Advances in Marine Biology, Volume 15

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Advances in

MARINE BIOLOGY VOLUME 15

This Page Intentionally Left Blank

Advances in

MARINE BIOLOGY VOLUME 15 Edited by

SIR FREDERICK S. RUSSELL Plymouth, England

and

SIR MAURICE YONGE Edinburgh, Scotland

Academic Press London New York

San Francisco 1978

A Subsidiary of Harcourt Brace Jovanovich, Publish-srs

ACADEMIC PRESS INC. (LONDON) LTD.

24-28 OVAL ROAD LONDON NW1 7DX

U.X. Edition published by ACADEMIC PRESS INC.

111

FIFTH AVENUE

NEW YORK, NEW YORK

Copyright

10003

0 1978 by Academic Press Inc. (London) Ltd.

All rights reserved

NO

p a r OF THIS BOOK MAY BE REPRODUCED IN ANY FORM BY PHOTOSTAT,

MICROFILM, OR ANY OTHER MEANS, WITHOUT WRITTEN PERMISSION FROM THE PUBLISHERS

Library of Congress Catalog Card Number: 63-14040 ISBN:

0-12-026115-4

PRINTED IN GREAT BRITAIN BY THE WEITEFRIARS PRESS LTD., LONDON A N D TONBRIDGE

CONTRIBUTORS TO VOLUME 15 CHRISTOPHER J. CORKETT,Dalhousie University, Halifax, Nova Scotia, Canada.

E. D. S. CORNER, The Laboratory, Marine Biological Association, Plymouth, England.

ANTHONY G. DAVIES,The Laboratory, Narine Biological Associa,tion, Plymouth, England. IANA. MCLAREN,Dalhousie University, Halifax, Nova Scotia, Canada.

M. R . REEVE,University of Miami, School of Marine and Atmospheric Science, Miami, Florida, U.S.A.

F. S. RUSSELL,Marine Biological Association, Citadel Hill, Plymonth, England.

M. A. WALTERS,University of Miami, Xchool of Marine and Atmospheric Science, Miami, Florida, U.S.A.


CONTENTS CONTRIBUTORS TO

VOLUME 15

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The Biology of Pseudocalanus CHRISTOPHERJ. CORKETTAND IAN A. MCLAREN I. Introduction

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11. Systematics . . A. Nomenclature.. .. .. B. " Physiological " Species . . C. Variations in DNA Content D. Retrospects and Prospects . .

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.. .. .. 111. Distribution and Abundance A. Geographical Distribution . . .. .. B. Abundance .. .. .. .. .. C. Temporal Variations. . .. .. D. Vertical Distribution. . .. .. . . E. Sampling Problems and Microdistribution F. Physical-chemical Limits to Distribution . . G. Retrospects and Prospects . . ..

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VI. Excretion . . .. .. A. Nitrogen . . .. B. Phosphorus . . .. C. Retrospects and Prospects VII. Locomotion . . .. .. A. Routine Swimming . . B. Escape Reaction .. C. Retrospects and Prospects

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VIII. Nutrition .. .. .. .. .. .. A. Feeding Mechanism . . .. B. FoodEaten .. .. .. .. C. Feeding Rate . . .. .. .. .. D. Die1 Feeding Rhythms .. E. Assimilation . . .. .. .. F. Food Requirements for Sustenance G. Retrospects and Prospects . . .. IX. Reproduction .. .. .. .. A. Sex Ratio .. . . .. .. .. B. Oogenesis and Egg Laying . . C. Sperm and Spermatophore Production D. Mating .. .. .. .. E. Reproductive Rate . . .. .. F. Retrospects and Prospects . . ..

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.. .. X. Development and Growth . . .. .. .. A. Embryonic Development Rate .. .. .. B. Hatching .. .. .. .. C. Development Rate of Nauplii and Copepodids . . D. Longevity of Adults . . .. .. .. .. E. Body Size .. .. .. . . .. .. .. F. Body Composition and Weights . . .. G. Oil Storage . . .. .. .. .. .. H. Growth Rates. . .. .. .. .. .. I. Rate of Production of Egg Matter .. .. J. The " Balance Equation " and Growth Efficiencies K. Retrospects and Prospects . . .* .. ..

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XI. Life Cycles in Nature .. .. .. * . .. A. General Features, Terminology and Approaches

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B. Representative Life Cycles . . C. Retrospects and Prospects . .

.. .. XII. Vertical Migration . . A. Ontogenetic -Migrations .. B. Seasonal Migrations . . .. C. Die1 Migrations .. .. D. Retrospects and Prospects . . .. .. XIII. Production . . A. General Methods .. B. Production Estimates C. Retrospects and Prospects .. .. .. XIV. Parasites A. Dinoflagellates .. B. Gregarines . . .. C. Trematodes . . .. D. Nematodes . . .. E. Crustaceans . . .. F. Retrospects and Prospects XV.

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Role in the Food Web . . .. A. Effect on Phytoplankton . . B. Predators .. .. .. C. Significance in the Food Web D. Retrospects and Prospects . .

XVI . Acknowledgements . .

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Marine Biology and Human Affairs F. S. RUSSELL

I. Food from the Sea 11. Fish Farming

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111. Poisonous and Venomous Plants and Animals

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.. Physiological and Medical Aspects. . Pesticide . . .. .. .. Geology and Meteorology . . .. .. .. .. Pollution .. Conservation . . .. .. .. Man and the Marine Environment. .

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IV. Underwater Structures

V. Ship Design VI. VII. VIII. IX.

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Echo-sounding and Noise

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Review of

Nutritional Ecology of Ctenophores-A Recent Research

M. E. REEVEAND M. A. WALTER

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11. Feeding Mechanisms and Behavior .. .. .. 251 A. Feeding Mechanism and Behavior in Mnemiopsis 251 B. Comparison of Feeding Behavior in Other .. .. .. .. . . 259 Tentaculata. . C. Food of Tentaculata . . .. .. . . .. 263 D. Food and Feeding Behavior of Nuda . .. 265

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IV. Chemical Composition

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VI. Digestion

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VII. Respiration and Excretion. .

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Conclusion

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Pollution Studies with Marine Plankton: Part 1. Petroleum Hydrocarbons and Related Compounds

E. D. S. CORNER

I. Introduction

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11. Hydrocarbon Levels in Sea Water .. .. A. Studies Primarily concerned with Alkanes. . B. " Dissolved " and Particulate Hydrocarbons C. Hydrocarbons in or near the Surface of the Sea D. Comprehensive Analyses .. .. ..

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111. Hydrocarbons in Plankton . . .. .. .. .. A. Phytoplankton .. .. .. .. . . B. Phytoplankton and Crude Oil as Sources of Hydro.. .. .. . . carbons in the Sea . . C. Zooplankton . . .. .. .. .. ..

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IV. Toxicity Studies with Phytoplankton .. .. .. 317 A. Studies using Crude Oils and their Water-soluble Fractions . . .. .. .. .. .. 319 B. Studies using Naphthalene . . .. .. . . 327 V. Mechanisms of Phytotoxicity

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VII. Fate of Hydrocarbons in Zooplankton . . .. .. A. Uptake and Release . . .. .. .. .. B. Quantitative Importance of the Dietary Pathway C. Long-term Exposure Experiments . . .. .. .. .. .. .. D. Metabolism .. .. .. E. Release of Hydrocarbons in Faecal Pellets. . VIII.

Toxicity Studies with Zooplankton .. .. .. .. .. .. .. .. A. Crude Oil .. B. W ater-soluble Hydrocarbons .. .. .. C. Possible Effects of Hydrocarbons on Reproduction by Zooplankton .. .. .. .. . . D. Summary and General Comments . . *. ..

IX. Conclusions . . .. A. Chemical Analyses B. Toxicity Studies C. Biochemical Work

X. Acknowledgements XI. References

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Pollution Studies with Marine Plankton: Part II. Heavy Metals

ANTHONY G. DAVIES

I. Introduction

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11. The Turnover of Heavy Metals by Phytoplankton .. A. The Kinetics and Mechanism of Metal Uptake by Phytoplankton .. .. .. .. . . B. The Effect of the Chemical Form of a Metal upon its Uptake by Phytoplankton .. .. .. C. The Role of Phytoplankton in the Biogeochemistry of Heavy Metals in the Sea .. ..

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111. Laboratory Studies of the Toxic Effects of Heavy Metals . . .. .. .. 398 upon Phytoplankton A. The Effects on the Growth of Phytoplankton . . 398 B. Synergism and Antagonism of Mixtures of Heavy Metals towards Phytoplankton . . .. .. 411 C. The Nature of Metal Toxicity in Phytoplankton . . 412

IV. Studies of the Toxic Effects of Heavy Metals upon Natural Populations of Phytoplankton . . .. 415 . . 416 A. The Effects on Primary Production Rates B. The Effects in Large Volume Sea Water Enclosures 419 V. Heavy Metal Concentrations in Natural Populations of Marine Phytoplankton .. .. .. .. 425

.. VI. The Turnover of Heavy Metals by Zooplankton . . A. Studies of Metal Fluxes through Zooplankton .. B. Food and Water as Sources of Metals for Uptake by Zooplankton. . .. .. .. .. .. C. The Effect of the Chemical Form of a Metal upon its Uptake by Zooplankton .. .. .. D. The Role of Zooplankton in the Biogeochemistry of Heavy Metals in the Sea . . .. .. .. VII. Laboratory Studies of the Toxic Effects of Heavy Metals upon Zooplankton . . .. .. .. .. A. The Effects on the Metabolic Activity of Zooplankton .. .. .. .. .. .. B. The Effects on the Feeding and Ingestion Rates of Zooplankton. . .. .. .. .. *. C. The Effects on the Growth and Development of Zooplankton. . .. .. .. .. .. D. The Effects on the Fecundity of Zooplankton .. E. The Effects on the Phototactic Response of Zooplankton .. *. .. .. .. .. F. The Effects on the Swimming Activity of Zooplankton .. .. .. .. .. .. G . The Combined Effects of Heavy Metals and Additional Environmental Stress upon Zooplankton

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Studies of the Toxic Effects of Heavy Metals upon Natural Populations of Zooplankton in Large Volume Sea Water Enclosures . . .. .. 457

IX. Heavy Metal Concentrations in Natural Populations of Marine Zooplankton .. .. .. . . 460

X. Conclusions

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XI. Acknowledgements References . . Appendix1 . . Appendix I1 . . Appendix 111.. Taxonomic Index .. Subject Index .. XII.

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Adv. mar. Biol., Vol. 16. 1978 pp. 1-231.

THE BIOLOGY OF PSEUDOCALANUS CHRISTOPHER J. CORKETTand IANA. MCLAREN Dalhousie University, Halifax, Nova Xcotia, Canada I. Introduction

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CHRISTOPHER J. CORKETT AND IAN A. MCLAREN

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Reproduction .. .. A. SexRatio .. .. .. .. .. .. B. Oogenesis and Egg Laying . . .. .. .. C. Sperm and Spermatophore Production . . .. D. Mating . . .. .. . . .. .. . . E. Reproductive Rate .. .. .. .. F. Retrospects and Prospects . . .. .. .. Development and Growth . . .. . . .. .. A. Embryonic Development Rate .. .. .. R. Hatching .. .. .. .. .. .. C. Development Rate of Nauplii and Copepodids .. D. Longevity of Adults . . .. .. .. .. E. Body Size .. .. .. .. .. .. F. Body Composition and Weights .. .. G. Oil Storage .. .. .. .. .. .. H. Growth Rates . . .. .. .. .. .. I. Rate of Production of Egg Matter . . .. .. J. The ‘‘ Balance Equation ” and Growth Efficiencies .. K. Retrospects and Prospects .. .. .. .. Life Cycles in Nature .. .. .. .. A. General Features, Terminology and Approaches . . B. Representative Life Cycles . . .. .. .. .. .. .. C. Retrospects and Prospects .. .. .. Vertical Migration . . .. .. .. .. A. Ontogenetic Migrations . . .. .. .. .. B. Seasonal Migrations . . .. .. .. C. Die1 Migrations .. .. .. D. Retrospects and Prospects . . .. . . .. I .

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Production .. .. .. A. General Methods .. B. Production Estimates C. Retrospects and Prospects Parasites .. .. .. A. Dinoflagellates . . .. B. Gregarines .. . . C. Trematodes .. .. D. Nematodes .. .. E . Crustaceans .. .. F. Retrospects and Prospects Role A. B. C. D.

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in the Food Web .. . . Effect on Phytoplankton .. Predators .. .. .. Significance in the Food Web. . .. Retrospects and Prospects

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I. INTRODUCTION Over forty years ago, at a conference sponsored by the National Research Council of Canada, Russell (1934) put our subject into context: “ intensive study of the plankton in northern waters . . . supplemented

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by recent observations on the food of plankton-feeding fish have all pointed to the economic importance of a few species only. I n first rank can be placed Calanus Jinmarchicus, Temora longicornis, and Pseudocalanus elongatus . . , ” These three genera have all been extensively studied since, and Calanus has been admirably ‘(booked ” (Marshall and Orr, 1955). Perhaps because of its relatively large size, Calanus has been most favoured as an experimental animal and is much the best known copepod in a number of ways. Our knowledge of Pseudocalanus is somewhat complementary to that of Calanus. Out of an awareness, expressed even in the earliest copepod literature, of the extreme variability of size of PseudocaZanus in nature, has grown a rather precise set of (‘rules ” concerning its development, growth, and reproductive rates. Perhaps it can also be said that there has been more concern with the mean response to environmental variables in studies of Calanus and more interest in individual variation in studies of Pseudocalanus. The reader should be aware that we have generally avoided using papers in the vast copepod literature that make no direct reference to Pseudocalanua. This may disappoint readers who feel that a more complete or deeper account might have been inferred from systematic relationships. For example, the swimming of Calanus nauplii has been well described, and there is no reason to suppose that the morphologically very similar nauplii of Pseudocalanus would behave differently. However, since we can find no description of swimming of Pseudoculanus nauplii, we do not cover the subject. We have attempted to be analytical and synthetical where possible in our review, and do not simply summarize the observations and conclusions of other authors. Some readers may feel that on occasion we have selected or even abused the writings of others in the search for patterns and regularities. However, we have reserved our most personal assessments of research on Pseudocalanus for the sections in each subsection that we call ‘(retrospects and prospects ”. Therein we broadly assess what has been done and suggest promising (and unpromising) lines for future investigation. Some of our suggestions for future research may seem a little vague ; perhaps they have to be since real discovery is by nature unpredictable.

11. SYSTEMATICS A. Nomenclature 1. The Genus

The Genus was established by Boeck (1864) with the name Clausia, in honour of the late C. Claus. Later Boeck (1872) discovered that the

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name Glausia had been preoccupied by a parasitic copepod and therefore substituted the name Glausia with the new name Pseudocalanus. 2. Described species

(a) Pseudocalanus minutus (Kreryer, 1845) The first description of a species of the genus was the publication of a plate by Kreryer (1842-45), on which the animal was given the binomen Calanus minutus. No description of the plate was pubIished a t the same time, but since the plate was published prior to 1931 the plate and accompanying binomen are sufficient to describe a new species (I.C.Z.N.,Art. 16, a, vii). The original drawing is reproduced in Fig. 1 and is clearly a male copepodid V (see p. 30, Table I), although

FIQ. 1 . Calanus minutus Kreyer, 1845, the type species of Pseudocalanus. A male copepodid V. ( x 2.6 from original plate 41 in Kreyer, 1842-46.)

the diagram shows five thoracic segments and not the usual four. K r ~ y e r(1848) did publish, separate from the plate, a description of a male copepodid V of Calanus minutus in which he described the fifth thoracic segment as being rudimentary and free on its lateral and ventral sides. This evidence suggests that the fourth and fifth thoracic segments were incompletely fused or that the suture line of the fusion was still visible. This is not uncommon in Pseudocalanus and With (1915) illustrated copepodids V of both sexes showing small fifth thoracic segments. A problem arises since the date of publication of the binomen Calanus minutus is the date of publication of Kreryer’s plate, and we have been unable to obtain this exact date. It is known that the date must have been during or before 1845, when the last plates of this

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work were published (Sherborn and Woodward, 1901), and the date 1845 can therefore be used after the binomen (I.C.Z.N., Art. 21, f ) . According to de la Roquette (1842, p. 446), publication of the first plates had begun by 1842. We, therefore, cite both dates in our references except in purely nomenclatorial citations, K r ~ y e rpreserved some specimens which were examined by With (1915), who described them as “ belonging all to the penultimate stage (18 29) ”, presumably meaning one male copepodid V and two female copepodids V. However, Dr B. Frost (personal communication) has recently examined the same material and reports that it consists of three female copepodids V and one male copepodid IV. This appears t o exclude the possibility that the holotype is extant. I n view of other taxonomic problems to be documented below, great care should be taken in any future designation of a neotype.

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(b) Pseudocalanus elongatus (Boeck, 1864) P. elongatus was first given the binomen Clausia elongata by Boeck (1864) in a short description of adult males and females, with the observation that females were common and males rare in Christiana (Oslo) Fjord. Boeck made no reference to the earlier publications of K r ~ y e r(1842-45, 1848).

(c) Pseudocalanus clausii (Brady, 1865) Specimens of this species were originally found by Brady (1863) in the North Sea and erroneously ascribed by him to a quite different genus and species, Phadnna spinifera. Later Brady (1865) gave his specimens the new binomen Calanus Clausii, after the carcinologist C. Claus. (d) Pseudocalanus acuspes (Giesbrecht, 1 881) This species was originally described by Giesbrecht as Lucullus n. gen. acuspes, from the Bay of Kiel, and later given a very thorough description with excellent illustrations, by Giesbrecht (1882). (e) Pseudocalanus major G. 0. Sars, 1900 This species was described by Sars (1900) as “ so very resembling the type species [by this he meant P. elongatus] that I should have been very much inclined to regard it as only a large variety if both forms were not found together in the very same samples, without exhibiting any transitions ”. Sars (1900) did not refer to the publications of Krayer (1842-45, 1848), but does refer to Boeck (1864) and, implicitly, Boeck (1872),

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so that clearly he assumed that prior to his work the genus contained only P. elongatus (Boeck, 1864).

(f) Pseudocalanus gracilis G. 0. Sars, 1903 The classic work of Sars (1903) contains a description and figures of P. gracilis in the supplement at the end of the volume. He described the females of P. gracilis as being more slender than those of P. elongatus, as having a more conspicuously projecting frontal region and as having longer and narrower caudal rami. When females were placed on their side, the flexed first antenna was said to reach the end of the third urosome segment in P . gracilis, whereas in P . elongatus the first antenna reached only to the end of the genital segment. The male of P. gracilis was said by Sars ( 1 903) to resemble that of P. elongatus, the only distinction between them being the longer first antenna of the former. 3. Subsequent delimitations of described species

Pseudocalanus has been referred to under a variety of species names in the subsequent literature. Clearly the designation of at least some of the species has been less than satisfactory. We are concerned here with those papers that have attempted to clarify the status and characters of species. Much of the difficulty in subsequent work on the nomenclature of Pseudocalanus comes from the fact that Boeck, Brady, Giesbrecht, and G. 0. Sars did not mention the work of Krrayer in relation to the genus Pseudocalanus. Brady (1878) synonymizes his Calanus Clausii, 1865, with Pseudocalanus elongatus (Boeck, 1864). Giesbrecht (1882, addendum p. 167) admits the synonymy of Lucullus acuspes Giesbrecht, 1881, with Pseudocalanus elongatus (Boeck, 1864) and P. clausii (Brady, 1865). Giesbrecht (1882) says that he had not previously been aware of the identity of the species he described due to the poor original accounts given by Boeck and Brady. Giesbrecht also lists in his bibliography Kraryer’s (1848) text description of P. minutus, but not Krayer’s (1842-45) plate. Giesbrecht was thus clearly aware of Krrayer’s work, but probably did not consider the description to be detailed enough to be worthy of comments in connection with the genus Pseudocalanus. It seems inconceivable that Sars did not know of the work of his compatriot, H. Kraryer, but since Kraryer described an immature specimen, Sars may not have viewed it as Pseudocalanus. Clearly the species name minutus is available for a species of Pseudocalanus, and

THE BIOLOGY OF PSEUDOGALANUS

7

the question arises: is the form that Krayer described synonymous with P. elongatus (Boeck),P. major, G. 0. Sam, or P. gracilis, G. 0.Saw? With (1915) considered this question in detail and examined what he referred to as “Kraryer’s original specimens”, and was of the opinion that the three species described by Boeck and G. 0. Sars were synonymous, since he found transition specimens in shape of head, length of first antenna, and size. With did, however, state that Krayer’s specimens were in shape of the head most like P. gracilis, and were of middle size ’,. With (1915) therefore recognized only one species: Pseudocalanus minutus (Krcryer). Wiborg (1954) considered that G. 0. Sars was right in establishing three species and made use of the observations by With (1915) on Krcryer’s “ original specimens ” (see above) to designate P. gracilis as a synonym of P. minutus. He retained P. elongatus as a separate species and expressed some doubt about P. major, which he thought “may be an independent species or a large-sized P. elongatus”. He noted that P. minutus is normally larger than P. elongatus, but felt able to distinguish the two in samples from Norway, even when size showed considerable overlap, on the basis of body shape and length of second antennae. Although Brodskii (1948) indicated that two kinds of Pseudocalanus, differing in robustness of body, might be found in the Sea of Japan, he was content to follow With’s (1915) judgment of Sars’ species and to refer all his material to P. minutus. Later Brodskii (1950), in his major monograph on Calanoida of Soviet Far Eastern Seas and the Polar Basin, recognized three species : P. elongatus, P. major, and P. gracilis. In doing so he added to Sars’ (1900, 1903) criteria for separating the species, using relative lengths of the urosomes of adult females and the proportions of segments of the fifth legs of the adult males. However, in the synonomy of P. elongatus, Brodskii (1950) quotes Kraryer’s binomen, Calanus minutus, so that his three species should have been given as P. minutus, P. major, and P. gmcilis, according to the Law of Priority. Parran and Vervoort (1951) recognized three ‘‘ forms ” in one single species : Pseudocalanus minutus elongatus, P . minutus major, and P. minutus gracilis. Today, however, these “ forms ” should be considered as subspecies (I.C.Z.N., Art. 45, d, i, and Art. 45, e, i) and one of the three subspecies should be a nominate subspecies and have the same name as the species, i.e. Pseudocalnnms minutus minutus (I.C.Z.N., Art. 47, a). Fontaine (1955) synonymized all the described species under Pseudocalanus minutus (Krayer) and attributed size variations (some(‘

8

CHRISTOPHER J. CORKETT AND

IAN A. MCLAREN

times continuous, sometimes polymodal) in her material from northern Canada t o environmental influences. Kamshilov (1961) stressed the very great variation in size with no evidence of polymodalism, of Pseudocalanus in the White and Barents Seas and showed that the coefficient of variation (standard deviation/ mean) of size in his samples was twice that of Calanus (species not given). Furthermore, the ratio of cephalothorax length to length of urosome, which had been used (Brodskii, 1950) t o separate supposed species, had a continuous, unimodal distribution. He concluded that all his material should be referred to P. elongatus. However, here again, if this is done the name P. minutus has priority. Grice (1 962) stated that '' Pseudocalanus minutus was represented by two size groups ( P . minutus f. elongatus and f. gracilis) " in his collections from the Arctic Basin, but he did not routinely discriminate them. Cairns (1967) in his samples from the Canadian Arctic examined one criterion that had been used to define kinds of Pseudocalanus: there appeared t o be two groups of females, not completely separated by size, but showing a possible discontinuity, on a graph, of urosome length against cephalothorax length. The regression coefficients of urosome length on cephalothorax length were 0.520 for the small and 0.376 for the large ones. Within the wide continuous size range (about 1.0-1-4 mm in cephalothorax length) of the large animals, the length of the urosome relative to the cephalothorax decreased with size. Cairns did not attempt to refer his specimens to any species of the genus Pseudocalanus, and suggested that the large and small females might represent reproductively isolated forms or have resulted from different environmental conditions. Lacroix and Filteau (1971) believed that two " forms (per Farran and Vervoort, 1951), the small elongatus and the large major of Pseudocalanus minutus occur in the Baie-des-Chaleurs, off the Gulf of St. Lawrence. Adult females of the large form (cephalothorax mean 1.4 mm) were common in spring, but the small form (- 0.9-1.0 mm) predominated in spring and summer. The large form predominated as copepodid V (1.2-1.3 mm) in the deep, cooler waters throughout the summer. Enough examples have been given to indicate that problems of nomenclature and of delimitation of named species pervade the literature on Pseudocalanus. A formal systematic revision would involve the examination of much new material. Since we cannot do this here, we follow the practice of McLaren (1965) and refer only t o the generic name throughout this review on the biology of Pseudo))

-


9

calanus. This is not t o deny the certainty that different kinds of Pseudocalanus exist, but that these kinds may be difficult t o accommodate either in the formalities of nomenclature or in prevailing concepts of species (see p. 11).

B.

"

Physiological '' species

Even if morphological differences among geographically isolated populations of Pseudocalanus are elusive, physiological differences occur that may signify reproductive isolation (cf. Carrillo B.-G. et al., 1974).

McLaren (1965, 1966) showed that the temperature response of adult female size and of embryonic development rate varied geographically. For example, extrapolation of the size-temperature relationship (Fig. 26) for Loch Striven, Scotland, to 0°C suggeststhat at this temperature (normal for a female from the Canadian Arctic) a monster larger than any known species of copepod would result. Of course this is hypothetical, since development would simply not take place a t this low temperature, and furthermore the size-temperature relationship may break down a t excessively low temperatures (see p. 122). Clearly, however, there are inherent differences between populations in these two parts of the world. Regional differences in development rate, for example, expressed as time to reach various stages (Fig. 25), are less pronounced. C. Va&ations in DNA content I n recent years a novel source of variations within and between populations of Pseudocalanus has been discovered. McLaren (1 965) described a large form of Pseudocalanus that coexists with a more abundant small form in Ogac Lake, a partially landlocked fiord on Baffin Island, northern Canada. The small form was believed t o be the same as the widespread Pseudoealanus of waters outside the fiord, the size of which had been reduced inside the fiord by elevated temperatures (see p. 117, Fig. 26). I n the large form embryonic duration (McLaren, 1966; see also p. 103, Fig. 22) and development times of older stages (McLaren, 1965 ; see also p. 113) are longer than those of the small form. McLaren (1965) speculated that the large form of Pseudocalanus was a polyploid. However, later work (McLaren et al., 1966) showed that both forms of Pseudocalanus from Ogac Lake contained the same chromosome number (n = IS), but that chromosomes in undivided

10

CIIRISTOPHER J. CORKETT AND IAN A. MCLAREN

eggs of the large form were much larger than those of the small form. The DNA content of nuclei a t the 32-cell stage was about seven times greater in the large form. This was attributed to polyteny, although today the whole question of repetitive or otherwise increased amounts of DNA tends t o be discussed in different terms. Woods (1969) added more information, demonstrating that the large forms in Ogac Lake and also in another landlocked fiord, Winton Bay on Baffin Island, were morphologically very similar, except in size, to the small forms and to the phenotypically larger forms of the cold seas outside. Female cephalothorax lengths of the large forms were respectively (means f S.E.) 1.09 f 0.040 mm and 1-16 f 0.044mm in Ogac Lake and Winton Bay, whereas the small forms were 0.85 & 0.009 mm and 0.84 f 0.007 mm. The small form is larger in cold waters outside the lakes, but its eggs are always smaller than those of the large form (see Table XVIII, and McLaren, 1965, his Fig. 1). Woods speculates on the adaptive meaning of these large forms. Noting that the effect of increased DNA per nucleus is probably an increase in cell size and a decrease in cell division rate, she suggests that this restores the normal size and cycle for an arctic population forced to exist in abnormally warm environments. Indeed, in Ogac Lake, McLaren (1969) showed that the small form may " waste '' much of its reproductive effort, since early broods matured and produced an unsuccessful second generation in summer. Under these conditions, there should be selective pressure for maturation later in the season, which would be thwarted by genetic exchange with the populations from outside the lakes, brought in by periodic high tides. Woods also notes arguments that larger size allows a greater range of food (see also p. 63). The large form during summer does show retarded maturation of the overwintered generation and slow progress of the new generation, compared with the small form (McLaren, 1969 ; Woods, 1969) thus restoring an essentially normal arctic life cycle (see p. 139). The large forms can be viewed as an " instant species ", almost certainly reproductively isolated from the coexisting small forms, in the manner of polyploid species among plants. It may be wondered if such discontinuous DNA variation is partly responsible for some of the sizepolymodalisms in Pseudocalanus noted in the literature. Clearly this raises nomenclatural and systematic problems : how many of the described species are of this sort? Can such variants, morphologically identical to widespread forms except in size, spring up independently among different populations, and should they be classed together on the basis of size? To what extent does such a size change allow rapid morphological divergence to occur!


11

Recently the whole question of DNA variation in Pseudocalanus has become more complex. Hart and McLaren (1978) have shown that there is continuous variation in body size, egg size, and attendant embryonic duration in populations of Pseudocalanus from Halifax, Nova Scotia (p. 105). McLaren (1976b) showed that the size of adult females is strongly heritable (p. 123) and that size of adult females is strongly related to DNA content of somatic nuclei (p. 124). D. Retrospects and prospects What started out as a rather classical nomenclatural muddle has led t o a frontier ” problem in systematics. We feel that some of the nomenclatural confusion has been exacerbated by the attempts (e.g. Brodskii, 1950) to define species limits in terms of size and its correlates that are highly responsive to environmental influences and are also perhaps subjected to strong local differentiation under natural selection. We hope that the nomenclatural and systematic problems in Pseudocalanus will be cleared up by a revision of the genus that takes into account these aspects of variability. Further investigation is clearly needed on the role of quantitative DNA variation at the ecological, evolutionary, and molecular level. The DNA content of nuclei, presumably by mediating cell size and cell division rates (Woods, 1969),may act as a basis for the quantitative inheritance of body size and durations of developmental stages. This genetic basis for maintaining phenotypic diversity may be aided by size-assortative mating (see p. 84). Not only is such a mechanism quite extraordinary but its consequences may defy simple systematic analysis. Consider the possibility, given the strong heritabilities of size together with assortative mating, that disruptive selection could very quickly lead to two reproductively isolated populations where once there was one. Indeed, it is possible that ‘‘ biological species ” (sensu Mayr, 1963) could come and go rather quickly in this widespread genus of copepods. The situation in Pseudocalanus may find its counterpart in other groups of copepods, including the sibling species of Calanus, as mooted by McLaren et al. (1966).

111. DISTRIBUTIONAND ABUNDANCE

A. Geographical distribution 1. General Our survey of the distribution of Pseudocalanus is summarized in Fig. 2. Although well known in broad terms, its precise limits are

12


obscure in some places and its reported presence in some localities is dubious or in need of confirmation. Sewell (1948) collates virtually all earlier references to distributions of marine copepods, and it remains largely to update and correct his assessments. Sewell, like most previous and subsequent reviewers, concludes that Pseudocalanus is basically a neritic, northern genus, found in arctic seas extending southward along cooler coasts, and even beyond in deep waters.

FIQ.2 . World distribution of Pseudocnlnnus. Open-ocean boundaries in Atlantic after Edinburgh Oceanographic Laboratory (1973) and in Pacific after Omori (1965). Other sources in text. We consider this t,o represent the distribution of normally reproducing populations, although there are deep-wster records outside these limits, and animals may not commonly breed in the mid-Arctic Ocean.

I n considering the limits of the range of Pseudocalanus, Sewell cites records from as far south as Chesapeake Bay in the eastern U.S.A., from the North Atlantic Drift south of Iceland, from European waters as far south as Portugal, and from the Mediterranean. I n the North Pacific, he records it south t o Japan and Vancouver Island. I n addition, some anomalous records can be gleaned from Sewell’s review, and these must be examined.


13

Sewell himself notes that supposed occurrences in the northern Gulf of Suez of Pseudocalanus and other North Atlantic forms are open to doubt. The samples in which these copepods occurred were from seawater taps draining tanks that were probably filled prior to passage of the ship through the Suez Canal. Sewell (p. 497) implies that Pseudocalanus reaches subantarctic or even antarctic waters through the deep Atlantic, but does not document this statement with references. Although he later (p. 499) lists the genus for deep Atlantic waters, he does not include it in his list (p. 513) of arctic or North Atlantic forms recorded from subantarctic or antarctic waters. Nor does it occur in the most extensive modern review of copepods of these waters (Vervoort, 1965). Sewell’s report of Pseudocalanus off western South America is based on the work of Wilson (1942). This very large work and a subsequent one by Wilson (1950) extended the distribution of Pseudocalanus over vast areas of the tropical and subtropical Pacific and Atlantic, far outside previously accepted limits. Some authors have corrected or expressed doubts about other records in Wilson’s (1942, 1950) lists. His records of Pseudocalanus seem to have been evaluated simply by being ignored in a number of subsequent publications on copepods of the waters surveyed by him. Contrary to Wilson’s claims, Pseudocalanus has not been found in extensive sampling of the California Current (Fleminger, 1967), off western South America (Bjornberg, 1973), in near-surface waters of the southern North Atlantic (Deevey, 1971), or in the tropical Pacific (Grice, 1961 ; Vinogradov and Voronina, 1963). A number of papers subsequent to Sewell (1948) give a more refined view of the distribution of Pseudocalanus. We cannot possibly consider more than a fraction of these, and confine our review to those that give a wide perspective or a more accurate assessment of the margins of its range.

2. Arctic Basin

Pseudocalanus is common in coastal arctic waters and has been recorded from many parts of the Arctic Ocean proper, generally in the upper 300 m (e.g. Dunbar and Harding, 1968). It is, however, evidently scarce and patchy in the more central parts of the basin, and has not been found in some surveys (e.g. Minoda, 1967). Harding (1966) found no subadults in his samples from the basin, and concludes that Pseudocalanus there is a n expatriate from surrounding neritic waters, especially the Chukchi Sea, where it is common (Grice, 1962).

14


3. North Atlantic and adjacent waters An excellent overview of North Atlantic distributions of adult Pseudocalanus has been constructed from the Continuous Plankton Recorder surveys (Fig. 2 18 in Edinburgh Oceanographic Laboratory, 1973). The marked abundance in upper waters off eastern Canada and western Europe contrasts with its general scarcity in the open Atlantic, where scattered records are shown southward to about 41"N. I n the inshore waters of eastern North America, Pseudocalanus has been noted as far south as Beaufort, North Carolina, a t latitude 34'40" (Pearse, 1936). However, this and a number of other identifications made by Wilson for Pearse's study must remain suspect, especially one reputed finding of Pseudocalanus innear-fresh water. Bowman (1971) states that Pseudocalanus does not occur south of Cape Hatteras, a zoogeographical boundary for many northern forms. It penetrates the Gulf of St. Lawrence to at least 60"20'W (Prdfontaine and Brunel, 1962). I n the eastern North Atlantic it can be common in the Bay of Biscay and off northwest Spain, but it is not listed for the waters off southwest Portugal (Vives, 1970). I t s distribution in the Baltic region has been recently summarized by Ackefors (1969a) and Arndt and Stein (1973). It penetrates the Gulfs of Bothnia and Finland in small numbers, but is evidently not found in shallow waters even in the northern extremities of the Baltic proper (Eriksson, 1973b).

4. Nediterranean and Black Xeas I n spite of the earlier accounts reviewed by Sewell (1948) the status of Pseudocalanus in the Mediterranean is uncertain a t best. Rose (in Trdgouboff and Rose, 1957) includes the genus in his taxonomic keys to Mediterranean copepods, but makes no mention of its occurrence in his text. Surveys and biological studies of copepods in the western Mediterranean by Gaudy (1962) and Vives (1967) fail to mention it or note its absence specifically. If it occurs a t all in the western Mediterranean, it must be as a rare expatriate from the Atlantic. I n the eastern Mediterranean, the thorough survey by Kimor and Wood (1975) failed to report it. However, Pseudocalanus does occur in the Adriatic. VuEeti6 (1957) states that " sporadic individuals '' occur all over the Adriatic, but Hure and Scotto di Carlo (1968, 1969) found it only in northern parts, where it was most common in May, although never dominant numerically. Recent work (Dr J. Hure, personal communication)

THE BIOLOGY O F PSEUDOCALANUS

15

indicates that it extends in some numbers down the coast of Italy, but not evidently beyond the Strait of Otranto. Pseudocalanus is also well known as a disjunct population in the Black Sea. Its distribution there is detailed by Afrikova (1975)) who maps its abundance by season and depth. 5. North Paci$c and adjacent waters

The best modern overview of the southern limits of distribution of PseudocaZanus in the North Pacific is supplied by Omori (1965, his Fig. 4). It is shown as most abundant in shallow waters of the Bering Sea and near the Aleutians, relatively abundant near the coasts of Hokkaido and southern British Columbia, less so in the open ocean in between. It was absent from some samples along the 43"N parallel between about 170"E and 175"W. On the Pacific coast of Japan, Pseudocalanus seems to be one of a number of boreal species that is not found west of the Bonin Ridge running south from the Tokyo region, although it occurs in Sagami Bay at the landward end of the ridge (Furuhashi, 1961). Furuhashi's southernmost records offshore are at 38"OO'N 145"23'E and (Furuhashi, 1966) a t 40"03'N 152'01'N. I n the Sea of Japan, Pseudocalanus occurs in the extreme southeast (Morioka, 1973) and off the coast of Korea (Mori, 1937). On the American coast, the southernmost reliable record appears to be at 38"52'N, just off the coast of northern California (Davis, 1949). 6 . Expatriates in deep water

The geographical limits outlined above can be considerably extended (and probably will continue to be) by scattered records from deep waters. These represent individuals carried from waters farther north, unable to rise to warmer surface waters, and presumably incapable of sustaining populations indefinitely. Ignoring problematical earlier records in Sewell (1948),we find records in deep water of two individuals off the Azores (Roe, 1972)) seven females a t 31"31'N 64"OO'W near Bermuda (Harding, 1972), and a southernmost recorded specimen a t 29'58% 22'58'W (Grice and Hulsemann, 1965). 7. Distribution in relation to water masses Copepod distribution is frequently discussed in relation to water masses or marine biogeographic zones. Pseudocalanus often figures as one of many " indicator " forms in such studies, only a few of which will be reviewed here. In the North Atlantic (e.g., Edinburgh Oceanographic Laboratory,

16


1973) Pseudocalanus is found in pure Atlantic as well as mixed arctic and Atlantic (subarctic, sensu Dunbar, 1947) waters. A sophisticated approach is found in Colebrook (1964), who used principal component analysis to group and classify copepods of the North Sea and North Atlantic. This results in an objective designation of " Para-Pseudocalanus " as a member of the intermediate group with respect to northsouth and neritic-oceanic gradients. Unfortunately, the lumping of Pseudocalanus with Paracalanus, a more southern form, makes the designation less useful. The southern limits of Pseudocalanus at about 42"N in the open waters of the western North Pacific (Omori, 1965) coincides quite well with the subarctic boundary, which is defined in strictly hydrographic terms (Dodimead et al., 1963). Pseudocalanus occurs in and is used in the definition of the North Pacijic temperate region of Brodskii (1956). 8. Distribution uith respect to distance offshore

Pseudocalanus is generally reckoned as a neritic copepod. This is very evident in maps of late-summer distribution in the Barents Sea (Zelikman, 1966, his Fig. 7), and on a grand scale in the North Atlantic surveys of the Continuous Plankton Recorder (Figs. 217, 218, in Edinburgh Oceanographic Laboratory, 1973). All the areas with the highest abundance of Pseudocalanus are within about 400 km of land. Nevertheless, Pseudocalanus does occur abundantly further offshore in northern extensions of the North Atlantic (Ostvedt, 1955). Motoda and Minoda (1974) refer to it as " typically oceanic " as opposed t o neritic in the Bering Sea. Possibly this is a matter of definition. It is at times most abundant in the central region of the Black Sea (Afrikova, 1975).

On a smaller scale, a number of authors have stated that Pseudocalanus is generally commoner away from the immediate vicinity of the coast. For example, Evans (1973) found that Pseudocalanus in 1969 was four times as common ten miles off the Northumberland coast as it was two miles offshore. However, Petipa et al. (1963) in a series of transects off the coast of the northern Black Sea found that regions of concentration varied, sometimes near shore and sometimes farther out. Furthermore, it may tend to become more abundant in enclosed bays than in the open waters outside. This is shown most clearly in a series of samples taken in summer 1960-62 from the Baie-des-Chaleurs, in the Gulf of St. Lawrence (Lacroix and Filteau, 1971). We conclude that Pseudocalanus is indeed predominantly a coastal form, but that the neritic-oceanic gradient is an unrefined one, allowing for many exceptions.

17

THE BIOLOGY OB P,SEUDOCALAhrUS

B. Abundance 1. General abundance

Pseudocalanus is not only widespread in northern seas, but is often said to be the most abundant form in many surveys of these waters. Perhaps the most impressive testimony to its numerical importance is from the long-term surveys with the Continuous Plankton Recorder around the British Isles (Fig. 3). Along with Calanus jnmarchicus (including C . helgolandicus, no doubt), Pseudocalanus (with a small admixture of Paracalanus) is found in virtually all the sampled areas. It is also numerically the most abundant form per sample. It ispossible, in our opinion, that Pseudocalanus is the most abundant metazoan in the world. 2.

'' Patches " and mms occurrences

Pseudocalanus may be found in '' patches ", many kilometres in diameter, that may be treated as dynamical and productive units (e.g. Thompson, 1976). This may be of considerable significance to A 1.6 0.4 02

B 0.01

0

0.05

0.1

0.5

I

5OloO 5

5

Pam-Reudacalanus rpp. Acartla a m .

Cantrapagas hamatus

Euchaob habas

Houromamma rabusta Pareuchadta narvefica Rhincalanus nasutus Plauramamma banalis Ploummamma adominah8 Phuramamma gmcilis Labidocero wllastoni Sapphirina app. Candacia armata Euchaeta acuta hfstridia /onfu Calanus minor Astidius armatus Anoma/acwa patsrsoni Calanus amcilis Contrapagas bmdy!'

i I

Plsummamma xiobias

).6 0.4 0.2

0

0.01

0.1 0.05

0.5

'

i 5

FIQ.3. Histograms of A, the proportion of sampled area (vicinity of British Isles) in which the species occurred, and B, the abundance of each species during 1948-66, as revealed by the Continuous Plankton Recorder Survey. (From Colebrook el al., 1961.) A.M.B.-15

3

18

CHRISTOPHER J. CORRETT AND IAN A. MCLAREN

fisheries (seep. 201). Fish (1936) interpreted such concentrations around the Gulf of Maine as " stocks " in the manner of fishery science. He felt that breeding occurred first in offshore areas and later inshore, where local concentrations were sustained by hydrographic circumstances from areas of higher production offshore. The number of stations involved makes some of his isopleths of abundance open to question. Soviet researchers have shown particular interest in such concentrations. Zelikman (1961) found mass occurrences of over 1oQ individuals per m3 near the mouth of the White Sea in midsummer 1956. Meshcheryakova (1964) describes less dense concentrations of Pseudocalanus and other copepods in the eastern Bering Sea. Explanations for this are vague, but a lack of coincidence with concentrations of Calanus is of interest. Kamshilov (1961) describes abrupt increases in abundance at boundaries of sharp temperature changes in surface waters on transects through the Barents and White Seas, ascribed to concentration by hydrographic forces. Zelickman and Golovkin (1972) agree that hydrographic forces are responsible for concentrations of Pseudocalanus and other zooplankters near bird colonies on Novaya Zemlya, but stress that the concentration is due to productivity, not " mechanical " consequences of hydrography. C. Temporal variations 1. Seasonality of occurrence Throughout its range, Pseudocalanus shows seasonal fluctuations in abundance in relation to primary production and other factors. Where life cycles are annual, it is clear that a numerical peak must occur during the season of reproduction. But even where more or less continuous generations occur, there may be marked seasonality in abundance. Some authors have attempted to discern large-scale patterns in this seasonality. Pavshtiks and Timokhina (1972) summarized the annual cycle of Pseudocalanus in the Norwegian Sea, showing that the summer peak of abundance occurs in late June in Atlantic waters, mid-July in mixed waters, and late July in the East Icelandic Current. Colebrook (1969) has systematized data from surveys with the Continuous Plankton Recorder by using the centre of gravity on the time axis of the area included under seasonal curves of abundance. Geographical variation in this statistic for Pseudocalanw (his Fig. 8, probably including some Paracalanus, although this was not stated) shows a reasonable pattern of early peaks in southern and coastal waters


19

and later ones in northern and oceanic parts. Analysis of covariance shows that seasonality is correlated with temperatnre, but of course causes may be indirect. In the southern parts of its range, Pseudocalanus is a winter-spring form, and may disappear altogether from sampling areas during summer. Since this disappearance seems clearly related to high temperatures, i t is discussed separately (p. 24). 2. Year-to-year and long-term changes in abundance The whole subject of secular changes in the marine environment is of profound importance (Russell et al., 1971) and Pseudocalanus has figured in some of the discussions. 155C 965

-n E

oc

0

e"

594

36C 212

P .x 119 61

23

I

u +0 50 Ye0 r

FIG.4. Average numbers, per sample of 20 miles, o f Pseudooalanua (including Paracalanua) from the east-central North Sea in monthly periods from January 1948 to December 1972, taken by the Continuous Plankton Recorder. (From Glover et al., 1974.)

Pavshtiks and Timokhina (1972) tabulate a five-fold variation in production of Pseudocalanus (p. 187) in the Norwegian Sea in seven seasons between 1959 and 1969. This is vaguely related by them to the temperature regime and the timing of the spring maxima. Lacroix and Filteau (1971) found that Pseudocalanus averaged two and a half times as common in the Baie-des-Chaleurs, Canada, in 1962 compared with 1960. They suggest that a warm hydrographic

20


winter promoted strong vertical mixing and high production in the subsequent summer season in 1962. Meshcheryakova (1964) describes a roughly two-fold difference in abundance of Pseudocalanus and other forms in the eastern Bering Sea in 1958 and 1959. I n the former year, an earlier warming led to a strong diatom bloom in summer, which in turn encouraged strong representation of the copepods. Peterson and Miller (1975) found a marked reduction in abundance of Pseudocalanus off the coast of Oregon in 1971, evidently associated with reduced upwelling and warmer water than usual. I n the Black Sea, annual production of Pseudocalanus (p. 183) varied almost two and a half fold during the period 1960-66 (Greze et al., 1968.) The remarkable summary of long-term changes in the east-central North Sea by Glover et al. (1974) is summarized on Fig. 4 (whichincludes Paracalanus; G. A. Robinson, personal communication). These authors conclude that the long-term reduction in mean annual abundance is related to retardation in the time of the spring phytoplankton bloom, from late March to mid-April in the Atlantic off the British Isles, and from mid-March to mid-April in the North Sea. This has led to a reduced length in season of sustained production by the zooplankton from slightly more than seven months in the fifties to about six months in the early seventies. Underlying the biological trends is said to be a climatic trend involving the withdrawal of Atlantic influence from the North Sea,

D. Vertical distribution Pseudocalanus is generally found in the upper layers of the sea, although individuals have been taken as deep as 4 000-5 000 m (Grice and Hulsemann, 1965). Here we first outline briefly the main features of vertical distribution in the open sea, where the bottom may not set the deepest penetration. Then we consider inshore waters, where details of vertical distributions with respect to phydcal, chemical, and biological factors may be more evident than in the open sea. There is of course a dynamical aspect to this subject, which is dealt with at length elsewhere (Section XII). We refer throughout this section to daytime distributions of Pseudocalanus. The broad capabilities of Pseudocalanus are evident in vertical samples from deep, oceanic waters in various regions. I n the Norwegian Sea, most individuals occur above 50 m in spring, but below 1 000 m at other times of the year (Ostvedt, 1965). I n the southern Bering Sea,

TEE BIOLOGY OF PSEUDOCALANUS

21

&oda (1971) found that most animals were between 0 and 50 m in a series of samples taken from 28 May to 19 June 1962. Only a tiny fraction (average 0.1%) occurred in the deepest hauls (between 707 and 1 350 m). Over the deep Kuril-Kamchatka trench, 98% of the biomass of Pseudocalanus occurs in the upper 50 m, according to Arashkevich (1969). Dunbar and Harding (1968) found that almost all individuals were taken between 50 and 300 m under the ice of the Arctic Ocean ; at these depths, largely unmixed arctic waters are found. I n offshore regions of the Black Sea, which is of course anoxic in deeper waters, Pseudocalanus is found down to at least 200 m but is generally more common above 50 m (Afrikova, 1975). We conclude from these studies that Pseudocalanus is capable of living in very deep waters (unless prevented by lethal conditions, as in the Black Sea), but may only be evident if seasonal samples are taken. Studies of vertical distributions in shallower, inshore waters give more insights into the physical, chemical, and biological factors, that might control such distributions. Minoda and Osawa (1967) found that Pseudocalanus and other small copepods were concentrated by day at depths of the sonic scattering layers in the Okhotsk Sea in summer, 1963, and this coincided with the thermocline at the time. I n the Landsort Deep of the Baltic, Pseudocalanus was most abundant at 50-100 m, just below a thermal minimum, absent above 30 m, where temperature began to rise sharply, but present even down to 300-400 m, in spite of virtual absence of oxygen (Ackefors, 1966). At a shallower station south of Stockholm, Pseudocalanus always occurred below the thermocline at 20-30 m in spring and autumn, although a few were found near the surface in unstratified waters in winter (Ackefors, 1969b) ; salinities were low but varied only slightly with depth. I n a semi-landlocked bay on the island of Split, Yugoslavia (VuEetiE, 1961), Pseudocalanus occurred at the surface only in January and November, when the water column was almost isothermal and 900, carnivorous copepods. Schnack (1975) found Pseudocalanus females had an E.I. of 365 and they were placed with Paracalanus parvus females (E.I. of 265) in the first category. Sullivan et al. (1975) examined the teeth on the mandibular blades of eleven species of copepod in detail using a scanning electron microscope. They confirmed the work of Beklemishev (1 954a) that the teeth had siliceous crowns set in a chitinous mandibular blade. They also showed that the right and left blades were not identical. The sharp projections on the teeth of one mandible fit into the grooves on the teeth of the opposite mandible, suggesting a cracking rather than a grinding action. I n the herbivorous copepods such teeth would be well suited for breaking diatoms, and Sullivan et al. (1975) comment that " possession of glass teeth for eating food in glass cases is surely one of the lyrical symmetries of nature ". Based on the work of Beklemishev (1954a),Sullivan et al. (1975) have divided the teeth into three groups. Starting with the ventral edge of the blade and progressing to the dorsal edge these groups are : ventral, central, and dorsal. The right mandibular blade of PseudocaZanus has a single large ventral tooth separated by a diastema from the rest (Fig. 11A). The left mandibular blade of Pseudocalanus was not studied but based on work on other species of copepods, the left blade probably has two ventral teeth into which the single ventral tooth on the right blade would fit. The ventral tooth on the right blade of Pseudocalanus is followed by four central teeth (Fig. 11A) which are followed by three dorsal teeth of a complex nature (Fig. 11B) and Sullivan et al. (1975) suggest that these dorsal teeth can " tightly grip food of a softer nature ". 2. Peeding on large particles Cushing (1955) states :

" I have Been a Psedocalanus take a Biddulphia sinensis almost as big as itself, break it and filter off some of the contents ". This is an important observation because it suggests that, despite evidence given above that Pseudocalanus is basically a

58


continuous filter feeder it is, nevertheless, able to feed by another mechanism, evidently involving selection of larger particles. Gauld (1964) suggests that larger particles are captured by Pseudocalanus as in other copepods, by use of a sweeping movement of the second maxillae. He also pointed out that the second maxilla of Pseudocalanus has at its tip a long stout sets (Fig. 7F) which ‘‘ would be a very effective seizing and holding weapon ”. The maxillipeds may be involved in this feeding process as well since they are known to play an important part in the grasping of food by carnivores such as Euchaeta norvegica (Gauld, 1964) and Oithona similis (Schnack, 1975).

B. Food eaten 1. Xpecies eaten in nature

Pseudocalanus is capable of ingesting a wide variety of food. Corkett (1966) has shown that individuals in the laboratory will take in fine sand and produce faecal pellets and Schnack (1975) finds “ sand ” (fine mineral particles) in guts in nature. Pavlovskaya and Pechen’Finenko (1975) have shown that Pseudocalanus in the laboratory will ingest and assimilate algal detritus, humus particles, and even melanin. These and other such experiments are reviewed later, but they tell us nothing about the food available t o and chosen by animals in nature. Until recently, the gut contents of wild-caught Pseudocalanus had not been extensively studied. Lebour (1922) concluded that diatoms formed the main food, especially Coscinodiscus and Thalassiosira. Flagellates were also thought to be eaten although indistinguishable in the guts. Later, Lebour ( 1 923) found coccoliths in guts, as evidence that coccolithophorids are eaten. Marshall (1949) examined guts of over 100 live Pseudocalanus from off Millport, Scotland, and found that 73 were empty or had indistinguishable remains, 18 had diatoms, 4 had radiolarians, 1 had a flagellate, and 10 had crustacean remains. Although the crustacean remains show that Pseudocalanus can be carnivorous (and we have found that females will eat their own nauplii) the morphological evidence of the previous section and other studies in nature (below) imply that they are overwhelmingly herbivorous. Beklemishev (195413) stresses this, and found only the diatoms Chaetoceros and Thalassiosira in guts of adult females from the Bering Sea. Schnack (1 975) presents a great amount of information on food and feeding of copepods off Kiel Bay, near the mouth of the Baltic. She determined the kinds and amounts of food in guts of adult female Pseudocalanus taken in November and December 1970, and in July,

THE BIOLOGY OB PSEUDOCALAh’US

59

September and October 1971. These contents were compared with food in the water column, sampled by a net with mesh of 54 pm and by plankton pump which sampled particles too small to be caught by the net. She found that the spiny diatoms Chaetoceros spp. were almost uneaten. Xkeletonema costatum was common in the water but scarce in guts, possibly due t o its fragility. I n general, she concludes that Pseudocalanus is a herbivore, that individuals favour small food species, that they remove only a fraction of the range available in the plankton, that they favoured centric over pennate diatoms, and that small forms like Exuviaella baltica and Heterocapsa triquetra were a t times important. These conclusions do not take into account the possibility of local concentrations of food or copepods in the water column (which would complicate conclusions about selection of one sort of food or another), and they are unsupported by statistical analysis. Zagorodnyaya (1974) has produced by far the most detailed assessment of food in guts of Pseudocalanus from samples taken in the Black Sea off Sevastopol in January and March 1973. She identified and tabulated some 50 food species, predominantly diatoms and dinoflagellates, with some chrysophytes. No animal food was found. The three most regular species were the dinoflagellate Exuviaella cordata, the diatom Cyclotella caspia and the chrysophyte Coccolithus huxleyi. Diatoms were selected in excess of their proportionate representation in the water column, and the reverse was generally true of dinoflagellates (depth distributions of copepods and food species were taken into account). However, she concludes that species selection was generally based on size. This and other aspects of Zagorodnyaya’s important work are dealt with elsewhere. Feeding experiments conducted in the laboratory using natural seawater and its contained food give some indication of the food species used in nature, even with the reduced options in time and space. Curl and McLeod (1961) give anecdotal observations on the selective removal of Skeletonema sp. from stored plankton samples by Pseudocalanus and Acartia tonsa. Parsons et al. (1967) also noted use of Xkeletonema in more formal experiments. Geen and Hargrave (1966) found that Pseudocalanus did not eat many of the long-spined Ceratium sp. nor the spiny, chain-forming diatom Chaetoceros, but rather favoured larger flagellates in natural seawater samples. Parsons et al. (1967) also indicated that Pseudocalanus was unable to derive much value from samples of a bloom of Chaetoceros socialis and C. debilis. In contrast, Poulet (1974) observed chains of Chaetoceros sp. being devoured by females kept in unfiltered seawater. A species by species account of the food of Pseudocalanus in nature

60


could in principle become almost endless. A number of the above authors have indicated that size is a chief determinant of suitability of a food species. This subject is dealt with next. 2. Xixe of food

Clearly there must be some lower limit to the size of food particles that can be filtered and some upper limit to the size of organisms that Pseudocalanus can “ handle ”. Observations on the maxilla, show that. the smallest distance between setules on the setae is 3 pm (p. 5 5 ) and individuals can evidently contend with food almost as large as themselves (p. 57). However, much effort has been expended on the search for size-selective feeding within these limits. As shall be seen the evidence for size-selective feeding by filter-feeding animals is by no means conclusive. Evidently the first formal consideration of size-selective feeding by Pseudocalanus was by Hargrave and Geen (1970). They showed that filtration rate was significantly higher for cells about 10 pm in maximum diameter than for cells of about 0.5, 5, and 7 pm (about 12 v. 4-5 ml/cop./day respectively). Their results are marred by being based on experiments with a mixture of C I V and C V of Pseudocalanus and Temora longicornis feeding in water from which particles > 35 pm had been removed by filtration. Zagorodnyaya’s (1974) analysis of gut contents of Pseudocalanus in the Black Sea is especially valuable for its information on several stages of copepodids and on adult females (Table V). Counts and measurements are based on unspecified “ standard methods ”, and unfortunately there is no clear indication in her paper that the percentage values in Table V are for cell numbers or total cell volumes, although

-

TABLEV. PERCENTAGE REPRESENTATION OF DIFFERENT SIZE GROUPS OF UNICELLULAR ALGAEIN THE GUTS OF Pseudocalanus AND IN THE WATER COLUMN. (After Zagorodnyaya, 1974.) Size group

(rm)

< 10 10-20 20-30 30-40 40-50 >50

January

March ~

CIIICIV 43 50 7 -

_ _

59 34 6 1

_ _

CV 38 37 19 1 1

Ad. Q Water 16 38 31 8 5 2

25 41 23 4 3 4

C IIf C I V

~___

50 7 36 7 -

-

53 21 21 3 2

C V 61 16 13 8 1 1

A d . ? Water 54 15 20 8 2 1

14 66 17 1.6 1-4

THE BIOLOGY OF PSE U DOCA LAN U S

61

one can infer the former. Formal statistical analyses of the data as presented in Table V cannot be made, but they support Zagorodynyaya’s conclusions that the copepods consumed mostly cells < 10 pm (which were especially Cyclotella caspia and Coccolithus huxleyi) and that older stages and adults were more competent with larger cells. Extensive studies by Poulet (1973, 1974, 1976, 1977), and Poulet and Chanut (1 975) have advanced the whole subject of grazing by copepods to new levels of sophistication. The recurrent theme in Poulet’s work is size-selective feeding. For each grazing experiment, Poulet placed 50 or 100 lively adult female Pseudocalanus in a liter beaker containing seawater screened through a 160 pm mesh. Duplicate containers filled with screened seawater served as controls. All experiments were carried out for 19-20 h a t temperatures close t o those of the water from which the sampies were removed. The experimental and control samples were analysed with an electronic particle counter set for particles between 1.58 and 114 pm (earlier work) and up t o 144 pm (later experiments). This produced data on concentrations (volume in p.p.m.) versus particle diameter (spherical equivalent). Poulet (1973) studied grazing in samples from 5 m a t five stations in a transect from the head of Bedford Basin, a highly enriched environment, to beyond the entrance of Halifax Harbour, Nova Xcotia. He also used a vertical series of samples from five depths between 0-60 m from the middle of Bedford Basin. From his analyses of the changes in the concentration-size distribution of particles after grazing, he concluded that the copepods were well able t o consume particles from 1.58-114 pm (although not readily if < 4 pm). Poulet (1973) found, however, that grazing occurred on smaller particles (< 25 pm) when these were more than about half of the total concentration and occurred on larger particles when these were equally concentrated as or more concentrated than the smalIer ones. That is, “ the heterogeneity of particle distribution in time and space can be overcome by copepods by shifting their grazing pressure from one size of food t o another ”. Poulet (1974) expanded his work to a two-year study using water samples from 5 m in Bedford Basin. He described the seasonal cycles of particles in six size categories : 1.6-3-6 pm, 4-0-9-0 pm, 10-1-22-6 pm, 254-57.Opm, and 64-1 14 (or 64-144) pm. The seasonality of abundance of particles in nature is of course a property of the environment he studied, and is not reviewed here. Against this background of seasonal availability, Poulet studied possible selection of particles using electivity indices for all but the smallest of the above six size categories. I n agreement with his earlier conclusions (Poulet, 1973), he argued that

62


" in general, and within certain limits, Pseudocalanus minutus consumed those particles that were present in the greatest concentration ',.. This evidently need not be understood as indicating selection of those that are most concentra,ted. Poulet (1974) is somewhat equivocal on this question. Although he applies no statistical tests, he discusses seasonal variations in electivity indices a t some length, in this sense endowing the indices with " reality ". Finally, however, he concludes that Pseudocalanus is " unselective in its feeding. There is, however, no doubt that electivity varies with particle size. The numbers of positive and negative electivity indices can be estimated for each of his five particle-size groups from Poulet's (1973) text and his Fig. 5 . The indices were positive in la%, 33%, SOY0, 68%) and 59% of experiments for the smallest through largest particle size categories respectively (heterogeneity x2 = 45.3, d.f. 4, P < 0.01). This would seem to suggest that smaller particles ( < l o pm) are less readily removed by the animals. Poulet also presents a series of graphs with regressions of rate of consumption against particle concentration, which we summarize in Table VI. He concludes that " the highest ')

TABLEVI. REGRESSIONS OF FOOD CONSUMPTIONBY ADULTFEMALE Pseudocalanus ON PARTICLE CONCENTRATION (After Poitlet, 1974.)

Particle size

y=a+bx a

PS 1.6-3.8 4.0-9.0 10.1-22.6 25.4-57.0 64.0- 144.0

__

n

60 80 89 84 73

-0.413 - 0'093 0.365 0.430 0.341

r

b 0.214 0.707 0.991 0.932 0.636

0.17 0.54 0.63 0.83 0.62

c

z = particle concentration (In of mg/l). y = food consumption (In of mg/h/cop. x

Given as log in original, but In meant, and with corrigendum from author (regression and correlation coefficients reversed in original).

[correlation] coefficients were computed in size group 3 and 4, showing a good feeding response towards particles in the 10 to 50 pm range ". This conclusion cannot be inferred from correlation coefficients. More interesting questions might be asked using analysis of covariance, but this cannot be done from the data given. However, the elevations ( a ) of the regressions for the two smallest particle sizes (1.6-3.6 pm and 4.0-9.0 pm) in Table V I are lower than for larger particles. Except for the smallest particles, for which the variance of estimate must be very

THE BIOLOGY O F PSEUDOCALANUJY

63

large (r not significant a t P = 0.05), the slopes (b in Table VI) are similar for each regression. The value of a for particles < 4 pm is about -0.4, and for particles > 10 pm is about 0.4. The difference suggests that the smallest particles are retained about half as efficiently 2) as are larger ones. (i.e., eO.8 Poulet and Chanut (1975) come t o somewhat different conclusions by using two non-parametric tests t o detect possible differences in the size-frequency distributions of particles in diets and in controls. The more sensitive Kolmogorov-Smirnov test for the maximum difference between the cumulative frequency curves in controls and diets showed significant differences ( P < 0.05) in 16 of 42 experiments. However, in each of these experiments the difference was due t o the increase in particles over control level, either substantiaIly (5-25% over control) or grouped in a narrow size-range. Poulet and Chanut conclude that statistically significant examples of apparent selective feeding are due to the formation of smaller particles from larger ones by the activities of the copepods-for example by the breakup of chains of diatoms. Certainly this may partly explain the low electivity of the smallest particles and the differences in the regressions of consumption rate on particle concentration between large and small particles. The general conclusion t o be reached from Poulet’s earlier work does not altogether agree with the observations of Zagorodnyaya (1974) who found that Pseudocalanus favoured cells < 10 pm (Table V). Her experiments cannot be considered as well controlled as Poulet’s, but her observations that the diets of older copepodids and adults may include larger food particles is an amplification rather than a contradiction of Poulet’s work. It seems that Pseudocalanus may make use indiscriminately of a wide range of food, but that the upper limit of that range may increase with body size. We have given anatomical evidence (p. 5 5 ) that seasonally smaller females may be able t o filter smaller particles. Finally, in his most recent paper, Poulet (1977) concludes that copepodids (C I-C IV, mostly C 111) consume food particles30 000 cells/ml, replenished weekly ; Table XV). Production rate of clutches begins to drop at levels below 150 000 cells/ml, but probably not much above 30 000 cells/ml, when Iaochryaia galbana is

p

z

015,000 Cclls/ml

5-

mo 30,000

Cellr/ml

~ I S 0 . 0 0 0Celb/ml

91


used. It is interesting to note that a t only 15 000 cells/ml the number of eggs in a clutch is not reduced (Fig. 20). Now we may examine other, less extensive estimates of rate of production of clutches against the observations given above. Sazhina (1971) assumed an interval of 3-5 days and later (Sazhina, 1974) 3-5 days between successive clutches for Pseudocdanus from the Black Sea. She did not consider possible effects of temperature on the interval but these estimates refer to 8-10°C (see Fig. 22). Corkett and Zillioux (1975) derive an estimate of the maximal rate of production of sacs for well fed animals from Plymouth by dividing 12-6 (the mean number of eggs in a sac) by the time taken for development to hatching at their four experimental temperatures. They found that the observed rates of egg production were only about 50-70y0 of these maximal rates (compared with 83% for Halifax females, above). However, they based their estimates on rate of egg production during the whole laboratory life of the female, including the post-reproductive period. The extensive work of Thompson (1976) allows us to estimate the time between hatching and sac formation for seven females reared and mated in the laboratory. Here the reproductive period was explicitly designated, as time of appearance of last clutch was noted. It is possible, however, that females could have slowed down rate of production of sacs before this in some cases (cf. Fig. 18). From Thompson's data, we estimate that there was generally a mean lapse of a day or so between clutches of females (Table XVI). Longer periods occurred TABLEXVI. PARAMETERS OF REPRODUCTION BY SEVENFEMALE Pseudocalanue REAREDIN THE LABORATORY. (After Thompson, 1976.)

