominate as they often do in the wild. Caloglossa leprieurii is present, though not abundant. Since this community was established in the mesocosm as rather small saplings and seedlings, the Bostrychia–Caloglossn association had developed with time from exceedingly small “seed” areas in remarkable conformity with its pantropic occurrence. Several key invertebrate species occurred in low numbers or were missing in the subaerial environment below the mangroves by 1995: these included the coffee snail Melampus coffeus; the ladder horn cerith Cerithidea scalariformis; the marsh crabs Searma spp.; the fiddler crabs Uca spp.; and the southern periwinkle Littorina anguilifera. Initially the mangrove canopy was relatively thin and the forest floor bare except for the mangrove pneumatophores. Resulting low relative humidity and high light conditions exposed these animals to high desiccation pressure. In later years, there was a thicker canopy and an accumulation of moist

decomposing leaves on the forest floor. This provided an improved environment for land-dwelling snails, and additions of the coffee snail and southern periwinkle in the year after the survey was accomplished proved successful, at least in the short term. The later find of a few Detracia bullaoides and Melampus bidentatus under the leaf litter in tank 5 seems to confirm this view. Four now extinct crabs, Uca spp. and Sesarma spp., might also benefit from the more mature mangrove environment, if they were to be introduced. Perhaps the most obvious difference between the mesocosm and wild prop roots is the absence of barnacles (which initially reproduced, as seen in places on the tank walls) and some lesser constituents of the prop root community (sponges, barnacles, tunicates, oysters) (Odum et al., 1982; Schomer and Drew, 1982). On the other hand, some filter feeders have been extremely successful in the mesocosm (e.g. the bivalve Codakia). Some of the key missing elements might have established in the later years when the system was more stable and the disc-flow pump provided a nontraumatic planktonic environment. Unfiltered exchange sea water (⬍0.1%/day) for the mesocosm had been brought in by truck from the Maryland shore and stored for use over about 6-month intervals. Without the capability to closely monitor all inorganic elements, particularly adjunct salts and trace elements, small seawater exchanges have been our only means of adjusting potential salt drift. Several species of invertebrates may have colonized the system as larvae carried in the water. Among these are some polychaetes (Sabella spp., Spirorbus spp., and Hydroides sp.), the tanaids (Tanais cavolini and Leptochelia savignyi), the isopods (Erichsonella spp.), and several other microcrustaceans and protists. The introduction of these species is difficult to demonstrate as there is some similarity between the fauna of the mid-Atlantic states and South Florida. It is interesting to note that none of the potentially “exotic” species seem to be explosive and therefore destructive. The most abundant fish species in the estuary was the sheepshead minnow, accounting for approximately 40% of the total individuals. As the estuary was composed of five interconnected units, the fish were free to migrate between tanks. However, despite the abundance of sheepshead minnows, the dominant species in each tank varied. Based on the literature, the estuary fish population was quite similar to a South Florida estuary. Odum et al. (1982) indicate that there was a progression of species throughout an estuary based on salinity tolerances, substrate preferences, and relative importance of mangrove detritus to the food web. They report that the black mangrove forest area is dominated by cyprinodonts and poeciliids, while the estuarine bay fringing

439

Estuarine Restoration

community is dominated by large numbers of a few species such as the silver jenny and the pinfish. The skewed nature of the fish populations of the Gulf shores tank 1, as we have noted, was probably related to the planktonic nature of many of the larval stages combined with a lack of a suitable “offshore” refugium. In the upper reaches of the estuary, tank 5 was dominated by the mangrove rivulus, while tank 6 was dominated by the least killi. The mangrove rivulus was a permanent resident of both tanks 5 and 6, while the least killi was a permanent resident only of tank 6 in the estuary. While other species could be found in these systems (tank 5 in particular), their existence was only temporary as they were migrants with the tide. This was a more extended case of the increasing specialization with salinity gradient passing up the estuary. As in the wild analog, the oligohaline unit (6) was a very difficult zone of changing and extreme salinities and is relatively depauperate for macroinvertebrates. Only ostracods were well represented. On the other hand, as we described above, this very small system was quite rich in smaller acoelomate and pseudocoelomate invertebrates (nematodes, rotifers, gastrotrichs, etc.) and protists. This could have represented a significant survival capability of freshwater species of protists and acoelous invertebrates in the low and sometimes fluctuating salinities of tank 6. However, of the 36 species of protists and acoelous invertebrates tabulated for the adjacent freshwater system, only 7 species also occurred in the oligohaline unit (6). Removing those species from the list as merely “flowovers” from freshwater still leaves 30 species, nearly as many as the freshwater total and almost four times the number in unit 5. Perhaps the dearth of macroinvertebrate species that browse or graze on protozoans and micrometazoans in unit 6 led to this rather striking development of a microcommunity in an otherwise quite depauperate aquatic system. The diatoms of the aufwuchs community in the estuary were reduced in number and diversity compared to the Gulf shore. This was clearly related to the change to intense shading and the basing of food webs in the aquatic communities on mangrove detritus. However, in general, the protozoa were arrayed abundantly throughout the system by species limited in their salinity ranges. This demonstrated that there was a large range of feeding niches based on bacteria and diatom size, shape, and abundance; cyanobacteria type; and probably also on size, shape, and texture of settled and trapped particles bearing bacteria. The spatial limitations that apply to many larger organisms had little effect at this scale. One of the most interesting features of selforganization in the Everglades mesocosm had been the general lack of epidemic or explosive growths of single species, which had been so characteristic of exotic

species in the Everglades itself. The insect pests that ravaged the red mangrove for 2 years in midlife are an example of this process in the model. However, this problem was apparently contained by increasing the rigor of the internal climate, a step that appeared to have been successful, at least in part. The general lack of examples of population explosion reflects the complexity and stability of the mesocosm, with population control occurring through webs of ecological interactions and appropriate environmental management.

NUTRIENT DYNAMICS IN ESTUARINE MODELS A summary of the distribution of nitrogen (nitrite plus nitrate) concentrations in both the Chesapeake and Everglades estuarine systems is given in Figure 22.14. Both systems show very similar patterns of nutrient distribution in spite of their great differences, climatically and biotically. Through the middle salinities of both estuaries, dissolved nitrogen was 3–10 µM (0.04–0.14 ppm). In the Everglades system there was a significant summer–winter difference of about 3–4 µM due to high productivities and standing crops in summer. This seasonal pattern probably also applied to the Chesapeake model, but our long-term efforts to examine the effects of reducing nitrogen input on concentrations through the middle of the estuary have masked any seasonal differences. These features would be normal for large, wild, and undisturbed estuaries (Day et al., 1989). The pattern matches most wild systems where both ocean and mid-estuary itself are sinking nitrogen and producing a concave downward distribution rather than a straight line from river input to ocean. Also, it is clear that the scrubbers at the high-salinity end are “pulling” nutrients through the system and acting in the “sink” role that they were meant to play. Unfortunately, nitrogen levels are lower in the highest salinity tanks of the Chesapeake system (⬍1 µM) than would be desired in a truly accurate model. This problem could be circumvented without losing the required amount of sinking by making the high-salinity tank somewhat larger, as has been done in the Everglades model with the effect seen in Figure 22.14.

ESTUARINE RESTORATION Many human factors enter into estuarine degradation. Since estuaries often support ports and major cities, direct destruction of shorelines and wetlands is often an important factor. Rarely can this be turned around, and unless the estuary is small in relation to the ports, this in itself is not necessary for large-scale restoration. In other

440

22. Estuaries

FIGURE 22.14 Summary of principal nutrient patterns in the Smithsonian estuarine mesocosms (see text).

cases where commercial use is terminated, and primary, degrading elements removed (e.g. toxic sediments, sewer outfalls), some natural replacement of the original biota can occur naturally. Hawkins et al. (2002) document such recovery. Direct industrial pollution is certainly a major problem, but this tends to be point source, and in many cases has already been remediated, though toxic sediments often remain. Declining or dead fisheries, mostly due to over-fishing, are a widely recognized problem, and we discuss both the toxic recovery and the fishing issues in Chapter 25. These provide the more traditional problems of estuarine restoration and are also treated in some detail by Hawkins et al. (2002) and Livingston (2006). However, in the later decades of the 20th century, a more deeply rooted and apparently more intractable problem has been introduced: namely landscape scale, nonpoint, river eutrophication and introduction of toxic and other synthetic organic, ecosystem-disruption chemicals (e.g. hormones). Many of the synthetic compounds have very long half lives, and move into estuarine, coastal, and ocean waters where they can affect ecosystems globally. The eutrophication problem is so serious that the Gulf of Mexico, off the Mississippi River, now has a very large and growing dead or hypoxic zone (U.S.G.S., 2005). Also, after 25 years of concentrated

effort by combined adjacent states, the EPA, and several private environmental organizations, spending enormous sums (reportedly $6B by 2005), one of the largest estuaries in the world, the Chesapeake Bay, also has a large and growing dead zone (Livingston, 2006; Blankenship, 2005). These nutrients, primarily nitrogen and phosphorus are derived from sewage plants and farms throughout the watersheds, in effect from the population at large. Some researchers propose to solve this problem using filter-feeder rehabilitation (i.e. top-down methods) using typically oysters or mussels (e.g. Hawkins et al., 2002). However, this is somewhat of a chicken/egg problem and sometimes involves the introduction of alien species; often the native species cannot withstand existing environment conditions, which have enhanced significant disease problems. We propose to solve the eutrophication problem of the estuaries by using bottom-up methods and cleaning up the rivers that introduce most of the nutrients and toxics. This can be done, as described in Chapter 25, using large-scale algal turf scrubber systems. These systems can remove nutrients in algal biomass with greater cost efficiency than any other technique currently available. They are also capable of removing or breaking down many toxic chemical elements and compounds and sequestering

References

atmospheric carbon while introducing oxygen and producing an energy by-product. Eutrophication is not the only problem of most degraded estuaries, as we have noted. However, in most cases, it is the most serious, and the required first solution to overall restoration.

References Adey, W., Finn, M., Kangas, P., Lange, L., Luckett, C., and Spoon, D. (1996) A Florida Everglades mesocosm – model veracity after four years of self organization. Ecol. Eng. 6: 171–224. Audubon Society (1983) Field Guide to North American Fishes, Whales and Dolphins. Knopf, New York. Blankenship, K. (2005) Bay experiences largest recorded anoxic zone this summer. www.bayjournal.com Britton, J. and Morton, B. (1989) Shore Ecology of the Gulf of Mexico. University of Texas Press, Austin, Texas. Burkholder, P. and Almodovar, L. (1973) Studies on mangrove communities in Puerto Rico. Fla. Sci. 36: 66–74. Davis, S. and Ogden J. (Eds) (1994) Everglades: The Ecosystem and Its Restoration. St. Lucie Press, Delray Beach, Florida. Day, J., Hall, C., Kemp, W., and Yonez-Arancihia, A. (1989) Estuarine Ecology. Wiley, New York. Douglass, M. (1988) The Everglades. Pineapple Press, Sarasota, Florida. Drew, R. and Schomer, N. (1984) An Ecological Characterization of the Caloosahatchee River/Big Cypress Watershed. US Fish and Wildlife Service FWS/DBS-82/58.2 Godfrey, R. and Wooten, J. (1979, 1981) Aquatic and Wetland Plants of the Southeastern United States. Monocotyledons, 1979. Dicotyledons, 1981. University of Georgia Press, Athens, Georgia. Gosner, K. (1978) A Field Guide to the Atlantic Seashore. Peterson Field Guide Series. Houghton Mifflin, Boston, Massachusetts. Hawkins, S., Allen, J., Ross, P., and Genner, M. (2002) Marine and coastal ecosystems. In: Handbook of Ecological Restoration. Vol. 2. Restoration in Practice. M. Perrow and A. Davy (Eds). Cambridge University Press, Cambridge. Humm, H. (1979) The Marine Algae of Virginia. University of Virginia Press, Charlottesville, Virginia. Kangas, P. and Lugo, A. (1990) The distribution of mangroves and saltmarsh in Florida. Trap. Ecol. 31: 32–39. Kaplan, F. (1988) A Field Guide to Southeastern and Caribbean Seashores. Petersen Field Guide Series. Houghton Mifflin, Boston, Massachusetts.

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Lippson, A. (Ed.) (1973) The Chesapeake Bay in Maryland: An Atlas of Natural Resources. Johns Hopkins University Press, Baltimore, Maryland. Lippson, A. and Lippson, R. (1984) Life in the Chesapeake Bay. Johns Hopkins University Press, Baltimore, Maryland. Lippson, A. and Lippson, R. (1997) Life in the Chesapeake Bay, second edition. Johns Hopkins University Press, Baltimore, Maryland. Lippson, A., Haire, M., Holland, A. F., Jacobs, F., Jensen, J., MoranJohnson, R. L., Polgar, T., and Richkus, W. (1979) Environmental Atlas of the Potomac Estuary. Martin Marietta Corp., Environmental Center, Baltimore, Maryland. Livingston, R. (2006) Restoration of aquatic Ecosystems. Taylor and Francis, Boca Raton, Florida. Odum, W., Ivor, C. M., and Smith, T. II (1982) The Ecology of the Mangroves of South Florida: A Community Profile. US Fish and Wildlife Service FWS/OBS-81/24. Odum, W., Smith, T. III, Hoover, J., and Mclvor, C. (1984) The Ecology of Tidal Freshwater Marshes of the United States East Coast: A Community Profile. US Fish and Wildlife Service FWS/OBS-83/17. Osmond, B., Ananyev, G., Berry, J., Langdon, C., Kolber, Z., Gunghai Lin, Monson, R., Nichol, C., Rascher, U., Schurr, U., Smith S., and Yakir, D. (2004) Changing the way we think about global change research: scaling up in experimental ecosystem science. Glob. Change Biol. 10: 393–407. Petersen, J., Kemp, W. M., Bartteson, R., Boyuton, W., Chung-Chi Chen, Cornwell, J., Garnder, R., Hincklel, D., Houde, E., Malone, T., Mowitt, W., Murray, L., Sanford, L., Stevenson, J.C., Sundberg, K., and Suttles, S. (2003) Multiscale experiments in coastal ecology: improving realism and advancing theory. Bioscience 53: 1181–1197. Schomer, N. and Drew, R. (1982) An Ecological Characterization of the Lower Everglades, Florida Bay and the Florida Keys. US Fish and Wildlife Service FWS/DBS.82/58.1. Tabb, D. and Manning, R. (1961) A checklist of the flora and fauna of northern Florida Bay and adjacent brackish waters off Florida mainland collected during the period July 1957 through Sept. 1960. Bull. Marine Sci. II: 552–649. Turney and Perkins (1972) Molluscan Distribution in Florida Bay. Comp. Sed. Lab, University of Miami. U.S.G.S. (2005) Resource Data Base for Gulf of Mexico Research. www.gulfbase.org. Wass, M. (1972) A Check List of the Biota of Lower Chesapeake Bay. Special Science Reprint 65. Virginia Institute of Marine Science Gloucester Point, Virginia. Zieman, J. (1982) The Ecology of the Seagrasses of South Florida: A Community Profile. US Fish and Wildlife Service FWS/OBS-82/25.


C H A P T E R

23 Freshwater Ecosystem Models

The volume of fresh waters on the surface of the Earth is the tiniest fraction of the Earth’s total water. Roughly 97% of Earth’s water resides in the oceans. Of the remainder, over 2.5% is tied up in glacial ice and ground water. While less than 0.5% of the Earth’s water is in the form of lakes and rivers, it represents a tremendous diversity of physical/chemical conditions and a large species diversity. Virtually all humans live and work in the terrestrial environments that contain our fresh waters. We need water to drink, and if that water passing through our bodies were our only connection to our fresh waters, degradation of those environments would be minimal. Unfortunately, as our populations enlarge, streams and lakes are either physically in the way of our residential, urban, industrial, or agricultural growth, or we have felt the need of being protected from flooding and have channelized, dammed, or otherwise severely modified them. Perhaps in many ways more significant, because it extends far beyond the more immediate bounds of human occupation, has been our practice to use waterways as dumps for urban and industrial wastewater; although it may not be perceived that way, because it is a more remote for most people, the loss of nutrients and pesticides from agricultural areas is just as serious a problem for our waterways as urban/industrial effects. Livingston (2006) provides an unvarnished view of the problems that modern societies face in this regard. Our experience with modeling freshwater ecosystems is more limited than that of marine and estuarine systems. Nevertheless, it has been broad enough to suggest that these tools can be just as usefully applied to wild systems restoration. Freshwater aquaria have been widely used in research and education as biological holding systems. As we discuss in the introduction, the

argument that ecological systems are too complex and we do not know enough to build them to function like wild ecosystems is no longer relevant. All ecosystems on Earth have been modified by human activity and freshwater ecosystems rank high on any scale of modification. Therefore, we need to become rational interactors, using the tools of scientific research, on many scales from bench model to whole “wild” ecosystems. For general background reading on the subject of this chapter, the authors suggest the following books: Burgis and Morris (1987), Moss (1988), Pennak (1989), Dodds (2002), and Brusca and Brusca (2003). The earlier chapters in this book provide further background and more in-depth references to freshwater ecology. The Florida Everglades stream and wetland described in the first edition of Dynamic Aquaria operated about 13 years. The long-term history of this system has been described as part of a general survey of the entire Everglades mesocosm (Adey et al., 1996). The estuarine and freshwater portions of this system were described separately in the earlier edition, and since the interests of both modelers and aquarists seem to fall on those same lines of separation, we have kept the two systems separate in this edition.