Temp. "G

Est.a time to hatching

Total no. of sacs

6.1 8.6 10.8 13.5 13.5 14.5 14.5

5.2 4.0 3.2 2.5 2.5 2-3 2-3

7 10 5 16 6 16 3

Eat. time Obs. time Obs. time Obs.b between first to carrying of postmating to first clutch, laet clutch, clutch,es, reproduction day8 days time, days dW8 4 3 4 16 16 2 2

43 40 24 54 16 44 6

1.9 0.5 2-8 1.3 0.7 0.6 0.2

From Fig. 22. Time between appearance of last clutoh and death of female.

38 10 3 70 64 67 41

92


between clutches of the female at 10*8"C,which died shortly after her fifth clutch appeared and may have been abnormal. Excluding this female, the times between appearance of successive clutches averaged about 28% longer than the times for development to hatching of eggs of the various temperatures. This is a good match for the 20% estimate for females from Halifax (above). Paffenhofer and Harris (1976) tabulate the means in four experiments of number of sacs produced by females, numbers of eggs per sac, and periods of nauplii production in days. If the last are to be interpreted as mean times between hatching of first eggs and hatching of last, then an estimate of times between successive clutches can be made, as above, by subtracting one sac from the mean number produced, I n the one experiment with Thalassiosira rotula as food, four clutches (five minus one) were produced in 14.33 days. It is assumed that this experiment was carried out at 12-5'C like their rearing experiments and that embryonic duration is about 2.8 days (Fig. 22). This implies a mean period between appearance of successive clutches about 24% longer than the time for development to hatching. I n three other experiments using Peridinium trochoideum, (concentration?)the mean delays between hatching of one clutch and appearance of the next were 3.3, 4.7 and 6-0 days. This seems to confirm the conclusion of Paffenhofer and Harris (1976) that P. trochoideum is a poor food for Pseudocalanus. From all these sources, we conclude that successive clutches of well fed, fully reproductive females should appear at intervals equal t o about 1.25 multiplied by the duration of embryonic development for the given temperatures. The lapse of time between mating and the first clutch has been estimated for seven laboratory-reared females by Thompson (Table XVI). If we exclude the two females at 13.5"C as abnormally retarded, the first clutch in Pseudocalanus may appear in about the time taken t o hatch a clutch. Since the female is fertilized very soon after moulting to adulthood (see p. 83), a period between maturation and first clutch similar to that between hatching of successive clutches might be assumed for demographic or productivity studies. (c) Total number of clutches We have shown that females in the laboratory produce a number of normal or complete egg sacs, and then may produce smaller or infertile ones during an essentially post-reproductive period (Fig. 18). Among females captured in nature, some will have already


93

expended part of their reproductive potential. Those females producing maximal numbers of egg sacs are more revealing of reproductive potential. Of 33 females whose reproductive histories are depicted by Corkett and McLaren (1969), eight produced between 8 and 11 full-sized clutches and between 0 and 3 small, late ones. This strongly suggests that the normal reproductive potential for females off Nova Scotia is about 10 successive clutches. Sazhina (1971) suggests that Pseudocalanus in the Black Sea may produce 21 clutches, but this estimate is based on an assumed interval of 3.5 days (embryonic duration at 10°C) and an unsupported estimate of 75 days for the length of the reproductive period. The largest number of clutches produced by an individual captured off Plymouth was 9 (see Fig. 18A), all of which hatched successfully (Corkett and Zillioux, 1975). Laboratory raised and fertilized females can, in principle, give more precise estimates of potential number of egg sacs. Results of three such experiments are tabulated by Paffenhofer and Harris (1976). I n one experiment using Peridinium trochoideum as food, 15 females produced an average of only 2.27 (range 2-4) egg sacs. I n another experiment three females produced only one, two, and two sacs respectively. This is good reason (along with the delays between sacs noted on p. 90) for thinking that P. trochoideum is an unsuitable food. I n another experiment using Thalassiosira rotula as food, six females produced an average of five clutches (range 2-9), which is lower than might be expected from the maximal performances of wild-caught females. Paffenhofer and Harris state that unfertilized eggs were colIected when females were about to finish egg production, but it is possible that some of their females did not fulfil their reproductive lives. The experiments were carried out in bowls, in which T . rotula may not have stayed in suspension. Another experiment with 12 females in a rotating beaker prolonged the period of reproduction, but no data are given on total numbers of clutches. The seven females fertilized in the laboratory in Thompson's (1976) study (Table XVI) produced an average of 8.9 egg sacs, close to the potential indicated for wild females. The variation in number of sacs in her experiments may be " natural ", whether related to premature death (female at l0-S"C)or to premature infertility (females at 13.5, 14-5OC). We are given no information on whether the late clutches of the females producing 15 and 16 sacs were full sized. For purposes of calculating demographic or production parameters, it may be perfectly acceptable to assume a potential of 8-10 clutches. I n fact, observed or assumed mortality rates will ensure that very few

94

CHRISTOPHER J. CORKETT AND IAN A. MOLAREN

females will reach this potential, or food may become seasonally scarce long before this potential is reached. (d) The length of the post-reproductive period Evidently females can live for some time after reproduction has essentially ceased. We have suggested above that the eight out of 33 females that carried 8-11 successive complete clutches in the experiments of Corkett and McLaren (1969), had been captured soon after maturity. The mean reproductive span of these eight females was 51 days, and they lived an average 41 days beyond this. The seven females reared and mated in the laboratory by Thompson (1976) had mean reproductive periods (mating to last clutch) of 39 days and post-reproductive periods of 40 days (TableXVI). Elsewhere we suggest that the potential length of life may be set physiologically by temperature (p. 115), and the post-reproductive period would accordingly be shorter in females that have been thwarted from sustained reproduction by food shortages. However, for females producing a full complement of about ten clutches at a maximal temperaturedependent rate, the evidence suggests that an essentially postreproductive period can occupy the second half of adult life; however, given natural mortality rates this post-reproductive life is unlikely to be expressed in nature (but see work of Martens, 1975, discussed on p. 208). (e) Proportion of eggs hatching Corkett and McLaren (1969) and Paffenhofer and Harris (1976) found that infertile or otherwise unviable eggs are normally produced only when females approach the end of their reproductive lives. Death of some embryos at other times does occur, and might be expected among females confined to small experimental vessels. It would seem unlikely that infertility or embryonic death are frequent in natural populations. Therefore, it is a little surprising that Thompson (1 976) found that the rate of production of ‘‘ viable eggs ” by females from the North Sea was considerably lower than might be expected. Thompson gives estimates of average numbers of “ viable eggs ” per sac for a very large sample of females of known cephalothorax lengths. Those between 0.72 and 0.78 mm produced on average 5.1 such eggs and those 1.00-1.12 mm on average 9.3 eggs, or about half the mean number carried in sacs of females from Nova Scotia or Scotland (Fig. 19A). Her estimates of “ viable eggs ” for females mated in the laboratory and for females captured seasonally are also substantially below expected levels.


95

Thompson’s counts of “viable eggs” were based on counts of nauplii found on periodic examination of females. We have found (unpublished observations) that females may eat some and on occasion all their nauplii, often very soon after they have hatched. This is presumably the major source of discrepancy between Thompson’s results and those summarized in Fig. 19. A useful study of viability of eggs of Psezcdocalanus could be made with containers adequately large for females to oxygenate their eggs by swimming, and by removal of sacs shortly before they hatch, so that no eggs are lost. 2. Theoretical rates of reproduction

Embryonic durations can be established accurately, and we have suggested that the time between successive clutches (or hatchings) might be about 25% longer than these durations when food is adequate. We have also shown that numbers of eggs in a clutch can be predicted for local populations, and that inviable eggs can probably be ignored. Thus estimating the maximal potential rates of reproduction per individual female might seem straightforward : simply divide the observed or calculated mean egg number in clutches by 1-25 multiplied by embryonic duration at the given temperature. This is in effect what is suggested by Sazhina (1974). However, this needs further refinement, as some females may not have produced their fist clutches and others may be post-reproductive. I n populations with continuous, overlapping generations the relative abundance of fully reproductive females will depend on the age structure of the adult female population. If mortality rates or recruitment of new adults are high, the pre-breeding females will be relatively common. Post-reproductive females will be more prevalent if mortality or recruitment rates are low. We have suggested for purposes of approximation that the prereproductive phase might on average last as long as the interval between appearance of successive clutches and that the post-reproductive phase might occupy the second half of a female’s life. We have used these approximations to estimate the proportion of females that might be fully reproductive in populations of various age structures. For simplicity we assume that the number in each successive age-group is a constant fraction of the preceding one (which is the same as assuming that constant mortality and recruitment rates have prevailed for some time). For a series of such populations, in which the oldest reproducing females (tenth clutch) ranged between 1% and 50% as common as the newly matured ones, elementary analysis shows that reproducing females constitute between 59% and 73% of the population.

96


We suggest that it might be assumed that an average of 65% of females in populations with continuous, overlapping generations are fully reproductive. It is on this basis along with the assumption that 25% of fully reproductive females will be between clutches a t any given time that we have calculated the potential rates of reproduction depicted in Fig. 21.

Temperature PC)

FIG.21. Average number of eggs produced per day by populations of food-satiated females of various lengths as functions of temperature. Unbroken curves are for females from off Halifax, Nova Scotia, and broken curves for females from southwest B a 6 n Island (see Fig. 19).

3. Reproductive rates in nature Although there are a number of published observations on the number of eggs borne by females in nature, these generally fail to account for inevitable disruption of sacs and masses in preserved samples. To ensure accurate estimates, free and attached eggs must be counted in samples taken with suitably fine-meshed nets. There are numbers of estimates of egg numbers in the literature for which no such information on methods is given. Reproductive rates have been estimated for one population in which egg production was highly discontinuous. From counts of adults, nauplii and free and attached eggs in successive fine-mesh samples from Ogac Lake, Baffin Island, McLaren (1969) estimated that clutch size was 19.6 f 5.0 (mean and 95% confidence limits from his Table 2). The wide confidence limits for this estimate from 14 " broods '' (eggs or young from roughly synchronous clutches ; see p. 135) are not surprising considering the many possible sources of error, but the mean

97


estimate is gratifyingly close to the expected clutch size of about 18 eggs for females of about 0.85 mm (mean for the season from McLaren's Fig. 6) as suggested in Fig. 19A. McLaren (1969) also estimated that the time between successive broods was approximately a week, which is about as expected at the temperature of 2-7°C that prevailed in the

2

4

6

8

10

12

14

Temperature ( T I in "C

FIG.22. Embryonic durations of Pseudocalanus from three localities. BBlehrQdelr's temperature function for Halifax animals from McLaren et a2. (1969). Function with b = -2.06 fitted to data in McLaren (1966) for the large form from Ogac Lake and to data for North Sea animals from Thompson (1976).

upper waters of Ogac Lake at the time of his studies (i.e. 1.25 x 4-5to 8 days, the times taken for embryonic development a t 7 O C and 2°C; Fig. 22, Table XVIII). After two or three successive broods in early summer in Ogac Lake, the food supply diminished rapidly, and the consequence was evidently not simply reduced reproductive rate, but A.Y.B.-15

6

98

CHRISTOPHER J. CORKETT AND IAN A. MULAREN

virtual cessation of reproduction, and finally death of the overwintered females (see p. 138). I n continuously breeding populations, it should be possible to use egg counts (free and attached) and temperatures t o estimate reproductive rates, in the manner suggested by Edmondson et 02. (1962). This has not evidently been done for Pseudocalanue. However, Marshall (1949) lists total numbers of free and attached eggs in fine-meshed samples taken weekly from Loch Striven, Scotland, along with mean numbers of eggs on those females that were carrying full, unbroken egg sacs. This allows us to estimate the proportion of females that were carrying egg sacs at the time of sampling. This has been done for the purpose of understanding life cycles (see later, p. 143). On average about 40% of females in the population bore egg sacs during the season of sustained reproduction, in March through August (Fig. 29, p. 142). From laboratory evidence (previous section), we have estimated that about 65% of females should be in full reproductive condition and that a further 25% of these should be between clutches, so that we expect that some 50% of females should be bearing egg sacs in any given sample. The slightly lower estimate from animals from Loch Striven suggests that the pre-reproductive period or the period between clutches has been underestimated in laboratory experiments, or possibly that predation takes a toll of eggs from prematurely broken sacs. Preliminary observations by Corkett (1 969) suggest that egg numbers may at times indicate near maximal reproductive rates for a population of females in which there are no pre-reproductive or postreproductive individuals (i.e. 1.25 multiplied by the observed number of eggs per female in Table XVII, close to the predicted numbers on April TABLEXVII. PREDICTED AND OBSERVED NUMBERS OF Ecas PER FEMALE IN BEDFORD BASIN,NEAR HALIFAX, NOVA SCOTIA,DURING 1969. (After Corkett, 1969.)

Dale

25 March 3 April 9 April 15 April a

Number of eggs per female Predicteda 0bse~ved 15.2 18.5 19.5 24.5

6.0 13.9 14.6 9.5

Based on mean size of 99, from Fig. 19A. Determined as by Corkett and McLaren (1969).

Relative size of oil sacb (mean f 95% c.1.) 0.01 f 0.003 0.02 & 0.006. 0.03 f 0.005 0.04 f 0.008

99


3 and 9). However, on March 25 and April 15, observed numbers were less than expected even for a population composed in part of nonreproductive females (i.e. 25% non-reproductive on average, as estimated in previous section). On March 25 some females had no visible stored oil, and 88% of oil sacs were less than 0.02 in relative volume (Table XVII). However, on April 15 oil sacs were relatively large and 17% of females had oil sacs less than 0.02 in relative volume. This suggests that the presence of stored oil in these females reflected a level of food in excess of that required to support maximal reproductive rates. TABLEXVIII. PARAMETERS OF B~LEHRADEK’S TEMPERATURE FUNCTION, WITH b = -2.05, DESCRIBINQ EMBRYONIC DURATIONS OF Pseudocalanw. (Data from McLaren, 1966; McLaren et al. 1969; and, for the North Sea, from Thompson, 1976.)

Locality Halifax, N.S. Woods Hole, Mass. Frobisher, N.W.T. Ogac Lake, N.W.T. (small form) Ogac Lake, N.W.T. (large) Millport, Scotland North Sea

Mean egg diameter pm f.95% c.l.

Temp. at time of sampling

Parameters a

a

121.6 & 1.8 127-4 & 3.7 130.4 &- 3.3

0.1 -0.7 - 1.7

2 144 2 312 2 280

- 13.40 - 13.87 -13.84

108.5 & 2.3

4.6

2 105

- 13.00

155.3 & 2.6 123.6 f 1-8 -

4-6 8.9 1o a

3 467 2 290 1 845

-13.17 -13.63 -11.45

Approximate annual mean temperature of southern North Sea; not given in Thompson (1976).

F . Retrospects and prospects A number of mysteries remain concerning reproduction by Pseudocalanus. The nature of the mating act and the reasons for low mating success in the laboratory are unknown. The reasons for unbalanced sex ratios in some laboratory rearings (Thompson, 1976) are obscure. Perhaps qualitatively or quantitatively inadequate food promotes a tendency for a greater proportion of females to be produced. This strategy could be adaptive for Pseudocalanus, since females live longer (p. 114) and, even ifthey mature at a time when foodis inadequate for their young, they need not ‘‘ waste ” all their reproductive efforts then.

100

CFLRISTOPHER J. CORKETT AND IAN A. MULAREN

Because of the evidently simple rules governing clutch size and clutch frequency in Pseudocalanus, control of its potential reproductive rate is well understood. Evidently these potential rates may at times apply in nature. We need more studies from nature to investigate this supposition using frequent sampling with fine-meshed nets, like that of Marshall (1949). Possible indicators of maximal reproductive rate such as presence of adult males a t a certain frequency or sizes of the oil store in adult females, should be explored. Pseudocalanus has been noted as having a generally lower reproductive rate than that found in some other common copepod genera such as Acartia, Centropages and Temora (Corkett and Zillioux, 1975; Dagg, 1977). After demonstrating that Pseudocalanus females (unlike those of Acartia tonsa and Centropages typicus) did not show reduced reproductive rate when fed intermittantly (12h/day), Dagg (1977) concluded that Pseudocalanus is adapted to patchy and irregular food availability. Since we have already shown (p. 73) that Pseudocalanus has a marked die1 feeding rhythm, Dagg’s laboratory feeding schedule may not have been altogether appropriate as a model of such patchiness. However, clearly the restrained reproductive rate of Pseudocalanus does require more exploration in the comparative manner begun by Dagg.

X. DEVELOPMENT AND GROWTH Readers will find this section of our review perhaps the most difficult and condensed, but we believe that it is through the observations and analyses outlined here that the role of Pseudocalanus as an important producer in the food web of northern seas may be best understood. It is possible to describe rates of development in terms of the moult into successively different morphological stages (Egg, N I-C VI). Growth is a conceptually separate phenomenon from development, and indeed some authors have expressed growth rates of copepods directly as a continuous increase in weight (wet or dry, or of some element). However, if the weight of particular stages can be determined, then growth rates can be estimated by using the times taken to reach these stages. We therefore pay considerable attention in this review to the determinants of development rates and body sizes as separate processes. We will show that temperature is of profound significance in determining development rates and sizes, and therefore growth rates, of Pseudocalanus. I n considering these matters, we make some use of BBlehrBdek’s (1935) temperature function. Empirical justification for the use of this function has been given by McLaren (1963). We use it in

THE BIOLOGY OF PSEUDOCALAN US

101

this review partly because it has already been used in publications about Pseudocaianus, and partly because of the need of some analytical function for interpolation and prediction. Since the use of BBlehrAdek’s function has recently been subjected to some criticism (Bottrell, 1975), we describe its properties briefly here. BBlehrBdek’s equation is one of several three-parameter equations that can adequately describe responses of physiological rates to temperature. The development time (D) in days of a development stage or stages (eggs, N I-C VI), of Pseudocalanus is represented as a function of temperature (T) in “C by: D = a(T-u)b, where a , u and b are fitted parameters. On a linear plot the constant u (often called the biological zero since it is the theoretical temperature a t which development time is infinite) describes the position or origin on the temperature scale. D = a when T = 1 u and therefore the constant a is the theoretical development time one degree above u ; log a is also the intercept on the y-axis of a plot of the log of development time against the log (T-u), the parameter b is the slope of this line. The parameter b in this equation can be assigned a constant value. The assignment of a constant value to b is arbitrary; however, as pointed out by McLaren et ai. (1969) when b is made a constant then a for embryonic duration among closely related animals is related to egg size. Furthermore, they show that a is strongly correlated with habitat temperature among more distantly related copepods.

+

A. Embryonic development rate 1. Zffects of temperature Figure 22 shows that BBlehrBdek’s temperature functions with

b = -2.05 (from McLaren et al., 1969) describes quite well the differences between three geographically separate populations of Pseudocalanus. The wide 95% confidence limits for means of North Sea animals in Fig. 22 generally exceed the ranges in development times for individual clutches given by McLaren (1966) and McLaren et al. (1969). These wide intervals and the anomalous duration at 8.6”C probably result from less frequent experimental observations (Dr B. Thompson, personal communication). However, this also illustrates the usefulness of having a general temperature function, like BBlehrQdek’s, for interpolation with such data. The assumed value of b = -2-05 (see above) has been used to fit the parameters of BBlehrAdek’s function to development times of different populations of Peeudocalanzcs (Table XVIII). Clearly, the great

102


difference of the large form from Ogac Lake (Table XVIII, Fig. 22) from all other populations is its proportionately slower development at all temperatures. If curvature ( b ) is held constant, the position on the Celsius scale (x)of its temperature response does not differ palpably from that of the small form, but the value of a is substantially greater (Table XVIII). The regression of a on egg size for the populations of Pseudocalanus given in Table XVIII, even when the large form from Ogac Lake is excluded, is significant at p = 0.05. McLaren et al. (1969) showed that with b = -2-05 the parameter u for 11 species of copepods from the arctic to the tropics was related to average environmental temperature and suggested that u may be used in this manner to indicate temperature adaptation. The regression of u on the temperature at time of sampling for populations of Pseudocalanus given in Table XVIII is not significant (p 0.09). Other estimates of development time in the literature (Marshall, 1963; Katona and Moodie, 1969; Sazhina, 1971, 1974) are not sdEciently accurate (usually given to the nearest whole day) to express possible regional differences. The earlier work of McLaren (1965) gives estimates of the relative times taken to hatch at different temperatures of embryos of Pseudocdanus that had undergone partial development, and has been superseded by the subsequent work cited above.

-

2. Effects of salinity

McLaren et al. (1968) found that the effect of salinity on development times of Pseudocalanus from Halifax, Nova Scotia, was slight. Only in one of several experiments was development significantly slower at abnormally high salinities (about 9% slower at 39x0 than at 29-35%,). Survival of embryos, however, may be affected by salinities (see p. 24). 3. Xeasonal and short-term temperature acclimation

Recent work (Hart and McLaren, 1978) shows that embryonic duration of Pseudocalanus varies to some extent with the temperature experienced by females. The seasonal differences in development time are given in Table XIX. If one considers the females collected in April t o be cold acclimated and those collected in October to be warm acclimated then one would expect that development in the laboratory at 10°C and 6°C would be relatively shorter for the April animals than the October ones. This does not occur and Hart and McLaren (1978) conclude that the seasonal differences in development times can not be attributed to temperature acclimation, but is possibly explained by the larger size of females and their eggs in the colder season (see p. 105).

103

THE BIOLOUY OF PSEUDOUALANUS

Hart and McLaren (1978) also looked a t short-term acclimation by keeping females a t lO"C, 6°C and 2°C during the period of oogenesis. They found that eggs hatched slightly but significantly later at 10°C when females had been kept at 2°C or 6°C. Thus short-term differences in development appear to be attributable to temperature acclimation unlike the seasonal differences noted on Table XIX. TABLEXIX. SEASONAL VARIATIONS IN BODYSIZEAND EWRYONIC DURATION OF Pseudocalanw FROB HALIFAX, NOVASCOTIA. (From Hart and McLttren, 1978) Month of collection of females April October

A~~Tox. Mean cephalothorax Temp. at time of length i n females (mm) collection 2 13

1.12 0.86

Mean development times i n hours (f 95% c.1.)

10°C 82.0 f 2.3 73.4 f 1.3

6°C 125.0 f 1-7 117.0 f 1-6

4. Effects of body and egg size The constant a in Brjlehrtidek's equation is the theoretical development time one degree above a (p. 101). It must be stressed that under no circumstances do we visualize actual development of Pseudocalanus taking place either at a (biological zero) or one degree above u. However, it is of interest that, when b is given the constant value of -2.05, then a is positively correlated with egg diameter amongst geographically different populations of Pseudocalanus (p. 102, Table XVIII). Thus, as suggested by McLaren (1965) and McLaren et al. (1969), by accounting for local differences in temperature through fitted values of a, the fitted values of a reflect the effects of egg size. The effect of size is of course most clearly shown by the embryonic duration of the large form from Ogac Lake (Fig. 22). If Bi5lehr&dek's equation is used with the values for the parameters given in Table XVIII for the large and small forms of Pseudocalanus from Ogac Lake, then it can be shown that the ratio of the embryonic duration of the large to small form is about 1.6:1 ab any temperature between 0 and 10°C. This ratio is more similar to that of egg diameters than to that of egg volumes (-3:l). McLaren (1 966) points out that proportionality of development time and egg diameters might be expected if control were through surface : volume restrictions. Corkett and McLaren (1969) give a positive correlation between egg diameter and cephalothorax length for the Halifax, N.S., population

104


IA

**

I

80

I

* A

. +

I

.

**

4 March April

70

Odune

* *

July

*oci. 7

Aua.

0.15

0.14

E E

v

0.13

. v

m

4 4

Fro. 23. Relations botween embryonic duration at 10°C (A) and egg diameter (R) with size of adult females. (After Hart and McLaren, 1978.)


105

and recently Hart and McLaren (1978) have investigated this relationship in detail for samples taken from March to October (Fig. 23). The;y showed that within the local Halifax population embryonic duration at 10°C (Fig. 23A) and egg diameter (Fig. 23B) are strongly correlated with cephalothorax length. It might be expected that egg size by itself would be responsible for differences in development times through, for example, the surface :volume ratio decreasing with increasing diameter (McLaren, 19GG). Hart and McLaren (1978) present evidence that shows that factors other

FIG.24. Hatching of Pseudocalanus. Note the bulging of the inner membrane, followed by the crumpling of the outer membrane, and finally the rupture of the inner mombrane, which is left protruding from the outer membrane. (From Marshall and Om, 1964.)

than egg size alone determine development time. They showed (using partial regression analysis) that female size had a significant effect on embryonic duration independent of egg size and that embryonic duration was significantly correlated with size of male parent as well. In addition they found that individual egg size within a clutch had no effect on the development time of that individual egg. I n the previous section we discussed seasonal and short-term acclimation and we now see how such acclimation may be affected by size. Since size of female P ~ e u ~ ~ ~changes u l u seasonally ~ ~ ~ ~ near Halifax (Table XIX) and elsewhere (p. l l G ) , seasonal differences in embryonic development rate can be partly attributed to such changes.

'"1

A

t

"1 501

D=u(T+ 13.40)-2'05

Ad.?, u=19350\

t\

m

\

\:

c III, u- I1890

\

crn.u=12850*

\

\

.

= 9190

"r 2ot

x

IO

O

'*\

2

4

06

8

10

12 l Temperature ("C)

FIQ.26. Times between hatching and the beginning of various stages of Paeudocalanw from (A) new Halifax, Nova Scotia (each point an individual, after McLaren, 1974) and from (B) the North Sea (open circles are means, closed circles individuals, after Thompson, 1978).

BBlehr6dek'e funQtiOIIf3 aa for embryonic duration (see Fig. 22). exoept for differences in a for each stage.


107

In conclusion Hart and McLaren (1978) have shown that short-term temperature acclimation affects embryonic duration in Pseudocalanus slightly, and in the expected compensatory way, but that seasonal differences can be attributed to environmentally and perhaps genetically (p. 124) determined differences in sizes of parents and eggs.

B. Hatching Hatching in Pseudocalanus has been described by Marshall and Orr (1954). The embryo is surrounded by two membranes and during hatching the outer one splits, the inner one bulges out, increasing in volume t o about twice that of the embryo, and eventually the nauplius struggles and breaks out through the inner membrane (Fig. 24). The discarded inner membrane may remain attached to the outer (Marshall and Orr, 1954) or the inner membrane may become completely detached from the outer during hatching (Corkett, 1968, who gives a photograph of a newly hatched nauplius, a hatching one, and two embryos).

C. Development rate of nauplii and copepodids The phyaiological and hormone control of development rate (i.e. moulting rate) of some Crustacea is reasonably well understood. However, the subject has barely been explored in Copepoda (Carlisle and Pitman, 1961) and evidently not at all in Pseudocalanus. Of particular interest would be information on physiological or hormonal causes of suspended development during the winter at middle and a t higher latitudes (see p. 157). However, for many purposes it is of greater interest to enquire into the two obvious controls of development rates in nature-temperature and food supply-which are the substance of the following sections. 1. Eflect of temperature

Although Pseudocalanus has been reared in a number of laboratories, the effect of temperature on times taken to reach various postembryonic stages of development has been examined only in populations from Nova Scotia (Corkett and McLaren, 1970 ;McLaren, 1974) and the southern North Sea (Thompson, 1976). These researchers used excess amounts of food and argue that the development rates of the copepods were maximal at the various temperatures. Their results are summarized in Fig. 25. Corkett and McLaren (1970) supposed that time taken to reach any given stage might be the s-me multiple of embryonic

108


duration a t any given temperature. Assuming that B6lehrBdek's function applies with a = 13.4 and b = -2.05 (i.e. the same as for embryonic duration in Fig. 22), this is the same as assuming that the temperature responses of times to develop to older stages can be adequately described by differences in a alone. This can be amplified as follows. If for stage I,

D,

= a, (T

- a)b

and for stage 11,

:.

D,, = a,,(T - a)b A t any temperature T

DIP,, = %/a11 if b and cc are common to all stages. Figure 25A strongly supports this view for Pseudocalanus. Thompson (1976) estimated average times (by planimetric integration of numbers versus time) taken to reach various stages from samples taken at regular intervals from large populations. She did not separate males and females in these estimates. I n spite of methodological differences, her results (Fig. 25B) are very similar to those for Pseudocalanus from Nova Scotia. Here, too, the times taken to reach various stages are well described by the equation for embryonic duration (see Fig. 22), with changes only in the proportionality constant, a. However, there is an awkward " step " in the relationship for older stages at about 8°C. This suggests that the animals at colder temperatures were somehow thwarted from more rapid development. Possibly there was some abnormality of response in the laboratory cultures a t these rather low temperatures for this North Sea population. Additional evidence for this assertion comes from the fact that Thompson (1976) was unable to obtain successful hatching of eggs a t temperatures below 3.7"C, or successful rearing of stages above N V at 3.7"C. Table XX gives estimates of the relative amounts of time required to reach successive stages of development, expressed as multiples of the time for embryonic duration; that is, the a of Bglehrhdek's function for each stage, calculated as in Fig. 25, is divided by the a for embryonic duration from Fig. 22. Because of the possibly abnormal retardation of development below 8°C among North Sea animals (see above), we have calculated for use in Table XX the a values for successive stages only for data from higher temperatures in Thompson (1976). This gives estimates of a for the older stages that are 3-5-4.8% smaller than those in Pig. 25B.

THE BIOLOQY OF PSEUDOCALANUS

109

OF THE RELATIVE TIMES TAKEN TABLExx. ESTIMATES BY Pseudocalanus TO REACH VARIOUS STAGES. (Data from Fig. 25.)

Beginning of stage N I1 N 111 N IV NV N VI CI

c I1 c I11 c IV cv c VI

a

Nova Scotia

North Seaa 0.18 0.55

4.29

-

5-99

-

9.03

2.01 2.82 3.51

3.91 5-14 6-14 7.12 8.14 9.46

Multiples of embryonic duration only for data >S"C (see text).

The estimates for Pseudocalanus from Nova Scotia and the North Sea, of the relative times taken to reach various stages are very similar (Table XX). Among all nauplii, N I11 (the first feeding stage, see p. 112) has the longest duration (1.5 embryonic durations). All copepodid stages have roughly the same relative durations. It is probably sufficiently accurate for some purposes to assume that each copepodid stage has about the same duration as embryonic duration a t any temperature ; from Table XX the five stages average 0.95 embryonic durations (i.e. (9.03-4+29)/5)in the Nova Scotia animals, and 1-11 (i.e. (9.46-3-91)/5) in those from the North Sea. We believe that the estimates in Table XX, or perhaps the approximations noted above, can be used to predict the duration of developmental stages of Pseudocalanus in conditions of excess food, provided embryonic durations are known for at least two temperatures (the minimum required to fit BGlehrBdek's function with b assumed to be constant at -2.05). Since embryonic duration, ignoring the large form of PseudocaEanus, differs little among regions (Table XVIII), especially at higher temperatures (Fig. 22), we propose that estimates for older stages from different geographical localities should not differ much from those shown in Fig. 25. It is possible to examine this proposition using scattered estimates for other localities. I n using published estimates, the possibility has to be considered that food shortages, disease and other such factors can prolong development times beyond those possible a t the given temperatures. Indications of

110


such retardation might be the occurrence of a wide range in development times, or of some " stragglers " that moult long after the others. The first recorded laboratory rearings were those off Plymouth by Crawshay (1915) who found that adulthood was reached 35-40 days after hatching at 12.3"C. Although the food supply used by him cannot be assessed, it was probably inadequate for maximal development. Katona and Moodie (1969) succeeded in rearing large numbers of Pseudocalanus over perhaps four generations in large-volume containers a t 15°C. They obtained information on developmental durations only from eight smaller vessels of 250 ml volume, in which the progeny of individual females were reared. These gave estimates considerably longer and more spread out than those in Fig. 25B: 16-25 days for the time from hatching to C I and 30-38 days to adulthood. Numbers and sexes are unspecified. Although Katona and Moodie give no information on feeding procedures in the small vessels, they indicate that the rearing medium in the large-volume containers was renewed only every two weeks. Algal food (mostly Platymonas sp. and Isochrysis galbana) was added to these containers to keep cell concentrations at 100000/ml, but altogether the conditions of rearing do not seem to have been as optimal as those used by Corkett and McLaren (1969) and Thompson (1 976). Corkett (1970) reported on the successful rearing of three individuals from Halifax, N.S. beyond C I from among those reared to this stage by Corkett and McLaren (1969). Although the fastest individual developed at precisely the rate predicted from Fig. 25A (26 days to adulthood), the other two lagged considerably, so that mean time to maturity was 35 days. The food medium was added to but not changed every few days as by McLaren (1974). We assume that the retarded individuals were not developing at a physiologically maximal rate. The large number of experiments conducted on Pseudocalanus off the island of Sylt in the North Sea by Paffenhbfer and Harris (1976) were designed to test the effects of food concentration on growth rates (see p. 130). They used large-volume, rotating containers, and changed food frequently. Within the range of food concentrations used by them, there was little or no evidence of retardation. I n eight experiments, the times between hatching and C I were 10.5-12.5 (mean 11.4) days, and between hatching and 50% adult were 24-32 (mean 25.3) days. If we assume that embryonic duration for animals off the island of Sylt is the same as for the North Sea animals studied by Thompson (see Fig. 22), then the times estimated by Paffenhbfer and Harris are precisely as predicted from Table XX : 10-7-11.8 days for hatching to

THE

nIoLom OF

PSEUDOCALANUS

111

C I and 24-8-26.0 days for hatching to adulthood (the range representing both Nova Scotia and North Sea ''multipliers" respectively). Sazhina (1968) reared individuals of the Black Sea population of Pseudocalanus to maturity in the laboratory at 8-10°C. Details of experimental procedures and numbers of animals involved are not given, and estimates are presented only to the nearest day. However, results conform quite well to those summarized in Fig. 25. Durations for nauplii in days were: N I (l), N I I (2), N I I I (3), N I V ( 3 4 9 , N V (3-4), N VI (2-3) for a total naupliar period of 14-18 days. The lower value is probably a better indication of potential rates. For copepodids, the times were: C I (2), C I1 (2), C I11 (3), C I V (5) and C V (5). Lengthening of duration in later stages (contrary to Table XX) indicates to us that these stages were not developing a t maximal rate. Nevertheless, the lower estimate of the range 3 P 3 9 days given by Sazhina as time from hatching to maturity agrees with mean estimates for other populations (Fig. 25). Sazhina (1974) gives duration of the naupliar stages (presumably equivalent to appearance of C I ) for animals from the Black Sea as 14-18 days at 8-10°C (a summary from Sazhina, 1968) and 1 6 1 9 days at 11-13°C ; the times at the higher temperatures suggest that development was retarded (see Fig. 25). For " Mediterranean " animals (no locality given, but presumably the Adriatic) she gives 12.3 days at 11-13"C, very close to times in Pig. 25. There are no details on numbers of copepod or conditions of rearing, except that green algae were used in the Black Sea experiments and mixed food in the " Mediterranean '' ones. However, we predict with some confidence that rates applying elsewhere (Fig. 25) will also apply to Black Sea and Adriatic populations. Andreeva ( 1 976a) determined the relationship between temperature and the duration of C I from the Sea of Japan as about 12 days a t 3.5"C and 4 days a t 15°C. These times are much longer than predicted on the assumption that stages take about the time required for embryonic duration (about 7 days at 3.5"C and 2.2 days at 15°C in the North Sea ; Fig. 22). However the ratio of times a t 3.5"C and 15°C is appropriate (3-0 in the Sea of Japan, 3.2 in the North Sea). Andreeva's (1976a) plot of individual durations shows considerable scatter (the range averaging about & 40% of the mean durations between 10" and 15OC). The animals may have been experiencing physiological or feeding problems that retarded their development rates. I n an earlier note, Andreeva (1975) gives 2-3 days for embryonic duration, 12-13 days for the naupliar period, and 23-25 days for the copepodid period, but does not state the experimental temperature involved. The first two are reason-

112

CIIBISTOPHER J. CORKETT AND IAN A. MCLAREN

able for temperatures of ca. 10-12"C (see Fig. 22, 25)) but the last shows clear evidence of retardation (see Table XX). 2. Effects of food supply

We have indicated above that inadequate food may retard development in rearing experiments. Differences in quality of food have evidently not been looked into, but therc is much information on effects of amounts of food. Thompson (1976) found that nauplii reach N I11 but do not develop further if starved. From her estimates of stage duration at the eleven temperatures shown in Fig. 25B, it can be estimated that the relative times (i.e. as units of embryonic duration) taken to reach N I1 and N I11 were 0.22 and 0.53-almost precisely as for the fed N I1 and N I11 in Table XX. Her estimates of duration of starved N I11 are invalidated by the death of all of them in this stage. We conclude (with Thompson) that food is unnecessary to sustain maximal development rates during the first two nauplius stages and that N I11 may be the first feeding stage. Corkett and McLaren (1970) found no retardation in individuals reared a t 11 6 ° C in concentrations of Isochrysis galbana replenished weekly at 1.5 x lo5, 3 x lo5, or 6 x lo5 cells/ml. Mean time from hatching to C I was 10.6 days and range of individual times was 9.612.5 days. However, a t 3 x lo4 cells/ml, the results were complex. I n two dishes with three nauplii each, three individuals reached C I in 11.5, 12.6 and 14.5 days. The rest remained in nauplius stages for 25 days, and then were fed abundant food (6 x lo5 cells/ml) and reached C I after about nine days. Nine days is close to the number of days that would be predicted to be taken if these retarded nauplii were stopped a t N I I I (9.6 days between beginning of N I I I and C I at ll*5OC, from Fig. 25B). These results suggest that 3 x lo4 cells/ml of Isochrysis galbana replenished weekly is a critical, threshold level for sustaining development rate. It has been shown (p. 90) that this is also a critical level for maximal production of eggs and will be shown (p. 129) that this is the level at which fat is laid down. This level of I . galbana, a t the time of replenishment, is about 500 pgC/I. calculated from Table V I I and may be effectively about half this level in view of probable filtering inefficiencies of such small cells (see p. 63). Paffenhofer and Harris (1976) examined effects of food supply extensively and rigorously. As noted above (p. 110) there was little evidence of developmental retardation at any food concentrations used by them. At (nominal) food concentrations of 5 6 2 0 0 pgC/l., the ranges of times for individual experiments were 10.5-11.5 days to reach C I


113

and 24-26 days to reach adulthood. At a nominal food concentration of 25 pgC/l. (actually about 30 pgC/l.) C I was reached on average in 10.5 days. However, at the same nominal food concentration (actually about 21-27 pgC/l.) subsequent development was retarded slightly, and time t o 50% adult was 29 days. It appears that this level of food is about a t the threshold for sustained development. Since the experiments of Paffenhofer and Harris involved the diatom Tholassiosira rotula in rotating culture vessels, the lower estimate of this critical level compared with the results using the smaller I . galbana (above) is probably more nearly natural. Paffenhofer and Harris’ (1976) work is of great importance in demonstrating that development times are little affected by food concentrations comparable with those occurring in nature. They report that algal concentrations near the island of Sylt ranged from 68-780 pgC/l. (annual mean 192), and refer to comparable values for total particulate C for the northern North Sea. They conclude: (‘This suggests that all developmental stages of the neritic P . elongatus are able t o adapt t o a range of food concentrations, neither mortality nor generation time being markedly affected by low food concentrations” . 3. Genetic variation of development rates Differences in development rate between populations of Pseudocalanus may have a genetic component. McLaren (1965) concluded from field samples that the small form from Ogac Lake developed at about 0.42 stages per day compared with 0.28 stages per day for the large form. This ratio of development rates (1.5 :1) is about the sarne as the ratio of embryonic durations (1.6 :1, p. 103) determined in the laboratory for the large and small populations of Pseudocalanus from Ogac Lake. These differences in development rates are clearly genetical. I n eggs a t the 32-cell stage the DNA content was about seven times greater in the large form than found in the small form (McLaren et al., 1966). Woods (1969) speculates that this larger amount of DNA is itself responsible for the slower development rate and that this slower development rate serves t o restore a life cycle more suitable for the environments of Ogac Lake (p. 139), and we have in fact referred earlier to the large form of Pseudocalanus as a possible ‘(instant species ” (p. 10). Hart and McLaren (1 978) found that embryonic duration was significantly related t o size of males chosen for extreme sizes from a sample taken near Halifax, Nova Scotia. Since the male could only contribute

114


genetically, Hart and McLaren conclude that development rate, like size (see p. 124) was heritable among these animals.

D. Longevity of adults We have already indicated (p. 93) that female Pseudocalanus may potentially produce of the order of ten successive clutches of eggs over a period of time determined by temperature, and that they might live for an equal post-reproductive period. However, in nature it is unlikely that maximal potential longevity is often attained, and post-reproductive life is inconsequential for demography and production since neither growth nor egg production takes place. The brief review here may, however, be of some intrinsic interest. The maximum realized length of life in nature is over two years in the high arctic, where adult females may live for some months at least (p. 137). Adult males, as already noted (p. SO), are scarce in nature because of their shorter lives. I n Crawshay's (1915) pioneer work, one adult female survived for 121 days in the laboratory at 12.3"C. The laboratory work of Urry (1965) and Corkett and Urry (1968) on effects of quantity and quality of food on mean survival of adult females has already been discussed (p. 177). However, as their experimental animals were captured in nature, the maximum, rather than the mean might be a better reflection of their potential longevity. Accordingly, we have estimated from Urry (1964) the age of the longest lived individual in each of 21 experiments at 10 5 1 ° C in which food was considered to be adequate for sustained existence (i.e. Isochrysis at 30 000 cells/ml or more replenished weekly, and food species that gave comparable survivorship, Table XII). The mean of these 21 estimates is 107 days (range 84-144). Because different numbers of copepods were used to initiate these experiments, confidence intervals cannot properly be estimated. The eight wild-caught females considered by Corkett and McLaren (1969) to have fulfilled their reproductive potential of 8 or more clutches (see p. 93) lived on average 92 days (range 75-103) at 6-7". The seven females reared and mated in the laboratory by Thompson (1976) lived on average 79 days (range 31-140) after mating, which occurred soon after maturity (Table XVI). The most that can be said from these scattered results is that adult female Pseudocalanus are capable of living for more than 100 days at quite elevated temperatures. Males, by contrast, were found by Urry (1964) to live for only 15 days on average, compared with 33 days for females when both were given 30 000 cells/ml Isochry& galbana. Mean survival for starved

115


females in several experiments ranged from 17 to 19 days indicating that males evidently gained no sustenance from I . galbana. Probably because of small numbers, there was no evident effect of temperature on longevity of the seven females reared by Thompson (Table XVI). However, a trend is evident (Table XXI) for starved adult females as reported by Corkett and Urry (1968). The very short survivals a t 19.5-21°C are surely pathological, but those at lower temperatures may reflect normal physiological processes that may also apply to the determination of potential length of life of feeding adult females. TABLEXXI. LONGEVITY OF STARVED FEMALE Pseudocalanus IN TEE LABORATORY. (After Corkett and Urry, 1968.) No. of copepods 91 11

13 7

Temperature “C 5-7 10-17.5 11-19.5 19-5-21

Mean longevity (days) 71 35 24 4

Recently, Dagg (1977) compared survival over a short period of ten starved and ten continuously fed (superabundant Gonyaulax tamarensis) female Pseudocalanus and found no difference (six alive after sixteen days). However, these numbers seem rather small on which to base his conclusion that Pseudocalanus “can withstand rather low periods of total starvation, suggesting that they are capable of metabolically removing themselves from changes in the food environment.”

E . Body size Pseudocalanus shows a great deal of variation in body size. Cephalothorax lengths of individual adult females have been recorded as small as 0.67 mm (Carter, 1965) and as large as 1.8-1.9 mm (Lacroix and Pilteau, 1971, their Fig. 4). We believe that explanations for this variability are now largely complete. Therefore we attempt to review only a fraction of the large literature that refers to seasonal and local variations in size of Pseudocalanus with its many speculations. Rather, we will attempt to demonstrate the propositions that size is affected by temperature, but not directly by food supply, and that there is marked genetic variation in size, both within and between populations. The systematic significance of this variability has already been referred to (p. 11).

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1. Effects of temperature on size (a) Inferences f r o m nature The earlier literature on size variations of Pseudocalanus in nature is admirably reviewed and analysed by Deevey (1960b). She found high negative correlations ( r < -0.6) between length of adult females and temperature in waters with annual temperature ranges of 14°C or more. Conversely, correlations with temperature were smaller, but high positive correlations ( r > 0.5) were found with various measures of phytoplankton during the month prior to sampling where waters had an annual temperature range of 13°C or less. Where possible, she came to these conclusions using partial correlations. Deevey (1960b) concluded that these correlations imply causality : that the relative effects of temperature and food on seasonal variations in length depends on the extent of the annual temperature range and the quantity of phytoplankton present. McLaren (1963) argued that the association between size and food supply was indirect, operating through the effect of food shortage in retarding development (p. 112). I n all localities from which data were available, Deevey (1960b) found that food supply was negatively correlated with temperature-partly a consequence of spring maxima in phytoplankton. This means that size might be most closely correlated with immediate temperatures when they are low since food would allow rapid development then, and this form of dependence cannot be eliminated by partial correlation. I n order t o stress the sufficiency of temperature as an explanation of seasonal differences in size, we will first discuss some examples from nature in which Deevey (1960b) and others have implicated food as well. Loch Striven, Scotland (Marshall, 1949; Marshall et ab., 1934) has a fairly narrow annual temperature range (6O-l3"C, means for water column, see Fig. 29). I n 1933 the major diatom bloom occurred in late March to early April, with smaller bloom in May, July and late summer. Few diatoms were found in winter. Adult female Pseudocalanus showed small size in winter, an abrupt increase to maximal size in April, and then a gradual decrease during summer (see p. 143, Fig. 29). Size and temperature are strongly and negatively correlated between April and autumn, but the persistence of small animals during the cold, diatom-poor winter reduces the correlation with temperature, and introduces the strong partial correlation between size and food during the previous month, as calculated by Deevey (1960b). However, the original papers make it clear that these small overwintering adults had been developing from about mid-July of the previous year, whereas the large adults in April were born beginning in February (see also


117

p. 143). McLaren (1963) used such information from Marshall (1949) and Marshall et al. (1934) to plot mean size of adult females on each collection date against estimated mean temperatures during their lifetimes. The results (Fig. 26) indicate that temperature is a sufficient explanation for size variations. Similar arguments, taking into account small overwintering copepodids and adults from the previous warm autumn, can be used to explain the reduced correlation between size and temperature at time of sampling in other mid-latitude areas with narrow temperature ranges considered by Deevey (1960b); for example, the North Sea (see p. 147), the English Channel (see p. 146) and Norway (see p. 151). I n high latitudes, the protracted life histories of Pseudocalanus may even lead to spurious positive correlations between size and temperature at time of sampling. Thus Ussing (1938) found in East Greenland that reproduction during the phytoplankton maximum in June gave large young copepodids in July which developed (probably in deeper water) to large, overwintering C V by September (see p. 141). Reproduction in summer, when food is scarcer and temperature slightly higher, gave smaller copepodids that did not moult into C V until the following spring. There was little size variation in the subsequent adults. Clearly temperature at the time of capture would be a poor indicator of size under these conditions, with large C V occurring during the warm summer and smaller ones in the cold spring. But it cannot be concluded, as Ussing (1938) and Deevey (1960b) did, that food is directly responsible for the observed size differences. Similar interpretations can be applied to size variations described in other northern localities (see also p. 141) by Digby (1954), Fontaine (1955), Grainger (1959) and Cairns (1967). However, in some of these localities there is bimodalism of size that might also reflect genetically different size forms (see p. 123). Studies of two landlocked populations in northern Canada are free from effects of larger or smaller individuals being recruited from outside the study areas. Carter (1965) found that size of adult females varied little in Tessiarsuk, Labrador. From depth distributions and temperature profiles it seems that this population was subjected to a narrow range of temperatures during the season. A group of small, rapidly disappearing females a t the beginning of the summer may have largely or completely matured in the warmer waters of the previous autumn (see p. 140). McLaren (1969) described seasonal variations in sizes of all copepodids and adults in the three basins of Ogac Lake, Baffin Island. By detailed analysis of phytoplankton, temperatures and depth distributions of the copepods, he concluded that size variation

118

CHRISTOPHER J. CORKETT AND LBN A. MCLAREN

could be attributed to temperature during development. A paradoxical recovery of size of young copepodids during later summer when food was scarce and temperatures rising he suggested might be due to relatively more rapid development of smaller individuals or to their disproportionately high mortality. McLaren's (1969) study stresses the complexity of interpretation that is required to explain size variations in high latitudes, even in a relatively " controlled " situation. All in all, size varies rather narrowly within most of these highlatitude areas, and variations between localities with different thermal

Temperature ("CI

FIG.26. Relationships between female size and environmental temperatures in various localities. Points for Canadian arctic are (see text): 1, Tanquary Fiord; 2, Foxe Basin; 3, Ungava Bay; 4, Tessiarsuk; 6, Ogac Lake. (After McLaren, 1966, with additions for the Canadian arctic from Cairns, 1967, and Carter, 1966.)

regimes can be more revealing (Fig. 26). The points for Foxe Basin (2 in Fig. 26), Ungava Bay (3) and Ogac Lake (5) have been used and explained previously (McLaren, 1965). That for Tessiarsuk (4) is from Carter (1965), and represents the mean size of females on 10 and 20 September (estimated from his Fig. 5), since these developed during summer (his Fig. 4) at depths around and below 10 m (his Fig. 7) where temperatures can be estimated (his Fig. 3). The point (1) for Tanquary Fiord represents mean size in 1963 and 1964 combined from Cairns (1967, his Fig. 5) and assumes that small seasonal temperature variations near the surface are unimportant relative to the almost uniform temperatures of -1"C throughout the season between 20 and 100 m (his Fig. 1). Given these approximations and assumptions, Fig.


119

26 indicates that there may be uniform temperature response of populations of Pseudocalanus throughout the Canadian north. As noted above, Deevey (1960b) concluded that temperature is all-important when its seasonal range is wide. McLaren (1963, 1965) chose to depict her size-temperature relationship for Long Island Sound (Fig. 26). Here the copepod populations might be relatively “ enclosed ”. A ten-fold variation in chlorophyll had no statistically significant effect on size, and the water is almost unstratified during the growing season, so that mean temperatures are more reliable. Unfortunately, there appears only limited information on seasonal size variations of the otherwise extensively studied populations of Pseudocalanus in the Black Sea. Kovalev (1967) lists mean total (?) lengths for animals from several depths for the months of February (1.17-1.19 mm), August (1.09-1.12 mm) and September (1.08-1.09 mm), which suggest that seasonal size variations in this population may be rather narrow. A later note (Kovalev, 1968) indicates a range of 1-00-1.23 mm in the Black Sea and 0-8P1.04 in the Adriatic. The relationships in Fig. 26 together seem to be overwhelming evidence from nature that temperature is the primary environmental determinant of body size of Pseudocalanus. They also reveal clear regional variations in response. McLaren ( 1965) fitted BBlehrAdek’s temperature functions to the data (with fewer points for northern Canada) in Fig. 26. This is not necessary to describe the obvious adaptation of each temperature-response curve to the regional thermal r6gime. Adaptation is hardly surprising ; otherwise monstrously large copepods might occur in cold northern waters, and exceedingly small ones in warmer regions. It is also interesting that the same range in mean body size seems to be maintained in all three geographical regions in Fig. 26.

(b) Evidence from the laboratory Only recently has the effect of temperature on body size been confumed in experiments. A hint of the effect is first found in the work of Katona and Moodie (1969), who collected females off Plymouth when the surface temperature was 86OC. These produced laboratory cultures that went through about four generations in the laboratory at 15OC. Means of cephalothorax lengths are given as 1.01 f 0-05mm in the females from nature and ranged from 0.84 f 0-02 to 0.89 f 0.004 in successive samples from the laboratory stock (the & values are said to be S.D., but are very small and are presumably S.E.). Without data for other temperatures the reduced size of females in the laboratory cannot be assigned with certainty to temperature.

120


A series of experiments were carried out with C I11 captured near Halifax, Nova Scotia, and reared to maturity at constant temperatures of about 5, 8 and 12°C and varying temperatures of 8-12", with a mean of 10°C (Lock and McLaren, 1970). The results showed the expected inverse relationship between female size and temperature, and no significant response of male size. The founding populations of C I I I differed in mean size, so that the effect of temperature is best expressed as percentage increments of size between stage I11 and adult (Table XXII). Although the size difference of the females at the temperature extremes proved to be highly significant, confidence intervals cannot be set for the percentage increments, as the animals were not reared individually. McLaren (1974) added to these results by rearing animals to C I11 in the laboratory. Somewhat surprisingly, he found no effect of temperature. Mean cephalothorax lengths (k95% c.1.) were 0.60 f 0.04 mm a t 4.2"C, 0.60 f 0.02 mm a t 7-3"C and 0.59 -& 0.02 mm at 11*7"C. TABLEXXII. MEAN SIZEINCREMENTS OF Pseudocalanus C I11 FROM HALIFAX, NOVASCOTIA, REARED TO ADULTHOOD AT VARIOUS TEMPERATURES. (After Lock and McLaren, 1970.)

yo size increment to ad. $2

Mean size C 111 mm 0.55 0.63 a

5°C

8°C

10°C"

60 59

52 51

45 49

12°C 43

45

12 h at 8" and 12 h at 12" each 24 hour.

Thompson (1976) carried out extensive experiments to determine the effects of temperature on size. She presents her data as tables with mean lengths, S.D. and numbers, and graphs the means without regressions. We have chosen to present her results by fitting regressions to her means (weighted by n ) for each temperature (Fig. 27, insert). This allows us to express the relative effect of temperature as the percentage decrement in length (mean calculated for all temperatures) for each degree Celsius. This in turn allows comparisons between the effects of temperature on each stage (Fig. 27). A striking pattern emerges from Thompson's results. If two groups of copepods were reared a t 10" and 11°C respectively, the latter should average about 1%longer at N V . However, if they are reared further t o

121


C I, they might differ little in length. This suggests that during the interval between NV and C I, temperature may have a positive effect on size. After C 111, the effect is clearly negative again. However, the confidence intervals for C V and adult animals are very wide. This is I I I I

II

, I I I

II

I I

I

I I I I I

I I I f I I

-5.0 4

6

8

10

12

( I

I

I I I I

I

I I I II

1; I I

14 I0

OC

I

I I I

I I I

N I N I I N I I I N I P N Y N P I CI

CII

CIIl C E C Y Ad.

Fra. 27. Effect of temperature on body size of North Sea Psewlocalanus reared in the laboratory (data from Thompson, 1976). The unbroken lines are based on linear regressions of lengths on all experimental temperatures. The broken lines are based only on linear regressions of lengths on temperatures above 7.3"C, as shown in the insert for C 111-adult (cephalothorax lengths, sexes combined). Overlap of the 95% c.1. with a length decrement of 0% indicates non-significance of the temperature effect.

not a consequence of small numbers of older stages ; the same numbers of individuals of each copepodid stage were measured at each temperature. Rather, it is due to the erratic effects of low temperatures on size of these older stages, as clearly shown on the insert of Fig. 27.

122

CSIRISTOPRER J. OORKETT AND L4X A. MULAREN

The older stages at the three lowest temperatures in Thompson's experiments also seemed to develop more slowly than expected (Fig. 25B),and we have suggested (p. 108) that temperatures below 8°C might have caused abnormalities in the laboratory. Therefore we have fitted regressions to the means for higher temperatures, as indicated on the insert of Fig. 27. The regression coefficients,expressed as percentage length decrements per "C, show a more persistent and significant pattern of increase among older stages when only temperatures above 8" are used. Thompson's results, as expressed in Fig. 27, are compatible with those of McLaren (1974) in showing the small effect of temperature on size of C I11 as compared with adults (see above). However, they do not confirm the conclusions by Lock and McLaren (1970) that adult males were little affected by temperature. From tabulated results in Thompson (1976), the percentage decrement in length per "C is calculated as 3.43 & 1.86% for adult females and 2.92 f 1.54% for males (the 95% confidence limits are calculated for regressions on temperatures above 8"C, as for Fig. 27). There is some resemblance between the regression for adults from the southern North Sea and that for females from Lock Striven (cf. Fig. 26, Fig. 27 insert). 2. Effects of food on size

We have already suggested (p. 116) that the association between body size and food supply in nature is indirect : that food shortages may retard development and therefore diminish the correlation between size and current temperatures, but that body size is not ultimately affected by this shortage. Certainly the association between temperature and size in the field leaves little room for a further effect of food. McLaren (1963) showed from data in Deevey (1960b) that a ten-fold variation in chlorophyll (as an index of food) did not correlate with the deviations from the size-temperature curve for Pseudocalanus in Long Island Sound. Food was kept a t very high levels in the experiments of Lock and McLaren (1970), McLaren (1974) and Thompson (1976), ao that any effect of food supply was not evident. We have suggested (p. 110) that animals from Plymouth reared by Katona and Moodie, which were retarded in reaching maturity, may have been short of food. However, their size (female cephalothorax lengths 0.84-0.89 mm) was similar to that predicted for females from the southern North Sea (0.83 mm, from regression for females a t temperature > 8°C.) The extensive experiments of Paffenhofer and Harris (1976) give excellent evidence on the effects of food on size. They give sizes only

123

THE BIOLOGY OF PSEUDOOALANUS

as ash-free dry weights, which are not directly comparable with the cephalothorax lengths considered above. It is clear that wide variations in food supply have little influence on ash-free dry weight, except for males a t the lowest concentration of food (Table XXIII). The great importance of these results (as for their results on development times described on p. 113) is the demonstration that food has such a small effect on body size at food concentrations a t the lower range of possible food supplies in nature. TABLEXXIII. WEIGHTS OF Pseudocalanus ADULTSREAREDFROM NORTH SEA POPULATIONS. (After Paffenhofer and Harris, 1976.)

Nominal food concentration (pg (711)

No. experiments Mean pg ash-free dry wt Mean 68 pg ash-free dry wt a

25

50

1

2

16.0 3.1

100

200

4

1

18.3 (14*0-22.5)a 22.1 (19.0-23.7) 9.5 (7.0-12.0)

11.3 (8.4-13.9)

17.5 13.2

Ranges in parentheses.

3. Genetic variation in body size Differences in the size-temperature relationship between populations of Pseudocalanus (e.g. Fig. 26) are more marked than the differences in developmenctemperature relationships (e.g. Fig. 25). The differences in size (p. 9) between the large and small forms of Ogac Lake and Winton Bay are also genetic, and McLaren (1965) suggested that the differences might be due to cell size, rather than cell number. Woods (1969) enlarged on this possibility and argued from the literature that " an increase in the amount of DNA should result in an increase in the cell volume but a decrease in the metabolic and division rates". However, Pseudocalanus also shows a great deal of continuous size variation within samples from any given locality (see Figs 29-33). Some of this variation is doubtless due to the occurrence of animals that have been exposed to different temperatures during maturation. Recent evidence (McLaren, 1976b) indicates that size is also markedly heritable. McLaren reared at 10°C femaIe offspring of families from 9 males each mated to 2-4 females. This enabled him to estimate by analysis of variance the contributions of males and females to the cephalothorax length of adult female offspring (see Falconer, 1960). McLaren found the heritability (h2)of cephalothorax length of adult

124


females at 10°C was 0.93 (significantly different from 0,P OeOl), based on male parents. This is extraordinarily high, and indicates that size (which we have already shown to be little influenced by food supply) under uniform conditions a t 10°C is almost entirely genetically determined. Most interestingly, the female contribution to size of her offspring (which is normally greater than that of the male in most such experiments, because of non-genetic maternal effects) was very small and not significantly different from zero. McLaren (1976b) suggests that this result is related to size-assortative mating. A further development of our understanding of the continuous variation in size of Pseudocalanus near Halifax, Nova Scotia, comes from the recent demonstration (McLaren,1976b) that size of females in the smaller range (ca. 0.8-1.05 mm in Fig. 23) is strongly correlated with cellular DNA contents. This suggests that the continuous variation iii body size is a result of continuous variations in cell size, caused by the continuous variation in nucleus size. N

F. Body composition and weights The composition of the marine plankton has been extensively studied, sometimes with little obvious application to problems of growth, development and production. Much of the literature on copepods is reviewed by Ikeda ( 1 974), but there is little information on Pseudocalanus. Here we will review what is known, and will focus ontjhat which is useful in describing the size and growth of the animals. This approach leads into a consideration of oil storage in the next section. 1. Wet and dry weights Wet weights are probably unsatisfactory as a measure of size of Pseudocalanus. Marshall and Orr (1966) give a range of estimates of from 50% to 80.7% water (mean 72.3%) for 15 lots of C IV, C V, and adult female animals. Nakai (1955) lists a value of 87.7% water for a very large lot of unstaged animals. Ikeda ( 1 970) gives a mean wet weight of 40 pg and a mean dry weight of 12 pg (i.e. 70% water) for one lot of 80 adult females and 8 adult males. Harris and Paffenhofer (1976) used ash-free dry weights as a measure of size in their experiments with Pseudocalanus and state that the average animal was 12.8y0 ash. Ilceda (1970) found that the ash-free weight of the above-mentioned lot of Pseudocalanus was 9.66 pg/animetl (i.e. ash was 20y0 of total dry weight). Nakai (1955) found that ash was only 2.3% of dry weight of his samples, and Laurence (1976) obtained a value (mean S.D.) of 8.50 f.0.11%.


125

2. Calori$c content Martens (1975; see also Kraneis and Martens, 1975) has measured

calorific content of Pseudocalunus. He expresses his results in a regression on carbon (dry wt in pg) as: cal = 0.023 0.0067 x carbon. Assuming that the relationship is actually a proportional one, 1 pg C = 0.011 cal. This agrees well with an estimate of 4.6 cal/mg dry wt (at 50% carbon, giving 1 pg C = 0.009 cal) in Greze (1970) and with a mean (& S.D.) of 5-07 5 0.18 cal/mg dry wt (5-54 & 0.20 cal/mg ashfree dry wt) in Laurence (1976).