A FLORIDA EVERGLADES STREAM AND WETLAND In 1987, the Smithsonian’s Marine Systems Laboratory built a 40-foot-long by 9-foot-wide stream and small pond flanked on one side by a series of “woodlands” or hammocks of different hydroperiods and on the other by a wet to dry prairie (Figure 23.1, Color Plates 45 and 47). In 1992, an upper pool of 2500 gallons

443

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23. Freshwater Ecosystem Models

FIGURE 23.1 Freshwater/wetland portion of the Florida Everglades mesocosm. Note that the system was expanded to add an upper pool and several community designations have changed since the publication of the first edition of Dynamic Aquaria. From Adey et al. (1996).

was added to the system to provide an area of welllighted open water because the continued growth of both hammock trees and mangroves had changed the original stream to a deeply shaded environment with few submerged aquatics or algae. The reader is referred to Chapter 22 and to Drew and Schomer (1984) and Duever et al. (1986) for background information on the wild ecosystems that relate to this model. As described in Chapter 22, the tank itself was constructed of cement block and was lined with a nontoxic butyl rubber sealant. The critical bedrock geology of the Everglades in relation to the water table was desired. However, funds were inadequate to transport Florida limestone. To partially overcome this difficulty, an uncoated cement slab and block platform was constructed within the tank at about the level of the seasonal low-water table (Figure 23.2). The “ground water” is turned over about once per day (from downstream to upstream) with a 3 gpm centrifugal pump. The approximate water volumes of this freshwater microcosm segment of the larger estuarine mesocosm are 5000 gallons during the dry season and 6500 gallons in the wet season. As with the estuary that this stream and wet savanna accompany, light was ambient (a greenhouse in Washington, DC), and maximum and minimum temperatures are 10–35°C (air) and 18–29°C (water). Immersion heaters were used in winter to keep stream temperatures above 18ºC. Wet season (June–November) rainfall amounted to 0.3 inch/day; dry season (January–May) rainfall was 0.1 inch/day. Freshwater supply to the stream, in addition to the rainfall, was derived from reverse osmosis treatment of tap water. In 1992, two 1-square meter algal scrubbers were added to the system to maintain pH at levels characteristic of the Everglades environments being modeled (⬎8.00). This Everglades wetlands system was designed with floating and emergent aquatic plants fringing the pond

(Color Plate 44) and with hydroperiods (or watersaturated surface soils) ranging from about 2 to 10 months in the hammocks and prairies (Color Plate 47). The plant and animal species that we tallied in the system, in 1987–1992 and 1995, are listed in Tables 23.1–23.5. Except for fish and a few large invertebrates, the model was stocked over roughly a 6-month period using block transfer methods. The primary trees in the hammock community were purchased from native plant greenhouses in Florida. In the early stages of operation, a few trees and bushes were lost to insects, primarily aphids and red spider mites. Further losses have been greatly reduced by periodically using a strong spray from a garden hose (thereby simulating the occasional heavy wind and rain that characterize the wild). In recent years, we had very few problems from epidemic plant pests, although they were present. Whether the species of the system had developed resistance to the pests, their presence to be considered endemic, or whether our wind/rain management more accurately matched the wild environment is unknown. In any case, we strongly recommend that commercial greenhouses not be the source of terrestrial plant communities for mesocosms because of the pests usually associated with this source. If it is necessary to utilize commercial greenhouse material, quarantine and total elimination of pests is probably desirable, preferably by biological methods. Stream flow in this mesocosm was achieved by recycling with a 50 gpm disc-flow pump. Although this was slower than some streams in southwest Florida, particularly in the wet season or approaching tidal influence, it had the typical sluggish character of many streams in the area. Most crucial in the management of this model is that it is a “balanced” one in most respects. No feed is added, and all deciduous and cropped vegetation is allowed to break down within the system. Water is added directly

A Florida Everglades Stream and Wetland

445

FIGURE 23.2 Florida Everglades stream mesocosm during construction. The double course of cement block defining the stream itself is placed on a mosaic of 4-inch-thick cement slabs that separate “ground water” from surface water.

and by rain to overcome evaporation (about 50 gallons/ day). The ultimate water source used for evaporative makeup is Washington, DC, tap water (which is 2⫺ eutrophic: nitrogen as NO⫺ 2 ⫹ NO3 ⫽ 130–200 µM). However, this input water is treated with a Milli-RO reverse osmosis system. Actual reverse osmosis injec2⫺ tion levels are 5 µM for nitrogen as NO⫺ 2 ⫹ NO3 and 3⫺ 1–3 µM for phosphorus as PO4 . The addition of the algal turf scrubbers (ATS) has elevated pH to levels ⬎8.0 and has stabilized the open water of the stream model at ⬍2 µM for dissolved nitrogen. The stream and its surrounding prairie and hammocks (which continued to increase biomass throughout the entire life of the system) further reduce dissolved nitrogen. Construction of this system was completed in 1987, and from that time until mid-1991, a few additional key species were added and some species, especially predator fish, were repeatedly cropped. From mid-1991 to late 1995, no new additions were made to the system, and it was allowed to “evolve” or self-organize with the populations already present. The following is a status report of that period of self-organization without benefit of species immigration. It is clear that the basic population parameters of this model ecosystem, with its large number of higher plant and especially woody,

swamp species, are very different from those in the estuary, where a large part of the diversity and numbers are made up locally of near monocultures of mangroves, and high diversities of algae and invertebrates. This stream and wetlands community, in the model, was larger than any of the estuarine units. Nevertheless, as we shall discuss, it was clearly too small, in some ways to provide the veracity of many of the systems we have described. The difference is one of scaling, a much larger area of model is required to successfully sustain diverse populations of forest hammocks than is required in any of the estuarine units. In the following, we briefly discuss 8 years of natural history in this model. Properly speaking, the entire period has been one of self-organization of species populations, though a very limited immigration was allowed in the early years, with a human filter. Humans operate as the higher predators at the third or fourth trophic level.

Community and Trophic Structure, 1995 The dominant woody plant species that bordered the pond area at the base of the stream were Typha domingensis (southern cattail), Zizaniopsis milliacea (southern wild rice), Annona glabra (pond apple), Ludwigia octovalvis

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TABLE 23.1 Higher Plant Species in the Florida Everglades Freshwater Stream and Wetland Mesocosma

TABLE 23.1

(Continued)

Species (common name) Species (common name) Acoelorrhaphe wrightii (Everglades palm) Alisma sp. (water plantain) Ampelopsis arborea (pepper vine) Andropogon capillipes (broomsedge) Andropogon glaucopsis (broomsedge) Andropogon rhizomatum (broomsedge) Annona glabra (pond apple) Baccharis glomeruliflora (groundsel tree) Baccharis halimifolia (salt bush) Bacopa monnieri (water hyssop) Billbergia pyramidalis (bromeliad) Bidens pilosa (beggars ticks) Blechnum sp. (hammock fern) Birsera simaruba (gumbo limbo) Canna generlis (Indian shot) Carex lupuliformis (sedge) Cassytha filiformis (love vine) Centella asintica (centella) Chamaesyce hypercifolia (spurge) Chloris glauca (finger grass) Chrysobalanas icaco (cocoplumb) Cladium jamaicensis (sawgrass) Colocassia esculentum (violet-stemmed taro) Cornus foemina (swamp dogwood) Crinum americanum (swamp lilly) Cyperus pseudovegetus (sedge) Eclipta alba (eclipta) Eichhornia crassipes (water hyacinth) Fimbristylis spp. (cone grass) Flavereia floridana (yellowtop) Gratiola sp. (hedge hyssop) Heliconia latispatha (lobster claw) Hieracium sp. (hawkweed) Hydrocotyle verticillata (water pennywort) Hymenocallis palmeri (alligator lilly) Hyptis alata (musky mint) Ilex cassine (dahoon holly) Ipomoea sagittata (marsh creeper) Juncus megacephalus (big head rush) Leersia oryzoides (rich cutgrass) Lemna minor (duckweed) Ludwigia octovalvis (water primrose) Ludwigia repens (red ludwigia) Magnolia virginiana (sweetbay magnolia) Manisuris rugosa (jointgrass) Mikania scandens (climbing hemp weed) Myrica cerifera (wax myrtle) Myrsine guianensis (myrsine) Pandanus veitchii (variegated screw pine) Panicum dichotomum (panic grass) Parthenocissus quinquefolia (woodbine) Peltandra virginica (arrow arum) Persea borbonia (red bay) Pinus elliottii (slash pine) Pistia stratiotes (water lettuce) Polygonium hydropiperoides (smart weed) Pontederia cordata (pickerel weed) Quercus laurifolia (laurek oak)

1987

1991

1995

U U U U U U U M U A U A U U A U U A M U U A U U M U U U U U M U U A U M U M U U A U M R U U R R U A R U U U U U M R

U U U U U M U U U A U A U R A A M M U M U A A U A M A A M U M M M M U U U M M U A R A R M M R R U A R R U U M U U R

U U U O O M U O O O U O U R U O M O O A U A O A A U O O U O O O U O M O U O A A A R O R U O R R U A O R R U O O O R

(Continued)

Quercus virginiana (live oak) Rhizophora mangle (red mangrove) Rhynchospora inundata (beak rush) Riccia fluitans (thallose liverwort) Roystonea elata (royal palm) Rubus cuneifolium (sand blackberry) Rumex sp. (dock) Sabal palmetto (cabbage palm) Sabatia sp. (sabatia) Sagittaria falcata (duck potato) Salvinia rotundifolia (water velvet) Salix caroliniana (coastal plain willow) Serenoa repens (saw palmetto) Setaria verticillata (bristle grass) Smilax laurifolia (laurel leaf briar) Solidago fistulosa (golden rod) Solidago sempervirens (golden rod) Spartina spartinae (prickly cordgrass) Sporobolus virginicus (dropseed) Syzygium cuminii (myrtle) Swietenia mahogoni (mahogany) Taxodium distichum (bald cyprus) Thalia geniculata (arrowroot) Thelypteris kunthi (shield fern) Typha domingensis (southern cattail) Vicia acutifolia (vetch) Wedelia trilobata (creeping ox-eye) Wolffella floridana (mud midget) Yucca gloriosa (yucca) Zizania aquatica (southern wild rice)

1987 1991 R O U U R R U U U M O U U A R U U U A R R M U M A U U A U U

R O M A R R U U R U U U U A R U U U A R R M A A A U A A R U

1995 R R M O R O O U O U A U U A R U U U A R R M M A M O U O R M

a This list only includes species that originally became established in the system (or migrated from the estuary) and were still present even if rare or uncommon after the first few years of operation. For a complete list, see Adey et al. (1996). Of the original list of 87 species considered to have been established, 60 (69%) remained in late 1995. Two new species become established between 1987 and 1995. Abundance codes: (O), no individuals found; (R) rare, one individual; (U) uncommon, 2–4 individuals; (M) moderate, 5–10 individuals; (A) abundant, more than 10 individuals.

(water primrose), Pandanus veitchii (variegated screw pine), Ilex cassine (dahoon holly), Cornus foemina (swamp dogwood), and Chrysobalanas icaco (cocoplumb). The Typha plants were dense, as in the wild, but very large, reaching to the apex of the greenhouse. Every year they produced abundant, characteristic fruiting spikes and abundant seeds. Although the vegetation was dense, since the pond is open to light to the east it received more sunlight than the remainder of the stream. The miniature floating fern Salvinia rotundifolia (water velvet) and flowering plant Lemna minor (duckweed), periodically formed a dense cover on the water surface. Under water, the filamentous green Rhizoclonium crispum occurred as scattered small tufts in a thin bluegreen-dominated periphyton.

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Further upstream, the prairie community consisted of a vegetation strip, 0.7 meters wide and 9 meters long, lying alongside the stream. The east end of the prairie was the lowest and the strip gradually increased in elevation to the west. This grade was installed in an attempt to support an ecotone ranging from wet sawgrassdominated conditions to drier (during the dry season) prairie habitats. In general, the gradient was achieved. However, the dry end did not get as dry as desired. It was too close to the wet end and lateral “capillary” movement of water prevented drying. For this reason, the sawgrass tended to expand into the drier section. At this scale, the slope would have to be greater to support the wet to dry range desired. The invading sawgrass had to be occasionally pruned out of the area, so as not to lose the established plant communities at the dry end. Only one of the indicator species of wild dry prairie genus, Andropogon sp., grew well and a rush, Juncus megacephalus (big head rush), became dominant. Many subsidiary species of monocots and dicots occurred throughout the prairie community. There were three communities originally established along the stream bank opposite the prairie: bald cypress, hardwood, and pine/palm hammocks. These communities maintained their basic integrity throughout the life of the model. The major understory species in the bald cypress hammock were sawgrass and Billbergia pyramidalis (a bromeliad). The subsidiary species were Wedelia trilobata (creeping ox-eye), Panicum dichotomum (panic grass), and the swamp lily Crinum americanum. The cypress trees are deciduous and their old leaves provide litter that extends into the mangrove community. As with most of the trees, they were very much limited by the roof of the greenhouse, though the cypress seem to do particularly well in this very limiting context, and continue to increase in diameter. The hardwood hammock was composed of a selection of trees, including Magnolia virginiana (sweet bay), Persea borbonia (red bay), Quercus laurifolia (laurel oak), Quercus virginiana (live oak), Swietenia mahogoni (mahogany), and Bursera simaruba (gumbo limbo). However, one particularly large inland leather fern had grown up out of the understory between the oaks. This prolific fern reached a height in excess of 2.5 meters and blocking light, already limited in this northlight situation, to the hardwoods. The heights of the trees were limited by the greenhouse ceiling and therefore could not overtop the fern as happens in the wild. The pine and palm hammock contained four palm species with dense vegetation; these included Acoelorrhaphe wrightii (Everglades palm), Roystonea elata (royal palm), Sabal palmetto (cabbage palm), and Serenoa repens (saw palmetto). The pine species Pinus elliottii (slash pine) continued to grow rapidly in diameter throughout the

TABLE 23.2 Algae Present in the Florida Everglades Stream and Wetland Mesocosm 1989 (3 species)

1995 (16 Species)

Rhodophyta Chlorophyta

Audouinella violacea Ulothrix rivularis Cladophora crispata Rhizoclonium crispum Oedogonium sp.

Cyanobacteria

Bulbochaete sp. Spirogyra nitida Spirogyra sp. Vaucheria polysperum Microcoleus paludosus Microcoleus lacustris Oscillatoria rubescens Oscillatoria nigra Oscillatoria limosa Scytonema mirabile Microchaete goeppertiana Calothrix parietina

Microcoleus sp. Oscillatoria sp.

TABLE 23.3 Invertebrates Present in the Florida Everglades Stream and Wetland Mesocosma Species Coelenterata Hydra sp. Mollusca Corbicula manilensis Elliptio jayensis Gyraulus parvus Lampsilis teres Melanoides tuberculata Physa sp. Physella cubensis Physella hendersoni Planorbella duryi Planorbella scalaris Planorbella trivolis intertexa Polygyra uvulifera Pomacea palidosa Popenais buckleyi Pseudosuccinea columnella Terebia granifera Viviparus georgianus Arthropoda Cypridopsis vidua Hyalella azteca Palaemonetes palidosis Procambarus alleni Unidentified chironomid larvae Unidentified cyclopoid copepod Unidentified cyclopoid copepods

1987

1988

1989

x

x

x

A

x x x x x x

x x

R

x x x

x x x

x x x

x x x x x x

x

x x

x

x

x

x x

x x

x

x

x

x

1992 1995

A x M M

x

x x x x x

A A M R A A

a Insects were not identified in 1991 or 1995. See first edition for insects identified in 1989. Abundance codes: (R) rare, 1–10 individuals; (U) uncommon, 10–25 individuals; (M) moderate, 25–200 individuals; (A) abundant, 200 individuals; (x) present.

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TABLE 23.4 Fish Present in the Florida Everglades Stream and Wetland Mesocosma Status, 1995 Species Elassoma evergladei Fundulus chrysotus Gambusia affinis Heterandria formosa Ictalurus nebulosus Jordanella floridae Labidesthes sicculus Lepomis gulosus Lepomis macrolophus Lepomis microlophus Lepomis punctatus Lucania goodie Poecilia latipinna Poecilia reticulate

1987

x x

1988

1989

1992

1995

No. adults

Reproducing

x x x x x x x x x x

x x x x x x

x x x

U R U

2 ⫹20 ⫹15

Yes Yes Yes

x x x

x xnd

R R M U U

2 3 ⫹25 ⫹15 ⫹20

Possibly Possibly Yes Yes Yes

x x x

x x x

x x xnd

a Abundance codes: (R) rare, 1–4% of individuals within tank; (U) uncommon, 5–19% of individuals within tank; (M) moderate, 20–34% of individuals within tank; (A) abundant, 35–100% of individuals within tank; (x) present; (xnd) present, not documented.