+

3. Lipid and protein

Substantial work has been done on the lipid and protein fractions of copepods, but only the work of Nakai (1955) seems to have dealt with Pseudocalanus. For a large number of animals he calculated that fat was 17.3% of dry weight and protein 71.5%. This estimate of fat content cannot be taken as average for purposes of calculation. The variability of lipid (in the " oil sac ") is implicit in some of the following sections. Nothing seems to be known of the qualitative aspects of lipids in Pseudocalanus although other copepods have been extensively studied. The composition of body proteins of Pseudocalunus has evidently not been studied. However, Jeffries and Alzara (1970) have assayed free amino acids in this and other copepods, largely in the context of environmental salinities. They detected all the standard amino acids except cystine and ornithine. Glycine was about one-third and proline about one-fifth of the total, and taurine, alanine and arginine were also well represented. The total free amino acid (about 550 pmoles/g dry weight) was about as expected for marine fornis, but the predominance of the two above-mentioned amino acids gives Pseudocalanus the highest index of " biochemical dominance " and the lowest index of " biochemical diversity " of the six species studied by Jeffries and Alzara. They believe that this is related to its euryhalinity and general adaptability (p. 2 5 ) . 4. Carbon, nitrogen, phosphorus, hydrogen and silicon

Some elements have been used as measures of size, biomass and condition " in studies of growth, production and excretion of copepods. Carbon was estimated by a wet-ashing method to be 49% by regression on individuals of dry weight between 3 and 30 pg by McLaren (1969). These were formalin-preserved animals and had lost "

126


much of their lipid. Two lots of unpreserved animals from Ogac Lake (where little lipid is found in the copepods) deviated little from the overall regression. Ikeda (1974) gives estimates of 45-1-46.5% C for four samples of individuals (stages not given) taken in May and June 1971, off Japan and weighing 10.7-16.4 pg in dry weight. Another four samples of C V taken in September 1970, weighed 25.5-27-9 pg/ individual and were 63.3-66-7 % C. Ikeda’s samples were fresh-frozen and analysed by gas chromatography. The very high C values in the September sample were presumably attributable to high lipid content in large oil sacs. Indeed Ikeda illustrates an individual stage V copepodid from the September sample showing a very large oil sac. Martens (1975) gives a regression of carbon (C) on dry weight (W) as: C = 2.27 0-187 x W (expressed in the same weight units). However, such a regression might more properly be fitted through the origin. His mean estimate is 36% carbon, with wide variations. To convert Pseudocalanus dry weights to carbon, Paffenhofer and Harris (1976) use conversion factors of 30% for N I-C I, 34% for C I-C 111, and 37% for C 111-adult. However, they later (Harris and Paffenhtifer, 1976) make it clear that these estimates are based on the much larger Calanus helgolandicus from California. We suggest that dry weights of Pseudocalanus when they are not very lipid-rich are about 50% carbon. I n calculations of growth and production, it may be better to consider the highly mobile lipid carbon separately. Ikeda (1974) determined that nitrogen was 11.4-12-4% of dry body weight of Pseudocnlanus in MayJune and only 6.4-7.2% in September. The low C :N ratio in September is presumably due to high fat content (see above). Christiansen (1968) reported higher N contents for NV-VI (dry w t 0.60 pg, 15% N), CI-I11 (2.73 pg, 27% N), C V (9.75 pg, 28% N) and adults (14-42 pg, 20% N). These animals, unlike those analysed by Ikeda, had been feeding in the laboratory. We have shown (p. 45) that feeding animals produce substantially more NH,, and the high N values in Christiansen’s animals may in part represent gut contents. Martens (1975) gives a regression of nitrogen (N) on dry weight (W) as : N = 0.477 0.027 x W (expressed in the same weight units). The average N content was 6.5% of dry weight. Butler et al. (1969) reported that N was 7.8% of dry body weight in “ mixed small copepods ”, which were in fact almost all C IV and C V Pseudocalanus. We suggest that a figure of 7% N for ‘‘ average ” unfed Pseudocalanus might be used. Hargrave (1966) lists phosphorus contents for starved animals as 0.58 pg for copepodids and 0.01 for nauplii; this seems high. Butler

+

+


127

et aZ. (1969)give the only estimate known to us of P as a per cent of body weight of Pseudocalanus (see above qualification) : 0-61% of dry body weight. Hydrogen content wa8 estimated by Ikeda (1974),who found that, as might be expected, it varied with carbon. He found C:H ratios of 6.5-6-9:l in samples from MayJune and 6-6-6.9:l in September, evidently unaffected by amount of fat present. Nakai (1955) lists SiO, as constituting 0.04% of dry weight of Pseudocalanus. Although they have been studied in the marine plankton, we can find no information on other elements in Pseudocalanus. 5. Weight-length relationships

A number of authors have listed weights or other measures of body size for various purposes. We believe that cephalothorax length is often the most useful measure of size, not only because it is easier to determine, but because it is not subject to variations due to food contents, oil storage and preservation effects. Given this variability, it may be better for some purposes to calculate weights from a general weight-length regression. Krylov (1968) determined the weight-length relationship of a variety of formalin-preserved copepods (unfortunately total length in mm and wet weight in mg). He found that K in the expression, w t = K (length)3was roughly the same for all copepodid stages of a species. He gives two estimates of this constant for Pseudocalanus : 364 for White Sea animals, and 336 for Black Sea animals. Robertson (1968)gives dry weight to length relationship for seven samples of " Para-Pseudocalanus " in which the calculated exponent (2-13) is substantially less than the above. The size range of his samples (means 0.70-0.91 mm) was probably too small for an accurate determination. McLaren (1969) showed that the exponent in the weight-length relationship was greater than 3.0 (from his original data, 95% c.1. 3.40-3-88)for a much greater size range of formalin-preserved specimens (C 111, C IV, CV, adult 3 and adult $2) from the Canadian arctic : dry wt in pg = 11.9 (cephalothorax length in mm).3*64 The greater-than-cubic exponent is also implicit in observations that large Pseudocalanus are relatively wider (McLaren, 1965). We suggest that the above formula is much the most reliable available. It applies to " lean " animals, and may be a good indicator of weight for various metabolic contexts. However, there is no doubt

128


that unpreserved animals may be heavier than predicted by this regression. The mean weights of four lots of preserved animals from Plymouth (Conover, 1959) averaged only 7% higher than predicted by the above equation from their lengths. Weights of 13 unpreserved samples from Loch Striven (Marshall and Orr, 1966) average fully 67% larger than predicted. We suggest that the difference is due to fat contents. 6. Weight of eggs Adults do not grow (although females may increase their store of oil ; see next section), but females do produce eggs. Two lots of preserved eggs from southwest Baffin Island gave almost identical dry weights of 0.30 and 0.31 pg per egg (McLaren, 1969). Clutches from this locality averaged about 70 eggs with a total volume of about 0.65 mm3 (Fig. 19B). This allows us to write a general relationship for all localities from Fig. 19B : Dry weight of clutch in pg

=

6.35 (cephslothorax length in mm).4*1s

G. Oil storage The oil sac in Psezcdocalanus in nature can vary greatly in size from non-existence t o a condition where it almost fills the body (see illustration in Ikeda, 1974). Some laboratory studies have been made on possible sources of variation. Lock (1968) carried out rearing experiments on C I11 animals captured in nature, in an effort to determine the effects of temperature on size (seep. 120). He also measured the oil sacs in animals maturing in one experiment. He approximated the size of oil sacs by making models of them on a scale of 100 :1with modelling clay, and determining volumes by displacement. More oil was stored at low temperatures (Table XXIV), a t which temperatures females, but not males, were also larger in body size (p. 120). Because of great variability among individuals, this effect is only significant (p < 0.05) among males. The size of oil sacs is significantly smaller (p < 0.01 at 5 and 10°C) in eggbearing females, suggesting that other (unfertilized) females had not used their oil store in oogenesis. The size of oil sacs in males and females a t alternating temperatures of 8-12°C (mean 10°C) was larger than for animals raised at 8" and 12", but because of great variability, the effect fell short of significant. Even so, there is a hint in these results that some sort of energy bonus may accrue from alternating temperatures.

129

THE BIOLOGY OF PSEUDOCALANUS TABLE

XXIV.

OIL STORAGE IN Pseudocalanus ADULTSREARED FROM TAKEN IN NATURE.(From Lock, 1068.)

CIII

Mean size of oil sac in p 3 >: l o 0 f 95% c.1. (no. measured) Temperature "C 5 8 1On 12 a

Males 7 . 3 & 1.69 (18) 4.3 f 1.75 (10) 4.8 1.42 (25) 1.6 & 0.91 (16)

Females without eggs

Females with eggs

9.2 f 3.08 ( 7 )

4.6 f 3.90 (8) 1-7 f 1-06 (16) 3.6 f 2.59 (13) 2.0 f 1.33 (12)

-

11.6 f 2.41 ( 7 )

-

8" for 12 h, 1 2 O for 12 h each 24 hour during rearing.

Corkett and McLaren (1969) found that oil sacs of adult females in the laboratory were more-or-less constant in size a t given food levels during the period of egg production. Generally the oil sacs became smaller and sometimes even disappeared altogether before death. Experiments with a small number of females suggested that oil sacs did not increase much in size when food concentrations (Isochrgsis galbana replenished weekly) were increased beyond 1 x lo5 cells/mI, but that they were very small or absent at food concentrations of 3 x lo4 cells/ml or less. As we have shown elsewhere, at these low food concentrations eggs are not produced at the maximal rate (p. go), and development rates may be retarded (p. 112). Paffenh6fer and Harris (1976) noted well-developed oil sacs in all copepodids and adult stages at food concentrations of 50, 100 and 200 pgC/l., and by inference not in those reared at 25 pgC/l. At 25 pgC/l. time to adulthood was slightly longer (p. 113) and adult males weighed less (p. 123), perhaps due to reduced oil content. Observations of occurrence and sizes of oil sacs in Pseudocalanus in nature may thus be of great importance, for we believe that the presence of an oil sac in copepodids (except when they are overwintering and perhaps " resting '' in some sense) indicates that development is proceeding a t a temperature-determined rate. This has to be verified. Similarly, we believe that oil sacs in adult females may mean that they are producing eggs at maximal, temperature-dependent rates (cf. p. 98).

H. Growth rates Growth rates are implicit in the previously described observations on development rate, body size, and length-weight relationships. For example, for animals from Halifax the length of C I11 animals and A.Y.B.-16

7

130


the length increment to adult females has been given on p. 120 and in Table XXII. We assume that each copepodid stage takes the same amount of time as does embryonic development a t each given temperature (p. 109, Fig. 22). From these times and the estimated weights (equation, p. 127) of the C I11 and adult animals, the instantaneous coefficient of increase (k)of dry weight on a daily basis (t is time in days between stages) can be calculated from the weight of the earlier stage (W,) and weight of the later stage (W,) from : W, = Woekt. Then, 100(ek-1) gives growth rates as percentages. of body weight per day which is convenient for comparison with the practice (which we have followed) of giving rations, respiration losses, etc., in this form. For Pseudocalanus C I I I to adult female from Halifax, these are then approximately 7, 10, 12, 14, 15 and 17% of body weight per day at 0", 3", 6", So, 10" and 12.5". The same procedure can be used for Pseudocalanus (sexes combined) from the southern North Sea, using data from Thompson (1976). The regressions for length (L) on temperature (T) between 8 and 14°C are from Fig. 27 (insert): L = 0.4270-00264(T-11-74) for C I ; L = 0-577-0*00336(T-ll.74) for C 111; L = 0.900-0-3452 (T-11-74) for adults. Using the same procedure as for the Halifax animals, growth rates for C I to C I11 are estimated at 16, 19, 25 and 32% ,at So, lo", 12.5" and 15OC respectively. For the period between C I11 and adulthood (both sexes combined), the estimates are 16, 18, 18 and 17% respectively at the same temperatures. It can be seen that growth rates increase with temperature among older copepodids in the Halifax population, but not in the North Sea animals. This is because the negative effect of temperature on size is especially marked in the North Sea animals. Clearly, different populations will exhibit quite different responses of growth rate to temperature, depending largely on the size-temperature relationship. Paffenhafer and Harris (1976) estimated instantaneous growth rates a t 12.5OC directly as increase in ash-free dry weights of copepods. They indicate that little fat is included in these estimates. We have already discussed their observations that food had no effect on development rate, except at the lowest concentrations used by them (p. 113), and that low food levels had little effect on weight of adult females, but more on adult males (p. 123).Table XXV summarizes their findings on effects of food on growth rates, converted from instantaneous rates to percentages of body weight per day. The manner in which they evaluated naupliar weights is not evident, as young nauplii may not feed (p. 112) and may lose weight during early stages. The low growth rates between C I and adult a t a food level of 25 pgC/l. are probably related to the smaller size of adult males and slightly retarded develop-


131

ment rates a t this level (Paffenhofer and Harris, 1976). The high values for C I-C I11 and low values for C III-adult at food levels around 50 pgC/l. are interpreted by Harris and Paffenhsfer (1976) to mean that older copepodids are less able to secure rations a t this low food level. However, it is possible (since the rates for C I-C I11 are unusually high) that experimental error is involved. At any rate, the extreme rates at 50 pgC/l. tend to cancel out, giving overall rates of 18-23% growth of body weight per day between C I and adult. There is thus excellent agreement between growth rates at 12.5" given by Paffenhofer and Harris (1976) and those estimated above from the work of Thompson (1976) for animals from a nearby part of the North Sea. We therefore feel that laboratory or field estimates of the relationship between size and temperature in any given locality are all that is required (given the relative invariance geographically of development rate in relation to temperature) to calculate potential growth rates in nature when the food supply is adequate.

I. Rate of prodwetion of egg matter Adult males may not feed (p. 114), but adult females certainly do. Yet they cannot grow in the usual sense after the final moult to adulthood. Paffenhofer and Harris (1976) and Harris and Paffenhofer (1976) make a curious attempt to calculate growth rates of adults from " 50% adult to full adult ". This may compound the effects of larger adults maturing later, oogenesis and possibly fat deposition, and the very small estimates of growth rate do not appear to be very useful. The most significant use of food by females is surely in egg production. It is possible to determine the potential rate of production of egg matter in the same terms that we have used for growth of body dry weight. As an example, we use Thompson's'(1976) data, from which cephalothorax length (L) of an adult female (note that the regression in our Fig. 27 is for adults of both sexes) is given as a function of temperature (T), when greater than S"C, by:

L

= 0.939

- 0.0322 (T - 11.57).

Dry weight of adult femalesis calculated from the expression on page 127 and weight of their clutches from formula on page 92. Time between clutches is assumed (see p. 128) to be 1-25 multiplied by the duration of clutches (Fig. 22). This allows us to express amount of egg matter produced per day as a percentage of female weight, which is determined by the given temperature. These values are lo%, 12%, 14% and 16% per day at 8, 10, 12.5 and 15°C respectively. These estimates for the

132


southern North Sea are thus not far short of those for growth rate of older stages given in the previous section. Since eggs may be more calorific than most body tissues, egg production might be nearly equivalent to growth of younger stages.

J. The ‘‘ balance equation and growth efliciencies ”

There have been a number of attempts with zooplanktonic species to determine growth rates and the various efficiencies involved by estimating values of the components in the “ balance equation ” of growth (review in Conover, in press). The general equation can be written : G=I-E-U-R where G is growth rate, I ingestion rate, E egestion rate (faecal production), U excretion rate and R respiration, all in the same units. Gross and net growth efficiencies are respectively the proportions of I and of I - E that appear as G, all in the same units for a particular time period. These efficiencies are sometimes calculated by use of information on chemical composition, respiration, excretion and population data. The only such calculations known to us for Pseudocalanus are in Christiansen (1968). He used nitrogen contents and excretion rates to estimate a gross growth efficiency of 74y0and a net growth efficiency of 12.3% for the interval N V to adult for animals in Bras d’Or Lake, Nova Scotia. The values are at best approximate, since some components were calculated by difference from outmoded observations. We have described assimilation efficiencies (I-E),/I, averaging about 65% in Pseudocalanus (p. 76). Respiration losses (R) have been estimated to amount to about 10% of body weight per day (p. 43). As Conover (in press) points out, we seem to know least about the significance of excretion (U) in terms of the balance equation of growth. Dissolved organic N and P might be represented by an equivalent loss in body weight, but even NH, excretion involves some loss that is not expressed in respiration. It has been suggested that about 5% of body N (p. 49) and about 10% of body P (p. 51) might be required each day by Pseudocalanus for maintenance. Perhaps 213 of the P might represent organic loss (p. 49) and a small amount of N (not measured in Pseudocalanus) likewise. A figure of 10% of body weight for U is probably generous. The work of Paffenhofer and Harris (1976) showed that older stages of Psewdocalanw may grow (Table XXV) at about 10% to 17%

133


TABLEXXV. EFFECTSOF FOODSUPPLY(Thalassiosira rotula) RATESOF Pseudocalanus FROM THE NORTHSEA. (After Paffenhofer and Harris, 1976.) Growth as N o . of experiments 1 2 4 1

Food

cone.=

ON

GROWTH

yo body wt/day

(pgC/Z.)

Hatching to CI

C I to end c III

End C I I I to adult

25 50

20 15 16-17 20

12 30-46 22-37 19

11 4-7 17-21 17

100 200

Nominal levels; actual levels deviated somewhat.

of body weight per day at ingestion rates (Fig. l2F) of 60-140% per day. Entering these values as G and I along with the above estimates for E, R and U, we can see that the balance equation may in fact be balanced only at the lower ingestion rate of 60% of body weight per day. Harris and Paffenhofer (1976) have fortunately estimated gross growth efficiencies directly from measurements of ash-free dry weights of accumulated rations and of growth in the same units during various intervals between hatching and adulthood (Table XXVI). Paffenhofer and Harris (1976) concluded that daily ingestion rates continued to increase at food levels above those at which growth rates did not increase further. This should lead to reduced growth efficiencies (probably due to reduced assimilation efficiency) at higher food levels. Although Harris and Paffenhofer (1976) found that the regressions of growth efficiencies for various developmental stages on food concentrations were all negative, none was significantly different from zero a t the 5% level. However, since the estimates of daily ration were based on large numbers of measurements, the reduced efficiencies implied in the work of Paffenhofer and Harris (1976) might on analysis prove significant. I n other words, we suggest that the lack of significance between growth efficiencies and rations in Harris and Paffenhofer (1976) results from unnecessary grouping into reduced sample sizes. At any rate, the results in Table XXVI may be taken to imply gross growth efficiencies of the order of 25% at food levels that are comparable to those occurring routinely in coastal waters. I n order to grow at rates of 10-20% per day, or produce egg matter at about the same rates, a copepod must thus consume at least 4 0 4 0 % of its weight per day. Most laboratory studies of feeding rate have not revealed such high values for daily rations (p. 72).

134

CHRISTOPHER J. CORKETT AXD IAN A. MCLAREN

TABLEXXVI. GROSS GROWTHEFFICIENCIES OF Pseudocalanus. (After Harris and Paffenhofer, 1976.)

Nominal food level WCP. Thalassiosira rotula 25 50 100 200

Number

Mean growth eficiencies

of

experiments

N I-C I

C I-C 111

C 111-Adult

1 2 5 2

24.7 25.8 24.4 25.6

39.7 24-7 24.8 25.8

21.5 27.1 20.1 14.5

K. Retrospects and prospects It is we think possible that more is known about the growth and development of Pseudocalanus than of any other copepod. There have been a number of themes in the work that we have reviewed that are only now coming into a coherent focus. First of all, the work on Pseudocalanus stresses the great importance of temperature in the control of growth and development of planktonic animals. I n the zooplankton literature in general, there has often been more stress on food and feeding and a tendency to carry out elaborate experiments a t single temperatures, instead of attempting to determine the temperature functions of growth processes. Secondly, as already noted (p. 133), we believe that most estimates of feeding rates in the laboratory are too low to support observed growth rates, such as those found by PaffenhOfex and Harris (1976). We will later argue (p. 155) that Pseudocalanus can develop and grow a t temperature-dependent rates in nature, indicating that no shortage of food occurs during large portions of the year. Thirdly, we have shown that approaches to questions of growth and development through the " balance equation ", admittedly somewhat desultory in the case of Pseudocalanus, are outclassed by the direct approaches of Paffenhofer and Harris (1976). Respiration, excretion, assimilation and grazing are all of interest in their own right, but are unlikely to give a very accurate appraisal of the growth status of the animal in nature. Finally, we suggest that the conclusion that Psezcdocalanus frequently grows at maximal, physiological rates in nature may be true of other important copepods as well. We believe that use of temperature functions of size and development rate and perhaps simple transforma-


135

tions between species based on size (Corkett and McLaren, 1970), or perhaps DNA content (McLaren et al., 1966), will lead to powerful, predictive techniques for the future.

XI. LIFE CYCLESIN NATURE A. General features, terminology and approaches We have learned enough about the biology of Pseudocalanus from laboratory studies to know that even the most obscure or complicated life cycles must have some general features. It will help to review these before considering examples from nature. The nauplius emerges after an embryonic duration that is controlled by temperature (p. 101). The individual may develop after a temperature-dependent time up to N I11without food (p. 112), but any further development cannot occur without food. Above a certain threshold level of food supply, development will proceed at a temperature-dependent rate. If food is sustained, each copepodid stage may take roughly the same amount of time that is required for embryonic duration at the given temperature (p. 109). Mating must occur shortly after the females moult into adulthood (p. 83) and her first eggs may appear after moulting on average about the time taken for embryonic duration (p. 92). The female carries sacs or masses of eggs that constitute a clutch of eggs. If food is sustained, females may in theory produce up to ten or so clutches (p. 93), but this number is probably seldom achieved even in continuously breeding populations, because of natural mortality. A new clutch can appear after the previous one hatches, and after a further lapse of on average about 25% of the time taken for embryonic duration a t the given temperature (p. 93). Each clutch gives rise to a brood of young and all the broods produced by a female belong to the same generation (sometimes wrongly called a brood in the plankton literature). Although the time between hatching and appearance of first eggs has been called generation time in the literature on zooplankton, including Pseudocalanm (e.g. Paffenhsfer and Harris, 1976), this is incorrect. The true length of a generation is technically difficult to calculate, and we will find no use for it in this account. Nevertheless, the appearance of successive generations can often be recognized, as we shall see. We distinguish the productive season as that time of the year when growth, development and reproduction are sustained. Pseudocalanus suspends development during winter at high latitudes and may dis-

136


appear, at least from inshore waters, during summer in the southern parts of its range. We shall present evidence that animals may store much oil and " voluntarily" suspend development in summer or autumn. We refer to these animals as being in " resting stages " although we do not imply that they give up all activities. Because of such periods of rest, the productive season tends to start with a population of animals that are largely at the same stage of development, generally late copepodids or adults, so that the initial and even subsequent generations can be more-or-less synchronous. We shall show that at high latitudes where development is slow this synchrony of life cycles allows us to identify, not only generations, but also more-or-less synchronous broods within these generations. Such a nearly simultaneous spawning gives a cohort (a generation or even a single brood) of animals that can be identified in sequential samples. Although attempts have been made in the literature on Pseudocalanus to infer life cycles from counts of various stages in temperate waters, this is much more difficult. Females may spawn a series of broods that nre unlikely to be synchronous, so that it is not possible to follow a single cohort of offspring through successive developmental stages. However, we can take advantage of two facts : (1) even when younger stages develop rapidly and are ephemeral, adult femsles are long-lived (p. 114) ;and (2) the size of adult females is strongly affected by seasonal differencesin temperature (p. 11 6). Thus where generations are more-orless synchronous and successive, there should be periods when female size is stable, followed by periods of rapid change in size, followed by periods of renewed stability at a new size. We shall see that this is precisely what is observed when samples are taken with sufficient frequency. Most attempts to describe life cycles have been based on samples taken in the open sea, where exchange of water and populations with different histories makes interpretation more difficult. Only Fish (1936), working in the Gulf of Maine, has attempted to follow life cycles while tracing presumed movements of populations in a, region. Studies in semi-enclosedbodies of water (Marshall, 1949 ; Carter, 1965 ;McLaren, 1969) have produced the most detailed and accurate information, giving us insights into life cycles elsewhere.

B. Representative life cycles 1. Tanquary Fiord, Ellesmere Island The most extreme environment in which Pseudocalanw has been studied in detail is Tanquary Fiord, at 81'N in the high Canadian arctic.

137

THE BIOLOGY OF PSE UDOCALAN US

Here Cairns (1967) took a series of samples with fine-meshed nets in 1964 and estimated the relative abundance of stages (Fig. 28A). At the beginning of the season, in late May, at least some adult females had already reproduced, but the young were “ stalled ” in NIII (which can be reached without food). After the first week of June, wasting of the snow-cover over 2-5 m of ice allowed light to penetrate the water, and development of these nauplii commenced.

.

...

EGGS-=

.

.

I

-

I

I

~

’

. ,

I

I

I

I

U

Tessiarsuk

,

NO/m2 -0

10

May

20,000

20

I June

July

Aug.

Sept.

FIG.28. Life cyclos of Pscudocnlanws in three localities in northern Canada as shown in the development of stages in samples from successive dates. Cohorts are traced as G,B,, where n is the generation number and m is the number of a brood within this generation. (A, after Cairns, 1967; B, after McLaren, 1969; C, after Carter, 1965.)

At the same time, a group centered on C I11 began to develop. Later in the season, a second mode of nauplii appeared, but did not gain much development before the end of the seaaon. We suggest that these two modes of nauplii represent respectively two groups of more-or-less synchronous clutches produced by the female population, which was clearly dying out by the end of the season. We have accordingly labelled these cohorts as G,B, and G,B, (as first and second broods of generation 2). We agree entirely with Cairns (1967) that the frequency distribution of stages can only be interpreted as reflecting a two-year cycle in this

138


population of Pseudocalunus. The oldest animals (Go) represent a generation that was born two summers previously. The mode of copepodids advancing from C I11 to C V during the summer (GI) represents a generation that was born in the previous summer. The older mode of the current generation (G,B,) advanced to C I I by the end of the summer. Each of these generations need only advance one more stage to achieve the level of development found at the beginning of the 1964 season. The younger animals (G,B,) presumably would die out. Although only coarser-net ( # 6) samples were available to Cairns from 1963, the patterns among copepodids were similar to those of 1964: adults and a mode a t stage I11 were present a t the beginning of the season, and modes at C V and C I1 a t the end. Cairns also noted that a few small individuals disappeared from C IV and C V largely before mid-June and appeared as small adults (mean ca. 1 mm) among the large ones (mean ca. 1.2 mm) thereafter. He suggests two possible explanations. The small animals may represent a basically annual form, perhaps genetically distinct (see p. 113). Or, they may represent the persistence of a limited number of individuals from the second seasonal brood of two years previously (i.e. a putative GOB,). Surface waters warmed from about -1°C on 12 May to +l"C on 25 August 1964. Although this does not seem to be a large difference, the size-temperature response in these cold waters is very steep (Fig.' 26), and could readily explain the difference in sizes. 2. Ogac Lake, B a B n Island

The most detailed study of Pseudocalanus in a high-latitude setting was made by McLaren (1969), who was able to follow life cycles of isolated populations in three basins of Ogac Lake, a landlocked fiord on Baffin Island a t 63"N. The cycle in the innermost basin in 1957 is summarized in Fig. 28B. The overwintering Go matured rapidly in mid-June, large numbers of eggs (G,B,) appeared on 18 June, and it can be inferred that G,B, largely died out in summer, and that GIBl formed the basis of the overwintering generation. McLaren (1969) concluded from size-frequency distributions that almost all adult females in early August were Go, and that they were largely replaced by G,Bl in mid-August, so nauplii in late August were members of a new generation, as indicated in Fig. 28B. Perhaps some of G,Bl participated in the overwintering group. Life cycles in the middle and outer basins of Ogac Lake in 1957 were also basically annual (McLaren, 1969). Because it is more productive than the inner basin, G,B, in the middle basin largely matured by

THE BIOLOOP OF PSEUDOCALANUS

139

late August, and GIB, reached older copepodid stages. The outer basin is more productive than the middle or inner basins, but colder, so that development of three broods was sustained, although slow, during summer. I n late August, a tidal incursion greatly reduced the population, and in mid-September the potentially overwintering older copepodids were derived from G,B, in the outer basin. The pattern in the middle basin in 1962 was similar to that of 1957, except that a third brood, G,B, was sustained and reached late naupliar stages by mid-August. McLaren (1969) showed that the frequencies of individuals in designated broods were about as expected if each of the females in the same samples had produced a clutch of a size determined by their mean body size (see p. 96). That is, each brood did indeed represent a more-or-less synchronous production of full-sized clutches by the entire adult female population. The time between broods was about as expected from the prevailing temperatures in the lake (see p. 97). The observations thus indicate that reproductive rate was maximal during the short period in early summer when food was above some threshold, but was negligible thereafter. Evidence from an experiment with fertilized polyethylene columns suspended in the middle basin in 1962 showed that production of G, was dependent on the size and abundance of females of Go, not on the amount of food that was present during the productive season (McLaren, 1969). I n the fertilized columns, GIBl and G,B, completely matured and GIB, reached late copepodid stages by early August, when a massive G,Bl appeared before termination of the experiment. The appearance of second summer generations in all basins of Ogac Lake, and especially in the fertilized column, indicates that the basically annual life cycle in these Pseudocalanus from high latitude need not be intrinsically controlled. That is, there is not some obligatory resting or overwintering stage a t the end of summer. I n the warm waters of Ogac Lake, the tendency for unseasonable and wasteful maturation and reproduction at the end of summer may be more pronounced than it is in colder waters of the seas outside. Woods (1969) suggested that the large forms in Ogac Lake and in the similar Winton Bay represent evolutionary attempts to restore normal arctic size and slower development rates in these unusually warm waters. I n support of this, she showed that two broods of the previous summer were represented in the overwintered generation of the large form in Ogac Lake in 1962, and that G,B, of the large form only reached young copepodid stages by early August, whereas (see above) G,B, of the small form had matured by this time. This means that the earliest broods of the large

140

CHRISTOPHER J. CORRETT AND IAN A, MCLAREN

form (and therefore those produced before overwintered females have suffered further mortality) are the most successful ones. 3. Tessiarsuk, Labrador Carter (1965) studied the life cycle of Pseudocalanus in Tessiarsuk, a landlocked fiord at 56'30" in northern Labrador. Here, as in Ogac

Lake, there were advantages of sampling an isolated marine population. At the beginning of the 1961 sampling season in the outer basin of the lake, the first brood of young had already developed to a mode at C I (Fig. 28C). Adult females (Go)during early summer were distinctly bimodal in size (means of about 0.75 and 0.95 mm in Carter's Fig. 5). The smaller females had presumably matured in the warmer waters late in the previous summer, whereas the larger ones had overwintered as copepodids and matured in the colder waters of spring and early summer. The disappearance of the small females after the beginning of August presumably signals the replacement of Go by newly matured individuals of G,B,, but not before Go had produced a second burst of clutches, G,B,. The young in September are clearly a new generation, G2BI. Samples taken by Carter (1965) in the following spring, on 10 April 1962, showed much reduced populations, with modes at C I11 and N 111. This suggests that most of G,B, had died out, and that the founding generation in 1962 originated largely in G,B, o i the previous summer, as in Ogac Lake. The presence of only a single size group of large (m. 0.95 mm) mature females on 19 May also indicates that all of them had matured from copepodids in the cool waters of spring. Carter suggested that copepodids in the lake in spring 1962 were probably remnants of G,B,, which would imply a basically semiannual cycle. Our analysis implies that G,B,, already " stalled " as nauplii in early September, died out during winter. The life cycle in the somewhat isolated inner basin of Tessiarsuk was very similar to that depicted above, except that GIBz was slightly more difficult to discern in midsummer, possibly due to sampling errors in this larger, deeper basin. The frequency distributions of stages at the end of the 1961 season and a t the beginning of 1962 were almost identical to those found in the outer basin. The life cycle in Anaktalik Bay, outside Tessiarsuk, did not show the same clarity as those in the lake. Both early and late naupliar maxima appeared, but whether these represented successive broods or generations cannot be discerned. A marked scarcity of older copepodids and adults, except at the beginning of 1962, suggested to Carter that most adults may have matured and spawned outside Anaktalik Bay.


141

4. Other arctic local~ties No other populations from arctic waters have been studied in the detailed way of those from Tanquary Fiord, Ogac Lake and Tessiarsuk. However, the few other studies in general conform to one another. Grainger (1965) indicates that breeding and development of Pseudocalanzts in the Arctic Ocean were unknown, and we know of no subsequent studies. Ussing (1938) and Jespersen (1939) found that the overwintering stock in fiords of East Greenland matured and began to breed in April and May, with egg-bearing females present until August. Most of G, reached C IV in late summer and overwintered in this stage. A few matured to produce nauplii of G,, probably unsuccessful, in autumn. Digby (1954) found that the cycle in Scoresby Sound, East Greenland, was basically annual small late copepodids giving rise to small adult females in spring, and younger copepodids developing in the cold waters to larger adults in early summer. Some of these large adults live through another winter, thus having an essentially 14-year cycle. A few individuals spawned early in the year may have matured between September and November and have been responsible for nauplii at that time, this G, being probably unsuccessful. Grainger (1959), working in a comparably high-arctic locality in Foxe Basin, northern Canada, found that adult males were abundant only in March through May, and adult females (and their nauplii) were common from April to September. The predominant overwintering stages were C I V and C V. Although Grainger concludes that the cycle was basically annual, he suggests that part of the population may have taken 14 or 2 years to mature. His argument is based in part on the occurrence of a size-bimodalism in C V females, but not clearly in any other stage. The larger size mode occurred between late September and early February, and disappeared at the time of appearance of substantial numbers of adults in the samples. Grainger (1959) interprets size differences (probably not correctly) in terms of food supplies, but we can only suppose that the large C V females represent a stock that had developed in colder water, perhaps elsewhere. Fontaine (1955) studied Pseudocalanus life cycles in the subarctic (sensu Dunbar, 1947) waters of Ungava Bay, northern Quebec. She concluded that the cycle was basically annual, but that a small portion reached maturity and spawned during late summer. 5. Loch Striven, Scotland

The magnificent survey by Marshall (1949) is by far the most thorough and revealing study of Pseudocalanus life cycles from tem-

142


perate latitudes. It is based on weekly vertical hauls from 40 fathoms with a fine-meshed (200 mesh/inch) net. Here, the most useful means of delimiting generations is by size changes in successive samples of

1.4

-I

mn

L I

I.2

1.a

0.e L

0.6

I Jan.

1 March

I

1 May

I

I

July

I

I Sept.

I

F I ~29. . Relative abundance of C IV and egg-bearing adult female Pseudocalanus, and length-frequency distributions of adult females in samples from Loch Striven, Scotland, with temperature data. Frequency scales of histograms varied and some samples left out for clarity. Generations designated as G,. (Data from Marshall, 1949, and Marshall et al., 1934.)

adult females. By reanalysing her data and expressing them in different ways, we have come to conclusions that extend or are a t slight variance with her own. Figure 29 summarizes much of what we have to say. As Marshall herself concludes, it seems clear that the adults (Go)at


143

the beginning of January trace their origin from warmer waters in the previous autumn. Some 50% of the overwintered animals at this time were in C V, and the slight size increase of adult females in subsequent weeks is a consequence of maturation of these small C V animals at the cooler temperature obtaining in late winter. By 20 February the proportion of egg-bearing females showed a sharp increase, and this proportion was generally maintained until early August. We can define the productive season in terms of sustained high egg production as late February to early August. The appearance of the new G, spawned and developed in cold waters is dramatic, and shows little overlap with the females of the overwintered generation. Subsequent generations of adult females were spawned in increasingly warmer waters, and this is expressed in diminished size through the season. If successive generations retain any of the synchrony evident in the appearance of G,, this should be expressed as a series of persistent size modes, representing the females of the current generation. Between these periods of persistent size, there should be periods of rapid change of size, as females of the new generation replace those of the previous one. This is precisely what is observed in Marshall’s (1949, her Table X) data. Provided a suitable spacing of samples is chosen (there is not room for all her samples in our Fig. 29), the succession of generations appears very convincing. I n each case, we have included the first and last samples in which a particular dominant size mode is expressed. We infer that during the productive season in Loch Striven, there were six successive generations (Gl-G,) of Pseudocalanw. Although useful in suggesting maximum reproductive rates in nature (p. 98), the information on proportion of egg-bearing females (Fig. 29, top) offers little insight into the possible succession of generations. There is perhaps a hint of reproductive decline among old females of Go in mid-March and G, in late April. However, the proportion of C I V in the samples supports our conclusion that six generations of adults were produced. Marshall (1949, her Fig. l ) shows abundance of each stage as a percentage of the total numbers of animals. However, this method of expression is influenced by the highly variable mortality of younger stages and the persistence of adult females, which do not pass through in a “ wave ” of abundance. We have thought it better to express abundance of C IV as a percentage of total copepodids (Fig. 29, top). If the population were at equilibrium and if no mortality occurred during copepodid stages, then C I V on average should constitute 20% of all copepodid stages. Clearly neither of these situations applies and C IV is generally scarcer at the beginning

144

CIXRISTOPHER J. CORKETT AND IAN A. MCLAREN

of the season. However, as the season progresses, and particularly after G,, there is clearly an accumulation of C IV, and we agree entirely with Marshall that these animals have suspended development to form an overwintering stock (Go); at the same time some animals clearly continue to undergo normal development. These animals are evident as a series of peaks, through the season, of C IV. Only in the case of G, is there any ambiguity in these peaks, and all of them fall, as expected, shortly before or around the time of appearance of the new size modes of females. TABLEXXVII. OBSERVEDAND PREDICTED TIMESOF APPEARANCE OF SUCCESSIVE GENERATIONS AND BODYSIZESOF ADULTFEMALE Pseudocalanua IN LOCHSTRIVEN, SCOTLAND.(See text.)

@en. no.

Mean temp “C

Dates

Times between generations (days)

Cephalothorax length (mm)

Observed Predicted 0 bserwed Predicted

G, G2

G, G, G, G,

< 20 Feb-4

April

4 April-15 May 15May-12 June 12 June-3 July 3 July-24 July 24Jdy-14A~g

6-5 8.5 12 12.5 14 15.5

>42

48

42 28 21 21 21

38 28 27 24 22

1-14 1.04 0.99 0.94 0.83 0.78

1.12 1-03 0.89 0.88 0.81 0-75

We now proceed to indicate that the successive generations of animals in Loch Striven were developing at a rate that was temperaturedependent. The first appearances of successive generations are shown in Fig. 29, as are temperatures during the developmental periods of each generation. We assume that successive generations spend their lives nearer the surface than the bottom. This is true of earlier generations and at least of young stages in later generations (Marshall, 1949, her Fig. 15). The times between appearances of generations from the data in Fig. 29 are influenced first by the basically weekly sampling schedule carried out by Marshall during much of the season. Second, the f i s t appearance of a generation of adult females represents the < 108 mg wet weightlday of copepodid and adult Pseudocalanus were produced over the study area in the southern North Sea during the winter-spring sampling period. From her estimate of the area sampled (30640 km2) this is about 1 mg wet wt/m2/day.


187

Since only about 5 % of this would be carbon (see p. 183), the implied production rates seem much lower than those for other localities. Although Thompson's actual measurements do not include egg production and probably contain small weight errors, they represent an admirable attempt to combine production estimates based on laboratory growth data with a sampling programme on a sufficiently large scale to be meaningful for a region. 5 . Baltic Sea

Production of Pseudocalanus in the Gdansk Deep area of the Baltic was briefly reported in a symposium abstract by Ciszewski and Witek (1975). By methods that are not detailed, they estimate that annual production of Pseudocabnus amounted to 137 g wet wt/m2/yr, about 5% of which would be carbon (see p. 183). This estimate is higher than any we have from other regions. The V/B ratio reported by them is 10-3, which seems similar t o those from elsewhere, if 0.103 on a daily basis is meant. 6. Norwegian Sea

Pavshtiks and Timokhina (1972) summarizing earlier work by Timokhina, attempt to estimate the production of Pseudocalanus and other major zooplankton species for the entire area of the Norwegian Sea. To do so, they depended on samples taken from the upper 500 m from two east-west and one north-south section during 1959-63 and 1968-69. They use the method of Boysen-Jensen (as described in modern terms in Winberg, 1971), which is essentially a simplified version of the cohort method for populations with an annual life cycle. The population loss during a year is estimated from samples a t the beginning and end of the annual cycle, and this is multiplied by the mean biomass per individual between the beginning and end of the cycle. To this is added the biomass not yet dead at the end of the cycle. Pavshtiks and Timokhina, however, gave no details on the ways in which they evaluated numbers or weights. Estimates for the Norwegian Sea as a whole, are given in a table as millions of tons. For Pseudocalanus, these estimates (wet w t ? ) ranged as low as 1.57 x lo6 tons in 1961 and as high as 5.28 x 106 tons in 1962. Pavshtiks and Timokhina point out that the method of evaluation gives minimal estimates, and also that the catching efficiency of their plankton nets was unknown. Nevertheless, we consider the attempt to be of interest in demonstrating that approximations can be made even from rather unpromising material.

188

CHRISTOPHER J. COREETT AND IAN A. MOLAREN

7. White Sea

Fedorov et al. (1975) have estimated production of phytophagous copepods, including Pseudocalanus, in the White Sea from a 24 h experiment on 26-27 June 1970, and a 3-day experiment on 18-21 August 1971. During these time periods they made frequent measurements of biomass of phytoplankton and zooplankton species in the 75 m water column and made less frequent estimates of phytoplankton production rates. They followed the approaches of McAllister (1969) to calculate consumption of phytoplankton by zooplankton, using observed phytoplankton production and changes in biomasses of phytoplankton. The rest of their analysis is based on the " balance equation " approach, with coefficients of assimilation and respiration assumed from the literature, evidently with no account of the (low?) prevailing temperatures. They conclude that production by phytophagous zooplankton (of which Pseudocalanus was 26% of the biomass) was 26 mg C/m2/day. The mean P/B ratio was about 0-17 ; the concordance of their ratio with estimates for Pseudocalanus from the Black Sea is of doubtful significance in view of the fact that some of the assumed rates used by Federov et al. are based on Black Sea studies.

C. Retrospects and prospects Although the estimates of production rate in Ogac Lake by McLaren (1969) are probably the least disputable that we have reviewed, the

environment of Ogac Lake is very special and the opportunity for using the cohort method is not available for most of the geographical range of Pseudocalanus. We believe that we have summarized enough information in this review so that production of Pseudocalanus in many localities (some with published data available for analysis) could be estimated with little or no further information, provided that development rate in the population over the period of interest is not limited by food. We have argued in several places in our review that this assumption is probably valid for a substantial part of the year in many temperate localities, and have demonstrated its validity for Loch Striven, Scotland (p. 145) and less completely for a number of other localities (see Section XI). However, the investigator wishing to validate the assumption for any given locality has been given a number of techniques (egg frequency counts, p. 9 8 ; oil sac sizes, p. 129; and especially intensive sampling and analyses of female sizes and perhaps relative number of specific copepodids, p. 143) that might be used. If it can be assumed or demonstrated that food is not limiting, then the


189

following methods (including some approximations and “ short-cuts ”) can be used to estimate the parameters of production. (1) We have shown (p. 11 1) that development rates of the various stages as functions of temperature differ little over various parts of the world, so that Fig. 25A or B might do as approximations. (2) We have shown that volume of a clutch of eggs is about the same function of female length in different regions, so that the potential rate of production of egg matter as a per cent of female body weight is a similar function of temperature everywhere (p. 131). (3) A general weight-length relationship for Pseudocalanus copepodids and adults (p. 127) allows weight estimates t o be made from length, if not made directly. (4)Unfortunately there are no direct estimates available of weights of nauplii. Evans (1977) estimated that “ growth factors ” (length multiples between moults) of 1.17-1.28 (mean 1.22, implying a weight increase of about 1-8 times) apply for Pseudocalanus. Since nauplii contribute very little to overall production, McLaren’s (1969) assumption that they double weight between moults, might do. From weights and stage durations, growth rates of stages can readily be calculated, and applied as P/B ratios to counts or biomasses of animals in samples. It should also be possible to construct purely theoretical models of Pseudocalanus production for various regions, since size-temperature relationships can be added to the above information. Although these are local in application (see, e.g. Fig. 26) they should be readily established from a small number of points from experimental or field data. From estimates of growth rates that we have given for various stages and temperatures, approximations might be made for P/B ratios applying to entire samples. For example, we suggested (p. 130) that older copepodids from the North Sea might grow a t about 17% of body wt/day irrespective of temperature. Younger copepodids and nauplii might be more affected by temperature, but generally contribute little to biomass in nature, so that an overall rate of 20% might do at North Sea temperatures. Production by adult females can be reckoned in terms of egg matter, and is more temperature dependent. Overall, a P/B ratio of 0.20 might suffice for the North Sea for some purposes. None of the attempts to estimate production of Pseudocalanus that we have reviewed take into account all the kinds of information alluded to above. However, there remains a more serious problem for the future of such studies. Only Evans (1977) has attempted (with shortcomings that we have noted) to discriminate generations in the field objectively. Some of the other estimates depend on the assumption that food is in excess, and temperature in control. However, we have also described the way in which overwintering, resting stages begin to accumulate

190


in the population in some regions while other members of the population continue to produce a t maximal rates (p. 144). I n our opinion, the most important work remaining to be done on the production biology of Pseudocalanus (and perhaps other copepods as well) is in the establishment of the “ growth status ” of individual stages in samples from nature. Does stored fat in young stages and in adults denote full production potential? Does fat above certain levels in C IV denote ‘‘ resting ”? Are there other morphological criteria of growth status? Of course, determining production of Pseudocalanus should not be viewed as an end in itself. We know very little about the impact this production has in nature, and what we do know is the subject of Section XV.

XIV. PARASITES A. Dinoflagellates 1. Blastodinium hyalinum Chatton, 191 1

(a) Taxonomy Apstein (1911) described and recorded this genus as ‘‘ Parasit 1 ” in a number of copepods including Pseudocalanus. Chatton (191 1) made observations on Apstein’s work and writes “ Dans le MBmoire que j’achhve, en ce moment, sur les Phidiniens parasites, je lui ai rhservh le nom de B. hyalinum, n. sp.”. Chatton (1911) does not give a description of this parasite in that paper although he does say it is closely related to B. contortum Chatton. I n his large monograph Chatton (1920) refers to this parasite as B. contortum hyalinum which differs from B. contortum in lacking torsion and pigmentation ; when removed from the host gut and left in Bea water this variety dies earlier than B. contortum since it is less resistant. Sewell (1951) from extensive study concluded that Chatton (1920) confused more than one species under the name B. contortum hyalinum. Sewell refers to the parasite discussed here as B. hyalinum Chatton, and confines this species to the form found in the North Sea, which was described but not named by Apstein (1911) and to the forms Chatton (1920) recorded from the Mediterranean. We adopt here the view of Sewell and refer to this parasite as B . hyalinum Chatton. I n addition Sewell (1951) examined a number of specimens of Pseudocalanus collected from the North Sea and confirmed that B. hyalinum infected

Pseudocalanw.


191

(b) Life history The parasite lies within the alimentary canal of Pseudocalanus and initially consists of a single cell, the trophocyte or trophozoite (Fig. 39A). Transverse or oblique division gives two daughter cells, the anterior (i.e. nearly always at the anterior end of the host) becoming Parasite

/

Gut

Secondary trophozoite

I

0

Tertiary trophozoite

C

Secondary layer of sporocytes

I I

A

First layer of sporocytes

/

F m t loyer o f sporocytes

I

Fro. 39. The dinoflagellateparasit,e Blastodinium hyalinum. A, parasite in the gut of a calanoid copepod. B, monoblastic stage from Pseudoculun~. C, diploblastic stage. D, polyblastic stage. (A after Chatton. 1920; B-D after Sewell, 1961.)

192


a secondary trophocyte and the posterior a gonocyte. The gonocyte forms a large number of sporocytes by repeated division (Fig. 39B). The monoblastic stage in the life cycle occurs when the secondary trophocyte is surrounded by one layer of sporocytes on all sides, apart from a distinct gap which may be present and is called by Chatton (1920) the hilum (Fig. 39D). The secondary trophocyte divides into an anterior tertiary trophocyte and a posterior gonocyte, which in turn undergoes repeated divisions to give a second layer of sporocytes lying within the first layer ; this is the diploblastic stage (Fig. 39C). The polyblastic stage is formed when the trophocyte continues to divide, ultimately into a number of layers of sporocytes (Fig. 39D). I n the genus Blastodinium the trophocyte may not divide into a trophocyte and a gonocyte, but into two trophocytes (i.e. by schizogony), and each of these trophocytes may subsequently undergo division into more trophocytes and gonocytes (Sewell, 1951). The end result is a single primary layer of sporocytes enclosing two separate layers of secondary sporocytes, each enclosing a trophocyte. Usually the release of sporocytes from the host sets the two daughter trophocytes free within the alimentary canal to develop into separate parasites. Schizogony enables more than one parasite to infect a host and hence gives rise to a larger number of sporocytes than would have been possible without schizogony. Chatton (1920) and Sewell (1951) agree that two or more individual parasites in a host have likely arisen by schizogony. Sewell does not state expIicitly that schizogony occurs in B. hyalinum inside Pseudocalanus but does give a table (his p. 329) in which size measurements of parasites are given for four cases of “double infections ” and one “ triple infection ” of B. hyalinurn from the North Sea, from which it may be inferred that B. hyalinum can undergo schizogony in Pseudocalanus. The rupture of the cuticle surrounding the parasite sets the sporocytes free into the alimentary canal of the host. The sporocytes are small immobile cells with two nuclei (Fig. 40A). Sometime after expulsion from the anus and after an unknown number of divisions they form dinospores (Fig. 40B),with 2-4 flagella attached in the region of the equatorial groove. Under unfavourable conditions the dinospores are able to encyst and host infection presumably takes place by ingestion of the dinospores or cysts (Fig. 40C)with the host’s food. (c) Eflect of infection on the host Chatton (1920) found that in host individuals parasitized with Blastodinium the gonad was immature and the genital ducts undeveloped. He also noted that he had never seen a parasitized male.


193

Cattley (1948) examined a number of Pseudocalanus from the North Sea, parasitized with 3. hyalinum, and found very distinct changes in the fifth pair of legs. He concluded that in the male the parasite is able to arrest the development of the male characters of the copepodid (externally, the fifth pair of legs), while in the final moult it causes the copepodid to undergo sex reversal and appear externally as a mature but sterile female ; he found spermatophores on three such individuals.

Transverse groove

/

Transverse

flogello

Longitutlinal groove

FIQ.40. The sporocytes (A), dinospore (B),and (C), a cyst of Blastodinium hyaliizurn, a parasite of Pseudocalanus. (After Chatton, 1920.)

Cattley believed that the parasite had no effect on the morphology of female hosts and that the C V moulted into a fully formed but sterile individual. Sewell (1951) examined a large number of individuals from several host species (not Pseudocalanus) infected with 3lastodinium and found both sexes infected with the parasite. In none of the infected males (usually C V, rarely adults) could Sewell detect any change of structure from the normal. I n females, a late infection evidently only partly reduces the development of the ovary and oviduct whereas an early infection has more profound effects. The first two segments of the A.M.B.-15

6

194


urosome may not fuse to form the genital segment, as occurs in a normal female (p. 34), but remain, separate as five segments, resembling the male condition. Even with fusion, the genital operculum may not develop, and there may develop a fifth pair of legs similar to that found in the male C V. Sewell (1951), therefore, was of the opinion that intersex individuals in copepods are modified females and not male individuals that have undergone partial or complete sex reversal as proposed by Cattley (1948) for Pseudocalanus. Sewell (1951) makes the further observation that those individuals in which a modified fifth pair of legs is present and which in all other characters appear to be females, but in which no parasite has been found, result from an early infection from which the individual has later recovered.

(d) Occurrence Blastodinium hyalinum is widespread (see ranges in above account) in the most wide ranging study (with Continuous Plankton Recorder). Vane (1952) states that it occurred in 3.8-60% of individual Pseudocalanus (mainly C V and adult females) in samples from the North Sea in 1948-49. It was most common in July-August, especially in the central part of the North Sea, minimal in December-March. 2. Dissodinium pseudocalani Drebes, 1969

(a) Taxonomy Dissodinium pseudocalani is a parasitic dinoflagellate found by Drebes (1969). The reproduction of this species resembles that of D . lunula and so the parasite was provisionally put in this genus. D. pseudocalani has thus far only been observed as an ectoparasite on the eggs of Pseudocalanus. Drebes (1972) subsequently indicated that his Dissodinium pseudocalani Drebes, 1969, is a synonym of Sporodinium pseudocalani Gbnnert, 1936 (see p. 196), and suggested that fwrther nomenclature changes will be made after he has concluded his revision of a few dinoflagellate genera. We accept the possibility that the two species discussed above are synonyms but we prefer here to give an account of the two forms separately, particularly since Sournia, et al. (1975) comment that the two parasitic species seem distinct. (b) f i f e history The life cycle includes a free drifting phase unattached to any host and an ectoparasitic phase on Pseudocalanus eggs. Mature primary cysts (Fig. 41A) usually drift unattached to the


195

host. They are spherical or oval, between 150-250 pm, and contain green or orange protoplasm, which is the same colour as the host’s eggs. The protoplasm invaginates in one region (Fig. 41B) and the nucleus divides mitotically to form nuclei on the periphery of the

FIG.41. Diagrammatic representation of the life cycle of Diasodinium pseudocalani, a parasite of Pseudocalanus. A, primary cyst in plankton. B, multinucleate protoplasm, invaginating. C, division into 16 cells. D, development into 16 secondary cysts. E, secondary cysts forming dinospores. F, liberated motile dinospores. G, infeotion of host egg. H, growth of mature trophont. I, the trophont still attached to egg membrane of host. (After Drebes, 1969.)

b

protoplasm, which then divides to form, generally, 16 segments (Fig. 41C),but sometimes 8 or 32. Secondary cysts (Fig. 41D) are formed by the rounding off of the 16 segments formed in the primary cyst; these become oval and about 76 x 47 pm.

196


Sporulation occurs when the secondary cysts divide to form 16 or 32 flagellated dinospores (Fig. 41E), which are colourless swarmers of the Gyrodinium type (Fig. 41F). Host infection occurs when a dinospore attaches itself to the surface of a host egg (Fig. 41G) and sucks out the contents. The trophont develops as an ectoparasite on the egg, then generally separates and continues its development in a primary cyst in the plankton (Fig, 41H, I). Later developmental stages were occasionally seen with the parasite still attached to the host egg membrane (Fig. 411). (c) Occurrence The parasite appears in the North Sea off Heligoland in the German Bight from late April until early June and is fairly common in the second half of May. The reason for this marked seasonality is not known. 3. Sporodinium pseudocalani Gbnnert, 1936 This parasite was found as a free cyst in the plankton off Heligoland in April 1934. At this time Pseudocalanw was the most numerous zooplanktonic species and one parasitic cyst was found in a clutch of eggs of Pseudocalanus. Gbnnert (1936) was unable to elucidate the complete life cycle, but described the formation of sporoblasts ( = primary cysts) which develop into sporocysts ( = secondary cysts) containing dinoflagellate-type nuclei. As Drebes (1972) observed, Gbnnert (1936) confused the membrane of the primary cyst with the egg wall of the host and therefore concluded that the dinoflagellatewas endoparasitic, although he did not rule out completely the possibility of ectoparasitism . This species is probably synonymous with Dissodinium pseudocalani Drebes, 1969, the life history of which has been described in detail above. 4. Ellobiopsis chattoni Caullery, 1910 Ellobiopsis chattoni is an external parasite of pelagic copepods first described by Caullery (19lo), who provisionally considered it to be a peridinian dinoflagellate, although no developmental stages or dinospores were observed. Apstein (1911, " Parasit 19 ") recorded an external parasite of Pseudocalanus which was identified by Jepps (1937a)as Ellobiopsis. Specimens of Pseudocalanus with Ellobiopsis have been recorded subsequently from the Gulf of St. Lawrence (Pinhey, 1927), Loch Striven (Marshall, 1949), the southern Norwegian Sea (Hansen, 1960) and off Ireland (Fives, 1969). Wing (1975) found a low level of

THE BIOLOGY OF PSEUDOCALAN US

197

infection of Pseudocalanw by Ellobiopsis chattoni in southeastern Alaska. Throughout the year only 1-6 Paeudomlanus were found to be infected each month from many thousands of potential hosts that were examined. Wing found no distinct seasonal trend of infection. The systematic position of this parasite has been disputed. Jepps (1937b) considered that the available evidence suggested a fungus relationship, but a t present the whole group is considered as belonging to the dinoflagellates by Loeblich (1976), and this is the view adopted here. An account of Ellobiopsis chattoni on Calanus finmarchicus is given by Jepps (1937b). It is assumed that spores formed by sporulation are responsible for infection of new hosts, although this process has not been observed.

B. Qregarines Apstein (1911, " Parasit 3 ") recorded gregarines in Pseudocalanus, and Jepps (1937b)observed them in the gut of Calanw. These parasites have not been studied in detail in copepod hosts, but the young parasite (sporozoite) becomes typically intracellular as it grows. It then leaves the host cell and the mature trophozoites adhere externally to the digestive lining. The trophozoites fuse in pairs (syzygy, observed in Calanus by Jepps, 1937b) and ultimately produce young sporozoites.

C. Trematodes Giesbrecht (1882) reported that Pseudocalanus was the most frequent host of a trematode, probably Hemiurw, that was also found free-living in Kiel Harbour. Entry into the host (later copepodids and adults) was between two thoracic segments or between cephalothorax and urosome, using the tapered posterior end for penetration. Other references to trematodes (probably H . appendiczclatus according to Thompson, 1976) in Pseudocalanzcs are Canu (1892), Apstein (1911), Wright (1907) and Marshall et al. (1934). Trematodes (or cestodes) were considered by Fives (1969)to be responsible for the red colouration often found in Pseudocalanus. Thompson (1976) concludes that these parasites do not have any detrimental effect on the copepod, merely acting as an intermediate host, the final hosts being fishes that feed on copepods.

D. Nematodes Apstein (1911, " Parasit 17 ") observed nematodes in Pseudocalanw, and Marshall and Orr (1955) reported them in Calanw as Contracaecum

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sp. The eggs of Contracaecum from the faeces of definitive hosts (birds or sea mammals) develop into larvae that may be eaten by copepods and subsequently by second intermediate hosts (Huizinga, 1966). The genus Thynnascaris parasitizes fish as adults and its larvae occur in fish and invertebrates. Popova and Valter (1965) and Valter (1968) have completed experimental studies on the intermediate hosts of Contracaecum aduncum (= Thynnascaris aduncum according to Norris and Overstreet, 1976) ; eight copepod species were subjected to experimental infection with larvae and Pseudocalanus was the second most infected copepod species (26% became infected). The larvae remained in the body cavity of the copepod where they increased in size (Popova and Valter, 1965).

E. Crustaceans All epicaridean isopods parasitize crustaceans and feed on blood. They undergo a marked metamorphosis in their life cycle (see Kaestner,

PIa. 42. Two mioronisoium larvae of an epicaridean isopod parasite, on Pseudocdanue. (From Sam, 1899.)

1970). The young leave the mother as pelagic epicaridean larvae and survive for a period on stored yolk before attacking a pelagic copepod or other host and transforming into a parasitic microniscium. After several moults on the host, its appendages become reduced and it becomes a free-swimming cryptoniscium stage, which then seeks out a final crustacean host. Sars (1899) gives an account of two microniscia on a female Pseudocalanus a t two different stages of development (Pig. 42), and Marshall (1949) found a microniscium on a female PseudoCaZanus, but nothing is known about final hosts of these parasites.

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.!I Retrospects and prospects

Our knowledge of the parasites of Pseudocalanus (as for marine parasites in general) is fragmentary, and advances will probably have to depend on the efforts of specialists working on the parasitic groups, rather than on the incidental findings of copepodologists. Although some of the parasites are fatal or sexually sterilizing to their hosts, their impact on Pseudocalanus populations is thought to be small (e.g. by Vane, 1952, and Wing, 1975). However, those parasites that use the abundant Pseudocalanus as intermediate hosts could have substantial impacts on less common final hosts. XV. ROLEIN THE FOODWEB We have indicated near the beginning of our review (p. 17) that Pseudocalanus is one of the most widespread and abundant metazoans in the world. Given this status, it is certain to be of substantial importance in the lives of other organisms. Here we review briefly the role of Pseudocalanus as a consumer, as a source of nutrients and as food for others (especially larval fishes), and discuss the first hesitant attempts to include Pseudocalams in descriptive and predictive models of marine food webs.

A. Effect on phytoplankton 1. Peeding on phytoplankton

The feeding of herbivorous copepods clearly removes phytoplankton from the water column, but evidently the impact of Pseudocalanus on its food species has not been fully assessed. Zagorodnyaya (1977) estimates the fraction of edible biomass of phytoplankton in the Black Sea removed by Pseudocalanus during two times of year. To do so she calculated daily rations of copepodids and adults, using the “balance equation” approach (see p. 132). She concludes that these animals removed about 18% of the standing crop daily (compared with 11 yoby Calanzis hegolandicus) in inshore waters in spring, and 8% (compared with 40% by C. helgolandicus) in offshore waters in winter. As these conclusions are local in implication, we feel that the following general account is useful. A population of Pseudocalanus growing or producing eggs a t about 15-20% of its biomass per day (pp. 130,131) might need a minimum of about four times this amount of food (p. 133), which it might obtain from food concentrations as low as 25 pgC/I. (p. 130). If we can imagine

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that such an unconcentrated phytoplankton biomass could, if ungrazed, double its quantity each day, then a population of 3 or 4 adult female Pseudocalanus per litre, each weighing about 10 pgC, could keep the plant population in check. However, we have shown that copepodids can consume up to 140% of their weight per day at phytoplankton concentrations of 200 pg C/1. (p. 67). Since growth rates do not increase with ration above at most 50 pgC/l. (p. 130, despite equivocal analyses from growth efficiencies, p. 133), this seems to us to indicate that " superfluous feeding " by Pseudocalanus could occur at phytoplankton levels substantially below the 390 pgC/l. suggested by Beklemishev (1962) for copepods. Possibly, however, die1 feeding cycles (p. 72) and vertical migration (p. 165) reduce this " wastage " in nature. The faecal pellets produced by Pseudocalanus (whether with superfluous food or not) may carry material below the photic zone. The pellets produced by Pseudocalanus are of the order of 106 to 3 x 106 pm3 (from Corkett, 1966 ; Martens, 1972), and these might sink at up to 100 m/day (Fig. 1 in Smayda, 1969). 2. flupply of nutrients

Although Pseudocalanus removes organic matter from the water column, it also resupplies nutrients to the phytoplankton. We have concluded that rates of excretion of nutrients by Pseudocalanus are strongly dependent on food concentrations (p. 51). Evidently the only estimates of the possible contributions of excretion by Pseudocalanus to phytoplankton requirements come from two studies in Bras d'Or Lake, a landlocked arm of the Atlantic in Nova Scotia. Here Christiansen (1968), using rates of NH3 excretion described elsewhere (p. 44), estimated from population densities that Pseudocalanus supplied about two-thirds of the N excreted by the copepod community, but that this was only about 4.8 mg N/m2/day, which was about 4% of the daily phytoplankton requirements of about 118 mg N/m2/day. I n the same environment, Hargrave and Geen (1968) calculated that the phytoplankton needed about 7.5 mg P/m2/day. From estimates of population densities and excretion rates of P (see p. 49), they suggested that about 15 mg P/m2/day could be supplied by copepods, sometimes predominantly Pseudocalanus. Although they note possible sources of error, they conclude that regeneration of P (unlike that of N, see above) by copepods like Pseudocalanus is important.


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B . Predators I. Fishes There are many records of the occurrence of Pseudocalanus in the diets of fishes, and we cannot refer to them all. Rather, we attempt to outline the possible importance of Pseudocalanus to numerically and commercially important fish species. Where possible we refer to recent, more general studies of diets in which Pseudocalanus figures. We also attempt to give geographical balance in our survey. Although Pseudocalanw occurs in diets of some postlarval fishes, it is much more important as a food for larval fishes. Most marine fishes have very high fecundities that are balanced by high mortalities. Most of this mortality occurs during the larval stage, as was first stressed by Hjort (1914). May (1974) restates ‘ I Hjort’s critical period concept ’’ as a concept that maintains that the strength of a year-class is determined by the availability of planktonic food shortly after the larval yolk has been exhausted ”. May concludes that field and laboratory evidence, although often circumstantial, indicate that starvation is indeed an important cause of larval mortality when yolk has been exhausted, as Hjort hypothesized. I n order to signify the relative commercial importance of each species of fish considered here, we quote the most recent available fishery statistics (P.A.O., 1974) on the nominal catch for 1973.

(a) Salmon Salmon as diadromous fishes breed in fresh water and their young may migrate to the sea at various stages of development. Among them, the pink (= humpback) salmon (Oncorhynchus gorbuscha) goes to sea as plankton-feeding fry. It produced a catch in the northeast Pacific of 34 x lo3 metric tons in 1973. Young pink salmon (36-104 mm) off southern Hokkaido have been shown to contain Pseudocalanus in their stomachs (Okada and Taniguchi, 1971). Parsons and LeBrasseur (1970) showed in the laboratory that young pink salmon 90 mm long fed best off Calanus plumchrw and less well off the smaller Pseudocalanus. I n the Strait of Georgia, however, it appeared that pink salmon less than 30 mm long fed best on smaller copepoda, such as Pseudocalanus (LeBrasseur et at., 1969). The chum (= keta or dog) salmon (0.keta) is an important food fish in Japan and North America, with a catch of 126 x lo3 metric tons in 1973. Okada and Taniguchi (1971) found Pseudocalanus in the guts of juveniles, and LeBrasseur et al. (€969)showed that such small copepods are an important food source.