lifetime of the system, even though effectively it is constantly “topped” by the greenhouse roof. In most cases, when a woody plant reached the greenhouse roof, it was pruned back. Due to intense shading, the algal community in the freshwater stream itself was limited; degrading higher plant detritus was the primary energy source. The dominant invertebrate grazers, for the small amount of algae (i.e. periphyton) that was available, were the amphipod Hyalella azteca and the snail Physella cubensis. The dominant detrivore was the small shrimp Palaemonetes palidosus. The important carnivores in the freshwater system were the centrarchid fish Lepomis punctatus and Lepomis microlophus (bluegills) as well as the small but abundant Hydra. The bluegills fed on the abundant Poecilia (mollies and guppies), Lucania goodei (bluefin killi), and Gambusia affinis (mosquito fish) that were successfully maintaining populations in the system. The Hydra was perhaps feeding on young fish, but more likely dominately on the protozoan fauna. The crayfish Procambarus alleni was numerous and reproductive when the system was young, feeding on a surplus of detritus, its primary food source. While it declined later, apparently due to predation by centrarchid fish, it remained a part of the community and continued to support a small reproductive population. The primary physical structural elements of the well-lighted upper pool, the equivalent of a sink hole in the wild, were fiberglass walls and siliceous sand. Thalia geniculata (arrowroot) was moderately abundant, rooted in the siliceous sand, though it was heavily coated with a calcareous periphyton. These habitats supported abundant primary producers, primarily the filamentous red alga Audouinella violacea, the matforming,

false-branching, blue-green Scytonema hofmanni, and the floating aquatic fern Salvinia rotundifolia. The dominant grazers on the algae were Poecilia latipinna and the snail Melanoides tuberculata. Unlike the highly shaded stream community, algal standing crop was high in this unit, provided the primary internal energy source here, and was undoubtedly an important input source to the stream proper. The pH values were well above 8.0, as in the wild, and considerable calcification occurred along the water line of the tank above the Scytonema hofmanni mat. Calcification also occurred on the higher plant Thalia, where the blue-greens Calothrix crustacea and a Tolypothrix species formed a whitish band similar to the periphyton mat of many Everglades prairies. The snail Melanoides tuberculata was particularly abundant in the algal mat on the shallow sandy bottom section of the pool. The dominant carnivores in the upper pool were Fundulus chrysotus and Lucania goodei. These fish were eating Hyalella azteca, Cypridopsis vidua, unidentified midge larvae, and copepods while the herbivorous mollies were consuming the algae and the rootlets of the periodically abundant Salvinia. On the microfaunal scale, while nearly 40 species were tabulated, the amoeba Cochliopodium and ciliates Vorticella microstoma and Platycola longicollis occurred repeatedly and abundantly. The entire species list tabulated in 1995, in comparison to 1987 and 1992, is given in Tables 23.1–23.5. The dominant species contrasted to the estuarine populations were shown in Figures 22.10–22.13. Unfortunately, no specialist was available to determine the insects in either 1992 or 1995. We refer the interested reader to the 1987 list in the first edition.


TABLE 23.5 Aufwuchs Organisms Present in the Florida Everglades Stream and Wetland Mesocosma 1989 Diatoms Cymbella sp. Cocconies spp Navicula sp. Pleurosigma sp. Synedra sp. Tabellaria sp. Amphora sp. Fragilaria sp. Nitzschia sigmoidea Gomphonema sp. Rhopalodia sp. Asterionella sp. Bacterial and particulate browsers Flagellates Anisonema sp. Peranema trichophora Peranemopsis sp. Amoebas Arcella sp. Arcella vulgaris Arcella dentate Centropyxis sp. Cochliopodium sp. Dufflugia sp. Grazing ciliates Nassula sp. Chilodonella sp. Cinetnchilum magaritaceum Paramecium bursaria Aspidisca costata Frontonia sp. Holosticha sp. Filter-feeding ciliates Vorticella microstoma Vorticella picta Vorticella convallaria Platycola longicollis Stentor mulleri Epistylis sp. Zoothamnium sp. Predators of protozoans (all ciliates) Laxophyllum sp. Coleps hirtus Litonotus sp. Heliophya sp.

II IV II II II II II II III

II II

III III II III I III II II II I II

1995

II II II II II II II II II II I II

II I II II II I III I III II II

I III

II II III I II II

II II

I I I II

a

Abundance scale (on standard settling plates): I, single individual seen; II, 2–10 individuals; III, 11–100 individuals. Data from D. Spoon; from Adey et al. (1996).

Mesocosm Success over 8 Years of Operation The higher plant communities of this mesocosm, except for a relatively few floating and benthic macrophytes, were largely located in the prairie and hammock communities bordering the stream. These communities generally maintained their integrity, with

449

most of the dominants of the wild analog remaining dominant for over the 13 years that this system operated. More than 223 higher plant species were introduced into this system as seedlings, saplings, or soil seedbank elements. Fifty-four of those species were ephemeral, never displayed good growth, and were only seen for a short time in the first year. No attempts at reintroduction of these species were made. Fourteen species were lost as a direct result of insect pest infestations; only one of these was due to infestations of “wild-type” insects (thrips on Ludwigia leptocarpa). There were 21 species of trees or woody bushes in this system, almost all of which are in the fully closed hammock area. Many flowered and some produced seed, but until an opening was created in the canopy, here, as well as in the same situation in the wild (by storms or ageing), the increase of populations through reproduction on the time scale of the model was neither possible nor pertinent to the measure of success. A single woody individual, a red mangrove, had invaded from the adjacent estuary system and apparently established itself. A few of the remaining trees did not do well, particularly the oaks and the mahogany, and earlier we mentioned the enveloping effect of a very large inland leather fern. Here, the effect of an approximately 10-foot (over soil) greenhouse roof is clearly more important than the very limiting surface area for the hammocks. Of the remaining roughly 40 species of herbaceous plants, primarily in the prairie, most maintained their populations quite well. Earlier, we mentioned the need to install a greater soil slope and a higher elevation, above water table than exists in the wild, if dry prairie were to continue to be a viable community. This was a design problem that needs to be corrected in future models. The primary problem with the prairie community, however, was simply that because of its orientation it received only northern light. The wild dominant, in these environments, Cladium jamaicensis (sawgrass) forms particularly dense stands (and provided even more shading) in the mesocosm. Many more secondary and tertiary species would almost certainly have survived in the mesocosm prairie communities if it had been possible to correct these structural and orientational problems. In terms of available light, the stream community in the freshwater system was more like a stream running through a hammock in the wild. Only the upper pool, the equivalent of a sink hole or old alligator hollow, in the wild, served to match the open stream environment characteristic of Everglades prairies. While few algae with their typical calcifying effects occurred in the hammock stream, the blue-green species Microcoleus (Schizothrix) calcicola and Scytonema hofmanni were abundant in the well-lighted upper pool. Both species were involved in carbonate deposition in the highly

450


oligotrophic environment of this system. Scytonema hofmanni and Microcoleus calcicola were the dominant elements of the calareous periphyton of the Everglades prairies and also form one of the dominant soil types of South Florida (Merz, 1992; Browder et al., 1994). Since they were abundantly present in the model system, simply providing direct sunlight on the prairie, which was now extensively shaded due to maturation of the tree canopies and its location on the north side of the greenhouse, would likely have significantly increased the list of keystone species in the mesocosm prairie. The stream and ponds had a representative selection of macroinvertebrates throughout much of their history. However, several snails (Viviparus georgianus, Pomacea palidosus, Pseudosuccinea columnella) disappeared midway through system operation. As we discussed above, the pond and stream portion were periodically covered by dense accumulations of floating aquatic plants (Salvinia rotundifolia, Azolla caroliniana, Lemna minor). These mini-macrophytes, along with the extensive tree canopy, prevented most light from penetrating into the water column, to the detriment of the primary production of algae and submerged aquatic vegetation and periphyton. Algal periphyton would be the normal fodder for these species. The numerous grazing snails, Melanoides tuberculata and Physella cubensis, that were present in the well-lighted scrubbers, the upper pool, and ancillary tanks support this contention. Two species of unionacean mussels, Popenais buckleyi and Lampsilis teres, also disappeared during system operation. However, only a few individuals were originally introduced, and their reproduction depends upon a larval phase parasitic in the gills of certain species of fish. In addition, during the first 4 years of operation of this stream environment, a large impellor pump (rather than the later disc-flow pump) was used. Thus, there were a number of reasons why these species did not produce sustainable populations. The remaining unionacean clam Elliptio jayensis probably relates to the longevity of some freshwater mussel species, often in excess of 50 years. Two large crustaceans that were no longer present in later years, were the giant prawn Macrobrachium carcinus and the duppy crab Cardisoma guanhumi. Both rely on estuarine water for larval development and would not likely have reproduced in this particular model, since return of fully aquatic species from the estuary to full fresh water was difficult. In terms of fish species assemblages, this mesocosm was very close to its natural counterpart. Carter et al. (1973), in their sampling of small Everglades freshwater habitats, found that all species belonged to the families Poeciliidae, Cyprinodontidae, and Ictaluridae. Schomer and Drew (1982) further reported that the cyprinodonts and centrarchids were most prevalent in terms of genera and species while Poecilia latipinna, Poecilia reticulata, and

Heterandria formosa fall into the ubiquitous category. As with the Gulf shore system (Chapter 22), diversity was limited, in part, due to lack of seasonal migration. The mesocosm contained three families of fish represented by eight species. There was approximately 110 adult individuals when the system was censused, though the numerous juvenile populations were impossible to estimate. No one species in particular was strongly dominant, although the bluefin killi apparently had the highest reproductive success. Although the sailfin mollies and golden topminnows did reproduce, their numbers remained low. The centrarchids that occur in the freshwater region were probably providing considerable predation pressure on the smaller species. The provision of refugia to simulate the larger area in the wild would likely have increased the number of small species and their population sizes. In summary, after 4 years of partial closure followed by another 5 years’ total closure, the Florida Everglades freshwater mesocosm described in this chapter had over 150 tabulated species (with insects and plankton not tallied). These species, a large percentage of which either were maintaining populations through reproduction or were capable of doing so if the internal space were to be made available, had self-organized into a complex food web. That food web was processing energy totally derived from in-system photosynthesis, as there was no organic input to this system. It is important to point out that in the wild no patch of this dimension is totally or even marginally closed. The biotic closure (but not physical or chemical) of wild patches of similar size for long periods would provide a comparative tool for a more precise judgment of model performance. It is interesting to note that in this system, sawgrass (Cladium jamaicensis), the key species in wild Florida Everglades prairie, is “weedy” in character, extending beyond the zone that we had prescribed for it in the model. We feel that we understand the reasons for this based on the limited space allocated for the ecotone to dry prairie. On the other hand, the cattails (Typha domingensis) have remained narrowly restricted in the model habitat. In Everglades restoration, using controlled marsh storm treatment areas (STAs), cattails have become dominant, often excluding Cladium. In this model, we maintained phosphorus below 10 ppb, while that has not been achievable with STAs in the Everglades.