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(b) Herring The Atlantic herring (Clupea harengus) yields one of the world's great fisheries, with a total catch in the Atlantic of some 1 956 x lo3 metric tons in 1973. Hardy's (1924) classical study in the North Sea showed that Pseudocalanus was numerically 86% of the food of herring between 12 and 42 mm. The importance for herring of food availability after the yolk sac has been absorbed has been investigated by Blaxter (1 963). He related the dimensions of food organisms to the maximum gape of the jaws, which is just sufficient to take an adult Pseudocalanus " end on "when larvae reach 12 mm. He found that Pseudocalanus were not generally taken until the larvae reached 12 mm, and that Calanzls was not taken until the larvae were 30 mm long. He concluded, however, that Calanus were rarely taken by postlarval fish, and then only when the copepods are in younger stages, but that Pseudocalanus is of major importance. Legare and Maclellan (1960) have carried out the most extensive study of herring feeding in relation to zooplankton in the western North Atlantic. They found that Pseudocalanus was the second most abundant copepod in the region of the mouth of the Bay of Fundy. It was third in incidence in stomachs from within Passamoquoddy Bay and, along with Calanus, even more common in stomachs from outside the bay, especially in fish longer than 200 mm. The Pacific herring (Clupea harengus pallmi) produced a catch of some 539 x lo3 metric tons in the North Pacific in 1973. Lowe (1936) investigated food in various sized herring from off southern British Columbia. For fish 9-12 mm long, the most important food items were small eggs and nauplii. Pseudocalanus was present in guts of all larvae longer than 13 mm. (c) Atlantic mackerel . The mackerel (Scomber scombrus) produced some 1 017 x lo3 metric tons in the Atlantic and 11 x lo3 metric tons in the Mediterranean and Black Seas in 1973. Bullen (1908) found that PseudocaZanus was common in stomachs of postlarval mackerel in the English Channel, especially in the month of May. Among " fishermen's signs " was one stating that mackerel are abundant in " yellow water which seldom appears before the last week in April. Bullen showed that phytoplankton was almost absent from " yellow water ", but that copepods were abundant, especially Calanus and Pseudocalanzls. )),


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(d) European pilchard The pilchard or sardine (Sardina pilchardus) makes up several important fisheries. I n 1973, Portugal took 101 x 103 out of a total of 177 x 103 metric tons from the northeastern North Atlantic, probably largely outside the range of Pseudocalanus. There is also an important fishery in the Mediterranean, of some 144 x lo3 metric tons in 1973. Although Lebour (1920) recorded Pseudocalanus among the food items of larval (9-25 mm) pilchard off Plymouth, the fish largely occurs south of the range of Pseudocalanus, except in the Black Sea, where the copepod may be an important food item (I. I. Porumb, 1969). (e) Sprat The sprat (Sprattus sprattus) is an important fishery for the U.S.S.R. and Denmark, which together landed over half of the 507 x lo3 metric tons taken in the northeastern North Atlantic in 1973. There is also a small fishery (9 x lo3 metric tons) in the Mediterranean and Black Seas. Nguyen et al. (1972) found that Pseudocalanus was important seasonally in samples of sprat from the Bornholm Deep in the Baltic, making up about 43% of food items in April and 59% in May. Miller (1969) found that Pseudocalanus also dominated the diet of fish taken in April and May off the Estonian coast, and that most feeding took place a t night. I n the Black Sea, Porumb (1971) found that a reduction of Pseudocalanus populations in April could be traced to its fate as a principal food of sprat, which is a migrant to Romanian coasts at this time of year.

(f) Atlantic cod The cod (Gadus morhua = G . callarim) yields the greatest catch among demersal fishes whose larvae feed on zooplankton. It is important both in the northeastern North AtIantic, where some 1 727 x lo3 metric tons were taken in 1973, and in the northwestern part, where some 808 x lo3 metric tons were caught. Wiborg (1948) investigated the food of larval cod in coastal waters of northern Norway during spring and summer of a number of years between 1930 and 1947. The larvae ranged from 3.1 to 13.0 mm long. When Pseudocalanm was abundant in the plankton in May 1933, copepodids occurred in larvae 4-7-6-5 mm long. Nauplii were found in small larvae, many with a yolk sac, in 1939. Pseudocalanus was not found in larvae taken in 1930 and 1947, evidently because the copepod

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was scarce at the times of sampling. As expected, copepods are not important in the diet of postlarval, " 0-group " cod, which feed almost exclusively on euphausiids, although Pseudocalanus was recorded in some stomachs (Wiborg, 1949). Marak (1960) investigated feeding by larval cod in the Gulf of Maine and over Georges Bank. He found " Pseudocalanus-type " (i.e. including Paracalanus) remains in six larvae 9-16 mm long. (g) Polar cod The small polar cod (Boreogadus saida) forms a significant fishery in the northeastern region of the North Atlantic, some 82 x lo3 metric tons having been taken in 1973. Diet of its larvae has been investigated by Ponomarenko (1967), who found that copepods were important t o larvae between 4.6 and 39 mm long, and that Pseudocalanus occurred in 57% of specimens in the size range 19.1-28.7 mm. Pseudocalanus nauplii have been used as food for polar cod larvae reared in the laboratory (Aronovich et al., 1975). (h) Haddock The haddock (Melanogrammus aeglefinus) offers a huge catch of some 593 x 103 metric tons in the northeastern North Atlantic, compared with only 26 x 103 metric tons in the northwestern part. Marak (1960) found among larvae between 4 and 46 mm long, " Pseudocdanus-type '' copepods (see under cod, above) mainly in larvae between 13 and 23 mm long. Ogilvie (1938) found Pseudocalanus commonly in larvae 3-5-31 mm long from Scottish waters. She considered the largest individuals to be postlarval. Pseudocalanus eggs and younger stages were found in smaller larvae, and adult females were common in those more than 12 mm long. (i) Whiting The whiting (Merlangius merlangus) formed an important fishery of about 207 x lo3 metric tons in the northeastern North Atlantic and a smaller one of about 1 x lo3 metric tons in the Mediterranean and Black Seas during 1973. Lebour (1920) found that Pseudocalanus was a favoured food item of larval whiting up to about 9 mm long during spring and summer off Plymouth. Although the larvae take other copepods, Lebour concluded that they select Pseudocalanus in preference to other like-sized forms, such as Temora.


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(j) European plaice The plaice (Pleuronectes platessa) yielded 164 x lo3 metric tons in the northeastern North Atlantic in 1973. Scott (1922) examined over 600 larvae 13-87 mm long from off the coasts of Wales and the Isle of Man, and found that 22% of them contained Pseudocalanus.

(k) European hake Of the several commercial species of hake, the European hake (Merluccius merluccius) gave an important catch in the northeastern North Atlantic of some 110 x lo3 metric tons in 1973. Lebour (1920) found a Pseudocalunus in a single larval hake (5-5 mm long) in a sample of 12, but felt able to conclude that " it seems likely that young Hake, like the Gadus species, begins by taking Pseudocalanus, Calanus afterwards being frequently taken ". (1) Sandeels

Sandeels (sandlances or sand launces) of several species (Ammodgtes spp.) are important fisheries, especially for Denmark, which landed 283 x lo3of the 307 x 10%metric tons taken in 1973 in the northeastern North Atlantic. Sandeels occur in large shoals in shallow waters and are caught by fine-mesh trawls, so that in this sense they can be classed as demersal fishes. They are important as food for other larger demersal fishes. Lebour (1919b) found Pseudoculunus in the guts of fish 19-21 mm long in a sample of 109 A . tobianus ranging from 3 t o 21 mm long. She also found (Lebour, 1918, 1920) Pseudocalanus frequently in the guts of Hyperoplus lanceolatus ( = A . lanceolatus) 1 P 2 5 mm in length. The Pacific sandlance ( A .personatus) forms an important fishery for Japan, which took 194 x 103 metric tons from the northwestern North Pacific in 1973. LeBrasseur et al. (1969) examined gut contents of larvae (< 30 mm) and young (> 30 mm) of this fish from the Strait of Georgia, British Columbia. At the time of sampling, Pseudocalanus and two larger Calanus spp. were available as food. Fish of the size range 20-40 mm had 48% of their stomachs filled with zooplankton in the 0.5-1.0 mm size range, whereas large (> 40 mm) fish had 85% of their stomachs filled with zooplankton in the 1-1-1.5 mm range. Species of zooplankton were not identified, but it can be inferred from these sizes that Pseudocalanus and young stages of Calanus must have been of prime importance.

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(m) Other denzersal species Pseudocalanus has been identified in the gut contents of a number of other demersal species by Lebour (1918, 1919a, 1919b, 1920). Among these, the ling (Molva molva), common dab (Limanda Eimanda) and turbot (Psetta maxima) are of some commercial importance, producing a combined catch of some 91 x lo3 metric tons in 1973, mostly in the northeastern North Atlantic. 2. Crustaceans

No doubt Pseudocalanus is preyed upon by a variety of planktonic crustacea, but only euphausiids appear to have been implicated explicitly. Ponomareva (1954) concluded that Pseudocalanus was about the right size among copepods of the Sea of Japan as food for Thysanoessa inermis, T . longipes and Euphausia pacifica. I n the aquarium, euphausiids caught Pseudocalanus readily and ate out their soft parts, leaving the exoskeleton. I n nature, parts of Pseudocalanw were regularly found in gut contents of euphausiids. 3. Chaetognaths

Chaetognaths are highly predaceous animals, eating many small animals of suitable size with which they come into contact. Since Pseudocalanus in its various stages is abundant and of suitable size, it is hardly surprising that it is eaten by chaetognaths. The most widespread chaetognath within the range of Pseudocalanus is Sagitta elegans (= Parasagitta elegans), but Sagitta setosa also occurs in the more southern parts of the range of the copepod. Adult female Pseudocalanus were prominent in the guts of 6-19 mm 8.elegans in the North and Celtic Seas in summer and the Irish Sea in winter, according to Rakusa-Suszczewski ( 1969). Pseudocalanus was evidently selected by small chaetognaths in preference to Calanus and Temora, even though Calanus was more abundant than Pseudocalanus in the plankton. Rakusa-Suszczewski (1969) found that most feeding on Pseudocalanus took place at night. Pearre (1973), working with the same samples from Bedford Basin, Nova Scotia, from which vertical distributions of Pseudocalanus had been determined (Fig. 38) found that Pseudocalanw living near the surface in July were largely taken at night. McLaren (1969) gives a detailed account of the ways in which populations ofS. elegans in Ogac Lake, Baffin Island, depend on Pseudocalanus. Adult chaetognaths produced eggs over a protracted period in


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spring, but recruitment of their young was only successful when the seasonal burst of nauplii of Pseudocalanw occurred. The sizes of the subsequent juvenile populations of chaetognaths were determined by the number of adult chaetognaths present at the times of these bursts of nauplii, but not on the number of nauplii present. McLaren also concluded that the overwinter survival of older S. elegans in Ogac Lake was dependent on accessibility of copepods, largely Pseudocalanus, in deeper water. Mironov (1960) studied the feeding of Sagitta setosa in the Black Sea in some detail. He found that Pseudocalanus was not very important aa a food item in Sevastopol Bay in September 1961, but that it constituted about 77% of the daily ration of S. setosa by numbers and 97% by weight in offshore waters in February 1951. RakusaSuszczewski (1969) showed that Pseudocalanus was taken by S. setosa around the British Isles, but that it was never as important in the diet as was Temora. 4.

H ydromedwsae

Lebour (1922) studied feeding of a number of species of hydromedusans and recorded Pseudocalanus in the guts of the following species in samples from nature : Sarsia tubulosa, Rathkea octopunctata, Leukartiara octona (as Turris pileata), Phialidium spp. and Obelia spp. Although Pseudocalanus is eaten by Aglantha digitale in Ogac Lake, Baffin Island, McLaren (1969) found that recruitment of the tiny young of this hydromedusan appeared to be related to availability of phytoplankton, and that its overwinter survival was unrelated to abundance of Pseudocalanw. It seems probable that, in general, hydromedusae are less important than chaetognaths as predators on Pseudocalanus. 5. Ctenophores

The tentaculatan ctenophore Pleurobrachia pileus occurs widely in northern waters and is known to be a predator on Pseudocalanw. Lebour (1923) found Pseudocalanus in a specimen of P. pileus from off Plymouth and Fraser (1970) included the " group Pseudocalanw and Paracalanus " as important to P. pileus in the North Atlantic. Carter (1965) considered that P. pilew had an important impact on Pseudocalanus in Tessiarsuk, a landlocked bay on the coast of Labrador. We infer that P. pilewr feeds on Pseudocalanws in the Black Sea from Petipa et al. (1970). Two studies of predation by P. pileus give more details. Bishop (1968) studied feeding in the laboratory by P. bachei (= P . pilew of

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CIIRISTOPHER J. CORKETT AND LAN A. MCLAREN

some authors) from waters of Washington State and found that they fed on adult and copepodid Pseudocalanus a t a rate of 1-7 copepods/ ctenophore/h, at a copepod density of 2511. of each stage. They fed more slowly on nauplii of Pseudocalanus (1.0 nauplii/ctenophore/h), but the significance of this difference cannot be ascertained (SD only given). Anderson (1974) found that 89% of gut contents of P. pileus in St. Margaret’s Bay, Nova Scotia, consisted of C V and adult copepods, including Pseudocalanus. He found that Temora and Centropages were about 10 times more likely than Pseudocalanus to be captured in the sea when the relative concentrations of the copepod species in the sea were taken into account. He attributes the relative invulnerability of Pseudocalanus to its manner of swimming (see p. 53). He also disputes Bishop’s (1968) rates of feeding of P. bachei (see above), suggesting that Bishop’s animals were feeding past satiation levels. However, Anderson does stress the great natural importance of P. pileus on copepods in general. The tentaculatan Bolinopsis microptera was also studied in the laboratory by Bishop (1968) in conditions as described above for P. bachei. He found that B . micropteya fed on Pseudocalanus of all stages at a rate of 0.9 copepods/ctenophore/h, somewhat lower than the rates for P. bachei. Anderson (1 974) found that Bolinopsis infundibulum also fed on Pseudocalanus, but preferred Oithona in particular. We conclude that ctenophores may be significant predators on Pseudocalanus, but probably less so than on some other species of copepods.

C. Significance in the food web A species-by-species account of the species eaten by and the species that eat Pseudocalanus does not altogether fix its significance in the economy of the sea. Cushing (1970) and Steele (1974) are examples of the thrust toward systems analysis of production and the flow of matter or energy throughout the food webs of the sea. That Pseudocalanus is an important secondary producer ‘innorthern seas cannot be doubted. However, an initial note of caution must be made concerning the significance of this production in the food web. Recently Martens (1975) counted the numbers and estimated biomasses of dead Pseudocalanus sedimenting out of the water column and into collectors set in the western Baltic. He found that some 2.8 g C/m2/yr of Pseudocabnus was sedimented in this way. The figure compares with estimates of total production in some localities (see Section XIII). The great bulk of the Pseudocalanus carbon was sedimented in April-


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May, shortly after a numerical maximum in this copepod. It is possible that in regions with highly seasonal life cycles a major fraction of the production of Pseudocalanus can at times end up as detritus, even of “ spent ” adults, unused by predators. Marten’s work cries out for repetition elsewhere. One of the more detailed food chain analyses involving Pseudocalanm is presented by Petipa et al. (1970). They express on diagrams the standing crops and specific transfer rates (rates per unit of biomass) for the major components of the pelagic food web in the Black Sea (it should be noted that the captions in their Figs 1 and 2 are reversed). I n the near-surface waters (the “ epiplankton ”) older stages of Pseudocalanus contribute little, although their young (grouped among nauplii) may be important as consumers of medium-sized phytoplankton. I n deep water (the “ bathyplankton ”) C IV-adults of Pseudocalanus and Calanus are represented as’having a dominant role, forming the largest standing crop among the herbivores and consuming much the greatest amount of the relatively common large phytoplankters at these depths. They conclude that “ at the herbivorous level the most powerful flow of matter and energy is through the migratory copepodites and adult large-sized copepods (Pseudocalanus and Calanus) ”. While it may rest on huge accomplishments in data acquisition and analysis, a detailed assessment of the flow of matter and energy through a food web is nothing more than descriptive science. However, steps are being made toward the study of food webs as a predictive science. The early systems analysis by Cushing (1959) included Pseudocalanus among “ other copepods ”, but made no direct use of its parameters of feeding, growth rates, etc. An example that explicitly contains parameters for Pseudocalanus is by Menshutkin et al. (1974). They developed a mathematical model of the pelagic ecosystem of the Sea of Japan, which includes Pseudocalanus as an important part of the “ mesoplankton ” component of the “ boreal epiplankton ”. They took into account all the variables of growth and advection that influenced the transfer functions of biomass (energy) through the food web, including such variables as currents, temperature, vertical migrations, etc. I n this way they predicted the quantitative distributions of biomass (energy) of various categories throughout the Sea of Japan at various seasons. Although their results have not been fully tested, they do match fragmentary observations of the real patterns in the Sea of Japan. Another example is by Steele and Frost (1977), who construct a simulation model of nutrient-plant-herbivore-carnivore dynamics using parameters for small (= Pseudocalanus) and large ( = Calanus) cope-

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pods. Some of their assumptions match what we have shown: that there is an upper limit to assimilation and growth rates (set at a food level of 80 mg C/m3, which is probably too high, cf. p. 130), and that reproductive rate (as C) is the same as growth rate before maturity (see p. 131). Other assumptions about size-selection of food particles may be premature (see p. 63). Although their model produces some general results that match general observations, it fails in an attempt to simulate the seasonal cycle of Pseudocalanus in Loch Striven, Scotland. Steele and Frost conclude that this failure results largely from misassumptions about hydrographic restoration of nutrients, rather than from errors in the parameters of grazing and growth by copepods.

D. Retrospects and prospects The importance of Pseudocalanus as a consumer, replenisher of nutrients and food base have been amply demonstrated. The genus is of particular significance to fish, and therefore to fisheries, of northern waters. Gulland (1970) notes " that the potential for great expansion of catches are among species lower in the ecological pyramid " ; that is, among fishes that feed on zooplankton. Lishev and Freimane (1970) have found high degrees of correlation between biomasses of Pseudocalanus sampled at different times of year (see critical account of their work, p. 156). They argue that it should thus be possible to predict food supplies for planktivorous fishes. They also suggest that deviations from long-term regressions of population estimates of Pseudocalanus at a given time of year on estimates at an earlier time of year (i.e. deviations from the usual mortality rate) may reflect differences in the amount consumed in the interval by plnnktivorous fishes. This in turn may give a new technique for estimating fish populations from the amount they consume. Altogether these possibilities, which stand apart from the main thrust of food-web studies in the sea, seem very worth exploring. A common aim of systems analyses of production in marine food webs is the substitution by general categories (e.g. trophic levels, biogeographic units, particle sizes) of the actual species involved. We hope that we have said enough in our lengthy review on the biology of Pseudocalanus to indicate that it may not be possible altogether to substitute somewhat abstract categories for the more objective realities of this interesting marine copepod.

XVI. ACENOWLEDGEMENTS We are grateful to Dr R. J. Lincoln and the staff of the Crustacea Section, British Museum (Natural History) for allowing us the use of


21 1

the section library, and also to Miss S. Fullerton and the staff of the ScienceLibrary, DalhousieUniversity, for much bibliographic assistance. The Trustees of the British Museum (Natural History) gave us permission to reproduce Fig. 39B, C and D. The Centre National de la Recherche Scientifique allowed us to reproduce Fig. 39A and Fig. 40. We are grateful to authors of theses who allowed us to make use of often previously unpublished material, and especially to Dr Brenda Thompson, whose thesis we have used so extensively. A large number of scientific colleagues throughout the world have given us advice, information and assistance throughout the preparation of this work. We are especially grateful to Robert Conover, Barry Hargrave, Kenneth Mann, the late Sheina Marshall, Georges Merinfeld, Eric Mills, Serge Poulet and Sharon Smith for reading the typescript of one or more sections and to Georges Merinfeld for bibliographic assistance. Despite their help, inadequacies remain for which we are entirely responsible. Our research has been supported by grants from the National Research Council of Canada to I.A.M.

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Paffenhofer, G.-A. and Harris, R. P. (1976). Feeding, growth and reproduction of the marine planktonic copepod Psewlocalanus elongatus Boeck. Journal of the Marine Biological Association of the United Kingdom, 56, 327-344. Parsons, T. R. and LeBrasseur, R. J. (1970). The availability of food to different trophic levels in the marine food chain. I n “ Marine Food Chains ” (J. H. Steele, ed.), pp. 325-343. Oliver and Boyd, Edinburgh. Parsons, T. R., LeBrasseur, R. J. and Fulton, J. D. (1967). Some observations on the dependence of zooplankton grazing on the cell size and concentration of phytoplankton blooms. Journal of the Oceanographic Society of Japan, 23, 10-17. Parsons, T. R., LeBrasseur, R. J., Fulton, J. D. and Kennedy, 0. D. (1969). Production studies in the Strait of Georgia. Part 2. Secondary production under the Fraser River plume, February to May 1967. Journal of Experimental Marine Biology and Ecology, 3, 39-50. Pavlova, E. V. (1975). On certain factors influencing rate of oxygen consumption of marine planktonic animals. Biologiya Morya, Kiev, 33, 73-78. (In Russian. ) Pavlovskaya, T. V. and Pechen’-Finenko, G. A. (1975). Comparison of the relative role of living and non-living organic matter in the nutrition of Pseudocalanus elongatus (Boeck). Biologiya Morya, Kiev, 34, 66-70. (In Russian.) Pavshtiks, E. A. and Timokhina, A. F. (1972). History of investigations on plankton in the Norwegian Sea and the main results of Soviet investigations. Proceedings of the Royal Society of Edinburgh, B, 73, 267-278. Pearre, S. (1973). Vertical migration and feeding in Sagitta elegam V e r d . Ecology, 54, 300-314. Pearse, A. S . (1936). Estuarine animals at Beaufort, North Carolina. Journul of the Elisha Mitchell Scientijk Society, 52, 174-222. Peterson, W. T. and Miller, C. B. (1975). Year-to-year variations in the planktology of the Oregon upwelling zone. Fishery Bulletin. Fish and Wildlye Service. United States Department of the Interior, 73, 642-653. Petipa, T. S. (1975). Origin and classification of certain ecological types of feeding of Calanoid Copepoda. Biologiya Morya, Kiev, 33, 27-49. (In Russian.) Petipa, T . S., Sazhina, L. I. and Delalo, E. P. (1963). Vertical distribution of Zooplankton in the Black Sea. Trudfj Sevastopol’skoi biologicheskol stanti% Akademiya nauk SSSR, 16, 119-137. (In Russian.) Petipa, T. S., Pavlova, E. V. and Mironov, G. N. (1970). The food web structure, utilization and transport of energy by trophic levels in the planktonic communities. I n “ Marine Food Chains ” (J.H. Steele, ed.), pp. 142-167. Oliver and Boyd, Edinburgh. Pinhey, K. F. (1927). Entomostraca of the Belle Isle Strait Expedition 1923 with notes on other planktonic species. Part I. Contributions to C a n a d h Biology and Fisheries, 3, 179-234. Polyakova, T. V. and Perueva, F. G. (1976). Oxygen consumption by some planktonic organisms from the White Sea. Zhurnal obshchel biologii, 31, 450-458. (In Russian.) Ponomarenko, V. P. (1967). Feeding of the larvae and fry of the arctic cod (Boreogadus saida Lepechin) in the Barents and Kara Seas. Materia@ rfjbokhozyahtvenngkh issledovanii severnogo bamelna, 10, 20-27. (English transl. Bureau of Sport Fisheries and Wildlife, Narragansett, Rhode Island.)


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MARINE BIOLOGY A N D HUMAN AFFAIRS* F. S. RUSSELL Marine Biological Association, Citadel Hill, Plymouth, England I. 11. 111. IV. V. VI. VII. VIII. IX. X. XI. XII.

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The study of marine biology may be said to have started as long ago as when Aristotle described many of the animals which live in the sea and wrote in detail on such matters as the migrations of the tunny. These marine animals always held a fascination for the early naturalists because of their great diversity of form. But it was only when enough was known to encourage attempts at classification that their study became truly scientific, developing through Linnaeus to Cuvier and finally to Darwin. It is noteworthy that both Huxley and Darwin went on voyages on which the investigation of marine life occupied much of their time. Huxley, for instance, on the voyage of the “ Rattlesnake ” disclosed the true affinities of the coelenterates, or Cnidaria as they are now known, with their two cell layers, thus amending Cuvier’s classification which combined jellyfish with echinoderms as radiate animals. Darwin produced a classic monograph on barnacles, published by the Ray Society. It was not so very long after the publication of Darwin’s “ Origin of Species ” that an international marine biological laboratory was founded in 1874 by Anton Dohrn a t Naples. This was to be followed during the next decade by similar laboratories in the United Kingdom, France and the United States, so that by the close of the century

* Being the third John Harris Memorial Lecture, delivered a t Bristol University on 4 M a y 1976. (Reprinted from Biology and Human Affaira, Vol. 42, 1976). 233

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there were twenty-one European marine laboratories, either independently established or under university management. The setting up of such laboratories had three main objects. First, the purely academic study of the structure and habits of the many animals that live in the sea, whose diversity and number of species apart from the insects far exceeds those on land. Second, the investigation of marine animals for the furtherance of physiological knowledge, for different tissues and organs are to be found in their simplest form in some of these animals. And, third, and slightly later, for the essentially practical study of the habits and life histories of fish, because fears were beginning to be expressed that the sudden increase in trawling due to the introduction of steam might damage the commercial fisheries. From these small beginnings there has grown an immense organization, found necessary as a result of the realization that many aspects of marine biology have a bearing on the practical affairs of life. Marine biological and fishery research laboratories around the world can now be numbered in their hundreds, while the world fleet of research vessels of all kinds now exceeds a thousand. I propose to mention some of the more important discoveries and fields of research in marine biology that have proved useful, and indeed necessary, for mankind.

I. FOOD FROM THE SEA I suppose that the most obvious field is that of food from the sea, which is now estimated to yield something of the order of nearly a hundred million tons of fish a year. I n Great Britain as long ago as the fourteenth century some were calling for fishing restrictions, and in the sixteenth and seventeenth centuries objections were continually being raised against foreigners fishing in so-called " British waters ". I n succeeding years numerous regulations were brought into force restricting methods of fishing in different areas. Commissions were set up in 1854, 1865 and 1878 to study the availability of fish and no trustworthy evidence could be found that there was any overfishing. The seas were thought to be inexhaustible. As a result an Act was passed in 1868 ruling " that all Acts of Parliament which profess to regulate or restrict the mode of fishing pursued in the open sea be repealed, and that unrestricted fishing be permitted hereafter ". Before the end of the century further experimental closing of certain areas off the coasts of Scotland in which scientific observations were made still led to the conclusion that no serious damage could be done by commercial fishing.

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One of the main contentions by the fisherman was that beamtrawling by steam vessels was destroying the spawning grounds of commercially important fish. Many fishermen thought that marine fish laid their eggs on the sea floor or attached to weeds or rocks. But as early as 1864 the Norwegian naturalist G . 0. Sars had shown that the eggs of cod and gurnards were in fact planktonic, being spawned in the upper water layers well above the sea floor. So one of the first practical investigations at the marine laboratories was to study in detail the early life histories of fish in the sea, and to describe their eggs and young stages so that their distribution could be plotted. Despite the earlier predictions that the supply of fish was inexhaustible, the increasing numbers of fishing vessels and advances in the efficiency of fishing gear provided evidence that there were indeed dangers of overfishing. So, in 1902, an International Council for the Exploration of the Sea was set up, supported by the Governments of a number of European countries, with the object of obtaining by cooperative research sufficient knowledge to enable stocks of fish in the sea to be rationally exploited. For this a thorough knowledge of the biology of marine organisms and of the chemistry and physics of sea water was required, for it is not possible to divorce the fish from their ecological environment. The example of this International Council has now been followed in most regions of the world, and similar organizations have been set up for different areas of the oceans, as well as special Commissions concerned with individual species of fish such as halibut, tuna and salmon. Besides fish, other organisms are much sought after from the sea; seaweeds and squid are eaten in quantities by eastern nations, and shrimps and prawns now form a significant part of the food from the sea. These need also to be guarded. These International organizations have enabled cooperative research to be undertaken over wide areas. Up to the last war this was mainly done to obtain knowledge on the bioIogy of marine fish and their ecology, but since the war, research has been aimed especially at problems of the estimation of fish stocks and their rates of recruitment. While the scientific information thus made available in the North Eastern Atlantic has been sufficient to enable some advice to be given on management of the fisheries, on the administrative level this has not been fully made use of and some species are becoming seriously overfished. This situation should change when legislation on national limits is enacted and countries bordering the sea will have sovereignty over their own areas. This should enable much greater management of local stocks by those countries determined to do so, but it may restrict

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the operations of rescarcli vessels because, already, permission is now needed to visit waters controlled by other countries. The establishment of quota systems for different countries has already started. Much monitoring of biological conditions will thus be required in the future. Indeed the whole problem of stock management still requires a great deal of investigation to find the effects of fishing on the recruitment of each species and the relationship between one species and other competing species and with the ecological environment.

11. FISHFARMING But the supply of food from the sea, even if well managed, is not inexhaustible. It can be supplemented to some extent by the farming of fish and shellfish in confined areas. While the cultivation of freshwater fish has long been practised, as has that of shellfish such as oysters and mussels, the cultivation of marine fish was found to be difficult and awaited the necessary discovery. The difficulty was that most sea fish hatch at a very small size, usually about 3 mm long, and have extremely small mouths. When they have absorbed their yolk they are still only able to capture and eat tiny organisms. It was found just before the last war that a food supply of animals of the right size was available in salt pans in which the brine shrimp Artemia lays its hardy eggs. These eggs can be transported in sufficient quantities to enable their newly hatched nauplius larvae to be used as food. The earlier work on rearing in Great Britain was concentrated on the plaice, for which it was soon possible to obtain survival values of 70% or more. This made the suppIy of baby fish ample for rearing purposes seeing that one female plaice might produce 50 000 eggs. But the cost of rearing plaice to marketable size is still somewhat higher than that of sea caught fish, and the main experimental emphasis is at present on luxury species such as the sole, turbot and halibut. There is no doubt that mariculture will play an increasing part in the future supply of food, but it should be remembered that fish require protein for their nourishment and are thus likely to remain a luxury food. This is not so with shellfish which feed mostly on planktonic plants and can be cultivated on a large scale in unpolluted estuaries. The rearing of shellfish such as oysters and mussels was much advanced by a systematic, study and culture of unicellular flagellates: on which their larval stages can be fed.

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The cultivation of different kinds of shrimps is also now receiving much attention, for shrimps form quite a large portion of our food supply from the sea. Seaweeds are cultivated by the Japanese as food, especially species of the red seaweed Porphyra, or laver. The discovery in 1949 by the British algologist Kathleen M. Drew that there was a stage in the life history of this weed which bored into mollusc shells (the so-called Conchocelis stage) was seized upon by the Japanese, who now culture this stage so that they have a continuous supply of spores for the next stage of development. As a result, the amount of weed cultivated in Japan has grown enormously. Indeed, so beneficial was this discovery to the industry that fishermen at Uzuchi near Tokyo erected in 1963 a polished grey granite memorial on which was inset in bronze a portrait of Dr Drew, their “Mother of the Sea”. Each year they meet in commemoration of her.

111.POISONOUS AND VENOMOUS PLANTS AND ANIMALS Every kind of marine fish is not necessarily good to eat. Many can be very harmful. From time immemorial people have been warned against poisonous species. It was.an ancient Jewish rule that fish with no fins or scales should not be eaten. The puffer fish was recognized as poisonous in the times of the Pharaohs, and the Japanese have for long had regulations about their preparation as food. I n World War I1 American troops were warned never to eat fish which blew themselves up like balloons. It was in fact during that war that attention was really drawn to the dangers of poisonous food from the sea, when so many troops were dispersed over so wide an area of the oceans. More attention was then paid also to the occurrence of venomous animals. I n 1942 the Japanese produced a survival manual for the fighting forces with beautiful illustrations, and in 1943 a book was published in Australia on poisonous and harmful marine fishes. These have been superceded by the great three volume work by Dr Bruce Halstead published in 1965-70. Much research is now directed to the extraction and identification of poisons from fish, which may be dangerous to eat throughout the year or only at certain seasons. The poisons from organisms upon which shellfish may feed is also a special field for research. An outbreak of paralytic shellfish poisoning was recorded in 1793, but it was the much later outbreak which occurred near San Francisco in 1927 which resulted in the instigation of long-term investigations. These showed, ten years later, that the unicellular flagellate

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Goniaulax was the causative organism. The excessive blooming of this flagellate may give rise at times in the sea to " red tides ", whose resulting depletion of oxygen produces mass mortality of fish. Apart from this kind of poisoning, shellfish may of course also be harmful if taken from sewage polluted waters. I cannot leave the subject of dangerous marine animals without mention of the jellyfish Chironex which lives in waters along the Queensland coast of Australia and has been the cause of many bathing fatalities. A person badly stung by this jellyfish may be dead within two minutes. It is in fact the most venomous animal at present known. Its presence is thus a danger comparable with that of sharks in areas frequented by tourists.

IV. UNDERWATER STRUCTURES One of the early practical aspects of marine biology was the attempt to combat damage to the hulls of wooden ships by the boring shipworm Teredo. The Phoenicians and Trojans are known to have sheathed their ships with lead, and Pliny and Ovid wrote about shipworm and the use of lead. I n more modern times the rise of naval fleets and the building of harbours and dockyards increased the need for the scientific study of the deterioration of structures in sea water. Apart from boring animals such as Teredo and a few crustaceans, marine growths in general can also cause trouble. Corrosive pitting may arise in steel hulls under decaying masses of sedentary plants and animals. But even greater harm is caused by the growth of fouling organisms beneath the water line which increases the drag on ships, thus slowing them down and leading to great financial loss. One of the most general methods for the prevention of this growth is by the use of antifouling paints, whose principle is the gradual leaching out of toxic substances such as copper and mercury. It is easy to realize how much fundamental knowledge on the life histories, feeding habits and rates of growth of boring and fouling organisms must be acquired in such research. I remember occasions when we were asked how long ago enemy mines recovered from the sea had been laid. From the size of the marine organisms on them and a knowledge of their rate of growth it. was possible to supply the answer.

V. SHE-DESIGN While the study of the shapes and flight of birds has undoubtedly influenced the design of aircraft, observations on fish have probably played little part in the design of ships. Fish swim totally submerged,


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whereas, except for submarines, ships move on the surface of the sea. No doubt the very idea of a streamline shape must have originated from looking at fish, and this was certainly in the mind of Sir George Cayley, a founder of modern hydrodynamics, and it is on record that fish have been towed in experimental tanks by ship designers. There is of course another factor; fish propel themselves through the water by bending the body. I seem to remember a suggestion that one of the universities might experiment with a flexible boat in which the oarsmen rowed with a metachronic rhythm. Be that as it may, there is still very much interest in finding out how fish get their swimming efficiency, whether by using mucous secretion to reduce friction, by having porous skins, or by changes in the shape of the body. Certain skin movements are indeed to be seen in swimming dolphins. The bulbous swelling now given to some ships beneath the water line to reduce drag is reminiscent of the shape of fish and whales.

VI. ECHO-SOUNDING AND NOISE The introduction of echo-sounding after the first war added a new tool for marine biological research. It was noticed that some of the records showed not only a tracing of the bottom of the sea, but also, a false bottom in mid-water. It was soon realized that these must be caused by shoals of fish, and the use of echo-sounders for locating fish is now general throughout the fishing industry. But it was also found that in the open ocean such traces appeared at different depths and that they moved up and down through the twenty-four hours. These traces have proved to be caused by small oceanic fish and by some plankton animals which make nightly vertical migrations towards the surface. The method has been used to demonstrate that plankton animals move upwards during an eclipse of the sun, the vertical migration being stimulated by decreasing light intensity. Underwater hydrophones are used in war for detecting the presence of enemy vessels by the sounds they make. During the last war listeners were often confused by background crackling noises which rendered sonic listening valueless. These noises were found to be made by a small shrimp AZphaeus, known as the snapping or pistol shrimp because of the clicking noise it can make with its claw. As with birds, these sounds made by the shrimps are now found t o be related to their territorial behaviour. The important thing is that this discovery stimulated almost a new branch of marine biology to study under-

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water noises, which are now known to be made by many marine animals. The playing of records of the mating calls of such fish as the cod may have practical results.

VII. PHYSIOLO~ICAL AND MEDICALASPECTS I n my introduction I referred to the use of marine animals and plants for physiological research. I have also mentioned the puffer fish whose flesh is poisonous to eat at certain times of the year. The poison extracted from this fish has proved of use in research, and this leads me on to the subject of physiological and medical aspects of marine biology. It was early realized that animals would prove useful for physiological research. T. H. Huxley, on the occasion of the founding of the Marine Biological Association of the United Kingdom, remarked especially on this. It is perhaps significant that Huxley, as first President of the Association, has been followed in recent years by A. V. Hill and A. L. Hodgkin. Many marine animals are remarkable in having some organ or tissue which is specially suitable for physiological study. It is probably not generally realized for instance that the first direct evidence that insulin comes from the islet tissue of the pancreas was provided by the angler fish Lophius. This fish has islets up to one centimetre in diameter and it was in this easily isolated tissue that McLeod showed the presence of insulin in 1922. The fact that this special tissue was thus available in an exaggerated size in Lophius supports the hope that in the animal kingdom there will be found one specially suited for each physiological problem. A detailed knowledge of the structure and biology of marine animals is thus worth while. I n this respect none has proved more useful than the squid Loligo, in which J. Z. Young demonstrated the presence of giant nerve fibres. These radiate from two ganglia to different areas of the mantle to enable a simultaneous contraction resulting in the violent backward movement by jet propulsion. The largest of these long fibres is one millimetre in diameter allowing the insertion of an electrode or the rolling out of the axoplasm and refilling with fluids of known composition. I n conjunction with research on the nerve fibre of the squid two other marine animals have proved of great value. A common jellyfish Aequorea has the habit of luminescing. It was found that the luminescent reaction is triggered off by the presence of calcium, even in

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molecular quantities. The substance has been extracted and suitably named Aequorin. It is now in general use in research on the squid axon, for it immediately lights up on the passage of calcium through the axon membrane. The puffer fish Tetraodon produces a poison which on extraction is suitably named Tetrodotoxin. This substance blocks the membranes of nerve and muscle fibres so that they are no longer highly permeable to sodium ions. It is 100 000 times more active than local anaesthetics such as procaine and cocaine and has been used as an analgesic. A somewhat similar poison, Saxitoxin, extracted from flagellates such as Goniaulax, has comparable characteristics. I n the study of nerve physiology the sea hare Aplysia is complementary in value to the squid, for it has a giant nerve cell suitable for similar experiments to those on the squid axon. Marine animals have been much used for research on muscle physiology and here again the common barnacle Balanus has proved most useful for it has a specially large muscle fibre. . It was in the first decade of this century that C. R. Richet and P. Portier, working with extracts from the tentacle of the stinging Portuguese Man of War, Physalia, demonstrated the phenomenon of maphyllaxis or allergy, whereby the subject becomes hypersensitive as successive doses of the extract are administered. A few other examples of the special use of marine animals may be given. The horse-shoe crab Limulus is used for its eye and the skate for its labyrinth. The hagfish Myxine, which lacks a thymus, can be useful in immunological studies ; the sand-dollar Echinorachis has been used for studying anti-cancer drugs; and the spiny dogfish Squalus acanthias for investigating the transport of compounds across the blood-brain barrier. And one should not omit the egg of the sea urchin for the part it has played in developmental biology. And now one hears that the spines of this sea urchin may possibly be used as templates for making artificial blood vessels for coronary surgery. The realization that marine organisms may contain unusual substances has led in recent years to a widespread search throughout the plant and animal Kingdoms. The variety of animal life is so much greater in the sea than on land that it is likely that eventually many useful substances will be found. Many organisms have already been screened, especially for the presence of antibiotics and growth-inhibiting substances that might prove useful against cancer. Many have indeed been found to have cell-growth inhibiting characters, such as the extract from the liver of the clam Mercenaria, but apparently only one has so far proved to be A.M.B.-lB

11

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of practical value. This is an extract from a Carribean sponge Cytotehya crypa. This substance has now been synthesized and is used in the treatment of acute leucaemia. But the search goes on, and since there are thousands of different marine organisms it is necessary that the study of systematics should be encouraged, for the specimens must be correctly identified. Among substances obtained from marine plants alginic acid from brown seaweeds has many uses. It is much used in the food and cosmetic industries. Artificial fibres can be made from it and during the war it was in demand for making camouflage material. It has pharmaceutical and medicinal uses. Gauze impregnated with calcium alginate will prevent bleeding. It is used in material for making dental impressions. It has been shown to have a high specificity for binding strontium, and can thus be used in the inhibition of absorption of radioactive strontium by the intestine. The world supply of seaweed for alginate was 12 800 metric tons in 1970. I n the United States its proportional use in 1966 was as follows : 40% for laboratory, pharmaceutical and dental uses; 30% for bakery and confectionery industries ; and 10% for meat packing. Carageen from a red seaweed was used as a laxative in Roman times. An antibiotic which was extracted from a marine fungus obtained from a sewage outlet off the coast of Sardinia was found to be active against some bacteria which are resistant to penicillin and is now widely used under the name " Keflin ". VIII. PESTICIDE The search for possible useful substances has produced some of other than medicinal value. For instance, fishermen in Japan, using a polychaete worm Lumbrinereis brevicirra as bait, noticed that flies and ants died when they settled on the worms. Isolation of the so-called " nereistoxin ", which was found to have a ganglionic blocking action, led to the production of a new insecticide. This has been marketed as " Padan " since 1967 and is used in the control of the larvae of rice stem borers and other insects. I X . GEOLOGY AND METEOROLOGY The study of fossil marine organisms has always been a prominent feature in geological science. It is, however, only rather recently that there have been major advances in micropalaeontology made possible by investigations on the life histories of marine nanoplankton


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organisms in culture, and of their systematics which have been so advanced by the use of the electron microscope. A knowledge of the present distribution in the oceans of foraminifera has been useful in the study of cretaceous climatic zones. Increased knowledge of the life histories of coccolithophores should prove valuable, for these organisms form stratigraphical markers and are associated with oil shales. Microfossils, whose identity was previously unknown, have been shown by culturing to be the resting spores of dinoflagellates. Their distribution on the sea floor is at present little known, but it is thought that when this has been worked out these cysts will prove useful for studying palaeoclimatic changes and in stratigraphy. Only quite recently the elucidation of the life history of planktonic algae of the genus Pterosperrna, previously thought to be dinoflagellates, has proved of interest, for these organisms whose identity was unknown are used by geologists in stratigraphic studies of oil bearing rocks. There is increasing interest by geologists in the systematics of diatoms, while a study of the habits of living animals is being more used to understand the ecological conditions in past ages. The daily deposition of calcium by hermatypic corals is even being examined in the hope that it will throw light on the length of the day millions of years ago. Short term changes in weather and climate also have a notable effect on marine organisms, whether by altering the sea temperature on which their distribution depends, or on a greater scale such as the cooling or warming of the a.rctic which affects the pattern of oceanic circulation, a phenomenon that we have experienced over the last half century.

X. POLLUTION Until after the last war i t was probably a general opinion that the oceans are so vast that they can afford sufficient dilution and dispersion to allow industrial wastes to be poured into them without causing harm. But ever since World War I, when oil was beginning to replace coal in steam ships, damage to amenities on bathing beaches and the oiling and death of sea birds has become increasingly noticeable. The risks from oil pollution were highlighted by the " Torrey Canyon " disaster in 1967 when some 177 000 tons of crude oil were released to come ashore along the coasts of Cornwall and Brittany. This is the most documented of any such disaster, and this was made possible by

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the existence in the vicinity of an independent marine research laboratory at Plymouth, whose staff was composed of research workers in widely different scientific disciplines. Observations and experiments could thus immediately be made by chemists, physiologists, zoologists and botanists, all with the necessary ecological background and outlook. This is a very strong argument for the retention of such independent establishments in which the staff are not committed to some previously designed aim and whose research is in no way planned. On this occasion it was in fact the detergent oil dispersant which did the most damage to shore life. Now less toxic substances are available, and most Governments have organizations with stocks of material ready to deal with such emergencies. Little damage to marine life is likely to occur in the open ocean from oil which is biodegradable, but this is not so in enclosed seas. I n the Black Sea and in the Caspian, oil has caused damage by reducing the reproduction of algae which form the base of the food chain. It was perhaps in the year 1967 also when it was first fully realized how widespread in the ocean might be pollution from other substances. It was in that year that the occurrence of the pesticide DDT was recorded from penguins in the Antarctic. Since then there have been serious occurrences such as the death of 52 persons from mercury poisoning after eating fish in Japan, and similar pollution has occurred in the Baltic. Most enclosed seas have suffered a gradual build up of pollution and this is even noticeable in so large a sea as the Mediterranean. It should be realized that substances taken up by the smaller organisms get passed up the food chain to be concentrated in the larger animals and plants eaten by man. Damage can be caused to marine life, especially in estuaries, by excessive rise of water temperature created by heated effluents from power stations and other industrial plants requiring water for cooling purposes. This is, however, only a serious problem in tropical area.s, for in those regions marine organisms are often living very near their upper lethal limits of temperature. I n temperate regions damage is rarely found, because the animals and plants are adapted in their normal environment to a wide range of temperatures between winter and summer. Slight warming of the water in winter may in fact be beneficial to some shellfish in very cold winters. It is evident that a major effort in marine biology must in the future be concerned with the monitoring of the environment for pollution and with studying the effects of different substances on marine life before they are allowed to drain into the sea.


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XI. CONSERVATION The part played by marine biological research in the conservation of food supplies has already been touched on. But there is now need to have conservation in littoral and sublittoral regions for other reasons. Pollution, dumping and dredging may upset the natural ecology if not carefully controlled. Tourism may cause damage by over population of beaches, and the recent increase in subaqua diving and the growing demands for marine specimens for teaching purposes may cause some animals to be a t risk. One of the first instances of the effects of subaqua diving was that of the fishery for ormers, Haliotis, in the Channel Islands. These shellfish, which are much enjoyed as food, occur intertidally where they may be collected by hand. With the increase in tourism fears arose that the stocks might be depleted by the many visitors who collected these molluscs on the shore. Diving investigations showed a t first, however, that there was a large enough sublittoral population of ormers to keep the stocks going. But these were soon discovered by increasing numbers of visitors with subaqua equipment and the species is thus a t risk. The British Subaqua Club, which probably has something like 20 000 members, draws up Codes of Practice advising members not to cause unnecessary damage to certain species by over-collecting and spear fishing. Apart from the ormer, the gorgonid coral Eunicella is a favourite species for hand collecting, as is the wrasse for spear fishing. There are, however, many independent divers who collect specimens for profit. Sea urchins are special favourites and also starfish, whose dried skeletons are to be seen on sale in many craft and souvenir shops. While much of this type of collecting is very local and not likely to damage on a large scale, it is probably quite otherwise in the tropics where exot,ic shells and corals are collected in quantities for sale all over the world. Before the last war the few marine laboratories in the British Isles collected specimens for sale to schools and universities for teaching purposes and ran courses in marine biology. Thus there were known collecting areas which became examples of different types of habitat for teaching ecology. Since the war the teaching of biology has so increased that the pressure on some marine plants and animals has grown significantly. It is natural that the most popular grounds to be visited are those whose ecology has been fully described in the literature. There is thus a growing danger that certain animals typical of different habitats may be over-collected and the grounds themselves

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disturbed, not only by students but also by the crowds of tourists. I remember that even early in this century the old fisherman collector a t the Plymouth laboratory, when he found a rare animal, used to plant it out in a special place which he kept secret. When one was asked for he could thus miraculously supply it. Some animals may be wanted for special investigations or demonstrations. For instance, after the first war the spider crab Maia became in great demand for the supply of its blood for demonstrating the chemistry of haemocyanin. It is still in demand, but fortunately it is a common and abundant amimal. A less common animal might be required and its collection would need to be watched. It may in fact prove necessary one day to rear some animals for teaching, just as many unicellular plants are now cultured for feeding and rearing experiments. Thus, it can be seen that there is a need for the designation of some localities as marine conservation areas, both above and below low water mark, and for the limitation of collection of certain animals. I n the British Isles the only area so controlled is Lundy Island, but the whole question is under active consideration. I n other parts of the world there are now many so-called " marine parks ". These may be set aside for recreational enjoyment, but will have restrictions on fishing and collecting. There are many such areas on the coast of Queensland in the Great Barrier Reef area, in America, and in the Pacific. Typical is the Eilat Coral Nature Reserve in the northern end of the Gulf of Aqaba, where a coastal strip 1 2 0 0 metres long is fully conserved. There must be close on 100 such areas now regulated or under consideration. Before any area can be selected a detailed knowledge of its ecology is first required. As long ago as 1938 the coral reef surrounding Green Island off the coast of Queensland was designated a marine reserve, and except for recreational fishing full protection was given to marine organisms. At the last International Conference on Marine Parks and Reserves held in May 1975 at Tokyo, the Government of the Cook Islands offered the atoll of Manuae as a World Marine Park. This was one of the first islands in the South Pacific to be discovered by Captain Cook, who named the two small islands the Hervey Islands in 1773. To recapitulate, the services of marine biologists will be required for keeping watch on the ecology of the following types of reserves. 1. 2.

Scientific Reserves, for the study of marine and estuarine ecology. Conservation Reserves, to maintain unspoilt areas of different ecological types, or areas where rare species occur.


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Educational Reserves, to allow access for teaching purposes to different types of grounds. 4. Recreational Reserves, for the enjoyment of tourists in areas of special scenic beauty where underwater conditions are of special interest and can be viewed in underwater glass-walled buildings or by subaqua diving. 3.

XII. MANAND

THE

MARINE ENVIRONMENT

As well as changing the ecology by overfishing or pollution, man can alter the environment deliberately to his advantage. For instance, in the Caspian Sea the Russians noticed that there was a large area of bottom composed of sandy silt with much detritus, rich in organic matter, in which the fauna was very sparse. They accordingly introduced the polychaete worm Nereis diversicolor from the Sea of Azov in 1939 and 1940. The worm, which is a detritus feeder, thrived and by 1956 its biomass was estimated as one million tons with an annual production two or three times greater. This formed a greatly increased food supply for fish, including the sturgeon. Of course, a number of animals have been introduced in different parts of the world for intensive culture, but there is always a danger that an undesirable pest may be brought with them, such as the slipper limpet which competes with the oyster for food. Biological balance can thus be upset. I n this respect the introduction of species requires very careful consideration. The possibility of introducing the giant kelp into European waters as a source of alginic acid is at present under consideration, and this should be resisted. The Japanese brown seaweed Sargasswm has appeared off the Isle of Wight. It is spreading and will probably prove impossible to control. Other major developments by man may have unforeseen results. There used to be a major fishery for sardines, which appeared off the coast of Egypt at the time of the Nile Flood each year. But with the building of the Assouan Dam the Nile has ceased to pour its seasonal supply of nutrient rich water into the sea and the sardines no longer come to feed there. When the Suez Canal was built, the presence of the Bitter Lakes along its course formed an effective barrier to the migration of animals from the Red Sea to the Mediterranean. But over the years the continual stirring of the water in these lakes by passing ships has brought the bottom salt deposits into solution and the gradual dilution has so reduced the salinity of the water that it no longer forms a barrier. As a result, a number of different animals from the Red Sea are now finding

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their way into the Eastern Mediterranean. If poor quality fish were t o replace good quality fish such an interchange would not be beneficial. It is for this reason that it is necessary to know the fauna and flora of different regions and gain a full understanding of their ecology before some major undertaking can be started. It has, for instance, been suggested that the Panama Canal be replaced by a direct excavated channel, thus putting the Pacific fauna into complete connection with that of the Atlantic. The two faunas are very different and the effect of their mixing would be very difficult to forecast. I n this brief survey I have tried to show how a knowledge of marine biology bears on human affairs. It is absolutely essential for the management of our food resources, and is also necessary so that we may guard against excessive polhtion of the sea, and maintain and conserve some species and their environment. It has practical uses, such as in the prevention of structural deterioration and the growth of fouling organisms. A knowledge of the structure and biology of marine animals and plants is of undoubted value for physiological research and will no doubt play an increasing part in the development of medical science. It is necessary so that the effects of proposed major building works by man may if possible be foreseen. Above all perhaps it is necessary for its own sake, for the great variety of living forms to be found in the sea makes it essential in the teaching of biology. The seas cover nearly three-quarters of the earth’s surface and are nearly two miles in average depth. They thus afford infinitely more living space than can be found on land and will no doubt for many years to come yield for our interest many new and fascinating forms of life, if we will continue to search for them.

Adv. mar. Biol., Vol. 15, 1978, pp. 249-287.

NUTRITIONAL ECOLOGY OF CTENOPHOR€SA REVIEW OF RECENT RESEARCH M. R. REEVEAND M. A. WALTER University of Miami, School of Marine and Atmospheric Science, Miami, Florida, U . S . A .

.. ,. ,. .. .. .. I. Introduction . . .. .. .. 11. Feeding Mechanisms and Behavior . . A. Feeding Mechanism and Behavior in Mnemiopsia . . B. Comparison of Feeding Behavior in Other Tentaculata C. Food of Tentnculata . . .. .. .. .. D. Food and Feeding Behavior of Nuda .. .. 111. Ctenophore Predators . . .. .. .. .. .. .. .. .. .. .. IV. Chemical Composition . . .. .. .. . . . .. .. V. Ingestion Rates .. .. .. .. .. .. .. VI. Digestion .. .. .. .. .. VII. Respiration and Excretion .. .. .. .. . . .. .. VIIT. Growth Rate .. .. .. .. . . .. .. IX. Fecundity .. .. .. .. .. .. X . Growth Efficiency .. .. XI. Seasonal Variations in Ctenophore Populations .. . . .. .. .. .. .. XII. Conclusion XIII. References .. .. ..

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I. INTRODUCTION There has been a tremendous increase in quantitative studies on the ecological role of planktonic ctenophores in the marine environment during the last decade. Most earlier studies were restricted to observations on ctenophore blooms and their correlation with the rapid decline of the standing stock of the rest of the zooplankton community (Bigelow, 1915; Nelson, 1925; Bigelow and Leslie, 1930; Russell, 1931, 1935; Barlow, 1955; Praser, 1962, 1970; Cronin et al., 1962; Hopkins, 1966; and others). The few earlier observations of living ctenophores were concerned with feeding mechanisms and food types (e.g. Lebour, 1923; Nelson, 1925; Main, 1928; Weill, 1935; Hyman, 1940 ; Nagabhushanam, 1959 ; Kamshilov, 1960a, b) which are reviewed in detail by Fraser (1970). The phylum Ctenophora contains two classes and five orders (Bayer and Owre, 1968). 249

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I. Class Tentaculata. All with tentacles, at least as larvae. A. Order Cydippida. Well-developed tentacles throughout life. B. Order Lobata. Tentacles reduced in adults, with development of large oral feeding lobes, moderately compressed. C. Order Cestida. Body extremely compressed and laterally expanded, tentacles reduced in size. D. Order Platyctenea. Compressed, oral creeping surface, usually two well-developed tentacles, sessile. 11. Class Nuda. All lacking tentacles, even a.s larvae. A. Order Beroida. Carnivores on other ctenophores and other soft-bodied zooplankton. Nearly all detailed studies on distribution, seasonal population changes and ecology refer t o the genera Pleurobrachia, Bolinopsis, Mnemiopsis and Beroe, which are common to inshore waters. Within the class Tentaculata, Pleurobrachia belongs to the order Cydippida, whose members feed using tentacles exclusively. With an adult size in the range 10-20 mm, it is generally smaller than Bolinopsis and Mnemiopsis (order Lobata), which outgrow the tentaculate phase and develop oral lobes and other projections for feeding as adults, in the range 50-100 mm and larger. Beroe on the other hand, in the class Nuda, never develops tentacles or lobes, attains an intermediate size, and preys almost exclusively on other planktonic ctenophores. The phylum is not restricted to inshore waters, however, and members of both the Lobata and Cydippida have been reported in oceanic environments, as well as species of the order Cestida, which are long and ribbon-like, being compressed laterally in the sagittal plane. A fourth order of Tentaculata-Platyctenea are flattened in the oralaboral axis and are partially or entirely non-planktonic as adults. Beyond occasional records of occurrence, very few reports exist which provide information on the ecology of either the oceanic or benthic ctenophores. It may be premature, however, to assume that ctenophores in these environments are rare, or of little significance in terms of their predatory impact. There may be other reasons for their obscurity. Most ctenophores do not preserve in formalin solutions. Exceptions to this general rule are Pleurobrachia and Beroe. Many ctenophores are 80 fragile that anything but the gentlest of collection methods quickly fragments them or renders them as unrecognizable gelatinous masses. Mayer (1912) and Harbison et al. (1978) reported that Leucothea is destroyed by even a slight current of water. They questioned the worth of traditional collection methods for such animals. The latter authors have made numerous observations by SCUBA

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across the Atlantic and reported that ctenophores occur more widely and nearly as abundantly in the open ocean as they do close to shore and suggested that they occupy an important place in the community structure of the open ocean. This review summarizes information on their nutritional biology (from observations on living animals mostly in the laboratory) and discusses attempts to utilize laboratory data to interpret environmental fluctuations.

11.FEEDING MECHANISMS AND BEHAVIOR The feeding behavior of Pleurobrachiu, Bolinopsis and Beroe were well documented by the Institute for Scientific Film, Gottingen, West Germany, under the supervision of Wulf Greve who also described the contents of the films (Greve, 1975a, b). These films may be rented or purchased. We have maintained Mnemiopsis rnccradyi through multiple generations in the laboratory for several years and made detailed observations of its behavior. We have also made observations on living ctenophores in the laboratory representative of all the other orders. We also draw heavily on the report of Harbison et al. (1978) to provide information on oceanic forms. A. Feeding mechanism and behavior in Mnemiopsis The newly hatched larvae of M . mccradyi Mayer are equipped with the typical cydippid tentacles and sheaths and eight equally spaced meridional rows of plates composed of transverse bands of long fused cilia known as comb rows. This is the tentaculate stage (Fig. 1A). As the larva grows, it loses the tentacular sheath and the tentacles move orally to lie alongside the mouth in a very reduced form (Fig. 2F). The compression of the oval body of the larva can be seen in 5-6 mm animals (Fig. lB), which results in 4 of the 8 comb rows being longer. The 4 shorter rows form processes known as auricles, with a ciliated edge above the mouth, two on each side, and begin to appear in animals of 8-9 mm in length (Pig. 2F). The longer ones form rounded muscular lobes on either side of the mouth, and by the time the animal attains 1 6 1 5 mm the transition is complete (Fig. 2A-D). Both the larva and adult feed on actively swimming prey such as copepods. During the transition period both tentaculate and lobate methods of feeding may be employed, in proportion to the relative size of tentacles and lobes (Fig. 1B-D). Mnemiopsis larvae can entirely retract the two tentacles into their

FIQ.1. Mnemiopsis. A. A 6 mm larva sets its tentacles for fishing. B-D. Prey capture sequcnce in an 8 mm larva showing the beginning of lobe development. B. Several copepods are entangled in the tentacle which is rapidly contracted. C. The larva rotat,es to position the prey-bearing tentacle so that further contraction (D) will draw the copepod t o the mouth. (p prey, t tentacle).

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tentacular sheaths on either side of the body, between the oral and aboral poles. In order t o " set " their tentacles for food collection animals swim vigorously, oral pole forward, often in a curved or helical pathway, relaxing and trailing their tentacles behind them, while the lateral branches also relax and expand up to two bodywidths from the main tentacle. Figure 3A-D and E-F show two sequences of animals (photographed in aquaria) setting tentacles. As the tentacles reach an extension over 10 times the body diameter, the ctenophore body comes to rest as if restrained by the drag force of total tentaculate area. The tentacles can be some 25 times longer than the body diameter of the animal. The animals drift in this manner, often until disturbed by contact, such as with another animal or air-bubble (in the experimental container) or food organism such as a copepod. I n the absence of contact, animals will contract and then reset their tentacles, sometimes within a few seconds of the first " trial ". However, if prey is captured, it becomes entwined in the tentacular branches which are lined with sticky colloblast cells. It is generally believed (see Hyman, 1940; Fraser, 1970) that prey contact stimulates the release of colloblast filaments from the colloblasts borne on the tentacles, in a manner similar to the nematocysts of Cnidaria, but sticky rather than poisonous. These serve the purpose of restraining the prey as the main tentacle and branches are rapidly contracted to bring the food adjacent to the mouth. Weill (1935), Hyman (1940) and Ralph and Kaberry (1950) believed a poison was involved, but our observations indicate that after capture a copepod continues to struggle and occasionally frees itself and swims away. The ctenophore manipulates its tentacle into the mouth, deposits the prey, and withdraws its tentacle (Fig. 1B-D). Food is positioned at the mouth of the animal by quickly retracting its prey-carrying tentacle and by performing a 180" rotation which moves the foodbearing tentacle adjacent to the mouth (Fig. lC, D). The animal immediately resets its tentacle. Examining the prey after ingestion, small sections of the tentacle can be seen wrapped around it (Walter, 1976). The tentacles must presumably be continuously growing from the base to compensate for this loss. Lobate ctenophores searching for food swim mouth forward (Fig. 2C) with their lobes spread open like wings, upon the surface of which prospective food organisms impinge. The prey appear to become enmeshed on the mucus-lined inner surface of lobes which also contain colloblast cells. The currents set up by the auricular cilia move the prey towards the small tentacles (which further immobilize it), and dong the pharyngeal grooves into the mouth (Fig. SC, F). Newly

FIG.2.

(For legend see facing page)


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FIG.2. Mnemiopsis adult (total length 70 mm). A-B. Tentacular and sagittal plane vicws of animal. C. Oral view of animal swimming with lobes extended. D. Animal with lobes folded to enclose a Chamber. E. A bolus of captured copepods partially ingested. F. Close-up oral view. (p prey, t tentacle, 1 lobe, a auricle, m mouth, pg prey copepod in pharyngeal groove, c comb row).

ingested copepods can be seen to be still active as they move up the pharynx into the stomach area (Fig. 2F). Digestion time varies from 1-3 h from larva to adult a t 21°C. Larvae of M . mccradyi exhibit feeding behavior patterns in small containers which are dependent upon their level of starvation. When starved for 24 h the larvae extend their tentacles fully, frequently changing position and re-setting as described above. If no food is encountered, these search periods are followed by periods of inactivity. When food becomes abundant tentacle length is reduced to 1-2 x their body diameter (Fig. 3A), and animals make frequent contact with food as they swim actively until their guts are full. At this point, active swimming and feeding cease and their tentacles become extended to 2-3 x their body diameter as they drift. This behavior of the larvae is comparable to that described by Rowe (1971) for Pleurobrachia. I n a tank they remain active, although not necessarily feeding, if there is food present. However, in a tank with no food they tend to clump together at the surface. Lobate adults appear bell-shaped under starved conditions

FIQ.3.

(For legend see facing page)


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FIG.3. Mnemiopis larvae (8 mm). A-D and E, F. Two sequences showing setting of tentacles, the first in a curved and the second in a helical pathway.

(Fig. 2A-C). They often swim vertically up and down in an aquarium with their lobes extended a t right angles t o their direction of travel. The lobe width in this condition can be up t o 116% of the animal length. Upon the addition of food to the aquarium the lobe width decreases to about 79% of the body length (Fig. 2B) while the animal feeds. When a number of copepods are in the oral area, the ctenophore will fold its muscular lobes inward (Fig. 2D), which prevents the copepods from escaping and thereby ensures their ingestion. As with the larvae, adults alternate periods of inactivity a t either the surface or bottom of the aquarium, with active searching under prolonged conditions of starvation. Introduction of food invariably stimulates activity. I n high food concentrations (see Walter, 1976) after having been starved for 24 h, lobate ctenophores begin to exhibit what appears to be superfluous feeding. Once their guts are full they still continue to " feed ') by entangling prey in mucus, which results in a bolus a t the oral region (Fig. 2E). Quite frequently they will either " spit out " this enmeshed ball of copepods or completely evacuate their guts, and continue to feed. At the same time mucus strands are released into the water column in which other copepods become entangled. At times mucus strands containing 2-3 copepods can also be seen trailing from the oral region of the ctenophore, which eventually

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break away. This behavior pattern can continue for several hours until the concentration of food is reduced to a point where all the copepods that are captured can be ingested. By this time, the bottom of the experimental container is covered with a layer of partially digested, and undigested but dying copepods. Examination of the guts of these animals after one hour of exposure to low and high concentrations of food indicates a definite difference in the amount of digestion that has taken place. In high concentrations the food organisms are still whole and recognizable, whereas in low concentrations the copepods are partially digested and, in some cases, indistinguishable. Visual observations were made of lobate Mnerniopsis passing under the RSMAS laboratory dock on several occasions, and SCUBA observations were made off Bimini in the Bahamas on two patches of ctenophores of the genus Bolinopsis. I n most cases the animals were oriented against the current as in the laboratory, which potentially brought food to impinge on their extended lobes. An adult Mnerniopsis which had been starved in the laboratory for three days was also set free into the sea and observed for an hour in the natural environment. It exhibited the same behavior seen in the laboratory, i.e. swimming vertically up and down in the water column. On seven separate occasions when patches of ctenophores were observed in the water off the laboratory dock, lobate animals were individually withdrawn and isolated in copepod-free water for immediate microscopical examination of their gut contents. Additionally, quantitative 200 pm mesh net tows were made to obtain an estimate of the density of copepods in the vicinity o f the ctenophores a t the time of capture (Walter, 1976). At no time was the environmental food concentration in excess of 1 0 0 0 copepods/m3. Animals appeared to be feeding actively down to a t least 100/m3. The number of food organisms in the guts of some 200 ctenophores was also recorded as a function of animal length (Walter, 1976). These data confirmed laboratory observations (Reeve et al., 1978) that large lobate ctenophores can hold up to 100 food items in their gut a t any one time, but are contrasted to laboratory observations in that they accomplish this a t much lower food concentrations. At 1 000/m3 in the laboratory, ctenophores are rarely seen with food in their guts. Reeve, et al., (1978) suggested that this discrepancy may be due to the wild animals encountering small patches of food at much higher concentrations. These observations, measurements and photographs on both the larvae and adults under different conditions of food availability show that the mechanism of feeding can be adjusted to the degree of starvation of the ctenophore and the concentration of the food. The


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presence of such a wide range of control of the food collecting mechanism is surprising in light of the quantitative observations reported in Section V on the relatively automatic nature of the ingestion process. Because the food collection process is continuous in lobate ctenophores, i.e. not interrupted by the act of ingestion, there appears to be no practical upper limit to food density at which collection rate becomes independent of food density (i.e. no critical food concentration). I n tentaculate ctenophores, food collection is discontinuous because the tentacle must be withdrawn from fishing t o permit ingestion. As food concentration increases, the proportion of non-fishing time must also increase and Reeve et al., (1978) showed that at very high food densities their ingestion rate reaches a maximum and becomes independent of further food density increase. B. Comparison of feeding behavior in other !l'entacuZata Our observations on the feeding behavior of Pleurobrachia bachei Agassiz from British Columbian waters also cultured in our laboratory differ in some details from that described for Mnemiopsis larvae. I n laboratory aquaria, similarly-sized members of the two genera can be distinguished in their behavior because Pleurobrachia (Fig. 4A) is a more active swimmer trailing short tentacles, and rarely drifts with tentacles a t their maximum extension. I n this way it is more of it search than an ambush predator, when compared to larval Mnemiopsis. Greve (1975a, b) reported that an animal can contract one tentacle which has caught a prey organism while permitting the other to remain extended and fishing. As the tentacle contracts and prey approaches the mouth, Pleurobrachia begins to rotate in a plane which draws the tentacle across the mouth region. The portion of the tentacle bearing the prey gains entry to the mouth (Greve, personal communication) or is draped over the mouth and the prey is " wiped into ') the mouth (Rowe, 1971). I n Pleurobrachia (Greve, 1975a, b ; Rowe, 1971 ; Walter, unpublished) the animal may complete several rotations, but Mnemiopsis larvae (Walter, 1976) rarely rotate more than 180" to accomplish the same end. The portion of their tentacle attached to the copepod breaks off in the mouth and is digested. Very little is known in detail about the feeding of other members of the Cydippida. Representatives of such genera as Hormiphora, Tinerfe and Callianira have been observed by ourselves and Harbison et al. (1978). Unlike the simple filamentous threads of Pleurobrachia and Mnemiopsis, the tentacles of Hormiphora bear more than one kind of side branch (Mayer, 1912) which do not extend very far from the

Fro. 4. (For legend see facing page)


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FIG.4. A. PEeurobrachia. B. Beroe, showing mouth, 45 mm. C and D. VaEticula 15 mm. (body of animal not visible on substrate in C). E. Bolinopsis, 40 mm. F. Ocyropsis, 30 mm, swimming by muscular flapping of lobes. All photographs are of living animals, and in aquaria (except D, which was attached to glass in a dish).

body of the animal, and give it the appearance of already having captured small prey organisms. H . plumosa Agassiz carries large batteries of colloblasts on its tentacles (Harbison et al., 1978) similar to the batteries Qf nematocysts carried by some siphonophores, which might indicate an adaptation to the capture of larger prey such as small fish. Callianira is not readily recognizable as a cydippid in life because its pattern of movement through the water is very uncharacteristic. Instead of the sedate gliding motion of most ctenophores, this animal moves vigorously and rapidly through the water, making observations on its feeding very difficult. Amongst the lobate adult forms, Bolinopsis (Fig. 4E), which we have observed often in the laboratory, moves and feeds in a manner similar to Mnemiopsis. It is more susceptible to damage than Mnemiopsis and frequently suffers lobe atrophy in laboratory aquaria. It is also similar to Mnemiopsis in occurring in dense swarms in inshore waters. Harbison et al. (1978) described the feeding behavior of the lobate genera Eurhamphaea, Leucothea and Ocyropsis. The first two are progressive elaborations of the lobate feeding mechanism. In Euramphaea

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the wide-spread mucus-covered lobes enmesh copepods impinging on their inner surface, and contract in the region of contact moving the prey nearer the labial ridge, along which it is moved by tentacles and cilia to the mouth. The auricles move back and forth and may trap food themselves, or push a copepod onto the lobe surface. While feeding, Euramphnea is either motionless or moves slowly, lobes forward (as does Mnemiopsis). Harbison et al. (1978) reported that Leucothea multicornis Quoy & Gaimard, reaching 20 cm in diameter, has developed lobes larger than other members of the order. The huge diaphanous lobes are very delicate and the animal remains motionless while feeding, apparently relying on the constantly moving auricles to keep the lobes spread out by maintaining gentle water currents. I n addition to the auricles and mucus lined lobes, this ctenophore also has two very long tentacles, which extend beyond the confines of the lobe area. L. ochracea Mayer was reported to have numerous simple side branches on these tentacles (Mayer, 1912), which suggested to Harbison et al. (1978) the possibility that this genus also retained the typical cydippid tentaculate fishing ability. Ocyropsis (Fig. 4F) cannot be confused with any other lobate ctenophore when alive, because it is unique in being able to propel itself vigorously through the water in an aboral direction by a series of bursts of activity, involving muscular contraction of the oral lobes in unison, to give the impression of flapping wings (see descriptions of Mayer, 1912, and Harbison et al., 1978). It is also capable of the normal oral or aboral gliding movements produced by the comb rows. Both reports noted a lack of tentacles in the adults, and Harbison et al. (1978) stated that no mucus was evident on the lobes. They described a feeding mechanism quite different from other lobate adults, which we have also observed in the Iaboratory. The mouth of Ocyropsis is muscular and quite prehensile and " when a prey organism touches the inner lobe surfaces the lobe edge quickly curls over it. The entire lobe contracts somewhat toward the mouth, which simultaneously reaches over and snatches the prey out of the lobe. The feeding action takes a second or less '' (Harbison et al., 1978). They reported also that it could capture larger zooplankton such as small fish and euphausids. I n the mobility and extensibility of its mouth we are reminded of Beroe, although even Pleurobrachia has some ability to manipulate food with its lips (see above). The order Cestida, the ribbon ctenophores, are not uncommon in tropical waters and well-known for their serpentine swimming motion. Harbison et al. (1978) reported, however, that in nature they rarely


3G3

move in this manner, except when disturbed, Instead, the animal hangs motionless in the water, or swims slowly forward with the oral edge leading (as do most lobate ctenophores), its oral tentacles extended up t o the width of its body. Copepods contacting the tentacles are transferred to the oral groove by contraction of the tentacle, and moved along the groove to the mouth. We have had the opportunity to observe the feeding behavior of the Platyctenea as represented by Vallicula (Fig. 4C, D), a relatively small creeping form, which has lost its comb rows and attaches to macroalgae such as Halimeda. Valliczcla is easily overlooked, being inconspicuous, flattened and colorless. It is usually recognized first when an aquarium tank containing live algae in the laboratory is seen to have long delicate single side-branched tentacles (Fig. 4C) stretching and undulating in the circulation throughout the water column. On closer inspection these tentacles emanate not from obvious planktonic cydippid-type larvae, but small slime-like blobs attached to the surface of the algae. The delicacy and usual extension of the tentacles are reminiscent of lobate larvae such as Mnemiopsis, and contact with food elicits the usual ctenophore response of rapid tentacle contraction. I n good food conditions, they grow quickly and multiply by " a kind of fission which recalls pedal laceration in anemones " (Bayer and Owre, 1968). I n an aquarium, a t least, within a few days, a mass of delicate tentacles fill the available water column. Although they do not favor attachment to the bottom sediment, aquarium side-walls provide an acceptable site for them.

C. Food of Tentaculata The Cydippida and Lobata have almost entirely been cansidered to be exclusively carnivores but suggestions have occasionally been made (e.g. Nelson, 1925; Miller, 1970; Miller and Williams, 1972) that they must also rely on phytoplankton or detritus a t times. Baker and Reeve (1974) established experimentally that Mnemiopsis mccradyi starved when exposed to phytoplankton or detrital suspensions only. Hirota (1974) noted that on the rare occasions when phytoplankton was seen in the guts of preserved Pleurobrachia, it could have been originally in the gut of ingested copepods. Harbison et al. (1978) reported that Eurhamphaea vexilligera Gegenbaur could trap fine particles, such as carmine, and ingest them, but they did not know if this had any significance. Baker and Reeve (1974) noted that in a densely colored phytoplankton culture, some coloration of the gut of Mnemiopsis was observable, due no doubt t o adhesion of some cells

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to the mucus on the lobes and its subsequent ingestion. Survival of the ctenophores compared to animals in filtered water was not extended. To a greater or lesser extent, probably most zooplankton animals are susceptible to predation by Cydippida and Lobata, depending on the relative size of the organisms involved, and other considerations such as swimming ability of the prey. Fraser (1970), on the basis of gut analyses of preserved specimens, confirmed Lebour’s (1922, 1923) observations that they were miscellaneous carnivores. I n virtually any plankton sample, crustaceans, particularly copepods, predominate and this alone assures that copepods are their main source of food (Fraser, 1970; Hirota, 1974). Bishop (1968)reported that Bolinopsis and Pleurobrachia select small (1 mm) Pseudocalanufl in preference to Epilabidocera (3 mm), but both Lebour (1922)and Kamshilov (1959) considered the large Calanus to be the major food source of Bolinopsis. Walter (1976)has seen adult Calanw actively struggle free from the tentacles of Pleurobrachia. The experimental conditions (density of ctenophores and prey, size of container and condition of organisms) probably greatly affects the outcome of such experiments. Kremer (in press) found that in natural mixtures containing mostly cyclopoid copepods and veliger larvae, feeding rate of Mnemiqsis leidyi Agassiz was much reduced compared to when feeding on calanoid copepods and cladocerans. She cited prey behavior and palatability as possible reasons, but the small size of the former group may also be significant. Whenever food, which was offered to tentaculate ctenophores in aquaria, contained significant percentages of barnacle nauplii, we always observed that by the next day only barnacle nauplii remained. We subsequently observed encounters between these nauplii and the outstretched tentacles. When copepods of similar size make contact, they are immediately enmeshed in adjacent sidebranch tentacle strands, and rapid contraction towards the mouth occurs. Swimming barnacle nauplii do not disturb the fishing tentacles and the nauplii do not adhere to them. Preliminary experiments suggest that the ctenophores do not actively avoid capturing barnacle nauplii. Extracts of fresh nauplii in the surrounding water do not prevent the normal capture of copepods, nor does the extract of copepods stimulate capture of nauplii. The passive food capture mechanism of the lobate Mnemiopsis does not discriminate between copepods and barnacle nauplii , which both appear to be trapped on the mucus-lined lobes. Quantitative feeding experiments over four days confirmed that tentaculate Pleurobrachia and Mnemiopsis larvae lost weight when only barnacle nauplii


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were available. It is possible that the slow sculling action of the swimming barnacle nauplius does not stimulate the tentacle in the way that the copepod does, with its higher frequency vibrations. Other workers have suggested that swimming behavior affects chances of catchability by tentaculate ctenophores. Anderson ( 1974) made a study of the vertical distribution of zooplankton in St Margaret’s Bay, Nova Scotia. He attributed the small proportion of the copepod Pseudocalanus in the guts of captured P ~ ~ u r o ~ r a c ht oi athe fact that the population center of the copepod was deeper, and to its tendency t o a hop and sink swimming pattern which caused it to retrace its path on sinking. Temora, on the other hand, lives closer to the surface and swims more actively in a horizontal direction. Its chance of encountering tentacles is greatly increased and was reflected, according to Anderson, in its capture rate relative to its abundance. Oithona moves relatively little and was caught less frequently than any of the other common copepods. The same copepod, however, formed the largest fraction of the diet of the lobate Bolinopsis, possibly because passivity is no defense against the feeding mechanism of this ctenophore, and activity could be a potential survival factor. Since both types of ctenophore coexist, however, the swimming behavior of Oithona may have developed more through its own predatory requirements than any defense mechanism. According to Hirota (1974) potential prey of Pleurohrachia can be divided into three categories, those which are too strong and break away from the tentacles, those which struggle but get more entangled, and those which are passive ‘‘ often being dislodged from the tentacle hold, or, like some decapod larvae, are too spiny to be readily ingested and not eaten ”. Ctenophores have long been suspected as having serious effects on fisheries, not only through competing for the same food source, but by providing an alternative but less nutritious food which delayed summer fattening of herring (Manteufel, 1941) and perhaps (Scott, 1913) by retarding the sexual maturity of mackerel, and possibly by destroying fish eggs. Fraser (1970) discounted this latter possibility in Scottish waters on the basis of gut contents over four years, but cited the earlier workers’ positive beliefs regarding predation on the larvae of oysters and other shellfish.

D. Food and feeding behavior of Nuda The feeding behavior of Beroe (Fig. 4B), which preys on other lobate and tentaculate ctenophores, has been studied by Kamshilov

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(1959, 1960a, b), Horridge (1965), Greve (1970), Anderson (1974) and Swanberg (1974). Greve (1970) found prey specificity in that Beroe cucumis Fabricius fed successfully only on Bolinopsis infundibulum (Martens),while B. gracilis fed entirely on Pleurobrachia pileus Fabricius. Although Anderson (1974) reported that in aquaria B. cucumis would feed on either Pleurobrachia or Bolinopsis, Greve et al. (1976) believed this to be a rare occurrence and noted that although B. cucumis was found in the North Sea in the presence of Bolinopsis, i t was not abundant. They speculated that the Bolinopsis population did not support population growth of the beroid. They cautioned care in the interpretation of earlier literature regarding prey preferences of these two species because Bolinopsis do not preserve in formalin, and young of the species of Beroe are particularly difficult to separate. I n our limited experience of temperate-water Beroe cucumis we have been unable t o induce them to feed on Pleurobrachia. Swanberg (1974), on the other hand, stated that he observed B. cucumis and B. ovata Bosc to feed on any ctenophore with which they came in contact. These did not include Pleurobrachia spp. which were absent from his locality but did include such aberrant forms as Cestum veneris Lesueur (Venus’ girdle). Authors generally agree that beroids feed exclusively on other ctenophores. Greve (1971) and Swanberg (1974) reported instances of “accidental” cannibalism in which the smaller ingested animal was egested alive. Hernandez-Nicaise (personal communication), however, has fed Beroe on salps. Greve et al. (1976) suggested that warmer water beroids became progressively less specialized in their feeding in response to the requirements of “ optimal foraging ” in the two systems, and speculated on pathways of speciation of the class in relation to its food. A great deal of experimental work on food preferences, survival and growth rates are required before the somewhat clouded picture of feeding habits of Nuda can be clarified. Beroids feed on prey which range greatly in relative size. I n the case of prey larger than themselves, they appear to attach themselves and suck the prey tissues into their mouth (see Greve, 1971). According to Swanberg (1974), however, some 3 000 macrocilia, arranged in hexagonal arrays and forming part of a ciliary band around the inside of the entire mouth, beat inwards forcing prey tissue into the pharynx. When filled to capacity the enveloping lips contract, and the sturdy cilia cut through the tissue ‘‘ in the manner of moving teeth ”. Horridge (1965) described the fine structure and Swanberg ( 1974) illustrated his account by scanning electron micrographs. A young Beroe, introduced accidentally with a live sample of zoo-


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plankton as food for a population of Mnemiopsis, can easily go unnoticed. On more than one occasion we have discovered a large Beroe and no Mnemiopsis on revisiting the aquarium several days later. We have also observed large beroids t o quickly ingest smaller Bolinopsis in a manner graphically described by Horridge. The animal swims slowly oral end forward, and when its lips contact the smaller prey organism it “ opens its mouth (Fig. 4B)and gives a great gulp. The gulp is caused by the contraction of radially arranged muscle fibers throughout the whole animal. The mesogloea stiffens and the animal expands in size, drawing water rapidly into the mouth ” and the prey with it. Swanberg (1974) showed that Beroe swims more actively in the presence of prey organisms and suggested chemical recognition of food. Kamshilov (1960a) noted that swimming activity decreased with progressive starvation, which we have also seen for Mnemiopsis and Pleurobrachia. I n a laboratory aquarium the latter organisms tend t o clump together a t the water surface after 2-3 days of starvation, but separate and become active immediately when fresh food is provided.

111. CTENOPHOREPREDATORS Besides Beroe, the population dynamics of which have been extensively investigated in relation t o populations of other ctenophores (Greve, 1971; Hirota, 1973, 1974) there appear t o be no usual predators of large blooms of ctenophores, although this assumption might be attributable to difficulties in recognizing their remains in the gut contents of potential predators. Our unpublished observations of Biscayne Bay, Florida, populations of Mnemiopsis mccradyi and Saanich Inlet, British Columbia, Pleurobrachia and Bolinopsis where beroids are rare, suggest no major predator. Fraser (1970) reviewed several earlier observations showing that they were occasionally seen in the diet of some fish and the medusa Chrysaora. This scyphomedusan was reported t o be an important predator by Miller (1974) in the Pamlico River Estuary, North Carolina. Greve (1 972) reported the results of numerous encounters between Pleurobrachia and potential predators. These included the annelid worm Tomopteris, fish larvae, a hermit crab, a crab and a shrimp. On being contacted by medusae, Pleurobrachia discharged mucus which decreased the numbers of successful catches making them more easily detached. Greve (1972) also described experiments which suggested that

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newly-hatched Pleurobrachia were susceptible to having their tentacles tangled in the appendages of copepods which could result in the " destruction " of the ctenophore, or a t least, damage to its tentacles. He considered (personal communication) that large copepods such as Calanus could exert a drastic effect on larval ctenophore populations in this way. The work of Greve was done in small dishes where conditions were far from natural. Our observations in 30 1. aquaria, in which copepod nauplii were provided as food, suggest that mortality of the newly-hatched larvae of Mnemiopsis is very high a t densities of Acartia of 100/1., but a t lO/l., there is no effect. The lower density is rarely exceeded for total zooplankton in a 200 pm mesh net in Biscayne Bay from whence the ctenophore and copepods are derived. Colder waters are more likely to have higher densities a t peak production periods. The situation is made more complicated by the fact that a t intermediate copepod densities some mortality was observed, but those ctenophores which survived through the first 3-4 days became large enough to make use of the copepods and grow much more rapidly than the control animals. The analysis of this type of dynamic interaction of prey and predator requires further study. Fish have been reported a t various times as predators of Ctenophores, the most recent and quantitative account being provided by Oviatt and Kremer (1977). These authors reviewed a variety of reports concerning predation by the ocean sun fish, bluefin tuna, cod, sardine and flying fish. They reported that in Narragansett Bay (Rhode Island), the butterfish (Peprilus) could consume enough Mnemiopsis to support the metabolism of the fish, and account for observed population declines of the ctenophore a t certain times of the year. Hirota (1 974) reported on the infestation of a Pleurobrachict bachei population off California by the endoparasitic larval stages of the amphipod Hyperoche. Harbison et al. (1977) and Harbison et al. (1978) discussed predatory and parasitic associations of hyperiid amphipods with a variety of gelatinous zooplankton, including ctenophores. Some of these could be considered parasitic when small and predatory when large. Flores and Brusca (1975) did not see any permanent damage by two species of Hyperoche on Pleurobrachia, even though amphipods were sometimes present in 100% of the population. Harbison et al. (1978) noted that Oxycephalus can reduce ctenophores and salps to fragments within minutes. A female with young, however, does not feed, but releases the young from her marsupium onto the host, where they commence to feed. These authors have also seen predatory attacks on ctenophores by the heteropods Pterotrachea and Cardiapoda, and the hydromedusa Aequorea.

NUTRITIONAL ECOLOQY O F CTENOPHORES

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COMPOSITION IV. CHEMICAL Ctenophores have long been recognized t o be relatively poor for their size as a food source for other animals on account of their watery body tissue. The percentage of dry material t o live (wet) weight ranged between 3 - & 5 * 0 ~(Cooper, 0 1939 ; Curl, 1962 ; Reeve and Baker, 1975 ; Kremer, 1976a). Most of this dried material is, necessarily, inorganic (ash), the ash-free dry weight (by ignition) being some 20-37% of the dry weight according t o these authors and Hirota (1972). Ash-free and organic dry weight are usually taken to be synonymous terms and the organic carbon content of living tissue comprises about half of this. Curl (1962) gave a value of 21% for Mnemiopsis. Baker (1973) and Reeve and Baker (1975) reported, however, that carbon content in Mnemiopsis mccradyi was only 9% of its ash-free dry weight, which was similar to a value for Pleurobrachia bachei determined by Mullin and Evans (1974) and Kremer (1976a) for Mnemiopsis leidyi. Reeve and Baker (1975) and Mullin and Evans (1974) discussed possible reasons for these discrepancies, and the former agreed with the suggestion of the latter authors that the determination of dry weight was probably a t fault because a substantial fraction of '' bound " water was not driven off a t the temperatures used. This, in turn, led to an overestimation of ash-free dry weight, which was only 12% of that calculated. The percentage of organic carbon of the total " dry )' weight ranges between about 2 4 % for Pleurobrachia and Mnemiopsis (Reeve and Baker, 1975; Mullin and Evans, 1974; Kremer, 1976a; Reeve et al., 1978). Various of these authors determined the nitrogcn and phosphorus contents t o be 0.2-1-3~oand 0-03-0.23~0of the dry weight respectively. Most of these data are summarized in a, table by Krerner (1976a). RATES V. INGESTION Over the past few years feeding rates of cydippid and lobate ctenophores have been measured in the laboratory in order to estimate their effects as predators in the environment. Perhaps the most significant aspect of their feeding behavior is that over an extremely wide range of prey concentration their ingestion rate is proportional t o food concentration. This was first demonstrated by Bishop (1967) for Mnemiopsis leidyi over a copepod food concentration range of 1053600/1., and subsequently by Miller (1970) and Kremer (in press) for the same species over ranges of 4-44 and 1-100 food organisms/l. respectively. Reeve et al. (1978) found this relationship t o hold

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over the entire tested range of 1-3 000 copepods/l. for two sizes of adults of Mnemiopsis mccradyi. For three sizes of larval animals of this species and for Pleurobrachia bachei adults (i.e. both tentaculate) on the other hand, ingestion rate appeared t o level off above 2OOjl. becoming independent of food concentration. Rowe (1971) also showed levelling off of ingestion rate for P. bachei above 400/1., although, unlike all the other studies, his animals were offered nauplii rather than adult copepods. At the highest laboratory food concentrations, the term (‘ingestion” is a misnomer for lobate forms which, as explained in an earlier section, reject mucus-entangled boli of copepods as they collect them a t rates faster than can be ingested and digested. The ecological consequences are similar, however, in as much as the food organisms are destroyed ”. Unlike many other zooplankton herbivores and carnivores, therefore, ctenophores do not appear to encounter in nature a critical ” food concentration a t which their ingestion rate becomes constant and independent of further food concentration increases. Their feeding behavior is not, however, completely automatic. Walter (1976) showed that starved Mnemiopsis ingested copepods at a higher initial rate and levelled off after a few hours t o a rate characteristic of animals which had not been starved. I n animals which had been starved from 1 to 5 days, higher ingestion rates were maintained for longer periods as a function of length of prior starvation. Also, as noted above, feeding activity in terms of tentacle and lobe extension, as well as swimming activity, are also correlated with feeding history. The relationship between food concentration and ingestion rate implies that the daily ration of ctenophores (i.e. the daily amount of organic carbon they ingest as a ratio of the body organic carbon weight) can become very large. Hirota (1972) indicated that this ratio rarely exceeded 40%, but his assumption that Pleurobrachia had a carbon content of 50% of its dry weight was in error (see above). Corrected for 2% carbon, this value would become 1000%. Kremer (in press) calculated that at a food concentration of 100 copepods/l., the ratio would be 115%. Walter (1976) computed the ratio for Mnemiopsis on the same food source as ranging from 10% to nearly 10 000% over a food range between 10 and 3 000 copepods/l., with values comparable to those of Kremer at about lOO/l. She computed a ration of 67 yo based on maximum estimates of zooplankton biomass from the natural environment. Several workers expressed the feeding activity of ctenophores in terms of volume of water swept clear ” per unit of time following ((

((

((


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numerical methods developed for copepods feeding herbivorously (e.g. Gauld, 1951). Walter (1976) reported that clearance rates of Mnemiopsis mccradyi between 5 and 70 mm total length (2-1 000 mg dry weight) ranged from 1 t o 74 l./animal/day a t 26°C. These values are some 2 times greater than those obtained by Kremer (in press) for M . leidyi between 20 and 25°C. Both workers found that weight specific clearance rates fell with size increase. Miller (1970) whose clearance rates for the latter species were intermediate, saw no such weight specific decrease, although his data were very variable and may, as Kremer suggested, simply have obscured such a n expected trend. VI. DIGESTION There are very few observations on the process of digestion in ctenophores. Kamshilov (1960b) observed the process in Beroe, which required three hours or more to completely digest Bolinopsis. He also noted that in situations where there was food in the gut of the ingested Bolinopsis, such as a copepod or fish larva, it was subsequently egested more or less intact. On the other hand, in one case in which the copepod had already been digested by the Bolinopsis to the point where it ruptured, Beroe completed the process, only egesting the chitinous exoskeleton. It appeared that in this case the Beroe was able to complete the process once the non-ctenophore food had been partially digested. He observed digested material to pass out of both the mouth and anal pores. Swanberg (1 974) reported a digestion time for Beroe feeding on Bolinopsis of 4.5 h (average). Anderson (1974) measured a digestion time of 2.4 h for Pleurobrachia feeding on copepods. Walter (1976) and Reeve et al. (1978) made quantitative observations on the digestive efficiency of Mnemiopsis feeding on adult copepods (Acartia). Ctenophores were allowed to feed for one hour a t various food concentrations, then removed t o clean water, and all material subsequently egested was collected for analysis. Up to a concentration of 100 copepods/l., digestion efficiency was about 74% on a copepod dry weight basis, which is comparable t o the digestive efficiency of chaetognaths and herbivorous zooplankton (see review in Cosper and Reeve, 1975). Beyond this concentration up to 1 000/1. values became much more erratic, yielding negative figures in some cases. This was because animals egested food boli without digestion which also included ctenophore-produced mucus. Average digestive efficiency at the highest food concentration was 20%,

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although values ranged widely. Unless food was rapidly egested, gut residence time beyond the initial hour during which feeding was permitted was fairly constant and not dependent on food quantity, and ranged between 29 to 34 hours. Fecal material always appeared to be evacuated through the mouth. The fecal material of ctenophores does not form a distinct pellet as does that of many other zooplankton (Reeve, Cosper and Walter, 1975), but is mostly loosely bound by mucus, and sinks to the bottom of the experimental container.

VII. RESPIRATION AND EXCRETION Several workers have made estimates of oxygen consumption and nitrogen excretion rates in ctenophores, usually in an effort to use these data to interpret the ecological interrelationships of ctenophores to the other organisms in the water column. Oxygen consumption measurements for Pleurobrachia were made by Lazareva (196l), Rajagopal (1963), Hirota (1972), Biggs (1977) and Reeve et al. (1978), and for Mnemiopsis by Williams and Baptist (1966), Miller (1970), Miller and Williams (1972), Baker (1973) andKremer (1978). Respiration increased with temperature in Mnemiopsis over a range of 4-29°C with a Qlo ranging from 7.1-1.1 (Miller, 1970), 21-31°C with a mean Qlo of 1.9 (Baker, 1973) and 10-26°C with a Ql0 up to 3.7 (Kremer, 1978). Williams and Baptist (1966) cited a value of 2.3. Kremer (1978) noted that her animals were probably more sensitive to temperature change at higher temperatures compared to those of Miller (1970), or Baker (1973), because her animals were at the extreme upper limit of their range. Baker (1973) noted that at comparable temperatures, the data of Miller (1970) were twice as high as those she obtained (on a pgO,/mg ash-free dry weight basis), which she suggested could have been attributed to the very low salinities employed by Miller (1970), which are known to result in higher energy expenditure in some marine animals (Prosser and Brown, 1961). Both Miller (1970) and Baker (1973) found that weight specific oxygen consumption decreased with increasing ctenophore size, but Williams and Baptist (1966), Hirota (1972) and Kremer (1978) reported that the reverse was the case. Kremer (1975a) noted that the latter situation was unusual and suggested it might reflect the “extremely simple nature” of ctenophores. Reeve, et al., (1978) confirmed the results of Hirota (1972) using the same species (Pleurobrachia bachei) and temperature (13°C). Information on excretion rates is minimal. Apart from isolated values (e.g. Jawed, 1973) measurements were made on a range of sizes


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of animals by Kremer (1975b, 1978) for Mnemiopsis and Reeve et al., (1978) for Pleurobrachia. Kremer measured ammonia, total dissolved nitrogen, urea, nitrite, nitrate, phosphorus and dissolved organic carbon. Urea, nitrite and nitrate did not constitute a signifi: cant proportion of excreted material but dissolved organic nitrogen was 46% of the total, the balance of which was in the form of ammonia. Kremer (1976a)reviewed previous literature which indicated that large percentages of excreted dissolved organic nitrogen are relatively rare for zooplankton. Reeve, et al., (1978) found 0: N ratios on the basis of ammonia nitrogen of about 15 for Pleurobrachia bachei, which was the same as Kremer reported for ivnemiopsis leidyi. They did not measure total organic nitrogen. Kremer (1976s) reported that ammonia excretion was independent of size on a weight specific basis. I n experiments with Pleurobrachia at low food concentrations they found that 45% of the nitrogen ingested was excreted. This fraction dropped to 16% at high food concentrations because a greater proportion of the food was unassimilated, but presumably quickly mineralized from fecal material.

VIII. GROWTHRATE Comparison of length measurements between workers is complicated because for Pleurobrachia (and larval lobate forms) body diameter may be measured in either the equatorial (Hirota, 1972) or polar plane (Reeve and Walter, 1976). For lobate adults, length may include the lobes (Baker and Reeve, 1974; Walter, 1976) or not (Greve, 1970). Comparison measurements were made for Pleurobrachia bachei (Walter, unpublished). The equatorial diameter was 80% of the polar diameter in adults. There are relatively few measurements of growth rate for ctenophores in the laboratory. Of the 4 genera commonly maintained in the laboratory, Bolinopsis is particularly sensitive to physical damage, its lobes frequently atrophying and growing back again. Our (unpublished) data for Bolinopsis growth rate is very similar to that of Greve (1970). Over a period of about 3 days his fastest and slowest growing animal increased in length from 4 mm to 40 and 8 mm respectively a t 16°C. I n our case, starting with a newly-hatched population, animal sizes ranged between 6-25 mm after 36 days at 13°C. Such wide variation is almost certainly an artifact of culture condition. Growth rate, when expressed as the logarithm of biomass increase (e.g. volume, dry weight, organic carbon) as a, function of time, can frequently be represented by a straight line over some or most of the A.M.B.-15

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life history of invertebrates (Winberg, 1971). Growth, in this case, takes place at a constant relative rate and is exponentialIy related to time. This coefficient of exponential growth (k) can be used as a basis of comparison between different animals. Hirota (1972) presented growth rate data for Pleurobrachia for which he subsequently (1974) computed growth coefficients. At 15"C, animals reached a maximum size of 14 mm diameter (population mean) after 80 days. At 20°C they reached a diameter of 6 mm in 35-40 days, which was some 1&15 days faster than a t 15°C. His animals grew slowly at first up to 2 mm (40 days), then rapidly up to 6.5 mm and then more slowly again. Growth coefficient ranges over these three periods were 0.12-0.17, 0.21-0.47 and 0-OPO-17 respectively. Hirota (1972) also obtained comparable growth rates in large (70 m3) tanks a t lower food concentrations. Reeve and Walter (1976), working with the same species, obtained much higher mean growth rates, although the same 3 phases were evident. The first phase (up to 2.5 mm) required only 5 days following which, up to the 20th day (6.0 mm) animals increased their biomass about 50% per day (k = 0.47), then grew more slowly up to about the 40th day (k = 0.09) after which they levelled off at about 10 mm. Growth rates were somewhat faster at 20"C, the maximum coefficient being 0-76 and final size being reached in 37 days. The final size of our laboratory populations of Pleurobrachia was considerably smaller than that reported by Hirota (1972) or Greve (1972). Greve, whose species was P. pileus, kindly identified our species as P. bachei, which was the same as that referred to by Hirota. Reeve and Baker (1975) reported on laboratory growth rates of Mnemiopsis mccradyi a t 21, 26 and 31°C. The intermediate temperature produced faster growth rates, and growth was divided into three phases of decreasing exponential growth rate from hatching. At 26°C Mnemiopsis reached 30 mm length in about 10 days (coefficient 0.78) by which time they had become completely lobate. Growth slowed over the next 10 days (k = 0-23, up to 40 mm) and again from 20 to 40 days (k = 0.07, up to 68 mm). The duration of these experiments did not permit animals to reach a final size, but we have had animals reach a total length of over 90 mm in the laboratory. It is worth noting that our highest growth rates recorded for young animals involved a daily doubling of biomass. They approach the extraordinary growth rates reported by Heron (1972) for population increase of the salp Thalia dernocratica, which he stated at that time to be " considerably higher than any other multicellular animals yet measured ".


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Miller (1970) attempted some growth rate studies with Mnenziopsis teidyi, although he considered conditions not very satisfactory because at 20°C his animals ceased growing above an average volume of 11 ml (about 40 mm long). He used a range of temperatures up to 20"C, at which fastest growth rates were observed (k = 0.25). I n order to compare other growth rate data in the literature which was expressed only in terms of length, we have estimated rough growth coefficients using the weightldiameter ratio of Hirota (1972). The assumption is made that Beroe and Bolinopsis (without lobes) are approximately spherical. Greve (1970) reported the maximum growth rate for Bolinopsis was 10-40 mm in 20 days at 16°C (k = 0.2). He reported similar growth rates for PEeurobrachia (1970, 1972) and a somewhat faster rate for Beroe (1970) which increased from 5-15 mm in 8 days (k = 0-4). Kamshilov (1960a) made several measurements of length increase in Beroe in which k ranged from 0.02-0-04 (e.g. 15-30 mm in 28 days). Several authors have reported the ability of ctenophores to undergo periods of food shortage or absence, by utilizing their own body tissue for their metabolic requirements and so gradually shrink in size (e.g. Kamshilov, 1960b;Greve, 1972; Kremer, 1976b; Walter, 1976). Kremer (197623) found that Mnemiopsis lost weight at a copepod concentration of 1011. and gained weight a t 100/1. Reeve, Walter and Ikeda (1978) computed growth coefficients for Mnemiopsis over a food concentration range from 0 to 350/1. and showed that growth decreased to zero at l/l., below which animals lost weight.

IX. FECUNDITY Pianka (1974) summarized information on the considerable regenerative powers of ctenophores. This is not known to be used as a means of reproduction in planktonic forms, but Greve (1970) noted feeding patterns in both the young and adult beroids where the predator would not consume completely the prey ctenophore, but detach itself, which would permit the prey animal to regenerate its missing parts. Coonfield (1938), for instance, showed that Mnemiopsis would completely regenerate new individuals when cut into quarters, and often much smaller fractions also regenerated. It was noted earlier that a form of asexual budding was common amongst some of the Platyctenea. All planktonic ctenophores are simultaneous hermaphrodites and capable of self fertilization, and thus viable offspring can be produced from a single adult, as we and others (e.g. Pianka, 1974;

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Hirota, 1973) have regularly observed. Planktonic ctenophores can produce offspring long before they reach their upper limit of size. Pianka (1974) reviewed cases of paedogenesis (sexual maturity of larvae and juveniles) and dissogony (sexual maturity of larvae followed by regression of gonads and subsequent rematuring of adults). Hirota (1972) documented an individual (Pleurobrachia bachei)which produced a total of 76 offspring as a larva between the 25th and 47th day and resumed egg-laying on the 69th day reaching a maximum of almost 1000 eggslday. Reeve et al., (1978) saw egg production begin at about 4-6 mm, which although a much shorter period from hatching than Hirota recorded, was at a later developmental stage. No indications of dissogony were apparent. Pianka (1974) and Greve (1970) also noted a similar size for the initiation of spawning in Pleurobrachia with no earlier larval maturity. Although dissogony had been mentioned for Bolinopsis in early reports, Pianka (4.v.) did not see spawning until animals had become lobate a t 10 mm, and it has not been reported for Mnemiopsis. Kremer (1975a) and Baker and Reeve (1974) investigated fecundity of Mnemiopsis by collecting wild individuals of various ages and leaving them in the laboratory overnight, after which any eggs and larvae produced were counted. I n both cases egg production was a function of size, the largest animals producing up to 9 990 (Baker and Reeve) and 14 000 eggs (Kremer). Baker and Reeve (1974) followed six individuals from newly-hatched larvae for 23 days. They started to produce eggs 13 days after hatching a t 26 mm total length and the maximum total production over the period was over 12 000 eggs each. There is a wide range of numbers of eggs produced for any given size of ctenophore and food supply is no doubt a very important controlling factor. Kremer (1975a)and ourselves have found differences in fecundity in wild animals brought into the laboratory at different times of the year which she attributed to differences in food supply. The provision of food is well known to be one of the ways to stimulate egg production of ctenophores in the laboratory (Greve, 1970 ; Baker, 1973). Reeve et al., (1978) fed young Pleurobrachia at two food concentrations (10 and 100 copepods/l.) over 6 days. They grew from 5-3 mm (polar diameter) to 7.3 mm and 9.6 mm respectively, and produced a total of 7 and 186 eggs/animal. The dry weight of each egg was 0.35 pg (0.02 pgC).

X. GROWTH EFFICIENCY Hirota (1972) estimated the growth efficiency of Pleurobrachia bachei as 60%. When we first started making similar computations

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from experimental data we arrived at values well in excess of loo%, on a dry weight basis. This stimulated a, search into problems of measuring the biomass (organic tissue weight) of ctenophores (Reeve and Baker, 1975), and the conclusion that organic carbon was only about 2% of the dry weight, compared to 40-45% in the food organisms (copepods). On a carbon basis growth efficiencies varied from 7% a t the lowest food concentration ( 3 copepods/l.) (Reeve et al., 1978) down to 2% a t the highest (300/1.). I n similar measurements made on Pleurobrachia at two food concentrations (10 and 100 copepods/l.) efficiency was 11 and 3% respectively. The 60% value of Hirota (1972) was recomputed to be about 9%. These values are very low compared to values obtained for other zooplankton (reviewed by Reeve, 1970). Even a t food concentrations where digestive efficiency is known to be consistently high (see above), growth efficiency is low, although animals grow as fast as zooplankton which have high growth efficiencies. An explanation of this apparent paradox appears to be in the relatively high energy requirements of Pleurobrachia. Reeve et al. (1978) calculated that these ctenophores required about 63% of their food intake to satisfy their metabolic activities, at food concentrations where digestive efficiency is high. The authors pointed out that the organic carbon content of a ctenophore whose dry weight is the same as that of a copepod would only be 5% of that of the copepod, i.e. the amount of living material generating the energy to move the body bulk of the ctenophore in its environment is, similarly, a tiny proportion compared to the copepod. This great disparity in the ratios suggests why a greater proportion of the ingested food must be directed to energy demands. XI. SEASONAL VARIATIONS IN CTENOPHORE POPULATIONS Fraser (1970), after many years of experience of the seasonal variations of ctenophores and other zooplankton in temperate waters, agreed with the remarks of Kramp (1913) that it is difficult to make reliable predictions of the seasonal appearance of any species, and often their appearance in great numbers seems fortuitous, with no obvious correlation with temperature, season or depth. They can occur throughout the entire year in great numbers (McIntosh, 1926) off the east coast of Scotland, reoccur in large numbers with regularity throughout P 5 months of the summer in Saanich Inlet, British Columbia (personal observations), appear once or twice at particular times of the year, especially later summer and autumn (Fraser, 1970), or sometimes pass through an entire year without appearing in bloom

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proportions (Kramp, 1913, for the English Channel ; our observations in south Florida inshore waters). Many references to ctenophore abundance quote numbers only, often not related to water volume collected, using a variety of different collection methods and meshes and related to differently-sized species. Even biomass, therefore, cannot be compared very closely. Production rates have been determined rarely. Reeve and Baker (1975) estimated the production of Mnemiopsis mccradyi in Biscayne Bay, Florida to be 61-123 mgC/m3 annually, with a daily production : biomass ratio of 0.12. The Biscayne Bay water column is very shallow (3 m) so this translates to a value of 369 mgC/m2/year. Hirota (1974) computed the production of Pleurobrachia bachei off California in terms of ash-free dry weight. When converted to carbon using a factor of 8.7% carbon in ash-free dry weight (Reeve and Baker, 1975) annual production was 472 mgC/m2/year with a production: biomass ratio of 0.02. Water column depth off southern California was in excess of 40 m, however, so that on a m3 basis the warmer-water Biscayne Bay ctenophore population had a much higher production rate, as might be inferred by their much faster growth rates noted in an earlier section. Kremer (1976b) developed a computer production model (discussed below). I n their experiments, Reeve and Baker (1975) maintained an abundant supply of food, which they noted was no less artificial than trying to maintain a uniform environmental average level of food, because it is highly likely that food is distributed in patches, and animals may be exposed to concentrations varying by several orders of magnitude over 24 hours. The bulk of production took place over a short period of the year in both studies, and it could be argued that ctenophores were not likely to be very food limited over this period of rapid population growth rate. Most recent studies which have related population changes of ctenophores to observations made in the laboratory have been designed to estimate the predatory effect of ctenophores on the rest of the plankton. Reeve and Baker (1975) and Hirota (1974) did this by relating ctenophore production to estimates of herbivore zooplankton production. For Biscayne Bay, Reeve and Baker estimated the ctenophore production as about 20% of the copepod production, and the production of another major carnivore, the chaetognath Sagitta hispida Conant, as 12% of the copepod production. Assuming a 32% conversion efficiency from copepod to carnivore biomass, two predators would account for all the copepod production of the bay. Hirota (1974) computed a transfer efficiency of 11% between various levels of the food chain including zooplankton to Pleurobrachia.


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Williams and Baptist (1966) reported (in abstract) that on the basis of respiration measurements of Mnemiopsis leidyi from estuaries around Beaufort, North Carolina, a large animal required all the copepods in 4-100/1. of water. Bishop (1967) directly measured feeding rates of the same species and related them to copepod abundance in the Patuxent River, Maryland. He estimated that 52% of the mortality of the dominant copepod, Acartia tonsa Dana, could be accounted for by predation. Burrell (1968) and Burrell and Van Engel (1976) also performed feeding experiments and estimated that M . Zeidyi was the major predator on zooplankton in the York River estuary, Virginia, accounting for 73% of the total predation exerted by a group of predators including medusae, chaetognaths and fish. He also noted that when Beroe made an appearance, Mnemiopsis populations were eliminated wherever it occurred. Populations of Pleurobrachia and Bolinopsis also decreased dramatically, according to the data of Anderson (1974), when Beroe increased in numbers in St. Margaret's Bay. As already noted, the first two species did not appear to be in direct competition because their gut contents showed that they relied on different components of the copepod population. Between them, they removed 40% of the total accounted for by the large Sagitta population. Miller (1970) used his estimates of ctenophore water clearance rate in the laboratory to compute total water clearance rates for the ctenophore population of the Pamlico River, North Carolina. When ctenophores were at their peak biomass they removed up to 48% of the copepod biomass, i.e. their daily total population clearance rate was 480 l./m3. Most of the season, ctenophore populations were much lower, yielding computed summer and winter mean clearance rates of 5.4 and 0.7% of the copepod population respectively. Since Miller also measured respiration and growth rates, he computed total population respiration and growth requirements in energy units and suggested that these requirements were in excess of food intake, if only copepods were considered as food. Averaged over the year, he estimated that ctenophores could obtain only 23% of their energy requirements from zooplankton. This led him to the suggestion that they must also, of necessity, have to make use of phytoplankton and detrital material present in the water at the same time. Miller and Williams (1972) reinforced this conclusion by taking ctenophore, zooplankton and phytoplankton population data from the Patuxent estuary from Herman et al. (1968) and respiration data from Williams and Baptist (1966), from which they concluded that during most of the season there was not enough zooplankton to satisfy even

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the respiratory needs of both the ctenophore and jellyfish population present. Heinle (1974) pointed out a substantial error in this treatment because ctenophore biomass had been incorrectly reported by Herman et al. to be some three orders of magnitude greater than really occurred. This meant that in some cases there would be enough zooplankton to account for the energetic needs of ctenophores, although he suggested that ctenophores could probably not rely entirely on other zooplankton for their food. Kremer (in press) also made calculations based on laboratory feeding rates and environmental biomass, and reached a similar conclusion as Miller (1970) regarding the fraction of the copepod standing stock removed. A t the time of their greatest abundance, ctenophores were estimated to achieve a maximum of 30% removal rate in a day. Kremer went on to calculate more precisely the effects of the ctenophores on the rest of the zooplankton by estimating the production capacity of the copepods rather than simply their standing stock. She estimated that ctenophores might be responsible for between 20 and 50% of the entire copepod mortality over the summer, but urged caution in generalizing from such computations. A major problem was that often the sequence of copepod decline did not correspond to maximum ctenophore predation pressure, suggesting that there could be other major unknown forces at work affecting the copepod populations independently of ctenophore predation. Ctenophores must recycle a significant fraction of their ingested nitrogen either though excretion of dissolved metabolic waste products, or, when feeding at very high food concentrations, by releasing either partly digested or dying copepods which subsequently become remineralized by bacterial action. Kremer (197510) calculated that at their population peak, they were responsible for the turnover of as much nitrogen as the rest of the zooplankton population. We have also performed similar calculations (Reeve et al., 1978) to indicate tha.t at the time of peak ctenophore standing stock in Biscayne Bay (from Baker, 1973) they could consume some 10% of the standing stock of copepods per day, although this fraction would be much less during most of the year. Nevertheless, taking the average population production rate estimated by Reeve and Baker (1975) it can be estimated that within seven days copepods would be reduced to only 25% of their original biomass assuming no copepod production over the period. Approximately the same figure would result assuming a high (0.3) daily production to biomass ratio for both populations. The characteristically rapid population increase of ctenophores is so striking that it is tempting to attribute it to migration of already

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28 1

developed populations from elsewhere. Kremer (1976b) used a simple computer model to show that in Narragansett Bay, the fecundity estimates derived in the laboratory could explain the rapid increase from a winter minimum of about 1 animal/lO 000 m3 over 5 orders of magnitude. Reeve et al. (1978) took the data of Baker and Reeve (1974) and Reeve and Baker (1975) for Biscayne Bay using a model similar to that described by Kremer . These computations suggested that the observed ctenophore population biomass increase over 45 days of the major seasonal ctenophore bloom in Biscayne Bay (2.5 orders of magnitude range) would require a production/biomass ratio of less than 0.2 at fecundities observed in the laboratory. Rapid growth rates and high fecundity in ctenophores mean that it is rarely feasible to follow cohorts in the environment and estimate patterns of growth and mortality directly. Por this reason estimates of the kind outlined above, which make use of laboratory data to interpret natural populations, are essential. There have been some attempts, however, to follow populations in situations where the same population is sampled successively, because it is confined in some way. Mullin and Evans (1974) established a phytoplankton/copepod/Plezcrobrachia food chain in a tank of approximately 70 m3 volume. The daily production/biomass ratio of the predators was 0.16. The production of carnivores was 3% of the primary production, which indicated a food chain efficiency greater than 10% between each trophic level. Reeve et aZ. (1976) reported on the populations of zooplankton in transparent closed plastic columns of 68 m3 volume floating at the sea surface to some of which had been added copper. Copepod populations declined throughout the experiment due to the presence of ctenophores aa well as copper, and estimates of the fraction of the observed mortality due to predation were made by computing ctenophore food requirements from their respiratory demands. I n a subsequent experiment, in which amounts of nutrients were varied in four containers (Parsons et al., 1977), ctenophore production was almost doubled in the container receiving most enrichment, compared with that receiving no enrichment, although the percentage of phytoplankton production converted to ctenophore production was much less (1.9 compared to 4.8%). Reeve and Walter (1976) illustrated how such containers could bo biologically manipulated. They described the withdrawal of most of the larger Pleurobrachia by a selective sampling technique which did not disturb the copepod population. Within a week copepods had more than doubled in this container. This provided a clear demonstration of the predatory significance of ctenophore populations at high

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density. The same containers also demonstrated the rapid ability for population increase of ctenophores initially a t very low density. The sudden appearance of a ctenophore bloom, therefore, and its subsequent effect on copepod populations, can be predicted from the observations of populations in the natural environment, estimated by application of laboratory data, and actually observed in a captured population. This does not necessarily imply that the population dynamics of ctenophores can be so readily explained under all circumstances. Kremer (in press) noted that there were often variations in natural populations of ctenophores and copepods which could not be effectively explained by trophic interactions, and this is certainly the case in the example cited by Reeve and Walter (1976). It is unclear, for instance, what caused the progressive mortality of ctenophores in containers in which there were no known predators, or why populations of adult copepods died off very rapidly in the container from which most of the ctenophores had been removed. Reeve and Baker (1975) suggested that in comparing two dissimilar plankton carnivores-ctenophores and chaetognaths-which depended on the same food source in south Florida inshore waters, the conclusion could be drawn that ctenophores needed a higher food density to enable population growth to occur. This could be deduced from the general correlation of absence of ctenophores in regions of low zooplankton biomass where chaetognaths continued t o occur, and their relatively infrequent appearance, compared to chaetognaths, which was associated in a general way with seasons of the highest copepod biomass. Laboratory data indicating their requirements of very high food concentrations for maximum growth rates and their continued capacity to increase ingestion at these high food concentrations also confirm their dependence on food abundance for rapid population increase. Their potential for self-fertilization, extremely high fecundity and rapid growth potential explain how, given good food abundance, their population can ‘(explode ”. They appear to be environmental specialists which can overwhelm the biomass of any competitor under conditions of peak food supply.

XII. CONULUSION Fraser (1962), Kremer (1976a), Greve (personal communication) and ourselves have pointed out that ctenophores should not be considered merely wasteful ‘(dead ends ’’ in the food chain. They may act sometimes to balance the ecosystem by restraining an overabundance

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of copepods from virtually eliminating all phytoplankton from the water column at a time when other more “ useful ” predators are failing to do this. The phytoplankton would also receive a positive stimulation to renewed growth by virtue of the high percentage of ingested nitrogen being returned in a dissolved form back to the water column. It is possible that the result might otherwise be the production of dead copepod biomass which accumulated in the sediments and was lost (at least on a, short time scale) to the water column. XIII. REFERENCES Anderson, E. (1974). Trophic interactions among ctenophores and copepods in St Margaret’s Bay, Nova Scotia. Ph.D. Dissertation, Dalhousie University. Baker, L. D. (1973). Ecology of the ctenophore Mnemiopsis mccradyi Mayer, in Biscayne Bay, Florida. Rosenstiol School of Marine and Atmospheric Science, University of Miami, Technical Report UM-RSMAS-73016. Baker, L. D. and Reeve, M. R. (1974). Laboratory culture of the lobate ctenophore Mnemiopsis mccradyi with notes on feeding and fecundity. Marine Biology, 26, 57-62. Barlow, J. P. (1955). Physical and biological processes determining the distribution of zooplankton in a tidal estuary. Biological Bulletin (Woods Hole), 109, 21 1-225. Bayer, F. M. and Owre, H. B. (1968). “ The Free-Living Lower Invertebrates”. MacrniHan, New York. Bigelow, H. B. (1915). Exploration of the coast water between Nova Scotia and Chesapeake Bay, July and August, 1913, by the U.S. Fisheries Schooner, Grampus. Oceanography and plankton. Bulletin of the Museum of Comparative Zoology at Harvard College, 59, 149-359. Bigelow, H. B. and Leslie, M. (1930). Reconnaissance of the waters and plankton of Monterey Bay, July 1928. Bulletin of the Museum of Comparative Zoology at Harvard College, 70, 429-581. Biggs, D. C. (1977). Respiration and ammonium excretion by open ocean gelatinous zooplankton. Limnology and Oceanography, 22, 1OS117. Bishop, J. W. (1967). Feeding rates of the ctenophore, Mnemiopsis leidyi. Chesapeake Science, 8, 259-264. Bishop, J. W. (1968). A comparative study of feeding rates of tentaculate ctenophores. Ecology, 49, 996-997. Burrell, V. G. (1968). The ecological significance of a ctenophore, Mnemiopsis leidyi (A. Agassiz), in a fish nursery ground. M.A. Thesis, The College of William and Mary, Virginia. Burrell, V. G. and Van Engel, W. A. (1976). Predation by and distribution of a ctenophore, Mnemiopsis leidyi A. Agassiz, in the York River Estuary. Estuarine and Coastal Marine Science, 4, 235-242. Coonfield, B. R. (1938). Symmetry and regulation in Mnemiopsis leidyi, Agassiz. Biological Bulletin (Woods Hole), 72, 299-310. Cooper, L. H. N. (1939). Phosphorus, nitrogen, iron and manganese in marine zooplankton. Journal of the Marine Biological Association of the United Kingdom, 23, 387-390.

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Corner, E. D. S. and Davies A. G. (1971). Plankton as a factor in the nitrogen and phosphorus cycles in the sea. Advances in Marine Biology, 9, 101-204. Cosper, T. C. and Reeve, M. R. (1975). Digestive efficiency of the chaetognath Sagitta hispida Conant. Journal of Experimental Marine Biology and Ecology, 17, 33-38. Cronin, L. E., Daiber, J. C. and Hulbert, E. M. (1962). Qualitative seasonal aspects of zooplankton in the Delaware River Estuary. Chesapeake Science, 3, 63-93. Curl, H. (1962). Standing crops of carbon, nitrogen and phosphorus and transfer between trophic levels, in continental shelf waters south of New York. Rapports et Pr5ckS-Verbaux des Rdunions, Conseil International pour I’Exploration de la Mer, 153, 183-189. Flores,‘M. and Brusca, G. J. (1975). Observations on two species of hyperiid amphipods associated with the ctenophore PZeurobraehia bachei. Bufletin of the Southern California Academy of Sciences, 74, 10-15. Praser, J. H. (1962). The role of ctenophores and salps in zooplankton production and standing crop. Rapports et Procks- Verbaux des Rbunions, Conseil International pour 1’Exploration de la Mer, 153, 121-123. Fraser, J. H. (1970). The ecology of the ctenophore Pleurobrachia pileus in Scottish waters. Journal d u Conseil. Conseil Permanent International pour I’Exploration de la Mer, 33, 149-168. Gauld, D. T. (1951). The grazing rate of planktonic copepods. Journal of the Marine Biological Association of the United Kingdom, 29, 695-706. Greve, W. (1970). Cultivation experiments on North Sea ctenophores. Helgolander Wissenschuftliche Meeresuntersuchungen, 20, 304-3 17. Greve, W. (1971). okologische Untersuchungen an Pleurobrachia pileus. I. Freilanduntersuchungen. Helgolander Wissenschaftliche Meeresuntersuchungen, 22, 303-325. Greve, W. (1972). Okologische Untersuchungen an Pleurobrachia p i l e w . 11. Laboratoriumsuntersuchungen. Helgolander Wissenschaftliche Meeresuntersuchungen, 23, 141-164. Greve, W. (1975a). Verhaltensweisen der Rippenqualle Pleurobrachia pileus (Ctenophora). Institut fur den Wissenschaftlicher Film, Wissenschaftlicher Film C 1181/1975. Greve, W. (1975b). Die Rippenquallen der sudlichen Nordsee und ihre interspezifischen Relationen. Institut fur den Wissenschaftlichen Film, Wissenschaftlicher Film C 1182/1975. Greve, W., Stockner, J. and Fulton, J. (1976). Towards a theory of speciation in Beroe. I n “ Coelenterate Ecology and Behavior”, (G. Mackie, ed.), pp. 251-258. Plenum Publishing Company, New York. Harbison, G. R., Biggs, D. C. and Madin, L. P. (1977). Associations of Amphipoda Hyperiidea with gelatinous zooplankton. 11. Associations with Cnidaria, Ctenophora and Radiolaria. Deep-sea Research, 24, 465-488. Harbison, G. R., Madin, L. P. and Swanberg, N. R. (1978). On the natural history and distribution of oceanic ctenophores. Deep Sea Research, 25, 233-256. Heinle, D. R. (1974). An alternate grazing hypothesis for the Patuxent Estuary. Chesapeake Science, 15, 145-150. Herman, S. S., Mihursky, J. A. and McErlean, A. J. (1968). Zooplankton and environmental characteristics of the Patuxent Estuary. Chesapeake Science, 9, 67-82.


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Heron, A. C. (1972). Population ecology of a colonizing species: the pelagic tunicate Thalia democratica. I. Individual growth rate and generation time. Oecologia, 10, 269-293. Hirota, J . r ( 1972). Laboratory culture and metabolism of the planktonic ctenophore, Pleurobrachia bachei A. Agassiz. I n " Biological Oceanography of the Northern North Pacific Ocean ", (A. Y. Takenouti, editor-in-chief), pp. 465-484. Idemitsu Shoten, Tokyo. Hirota, J. (1973). Quantitative natural history of Pleurobrachia hachei A. Agassiz in La Jolla Bight. Ph.D. Dissertation, Scripps Institution of Oceanography, University of California. Hirota, J. (1974). Quantitative natural history of Pleurohraclhia bachei in La Jolla Bight. United Statea National Marine Fisheries Service Fishery Bulletin, 72, 295-335. Hopkins, T. L. (1966). The plankton of the St. Andrew Bay system, Florida. Publications of the Institute of Marine Science University of Texm, 11, 12-64. Horridge, G. A. (1965). Macrocilia with numerous shafts from the lips of the ctenophore Beroe. Proceedings of the Royal Society of London Biological Sciences, 162, 351-364. Hyrnan, L. (1940). " The Invertebrates : Protozoa Through Ctenophora". McGraw Hill, New York. Jawed, M. (1973). Effects of environmental factors and body size on rates of oxygen consumption in Archaeomysis grebnitzkii and Neomysis awatschensis (Crustacea : Mysidae). Marine Biology, 21, 173-179. Kamshilov, M. M. (1959). Interrelations between organisms and the part they play in evolution. Zhurml Ohschchei Biologii Union of Soviet Socialist Republics, 20, 370-378. Kamshilov, M. M. (1960a). Size of ctenophore Beroe cucumis Fabricius. Doklady Akademii Nauk Union of Soviet Socialist Republics, 131, 957-960. Kamshilov, M. M. (1960b). Feeding of ctenophore Beroe cucumis Fabricius. Doklady Akademii Nauk Union of Soviet Socialist Republics, 130, 1138-1 140. Kramp, P. L. (1913).Medusae, Siphonophora and Ctenophora. Zoology of Iceland, 11, 1-37. Kremer, P. M. (19758). The ecology of the ctenophore, Mnerniopsis leidyi in Narragansett Bay. Ph.D. Dissertation, University of Rhode Island. Kremer, P. M. (1975b). Nitrogen regeneration by the ctenophore Mnemiopsis Eeidyi. I n " Mineral cycling in southeastern ecosystems ", (F. G. Howell, J. B. Gentry and M. M. Smith, eds.), pp. 279-290. United States Energy Research and Development Administr&on Symposium Series, N.T.I.S. NO. CONF-740513. Kremer, P. M. (197th). Excretion and body composition of the ctenophore Mnemiopsis leidyi (A. Agassiz) : comparisons and consequences. I n " Proceedings of the 10th European Symposium on Marine Biology", (G. Persoone and E. Jaspers, eds.), Vol. 2, pp. 351-362. Universa Press, Wetteren, Belgium. Kremer, P. M. (197613). Population dynamics and ecological energetics of a pulsed zooplankton predator, the ctenophore Mnemiopsis leidyi. I n " Estuarine processes ", (M. L. Wiley, ed.), Vol. 1, pp. 197-218. Academic Press, New York. Kremer, P. M. (1978). Respiration and excretion by the ctenophore Mnemiop.& leidyi. Mariwe Biology, 44, 43-50.

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Kremer, P. M. (In press). Predation by the ctenophore Mnemiopsis leidyi in Narragansett Bay. Chesapeake Science. Lazareva, L. P. (1961). Absorption of oxygen by the ctenophore Pleurobrachia pileus 0. F. Miiller of different sizes in relation to the temperature and salinity of the environment. Trudy Karadahs’koyi Biolohichnoyi Stccntsiyi, 17, 85-96. Lebour, M. V. (1922). The food of planktonic organisms. Journal of the Marine Biological Association of the United Kingdom, 12, 644-677. Lebour, M. V. (1923). The food of planktonic organisms. 11.Journal of the Marine Biological Association of the United Kingdom, 13, 70-92. Main, R. J. (1928). Observation of the feeding mechanism of the ctenophore, Mnemiopsis leidyi. Biological Bulletin (Woods Hole), 55, 69-78. Manteufel, B. P. (1941). Plankton and herring in the Barents Sea. Trudy Polyarnyi Nauchno-Issledovatel’skiiI Proektnyi Institut Morskogo Rybnogo Khozyaistwa I OkeanograJi of Union of Soviet Socialist Republics, 7 , 125-218. Marshall, S. M. (1973). Respiration and feeding in copepods. Advances i n Marine Biology, 11, 57-120. Mayer, A. G. (1912). Ctenophores of the Atlantic coast of North America. Publications of the Carnegie Institution of Washington, 162, 1-58. McIntosh, W. C. (1926). Additions to the marine fauna of St. Andrews since 1874. Annals and Magazine of Natural Hhtory, Series 9, 18, 241-266. Miller, R. J. (1970). Distribution and energetics of an estuarine population of the ctenophore, Mnemiopsis leidyi. Ph.D. Dissertation, North Carolina State University, Raleigh. Miller, R. J. (1974). Distribution and biomass of an estuarine ctenophoro population, Mnemiopsis leidyi (A. Agassiz). Chesapeake Science, 15, 1-8. Miller, R. J. and Williams, R. B. (1972). Energy requirements and food supplies of ctenophores and jellyfish in the Patuxent River Estuary. Chesapeake Science, 13, 328-331. Mullin, M. M. and Evans, P. M. (1974). The use of a deep tank in plankton ecology. 11. Efficiency of a planktonic food chain. fimnology and Oceanography, 19, 902-911. Nagabhushanam, A. K. (1959). Feeding of a ctenophore, Bolinopsis infundibuluna (0.F. Miiller). Nature, London, 184, 829. Nelson, T. C. (1925). On the occurrence and food habits of ctenophores in New Jersey inland coastal waters. Biological Bulletin (Woods Hole), 48, 92-1 11. Oviatt, C. M. and Kremer, P. M. (1977). Predation on the ctenophore Mnemiopsis leidyi, by butterfish, Peprilus tricanthus, in Narragansett Bay, Rhode Island. Chesapeake Science, 18, 236-240. Parsons, T. R., von Brockel, K., Koeller, P., Reeve, M. R. and Holm-Hansen, 0. (1977). The distribution of organic carbon in a marine planktonic food web following nutrient enrichment. Journal of Experimental Marine Biology and Ecology, 26, 235-247. Pianka, H. D. (1974). Ctenophora. I n “ Reproduction of Marine Invertebrates ”, (A. C. Giese and J. S. Pearse, eds.), Vol. I, pp. 201-265. Academic Press, New York. Prosser, C. L. and Brown, F. A. (1961). “ Comparative Animal Physiology”. W. B. Saunders Company, Philadelphia. Rajagopal, P. K. (1963). Note on the oxygen uptake of the ctenophore, Pleurobrmhia globosa, Current Science, 32, 319-320.