A BLACKWATER HOME AQUARIUM This 70-gallon, home aquarium system (Table 11.1) was initially established with pure silica sand, several inches thick, equivalent to typical small, tropical, blackwater tributary streams. This provided a silica-rich, poorly buffered environment, which, when coupled

A Blackwater Home Aquarium

with nutrient scrubbing, gave rise to a diatom-rich, poorly productive benthic community. The operational parameters were quite similar to those of the 2500-gallon low-nutrient tropical stream model described in the first edition of Dynamic Aquaria, though natural lighting in a shaded sunroom was supplemented with two 48inch very high output (VHO) fluorescent bulbs. Makeup water as well as subsequent evaporative replacement water were both “blackwater”-derived without filtering, primarily from sour gum/red maple swamps on the Virginia coastal plain. Unlike the larger system described in the first edition of Dynamic Aquaria, the home aquarium used a single bellows pump for recycling and scrubbers and was never operated with a centrifugal pump or filtration of any kind. The spatial and mechanical layout of this unit was the same as the small coral reef described in Figure 20.7. The primarily macroflora and fauna in this system tabulated at the end of one year of operation is shown in Table 23.6.

Blackwater streams and swamps typically derive their coloration (which is usually reddish rather than blackish) from the presence of tannins leached from soil and leaf litter. The tannins are very resistant to break down and are in large part responsible for the gelbstuff or reddish/yellow coloration of estuaries and coastal waters. Although all evaporative replacement water (about 5 gallons/week) in this tank is replaced as described above, the water of the system itself has no visible tannin coloration. Due to moderate ATS scrubbing and intense submerged aquatic plant biomass production within the tank, the essentially neutral input water is raised to a pH of about 7.8 in the tank itself. Perhaps the relatively high pH is responsible for precipitation of the tannin; if a more acid water were desired, the introduction of carbon dioxide as a fine bubble stream would likely achieve that objective. Typically operated at below 1–3 µM N–NO2 ⫹ NO3, a rough analysis of nitrogen import/export is useful

TABLE 23.6 Organisms Occurring in a 70-Gallon Blackwater Home Aquarium Emphasizing South American Flora and Faunaa Kingdom Monera Division Cyanophycota Oscillatoria rubescens Oscillatoria sp. Kingdom Plantae Subkingdom Thallobionta Division Chlorophycota Spirogyra aequinoctiales Mougeotia sp. Ulothrix aequalis Cladophora glomerata Division Chromophycota Numerous diatom spp. Subkingdom Embryobionta Division Magnoliophyta Lemna minor (duck weed) Echinodorus paniculatus (amazon sword plant) Potamogeten pusillus (pond weed) Heteranthera dubyi (water star grass) Nymphaeae elegans (blue water lily) Justicia americana (water willow) Ludwigia palustris (water primrose) Division Bryophyta Riccia fluitans Division Filicophyta Salvinia rotundifolia

451

Kingdom Animalia Subkingdom Eumetazoa Phylum Mollusca Melanoides tuberculata (red-rimmed melania) Planorbella duryi (seminole rams horn) Physella cubanensis-peninsularis (Caribbean Physa) Lampsilis sp. (freshwater mussel) Phylum Chordata (fish) Family Characidae Gymnocorymbus tennetzi (black tetra) Hyphessobrycon ersythrostigma (bleeding heart tetra) Pseudocoryinfopoma doriae (dragonfin tetra) Family Gasteropelecidae Gasteropelecus levis (silver hatchet fish) Family Callichthyidae Corydoras metae (coryoras) Family Poeciliidae Xiphosphorus helleri (sword tail) Poecilia reticulata (guppy) Gambusin affinis (mosquito fish) Family Cichlidae Pterophyllum altum (deep angelfish)

a Algae, higher plants, macroinvertebrates, and fish are included, while diatoms, plankton, and microinvertebrates are not cataloged.

452


for this small tank. A standard flake food was fed to the tank at the rate of 1.5 g (dry) per week. Estimating 10% nitrogen for the flake food, 6% for scrubber algae, and 2% for higher plant fragment removal, the algal scrubber of 0.072 square meter removed about one-half of nitrogen introduced; the removal of old degenerating leaves of the submerged aquatics exported the other half. In the 1–3 µM N range, there was probably little nitrogen fixation or denitrification. The scrubber, lighted by two 24-inch VHO bulbs, produced a typical basal mat of Oscillatoria spp. with some filamentous greens such as Ulothrix aequalis and Mougeotia spp. and abundant diatoms, but with a dark green upper story of Cladophora glomerata. This extensively branched and very coarse green algal species has basal cells that appear to extend through the basal mat and attach directly to the plastic screen. Several additional freshwater microcosms and mesocosms have been operated over the last 20 years using ATS control. We invite interested readers to consult Table 11.1 and the earlier editions for more information.

RESTORATION OF FRESHWATER ECOSYSTEMS As we describe in Chapters 9 and 25, eutrophication in wild streams and lakes is a serious, but mostly solvable problem, using managed aquatic plant system (MAPS) techniques. In streams the physical modifications may be more directly significant than the nutrient state and require rehabilitation first; Gordon et al. (2004) provide an excellent treatment of the problems and solutions. Ecosystem models can provide not only the testing tools to help provide a rational approach to a specific situation but the public demonstration and education that is almost always necessary for stream restoration. Lake and pond restoration problems are primarily related to nutrient state rather than physical state (see discussion by George, 2002). Conservation related to nutrient retention is extremely important for the future, but rarely provides the whole solution for the present. If direct rehabilitation is not undertaken in parallel with conservation (i.e. nutrient release limitation) then failure will be often assured. Although our emphasis in nutrient restoration in Chapter 25 is placed on rivers, MAPS techniques can be applied to stream inputs into lakes and ponds, and this has been accomplished at very large scale (see www.hydromentia.com). However, MAPS techniques, especially ATS as discussed below in this chapter, can also be directed to existing lake status. The problems of oxygen limitation in the hypolimnion and the long-term release of stored phosphorus in sediments (see e.g. Dodds, 2002) are both issues that can be

corrected with ATS systems. Particularly where phosphorus is a controlling issue, N to P ratio can be constantly adjusted during the process of ATS treatment. These have been called bottom-up methods, and can apply not just to nutrient limitation but also to direct management or input of plants (Weisner and Strand, 2002) or even algae (Stevenson et al., 1996). The management of trophic cascades (top-down approaches) requires adjusting predator status to control grazers and therefore primary production. However, the latter approaches are difficult and often fraught with the problems of having to introduce species. Prior testing with models can be very helpful in understanding the process and the likely outcomes. They can also help in making decisions and, again, may provide a crucial level of public understanding to achieve objectives. We quote Dodds (2002): “Much of the future job of aquatic ecologists may be in ‘damage control.’ We will be asked what is necessary to maintain ecosystem function and preserve desirable species. A more detailed knowledge of aquatic ecology than we currently possess is necessary to provide this information. For example, the link between diversity and ecosystem function is not well understood. The redundancy of ecosystem services by species (i.e. what is the minimum assemblage of species necessary to maintain productivity and the ability to neutralize pollutants in aquatic ecosystems) is not well documented. We simply cannot predict any but the most extreme effects of our impacts on aquatic habitats. Likewise, detailed knowledge of the biology of species is often required before they can be preserved. Such knowledge is sorely lacking for all but the most popular game fishes.”

All of these issues can be usefully addressed with living ecosystems models, as we have attempted to demonstrate throughout this chapter.