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Ralph, P. M. and Kaberry, C. (1950). New Zealand coelenterates. Ctenophores from Cook Strait. Zoology Publications from Victoria University of Wellington, 3, 11 PP. Reeve, M. R. (1970). The biology of Chaetognatlia. I. Quantitativo aspects of growth and egg production in Sagitta hkpida. I n “ Marine Food Chains”, (J.H. Steele, ed.), pp. 168-189. Oliver and Boyd, Edinburgh. Reeve, M. R. and Baker, L. D. (1975). Production of two planktonic carnivores (chaetognath and ctenophore) in south Florida inshore waters. United States National Marine Fisheries Service Pishery Bulletin, 73, 238-248. Reeve, M. R. and Walter, M. A. (1976). A large-scale experiment on the growth and predation potential of ctenopliore populations. I n “ Coelenterate Ecology and Behavior ”,(G. Maclrie, ed.), pp. 187-199. Plenum Publishing Company, New York. Reeve, M. R., Cosper, T. C. and Walter, M. A, (1975). Visual observations on the process of digestion and the production of faecal pellets in t h e chaetognath Sagitb hispida Conant. Journal of Experimental Marine Biology and Ecology, 17, 39-46. Reeve, M. R., Grice, G. D., Gibson, V. R., Walter, M. A., Darcy, K. and Ikeda. T. (1976). A controlled environmental pollution experiment (CEPEX) and its usefulness in the study of larger marine zooplankton under toxic stress. .77~ “ Effects of Pollutants on Aquatic Organisms ”, (A. P. Lockwood, ed.), pp. 145-162. Cambridge University Press. Reeve, M. R., Walter, M. A. and Ikeda, T. (1978). Laboratory studies of ingestion and food utilization in lobate and tentaculate ctenophores. Limnology and Oceanography, 23, 740-751. Rowe, M. D. (1971). Some aspects of the feeding behavior of the ctenophore Pleurobrachia pileus. M.S. Thesis, University of Hawaii. Russell, F. S. (1931). The study of copepods as a factor in oceanic economy. Proceedings of 5th Pacific Scientific Congress, 2023-2032. Russell, F. S. (1935). The seasonal abundance and distribution of the pelagic young of teleostean fishes caught in the ring-trawl in offshore waters in the Plymouth area. Part 11.Journal of the Marine Biological Association of the United Kingdom, 20, 147-180. Scott, A. (1913). The mackerel fishery off Walney in 1913. Report of the Lancashire Sealfisheries Laboratories, 22, 19-25. Swanberg, N. (1974). The feeding behavior of Beroe ovab. Marine Biology, 24, 69-76. Walter, M. A. (1976). Quantitative observations on the nutritional ecology of ctenophores with special reference to Mnemiopsis mccradyi. M.S. Thesis, University of Miami. Weill, R. (1935). Le fonctionnement des colloblastes. Comptes RendzLs de E’Academie des Sciences Paris, 201, 850-852. Williams, R. B. and Baptist, J. P. (1966). Physiology of Mnemiopsis in relation to its role as a predator. Association of Southeastern Biologkts Bulletin, 13, 48-49. Winberg, G. G. (1971). “ Methods for the Estimation of Production of Aquatic Animals Academic Press, New York, London.

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Adv. mar. B i d , Vol. 15, 1978, pp, 289-380.

POLLUTION STUDIES WITH MARINE PLANKTON PART I .

PETROLEUM HYDROCARBONS AND RELATED COMPOUNDS

E. D. S . CORNER The Laboratory, Marine Biological Association, Plymouth, England I. Introduction

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Fate of Hydrocarbons in Zooplankton A. Uptake and Release .. . . .. B. Quantitative importance of the Dietary Pathway C. Long-term Exposure Experiments D. Metabolism .. .. .. E. Release of Hydrocarbons in Faecal Pellets .

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I. INTRODUCTION Marine organisms, including plankton, having been exposed to petroleum hydrocarbons released from submarine seeps throughout geological time, are likely to have evolved physiological and biochemical mechanisms allowing them to adapt to the presence of small quantities of these compounds in their natural environment. Nevertheless, there is considerable current interest in understanding what might happen to planktonic organisms exposed to the additional and localized inputs of hydrocarbons and related compounds that result from accidental spillages arising from relatively recent industrial activities such as the off-shore production and transport of crude oil. Accordingly, consequent upon incidents such as the wrecking of the tanker " Torrey Canyon a vast and widely dispersed literature has arisen during the past ten years dealing with the effects of petroleum hydrocarbons on numerous marine organisms. The publications on plankton considered in the present review, most of which refer to laboratory studies, are discussed in the context of a simplified food-chain model that begins with sea water and proceeds through phytoplankton to zooplankton. Although such a frame-work serves to carry the main theme of the treatment, several additional but relevant topics have had to be included. For example, in dealing with hydrocarbons in sea water attention has had to be given to matters such as their spatial distribution and the relative amounts in solution and in particulate form. Again, in discussing the levels and types of hydrocarbons in plankton it has been necessary to consider compounds of recent biogenic origin, some of which can also occur in crude oil. Furthermore, as certain studies with zooplankton have shown that the animals do not exclusively accumulate hydrocarbons from phytoplankton diets, work is also described that deals with the direct uptake of these compounds from solution in sea water. Finally, although the simplified food-chain model is not extended to include fish and benthic animals, consideration is given to factors affecting the retention of hydrocarbons by zooplankton, particularly copepods, which is of key importance in the transfer of these compounds to fish ; as well as to the release of hydrocarbons in faecal pellets, a possible means by which such compounds originally present in the euphotic zone could be eventually transferred to animals that dwell in sediments. '))

11. HYDROCARBON LEVELSIN SEAWATER When studying the accumulation and fate of hydrocarbons in plankton, and the possible effects of these compounds on the organisms,

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it is necessary to bear in mind the levels of hydrocarbons that plankton normally encounter in various sea areas. Accordingly, a brief review of the available data is attempted by way of introducing the more detailed treatment of studies with plankton that are dealt with in later sections. Although numerous attempts have been made to ascertain the levels and types of hydrocarbons present in sea water under a variety of conditions, the methods used (reviewed by Farrington and Meyer, 1975) have usually provided data for only a particular fraction of the various kinds of hydrocarbons present. More comprehensive analyses have occasionally been made (Barbier, Joly, Saliot and Tourres, 1973; Brown, Searl, Elliott, Phillips, Brandon and Monaghan, 1973), but generally the data still refer to groups of hydrocarbons (e.g. monocyclic aromatics) rather than to individual compounds. Data for individual hydrocarbons do exist, but most deal with n-alkanes and the iso-alkanes pristane and phytane (see Figs 2 and 3). A. Studies primarily concerned with alkanes Swinnerton and Linnenbom (1967) detected the simplest n-alkane, methane, at concentrations ranging from 0.025 to 0.283 pg/l at various depths in sampling areas in the Gulf of Mexico and 0.047-0.060 pgll in the North Atlantic. Frank, Sackett, Hall and Fredericks (1970) found somewhat higher concentrations of methane, 0-06-1.25 pg/1, near oil seeps in the Gulf of Mexico: ethane and propane were also present, but at much lower levels. It is known from the work of Blumer (1970) that dissolved organic compounds in coastal waters include a variety of hydrocarbons. Thus, in a qualitative study he identified n-alkanes from C,, to C,, with maximum concentration at C,,-C,, : the compounds included those with odd and others with even numbers of carbon atoms in roughly equal amounts, a distribution different from that in recent marine sediments (where odd-numbered n-alkanes preponderate) but similar to that in marine algae (Clark and Blumer, 1967). Isoprenoid hydrocarbons were represented by pristane ((&), which is also found in marine algae (Clark and Blumer, 1967) and zooplankton (Blumer, Mullin and Thomas, 1963, 1964), as well as phytane (C2,,) which is not commonly detected in marine organisms. Olefinic hydrocarbons were also found, one being identified as squalene which is also present in copepods (Blumer et aZ., 1964) and the liver oils of various species of shark (Heller, Heller, Springer and Clark, 1957 ; Blumer, 1967 ; Corner, Denton and Forster, 1969). Some of the hydrocarbons detected by Blumer (1970) have been

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identified and estimated by Whittle, Mackie, Hardy and McIntyre (1973) in water samples collected from 13 stations off the Scottish coast. Using sub-surface samples (3 m depth) that had been filtered through a 20 pm mesh they found levels of 0.3-1.5 pg/l for total alkanes, 0.015-0-043 pg/l for pristane and < 0.001-0.014 pg/l for phytane. Similar to Blumer’s (1970) observations the peak levels for compounds. individual n-alkanes were usually obtained with C,,-C,, Hydrocarbon levels vary considerably with sea area. Thus, Mackie, Platt and Hardy (1978), using techniques similar to those of Whittle et al. (1973), found that sea-water samples from King Edward Cove, South Georgia, contained 5.8 pg/l of n-alkanes within the range n-C,5-n-C33, together with 0.18 pg pristane/l; Iliffe and Calder (1974), studying hydrocarbons in the Gulf of Mexico and Caribbean Sea, found an average level of 47 pg/l for non-polar hydrocarbons in the Florida Strait, 12 pg/l in the mid-Gulf region, 12 pg/l in the Yucatan Strait, 5 pg/l in the Cariaco Trench and 8 pg/l in the Caribbean Sea, the samples containing n-alkanes in the range C,, to C,, with peak concentrations in the C,, to C,, region ; Carlberg and Skarstedt (1972), using infrared spectroscopy, obtained values in the range < 50 to 120 pg/l for non-polar hydrocarbons a t ten stations in the Baltic and Kattegat. Hardy, Mackie, Whittle, McIntyre and Blackman (1977) have recently described further data for the amounts of n-alkanes (C15 to CS3)in samples of sea water from various regions surrounding the U.K. The lowest value for n-alkanes in the surface film (mean value 5.7 pg/m2) was found in samples from the open sea (Celtic Sea) ; the the mean value for off-shore samples from sites near urban areas (62.9 pg/m2) was close to that for samples taken near oil refineries (64.2 pg/m2)and greater than that for those collected close to North Sea oil fields (32.8 pg/m2). Mean values for n-alkanes in sub-surface (Im depth) samples ranged from 0.57 pg/l (Celtic Sea) to 4.6 pg/l (North Sea oil fields). Studies described later (Section VII) show that hydrocarbons can enter zooplankton in two different ways: first, by direct uptake from solution in sea water ; second, by assimilation from particulate diets. I n considering the quantities of hydrocarbons available to the animals in the sea it is therefore useful to know the relative amounts of the compounds that are present in solution and as particulate material. I n addition, as certain species of zooplankton feed near the surface of the sea it is necessary to consider the spatial distribution of hydrocarbons, especially evidence for the presence of high concentrations in the surface micro-layer. These topics are discussed in the next two sections.


B.

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Dissolved

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and particulate hydrocarbons

Spillage of Bunker C oil from the grounded tanker " Arrow " in Chedabucto Bay, Nova Scotia, led to several studies of oil levels in that area and along the coast to Halifax Harbour and beyond (Levy, 1971, 1972; Forrester, 1971). Quantitative data were obtained by Levy (1971) for the levels of petroleum residues in the open ocean off Nova Scotia and in the St Lawrence system. Water samples were filtered through a 0.45 pm millipore membrane and the hydrocarbon content of the retained material was determined as equivalents of Bunker C oil using U.V. fluorescence spectroscopy. Similar analyses were made of hydrocarbons that passed through the filter, these being described as " dissolved ". The fluorescence technique is a rapid way of detecting aromatic compounds and allows a large number of samples to be processed in ship-board experiments ; natur??- to occurring organic material can produce interference thatbut is difficul quantify (Gordon, Keizer and Dale, 1974), particularly highly conjugated alkenes (Farrington and Meyer, 1975). The total levels of petroleum residues found in Chedabucto Bay by Levy (1971) were in the range 1fj-41 pg/l (as Bunker C oil equivalents). At several stations substantially higher concentrations of dissolved than particulate compounds were detected. Thus, in surface samples (1 m depth) particulate levels ranged from 5 to 16 pg/l and dissolved from 15 to 90 pg/l. Zsolnay (1971) measured what he terms '' non-olefinic '' hydrocarbons and describes as saturated hydrocarbons and aromatic compounds with only one ring in the Gotland Deep, a Baltic basin. Thinlayer chromatography was used to separate the hydrocarbons which were then estimated as total carbon. Average concentrations, based on samples from all depths (20-200 m) and expressed as carbon equivalents, were 57-2 pg C/1 for the dissolved hydrocarbons and 1.1 pg C/1 for the particulate, dissolved material in this case being defined as that passing through a pair of Whatman GF/C glass filters. Another study using thin-layer chromatography to separate the hydrocarbons from other lipids was that of Jeffrey (1970), who measured unsaturated hydrocarbons in Baffin Bay (Texas) and found 180 pg/l as dissolved (passing through a 0.3 pm filter) and 70 pg/l as particulate material. The particulate material was mainly phytoplankton, Baffin Bay being a shallow, warm region of high primary production. Nevertheless, the distribution of hydrocarbons between dissolved and particulate forms does not always favour the soluble fractions. Sediments, for example, adsorb levels of these compounds far higher

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E. D. S. CORNER

than those found in the associated sea water. Thus, Di Salvo and Guard (1975), studying the hydrocarbons attached to suspended sediments in San Francisco Bay, found them to contain alkanes and aromatic compounds in concentrations ranging from 190 to 6 188 mg/kg dry weight; by contrast the levels in the associated sea water were o d y 15-450 11.811. Marty and Saliot (1976) have shown that the relative amounts of n-alkanes in particulate and dissolved form depend upon whether the samples are taken from polluted or unpolluted areas. Thus, for coastal waters of the English Channel (Roscoff area) the concentrations of total dissolved (i.e. passing through a Whatman GF/C filter) C,, to C,, n-alkanes at 0.5 m depth was 0.11 pg/l compared with 0.28 pg/l for those in particulate form; by contrast, for off-shore waters near the West African coast (2 m depth), the total quantity in solution was 5.66 pg/l but that in particulate form only 0.32 pg/l. One would expect the hydrocarbons detected off the West African coast to be associated with the high primary production in a region of upwelling, for Zsolnay (1973) has described a close correlation between hydrocarbon and chlorophyll a levels in water samples from the same sea area. Likewise Parker, Winters, Van Baalen, Batterton and Scalan (1976) detected higher levels of n-alkanes in spring (0.64 pg/l) than at other seasons (0.13-0.23 pg/l) in sea water samples from the Gulf of Mexico.

C. Hydrocarbons in or near the surface of the sea The presence of high concentrations of hydrocarbons in the surface micro-layer of the sea was noted by Garrett (1967) in samples from various Atlantic and Pacific sites near North America, but the compounds were not identified. Swinnerton and Linnenbom (1967) measured n-alkanes of low molecular weight (mainly methane) by gaschromatography in water samples from the Gulf of Mexico (South of Mobile, Alabama) and North Atlantic (500 km west of Ireland). They found higher concentrations a t the surface than a t depth (500 m) in the Gulf of Mexico samples, although peak concentrations occurred a t 30-40m. No significant change in hydrocarbon level with depth was observed in the Gulf of Mexico survey by Frank et al. (1970). Iliffe and Calder (1 974) found higher levels of non-polar hydrocarbons at a depth of 1 m (24 pg/l) than at other depths in the Yucatan Strait, but in the Florida Strait the highest hydrocarbon concentration (75 pg/l) was a t a depth of 144 m. Whittle, Mackie and Hardy (1974),

POLLUTION STUDIES WITH MBRINE PLANKTON-I

295

analysing hydrocarbons at different depths in the Clyde, found only 3.21 pg/l in the surface film compared with 7-8 pg/l in the top 15 cm, although at middle depth (10 m) the value obtained was an order of magnitude lower (0.31 pg/l). Duce, Quinn, Olney, Piotrowicz, Ray and Wade (1972) detected three hydrocarbons, tentatively identified as CZ1.,, C,,., and C,,., at a concentration of 8.5 pg/l in the surface micro-layer (100-150 pm) compared with 5.9 pg/l at 20 cm depth. Wade and Quinn (1975) measured the total hydrocarbons present in samples of the surface micro-layer (100-300 pm) from the Sargasso Sea and found the levels to vary from 14 to 559 pg/l (average 155) compared with 13-239 pg/l (average 73) at 20-30 cm depth: n-alkanes from C,, to C,, accounted for 11% of the total hydrocarbons in combined micro-layer and subsurface samples, being present at an average level of 25.1 pg/l. The authors concluded that a major source of the hydrocarbons was particles of weathered pelagic tar with diameter ranging from 1.0 mm down to 0.3 pm located in the surface micro-layer. Earlier, Morris and Butler (1973) had reported the large amounts of pelagic tar that could be collected by neuston net from the surface of the Sargasso Sea, the average value being 9.4 mg/m2. By comparison, the mean level recovered in the same way from the surface of the North Sea was only 317 pg/m2 (Offenheimer, Gunkel and Gassmann, 1977). The accumulation and retention of floating material in the Sargasso Sea is well known. The average level for pelagic tar in the Mediterranean was even greater : thus, Morris and Butler (1973) gave a figure of 20 mg/m2. However, evidence from a more recent study (Morris, Butler and Zsolnay 1975) indicates that the average level of pelagic tar in the Mediterranean has now fallen to 9.7 mg/m2, a value much closer to that for the Sargasso Sea. Conover (1971) has shown that zooplankton are able to ingest small droplets of oil and it seems probable that zooplankton species such as Anomalocera patersoni Templeton that live near the surface of the sea could also ingest small tar particles. Hydrocarbons assimilated from these particles might then be available for transfer to higher trophic levels ; in addition, unassimilated material could eventually reach the benthos as faecal pellets (see p. 348). Tar particles represent a persistent legacy of spilt oil, probably taking years to be degraded because they contain large amounts of high-melting point waxes and asphaltenes (Morris and Bulter, 1973). Further observations on surface enrichment of n-alkanes have been made by Marty and Saliot (1976). The ratio between the concentration of dissolved compounds in the micro-layer (0.44 mm film)

296

E. D. S. OORNER

and that in the underlying water ranged from 6.3 :1 (Etang de Berre : Marseilles) to 161 :1 (Roscoff area) : the corresponding values in terms of particulate hydrocarbons were 170 :1 and 350 :1 respectively. It should be noted that these ratios, if calculated for a micro-layer of only 100 d thickness, would give enrichment factors 104-106 times greater. Marty and Saliot (1976) concluded that the n-alkanes present in the surface micro-layer were in general of biological origin as they possessed a distribution concentrating on n-C,, to n-C,, which was found by Clarke and Blumer (1967) to be characteristic of marine algae. However, qualitative differences occur between sea areas : thus, Ledet and Laseter (1 974) describe the alkanes at the air-sea interface from off-shore Louisiana and Florida as mainly branched and cyclic compounds. Ideally, to establish the biological origin of hydrocarbons in sea-water samples from a particular area i t is necessary to make a direct comparison of these compounds with those present in the plankton: however, no detailed study of this type seems to have been made. Concerning work with aromatic hydrocarbons Levy (1971), in his studies of oil pollution in Chedabucto Bay, found values of 15-90 pgll for dissolved compounds a t a depth of 1 m compared with 7-9 pg/1 at 20 m. On the other hand, Gordon and Michalik (1971)) working in the same sea area, found slightly increasing concentrations with depth : 1.2 pg/l at 5 m, 1.4 pgll at 6-25 m and 1.8pgll at 26-50m. Subsequently, however, in a detailed study of this aspect in the northwest Atlantic Ocean, Gordon et al. (1974)) using Venezuelan crude oil as a reference standard for U.V. fluorescence measurements, obtained concentrations at the surface (0-3 mm) averaging 20-4 pg/l compared with 0.8 pg/l at 1 in and 0.4 pgll a t 5 m. Studies that include measurements of total mineral oil hydrocarbons have given conflicting evidence. Thus, Carlberg and Skarstedt (1972), using samples from Gijteborg Harbour, found values of 0.71 mg/l at the surface compared with 0.47 pg/l at 6 m depth. However, Pavletid, Munjko, Jardas and Matoricken (1975), estimating mineral oil concentrations at different depths in the Adriatic off the Jugoslaviaii coast, found values of 1-40, 0.65, 1.56 and 10.98 mg/l at depths of 0, 2, 5 and 10 m at Monte Gargano ;but at another station (Pelegrin) surface samples were higher than those at depth, being 4.23, 2.39 and 0.82 mg/l at 0, 5 and 10 m respectively. The various hydrocarbon levels in the sea that have so far been discussed are summarized in Table I.

TABLEI. EX~D~PLES OF HYDROCARBON LEVELSIN

Type of hydrocarbon Methane

Concentration 0.025 to 0.283

Methane

0.047 to 0.060

Methane

0.06 to 1.25

THE

SEA

Geographic location

Reference

Various depths between 0 and 500 m : Gulf of Mexico Various depths between 0 and 500 m : North Atlantic Various depths between 0 and 3 742 m : Gulf of Mexico

Swinnerton and Linnenbom (1967) Swinnerton and Linnenbom (1967) Frank et al. (1970)

3 m depth : Scottish Coast 3 m depth : Scottish Coast 3 m depth : Scottish Coast 0 to 20 m : King Edward Cove, S. Georgia 0 to 20 m : King Edward Cove, S. Georgia 1 m depth: Celtic Sea 1 m depth : North Sea 0 to 500 m :Florida Strait, Gulf of Mexico 0 to 500 m : Mid-Gulf 0 to 500 m : Yucatan Strait 0 to 900 m : Carioco Trench 0 to 200 m : Caribbean Sea 0 to 100 m : Baltic and Kattegat 0 to 100 m : Baltic and Kattegat 0 to 31 m : Goteborg Harbour 0 to 31 m : Goteborg Harbour 1 m depth : Chedabucto Bay, Nova Scotia 20 m depth :Chedabucto Bay, Nova Scotia

Whittle et al. (1973) Whittle et al. (1973) Whittle et al. (1 973) Mackie et al. (1978) Mackie et al. (1978) Hardy et al. (1977) Hardy et al. (1977) Iliffe and Calder (1974) Iliffe and Calder (1974) Iliffe and Calder (1974) Iliffe and Calder (1974) Iliffe and Calder (1974) Carlberg and Skarstedt (1972) Carlberg and Skarstedt (1972) Carlberg and Skarstedt (1972) Carlberg and Skarstedt (1972) Levy (1971) Levy (1971)

(PLgIl) n-Alkanes Pristane Phytane n-Alkanes (C15 to C=) Pristane n-Alkanes (C15 to CJ n-Alkanes (C15 to C3J Non-polar Non-polar Non-polar Non-polar Non-polar Non-polar Total Non-polar Total Dissolved aromatic Dissolved aromatic

0.3 to 1-5 0-015 to 0.043 100 pg/1) enhanced it ; suppression of photosynthesis by n-alkenes occurred at all concentrations in the range 5 to 500 pgll, higher amounts causing greater effects. Further studies, using unialgal species, have recently been made by Prouse et al. (1976) who, as in their earlier work with natural populations of phytoplankton, paid particular attention to the need to study the toxic effects of crude oil using concentrations similar to those found in the environment. I n addition they took care t o monitor changes in hydrocarbon composition and level during the experiments, using fluorescence spectroscopy and gas chromatography. During the course of the experiments ( 1 6 1 8 days) they found that the composition of the hydrocarbons " accommodated " in the sea water changed markedly with time, compounds predominant a t the end being, not unexpectedly, the least volatile, most soluble and most resistant to biological alteration : that is, aromatic compounds of medium molecular weight. The presence of algae had a marked effect on the levels of oil in the test media, which fell by over 90% in 12 days. One new feature of the work was that growth data for all five test species ~ D u ~ l i ~ ltertiolecta, la Fmgilaria sp., Monochvysis sp., Skeletonema sp. and Chaetoceros sp.) cultured under axenic conditions were only obtained after the lag phase had finished and the plants were growing exponentially ; another was that the experiments lasted much longer (average 11 days). An initial concentration of 50 pg/l of a No. 2 fuel oil stimulated the growth of Fragilaria and initial levels of 55 and 106 pg/1 of Kuwait crude oil enhanced that of Dunaliella. However, contrary to previous findings (Gordon and Prouse, 1973), no strong inhibitions were observed and any minor ones that occurred in occasional experiments were short-lived (Fig, 6). Furthermore, the experiments did not show any consistent differences in response between the five test species. Consistent with the evidence that petroleum hydrocarbons can stimulate photosynthesis by certain species of phytoplankton are data by Dunstan, Atkinson and Natoli (1975) who measured the growth of

324

E. D. 5. CORNER

4 phylogenetically different marine algae exposed to a wide range (0.1 to 100 mg/l) of concentratous of the volatile, aromatic hydrocarbons benzene, toluene and xylene. The growth rate of Dunaliella tertiolecta was markedly stimulated by all 3 compounds ; smaller effects were observed with Amphidinium carterae Hubert and HymenomonaS cartrterae (Braarud et Paged.) Braarud as Cricosphaera carterae ; no enhancement of growth rate was found with Skeletonema costatum. The

Days

FIG.6. Growth of Dunaliella tertiolecta in the presence of No. 2 fuel oil. Oil concentrations: 50 (initial) falling t o 2 (final)pg/l (open triangles) :380 (initial) falling to 45 (final)pg/l (open circles). Dashed line = control. (After Prouse et al., 1976.)

growth rate of Dunaliella was also stimulated and that of Skeletonema reduced by No. 2 fuel oil, both effects depending upon the presence of the volatile fraction. Winters, O'Donnell, Batterton and Van Baalen (1976) have continued the work of Pulich et al. (1974) with further studies of the effects of WSFs of fuel oils on the growth of individual phytoplankton species. The work was less concerned than that of Prouse et al. (1976) with using oil concentrations close to those found in the environment. Instead, the main emphasis was on analysing the numerous chemical components of the water-soluble fractions of the oils and attempting to identify those that are particularly toxic. The fuel oils used, referred to by refinery location, were Baytown (Texas), Baton Rouge (Louisiana), Billings (Montana) and Luiden (New Jersey): the algal species were

325


Agmenetlum quadruplicatum, Coccochloris elaabeus (Brkb.) Dr. et D., Dunaliella tertiolecta, Chlorella vulgaris var. autotrophica, Cylindrotheca sp. and Amphora sp. About half the water-soluble components of each oil were identified by gas-chromatography and mass spectrometry. Included were compounds such as naphthalene, alkyl-naphthalenes, benzene and alkylbenzenes identified earlier by others (e.g. Boylan and Tripp, 1971): particularly interesting, however, was the detection of phenols, methylanilines (o-, m- and p-toluidine) and indoles, the methyl-, dimethyland trimethyl- derivatives of which were present in relatively high amounts. Phenols accounted for more than half the total identified organic compounds in the WSF of the Baytown fuel oil and were also well represented in that of the Montana fuel oil (Table XI). TABLEXI. MAJORCONSTITUENTS OF WATER-SOLUBLE FRACTIONS OF FUELOILS

Montana (PgP) Total identified organics Methylnaphthalenes Dimethylnaphthalenes Phenols Anilines

8.07 0.53 0.31 2.33 2.57

Baytown New Jersey (Pg/l)

(PgP)

7.90 0-81

5.66 1.30 0.55 1-96 0.27

0.24 4.12 0-72

Baton Rouge 3-52 0.76 0.41 1-08 5.0 X lo* Lowest lethal concentration Lowest concentratiun causing 4.0 X lo* 25 growth inhibition 2.5 x lop Lowest lethnl concentration Lowest coocentrution cawing 3.0 X loa 50 mowtlr inhibition >2.5 x 10' Lowest Ivtllal concentration Little effect on "CO. 20 2 68 klux 3 x 10' 1-10 Tkachenko el ul. photoaynthetic rate (1974) P Photosyntliesis inhibited >10 especially after prolonged exposure to metal Final cell populatioir 7507: of Bentley-Mowat CU. 3.0 x 103 18 4.6 klux that in control nt end of 12 h/day -3.0 X 10' and Reid (1977) exponential yhnse 1 5.6 x 106No eflect upou rate of 0, Overnell (1976) 18-20 production in saturating red liyl I t 1.1 x 106 after 15 mins dark incubntion with metal Berland et d. 20 104klux 1.1 x 104 50 ].owest concentration causing (1976) growth inhilJiti(Jn 14 h/day Lowcst lethal concentration 5.0 x 10' Ro l.ncct upon rate of 0, Overnell(l976) 13-20 ? 1.1 x 106 production in saturntiug rod light after 15 mi118 dark incubation with metal 25 Berland e l d. Lowest concentration causing 20 10.2 klux 1.3 x 10' growth inhibition (1976) 14 h/day 20

102klux 14 h/day

3.0

25

>5.0 x 10' 6.0 X 10' 25

Heterolhrir sp.

8.0 X10*

Monullanlus salinu

2.5 x

lo4

>102 2.5

X

lo*

>10' 50

2.5 X 10'

Lowest lethal concent rat ion Lowest concentration causing growth inhihition Lowest lethal conceotration Lowest roncrntration causing growth inhibit ion Lowest lethal roncentration

Temp. IUumina-

Medium

SpscieS

('C)

+ +

-+

Artiflcial SW 1 mM NO 57 UM HP0,'micronnhents 0.15 mM EDTA

+

+

+

+

+ ++

Chaetmros

closteriun

SW 0.18 mnl NO,7 UMH;PO,micronutrients 5 p N EDTA SW f 0.2,mM NO,20 pM H,PO,micronutrients 2 mM TRIS

Ditylum b r i g h t d i i (West) GrUn.

SW 2 mM NO.0.35 d v 1 HP0,'trace elements 0.1 M citrate

Cylindrdheea

Frogilaria pinnda

+ +

+ + +

+

+

-

102 klux 3.3 x 10' 14 hiday

15

5.4 klux

20

24 hlday 102klux 14 h/day

9

25

z50 10'

0 5 X 10'

5.0 50

20 f 2 68kluX

1-10;

10

9

+

+

102klux 3.0 x 10'

14 h/day

Phaeodaclylum

-

+

SW 0.2 mM NO.20 pM H,POI1micronutrients + 2 mM TRIS

+

+ +

+

Artiflcial SW (16%sslinity) 1 mM NO.57 WMHPO trace elements 0 1 3 mM EdTA SW 0.2,mM NO,- 20 p N H,PO,micronutrients 2 mi TRIS

+

+ + + Artiflcial SW + 1 mM NO - + 57 PM HPO,~- + micronutri&ts +

18 20

18-20

4.6 klux 12 hlday

10'

P

10.2 klux 6.0 14h/day

X

50 22.5 x 10' 50 >2.5 x 10'

?

5.4 k l u 24 hiday

tricmulum

Skeletonemu m l a t u m

1.1 x 10'

10%

'-+

1.1 x

10'

IW

10'

>108

P

ca. 3.0 x 10'-

3.0 x 10'

10,2k l u 1.3 X 10' 2.5 x 10' 14 h/day >5.0 x 10' 9 1.1 x 10'

-

0-15DIMEDTA

+ + SW -4 0.18 mM NO - + 7 pId H,PO,- + micronutrients + 5 ;M EDTA f 0.2 mM NO.20 pM H,PO; micronutrienta + 2 mM TRIS

SW

Effecl

added (&I)

5.6 x 104-

P

20

Lauderia boredis

+

Initial mctal c m .

10'-10*

SW 0.2 mM NO.20 pM H.PO,micronutrients 2 mM TRIS

+

18-20

+

SW 0.2 mM NO.20 pM H,PO.micronutrients + 2 mY TRIS

+

Initial no. oj cellal rnl

CADMIUM (aontinued)

Chaetocero8 didymue

gdveetonenais

liMI

20 15

10.2klux 5.0 14 hiday

X

5.4 klux 24 h/day

P

10'

10 >5.0 x 10' 10'

Overneil(l976) No effect upon rate of 0, production in saturating red light Bfter 15 mins dark incubation with metal Lowest concentration causing Berland e l al. (1976) growth inhibition Lowest lethal concentration Hanuan and Little effect upon growth Patouillet (1972) Berland et ad. Lowest concentration (1976) causing growth inhibition Lowest lethal concentration Tkachenko el al. "CO,-Photosynthetic rate (1974) increased relative to control Photosynthesis decreased but still greater than in control Berland et d. Loweat concentration causing (1976) growth inhibition Lowest lethal concentration Lowest conceutration causing growth inhibition Lowest lethal concentration Little cEwt upon growth

No effect UDOU rate of 0, productionin mturatingred light after 15 mins dark incubation with metal Lowest concentration causing growth inhibition Lowest lethal concentration Final cell population 100-5% of that in control a t end of exponential phase Lowest concentration musing growth inhibition Lowest lethal concentration No effect upon rate of 0, production in saturating red light after 15 mins dark incubation with metal Lowest concentration causing growth inhibition Lowest lethal concentration Little effect upon growth

Berland el d. (1976) Bentley-Mowat and Reid (1977) Berland a6 d. (1976) Overnell (1976)

Berland el d. (1976)

Hannan and Patouillet (1972)

Prasinocladus marinue

+

+ +

SW 0.2 mM NOs20 p M H,PO,micronutrients 2 mM TRIS

+

20

10.2 klux 4.0 x lo" 14 h/day 10'

Tetradelmis strialu Tetradelmis spp.

Brachiomonaa SUbmaritUZ

Chlamgdmnwm palla

Dundiedla bioculata

Dundiella primdecta

Butcher

Dundiclla lerlidecla

+

18

Artificial SW (16% salinity) 1mM NO - 4-57 MM HP0,'hce elements 0.13 mM EDTA Artificial SW 1mM NOs-. micronutrients 57 pId H P O p 0.15 mId EDTA

+ + +

++

+

+

SW 0.2 mM NO.20 pM H,PO,micronutrlents 2 mM TRIS Artificial SW vitamins

+

18-20

+

9

>10' ca. 3.0 x 3.0 x 10'

7

1-1x

10.2 klux 2.5 x 10' 14 h/day

lo*-

lo6

25

-

10'

5 . 0 ~10' 243 x lo62.1 x 10'

?

?

?

7

39-8 x 10.

9

9

7

7 9

>8 x 10s M. 8.0 x 10'

+

Artincia1 SW (16% ealiniiy) 1mM KO,57 pM HP0,'trace elements 0.13 mM EDTA Artificial SW 1mM NO.-, 57 uId H P O P micronutrients 0.16 m~ EDTA

+

20

+ ? NO.- + ? PO4'- + + + +

4.6 klux 12 h/day

25 25.0 x 10' 5.0 x 10'

+

+

+

+ li 20

4.6 klux 12 h/day

-3.0 x

lo*

Lowest concentration causing growth inhibition Lowest lethal concentration Lowest concentration causing growth inhibition Lowest lethal concentration Final cell population 1 0 5 5 % of that in control a t end of exponential phase Noeffectuponrateof 0, production in eaturating red light after 15 mina incubation with metal Lowest concentration causing growth inhibition h w e s t lethal concentration Oxygen production l W 6 % of that in control when culture intensely illuminated (16 klux) Growth inhibited

Berland et d , (1976)

Hannan and Patouillet (1972)

Overnell(1976)

Berland el d. (1976) Saraiva (1973)

PenedaSaraiva (1976) No growth Final cell population Beutley-Mowat ln&az.0% of that in control a t and Reid (1977) end of ex$nential phase Rate of 0, production in Overnell(l975) saturating red light reduced to 70% of that in control after 15 mi& dark incubation with metal

-

?

5.4 klux 24 h/day

Y

10'

Lethal concentratlon

?

10'

Little effect upon growth

9

10'

No growth

1.1 x 106

Bentley-Mowat and Reid (1077)

SILVER

+

SW 0.18 mM NO,7 pM H,PO.micronutrients 5 UMEDTA

+

+

15

Ip

00

4

le 00

00

Egmt

Med;um

LEAD Pmphyridturn

+

+ +

SW 0.2 mM NO,20 pJI H,PO,micronutrients 2 mM TRIS

+

3.0 x 10' 2.5 x 10'

Rhodophyta Bangiophyoeae

marinurn

CryptOPh~~ CrpptophyCCeae

p8ei6dObaJtiCa

Ctllptom-

>2.0 x 10. 6.0 x 10. 1.0 x 10.

Dinophyta Dinophyceae

Amphirlinium carterm

4.0

Emmadla mariadebouriae

3.0 x 10'1.0 x 10s

Prorocmtrum m k n a

Scrippsiella faeraense

20

1 0 2 klux 1 4 h/day

x 10' x 10'

>2.0

X

loa 2.5

2.0 x 10'

s7f f

1.2 mM NO,- f 013 m N H,PO,soil extract

+

15

6klux 1 4 h/day

>2.0 x 10' 1.2 x 10'25-1W

1.3 or 7.2 25-10' x 10'

>lo*

+ +

Haptophyta Hymnnmol~a Artiflcial SW (16% ealinity) 1mM NO.- + Prymnesiophyceae (Cricosphmra)elonrJaa 57 pM HP0,'trace elements (Haptoph yceae) 0.13 mM EDTA Pavloua ( M m e h r y g i s ) YW 0.2 mM NO.20 ~ dH,PO,l lutheri micronutrients 2 mM TRIS

4.6 klux 12 h!day

50

10.2kln~ 1.1 1 4 h/day

X

P a v h a pinguis

>2.0 x 10' 1.3 x 10' 5.0 x 10'

Heteothrix sp.

8.0

X

+

%%:tthg&%e

+

.M~ndantuaaalina %a!$&eae

?

18

+ + +

20

+

Asterimlla glucialia (A. japonica)

SW 0.66 mM NO,- f 25 pM Na, glycerophosphate micronutrients 14 mM EDTA

Chaetoceros didymus

+ 0.2 mM NO.- + 20 H,PO,- + micronutrienta + 2 mM TRIS

+

+

2

2.1 X 10'1.2 x 105

10' 1.0

loa

>e.o x 108 10' 2.0 x 10.

>2,0 x 10' 10.2 WUX 2.5 X 10' 2.0 X 10.

1 4 hiday ?

ea. 10'

>2.0 x 10. 5.6 x 10' 3.2

SW

X

Y

Lowest concentration causing growth inhibition Lowest lethal concentration Lowest concentration causing growth inhibition Lowest lethal concentration Lowest concentration causing growth inhibition Lowest lethal concentration Lowest concentration causing growth inhibition Lowest lethal concentration Little effect on growth rate

Berland st al. (1976)

Little effect on exponential growth rate Final population less than in control Cell population 85-5OA of that Bentley-Idowat in controi at end of exponential and Reid (1977) t%&t concentration causing growth inhibition Lowest lethal concentration Lowest concentration causing growth inhibition Lowest lethal concentration Lowest concentration causing growth inhibition Lowest lethal concentration Lowest concentration causing growth inhibition Lowest lethal concentration No effect upon growth Growth severely inhibited Lethal concentration Lowest concentration causing growth inhibition Lowest lethal concentration

Berland st al. (1976)

Aub& (1972)

6t

d.

Berland ct al. (1976)

rc P

u

8

m

Coscinodiseus granii Gough

+

+

SW 2 mM NO,0.35 mJI HPO.atrace elements 0.1 If citrate

+

+

+

20 pM H,PO,Cylindrotlreea closlen'um SW 0.2 mM NO.micronutrienta 2 mM TRIS 9 W + 2 mM NO.- + 0.35 mM HP0,'Ditylum brightrodlii trace elements 0.1 M citrate

Friragilaria pinnnta

+

+ +

+

SW 0.2 mM NOS- 20 pM H,PO.micronutrients 2 mM TRIS

+

+

20 f 2

68 klux ?

+

20

+

10.2 14 h/day

5

20 f 2 68!$ug

+

1-10

kina 6.5 x i o G i O a 1-10

10

20 1, ~

10'

I,nuden'a borealis

+

+

+

SW 0.22 mM NO,9 pM H,PO.micronutrients 6 pM EDTA YW 9 mM Na glutamate 160 pR.1 Na? glycerophosphate trace elements

+

+

+

+

+

Artificial SW 1mN HN0,57 pM HP0,'micronutrients 0.15 mM EDTA

+

+

22

20

+

+

20

10.2ldUX

14 h/day

++

SW 10 mM NO,320 pM Na glycerophosphate trace element:

>2.0 x 10s 10'

?

5.4 k l w

24 h/day 2 klux

24 h/day

+

S W C 0.2 mY NOJ20 pM II,PO.micronutrients 2 mM TRIS

+

15

+

__ 2.0 x 102

- _..

10' Lag phase increased from 37 to (1.8 x 108 51 days. Mean generation time in solution) 1.3 times that in control. Maximum yield 40% of that in control Rate of 0,production in ? 2.1 x 10' -4.2 x 104 saturating red light redured to 95-40% of thst in control after 15 mine dark incubation with metal Lowest concentration causing 6.0 x 10' 105 growth inhibition >2.0 x 102 Lowest lethal concentration Photosynthetic rate decreased 4 10*-104 with rising concentration to only 2 5 4 % of control a t highest level. also decrPAsd with lOnwx tinii'ofisposure to metal

3.0

X

10'

25* 30 35

4.3 klux

18

4.6 k l w 12 h/day

20

10.2 k l u 1.3 14 h/day

X

lW

5.0

X

22.0 x 10' 10' 2.5 X 10'

v

W O , Photosynthetic rate increased Photosvuthesis inhibited Lowesccnncentration causing growth inhibit ion "VO. Photiiwnthetic rstc incrgased Photosynthesis inhibited Lowest concentration causing growth inhibition Lowest lethal concentration Lowest Concentrationcausing growth inhibition Lawest lethal concentration Little effecton growth rate

Tkachenko et d. (1974) I3erland el al. (1976) Tkachenko ef al. (1974) Berland et al. (1976)

z u)

Hannan and Patonillet (1972) Dayton and Lewin (1975)

+

Thdaamouira peeudonnrta

+ + +

+

+

6.5 x 10'

?

10'

2.0 x lo"

Cell population little different from that in control a t end of exponential phase Lowest concentration causing growth inhibition Lowest lethal concentration Lowest concentration causing rowth inhibitlon oweat lethal concentration

e

3 4

ca 4

Overnell(1975)

Berland 6f d. (1976) Woolery and Lewin (1076)

__

Artificial SWz103 Stimulating in dialysis culture, 1.6 x 10' 10 1.1times growth rate in control >2.5 x 10% Qroatli rate decreased Lethal concentration 103 ? >2.5 x 10' Growth rate decreawd X

10'

5.0

X

? ?

108

-

6.4 x 1.4 x

4.0 klux 15 h/day

3.0

2.7 klug

9.0 x 10'

X

10'

1.1 x 10'1.1 x 106

10'

loa loa

50

(1.6-2.5)

20-30

SW 1.2 mM NO.57 pM HP0,'micronutrients 1.2 mM NO,57 pM Artiflcial SW HP0.Imicronutrients

+

+

?

12 h/day

Berland ct d. (1976)

metal.

+

Natural SW (dialysis cnlture)

+

4.0 klux 24 h/day 15.5 f 5 klux (1.4-2.0) x 18-12 0.5 16 hlday loo 20 1 0 4 klux 3.0 x 10' 2.5 x 14 h/day > 10' 25 10s ?

Lowest concentration causing growth inhibition Lowest lethal concentration Lowest concentration causinrc growth inhibition 10' Lowest lethal concentration x 10'Lowest concentration preventing growth Cell population after 90 hours only 77-38% of that in eontrol 10' Lowest concentration causinc growth inhibition Lowest lethal Concentration Lowest eonrentration causing growth inhibition 10' Lowest lcthal concentration No effect upon growth

-

10'

>5.0 x 1.6 x lo4 (1.3-1.9)

20-30

1s

SW

loa

25

>lo*

X

Jensen el al. (1970) Jensen et al. (1976)

Lethal Concentration Cell population 100-0:i, of that Bentley-Mowat in control a t end of exponential and Reid (1977) nhasn gingie dose in continuous culture had little effect Single dose in continuous culture caused increase in cell population Lowest concentration Mandelli (1969) Lowest preventing concentration growth preventing growth Cell population 80 rt 4% of that Erickaoo et al in control after 14 davs (1970) (.ell~opulationinrreised over that in control after 14 days Cell population 97% of that in controiafter 14 days I

Medium

pW;T-

COPPER (continued) Skel&onenso coslatum

(00,rrnWB)

SW

+ 0.2 mM NO,- + 20 pM H,P04- +

micronutrients

20

+ 2 mM TRIS

Natural SW (dialysis culture)

+

6-8

+

75% sw 0.18 mM,NO,7.2 pM H PO - micronutr~euts 4 8 pM E b T i

+

13

+

18-20

Artificial SW 1mM NO,-, 57 pM HP0,'micronutrients 0.15 mllI EDTA

+

Thdaesiorira plloialilia Host. Tholasrwsim pseudonana

+

+ +

+

Daylight

1.8 x 10'

SW 1.8.mM NO,72.5 pM &PO.micronutrients 9.3 pM EDTA SW, unenriched

3kIux 16 h/day

P

-

P

25 10

20*1

4.0 klux 24 h/day 2.7 k l m 14 hiday

20

10.2 k l m 14 h/day

20-30

3.2

3.0

X

5.0

X

5.0 x

+

+

SW 0.2,mJI NO.20 fl &PO,mcronutrients + 2 mM TRIS

+


+

+

+

Thala8&8ita

+

+

+

+ + + + SW + 1.2.mM NO;. + 57 pM HP04'- + mcronutnents SW 1.8 mM NO - 72.5 pX H,PO,micronutrients 8.3 p~ EDTA

10

Daylight

1.6 x 10'

4

lo*

20 f 1

3 klux 16h/day 7.2 klux 14 h/day

W.104

-

20

4.0 klux

2.0

2.3

20 f 2

2.7 klux 14 h/day

7.0 X 10'

X

lo*

X

lo1 210 2.5 10

13

X

10' (1.8-2.6) 10. lo" 25.0

5.0 x 10'

8-8

75,% SW 0.18mMNO.- + 7.2pMHyP0.mcronutrients 4 8 flEDTA SW 0.88 mM NO.36 fl H,PO,: micronutrlents 1.0 pM EDTA variable levels of TRIS bufFer

+ +

50

>5*0 x 10' 1.6 x lo6 10

25

+ +

+

10.2 klm 14hlday

X

10'

50

106

X

10'

24 h/day 50-3.5 X 10' 4 0 x lo*

Lowest concentration causing growth inhibition Lowest lethal concentration Growth rate 19% of control value Lethal concentration Growth rate 83% of control value Growth rate 50% of control value Rate of 0, production in saturating red light reduced to 50% of that in control after 15 mins dark incubation with metal Lowest concentration preventing growth Growth and W O , flxation rate decressed especially on extended Lxposure to metal Mean cell volume increased by extended exposure to metal Lowest concentration causing Lowest inhibition growth lethal concentration

Berland et d.

(1876)

Jensen el d. (1876)

OverneU(l976)

8

0 Mandelli (1969)

Q

Berland et d. (1878)

v1

Sunda and Growth inhibition was related to calculated concentration of Guillard (1976) free. uncomplened Cult ions: values > 1.6 ng/l reduced erowth rate which became zero 'st c0. 0.3 pg/l Lowest concentration Mandelli (1969) preventing growth Cell population increased over

after 14 days, smaller still at

higher metal concentrations

rc

Ericknon (1972)

Jensen et d. Growth rate 77% of control value (1976) Lethal concentration Growthrate 73% ofcontrolvniue

that in control after 14 days Cell population 87% of control

k

Ericbon el d. (1970)

Artiflcial SW 57 p M HPO.'-

+

++1.2micronutrients mM NOs- + +

SW 0.2.1nM NO.20 pM H,PO,mfcronutrients 2 mM TRIS

Ohlorophyta Prsainophyceae

TelraeclmiSspp.

+

20

t

Artificial S y J l 6 % salinity) + 1 mM NO,trace elements 57 pM HPO, 0.13 mM EDTA

+

+

++

+ +

+

+

+ +

+

Chlamydoinonas p a l k

SW 0.2mM NO.20 H,PO,micronutrients 2 mM TRIS

Dundiclla primdccta

1 mbl NO; Artiflcial SW (16% salinity) 57 pM HP0,'trace elements 0.13 mM EDTA

+ +

+

SW 1.8 mM NO.72.5 pM H,P04micronutrients 9.3 pM EDTA S W 1.2 mMNO,- 3.57 p M HP0,'micronutrients 1.2 mM NO,Artillcial SW 57 pM HPO,' - micronutrients Artiflcial SW 1 mM NO.57 pM HP0,'micronutrients 0.15 mY EDTA

+

20

+ +

+

+ +

+

++ +

+ +

+

18

16-20

Arti5cial SW 1 m?INO.-. 57 pM HPO.'micronutrients 0.15 mM EDTA

Chlorophyta Chlorophyoeae

Cell population 89% of control after 14 days; smaller a t higher metal concentrations Lowest concentration rsusing 1 0 2 k l m 4.0 x loa 50 growth inhibition 14 hiday >2.5 x lo3 Lowest lethal concentration Lowest concentration cansing 104 50 growth inhibition >5.0 x 10' Lowest lethal concentration 46klux 9 1.1 x 10'- Cell population 80-100% of that 2.0 x 10' in control at end of exponential 12 h/day Phase ? 2.0 x 104- Cell population 1000% of that 1.1 x 108 in control at end of exponential phase 1 (1.3-3.2) x Rate of 0, production in saturating red light reduced to 50% of that in control after 15 mins dark incubation with metal Lowest concentratlon causing 10.2 klm 2.5 X 10' 50 14 h/day growth inhibition 2.5 x 10' Lowest let,halconcentration 46klux ? 1.1 x 10'- Cell population little different 12 h/day 2.0 x 10' from control a t end of exponential phase ? 2.0 x 10'- Cell population loO-Oo/,of that 1.1 x 10' in control at end of exponential 1.5 x 10'

18

35

20*2

4.0 k l U 5.0 x 104 >6.0 x 103 24 h/day 2.7 khm 8.0 x 10' 4.5 x 10' 14 h/day 4.6 x 103

20

+

?

1.3 x 10'2.5 x 10' 4.4 x 10'

1e-20

Nannoelrlatw atomus Butcher

+

+

+

SW 0.88 mM NO,- 36 pJI H.PO.micronutrlenta 1.0 pM EDTA variable levels of TRIS buffer

+

+

20 f 1

1.3 x 10'2.5 x 10'

7.2 k l u 14 hjday

cu. 6.0

x 104

-

Berland ct al. (1976)


Overnell (1976)

L4

% Berland el al. (1976)

a

!2


Mandelli (1969) L%st concentration preventing growth Cell population 80% of control Erickson et a[. after 7 days (1970) Cell population 84% of control after 7 days Rate of 0, production in Overnell(1975) saturating red light reduced to 9 5 4 % of that in control, after 15 mins dark incubation with metal Potassium content of celb 8&10% of thnt in control Overnell(l976) Rate of 0. production in saturating red light reduced to 50% of that in control after 15 mins dark incubation with metal Growth inhlhition was related to Sunda and calculated Concentration of free, Quillard (1976) nnromplexed Cu' ions; growth rate reduced by values > 2.5 ug/l and became zero at M. 0.3 pg/l +

8

w

Form and effect

Medium

sw + 1.1 mar NO,-

+ 56 or ~

CHROMIUM ~ 0 , s -

+ 0.60 mM NO,- + 25 p M Na, glycerophosphata + micronutrient9 SW

+ 14 mM EDTA

PAaeodoetyl U N l lrieonzutum chlorophyta Chlorophyceae

SW

+ 1.1 mN NO,- + 56 uM HP0;-

?

(1-8) x lo*

1

P

?

2.0 x 2.8 x los

Cr I11 ; Growth inhibited by up to 50% at higher concentrations Cr M; Growth rate reduced at Anbert er al. first but later recovered; final (1972) population lower than in control 5.6 x lo8 Cr VI. Initial decrease In cell popudtion but culture recovered and grew giving flnal DoDulation onlv about loo/, .- of that in control1.1 x 10‘ Cr VI; Lethal concentration 10*-2.0 x 10’ Cr I11 ; No effect upon growth Bernhard and rate Zattera (1970) 4.0 x lo* Cr 111. Growth rate slight& inhibited 2.0 x 106Cr VI; Oxygen production Saraiva (1973) 2.0 x 10’ lOO-QZ% of that in control when cultures intensely illuminated (10 klux) 4 4 x loa Cr VI ’ Growth stimulated Pepeda-Saraiva 4 4 x los Cr VI Growth inhibited a t b t (1976) but cultures later recovered giving 0nal populations similar to that in control 9.2 x 10’Cr VI ; Qrowth increasingly 9.2 x 10‘ inhibited Cr V1; No growth 1.8 x 10’

18

? 12 h/day

9

?

?

?

18

P

?

lW

ca. 10‘

?

12 h/day ?

Artificial SW vitamins

Refem

+ 7 XO.,- + ? PO,’- +

20

-

107

?

?

f

?

?

?

(1-4) x 10.

Cr 111; No effect upon growth rate

Bernhard and Zattera (1970)

c

%

Haptophyb Cornlithue huZleyi .w Prymnwiophyceae I (Haptophyceae)

SW

+ 1.1 m M NO.- + 66 pb1 EP04a-

ZINC 18

?

12 hiday

Icn4

+ +

+

Artificial S W 1 rnM NO - 57 pbl HP0,'micronutrients'+ 0.15 mil1 EDTA

18-20

-

2

2.0 x 10'

Xo effect upon growth rate

?

4.0

?

(3.3-6.6) x 104

Growth inhibited especially a t higher concentrations Rate of 0, production in saturatingfed light reduced to 90-85% of that in control after 15 mins dark incubiLtion with

?

(1.3-2.0) x 105

X

10'-10'

Bernhard and Zattera (19iO)

mf+A ~. .-.

Rnte of 0, production in saturating red light reduced to

SOo& of that in control after 15

mini dark incubation with Asterionella glacialis Chrysophyta Bacillariophyceae (A. japonica)

+ 0.66 mM NO,- + 25 pM Sa, glycerophosphate + micronutrients + SW

14 mM EDTA

?

?

?

10'

1

?

18-20 Artiflcial SW f 1 mM NO,- f 67 W N HP0,'micronutrients 0.15 m31 EDTA

CylindrotWa (Nttz8chia) closterium Pllaeodactylum

Artiflcial SW 084 ml\I NO,- f 0.11 mM HaPO4SW 1.1 mM NO,56 3 1 HPO,*-

rricornl4tuTR

+

+

1.7 x 103 5.4 x 103 (9.3-6.6) x 10'

+


15.5f 0..5

16

1

5 klux (144.0)x 16-42 16 hjday 10' ? ? (2-8) x 10' 1 2 h/day 103-104 Daylight 6.7 X 10'- 5.0 44 x 10'

X

10a-lO'

6.7 x i o c 2.5 x 104 2.2 x 106 105 25

Skeletonema costalum

4 4 X 10'4.9 x 101

5.0-5 x

loe

(2.249)x 10' 10' 6.4 x 10'- 50-10' 107 9.0 x 104- 2.5 x 108-108 4.0 X 10" Chlorophyta Chlorophyceae Y

DunalisUaterfidcda

ArtiEf!l HPO, EDTA

(1972)

No growth. cell numbem constant Lethal conEentration Rate of0,productionin Overnell(1976) saturating red light reduced to 80-700/ of that in control after 15 m i d dark incubation with mpt,nl

+

+

-

Aubert et al.

metal Little effect upon growth

?

Attheya dceora

(hernell(1976)

?

+ 1mM NO - +0.1567 m@ I 18-20 +SWrnicronutrients'+ u

-

4.0 X 110'

.

104 6.6 X 10'

llosko and Cell populationafter 96hours only 70-80% of that in control Rachlin (1975) Bernhard and No effect uDon ~- growth rate Zattera (1070) Growth inhibited. esoeciallv at higher concentrations Jensen et al. Average growth rate greater than in control, little effect (1974) upon h a 1 population Average growth rate only about 77OL of that in control Grokth rate greater than in

.

rnntrol . . -....

Average growth rate only "-45% of that in control; flnal population also decreased kkhal concentration Average growth rate greater t,han in cnntrol Average growth rate only 89-33O' of that in control. final &ulation also decrhased Lethal concentration Rate of 0,production in saturating red light reduced to 80 7 of that in control after 15 gins dark incubation with metal ~

Overnell(1,976)

APPENDIXII CONCENTRATIONB (P.P.M.DRYWEIQHT)OF H?EAVYMETALS IN PHYTOPLANKTON AND MICROPWETON COLLECTEDFROM VARIOUS SEAAREAS

+

W

Mjcroplankton oonsiat of a mixture of phytoplankton microzooplanktonand detritus. The data of Vinogradovs and Koval'skiy (1962)were'converted from an ash weight to a dry weight basis using a factor obtained from Fujita (1972); the data of Szabo (1968)were similarly converted using a factor obtained from Szabo (1967). The data of Thomnson el al. (1967)were obtained from Suencer and Sachs (1970). Concentrations in brackets are m d a n values. ND = Not detectable. SA = Spectrographic analysis. AA =Atomic absorption analysis.

Maah size (wm)

Location

Method

Drying temp. YC)

RangeConcentrationMean

Reference

MERCURY Mixed phytoplankton

?

?

60

i6

Mixed phytoplankton I M i e d phytoplankton Miged phytoplankton I1 Mixed phytoplankton 111 Mixed phytoplankton

76 153

Microplankton

76 132 60

-

76 76 7

?

0.09-0.79 0.11-0.70 0.10-0.27

Yatsushiro-kai, Japan Ariake-kai, Japan E . Pnriflr nj

? ?

AA AA AA

60 60

0.12-048 0.15-0.59 0.01-0,52 L

0.46 0.41 (0.19) 0.19 (016) (0.16) 0.15 0.10

-

0.11-0$3 0,058-0.26 0.028-0.26

0.132 0.099

GO 60 FO

0,05457

0.21 0.19

65

2.2-65 04-695 1.1-35

$5

i

Hirota et d.(1974) Knauer and Mnrtin (1972) Martin and Knauer (1973) Cocofos et al. (1973) Martin and Knaner (1973) H i o t a et al. (1974) . , Martin and Knauer (1973) Fowler et d.(1976b)

METHYL MERCURY Mixed phytoplankton

!

Yatsushiro-kai, Japan Off Minamata Japan Atiake-kai, Jipan

? ? ?

iG

Monterey Bay, Californie

AA AA AA AA AA AA

?

004-040 005-0.17

Hirota et al. (1974)

-

CADMIUM MIxed phytoplankton I11 U e d phytoplankton Mixed phytoplankton I1 Mixed phytoplankton Mixed phytoplankton I Mixed phytoplankton

64 76 64 76 37 64

Paoiflc, off Hawaii Monterey Bay Caliornia Korthwest d f of Mexico

64 64 64 64 1$2 60 76

AA

AA

37

Microplankton

AA E. Paci5c Off Los Angela, California Nediterranean Sea E.Paci0c

AA AA A.4

AA AA AA AA

? 05 ?

65 ?

9,

i ?

? ? ?

65

1.0-2,o

0.4-4.8 lqphoh48 Sp. Serpeates sp. C l i m sp. SpirrUella (Limocina) t i & i J m & (D'Orbigny) Sagitca bipumlala Quoy Sagitta -and Sagitta minima Orassi Sagitla paci~%%Tokolka SW.tta r o h t a Doncaster Sagitta setosa and S. ew'na

Urochordata Thaliaeea

S d p a Jusifomi.9

Mixed zooplankton

%rotoma sp. (malnly copepoda and S-Ia

bfixed zooplankton Mixed zoophnkton

Mixed )r zooplankton Mixed zooplankton

E. Atlantic Mediterranean Sea Sagami Bay, Japan E. Atlantic Neditenanean Sea N. Pacific Ocean Sagami Bay, Japan Japan Sea Off Nova Scotia Sagami Bay, Japan Black Sea Japan Sea N. Pacific Ocean E. Atlantic sp.) N.W.African coast E. and N.E. United Stater coast N.W.Atlantic Off Puerto Rim North Sea FUh of Clyde

E.Pacinc N.W. Gulf of Mexico Firth of Clyde

65 69 745

Leatherland el al. (1973) Fowler et d.(1976b) Fujita (1972)

50 98 68 160 113

Leatherland et d.(1973)

60-79

156-170 -

75 224 162 394 134 86

9

i 105 ? ? ?

-

105 105 105 105 105 105 105 105 ?

105 105 9 ? 1 9

86

100

P

100 65 4

-

3 300-4 400

-

-

90-2 700 40-1 200

633 121 105 1 468 237

92-591 120-1 200

236 428

54-1 220 207-252 Ql-892 50-385 41-200 110-139

228 199 -

-

301

Fujih (1972) Fowler et d.(1976b)

b

8 Nayaaud and Martin (1975) Fujita (1972) Vinogradova and Koval'skiy (1962) Fujita (1972) Leatherland el al. (1973) Windom (1972)

Nartin (1970)

2 +4

?

!i

Taxonomic Index A

Beroe cucumia, 266,603, 504, 506, 506 gracilia, 266 ovata, 266 Biddulphia, 338, 348, 350, 361 &inesia, 57, 337, 349, 436 Blastodinium, 192, 193 contortum, 190 contortum hyalinum, 190 hyalinum, 190, 191, 193, 194 Bolinopsia, 260,251,258,261,264,266,

Acanthaphyra exirnia, 501, 502, 506, 608 purpurea, 316 Acartia, 17, 100, 268, 271, 352, 353, 465, 457

centropages, 506 clausi, 352, 368, 501, 502, 506, 506, 507

longiremis, 459 tonaa, 46, 48, 59, 100, 279, 449, 464 Aequorea, 268 Actidius armatus, 17 Aglantha digitale, 160, 207, 507 Agmenellum, 321, 322, 325, 326 quadruplicatum, 321, 322, 326, 326,

267, 271, 273, 275, 276, 279

infundibulum, 208, 266 mioroptera, 208 Boreogadus aaida, 204 Brachiomonas &marina,

401,

483,

487, 496 Brachionw, 506

330

Alphaeua, 239 Ammodyb, 205 lanceolatua, 205 per8onatus, 205 tobianua, 205 Amphidinium, 78 mrterae, 324. 401, 411, 479, 485, 488, 491

Amphora, 325, 326 Anomdocera, 603, 504, 506, 506, 507 patersoni, 17, 295 Aplyeia, 241 Artemia, 236, 432, 433 Asterionella glacialis, 481, 488, 492, 496, 497 japonka, 481, 488, 496, 497 Attheya decora, 401, 481, 486, 492, 497

0 Balanus, 241 amphitrite, 447 amphitrite niueus, 354 Belone belone, 463, 454, 457 Beroe, 250,251,261, 262,265, 266, 267, 271, 276, 279

C Calanipeda, 606 Calanua, 3, 8, 11, 18, 62, 63, 54, 67, 81, 84,85, 197, 202, 205,206, 209, 264, 266, 311, 337, 338, 360, 351, 436, 449, 469, 502, 505, 507 claUSii, 5, 6 crktatua, 507 jinmarchioue, 3, 17,46,197,312,348, 503, 604, 505, 506, 507 glacialis, 312 gracilis, 17 helgolandicus, 17, 126, 167, 199, 313, 317, 336, 337, 338, 339, 340, 341, 342, 343, 344, 348, 349, 353, 366, 359,436, 503, 504,506, 506, 507 hyperboreus, 17, 311, 312, 336, 337, 354,359 minor, 17 minuua, 4, 7 pacificua, 436 plumchrus, 201, 335, 336, 337, 343, 448, 449,469, 607 Callianira, 269, 261 Ca&uxtee aapidue, 366 608

610

TAXONOMIU INDEX

Cancer magister, 345, 355, 360 productus, 353, 368, 359 Candacia armata, 17, 312 ethiopica, 429 Carcinus maenas, 455 Cardiapoda, 268 Carinaria lamarcl~i,429 Carteria, 389, 483 Cavolinia injlexa, 429 Centropages, 100, 208, 352 bradyi, 17 hamatus, 17, 46, 503, 504, 505, 506 ponticus, 352, 358 typicus, 17, 100, 503, 504, 505, 506 Cerataulina bergonii, 333, 334 pelagica, 333 Ceratium, 59 Cestum veneris, 266 Chaetoceros, 68, 59, 67, 68, 323, 419,

Coccochloria, 325, 326 elabem, 325, 401, 491 Cocwlithophwus huxleyi, 69, 61 Coccolithus huxleyi, 308, 479, 491, 496, 497

Conchoecia, 3 12 Contracaecum, 197, 198 aduncum, 198 Corycaeus, 17 Coacinodiscus, 58 granii, 419, 489 Crangon, 50 Craasostrea gigas, 452, 464 Cricosphaera carterae, 324 elongata, 485, 488, 491 Cryptomonas, 308 pseudobaltica, 401, 479, 485, 488, 491 Cuvierina columnella, 429 Cyanea capillata, 503, 504, 605, 506 Cyclosalpa pinrmta, 429 Cyclotella caapica, 59, 61 menenghiniana, 384, 392 rmna, 308, 309, 401, 420, 482, 484,

420

costatum, 384 debilis, 59 didymus, 401, 481, 486, 488, 493 galvestonensis, 481, 484, 486, 487 socialis, 59 Chironex, 238 Chlamydomonas, 78, 320, 483, 484 angulosa, 327, 328, 330 coccoides, 78 palla, 401, 483, 487, 490, 495 Chlorella, 78, 321, 322, 325 autrophica, 321, 322, 325 pyrenoidosa, 404, 412, 414 stigmatophora, 7 8 vulgaris, 307, 321, 325, 330, 414 Chrysaora, 267 Chrysochromulina kappa, 333 Clausia, 3, 4 elongata, 5 Clausocalanus, 606 Clione, 508 limacina, 503, 604, 506 Clupea harengus, 202 harengus membras, 361 harengus pallasi, 202 pallasi, 36 1

486, 487, 494

Cylin,drotheca, 325, 326 closterium, 389, 401, 419, 420, 481, 486, 489, 493, 497

Cyphocaris challengeri, 336 Cystoseira barbah, 15, 16 Cytotehya cmjpa, 242

D

.