References Adey, W., Finn, M., Kangas, P., Lange, L., Luckett, C., and Spoon, D. (1996) A Florida Everglades mesocosm – model veracity after four years of self organization. Ecol. Eng. 6: 171–224. Browder, J., Gleason, P., and Swift, D. (1994) Periphytes in the Everglades: spatial variation, environmental correlates and ecological implications. In: Everglades: The Ecosystem and Its Restoration. S. M. Davis and J. C. Ogden (Eds). St. Lucie Press, Del Ray Beach, Florida. Brusca, R. and Brusca, G. (2003) Invertebrates, 2nd edn. Sinauer Associates. Sunderland, Massachusetts. Burgis, M. and Morris, P. (1987) The Natural History of Lakes. Cambridge University Press, Cambridge. Carter, M. et al. (1973) Ecosystems Analysis of the Big Cypress Swamp and Estuaries. U.S. E.P.A. 904/9-74-002. Dodds, W. (2002) Freshwater Ecology. Academic Press, San Diego, California. Drew, R. D. and Schomer, N. S. (1984) An Ecological Characterization of the Caloosahatchee River/Big Cypress Watershed. US Fish and Wildlife Service, Slidell, Louisiana, FWS/OBS-82/58.2. Duever, M. J., Carlson, J. F., Meeder, J. F., Duever, L. C., Gunderson, L. H., Riopelle, L. A., Alexander, T. R., Myers, R. L., and Spangler,

References D. P. (1986) The Big Cypress National Preserve. Research Report 8, National Audubon Society, New York. George, D. G. (2002) Regional-Scale Influences on the Long-Term Dynamics of Lake Plankton. In: P. J. le B. Williams, D. Thomas, and C. Reynolds (Eds). Blackwell Science, Oxford. Gordon, N., McMahon, T., Finlayson, B., Gippel, C., and Nathan, R. (2004) Stream Hydrology: An Introduction for Ecologists, 2nd edn. John Wiley & Sons, Ltd., Chichester. Livingston, R. (2006) Restoration of Aquatic Ecosystems. Taylor and Francis, CRC Press, Boca Raton. Merz, M. (1992) The biology of carbonate precipitation by cyanobacteria. Facies 26: 81–102. Moss, B. (1988) Ecology of Fresh Waters, 2nd edn. Blackwell, Oxford.

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Pennak, R. (1989) Fresh Water Invertebrates of the United States, 3rd edn. Wiley, New York. Schomer, N. S. and Drew, R. D. (1982) An Ecological Characterization of the Lower Everglades, Florida Bay and the Florida Keys. U.S. Fish and Wildlife Service Biological Services Program, Washington, DC, FWS/OBS-82/58.1. Stevenson, R., Bothwell, M., and Lower, R. (1996) Algal Ecology. Academic Press, San Diego, California. Weisner, S. E. B. and Strand, J. (2002) Ecology and management of plants in aquatic ecosystems. In: Handbook of Ecological Restoration. Vol. 1. Principles of Restoration. M. Perrow and A. Davy (Eds). Cambridge University Press.


P A R T

V THE ENVIRONMENT AND ECOLOGICAL ENGINEERING


C H A P T E R

24 Organisms and Natural Products Commercial Ecosystem Culture

All life has parasites and diseases; humans are no exception. During the first three-quarters of the 20th century, the optimists would have it that we were on our way to conquering disease. And indeed, a few diseases were conquered, and for many others, at least if “caught early”, they could be removed from an individual or small population. However, bacteria and viruses evolve fast; in significant response to our antibiotic and antiviral defenses, these pathogens achieve circumvention on the scale of years to decades. Probably we can keep our diseases at bay, and many structural and genetic dislocations of humans can also be corrected. However, a constant flow of drugs out of the pharmaceutical pipeline is required to do this. While some drugs are invented “de novo”, in the past most have come from nature, the pre-invention of other species, which we co-opt and then eventually synthesize. At least for many drugs, this pattern is likely to continue for the foreseeable future. To fight off our medical problems, we need other organisms. We need to know the offensive, defensive, structural, and functional chemistry of those organisms. We need to know that they exist and we need to characterize and classify them, if this has not already been done. Then we need to know how to obtain them in quantity for study and extraction. As a species and a society, we need global biodiversity, and we need extensive ecosystem services. As we presented in the early chapters of this book, we cannot survive as a species without a very wide array of other species, most of which can only exist in functioning ecosystems. Call it Gaia, or simply the localized situation of a physical universe; it is reality, and neither our hubris nor our mysticism will change it. However, even as individuals, most humans do not wish to escape their intrinsic connections to nature. Some still consort

with wild nature, to the extent that the wilder and more remote the better. However, the majority prefers to have it more controlled with gardens and pets. In the aquatic world, the tropical freshwater fish and plant industry is a half-century old, vast and growing; more temperate, high-cost sidelines, like Koi, are flourishing. In the last 25 years, the marine market for coral reef fish, soft and stony corals, live rock (i.e. coralline algae), a few fleshy algae, and mobile invertebrates has also rapidly expanded. Much of this market is wild caught; some is cultured. However, in the vast majority of cases, whether we are talking about the aquaculture producers or the hobbyist customers, these cultures are more appropriately referred to as polycultures rather than ecosystems. As we noted in several chapters, the effort in aquarium science has been primarily to operate aquaria as gardens and to use whatever techniques are available, mostly physical and bacteriological, to maintain them as simply as possible, in a controlled, garden-like state. We wish the beauty, and not the ugly, but both are in the eyes of the beholder. Unquestionably, gardening is a valuable endeavor of our lives; its consort with nature and teachings is extremely important. However, we cannot allow ourselves to slip into the view that gardening is a reality of the ecosystems that keep us alive as a species. Farming too is a necessity for our numbers, but too much will destroy the ecosystems that also support us. The eutrophication and toxification of our fresh waters, coastal waters, and to some degree ocean waters is in large measure as a result of our agricultural practices. The message of “Silent Spring” must always remain loud and clear. We are a terrestrial species, and many of us will note when the birds stop singing. How many of us will notice when the “song of the deep” is no longer heard,

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and one rivet too many has been removed from our flight through space and time. In this chapter, we discuss how microcosm and mesocosm techniques, with the emphasis on ecosystems, can help us in this need for other organisms.

THE AQUARIUM WORLD Many environmentalists consider the aquarium hobby, and especially the reef aquarium hobby, an anathema. While there are unquestionably some extremely undesirable practices connected with the hobby, including the potential for wild population reduction as well as ecosystem disruption and inevitably some invasives transfers, as well as collecting damage, shipping losses, and some poorly educated hobbyists, we feel that the environmental/conservationist benefits can outweigh the negatives. Most of the negative aspects of the hobby can be avoided, and that is the first subject of this chapter. Favorable environmental and conservation attitudes among a broad public are absolutely essential for society as a whole to “practice what it preaches” and hold a viable environmental ethic. It is important for “greens” to be tugging toward “deep ecology,” even if society will never get there. Direct familiarity with organisms is extremely important to humans ever more disconnected from the rest of the living world. The aquarium hobby provides this familiarity in the context of a husbandry that is fairly precise in its requirements. Environmental understanding cannot be truly learned in a book or park, and even if it could, we are in danger of “loving some of our wild areas to death.” Particularly with regard to coral reefs, if most of the people on Earth who wished to dive on coral reefs were able to do so, there would be few if any reefs left to visit. Even if the relatively few who can (at least hundreds of thousands per year) continue to do so, the effect might well be disastrous. Ecosystems, as many wild areas, are very sensitive to large numbers of people. Model ecosystems can provide an intimate ecological understanding to an increasingly city-bound populace not likely to obtain that understanding even through visits to wild ecosystems (Color Plates 1 and 11). A large part of the world’s population practices gardening. At least in the western world, the seeds, potted plants, and other paraphernalia to accomplish this are provided commercially. Virtually none of this living material is taken from wild ecosystems – it is cultured and distributed by a large number of companies. Although, as we have noted, growing a garden should not be confused with developing and operating an ecosystem, the biological lessons can be invaluable,

though the practices are sometimes counter-productive to sustainability. Commercial endeavors, given adequate capital, are now in a position to provide many of the organisms and mini-communities (live rock) needed coral reef aquaria from cultured systems. During the past decade, the practice of “wild culture” of reef organisms for the aquarium trade has developed. Typically, in the tropics, either shore-based, flowthrough systems, or artificial reefs, “in situ,” are established, and organisms that will continue to grow when fragmented are collected in the wild, broken into smaller pieces and established for growth out to transportable size. This process works especially well for stony corals, and could work well for live rock, though the cleaning processes used often destroy any value for ecosystem culture. Newer techniques of capturing larval fish over wild fore reefs before they settle into coral reef communities have also been developed. Since most of these fish would naturally not survive that critical step of settlement, this would seem to provide a sustainable supply for culture. However, it is essential that the efforts of these practices on wild reef fish communities be monitored very closely by trained scientists before this becomes an established and widespread practice. While these methods could provide for both local employment and reef conservation, in theory, without scientifically based management, the results could be disastrous. Equally important, the long-distance packing, transportation and distribution problems remain, and these have always been a prime source of mortality. The reproductive cycles of perhaps thousands of marine and freshwater organisms, invertebrates and fish, have been studied, and carried through to completion in university and biological station laboratories. Several hundred marine organisms derived from coral reefs would appear on any laboratory culture list, and the results of these studies can be found in marine biology, aquaculture and a wide variety of fisheries journals. However, it can be a difficult and often insurmountable step from Petri dish to commercial culture, a step likely to be taken by only a small fraction of the species studied. Many species have complex requirements that their respective ecosystems normally provide, but are very difficult to routinely achieve in a productiontype monoculture (or even in the laboratory). In 2001, for the Marine Ornamentals Conference in Orlando, Florida, Martin Moe circulated a questionnaire to hobbyists, commercial culturists, and scientists regarding the state of coral reef organism culture. It is the state of commercial culture that is most valuable at this point, and we paraphrase from his unpublished report. Of 34 responding commercial culturists, roughly two-thirds using closed (rather than flow-through) systems, only one-third describe their companies as

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“doing well.” Furthermore, 56% of the respondents accept that the breeding business is “small and struggling” while only 40% would accept that it is “important and growing.” They reported that “successfully cultured” species included 72 species of fish (in 15 genera) and 119 species of invertebrates, mostly more or less equally soft and stony corals. This is a considerable advance over the situation a decade earlier, and along with expected future advances may well support an ornamental aquarium industry (Color Plate 56). Assuming that commercial culturists need only to return occasionally to the wild for genetic stock, and can rely on controlled “reef culture,” this could be a sustainable and sophisticated process, as in the gardening industry. Also, a conservation attitude is much more likely to be strongly displayed by sophisticated companies dependent on wild stocks for their genetic material. Unfortunately, most of Moe’s responders indicated that their biggest single problem was financial; thus, none of this is likely to happen unless a system of culture credits (like carbon credits) is developed. In this context, a fee would be charged for every wild caught organism that is then made available, through a culture bank, for every organism cultured. As in food aquaculture, closed, nonpolluting, sustaining culture systems will never be viable as long as wild organisms can be freely collected. In our view, it is time that the marine aquarium industry took a more ecosystem-culture approach to the issues of ornamental culture. In this chapter, we describe a prototype-closed ecosystem that had been in operation in our laboratories for over 10 years. Hundreds of coral reef species, some rare or even unknown in the wild, have been bred and cultured in sufficient numbers so that when scaled up they could support a commercial operation. A wide variety of very high-quality softballsized live rock, with many dozens of species of algae, including crustose corallines and small invertebrates, were also routinely produced in these systems. Many reef fish, while not reproduced in great numbers in the systems we have worked on, routinely spawn and produce eggs that hatch (Table 24.1). Most of these are preyed upon by other fish and invertebrates, within the model systems, and never reach adult dimensions. In the wild, most hatched reef fish enter the ocean plankton for a period of weeks where they are subject to less voracious predation. Success with reef fish in large numbers depends less on water quality (in the systems we describe) than on producing refugium spaces and perhaps specially adapted feeds. Properly operated algal turf systems can achieve, and maintain under virtually any feeding conditions, the kind of high-quality, oxygen-rich water that is equivalent to open-ocean water.

TABLE 24.1 Fish That Have Spawned in ATS-Controlled Marine/Estuarine Systems and Recruited to Juveniles (ⴙ) and Maturity (*) Coral reef systems Aquatic Technologies, Terre Haute, INa *Amphiprion ephippicum (red saddleback anemone fish) *A. clarkii (Clark’s anemone fish) *A. frenatus (tomato anemone fish) *A. percula (clown anemone fish) *A. ocellaris (anemone fish) *Prennas biaculeatus (maroon anemone fish) *Pterapagon kauderi (banggai cardinals) *Hippocampus sp. (dwarf seahorses) *Poecilia velifera (newborn saltwater mollies) 130-gallon reef aquarium, Gloucester Amphiprion frenatus (clownfish) Exhibit reef, Smithsonian Eupomacentrus leucostictus (beaugregory) Stegastes dorsopunicans (dusky damselfish) Great Barrier Reef mesocosm, Townsville, Australia * Plotosus anguillaris (catfish) Biosphere II reef, Arizona ⫹2 Pomacentrid spp. (damselfish) ⫹Scarus inserti (striped parrotfish) ⫹Abudefduf saxatilis (sargeant major) Florida Everglades mesocosm Marine and brackish *Floridichthys carpio (goldspotted killi) *Fundulus confluentus (marsh killi) *F. grandis (gulf killi) *F. similis (longnose killi) *Heterandria formosa (least killi) *Cyprinodon variegatus (sheepshead minnow) a An additional 48 species have spawned in the Aquatic Technologies production unit but have not yet been brought to maturity and are not noted here.

A number of stony coral genera and species have successfully reproduced sexually (Table 20.9) in many of the Algal Turf Scrubber (ATS)-controlled systems that we have worked on (see Microcosm Biodiversity, Chapter 20). As is now well known, many stony corals can be induced into asexual reproduction by physical fragmentation. These fragments can then be grown into small individuals suitable for distribution. We have demonstrated (Small et al., 1998; Small and Adey, 2001) that high-density ATS-controlled systems can produce stony coral growth that exceeds mean growth in wild reefs (Chapter 10). Thus, there is no reason for distributors to mass collect stony corals in the wild. Equally important, there is no reason to continue to sustain the transport losses. It is quite possible to mass grow cultures of numerous stony coral species for sale to hobbyists (Color Plates 2, 5, 6, and 13) within the primary western country markets. As we noted above, like wild fishing, it is the economics that controls whether or not this is done, and a culture credit system could work.

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A Reef Culture System Figure 24.1 diagrams a basic culture system that has been used for commercially producing stony corals and hundreds of species of reef algae, and invertebrates. It would need to be manipulated to routinely produce fish, and we discuss that issue further below. The issue of physical/chemical parameters for reef aquaria is debated endlessly. We have assumed, and continue to maintain, that to culture a broad spectrum of reef organisms, and especially to operate in an ecosystem mode, the basic parameters characterizing well-developed wild reefs should be maintained. Table 24.2 provides the basic ranges and ideal levels that have been successfully used in an operating commercial system. It may well be that for emphasis of particular groups, adjusting these parameters could be important. Our techniques have been developed to emphasize “reproduction” of whole coral reef ecosystems rather than specific groups. It is quite clear that if a balanced,

high-diversity ecosystem is operated specifically to culture high diversity for sale, then the extremely low nutrients discussed in Chapters 11 and 20 are necessary. These are easily obtained with ATS systems, even with moderate feeding loadings, without negative side effects. It is also essential in these highly calcifying systems where production rate is a requirement, that calcium and total alkalinity be maintained 10–20% above normal (i.e. 460–500 mg/liter and 2.7–2.9 mg/liter). Pumping and filtering methods have also been extensively debated. However, the vast majority of reef species enter the plankton as larvae for some period. While some larvae, especially those of algae and very small invertebrates, can repeatedly pass through the shear and compressive stresses of impellor pumps, many cannot. In our years of experience, the most diverse reef systems by far, taking size into account, are those systems that have never had impellor pumps. For large culture systems that need high pumping volumes, disc-flow pumps, as described in Chapter 2, are

FIGURE 24.1 Commercial-scale culture system, based on ATS, for the production of fish and a variety of invertebrates (including stony corals) for the aquarium hobby. This basic system, expanded with numerous “refugia” and sub-culture units, was operated for many years for commercial production by Aquatic Technologies in Terre Haute, Indiana. In practice, the basic unit is adapted in a number of ways to enhance desired groups of organisms. Drawing by Charlotte Roland.

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TABLE 24.2

Basic Operating Characteristics of a Reef Organism Production Systema

Total volume: 4000 gallons Algal turf scrubber area: 4 ATS per 900 square inches turf (ATS, dump-bucket type) Pumps: Two Archimedes’ screws at 35 gpm each Lighting: Culture system: 12 at 400 W, 6500 K for 6 h/day, staggered ATS: 6 at 110 W, 5000 K for 16 h/day Temperature (°F): min 77; mean 80; max 84 Salinity (ppt): min 33; mean 35; max 36 pH: min 7.9; mean 8.2; max 8.5 Calcium (mg/liter): min 370; mean 420; max 480 Total alkalinity (meq/liter): min 2.4; mean 2.6; max 3.0 Production (e.g. for corals): 100 soft cutting/175 stony coral mounts/month Ca(OH)2 and KI: occasionally a

One of several units operated at Aquatic Technologies, Terre Haute, IN, in the late 1990s.

highly reliable, and function without problems for very long periods. For an operation that requires the maintenance of extremely sensitive larvae, and in which pump maintenance is a secondary issue, Archimedes’ screw pumps can provide good service for large flow rates (200–400 gpm). Bellows pumps (see Chapter 2) are adequate for small systems. Most of the reef organisms used in the commercial trade are from relatively shallow wild reefs (

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