Derbesia tenuissima, 309 Dicrateria inornata, 78 Disodinium lunula, 194 pseudocalani, 194, 195, 196 Ditylum, 319 brightwelli, 308, 319, 413, 486, 489 Dunaliella, 323, 324, 326 bioculatu, 483, 487, 490, 496 euchlora, 484 primolecta, 487, 490, 495 tertiolectu, 18, 309, 321,323, 324, 326, 385, 387, 388, 389, 400, 401, 413, 483, 484, 487, 490, 495, 491

511

TAXONOMIO INDEX

E Echinurachia, 241 Ellobiopaia, 196 chttoni, 196, 197 Emiliania hwleyi, 479 Elminius modestus, 343, 440 Engraulia mordux, 361 Epilabidocera, 264 E u a l w suckleyi, 355, 359 EUGbetiJ acuta, 17

hebea, 17 n o r v e g k , 58 Eucalrnw buqii, 31 3, 507 EUG-

japonica, 314,315,336,343,356,357, 360, 451, 452

marina, 429, 507 Euchirella rostrata, 3 12 aplendena, 429 Eucopia, 501 aculpticauda, 502, 506 Eunicella, 245 E ~ p h & , 502, 505, 507 krohnii, 503, 504, 505, 506 paci$ca, 206,430, 438,441, 442, 460, 501, 502, 503, 504, 505, 507

similia, 507 E u r h m p h a m , 261. 262 vedligera, 263 Eurytemora, 357 afinia, 339, 340, 341, 342, 354, 355, 357, 359, 360

herdmani, 84 Euterpina, 437 acuti,frons, 437, 439 Eutrepiella, 308 Evadne tergestina, 507 Exuuiaella, 401, 491 baltica, 59 cwdatu, 59 mariaelebouriae, 401, 419, 485, 488, 491

F Fragilaria, 323, 327 P;nmta, 401, 481, 486, 489, 493

Gadw, 205 callarias, 203 morhwt, 203, 361 Cammarus, 50 G e n d a s elegana, 502, 505, 508 Glenodinium, 322, 491 foliaceum, 401, 491

Mk&322 Gtaathophawk, 31 5 Conkulax, 238, 241 polyedra, 308 tarmarensis, 115 Gymnodiniurn, 196 halli, 321 kowalevskii, 71, 76 splendens, 308, 401, 436, 480 veneficum, 78 vitiligo, 78 Gyrodin,iumJissum, 485

H Halinaeda, 263 Haliotis, 245 Helicostomella subulata, 333, 334 Hemiselmis virescens, 78 Hemiurua, 197 appendiculatus, 197 Heterocapsa tripuetra, 59 Heterothrix, 401, 481, 485, 488, 492 Homarus amerimnus, 353, 356, 358 Homiphora, 259 plumosa, 261 Hymenomonas carterae, 305, 324 elongata, 485, 488, 491 Hyperoche, 268 Hyperoplus lanceolatus, 205

I Isiaa clavipes, 17 Iaochryak, 69, 78, 114 galbana, 65, 66, 67, 68, 77, 78, 80, 81, 86, 88, 90, 110, 112, 113, 114, 115, 129, 308, 384, 385, 387, 388, 401, 403, 405, 406, 407, 408, 409, 410, 413, 414, 427, 480, 485, 492, 497

612

TAXONOBUO INDEX

L Labidocera acutifrone, 461, 501, 502, 506 wollaatoni, 17 Lauderia borealis, 66, 67. 68, 77, 308, 401,436,481, 4 8 6 , 4 8 9 , 4 9 3 Leiostomus xanthurua, 457 Lewotheu, 250, 261 multkornia, 262 ochracea, 262 Leuckartia octona, 207 Lamacina retroversa, 312, 503, 504, 505, 506 trochqormia, 508 Gmanda limanda, 206 Limulus, 241 Loligo, 240 Lophius, 240 Lucifer reymudii, 508 Lucullua aouapea, 5, 6 kmbrinereia brewicirra, 242

M M a h a 246 , Mallotua villoaus, 361 Meganyctiphnea norvegica, 312. 348, 431, 432, 435, 439, 440, 442, 444, 445, 501, 502, 505, 506, 507 Melanogrammua aeglesnua, 204 Meloaira, 3 19 monil$ormia, 3 19 Mercenaria, 241, 355, 358, 359 Merlangiua merlangus, 204 M e r l k u a merlucciua, 205 Metridia, 449 longa, 17, 312 lwena, 17, 312 pacijca, 448, 449 Mnemiopais, 250, 251, 252, 255, 258, 259, 261, 262, 263, 264, 267, 268, 269, 270, 271, 272, 273, 274, 275, 276,279 leidyi, 264, 269, 271, 273, 275, 279 mccradyi, 251, 255, 257, 263, 267, 269,270,271, 2 7 4 , 2 7 8 , 4 5 9 Molva molva, 206 M m l h n t u a aalina, 401, 481,485, 488, 492

Monochryaia, 323 lutheri, 329, 383, 401, 481, 484,485, 488,492,497 My&, 50 Mytilua galloprovincialia, 463 Myxine, 241

N Nannochloris atomue, 495 oculata, 383 Navimla diatana, 420 pelliculosa, 424 Nematobrachion aexspinoaia, 315 Nenzatoacelia megalopa, 312 Neocalanus gracilia, 429 Neomyaia, 507 Nereia diversicolor, 245 Nitzachicc, 307, 322 dba, 307 cloaterium, 319, 389, 401, 419, 420, 481,493, 497 delicatiaima, 420 gotlandica, 78 Noatoc,'321

0 Obelia, 207 Ochrvmonas, 333 Ocyropsis, 261, 262 Oithona, 67, 208, 265, 352, 353 nana, 352, 358, 507 similia, 46, 58 O~~sthodisczce luteue, 401, 492 Ommaatrephea ih'icebroaa, 503, 504, 506, 506 Oncorhynchua gwbuachia, 201, 360, 361 keta, 201 Onkimua, 354 a@nia, 354, 359 Oplophorua, 461, 502, 506, 508 OacillatOria woronichinii, 307, 308 OX.ymphalu8,268

TAXONOMIa INDEX

P Pal5emonetes vulgaris, 450, 453, 454 Pandolus, 345 platyceros, 344, 345, 355, 360 Paraoalanua, 16, 17, 18, 19, 20, 57, 204, 207, 352, 449, 506

pamrvus, 57, 352, 358, 459 Paracentrotua livvidus, 452 Paralithodea camtachatica, 355, 359 Para-Pseudomlanua, 16, 127 Paraaagitto elegam, 206 Pamthemiato gaudichhadii, 312 o b l i a , 507 pacism, 336, 343 Pareucbta, 507 nurvqica, 17, 312 Pavlova lutheri, 329, 383, 401, 481, 484, 485, 488, 492, 497

phgui.4, 401, 481, 485, 488, 492 Pelagia, 501, 502, 506, 507 Penilia, 352 avirostrb, 352, 358 schmaokeri, 507 Peprilia, 288 PeMinium trochoideum, 75, 76, 92, 93, 308

Ph&nna spinifera, 5 Phaeocyatis, 395 p w h e t i i , 308 Phaeodccolylum, 320 Wbrnutum, 78, 320, 321, 332, 384, 386, 387, 388, 389, 390, 391, 392, 394, 400, 411, 412, 413, 481, 484, 486, 487, 489, 493, 496, 497 Phialidium, 207 Phrosina semilunatca, 461, 502, 505, 507 Phymlia, 241 PEdymonas, 110 szcecica, 353, 437, 438 eubcordifomis, 490 virb%, 76 Pleurobmhia, 250, 251, 255, 259, 261, 262, 263, 264, 265, 266, 267, 268, 269, 270, 271, 272, 273, 274, 275, 270, 277, 278, 279, 281 bmhei, 207, 208, 269, 268, 209, 270. 272, 273, 274, 276, 278, 459

613

Pleurobrachio pileua, 207, 208, 266, 274, 343, 459, 503, 504, 505, 506, 507

Pleuromamma abdominalis, 17, 429 borealis, 17 grmilis, 17 robusta, 17, 312 xiphias, 46, 429

Pleuronectes platessa, 205 Pontella, 503, 504, 505, 506, 507 Porphyra, 237 Porphyl-idium, 308 marinurn, 401, 479, 485, 488. 491 Praainocladua marinus, 401, 483, 487, 490,495

Prorocentmm, 401 micam, 71, 73, 401, 480, 488 minimum, 401, 479 Protocowus, 484 Protothem zop$i, 328 Psetta maxima, 206 Pseudocalanus, 3, 4, 6, 7, 8, 9, 10, 11, 12, 13, 14, 15, 16, 17, 18, 19, 20, 21, 22, 23, 24, 25, 26, 27, 28, 29, 30, 31,32, 33, 34,35,36,37, 38,39, 40,41,42,43,44,45,46,47,48,49, 50, 51,52,53,54,55, 56,57,58,59, 60, 61, 62, 63,64, 65, 66, 67, 68, 70, 71, 72, 73, 74, 75, 76, 77, 78,79,80, 81,82,83,84,85,86,87,88,89,90, 91, 92,93, 97,98,99, 100,101,102, 103, 105, 106, 107, 108, 109, 110, 111, 113, 114, 115, 116, 117, 119, 120, 121, 122, 123, 124, 125, 126, 127, 128, 129, 130, 132, 133, 134, 135, 136, 137, 138, 139, 140, 141, 142, 143, 144, 145, 146, 147, 148, 149, 150, 151, 152, 153, 154, 155, 156, 157, 158, 159, 160, 161, 162, 163, 164, 165, 166, 167, 168, 169, 170, 172, 173, 174, 175, 176, 177, 178, 179, 180, 181, 182, 183, 184, 185, 186, 187, 188, 189, 190, 191, 192, 193, 194, 195, 196, 197, 198, 199, 200, 201, 202, 203, 204, 206. 206, 207, 208, 209, 210, 264, 265, 335,459 awpes, 5 clauaii, 5, 6

514

TAXONOMIO MDEX

Pseudocalanua elongcatus, 3, 5, 6, 7, 8, 27, 113, 152, 153, 502, 504, 505, 507 gracilis, 6, 7, 8, 152 major, 5, 7 minutus, 4, 6, 7, 8, 62, 152, 153, 333 minutus elongatus, 7, 8 minutus gracilis, 7 minutus major, 7, 8 minutus minutus, 7 Pterosperma, 243 Pterotrachea, 268 Pyrosoma, 501, 502, 506, 508 verticillatum, 429

R Rathkea octopunctata, 207 Rhincalanus w u t w r , 17,311,312,313, 314

Rhithropampeus harriaii, 452, 453, 454

Rhizosolenia dda, 419 setisera, 306, 308 R h o d o m o w , 308 Rhmnbw maeoticw, 361

Sardina pilchardus, 203 Sargaasum, 247 Sarah tubulosa, 207 Scomber scombrua, 202 Scrippsiella faeroeme, 401, 413, 480, 488

Sergestes, 502, 505, 508 Skeletonema, 59, 66, 67, 68, 305, 313, 323, 324

coatatum, 59, 75, 305, 306, 308, 320, 322, 324, 383, 389, 401, 411, 425, 438, 441, 482, 486, 489, 493, 497

Spiratella retroversa, 503, 504, 505, 506 trochifmmia, 508 S p t u l a solidissim, 447 Sporodinium pseudocalani, 194, 196 Sprattus sprattus, 203 Squalua acanthias, 241 Synechococcus bacillaris, 307, 308 Syracosphaera, 305 carterae, 305 Syatellaapis debilis, 461, 501, 502, 500, 508

T Temora, 100, 204, 206, 207, 208, 265, 449,457

S

longicmnis, 3, 17, 44, 46, 47, 48, 49, 60, 348

Sagitfa, 279, 501, 502, 505, 506, 508 bipunctata, 508 elegans, 160, 167, 175, 206, 207, 312, 503, 504, 505, 506, 508

enJEata, 429 euxina, 503, 504, 505. 506, 508 hexaptera, 429 hispida, 278, 448 minima, 508 pacifica, 508 robusta, 508 s e m a , 206, 207, 503, 504, 505, 506, 508

Sdpa cylindrica, 429 fuaqormis, 429, 503, 504, 505, 506, 508

Sapphirim, 17

Teredo, 238 Tetraodon, 241 Tetraaelmt, 400, 487, 490, 495 striata, 401, 483, 487, 490, 495 Thalmsiosira, 58, 67, 308, 321, 322, 420

jueriatilis, 65, 66, 67, 68, 70, 300, 308, 401, 494

p s e u d m n a , 309, 321, 322, 392, 393, 401, 403, 407, 408, 411, 413, 415, 420, 425, 427, 482, 484, 486, 487, 489, 494, 497 rotula, 66, 68, 81, 92, 93, 113, 133, 134 Thalia democratica, 274 Themisto japonha, 507 Thynnaecaris, 198 aduncum, 198

616

TAXONOMIO INDEX

Thyeanmeasa, 607 inerrnis, 206 longipes, 206 raschii, 507 spinqera, 442, 501, 602, 504, 505, 507 Thyeanopoda triouspidata, 429 Tigriopus, 353 cali,fornicus, 352, 358 japonicua, 451, 462, 463, 460 Tinerfe, 259 Tomopteris, 267 Tortanwr disoaudatua, 46

Tribonema cceqwsle, 308 Turris pileata, 207

U Uca pugilator, 447, 455, 456 Ulva regida, 15, 76 Undinula vulgaris, 448 Uronema marinum, 75-76

v Vallicula, 261, 263 Vibilia gibboea, 607


Subject Index A Abdomen, Pseudocalanus, 30, 31, 33, 34

Abundance, Pseudocalanua, 17-18 long-term changes, 19-20 peaks, 146, 152 seasonal fluctuations, 18-19 temporal variations, 18-20 year-to-year changes, 19-20 Acclimation, Pseudocalanus, 41 Acenaphthenes, 301 Achlorophyllous algae, 328 Adenosine triphosphate (ATP), 64 Adriatic Sea Pseudocalanus in, 14, 25, 111, 119, 154, 167

mineral oil hydrocarbon levels in,

Adult Pseudomlanua-coalirrued light response, 173 longevity, 114, 116, 117 nitrogen content, 126 oil sac, 128, 129 respiration, 43 seasonal migration, 162 sex ratios, 80, 81 somite arrangement, 31-34 vertical distribution, 161 weight-length relationship, 127 Aequorin, 241 Aesthetes, Pseudocalanus, 34, 85 African northwest coast, 501, 502, 504, 505, 506, 508

Air-sea interface, hydrocarbons at, 296 Alaska, 197 Aleutians, Pseudocalanus at, 16

&=

296, 299, 357

zooplankton in, 461, 501 Adult Mnemiopia digestion time, 255 feeding mechanism, 252, 253 ingestion rate, 270 prey capture, 252, 253, 254, 256 starvation, 255, 258 swimming action, 255, 257, 258 tentacle setting, 252, 253, 255, 256,

n-alkane distribution in, 291, 303 aromatic hydrocarbon metabolization. 327, 328 carbohydrate, 330 chemical composition, hydrocarbon effects on, 330 growth inhibition, naphthalene by, 327, 328

growth rate stimulation, 324, 326,

267

326

Adult Paeudocalanua appendages, 34-37 ash-free dry weights, 123 body size-food supply relationship, 123

body size-water temperature relationship, 115-122 carbon content, 126, 126 die1 vertical migration, 166, 167, 169, 170, 171, 172

excretion rate, 46, 48 feeding rhythm, 74 generations, 143 growth rate, 131 gut contents, 74 617

multicellular, 75 naphthalene metabolism, 327, 328 photosynthesis mechanism disruption, hydrocarbons by, 329 pristane in, 291 protein, 330 Pseudocalanus gut content, 60 quality, Pseudocalanus food, as, 77 radiocarbon tagging, 184 A l m c acid, 242, 247 Alimentary canal, Pseudocalanus,dinoflagellate parasitic infection, 191 Alkanes ah-see, interface, at, 26 crude oil, in, 304

'

518

SUBJECT INDEX

Alkanes-continued oil tanker routes, in, 299, 300, 301 sea water, in, 291-292 sediments, in, 294 water-soluble fraction (WSF) of oil, in, 318 iso-Alkanes, 291, 302, 318 n-Alkanes, 291, 297, 299, 302, 303, 322, 323 biosynthesis mechanism, phytoplankton by, 305, 307 (C14t o C,,), 298, 303 (Cis t o Cm), 297 (Czd t o C,,), 305 coastal waters, in, 291, 292, 294 dissolved, 298 particulate, 298 surface micro-layer, in, 294, 295, 296 surface waters, in, 294, 295 unicellular algae, in, 305, 307, 308309 water-soluble fraction of oil, in, 318 Alkenes, highly conjugated, 293 Alkylbenzenes, 325, 354 Alkylnaphthalenes, 325, 354 lethal concentrations, 354 All-cis-3,6, 9, 12, 15, 18-heneicosahexarene (HEH), 306 Allergy phenomenon, 241 American lobster, 353, 355 Amino acids, 44 assay, Pseudocalanus, in, 125 Ammonia excretion, ctenophores, 273 Ammonia excretion, Pseudocalanus, see Nitrogen excretion, Pseudocalanus Ammonium ion uptake, phytoplankton, 423 Amphipods, 268,311,312,337,343,354 arsenic content, 506 cadmium content, 461, 502 copper content, 505 zinc content, 507 Amplitude of migration, Paeudocalanw, 166, 167 Anaktdik Bay, Labrador, 140, 159 Analgesics, 241 Anaphyllaxis, 241 Androgen hydroxylase, 356 Anemones, 263 Angler fish, 240

Anilines, 325 Annelid worms, 267 Annual life cycle, Pseudocalanus, 18, 138, 139, 141, 152, 153, 156 Annual production, ctenophores, 278 Antagonism, heavy metal phytoplankton growth rate relationship, 411-412 zooplankton growth rate relationship, 454 Antarctic penguins, 244 Antennae, Pseudocalanus, 34-36 first antenna, 34-36, 85 second antenna, 35, 36 swimming, function in, 52 Antibiotics, 77, 241, 242 Anti-cancer drugs, 241 Antifouling paints, 238, 382, 400 Anti-leucaemia drugs, 242 Appendages, Pseudocalanus, 31, 32, 34-37 first antenna, 34-36 first maxilla, 35, 36 mandible, 35, 36 maxilliped, 35, 36 second antenna, 36 second maxilla, 35, 36 structure, 34 thoracic, 37 Arctic Basin, Pseudocalanus, in, 8, 12, 13 Arctic Ocean climatic changes, 243 oil pollution, 364 Pseudocalanw in, 21, 141 zooplankton in, 337 Ariake-kai, Japan, 498, 501, 502 Aristotle, 233 Aromatic hydrocarbon metabolism, zooplankton, 342-348 carcinogen potential, 347 enzymes involved, 345, 347 mechanism, 346, 347 Aromatic hydrocarbons, 293, 322, 323 biosynthesis, phytoplankton by, 307, 308, 309 coastal waters, in, 303 crude oil, in, 304 depth concentrations, 296 faecal pellet release in, 348-351

519

SUBJEUT INDEX

Aromatic hydrocarbons-continued hydroxylation, zooplankton by, 343, 345 metabolism, copepods by, 343, 344 metabolism, phytoplankton by, 327, 328 oil tanker routes, in, 300, 301 phytotoxicity-molecular structure relationship, 330 sediments, in, 294 surface concentrations, 296 toxicity, zooplankton to, 354 water-soluble fraction of oil, in, 318 Aromatic pesticides, 346 “ Arrow ”, oil tanker, 293, 348 Arsenic content, zooplankton, 460,461, 506 Arthropods, 3 1 Artificial blood vessels, 241 Artificial fibres, 242 Aryl-hydrocarbon hydroxylase (AHH), 345, 346, 356 Ash-free dry weights, ctenophore, 269 production estimates from, 278 Ash-free dry weights, Pseudocalanus, 123, 124, 125, 130, 133 Assimilation efficiency, zooplankton, 350 Assouan Dam, 247 Atlantic cod, 203-204 herring, 202 mackerel, 202 Atlantic Ocean copepods in, 461 ctenophores in, 251 decapods in, 461 hydrocarbon levels in, 294, 296, 301, 348 phytoplankton populations in, 500 plankton in, 460, 461 Pseudocalanus in, 13, 14, 16, 18, 20, 152, 202 zooplankton in, 501, 502, 503, 504, 605, 506, 507, 608 Auxins, 322 Azores, Pseudocalanus off, 15

B Bacillariophyceae, 306, 308 Bacteria, hydrocarbon degradation, 328, 343 Bacterial surfaces, 384 Baffin Bay, Texas, hydrocarbon levels in, 293, 298 Baffin Island, Pseudocalanus at, 87, 96, 128 Bahamas, 499, 500 Baie-des Chaleurs, Gulf of St.. Lawrence, Pseudocalanwr in, 8, 16, 19, 152-153 Baja California heavy metal coriceiitration at, 396 phytoplankton populations at, 426, 498, 499, 500 Bakers’ yeast, 412 “ Balance equation ” of growth, zooplankton, 132, 134, 181, 199 Baltic garpike larvae, 454 Baltic Sea mercury pollution, 244 non-polar hydrocarbon levels in, 292, 297 Pseudocalanus in, 14, 21, 25, 156, 187, 208 sprat in, 203 Barents Sea Pseudocalanus in, 8, 16, 18, 167 zooplankton in, 506 Barnacles, 382 larvae, 440, 446 nauplii, 264, 343, 354 planktonic cyprids, 447 Batch culture, phytoplankton, 398 Bathing beaches, pollution, 243 “ Bathyplmkton ”, 209 Baton Rouge, Louisiana, 324 Bay of Biscay, Pseudocalanus in, 14 Bay of Fundy, 153, 202 Bay of Villefranche, 307 Baytown, Texa.s, 324, 325, 326 Beam-trawling, 235 Beaufort, North Carolina, Pseudocakznus at, 14, 279 Bedford Basin, Nova Scotia oil pollution, 320 phytoplankton in, 320

620

SUBJEOT INDEX

Bedford Basin,Nova Scotia-continued P a e u d ~ n w in, r 61, 169, 170, 171, 173, 175, 179, 206 Behaviour, Mnemiopeia, 251-259 B61ehrAdek’s temperature function, 100,101,119 development stages, and, 107, 108 embryonic duration, and, 99, 101, 102, 103 physiological rate response, and, 101 Benthic ctenophores, 250 Benthos, hydrocarbon transfer to, 348 Benzenes, 300, 301, 304, 317, 318, 322, 324, 325, 330, 361 Benzo[a]pyrene (BP), 304, 307, 335 carcinogenic activity, 347 metabolism, zooplankton by, 343, 345, 346, 356 retention, zooplankton by, 335, 336, 337 Benzothiophenes, 301 Bergen, Norway, 150 Bering Sea, Pseudocalanw in, 15, 16, 18, 20, 21, 68 Bermuda, 15 Beroida, 250, 266 feeding mechanism, 266, 267 food, 266, 267 population dynamics, 267 regenerative powers, 275 Bicyclic aromatic hydrocarbons, 302, 303, 317 Billings, Montana, 324, 325, 326 Bimini, Bahamas, 258 Bimodal depth distribution, Paeudocalanwr, 159 Bimodal size, Paeudomlanue, 140, 141, 161 Biogeochemistry, heavy metals, 395398, 440-446 Biological accumulation, heavy metals, 397 Biological function, naturally occurring hydrocarbons, 316 Biological origin, hydrocarbons, 296 Biology, Paeudocalanue, 2 et aeq. Biomass production ctenophores, 274, 277, 278, 279, 280 Paeudocdznua, I86 Biosynthesis, phytoplankton

Biosynthesis phytoplankton -continued n-alkanes, of, 305, 307 aromatic hydrocarbons, of, 307, 308, 309 Biphenyls, 304, 318 Biscayne Bay, Florida ctenophores in, 267, 278, 280, 281 zooplankton in, 268 Bitter Lakes, 247 Bivalve molluscs, 342 Black Sea chaetognaths in, 207 diatoms in, 462, 499, 500 multicellular algae in, 331 ‘‘ neritic zone ”, 183 oil pollution, 244, 319, 362 pelagic food web, 209 phytoplankton in, 319 pilchard in, 203 Pseudocalanus in, 14-15, 16, 20, 21, 24, 42, 59, 60, 71, 74, 75, 89, 91, 93, 111, 119, 127, 154, 158, 161, 162, 164, 166, 166, 183,186, 188, 199, 203, 207 sprat in, 203 whiting in, 204 zooplankton in, 603, 504, 506, 506, 507, 508 Block Island Sound, 153 Blood-brain barrier, 241 Blue crab, 356 Blue-green algae, 307, 326 Bluefin tuna, 268 Body, Paeudocalanue, 29, 30, 31, 34 Body composition, Paeudocahnwr, 124128 calori6c content, 125 carbon content, 125 elemental composition, 125-127 hydrogen content, 127 lipid content, 125 nitrogen content, 126 phosphorus content, 126, 127 protein composition, 125 silica content, 127 Body diameter, ctenophores, 273 Body proteins, Paeudocalanw, 125 Body size, Peeudocalanua daily food ration relationship, 72

521

SUBJECT INDEX

Body size, Pseudocakanw-continued die1 vertical migration relationship, 177 DNA relationship, 124 dry weight, 124 egg production relationship, 86, 88, 89,90 embryonic development rate relationship, 103-107 food ingestion rate relationship, 67 food size selection relationship, 63 food supply relationship, 116, 122123 genetic variation, 123-124 laboratory data, 119-124 latitude area relationship, 118 nitrogen excretion rate relationship, 60 phosphorus excretion rate relationship, 60 respiration rate relationship, 38-40, 41 seasonal variation, 66, 102, 103, 116, 117, 118, 119 somatic production estimates from, 180 thermal regime relationship, 118,119 water temperature relationship, 116122, 123-124, 131, 147 weight-length relationship, 127-1 28 wet weight, 124 Body weight, PeewZocalanua, 124-1 28 dry weight, 124 egg weight, 128 length-weight relationship, 127-128 wet weight, 124 Bonin Ridge, 15 Boothbay Harbour, Maine, 173 “ Boreal ” zooplankton, respiration rate, 39 Bornholrn Deep, Baltic, 203 Bovine serum albumin (BSA), 346,366 Bras d’Or Lake, Nova Scotia, Pseudomhnw in, 44,49, 60 Brest Harbour, hydrocarbon levels in, 299, 302, 303 Brine shrimp, 236 British Columbian waters herring in, 202 Pseudwabnua in. 16. 202

British Columbian waters--continued tentaculata in, 269 zooplankton in, 337 British Isles fishing restrictions, 234 marine conservation meas, 246 Pseudocalanua around, 17, 20, 207 British Subaqua Club, 245 British Waters n-alkane levels in, 292 definition, 234 Brittany coast, oil pollution, 243 Broods, Pseudocabnus, 136 maturation, 139, 140 production rate, 138 synchronous, 136 Brown algae, heavy metal tolerance, 400 Brown seaweed, 242, 247 Bunker C oil, 293, 318, 348 water-soluble fraction (WSF), 369 Bunker fuel oil F-12,352, 368 Buttefish, 268

C l4C uptake technique, phytoplankton photosynthetic rate measurement by, 416, 416 Cadmium turnover, zooplankton, 431,

432, 433, 434, 439, 461, 462, 463, 498, 602 egg hatching, effect on, 461 growth and development, effect on, 462 oxygen consumption, effect on, 447 swimming rate, effect on, 466 Cadmium uptake, phytoplankton, 387, 389,395,397,424,486-4a7 concentration-growth rate relationship, 407, 408 primary production, effect on, 417, 418 Calanoid copepods itntennae, 34 buoyancy, 316 dinoflagellate parasitic infection, 191 escape reaction, 63 feeding type classification, 66 monograph On, 7 nauplii, 452 Dredation. ctenoahores bv, 264

522

SUBJEUT INDEX

Calanoid copepods--continued pristane biosynthesis, 311, 316 sex ratio, 315 swimming pattern, 51, 52 water-soluble fraction (WSF) of oil toxic effects on, 354 Calcium alginate, 242 luminescent reaction triggering by, 240

California Current, Psewfocalanw in, 13

California-Hawaii transect, Eastern Pacific Ocean, 426 Californian coast ctenophores off, 268, 278 Pseudocalanw off, 15, 126 zooplankton off, 337 Calorific content, Pseudocalanus, 126 Camouflage material, 242 Canada, eaatern, Pseudocalanus off, 14 Canadian arctic, Pseudocalanwin, 8, 9,

Cell division, phytoplankton, 319, 327, 413, 414

Cell-growth inhibitors, 241 Cell membranes, multicellular algae, 329

Cell populations, phytoplankton heavy m0tal toxicity relationship 403-404, 405, 414

normal size distribution, 414 Cell size, Pseudocalanw, 123, 124 Cell surface, phytoplankton binding sites, 384, 387, 388, 389,404, 408

diffusion-controlled heavy metal ion uptake, 365, 386 extracellular binding sites, 387, 390 mercury binding capacity, 387 physico-chemical nature, 384 Cells, phytoplankton division inhibition, 413, 414 giant, 413-415 heavy metal tolerance changes, 4 0 6

24, 87, 118, 119, 127, 136-138

Cape Cod, Massachusetts, Pseudocalanus at, 40, 70, 153 Cape Cod Canal, Pseudocalanw in, 24 Cape Hatteras, Pseudocalanus at, 14 Carageen, 242 Carbon preference index, 306 uptake, ctenophores, 269, 210 uptake, phytoplankton, 424 Carbon content, Pseudomlanw, 126, 126

production estimates from, 182, 183, 184

Carcasses, zooplankton, heavy metal transfer in, 440 Caribbean Sea, non-polar hydrocarbon levels in, 292 Caribbean sponge, 242 Cariaco Trench, non-polar hydrocarbon levels in, 292, 297 Carmine, 263 Caspian Sea oil pollution, 244 phytoplankton populations, 417,418 polychaete worms in, 247 Crryley, Sir George, 239

406

heavy metal uptake, 403, 404, 406, 408

membrane permeability, 412-413 metabolic activity, 406 methionine production, 414 morphological abnormalities, 413 volume variations, 414 Celtic Sea, 206 n-alkane levels in, 292, 297 Centric diatoms, 306, 419, 420, 421 copper tolerance, 423 Cephalosome, Pseudocalanw, 29,30,31 Cephalothorax, Peeudocalanw, 8, 38, 86

body size, relation to, 127 egg clutch size. relation to, 86, 87 egg diameter, relation to, 103, 106 female lengths, 10, 86, 103, 115, 122 genetic size variation, 123, 124 size-food supply relationship, 122, 123

size-water temperature relationship, 115,119,120

viable egg " production, relation to, 94 cerium, 440 "

SUBJEOT INDEX

Cestida, 250 swimming action, 262 Chaetognaths, 206, 279 arsenic content, 506 cadmium content, 502 chromium content, 506 copper content, 459, 506 digestive efficiency, 271 heavy metal turnover, 429, 430 lead content, 504 nickel content, 503 pristane biosynthesis, 3 11, 312 production estimates, 278, 282 silver content, 503 zinc content, 508 Channel Islands, 245 Charles River, Boston, 300 Chedabucto Bay, Nova Scotia, hydrocarbon levels in, 298, 299 Chelating agents, 387, 392, 394, 400, 439, 451

Chemical analysis, petroleum hydrocarbons, 362 Chemical composition, ctenophores, 269

Chemical stratification, Irish Sea, 22 Chesapeake Bay, Maryland phytoplankton populations in, 498 Pseudocalanua in, 12 Chlorohydrocarbons, 346 Chlorophyceae, 306, 307, 309 Chlorophyle, 74, 119, 294, 311, 321 food index, as, 122 vertical migration of Pseudocalanus, effect on, 160, 161, 167 Chlorophyta chlorophyceae cadmium effect on, 487 chromium effect on, 496 copper effect on, 495 lead effect on, 490 mercury effect on, 483 organic mercury compounds, effect on, 484 zinc effect on, 497 Chlorophyla Prasinophyceae cadmium effect on, 487 copper effect on, 495 lead effect on, 490 mercury effect on, 483 Chlorophytes, 78

523

Cholesterol, 356 Christiana (Oslo) Fjsrd, 5 Chromium turnover, zooplankton, 500, 506 uptake, phytoplankton, 427, 496 Chromosomes, Pseudocalanua, 9, 10 Chrysomonads, 66 Chrysophytes, 59, 78 amino acid content, 78 Chukchi Sea, Pseudocalanus in, 13 Chum, 201 Circumpolar current, heavy metal concentration in, 396 Cladocerans, 264 Clams, 241 zinc content, 607 Clarke-Bumpus sampler, 22, 169 Classification, ctenophores, 250 Climate, short term changes, 243 Clyde River hydrocarbon levels in, 296 plankton in, 315 Cnidaria, 263 Coastal waters n-alkane levels in, 291, 292, 294 heavy metal levels in, 382, 396 hydrocarbon levels in, 291, 302, 303 Pseudocalanzlr, in, 16 Cobalt surface layers, removal from, 443 up take, phytoplankton, 397 Cobalt turnover, zooplankton, 429,430 daily turnover, 430 phototactic response, effect on, 465 Cocaine, 241 Coccolithophorids, 58 life history, 243 Cod, 235, 240 diet, 203-204, 268 Coelenterata arsenic content, 506 cadmium content, 502 chromium content, 506 copper content, 505 lead content, 504 mercury content, 501 nickel content,, 603 zinc content, 507 Coelenterata Hydrozoa, zinc content, 507

624

SUBJEOT INDBX

Collection methods, ctenophores, 260 Colloblaat filaments, Mmmiopsi8,253 Common barnacle, 241 Common dab, 206 Comprehensiveanalyses, hydrocarbons in sea water, 300-303 Conservation, marine, 245-247 Conservation Reserves, 246 Continuous culture, phytoplankton, 399 Continuous-flow systems, oil toxicity investigations in, 355, 356, 363 Continuous Plankton Recorder surveys, 14, 10, 17, 18 Controlled Ecosystem Pollution Experiments (CEPEX) 331-335,419, 424,458 Cook Inlet crude oil, 359 Cook Islands, 246 Coos Bay, Oregon, 498 Copepod Calanus, 3 abundance, 18 ctenophore destruction by, 208 egg laying, 81 faecal pellets, 348, 353, 449 feeding current, 54 feeding rate, 436 feeding rate inhibition, crude oil by, 353 feeding rate inhibition, heavy metals by, 448, 449, 459 grazing rate, 436 heavy metal uptake, 435, 436 lethal crude oil concentration, 354 mastication, 57 naphthalene metabolism, 343 naphthalene retention, 337, 338 nauplii, 3 predation, ctenophores by, 264 pristane biosynthesis, 3 1 1 , 3 12 sex hormones, 356 strontium uptake, 435, 436 swimming pattern, 52 zirconium uptake, 435, 436 Copepod Pseudmalanua biology, 2 et aeq. copper toxicity, 459 development and growth, 100-135 distribution and abundance, 11-27 DNA content variations, 9-1 1

Copepod Pseudomlanua-contued excretion, 43-61 food web role, 199-200 Genus, 3-4 life cycle, 135-168 locomotion, 51-63 morphology, 27-37 nomenclature, 2-9 nutrition, 54-80 parasites, 190-199 " Physiological " species, 9 predators, 200-210 production, 179-190 reproduction, 80-100 respiration, 37-43 species description, 4 - 9 vertical migration, 168-182 water soluble fraction (WSF) of oil, susceptibility to, 333 Copepodids, Pseudocalccnua basic structure, 29, 30 body size-water temperature relationship, 117, 118, 120, 121, 122 CIstage, 30, 109, 110, 111, 112, 113, 121 CII stage, 30,109,111,121, 138 C I I I stage, 30, 109, 111, 120, 121, 122, 128, 137, 138 CIV stage, 31, 109, 111, 121, 138 CV stage, 31, 109, 111, 117, 121, 126, 138 CVI stage, 109 carbon content, 126 depth distribution, 117 development rate, 107-114, 135, 137, 183 die1 vertical migration, 166, 69, 170, 171, 176, 177, 178 diet, 63 feeding depth, 167 feeding rhythm, 74 food assimilation, 76 food requirements, 133, 168 200 generations, 138 growth rate, 130, 131, 133, 189 gut contents, 60, 61, 74 laboratory rearing, 120, 128 mturation, 136-158 mortality, 143

525

SWJEO" INDEX

Copepodids, Pseudocalanw-continued nitrogen content, 126 non-migratory, 178 oil sac, 126, 128, 129 ontogenetic migration, 159, 160 overwintering, 139, 145, 150, 152 parasitized, 193 phosphorus content, 126, 127 phosphorus excretion, 50, 51 phytoplankton consumption, 200 respiration, 38 seasonal migration. 162 size-bimodalism, 141 size-selectivefeeding, 60, 63 stage abundance, 143, 146 vertical distribution, 159, 161 weight-length relationship, 127, 185 wet weight, 124 Copepodids IV, 5 maturation, 143 overwintering, 143, 144 relative abundance, 142, 143, 144 semonal migration, 162 sex ratios, 80 size-selective feeding, 60 Copepodids V, 4 die1 vertical migration, 171 female, 5 male, 4, 5, 8 " resting ", 190 seasonal migration, 162 sex ratios, 80 size-selective feeding, 60 Copepodids development rate, Pseudocalanus, 107-1 14 food supply effect, 11%113 temperature effect, 107-112,120,121 Copepods amino acid assay, 125 aromatic hydrocarbon retention, 339, 343, 344

arsenic content, 506 cadmium content, 461, 502 chromium content, 506 copper content, 505 copper toxicity, 459 crude oil toxicity effects on, 353 ctenophore destruction by, 268, 458 diminished light response, 172 egg production, 357, 451

Copepods-continued estuarine, 339, 355 faecal pellets, 65, 348, 349, 360, 361 feeding current, 54 feeding rates, 64, 279, 363, 436, 448450

filter-feeding, 55, 64, 65, 7 1 food, 60, 61, 436 growth rates, 100, 130, 134 healy metal content, 462 heavy metal turnover, 429,437 heneicosahexaene (HEH) biosynthesis, 311, 313 hormones, 356 hydrocarbon biosynthesia, 311, 312 hydrocarbon retention, 290, 337 lead content, 504 life cycle, 147 lipid content, 125 mandible, 57 mercury content, 501 mortality, 279, 281, 283 moulting rate, 107 naphthalene metabolism, 335, 336, 337, 338,339, 340, 341, 342,343, 344, 349 naupli, 451, 462, 453 nickei content, 603 nitrogen excretion, 43,44,45,47,48, 350 oil ingestion, 350 oil slick immobilization, 350 phosphorus excretion, 49, 350 population variations, 282 predation, ctenophores by, 253, 264, 255,257, 258,263,264, 270, 271, 277, 279, 280, 281 pristane biosynthesis, 311, 312, 314 production/biomms ratio, 181 production estimates, 186, 188, 278 reproductive rate, 100 sampling, 22 selenium content, 503 sex ratios, 80 silver content, 503 size-selectivefeeding, 61, 63 squalene in, 291 steroid metabolism, 357 swimming pattern, 62, 265 teeth, 57

526

SUBJEOT INDEX

Copepods-mntinued tidal pool, 352 vertical distribution, 22, 23 water clearance rate, 436 water soluble fraction (WSF) of oil toxicity effects on, 354 weight-length relationship, 127 weight-specific excretion rate, 46 zinc content, 507 Copper population dynamics study, in, 281 sulphate, 382 copper turnover, zooplankton, 460, 462, 463, 500, 505 CEPEX enclosure studies, 458 egg hatching, effect on, 451 faecal pellet production, effect on, 449, 459, 460 fecundity, effect on, 454, 460 feeding rate, effect on, 448, 459, 460 growth and development, effect on, 452

riauplii development, effect on, 451, 452 respiration rate, effect on, 447 Copper uptake, phytoplankton, 392, 393, 427, 491-495 cell membrane disruption, 424 cellular content, 393, 403 CEPEX enclosures in, 419-425 concentration-growth rate relationship, 408, 409 giant cell production, 413 growth rate reduction, 415, 419 long term effects, 419 metabolism, effect on, 423 natural populations, 419-425 photosynthesis rate, effect on, 422 potassium leakage relationship, 413 primary production, effect on, 396, 417, 418 seasonal growth relationship, 395 synergistic effects, 411 tolerance, species of, 401 Coral reefs, 246 Cornwall coast, oil pollution, 243 Corpus Christi Bay, Texas, 498, 499, 500 Costa Rica coast, 439

Crab iarvae, 362 naphthalene metabolism, 337, 343, 347 Crabs, 267 zoeae, 485, 456 Cretaceous climatic zones, 243 Crude oil, 290 hydrocarbon range in, 304 hydrocarbon source, as, 309-310 laboratory dispersion, 353 lethal concentrations, 353, 355 phytoplankton toxicity studies, in, 319-327 water soluble fraction (WSF), 318, 319-327, 358-361 world ocean inputs of, 309, 310 zooplankton toxicity studies, in, 352-354, 368-361 Crustacea Amphipoda arsenic content, 606 cadmium content, 461, 502 copper content, 505 zinc content, 507 Crustacea Cladocera, zinc content, 507 Crustacea Copepoda arsenic content, 506 cadmuim content, 461, 502 chromium content, 506 copper content, 505 lead content, 504 mercury content, 501 nickel content, 503 selenium content, 503 silver content, 503 zinc content, 507 Crustacea Decapoda arsenic content, 506 cadmium content, 461, 502 copper content, 505 mercury content, 501 zinc content, 508 Crustacea Euphausiacea arsenic content, 506 cadmium content, 602 chromium content, 506 copper content, 505 lead content, 604 mercury content, 463, 501 nickel content, 503 selenium content, 603

SUBJEOT INDEX

Crustacea Euphausiacea-conti~~ud silver content, 503 zinc content, 507 Crustacea Mysidacea arsenic content, 506 cadmium content, 502 mercury content, 501 zinc content, 507 Crustaceans, 3 1 diet, 206 hydrocarbon metabolism, 345, 356 limbs, 34 moulting rate, 107 oil pollution effects on, 361 parasitic infection, Psewlocalanus, 198 parasitized, 198 steroid metabolism, 356 water-soluble fraction (WSF) of oil toxic effects on, 355 Cryptomonads, 305 Cryptophyceae, 306, 308 Cryptophyta Cryptophyceae cadmium effect on, 485 copper effect on, 491 lead effect on, 488 mercury effect on, 479 Cryptophytes, 78 Chrysophyta Bacilliophyceae cadmium effect on, 486 chromium effect on, 496 copper effect on, 492-494 lead effect on, 488-489 mercury effect on, 481-482 organic mercury compounds, effect on, 484 silver effect on, 487 zinc effect on, 497 Chrysophyta Chrysophyceae, copper effect on, 492 Crysophyta Xanthophyceae cadmium effect on, 485 copper effect on, 492 lead effect on, 488 mercury effect on, 481-842 Ctenophores, 53, 457 ammonia excretion, 273 annual production, 278 behavior, 251-267

527

Ctenophores-continued biomass production, 274, 277, 278, 279, 280 body diameter, 273 CEPEX enclosure studies, 458 carbon content, 269, 270 chemical composition, 269 chromium content, 506 collection methods, 250 copepod predation, 264 copper content, 505 daily rations, 270 diet, 207-208, 251 digestion, 271-272, 277 dissogony, 276 dry weight, 269, 277 egestion, 271, 272 egg production, 276 excretion, 272-273 faeces, 272 fecundity, 275-276, 281 feeding mechanism, 251-267 growth rates, 273-275,278,279, 281 heavy metal toxicity, 459, 460 hydrocarbon uptake and release, 337, 343 ingestion rates, 26S271 lead content, 504 metabolic requirements, 275, 277 mortality, 281, 282 mucus release, 257, 267, 271 nickel content, 503 nitrate excretion, 273 nitrogen content, 269 nitrogen excretion, 272, 274 nutritional ecology, 249 et eeq. occurrence, 250 oceanic, 250 organic carbon content, 277 organic nitrogen excretion, 273 oxygen consumption, 272 paedogenesis, 276 phosphorus content, 269 population dynamics, 267, 268, 282 predators, 267-268 production estimates, 278 regenerative powers, 275 respiration, 272-273, 279 seaaonal population variations, 277-282

628

SUBJEOT INDEX

Ctenophores-oontinued self fertilization, 275 silver content, 503 size shrinkage, 275 spawning, 276 total population respiration, 279 water clearance rate, 271, 279 wet weight, 269 zinc content, 507 Culture media, phytoplankton heavy metal toxicitycomposition relationship, 400-403 heavy metal toxicityconcentration relationship, 406-

Daily rations, Pseudocabnus --continued body weight relationship, 72 die1 vertical migration relationship, 165, 166, 175

Darwin, 233 Daytime distribution, Pseudocalanwr, 20

DDT pesticide, 244 Dead Pseudocalanus, biomass, 208 Decapods, 3 15 arsenic content, 506 cadmium content, 461, 502 copper content, 505 410 zinc content, 508 heavy metal toxicity-growth larvae, 265 relationship, 4 0 6 4 0 6 mercury content, 501 Culture techniques, phytoplankton, Deep water 398 heavy metal levels in, 462 Cultured phytoplankton, heavy metal hydrocarbon levels in, 302 effect on, 398-415, 479-498 P8EudOcalanU8 in, 15, 161 cadmium, 485-487 Delaware Bay, 153-154 chromium 496 Demersai fish, diet, 201-206, 363 copper, 491-495 Demographic hypothesis, Pseudolead, 488-490 calanw die1 migration, 176-179 mercury, 479-483 advantage model, 177, 178 organic mercury compounds, 484 Dental impression material, 242 silver, 487 Depth, sea, hydrocarbon level variazinc, 497 tions with, 294 Cyanophyceae, 306, 307, 308 Cyanophyta Cyanophyceae, copper Desmosterol, 356 Detergent oil dispersants, 244 effect on 491 Detritus Cyclo-alkanes, 301-304 euphausiid, 444, 445 Cyclohexanes, 304 heavy metal levels in, 439, 440, 444 Cyclopentanes, 302, 304, 318 Pseudocalanua, 209 Cyclopoid copepods, 264, 354 Tentaculata food, as, 263 Cydippida, 250 zinc levels in, 444, 445 feeding mechanism, 259, 261 Development and growth, Pseudofood, 263 calanus, 100-135 occurrence, 250 adult longevity, 1 1 6 1 1 5 tentacles, 259 Cymenes, 322 body composition and weight, 124-128

D

body size variations, 115-124 embryonic development rate, 101-107

Daily migration, Pseudocalanus, 164 Daily rations, ctenophores, 270 Daily rations, PseudocaEanus, 66, 67, 71-72, 133, 199

genetic variation of development rates, 113-114 growth rates, 129-131 hatching 107

529

SUBJECT INDEX

Development and growth, Pseudowlanua-continued nauplii and copepodid development rate, 107-114 oil storage, 128-129 Development and growth, zooplankton, heavy metal effects on, 460-456 Development rate, Pseudocalanua, 9 high latitudes, at, 136 somatic production estimates from, 181

successive generations, 144, 151 temperate latitudes at, 141 temperature dependence, 167 warm waters, in, 139 Development stages, Pseudocalanwr,21 adulthood, 110, 111, 113, 114-116 BZSlehddek’s temperature function, 108,109

body size variations, 115-124 copepodids, 107-114, 135 DNA effect, 113 duration, 108, 109, 110, 111 embryonic, 101-1 07 food concentration effect, 110, 111 foodsupply effect, 112-113,, 122-123 frequency distribution, 137, 138, 140 146

genetic variations, 113-114, 123-124 graphical representation, 106 hatching, 107, 110 laboratory data, 119-122 laboratory rearing, 110 nauplii, 107-114, 136 relative abundance, 137 retardation, 116, 112 temperature effect, 107-112,115-122, 123-124

time required, 108, 109 Diadromous fish, 201 Dialysis culture, phytoplankton, 399 Diatoms, 68,69,66,75, 78, 81, 116, 146 amino acid content, 78 chain-forming, 69 chromium content, 600 copper oontent, 600 copper tolerance, 423 heavy metal content, 462 heavy metal tolerance, 400, 420 hydrocarbon content, 307

Diatoms-contind lead content, 499 nickel content, 499 silica frustules, 423, 424 silicic acid uptake, 423 silver content, 499 surface area, 383 systematics, 243 water soluble fraction (WSF) of oil, susceptibility to, 320, 326, 333. 334

zinc content, 500 Dibenzothiophenes, 301, 318 Diel feeding rhythms, Pseudooa~anua, 66, 72-75, 79, 100, 167, 176, 176, 200 Diel light cycles, 172

Diel specific gravity changes, Pseudocalanus, 166 Diel vertical migration, Pseudooalanua, 163-179

adaptive value, 173-174 amplitude, 166, 167 body size, and, 177 clutch size, and, 177, 178 demographic hypothesis, 176-179 depth layer residence time, 166 energy-bonus hypothesis, explanation, 175-176, 178 fecundity relationship, 176, 178 light response, 168, 172-173 metabolic advantages, 176 migrant classes, 166 physical-chemical condition relationship, 168 predation hypothesis explanation, 174-176

predator migration, 168 rates, 166 sexes, of, 171 size variance, and, 172 temperature response, 167 Diesel oil, 363, 368 Diet calanoid copepods, 3 11 chaetognaths, 206 ctenophores, 207-208, 261 commercially important fish species, 201-206

crustaceans, 206

630

SUBJECT INDEX

Dietcodnued hydromedusans, 207 Diffusion-controlled heavy metal ion uptake, phytoplankton by, 385, 386 Digestion, ctenophores, 271-272 Digestive efficiency, ctenophores, 27 1, 277 Digestive enzymes, Pseudocalanus, 79 Dihydro-diols, 346 Dimethyl-/%propiothetin, 400 Diminished light response, Paeudocalanus, 172 Dinoflagellate Blrntodinium hyalinum life history, 191-192 occurrence, 194 Pseudoca2anua host infection, 192194 taxonomy, 190 Dinoflagellate Dissodinium pseudocalani, life history, 194-196 occurrence, 136 Paeudocalanus host infection, 196 taxonomy, 194 Dinoflagellate parasites, Pseudocalanus of, 190-197 Blastodinium hyalinum, 190-194 Dissodinium psedocalani, 194-1 96 Ellobiopsis chattoni, 196 Sporodinium paezdocalani, 196 Dinoflagellates, 59, 73, 7 5, 7 6, 78, 382, 427 copper tolerance, 423 heavy metal tolerance, 420, 421 morphological abnormalities, 413 parasitic, 190-197 spores, 243 Dinophyceae, 306, 308 Dinophyta Dinophyceae copper effect on, 491 lead effect on, 488 mercury effect on, 479 Dinophyta Linophyceae cadmium effect on, 485 meroury effeat on, 480 Disodium ethylenediaminetetraa.cetate (EDTA), 387, 402, 439 Disperssnt BP llOOX, 353, 359 Dissogony, ctenophores, 276

Dissolved ” hydrocarbons, sea water in, 293-294, 301, 302, 316 n-alkanes, 298 aromatic, 297 non-olehic, 298 unsaturated, 298 Dissolved inorganic phosphorus (DIP) excretion, Psewlocalanus, see Phosphorus excretion, Pseudocalanus Dissolved metah, sea water in, 391 main species, 392 Dissolved organic phosphorus (DOP) excretion, Pseudocalanus, see Phosphorus excretion Pseudocalanus Distillate fractions, oils, 322 Distribution, Pseudocalanus distance offshore, in relation to, 16 geographical, 11-16 microdistribution, 22-23 oxygen concentration limits, 25 physical-chemical limits, 23-26 pollutant concentration limits, 25-26 salinity limits, 24, 27 southern limits, 26 temperature limits, 23-24, 26 vertical, 20-22, 27 water masses, in relation to, 15-16 Diurnal vertical migration Pseudocalanus, 7 1 zooplankton, 441 DNA, mdticellular algae, 331 DNA, Pseudocalanus, content vadabions, 9-11 development stages, effect on, 113, 135 genetic variations, effect on, 123, 124 Dog salmon, 201 Dohrn, Anton, 233 Dolphins, 239 Drew, Kathleen M. (“Mother of the Sea ”), 237 Dry weight, ctenophores, 269 growth efficiency estimates from, 277 Dry weight, Psedouxlanus, 123, 124, 125 carbon content conversion, 126 coefficient of increase, 130 “

SUBJECT INDEX

Dry weight, Pseudocahnus-continued nitrogen content conversion, 126 phosphorus content conversion, 127 production estimates from, 182 Dungeness crab, 345 Dusk and dawn rise, Pseudocalanus, 173

E East Greenland, Pseudocalanus at, 117, 141, 162 East-Icelandic Current, Pseudocalanus in, 18, 152 Eastern Mediterranean, 248 phytoplankton populations, 417,418 420 Echo-sounding, 2 39-240 Eco-systems, oil pollution effects on, 331-335, 364 Ectoparasites, Pseudocalanus of, 194, 196 Educational Reserves, 247 Egestion, ctenophores, 271, 272 Egg clutch, Pseudomlanus die1 vertical migration relationship, 177 dry weight, 128 egg number in clutches, 86-89, 95, 96 egg proportion hatching as nauplii, 94-95 embryonic duration, 95, 97 parasitized, 196 post-reproductive period length, 86, 92, 94, 114 production rate, 89-92, 100, 114 reproductive period production number, 92-94 synchronous clutches, 137 terminology, 85 Egg laying, Pseudocalanus, 8 1 Egg matter production rate, Pseudocalanus, 131-132, 189 Egg production, copepods heavy metal effects on, 451,454,456 hydrocarbon effects on, 357 Egg production, ctenophores, 276

531

Egg production, Pseudocalanus clutches, number in, 86-89, 100 general pattern, 85-95 maximal rates, 112 natural rates, 96-99 somatic production estimates from, 181 theoretical rate, 95-96 Egg production, zooplankton heavy metal effects on, 451, 454 heavy metal elimination by, 431 Egg size, Pseudocalanus cophalothorax length relationship, 103, 105 embryonic development rate relationship, 103-107 Eggs, Pseudocalanus, 10, 11 clutch production rate, 89-92 clutch size, 86, 88 clutches, number in, 86-89 counts, 98 daily production rate, 96 DNA content, 113 dry weight, 128 hatching proportion, 94-95 infertile, 94 sac production rate, 89, 91, 92 sacs, number in, 92, 93 temperature tolerance, 24 terminology, 86 production patterns, 85, 86 vertical distribution, 161 " viable ", 94, 95 E g p n 68" 08'N, 150, 151 Egyptian coast, 247 Eilat Coral Nature Reserve, 246 Ekofisk crude " oil ", 300, 361 Electropositive ion uptake, phytoplankton, 394 Elefsis Bay, Greece, 501, 502, 503, 505, 506, 507 Elemental composition, Paeudomlanus, 125-127 Embryo, Pseudocalanus, 29 Embryonic development, Pseudocalanus body and egg size effects, 103-107 salinity effects, 24, 102 seasonal and short-term acclimation, 102-103, 105

532

SUBJECT INDEX

Embryonic development, Pseudocahnua-continued seasonal variation, 102, 103 temperature effects, 23, 101-102 Embryonic duration, Pseudocalanus, 95, 97, 99, 110, 111, 113, 135 B&lehr&dek'stemperature function, 99, 103, 107, 108 cephalothorax length, relation to, 103, 104, 105 female size, relation to, 105 male size, relation to, 105, 113 seasonal variation, 103, 107 short-term temperature acclimation, relation to, 102-103, 105, 107, 111 successive development stages, relation to, 108, 109 Energetic cost of migration, Pseudocalanus, 174, 175 Energy-bonus hypothesis, Pseudocalanus die1 migration, 175-176 Energy requirements, ctenophores, 277 279 English Channel n-alkanes level in, 294, 298 ctenophores in, 278 hydrocarbon levels in, 302, 337 mackerel in, 202 phytoplankton in, 321 Pseudocalanus in, 117, 202 Environmental stress resistance, zooplankton, 456-457 Enzymes, marine animal, 345, 346, 356 Epicaridean isopods, 198 " EpipIankton ", 209 Epoxide hydrase, 346, 347 Erdschreiber growth medium, 76 Erythrocytes, 384 Escape reaction, Pseudocalanus, 53 Estonian coast, 203 Estuaries, ecology, 245, 246 Estuarine copepods, 339 water-soluble fraction (WSF) of oil toxicity effects on, 355 Estuarine phytoplankton, surface, physico-chemical nature, 383 Estuarine waters heavy metal levels in, 382 hydrocarbon levels in, 302

Ethane, 291 Euglenaphyceae, 306, 308 Euphausiids, 204, 206, 262, 311, 312, 315, 337, 343 arsenic content, 506 cadmium content, 502 carcass sinking rate, 444 chromium content, 506 copper content, 505 death rate, 444 execretion rat,es, 433 faecal pellets, 348, 432, 444, 446 food ingestion rate, 439 growth rates, 433 heavy metal turnover, 429, 431, 432, 433, 437, 440, 442, 450 lead content, 504 mercury content, 463, 501 metal fluxes, 431, 444 moult sinking rate, 444 moulting, 432, 442, 444 nickel content, 503 selenium content, 603 silver content, 503 zinc content, 507 Europe, western, Pseudocalanue off, 14 European hake, 205 European pilchard, 203 European plaice, 205 European waters, giant kelp in, 247 Excretion, ctenophores, 272-273 Pseudocalanus, 43-51 nitrogen, 44-49 phosphorus, 49-51 Expatriate Pseudocalanus, 15 Exponential growth coefficient, ctenophores, 273, 276 External parasites, pelagic copepods of, 196

F Faecal pellets, Pseudocalanus, 58, 66, 66, 73, 75, 200 heavy metal release in, 449 Faecal pellets, zooplankton heavy metal release in, 430,431,432, 433, 440, 449, 450, 455, 469 hydrocarbon release in, 348-361,363 oil sedimentation, 348

SUBJECT WDEX

Faeces, ctenophores, 272 Fecundity, ctenophores, 275-276 laboratory estimates, 281 Fecundity, zooplankton heavy metal effects OR, 454-466 Feeding current, Pseudocalanus, 54 Feeding depth, Pseudocalanw, 167 Feeding experiments, ctenophores, 279 Feeding experiments, Pseudocalanm, 59, 61, 64, 71, 72, 73, 79, 100

radiocarbon-labelled, 75 Feeding mechanism, ctenophores Beroe, 265, 267 beroids, 266 Bolinopsia, 261, 265 Cydippida, 259, 261, 269 Eurhcamphaea, 261 food concentration relationship, 255, 269

Hormiphora, 261 Leucothea, 262 lobate ctenophores, 257, 258, 261, 269

Nuda, 265-267 Ocyropsis, 262 Platyctenea, 263 Pleurobrachia, 259, 265 Tentaculata, 259-263 Vallicula, 263 water clearance rate relationship, 273

Feeding

Feeding rate, Pseudomlanua, 64-72 body weight relationship, 67 daily rations, 66, 67, 71-72 equation, 66, 67 food concentration effect, 65-70 individual variability, 69 regression, food concentration, on, 62, 69

satiation, 67, 68 saturation, 66 temperature effect, 70-71 Feeding rhythm, Pseudocalanus, 73 vertical migration relationship, 73, 74

Female Pseudocalanw antennae, 34, 52 ash-free dry weights, 123 bimodal depth distribution, 159 bimodal size, 140, 161 bodysize, 64, 105, 115, 116, 117, 119, 144

body size-cellular DNA relationship, 124 body size-food supply relationship, 122, 123

body size-water temperature relationship, 115, 116, 117, 118, 119,120, 122

carnivorous, 58 cephalothorax lengths, 115,119,122, 123, 124, 131

mechanism,

Mnerniopsis,

261-259

food concentration effects, 255, 256. 257, 258, 270

passive food capture mechanism, 264 prey capture, 252, 253,254, 255, 257 rate, 264, 270 starvation, adjustment to, 255, 257, 258, 270

stimulation, 265 tentacle setting, 252, 253, 254, 255, 256, 257

Feeding mechanism, Pseudocalanus, 54-58

filter feeding, 54-57 large particle feeding, 57-58 Feeding rate, copepods, 436 inhibition, crude oil by, 353 inhibition, heavy metals by, 448-450 A.Y.B.-IE,

533

daily egg production, 96 daily food ration, 71, 72 depth distribution, 117 development rate, 9 development stages, 3 1 diagrammatic representation, 33 diel specific gravity changes, 161 diel vertical migration, 168, 171, 172, 176, 179

egg-bearing, 141, 142, 143, 152 egg clutch size, 86, 87, 88, 90, 96, 135 egg matter production rate, 131-132 eggproduction, 85, 86, 87, 93, 94, 96, 98, 135

egg sac, 85, 89, 93, 98 embryonic duration-size ship, 105 feeding depth, 167 feeding rate, 69, 79

relation-

20

534

SUBJEOT INDEX

Female Pseudocahnua-continued Female PsewEocalanwr--contud feeding rhythm, 73, 74 teeth, 57 filtering rate, 70 temperature acclimation, 102, 106 food, 63, 64, 65 turnover times, 185 food assimilation, 75, 76, 131 vanguaxd ”, 144 food sustenance requirements, 76, 77 vertical distribution, 158, 159, 161, generation succession, 143, 144 165 genetic size variation contribution, “ viable egg ” production, 94 123 wet weight, 124 genital segment, 34, 194 Fiddler crab larvae, 447, 448 growth rate, 130 Filter feeding, Pseudocalanus, 54-57 gut contents, 58, 59, 60, 61 feeding current, 54 infertility, 93, 94 filtering rate, 64, 65, 70 life span, 80, 81, 114, 115 filtration, 54-55 mandible, 56 mastication, 56-57 mating, 83, 92 size selection, 60-63 maturation, 144, 145 Filtration rate, Pseudocalanus, 64, 65 non-migratory, 178 uptake experiments, 65 non-reproductive, 99 Firth of Clyde, 502, 504, 505, 507, 508 offspring size contribution, 124 Fish oil sacs, 99, 128, 129 aryl-hydrocarbon hydroxylase oogenetic cycle, 81 (m), 346 ovary development, 81, 82 ctenophore predation by, 267, 268 overwintering, 143 eggs, 265 parasitized, 193, 194 exploitation, 235 pheromone production, 36, 84 farming, 236-237 post-reproductive period, 86, 92, 94, hydrocarbon metabolism, 342, 346, 95, 114 364 production/biomass ratio, 181 larval mortality, 201 reproduction parameters, 91, 93 mating calls, 240 reproductive decline, 143, 145 mixed function oxygenases (MFO), reproductive life, 85, 94 346 reproductive potential, 93, 95, 96, 98 nematode parasitic infection, 198 reproductive rate, 86, 89-92, 95, 96, neoplasie, 347 98, 99 noise generation, 239, 240 respiration, 38, 40, 41 plankton-feeding, 3 poisonous, 237-238 sampling, 23 second maxilla, 54, 55 predation, ctenophores by, 262 short-term temperature acclimation, Pseudocalanua predation by, 201-206 103, 105 quota systems, 236 size-frequency distribution, 138, 146, recruitment rate, 235 147, 148, 150, 151, 153, 154 stocks, 235 size-selective feeding, 62 supply, 235 size variation, 149, 150 swimming efliciency, 239 stored oil, 99, 100, 136 trematode parasitic infection, 197 successive generations, 144 venomous, 237-238 survival food requirements, 77, 78, vertical migration, 239 115 Fishing restrictions swimming pattern, 52 Acts of Parliament, 234 tagmata, 32 history, 234

SUBJECT INDEX

Flagellates, 58, 59, 66, 67, 81, 145, 171 faecal pellets, 65 rnercury uptake, 386, 387 poison extraction from, 241 unicellular, 236 zinc uptake, 387 Flexible boats, 239 Florida coast, 278, 282, 296 heavy metal concentration at, 395 Florida J a y crude oil, 359 Florida Strait non-polar hydrocarbon levels in, 292, 294, 297 Fluorenes, 301, 318 Fluorescence spectroscopy, 320, 323 Flying fish, 268 Food, ctenophores, 268 concentration-ingestion -rate relationship, 270, 271 copepod nauplii, 268 Beroe, 265, 266, 267 beroids, 266 Bolinopeis, 264, 265, 266 Cydippida, 263, 264 daily rations, 270 density-ingestion rate relationship, 269 egestion, 271, 272 egg production relationship, 276 E u r h m p k a , 263 Lobata, 263, 264 manipulation, 262 Mnemiopaia, 264 Nuda, 266-267 Pleurobrachia, 264, 266 requirements, population growth for, 282 Tentaoulata, 263-265 Food, Paeudooalanw, 68-64 algae, 77, 110, algal detritus, 68, 60, 63, 75, 76 aasimilation, 76-76, 133 body size, effect on, 116, 122-123 chlorophytes, 78 chrysophytes, 59, 78 cryptophytes, 78 coccolithoporids, 68 concentration effect, 65-70 crustacean remains, 58 daily ingestion rates, 133

535

Food, Paeudocahnua-continued daily ration, 66, 67, 71-72, 133 development stages, effect on, 110, 112-113 diatoms, 58, 59, 63, 66, 75, 78, 81, 113 dinoflagellates, 69, 73, 75, 76, 78 egg clutch size, effect on, 90, 92 feeding rythm, 72-75 flagellates, 68, 66, 67, 81 growth rate, effect on, 130, 133 humus, 58, 64 ingestion rate-food density relationship, 66, 67, 69 longevity, effect on, 114, 115 melanin, 58, 64, 76 near-saturation concentrations, laboratory estimates, 68 nitrogen excretion rate, effect on, 45 non-living particles, 63-64 nutrient excretion rate, effect on, 200 oil sac size, effect on, 129 phosphorus excretion rate, effect on, 49-60 phytoplankton, 66, 116 radiocarbon tagging, 184 radiolarians, 68 respiration requirement, 42-43 satiation concentrations, 67, 68 size, 60-63, 210 species eaten, 68-60, 68 stage abundance, effect on, 166 sustenance requirements, 76-79 toxic, 78, 79 Food assimilation, Paeudocahnua, 76-76 vertical migration relationship, 176 copper effect on, 469 Food chain, phytoplankton/copepod/ ctenophore, 281 Food-chain models, 290 Food from the sea, 234-236 Food webs ctenophores, role in, 281, 282 petroleum hydrocarbon concentration in, 362 Food webs, Paeudocahnua role in, 199-200, 208-210 nutrient excretion, 200 phytoplankton feeding, 199-200

536

SUBJEOT INDEX

Foraminifera, 243 Fossil marine organisms, 242 Foxe Basin, northern Canada, 87, 118, 141, 162 Freshwater algae, chemical composition, hydrocarbon effects on, 330 Freshwater fish, 236 Frobisher N.W.T., Pseudocalanus at, 99 Fuel oil No. 2, 318, 320, 321, 323, 358 lethal concentrations, 353 phytoplankton growth-rate stimulation by, 323, 324 water-soluble fraction (WSF), 320, 322, 333, 334, 354, 359 Fuel oil No. 6, 320 water-soluble fraction (WSF), 320, 337 Fuel oils, water soluble fraction (WSF) composition, 325 Fungi, hydrocarbon degradation, 328

G Gas chromatography, 294, 323, 325 Gas-liquid chromatography, 302 Garpike larvae, 453 Gdansk Deep, Baltic, 187 Generation time, Psetdocalanus, 135, 138 high-latitudes, in, 138 temperate-latitudes, in, 143 Generations, Pseudocalanus, 136, 138 delimiting, 142, 147, 154 development period, 144, 145, 146 numbers when not food limited, 156 overwintering, 138, 141, 149 reproductive rate, 139 second summer, 139 size-frequency distributions interpretation from, 146, 147, 148, 150, 151, 154 statistical separation, 185 Genetic variation, Pseudocalanus body size, 123-124 Genus, Pseudocalanus, 3-4 Geochemical cycling, heavy metals, 397, 442

Geochemical sedimentation, heavy metals, 397, 442 upper mixed layer from, 443 Geographical distribution, Pseudocalanus, 11-16, 18 Geological science, 242-243 Georges Bank, 204 Giant cells, phytoplankton, 413-415 Giant kelp, 247 Global emission, hydrocarbons, 309 Glutathione-S-transferase,346, 347, 365 Glycylglycine, 402 Gorgonid coral, 245 Goteborg Harbour mineral oil hydrocarbon levels in, 296, 357 non-polar hydrocarbon levels in, 297 Gotland Deep, Baltic, hydrocarbon levels in, 293, 298 Grass shrimp larvae, 450, 453, 454 Grazing rate, zooplankton, 436 Great Barrier Reef, 246 Green algae, 326, 354 heavy metal tolerance, 400 Green Island, Queensland, 246 Greenland, 158 Gregarines, Paeudocalanus host infection, 197 Gross growth efficiency, Pseudocalanus, 132, 133, 134, 185 Growth, zooplankton, heavy metal effects on, 450-455 Growth efficiency, ctenophores, 276277 " Growth factors ", Pseudocalanus, 189 Growth-inhibiting substances, 241, 321 Growth rates ctenophores, 273-275, 278, 279, 281 euphausiids, 433 Growth rates, algae, 324 " algal lawn " measurement technique, 315 hydrocarbon toxicity effects, 325, 326 stimulation hydrocarbons by, 330 water-soluble fraction (WSF) of oil toxicity effects, 325

637

SWJEUT INDEX

Growth rates, phytoplankton, 321, 325 cellular nutrient content relationship, 407 copper concentration effects on, 419, 420, 425

heavy metal effects on, 398-410,411, 415, 427

hydrocarbon toxicity effects, 325, 326

membrane permeability relationship, 412, 413

naphthalene toxicity effects, 327-329 reduction, 415 stimulation, hydrocarbons by, 323,

Gurnards, 236 Gut, Paeudocalanua contents, 68, 59, 60, 73, 74, 79, 166, 176

daily fullness index, 71 dinoflagellate parasitic infection, 191 food passage rate, 7 1 size group of unicellular algae content, 60 Gut contents, ctenophores, 268, 266 Bolinopais, 211 Mnemiopaia, 263 Pleurobrachia, 263, 266 Tentaculata, 263, 264

324, 330

water-soluble fraction (WSF) of oil toxicity effects, 325 Growth rates, Paeudocalanua, 129-131, 181, 189, 210 "

balance equation ", 132, 134, 181, 199

efficiencies, 132-134, 200 food supply relationship, 133 maximal, 145, 185 Growth regulation compounds, 330 " Growth status ", Pseudocalanus, 190 Gulf of Alaska, hydrocarbon levels in, 299

Gulf of Aquaba, 246 Gulf of Bothnia, Paeudocalanus in, 14 Gulf of Finland, Pseudocalanua in, 14 Gulf of Maine, 311 cod in, 204 heavy metal concentration in, 395, 397

Pseudocalanus in, 18, 153 Gulf of Mexico n-alkane levels in, 294, 299 methane concentration in, 291, 297 non-polar hydrocarbon levels in, 292 phytoplankton populations in, 498, 499, 600 zooplankton in, 315, 316, 354, 461, 502, 603, 504, 605, 506, 508

Gulf of St. Lawrence, Paeudocalanus in, 14, 136, 196

Gulf of St. Malo, phytoplankton in, 321 Gulf of Suez, Pseudocalanus in, 13 Gulf Stream, phytoplankton populations, 417, 418

H Habitat temperature, Pseudocalanus, 40-42, 70

Haddock, diet, 204 Haemocyanin, 246 Hagfish, 241 Hake, 205 Halibut, 235, 236 Halifax, Nova Scotia hydrocarbon levels at, 293 Paeudocalanus at, 11, 24, 25, 61, 74, 86, 89, 93, 96, 97, 98, 99, 102, 103, 106, 106, 107, 108, 109, 110, 111, 113, 120, 129, 130 Halstead, Dr. Bruce, 237 Haptophyceae, 306, 308

Haptophyta Prymnesiophyceae (Haptophyceae) cadmium effect on, 485 chromium effect on, 496 copper effect on, 491-497 lead effect on, 488 mercury effect on, 480-481 organic mercury compound effect on, 484 zinc effect on, 497 Hardangerfjord, Norway, 601 Harpacticoid copepods, 353 cadmium uptake, 462, 463 copper uptake, 462, 453 heavy metal turnover, 437, 462 zinc uptake, 437, 438 Hatching, Paeudocalanus, 106,106, 107

638

SUBJEOT INDEX

Head, PseudocaZanw, 31, 33 Heavy metal biogeochemistry phytoplankton role in, 395-398 zooplankton role in, 440-446 Heavy metal content, microplankton 461, 498-500

cadmium, 498 copper, 500 chromium, 500 lead, 499 mercury, 461, 498 methyl mercury, 498 nickel, 499 selenium, 499 silver, 499 zinc, 500 Heavy metaI content, natural phytoplankton populations, 425-428, 462, 498-500

analytical techniques, 426 cadmium, 462, 498 chromium, 500 copper, 462, 500 growth rate, effect OR, 428 lead, 462, 499 mercury, 426, 427, 462, 498 methyl mercury, 498 nickel, 462, 499 sample collection, 425, 426 selenium, 499 silver, 462, 499 upwelling areas in, 426 wet weight basis, on, 427 zinc, 462, 500 Heavy metal content, natural zooplankton populations, 460-463, 501-608

analytical techniques, 460 arsenic, 506 cadmium, 461, 462, 463, 502 chromium, 506 copper, 460, 462, 505 deep waters, in, 462 dry weight baais, on, 461 gradient effects, 460 lead. 460, 462, 504 mercury, 460,461,462,463,501 methylmercury, 461, 502 nickel, 462, 463, 603 selenium. 503

Heavy metal content, natural zooplankton populations --continued silver, 462, 463, 503 trophic level variations, 462, 463 wet weight basis, on, 462, 463 Z ~ C 460, , 462, 463, 507-508 Heavy metal elimination, zooplankton egg production, by, 431 faecal pellet production, by, 430,431 432, 433

moulting, by, 430, 431,432, 433, 437 soluble excretion, by, 430,431,433 Heavy metal ions uptake, phytoplankton antagonistic effects, 411-412 cellular concentration, 385, 386, 393, 403, 404

concentration-growth rate relationship, 406-410 concentration-uptake relationship, 395, 396, 406

culture media experiments, 394, 400-403

diffusion controlled transport, 388 mechanism, 384, 386, 386, 388 nutrient ion concentration relationship, 396 passive uptake, 385, 388 primary production relationship, 396 radioactive tracer investigations, 385, 394

rate of uptake, 389 synergistic effects, 411-412 tolerance, species of, 400, 401 Heavy metal toxicity, phytoplankton antagonism effects, 411-412 cell metal tolerance changes relationship, 406406 cell population relationship, 403404

chemical state relationship, 405-410 concentration relationship, 406-410 culture medium composition relaionehip, 400-403 giant cell production, 413 growth-rate, effect on, 398-410 laboratory studies, 398-416 membrane permeability relationship, 412-413

SUBJEOT INDEX

Heavy metal toxicity phytoplankton --continued

412

synergism effects, 411-412 tolerance-species relationship, 400, 401

Heavy metal toxicity, zooplankton development, effect on, 450-465 environmental stress resistance, effect on, 466-457 faecal pellet production rates, effect on, 448, 449, 450 fecundity, effect on, 454 feeding rates, effect on, 448-450 growth, effect on, 450-465 ingestion rates, effect on, 448-450 laboratory studies, 446-457 large volume enclosure .studies, 457-460

activity,

zooplankton

--continued

natural population studies, 416-425 nature of, 412-415 nutrient ion concentration relationship, 402 resistance, 405, 419 species relationship, 400 sulphur binding capacity correlation,

metabolic

Heavy metal uptake,

539

effects

on,

447-448

natural populations in, 457-460 phototactic response, effect on, 455-456

sub-lethal levels, 447, 448, 450, 456, 457

swimming activity, effect on, 456 Heavy metal turnover, phytoplankton, 383-398

biogeochemical role, 395-398 chemical form effects of, 391-395 uptake kinetics and mechanism, 383-391

Heavy metal turnover, zooplankton, 428-446

biochemistry, role in, 440-446 chemical form, effect of, 439-440 food and water from, 434-439 mechanisms, 428 metal fluxes, 428-434 Heavy metal uptake, zooplankton chemical form, effect of, 439-440 efficiency, solution from, 436

food from, 434-439 phytoplankton, from, 434, 436, 437 rates, 437-438 surface adsorption, by, 437 water from, 434-439 Heavy metals, marine plankton pollution by, 381 et seq. Heligoland, German Bight, 196 Heneicoeahexaene (HEH) biosynthesis copepods by, 311, 313 unicellular algae, by, 306, 308 n-Heneicosane biosynthesis, 306 n-Heptane, 302 Herbivorous copepods, 57 Hermatypic corals, 243 Hermit crabs, 267 Herring diet, 202 hydrocarbon uptake, 341 larvae, 456 summer fattening, 265 Heteropods, 268 heavy metal turnover, 429 a-Hexane, 302 High aromatic heating oil, 359 Historical description, Pseudocalanwr, 4-9

History, marine biology, 233-234 Hokkaido, Pseudocalanwr at, 15 Holoplanktonic copepods, 364 petroleum hydrocarbon toxicity data 358-360

Horse-shoe crab, 241 Hulls, wooden ships, 238 Human erythrocytes, 412 Humpback salmon, 201 Huxley, T. H., 233, 240 Hydrocarbon biosynthesis, marine organisms by, 303 Hydrooarbon biosynthesis, phytoplankton, 306-309 n-alkanes, 306 aromatic hydrocarbons, 307 benzo[a]pyrene, 307, 309 carbon preference index, 306 heneicosahexaene (HEH) bio-synthesis, 306 mechanism, 306

540

SUBJEOT INDEX

Hydrocarbon biosynthesis, phytoplankton-continued tabulated data, 308-309 Hydrocarbonbio synthesis, zoo-plankton,311-317 iso-alkanes, 304 n-alkanes, 314, 316, 317 alkenes, 304, 314 exogenous sources relationship, 31 6 heneicosahexaene (HEH), 31 1 , 313, 314 mechanism, 31 1 phytol-derived, 311 polyunsaturated, 316 pristane, 291, 311, 312, 314, 316, 317 seasonal changes, 316, 317 squalene, 314, 316 Hydrocarbon fate, zooplankton in dietary pathway, 339-340 faecal pellet release, 348 long-term exposure, 340 metabolism, 342-348 uptake and release, 336-339 Hydrocarbon levels, sea water in, 290-303 alkanes, 291-292 analyses, 300-303 crude oil, from, 310 " dissolved ", levels, 293-294 particulate levels, 293-294 phytoplankton, from, 310 surface concentrations, 294-297 tabulated data, 297-299 Hydrocarbon uptake and release, zooplankton, 292, 335-351 depuration rate, 337, 338, 339 dietary pathway, 339-340 faecal pellet release, 348-351 hydroxylation, 345 long-term exposure, 340-342 metabolism, 342-348 naphthalene, 337, 348 radio-labelled hydrocarbons, 335, 336 reproduction, effects on, 356-367 Hydrogen content, Pseudocalanua, 127 Hydrographic forces, Pseudocalanus concentration, effect on, 18 Hydromedusans, 207, 268 Hydrophones, underwater, 239

Hydrozoans, zinc content, 507 Hyperiid amphipods, 268 Hypothetical migrant population, Pseudocalanua. 17 8

1 Icthyoplankton, 351, 364 petroleum hydrocarbon toxicity data 360-361 Indanes, 300, 301 Indenes, 300, 301 Indoles, 326 Infrared spectroscopy, 292 Ingestion rate, ctenophores, 261, 269-271 cydippids, 269 food concentration relationship, 269, 270 lobate ctenophores, 269 Mnemiopsis, 270 Pleurobrachia, 270 tentaculate ctenophores, 270 water clearance rate relationship, 270 Ingestion rate, Pseudocalanw, 64, 66 body weight relationship, 67 food density relationship, 66, 67 near-saturation, 68 regression, food concentration, on, 62, 69 saturation, 66, 69 Ingestion rats, zooplankton, copper effects on, 459 heavy metal effects on, 448-450 Inshore distribution, Pseudocalanus, 21 Instantaneous growth rates, Pseudocalanus, 130 Institute for Scientific Film, Grottingen, 251 Insulin, 240 Intensive culture, marine animals, 247 Intermediate hosts, parasites of, 199 International Conference on Marine Parks and Reserves 1975, 246 International Council for the Exploration of the Sea, 236 Invertebrates, growth rate, 274 Iodoacetamide, 414

541

SUBJEUT INDEX

Iran crude oil, 361 Irish Sea chemical stratification, 22 phytoplankton populations in, 499, 500

Pseudoealanus in, 21, 22, 168, 169, 173, 206 Iron, vertical transfer, 441, 442 Ise Bay, Japan, 500, 507 Isle of Man, 205 Isle of Wight, 247 Isoprenoid hydrocarbons, 291, 305 Italian waters, Pseudocalanus in, 15, 196

J Japanese waters Pseudocalanus in, 12, 15, 24, 126 seaweed cultivation in, 237 Jellyfish, 238, 240, 280, 337, 343 Jugoslavian coast, 296

K Kamchatka, 169 Kattegatt, 149 non-polar hydrocarbon levels in, 292, 297 total hydrocarbon levels in, 297 ‘‘ Keflin ” antibiotic, 242 Kelp shrimp, 355 Kerosene, 353, 358 Keta salmon, 201 Kiel Bay, Baltic, 5, 58, 197 Icing crab larvae, 355 King Edward Cove, South Georgia, n-alkane levels in, 292, 297 Kolmogorov-Smirnov test, 63 Korean coast, Pseudocalanus of, 15 ‘‘ Krogh’s normal curve ”, 183 Krayer’s plate, Pseudocalanus, 4, 6, 7 Kurile-Kamchatka trench, Pseudocalanus, in, 21 Kuwait crude oil, 318, 323, 353, 359 eco-system primary production, effect on, 331, 332 lethal concentration, 353 water-soluble fraction (WSF), 320, 321, 355, 359

L La Jolla, California, 439 Labelled hydrocarbons retention, zooplankton by, 335, 336, 337, 339, 340, 341, 344, 348, 349 Laboratory preservation, ctenophores, 250 Lake Pelto crude oil, 319 Landsort Deep, Baltic, 21 Laptev Sea, Pseudocalanus in, 25 Large-scale water enclosures phytoplankton toxicity studies in, 419-425 zooplankton toxicity studies in, 457-460 Larvaceans, 459 Larvae, Mnemiopsis “ destruction ” copepods by, 268 development stages, 251, 252 diet, 251 digestion time, 255 feeding behaviour, 255 feeding mechanism, 251, 262, 263 mortality, 268 prey capture, 252 starvation, 255, 258 swimming action, 253 Larval fish, diet, 201, 203 Laxatives, 242 Lead shipworm attack prevention by, 238 surface layers, removal from, 443 Lead turnover, zooplankton, 443, 460, 462, 463,499, 504 growth and development, effect on, 453 Lead uptake, phytoplankton, 417, 418, 427, 488-490 Lethal concentration (LC,,) values, zooplankton copper, 459 crude oil, 353 heavy metals, 446, 448 water soluble fractions (WSF), oil of, 355 Life cycle Blastodinium hyalinum, 191 Dissodiniuna pseudocalank, 194-1 96 Pseudocalanm, 135-158

542

SUBJEUT INDEX

Life cycle, Pseudocalanus, 98, 114-115, Lobate ctenophores-continued 136-158 feeding behaviour, 257,268, 261,262 Adriatic Sea, in, 154-155 gut contents, 268 arctic waters, in, 141 ingestion rate, 269 Baie - des - Chaleurs, Gulf of St. mucus release, 257, 262 Lawrence, in, 152-153 prey capture, 253, 254, 255, 257, 258 Bay of Fundy, in, 153 starvation, 255, 257 Black Sea, in, 154-155 superfluous feeding, 257 Coast of Norway, off, 150-152 swimming action, 253, 254, 255, 261 Delaware Bay, in, 153-154 Lobster larvae, 362 general features, 136-136 Loch Striven, Scotland Gulf of Maine, in, 153 annual temperature range, 11 6 high latitudes, in, 138, 157 Pseudocalanus in 9, 24, 86, 87, 98, Loch Striven, Scotland, in, 141-145 116,118,122,128,141-145,157, Northumberland coast, England, off, 162, 171, 188, 196, 210 147-149 Locomotion, Psewlocalanus, 51-53 Norwegian Sea, in, 152 escape reaction, 53 Ogac Lake, Baffin Island, in, 137, routine swimming, 51-53 138-140 Lofoten Islands, 160 Plymouth, England, off, 145-147 Long Island Sound, Pseudocalanus at, representative, 136-155 71, 87, 119, 122, 153 Sea of Japan, in, 155 Long term abundance, P~eudocalanus Tanquary Fiord, Ellesmere Island, 19-20 in, 136-138 Los Angeles, California, 498 temperate latitudes in, 141 Louisiana terminology, 135-136 crude oil, 353, 359 Tessiarsuk, Labrador,in, 137, 140off-shore, 296 141 Luiden, New Jersey, 324 West coast of Sweden, off, 149 Luminescent reactions, 240 Life-history strategy, Pseudocalanus, Lundy Island, 246 157 Light respiration rate of Pseudooalanua, M effect on, 42 vertica1 migration of Pseudocalanus, Mackerel, 202 effect on, 168, 172-173 sexual maturation, 265 Ligurian Sea, zinc levels in, 444, 445 Mmroalgae, 263 Ling, 206 Male Pseudocalanus Linnaeus, 233 antennae, 34, 52 Lipid, algae, 330 ash-free dry weights, 123 Lipid, copepod, 313, 315 body size-water temperature relaaromatic hydrocarbon uptake tionship, 120, 122 relationship, 339 die1 vertical migration, 168, 171 Lipid content, Psedocalanus, 125, 126 embryonic duration-size relationLobata, 250 ship, 105 occurrence, 250 genetia size variation contribution, food, 263 123 Lobate ctenophores growth rate, 130 copepod ingestion, 257, 258 life span, 80, 81, 114 digestion action, 258 light response, 173

SUBJMT INDEX

Male Paeudo&nua-continued mating, 83, 84, 85 maxillae, 36 offspring size contribution, 124 oil sac, 128 parasitized, 192, 193 seasonal migration, 162 spermatophore production, 8 1 swimming feet, 31 swimming pattern, 52, 84, 85 tagmata, 32 vertical distribution, 161, 165 wet weight, 124 Malgobek crude oil, 352 Malo Jezero, 155 Mandible, Paeudocalanua, 35, 36, 56, 56, 57 Manganese, surface layers, removal from, 443 Manganese uptake, phytoplankton, 395 Manual atoll, 246 Mariculture, 236-237 Marine biogeographic zones, Paeudocalanua distribution in, 15-16 Marine Biological Association of the United Kingdom, 240 Marine biology conservation aspects, 245-247 corrosion aspects, 238 echo-sounding as a tool for, 239-240 environmental modification, 247-248 fish farming aspects, 236-237 food supply aspects, 234-236 geological aspects, 242-243 history, 233-234 laboratories, 233, 234 medical aspects, 240-242 meteorological aspects, 242-243 physiological aspects, 240-242 poisonous organism studies, 237-238 pollution aspects, 243-244 ship design, application in, 238-239 Marine environment, human modification, 247-248 Marine growth, corrosive action, 238 Marine organisms, hydrocarbon biosynthesis, 303 " Marine parks ", 246 Mass spectrometry, 302, 303, 326 Mastication, Paedocalanus, 66-67

643

Mating, Paeudocal4anua, 83-85, 99, 135 clutch production time after, 92 laboratory experiments, 84, 92 male behaviour, 84 size-assortative, 84, 124 Maturation, Paeudocalanua, 136- 158 Maxillae, Paeudocalanua, 60 first maxilla, 35, 36, 55 second maxilla, 35, 36, 54, 55, 58 food Gltration, 54, 55, 58 Maximum growth rates, ctenophore populations, 282 Mean growth efficiencies, Pseudocalanua, 134 Mean productivity, phytoplankton, copper effects on, 422 Mediterranean amphipods in, 461 copepods, 14 dinoflagellate parasites in, 190 hydrocarbon levels in, 302 microplankton in, 461, 498, 490, 500 pelagic tar levels in, 295 phytoplankton populations, 417 pilchard in, 203 pollution, 244 Pseudocalanua in, 12, 14-15, 111 Red Sea animals migration to, 247 sprat in, 203 whiting in, 204 zooplankton in, 316, 316, 432, 433, 445,461, 501.502, 503, 605,506, 507, 508 Medusans, 267, 279, 457 CEPEX enclosure studies, 458 Membrane permeability, phytoplankton,412-413 Menai Straits, North Wales, heavy metal concentration in, 395 Mercury poisoning, 244 Mercury turnover, zooplankton, 431, 433, 434, 439, 461, 462, 463, 498, 50 1 chemical form effects, 440 faecal pellet production, effect on, 460 fecundity, effect on, 455 growth and development, effect on, 463

544

SUBJEOT INDEX

Metasome, Pseudoculanus, 29, 30, 31, 34 Metazoans, 1 7 Meteorological science, 242-243 Methane, 291, 294, 297 Methionine production, phytoplankton, 414 Methylanilines, 325 Methylbenzenes, 318 Methylbiphenyls, 318 Methylcholanthrene, 336, 343 Methylcyclohexane, 302, 318 Methylcyclopentane, 302, 318 Methylfluorenes, 318 Methylmercury, 416, 440, 461, 498, 602 Methylnaphthalenes, 318,357,359, 360 Methylpentanes, 318 Methylphenanthrenes, 318 Micro-algae freshwater, 327, 329 growth inhibition, hydrocarbons by, 326, 327 418 hydrocarbon biosynthesis, 305 tolerance, species of, 401 photosynthesis mechanism, hydroMeroplankton, 351, 364, 364 carbon molecules effect on, 329 petroleum hydrocarbon toxicity Micro-crustaceans, 343, 345 data, 358-360 heavy metal levels in, 439 Metabolic activity, zooplankton, Microdistribution, Pseudocalanus, 23 heavy metal effects on, 447-448 Microelectrophoretic techniques, 383 Metabolic requirements, ctenophores, Microflagellates 275, 277 heavy metal tolerance, 420, 421, 422 Metabolism, phytoplankton water soluble fraction (WSF) of oil, copper concentration effects on, 419, susceptibility to, 333, 334 423 Microfossils, 243 heavy metal effects on, 398-410,415 Micropalaeontology, 242 Metabolite retention, zooplankton by, Microplankton 343, 344 cadmium content, 498 Metal chromium content, 500 chelates, 387, 392, 394, 402, 439 copper content, 500 hydroxides, 391 heavy metal content, 498-500 Metal fluxes, zooplankton in, 428-434 lead content, 499 elimination rate relationship, 430 mercury content, 498 estimation, 430 nickel content, 499 food metal content relationship, 439 selenium content, 499 silver content, 499 radiolabelled studies, 428 zinc content, 500 rate constants, 434 Micro-tarballs, 316 Metal-organic complexes, 392, 394 Metal tolerance, phytoplankton species, Mid-Gulf, hydrocarbon levels in, 292, 297 400, 401

Mercury turnover, zooplanktoir -continued oxygen consumption, effect on, 447, 448 phototactic response, effect on, 455, 456 swimming rate, effect on, 456 Mercury uptake, phytoplankton, 384, 385, 387, 479-483 cell volume, effect on, 414 cellular content, 403 concentration-growth rate relationship, 405, 406, 407, 414, 415 diffusion coefficients, 388 driving concentration, 388 extracellularly bound, 387 giant cell production, 413 growth rate reduction, 415 natural populations, in. 426 oxygen evolution relationship, 413 photosynthesis inhibition, 416, 417 primary production, effect on 416,

SUBJEOT lXDEX

645

Millport, Scotland, Pseudocalanua off, Morphological abnormalities, phyto23, 58, 99 plankton, 413 Minamata, Japan Morphology, Pseudocalanua,27-37 phytoplankton off, 426, 498 adults (CVI), 31-37 zooplankton off, 461, 501, 502 copepodids (CI-CV), 29-31 Mississipi River plume, 461 embryo, 29 Mitochondria1 membrane, multinauplii, 27, 29 cellular algae, 329 Mortality, ctenophores, 281, 282 Mixed function oxygenases (MFO), 346 Mortality rates, Pseudocalanua, 177, 346, 347 178, 210 Mixed phytoplankton Motor oil, 328 cadmium content, 498 water-soluble fraction (WSF), 356, chromium content, 500 359 copper content, 500 Moulting zooplankton, heavy metal lead content, 499 elimination by, 430, 431, 433, 440, mercury content, 498 442 methyl mercury content, 498 Mouth, ctenophores nickel content, 499 beroids, 266 silver content, 499 Mnenz$opsb, 252, 255 zinc content, 500 Ocyropsis, 262 Mixed zooplankton Pleurobrachia, 259, 262 arsenic content, 506 Tentaculata, 259 cadmium content, 502 Mouth, Pseudocalanwr, 56 copper content, 505 Mucus release, ctenophores, 257, 267, lead content, 504 27 1 mercury content, 501 Mud-crab larvae, 452, 454, 456 methyl mercury content, 502 Multicellular algae, 329 nickel content, 603 biosynthesis, 331 silver content, 503 Muscle physiology, 241 zinc content, 508 Mussels, 236 Mobile, Alabama, 294 larvae, 453 Mollusca cephalopoda Mysids, 315 chromium content, 506 arsenic content, 506 copper content, 505 cadmium content, 502 lead content, 504 mercury content, 501 nickel content, 503 zinc content, 507 Molluscs, oil pollution effects on, 351 Monocyclic aromatic hydrocarbons, 291, 302 N phytotoxicity-molecular structure relationship, 330 NADPH dependent enzymes, 345 Monte Gargano, 296 Nanoplankton, 242 Monterey Bay, California Naphthalene, 300, 317, 318, 325 copepods in, 462, 463 algae growth inhibition by, 327, 328 heavy metal concentration in, 395, aqueous oil extracts, in, 327 assimilation, zooplankton by, 350 416, 462, 463 phytoplankton populations in, 427, faecal pellet release in, 348-351 462, 463, 498, 499, 500 lethal concentration, 354, 356 zooplankton populations in, 501, phytoplankton chemical composi502, 503, 504, 505, 507 tion, effect on, 330

546

SUBJEOT MDEX

Naphthalene-conted phytoplankton, toxic

effect on,

327-329

retention, copepods by, 337, 338, 339, 340, 341, 342

retention, zooplankton by, 336, 337, 350

unicellular algae photosynthesis, effect on, 328 zooplankton, toxic effect on, 354, 355, 359, 360

Naphthalene metabolism algae, 327, 328 copepods, 336-344, 349 crab larvae, 337, 343, 347 phytoplankton by, 327-329, 330 zooplankton by, 343 Naphthalenes, 301, 303, 304 Naphthenes, 300, 301, 302, 304 Naphthenoaromatics, 304 Narragansett Bay, Rhode Island, 268, 281

National Research Council of Canada, 2 Natural populations, phytoplankton copper tolerance, 424, 426 heavy metal concentrations in, 425428, 498-500

photosynthesis, heavy metals effect on, 416, 417, 418, 419, 422 Natural populations, zooplankton CEPEX enclosure studies, 458 copper tolerance, 467, 468 heavy metal concentrations in, 460463, 501-508

heavy metal toxic effects on, 457-460 Natural submarine oil seepage, 310 Nauplii, Cakaw, 3 Nauplii, copepods heavy metal effects on, 461,452, 463 Nauplii, Pseudocalanus, 3, 58 abundance relationships, 156, 157 body, 27, 28 cannibalism, females by, 95 carbon content, 126 development rate, 107-114, 135, 137, 183

die1 vertical migration, 166 excretion rate, 46 generations, 138 growth rate, 130, 189

Nauplii, Pseudocalanua-continued hatching, 105, 107 identification, 29 maturation, 135-158 maximal development rate, 112 microdistribution, 23 morphology, 27, 29 N I11 stage, 109, 112, 137 naupliar stages, 27,29, 109, 111, 112, 121, 137

nitrogen content, 126 ontogenetic migration, 159 phosphorus content, 126, 127 production periods, 92 respiration, 38, 43 seasonal migration, 162 size-water temperature relationship, 121

vertical distribution, 158, 161 Nauplii development rate, Pseudocalanua, 107-114 food SUPPIY effect, 112-113 temperature effect, 107-112 Nematodes, Pseudocalanue host infection, 197-198 " Nereistoxin ", 242 Nerve fibres, 240, 241 physiology, 240, 241 Net growth efficiency, Pseudocalanue, 132

Neuston, 316 New Jersey, 325 New York Bight, zooplankton in, 461 New York Harbour, hydrocarbon levels in, 299, 302 Nickel content, zooplankton, 462, 463, 499, 503

Nickel uptake, phytoplankton, 397 Nile Flood, 247 Niobium, 440 Nirate asaimfiation, phytoplankton, 423 excretion, ctenophores, 273 Nitrogen content ctenophores, 269 Peewlocalanua, 126 Nitrogen excretion, ctenophores, 272, 274

547

SUBJIGCT INDEX

Nitrogen excretion, Pseudocalanua, 44-49 body size-excretion rate relationship, 47 crowding effects, 45, 46, 47 food concentration effect, 45 measurement techniques, 44-45 nitrogen requirements, 48-49, 132 oxygen concentration effect, 48 phytoplankton nutrient requirement relationship, 200 salinity effect, 48 temperature effect, 47 Nitrogen uptake, phytoplankton, 423 Nomenclature, Pseudocalanus, 2-9 Non-migrant Pseudoca~anus,165, 175, 176, 177, 178 Non-polar hydrocarbons, 292 Non-volatile hydrocarbons, 299 Nordhvatn, Norway, 150 Norman Wells crude oil, 354 North America, eastern, Pseudocalanus off, 14 North American seaboard phytoplankton off, 463 zooplankton off, 461, 463, 501, 502, 504, 505, 506, 508 North Atlantic n-alkane levels in, 294 cod in, 203, 204 haddock in, 204 hake in, 205 herring in, 202 methane concentration in, 291, 297 pilchard in, 203 plaice in, 205 Pseudocabnus in, 13, 14, 16, 16, 168, 202 sandeels in, 205 sprat in, 203 tanker routes, 299 whiting in, 204 North Atlantic Drift, Pseudomlanua in, 12, 14, 294, 207 North Eastern Atlantic, fish stocks, 235 North Pacific herring in, 202 pink salmon in, 201 Pseudomlanuah, 12,16,16,202 temperate region, 16

North Pacific-continued sandlance in, 205 North Sea n-alkane levels in, 292, 297 Atlantic influence, 20 Bolinopsis in, 266 ctenophores in, 266 dinoflagellate parasites in, 190, 192, 193, 196 herring in, 202 off-shore oil production, 300 pelagic tar levels in, 295 Pseudocalanus in, 5 , 16, 20, 24, 81, 89, 97, 99, 101, 106, 107, 108, 109, 111, 117, 121, 122, 123, 130, 132, 133, 185-187, 189,202, 206 total hydrocarbon levels in, 299, 357 total particulate C, 113 zooplankton in, 502, 504, 505, 508 Northumberland coast, England, Pseudocalanus off, 16, 147-149 Norway coast, 150-152, 203 Norwegian Sea, Pseudocalanus in, 18, 19, 20, 80, 117, 152, 162, 163, 187, 196 Nova Scotia, 500, 505, 507, 508 Novaya Zemlya, 18 Nuda classification, 250 feeding mechanism, 265-267 food, 265-267 Nutrient excretion, Pseudomlanus, 200 Nutrient ions, phytoplankton, heavy metal ion concentration relation. ship, 396, 398, 402 Nutrient-plant-herbivor~arnivore dynamics model, 209 Nutrition, Psewlomlanus, 54-80 assimilation, 75-76 DieIs feeding rhythms, 72-75 feeding rate, 64-72 filter feeding, 54-57 food eaten, 58-64 , sustenance requirements, 76-79

0 Occurrence, ctenophores, 250 Ocean sun fish. 268

548

SUBJEUT INDEX

Oceanic circulation, 243 Oceanic ctenophores, 250 Oceanic plankton, heavy metal concentration in, 397 Octadecane, 336, 343 Offshore distribution, Pseudocalanus, 16

Ogac Lake, Baffi Island chaetognaths in, 206, 207 hydromedusans in, 207 Pseudocalanus, in 9, 10, 21, 23, 24, 25, 87, 96, 97, 99, 102, 103, 113, 118,123,126,137,138-140,156, 158, 159, 160, 167, 175, 182, 184, 189, 206 Offspring production, ctenophores, 275

Oil, water-soluable fraction

(WSF)

317, 318, 319-327, 363

Oil pollution, 243 planktonic communities, effect on, 351

oil sac, Pseudocalanus, 99, 125, 126 size variation, 128-129 Oil sedimentation, faecal pellets in, 348 Oil shales, 243 Oil slicks, 300 immobilization copepods by, 350 Oil storage, Pseudocalanus, 128-129, 157, 176

Oil tanker routes, hydrocarbon levels in, 299, 300, 301 Okhotsk Sea, Pseudocahnus in, 21 Olefinic hydrocarbons, 291, 308, 309 Ona, Norway, 150 One and a half-year life cycle, Pseudocalanus, 141 Ontogenetic migration, Pseudocalanus, 158-16 1

Oogenisis, Pseudomlanus, 81,86, 103 Oregon coast, Pseudocalanus off, 20, 23 Organic carbon content, ctenophores, 277

Organic metal complexes, 392,440 Organic nitrogen excretion, ctenophores 273 Organo-mercury compounds, 440, 484 “ Origin of Species ” (Darwin), book, 233

Ormers, 245 Oslo Fjord, Morway, 160

Ostracods, 311, 312 Outboard-motor oil, 320 Overfishing, 234, 235 Overwintering generation, Pseudocalanus, 138, 139, 141, 143, 144, 146, 147, 150, 152, 156, 157

vertical migration, 162, 163, 175 Ovid, 238 Oxygen consumption, ctenophores, 272 nitrogen excretion rate of Pseudocalanus, effect on, 48 toleration limits, Pseudocalanus, 25, 48

Oxygen consumption, Pseudocalanus, 37, 38

body size relationship, 38-40 light response, 42 Oysters, 236 larvae, 452, 454 predation, ctenophores by, 265

P Pacific herring, 202 sandlance, 205 tanker routes, 299, 301, 302 Pacific Ocean hydrocarbon levels in, 294 ‘‘ marine parks ”, 246 Pseudocalanus in, 13, 15, 168 phytoplankton populations in, 498, 499, 600 zooplankton in, 428, 430, 440, 501, 502, 503, 604, 505, 607, 608

Padan ” insecticide, 242 Paedogenesis, ctenophores, 276 Palaeoclimatic changes, 243 Pamlico River Estuary, North Carolina, 267, 279 Panama Canal, 248 Parachloro-mercuribenzene sulphonatte (PCMBS), 387, 388 Parclffins, 301 Parasites, Pseudocalanus of, 1 9 k 1 9 9 crustaceans, 198 dinoflagellates, 190-1 97 I‘

gregarines, 197

649

SUBJECT INDEX

Parasites, Pseudoca~anuaof-continued nematodes, 197 trematodes, 197 Particulate heavy metal elimination, zooplankton, 430, 431 Particulate hydrocarbons, sea water

in, 293-294, 298, 301, 316 n-alkanes, 289, 316 aromatic, 298 non-olehic, 298 unsaturated, 298 Particulate metals, sea water in, 392 Passamoquoddy Bay, 202 Patuxent River, Maryland, 279 P/B ratios, copepods, 181,183,184,185, 187, 188, 189

Pelagic food web, 209 Pelagic macruran crustaceans, 439 Pelagic tar, 295 Penguins, 244 Penicillin, 77 Pennate diatoms, copper tolerance, 419, 420, 421, 423

n-Pentane, 302 Peridinian dinoflagellates, 196 Perinaphthenone, 326 Pesticides, 242 Petroleum hydrocarbons, marine plankton pollution by, 289 et seq. Petroleum residues, sea water in, 293 Pharaohs, 237 Phenalen-1-one, 326, 354 Phenanthrenes, 301, 318 Phenols, 325 Phenylmercuric acetate, 413 Phoenicians, 238 Phosphorus content ctenophores, 269 Pseudocalanw, 126, 127 Phosphorus excretion, ctenophores, 273

Phosphorus excretion, Pseudocalanw, 49-51

body weight-excretion rate relationship, 50 food concentration effect, 49-50 measurement techniques, 49 phosphorus requirements, 50-51,132 phytoplankton nutrient requirement relationship, 200

Phosphorus excretions, Pseudocalanw +ontinu& salinity effect, 50 Photosynthesis, phytoplankton, 320, 32 1

copper effects on, 422, 424 heavy metal effects on, 416-425 hydrocarbon effects on, 323,329 mechanism disruption, hydrocarbon molecules by, 329 naphthalene, effect of, 327-329 radiocarbon studies, 327 rate determination, 415-416 stimulation, 323,330 water-soluble fraction (WSF) of oil, effects of, 322 Photosynthesis, unicellular algae, 322, 329, 364

supression, napthalene by, 329 Photosynthetic diatoms, 307 Photosynthetic rate, phytoplankton 14C uptake measurement, by, 416, 416-419

large volume enclosures in, 416, 419-425

measurement techniques, 416, 416 natural populations, 416, 418, 423, 424

Phototactic response, zooplankton, heavy metal effects on, 456-456 distillate oil fractions effect on, 323 Phylum Ctenophora, classification, 250 Physico-chemical nature, phytoplankton surface, 384 " Physiological " species, PBeudocalanua, 9 Phytadiene, 314, 317 Phytane, 291, 292, 297, 307, 314, 317 Phytol, 311 Phytol-derived hydrocarbons, 314 Phytophagous copepods, 188 Phytoplankton, 116, 157,290 n-alkane biosynthesis, 304, 306 alkene biosynthesis, 304 ammonium ion uptake, 423 annual hydrocarbon production, 310 aromatic hydrocarbon metabolism, 327, 328

batch culture, 398 1W-uptake,!321, 416, 416

560

SWBJEUT INDEX

P hytoplankton-continued carbon uptake, 424 cell division, 319, 327, 413, 414 cell populations, 403-404, 405, 414 chromium uptake, 427, 496 cobalt uptake, 397 continuous culture, 399 culture techniques, 398 diaIysis culture, 399 diffusion-controlled heavy metal ion uptake, 385, 386 edible biomass consumed, Pseudocalanus by, 199 electropositive ion uptake, 394 estuarine, 383 giant cells, 413-415 growth rate, 321, 325 heavy metal turnover, 382 et sep. hydrocarbon biosynthesis, 305-309 hydrocarbon levels in, 293, 305-309, 310 hydrocarbon source, as, 309-310 ingestion rate, Pseudocalanua, by, 66 lead uptake, 417, 418, 427, 488-490 manganese uptake, 395 maximum, 117 mean productivity, 422 membrane permeability, 412-413 metabolism, 398-410, 415, 419, 423 morphological abnormalities, 413 naphthalene uptake, 327-329, 330 nickel uptake, 397 nitrate assimilation, 423 nitrogen uptake, 423 nutrient ions, 396, 398, 402 nutrient requirements, 206 nutrients, 43 photosynthesis, 320, 321 predation, ctenophores by, 263, 279, 283 population data, 279, 404 potassium leakage, 412, 413 production estimates, 188 silica frustules, 423, 424, 427 silicic acid uptake, 423, 424 silver uptake, 397, 487 specific growth rate, 407, 408, 409 spring bloom, 20 strontium uptake, 427, 435 surface area, 383, 384

Phytoplankton-continued titanium uptake, 427 toxicity studies, 317-331 vertical migration of Pseudocalanua, effect on, 160, 161, 170, 171, 172 " yellow water ", in, 202 zirconium uptake, 435 Phytoplankton/zooplakton relationship, petroleum hydrocarbon effects on, 364 Phytotoxicity mechanisms, 329-331 Pilchard, 203 Pink salmon, 201 Pistol shrimp, 239 Plaice, 236 diet, 205 Planktivorous fish, 210 Plankton composition, 124 heavy nietal content, 461 petroleum hydrocarbon pollution, 289 et seq. predation, ctenophores by, 264, 278 sex ratios, 80 Plankton animals, vertical migration, 239 Planktonic algae, 243 Planktonic ctenophores, 250 offspring, 276 self fertilization, 275 Plasma membrane, multicellular algae, 329 Platyctenea, 260 asexual budding, 275 feeding mechanism, 263 Pliny, 238 Plymouth, England pilchard off, 203 PseudocIclanuaoE, 110,119,122,128, 146-147, 207 whiting off, 204 Poisonous marine plants and animals, 237-238 reference books, 237 Poisons, extraction, fish from, 237,240, 241 Polar Basin, Pseudoadanus in, 7 Polar cod, 204 Polonium. 431

661

SUBJEGT INDEX

Pollutants, Paeudocalanua toleration, 25-26, 27 Pollution, 243-244, 248

studies, marine plankton with, 289 el aeq. Polychaete worms, 242 larvae, 459 Polymodalism, Pseudocalanue, in, 8 Polynuclear aromatic hydrocarbons (DNAH). 302, 307, 335, 362 faecal pellet release in, 348-351 metabolism, marine animals by, 346, 347, 366

steroid metabolism, effect on, 357 Polyploids, 9, 10 Population density, phytoplankton, heavy metal uptake relationship, 404

Population dynamics ctenophores, 267, 268, 282 Paeudodanus, 156 Populations, ctenophore food density requirements, 282 growth rate, 278, 282 migration, 281 nitrogen turnover, 280 peak, 280 production rate, 280 seasonal variations, 277-282 total population respiration, 279 Populations phytoplankton, 279, 335, 404

Portuguese Man of War, 241 Portuguese waters, Pseudomhnue in, 12, 14

Postlarval fish, diet, 201, 202, 204 Potrnsium leakage, phytoplankton, 412, 413

Power station effluents, 244 Prasinophyceae, 306 Predation hypothesis, Paeudocahnus die1 migration, 174-175 Predators, ctenophores of, 267-268 Predators, Paeudocalaw of chmtognaths, 206-207 crustaceans, 206 ctenophores, 207-208, 264, 265 fishes, 201-206 food web significance, 208-210 hydromedusans, 207

Predators, Paeudocdanw of-continued vertical migration, 168, 174, 175 Prey capture beroids, 265 cestida, 263 Mnemiopsis, 252, 253, 254, 255 Ocyropaia, 262 Pleurobrachia, 259, 265 Primary production, eco-system, oil pollution effect on, 331, 332 Primary production, phytoplankton copper effects on, 422, 423 heavy metal effects on, 416-419 hydrocarbon effects on, 332 Pristane, 291, 292, 297, 304, 305, 307, 308, 335

biosynthesis, zooplankton by, 311, 312, 234, 316

Procaine, 241 Production, Pseudooalanue, 179-190 definition, 179, 180 estimates in nature, 182-190 estimation methods, 178-182 Production/biomass coefficients ctenophores, 278, 280, 281 Paeudocalanw, 181, 183, 184 Production estimates, ctenophores, 278 Production estimates, Paeudocakmua ‘‘ balance equation ” of growth method, 181, 188 Baltic Sea, 187 Black Sea, 183-184 cohort method, 180, 182, 187, 188 developmental stage growth rate method, 181, 183, 185, 189 factors involved, 188-190 North Sea, 185-187 Norwegian Sea, 187 Ogac Lake, B& Island, 182, 188 “ physiological method ”, 181, 185 radiocarbon tagging of food method, 184

Sea of Japan, 184-185 “turnover time” method, 181, 185, 186

White Sea, 188 Productive season, Paeudomlanue, 135, 136, 143, 146, 156, 157

vertical migration during, 161-163 Propane, 291

662

SUBJEOT INDEX

Protein composition, Pseudocalanua, 126

Radionuclides, downward transport, 44 1

Protozoa Radiolaria cadmium content, 502 copper content, 506 lead content, 604 mercury content, 601 nickel content, 603 silver content, 603 zinc content, 607 Prudhoe Bay crude oil, 360, 361 Pteropoda Gymnosomata copper content, 505 lead content, 604 nickel content, 603 zinc content, 508 Pteropoda Thecosomata chromium content, 506 copper content, 605 lead content, 604 nickel content, 503 zinc content, 508 Pteropods, 311, 312 heavy metal turnover, 429 Puerto Rico, zooplankton off, 461, 462, 502, 503, 504, 605, 508

Puffer fish, 237, 240, 241 Pyrosomatidae, heavy metal turnover, 429

Q Quahog clam larval, 358 Queensland coast, Australia jellyflsh off, 238 “ marine park ”, 246

R Radioactivity elimination, zooplankton, 428, 429, 430, 433 Radiolarians, 58, 427 cadmium content, 502 copper content, 505 lead content, 604 mercury content, 601 nickel content, 603 silver content, 603 zinc content, 607

Rance Estuary, France, 331 Rats, hydrocarbon metabolism, 346 ‘‘ Rattlesnake ”, ship, 233 Rearing experiments, Pseudocalanua, 81, 110, 111, 119, 128

Recreational Reserves, 247 Red algae, 329 growth stimulation, hydrocarbons by, 330 Red colouration, Pseudocalanua, 197 Red Sea, 247 phytoplankton populations, 417,418 Red seaweed, 237, 242 Regenerative powers, ctenophores, 276 Reproduction, Pseudocalanw, 80-100 egg laying, 81 food supply, relation to, 117 mating, 83-86 oogenesis, 8 1 parameters, female of, 91 reproductive rate, 85-99, 100, 143 sex ratio, 80-81 sperm production, 81-83 spermatophore production, 81-83 water temperature, relation to, 117 Respiration, ctenophores, 272-273, 279 Respiration, Pseudocalanua, 37-43 body size relationship, 38-40,41, 43, 132

food assimilation relationship, 76, 132

food requirement, 42-43 light response, 42 minimal food requirement prediction equation, 43 oxygen consumption, 38-42 rate prediction equations, 38, 39 temperature response, 40-42 “ Resting stage ” Pseudocalanua, 136, 163, 171

Rhodophyceae, 306, 307, 308 Rhodophyta Bangiophyceae cadmium effect on, 486 copper effect on, 491 lead effect on, 488 mercury effect on, 479 Ria de Arosa, Spain, 461. 601 RNA multicellular algae, 331

SUBJECT INDEX

Rock crab, 353 Romanian coast, 203 Roscoff, 294, 298, 302 RSMAS laboratory, 258

S S-adenosyl methionine, 414 Saanich Inlet, British Columbia ctenophores in, 267, 277 phytoplankton populations in, 419 Sagami Bay, Japan, 15, 507, 508 St. Lawrence, hydrocarbon levels in, 293 St. Margarets Bay, Nova Scotia, 208, 265, 279 Salinity embryonic development rate of Pseudocalanua, effect on, 102 metabolism of zooplankton, effect on 447 nitrogen excretion rate of Pseudocalanus, effect on, 48 phosphorus excretion rate of Pseudocalanua, effect on, 50 respiration rate of ctenophores, effect on, 272 toleration limits, Peeudocalanua 24-25, 27 Salmon, 235 diet, 201 Salps, 268, 274 heavy metal turnover, 429, 437 Sampling, Pseudocalanw, 22-23, 59 San Francisco Bay hydrocarbon levels in, 294 poisonous shellfish in, 238 Sand-dollar, 241 Sand launces, 205 Sandeels, 205 Sandlances, 205 Sardines, 203, 247, 268 Sargasso Sea heavy metal concentrations in, 395 hydrocarbon levels in, 295, 298, 357 pelagic tar levels in, 295 phytoplankton populations, 417, 418 Sam, G. O., 235 Saxitoxin, 241

663

Schizogony, Blastodiniurn, 192 Scientific Reserves, 246 Scores by Sound, East Greenland, 141 Scottish Waters n-alkane levels in, 292, 297 ctenophores in, 265, 277 SCUBA, 250, 258 Scyphomedusans, 267 Sea birds, oiling, 243 Sea-cucumbers, 440, 441 Sea-hare, 241 Sea of Azov, 247, 506 Sea of Japan pelagic ecosystem, 209 Peeudocalanua in, 7, 15, 24, 111, 165, 184-185, 206 zooplankton in, 507, 508 Sea urchins, 241, 246 larval, 452 Sea water, hydrocarbon levels, see Hydrocarbon levels, sea water in Sewonal bloom, ctenophores, 281, 282 Seasonal fluctuations, Pseudocalanua bodysize, 55, 102, 103, 116, 117, 118, 119 occurrence, 18-19 Seasonal migration, Pseudocalanw , 152, 161-163, 176, 179 Seasonal population variations, ctenophores, 227-282 Seaweeds, 236, 237 Second maxilla, Peeudocalanw, 35, 36, 64 food filtration, 54, 66, 68 setae, 54, 56, 60 setules, 54, 55, 60 Sedimentation, Pseudocalmus, 208 Sediments hydrocarbon levels in, 293,294, 305 heavy metal concentrations in, 397, 398,440 Selenium turnover, zooplankton, 431, 433, 434, 439, 603 Selenomethionine, 414 Self fertilization, ctenophores, 276 Semiannual life cycle, Pseudocalanue, 140 Sevastopol coast, 165, 183, 207 Sewage polluted waters, 238 Sex hormones, 366, 366

564

SUBJEOT INDEX

Sex ratios copepods, 80, 357 Pseudocalanus, 27, 80-81, 99 Sex reversal, Pseudo&nua, 193, 194 Sexual dimorphism, Pseudocalanus, 31 Sharks, 291, 311 Shellfish, 236, 244, 245 poisonous, 237, 238 predation ctenophores by, 265 Ship design, 238-239 Ships hulls corrosion, 238 fouling organism growth on, 238 Shipworms, 238 Shrimps, 237, 267 Silica content, Pseudocalanus, 127 Silica frustules, phytoplankton, 423, 424

metal contents, 427 Silicic acid uptake, phytoplankton, 423,424

Silver turnover, zooplankton, 455,460,462, 463, 499, 503

uptake, phytoplankton, 397, 487 Siphonophores, 261 Size-frequency distribution, Pseudocalanw, 138, 146, 147, 148, 150, 151, 152, 153, 154

Size-selective feeding, Psedocalanus, 60-63

electivity indices, 61, 62 seasonal variation, 61 Size shrinkage ctenophores, 275 Size-temperature relationship, Pseudocalanus, 9, 10, 189 Skate, 241 " Slick " copepod, 314, 315 Slipper limpet, 247 Snapping shrimp, 239 Sognesjeen, Norway, 150 Solar eclipses, 239 Pseudocalanucl response to, 172, 173 Sole, 236 Soluble heavy metal elimination, zooplankton, 430, 431, 433 Soluble heavy metal uptake, zooplankton, 436 Somatic production, Pseudocalanus, 180, 181

Somites, Pseudocalanus 30-34 Sonic listening, 236 Sorfjord, Norway, zooplankton in, 461 South America (Western), Pseudocabnus off, 13 Southampton, England, Pseudocalanus off, 38, 41 Soviet Far Eastern Seas, Pseudocalanus in, 7 Spanish waters, Pseudocalanus in, 14 Spatial distribution, petroleum hydrocarbons, 363 Spawning ctenophores, 276 Pseudocalanus, 150, 152 Species description, Pseudocalanus, 4-9 delimitations, 6-9 Specific food ingestion rate, zooplankton, 439 Specific growth rate, phytoplankton, heavy metal effects on, 407, 408, 409

Sperm production, Pseudocalanus, 81-83

Sperm whales, 311 Spermatophore production, Pseudocalanus, 81-83 Spider crab, 246 Spiny dogfish, 241 Split, Yugoslavia, 21 Sporocytes, Blaatodiniurn, 192, 193 Spot shrimp, naphthalene metabolism, 347,348

Sprat, 203 Squalene, 291, 314, 316 Squid, 235, 240, 241 " Solar " oil, 352 South Louisiana crude oil, 318,328,365 water-soluble fraction, 321, 359 Stage abundance, Pseudocalunus copepodids, 143,155,156,157,186 production number relationship, 186 Starfish, 245 Starvation, Mnenaiopsis, 255, 257, 267, 275

Steroid metabolism, zooplankton, 345, 356, 357, 365

Stockholm, 21 Stored oil, Pseudocalanua, 99 Strait of Georgia, 201, 205

565

SUBJEOT INDEX

Strait of Otranto, Pseudocalanus in, 15 Strathcona Sound N. B a n Island, 502, 505, 506, 507

Stratigraphy, 243 Streptomycin, 77 Strong migrants, Pseudocalanua, 165 Strontium alginate binding, 242 turnover, zooplankton, 435 uptake, phytoplankton, 427, 435 Structural formula, crude oil hydrocarbon types, 304 Sturgeon, 247 Subaqua diving, 245 Submarines, 239 Subspecies, Psedocalanw, 7 Sub-tropical zooplankton, 449, 455 Suez Canal, 13, 247 Sulphur affinity, heavy iiietals, 412 Sulphydryl inhibitors, 423 “ Superfluous ” feeding, Pseudocalanus,

Swimming action, ctenophores --continued Temora, 265 Swimming action, Mnemiopsia, 255, 257

food concentration effect, 265, 258 Swimming feet, Pseudocalanua, 30, 31, 36, 37

Swimming pattern, Pseudocalanus, 51-53, 265

escape reaction, 63 mating, prior to, 84 Swimming rate, zooplankton, heavy metal effects on, 456 Sylt, P s e d o d a n w , off, 110, 113 Synergism, heavy metal phytoplankton growth rate relationship, 411-412 zooplankton, growth rate relationship, 451, 453, 454, 456

200

Surf clams, 447 Surface area, phytoplankton, 383 physico-chemical nature, 384 Surface layers, sea, annual heavy metal fraction loss from, 442, 443 Surface micro-layer, hydrocarbon levels in, 294, 295, 298 Surface waters n-alkanes in, 294, 295, 296 hydrocarbon levels in, 294-297, 302 Suruga Bay, Japan, 507 Suspended sediments, hydrocarbon levels in, 294 Sustenance food requirements, Pseudocalanus, 7 6 7 9 amount, 76-77 quality, 77-79 Sweden, west coast, 149 Swimming action, ctenophores beroida, 267 Bolinopsis, 261 Callianira, 261 Cestida, 262 lobate ctenophores, 263, 254, 255, 261

Ocyropsia, 262 Oithona, 265 Pleurobrachia, 259, 260

T Tagmata, Pseudocalanw, 31, 32 Tanquary Fiord, Ellesmere Island, Pseudocahnus, in, 118, 136-1 38 Tar, 295 Taxonomy Blaatodinium hyalinum, 190 Dissodinium pseudocalani, 194 Teeth, Pseudocalanus, 56 dorsal, 57 “ edge index ” (E.I.), 57 ventral, 57 Temperature body size of Pseudocalanus, effect on, 115-122, 123-124, 131, 147 copepodids development rate of Psedocalanus, effect on, 107-112, 189

die1 migration of Pseudocalanus, effect on, 167, 172, 176 egg clutches of Pseudocalanus, effect on, 91, 96 egg matter production rate of Pseudocalanus, effect on, 131, 132

embryonic development rate of Pseudocalanus, effect on, 101-102, 107

660

SUBJEUT INDBIX

Temperatur+continued feeding rate of Pseudocalanus, effect on, 70-71 growth rate of ctenophores, effect on, 274 growth rate of Pseudocalanus, effect on, 130, 131, 134, 185 longevity of Pseudocalanua, effect on, 114, 115 metabolism of zooplankton, effect on, 447 nauplii development rate of Pseudocalanw, effect on, 107-112 nitrogen excretion rate of Pseudocalanua, effect on, 47 oil sac size of Psedocalanus, effect on, 128 respiration rate of ctenophores, effect on, 272 respiration rate of Pseudocalanus, effect on, 40-42 successive generations development rate of Pseudocalanw, effect on, 144, 147, 151, 176 toleration limits, Pseudocalanus, 23-24, 26 vertical migration of Pseudocalanus, effect on, 160, 179 Temporal variations, Pseudocalanus, 18-20 Tentacles, ctenophores Cestida, 263 Hormiphora, 259, 261 Ocyropsis, 262 Pleurobrachia, 265 Vallicula, 263 Tentacles, Mnemiopsis, 252, 253 setting, 256, 256, 257 Tentacles, Pleurobrachia, 259 destruction ”, copepods by, 268 Tentaculata classification, 250 feeding mechanism, 259-263 food, 263-265 ingestion rate, 270 swimming action, 260, 261 Tentaculata-Platyctenea,250 Tentaculatan ctenophores, 207, 208 Tentaculate feeding, Mnemiopsia, 251, 259

Terrestrial plants, 329 Tessiarsuk, Labrador, PseudocaZanus in, 21, 117, 118, 137, 140-141, 168, 207

Tetra-cyclic aromatics, 301 Tetralins, 304 Tetrodotoxin, 241 Texas coast, 354 Thin-layer chromatography, 302 Thioglycollic acid chelating agent, 387 Thoracic appendages, Pseudocalanus, 37 Thoracic segments, Pseudocalanus, 4 Thorax, Pseudocalanus, 30, 31, 33 Tidal pool copepods, 352 Tintinnids, water soluble fraction (WSF) of oil, susceptibility to, 333, 334 Titanium uptake, phytoplankton, 427 Tokyo Harbour, hydrocarbon levels in, 299, 303 Toluene, 317,322,324,330 Toluidines, 325, 326 “ Torrey Canyon ” ship, 243, 290 Total hydrocarbons, 296,297,298,299, 30 1 Total mineral oil hydrocarbons, 296, 299 Total population respiration, ctenophores, 279 Tourism, natural ecology, effect on, 244, 245 Toxic metal oxides, 382 Toxicity behaviour, phytoplankton crude oils, towards, 319-326 growth-rate inhibition, 321, 322, 326 naphthalene towards, 327-329 photosynthesis inhibition, 322, 323 seasonal variations, 321 water-soluble fractions of oils, using, 319-327, 358-361 Toxicity behaviour, zooplankton aromatic hydrocarbons, towards, 354 crude oil, towards, 362-354, 359-361 heavy metals, towards, 446-457 reproduction aspects, 356-357 water soluble hydrocarbons, towards, 354-356, 359-361 Toxicity data, crude oil and components, 368-361

657

WBJEaT INDEX

Trematodes, Paeudocalanus host infection, 197 Trishydroxymethylamino methane (TRIS) chelating agent, 392, 402 Trojans, 238 Trophic levels, hydrocarbon transfer to, 339, 341 Trout, hydrocarbon metabolism, 346 Tuna, 235 Tunny, 233 Turbot, 206, 236 “ Turnover times ”, Pseudocalanus production, 181, 185, 186 Two-year life cycle, Pseudocalanus, 137, 141

U Ultra violet fluorescence spectroscopy, 293, 296, 303

Underwater structures, 238 Ungava Bay, northern Quebec, 87,118, 141, 158

Unicellular algae .n-alkanes in, 305, 307, 308-309 detoxification mechanisms, 364 heneicosahexaene biosynthesis, 306 hydrocarbon biosynthesis, 305, 307, 308-309

hydrocarbon source as, 309 photosynthesis, 322, 329, 304 Unicellular flagellates, 236 blooming, 238 United States Eastern Coast phytoplankton off, 463 zooplankton off, 461, 463, 501, 502, 604, 605, 506, 508

Upwelling waters heavy metal concentration in, 397 phytoplankton populations in, 426 Urea, 44, 273 Urochordata Thaliacea arsenic content, 506 cadmium content, 502 chromium content, 506 copper content, 505 lead content, 504 mercury content, 501 nickel content, 503 zinc content, 508

Urosomes, Pseudodanua, 7, 8, 29, 30, 31

V Vancouver Island, Paeudodanua at, 12

Veliko Jezero, 167 Venezuelan crude oil, 296, 320, 321, 353, 354, 358, 359, 361

Venomous marine plants and animals, 237-238

Venus’ girdle, 266 Vertical distribution nitrites, 22 Pseudocalanus, 20-22, 27, 158-161. 164, 172, 173, 206

Vertical migration, Paeudocalanus, 72, 158-182, 200

adaptive value, 173-174, 179 diel, 163-179 diminished light response, 172, 173 dusk and dawn rise, 173 energy consumption, 173, 175 feeding rhythm relationship, 73, 74 ontogenetic, 158-1 61 seasonal, 161-163 thermally stratified waters, in, 175, 178

unstratified waters, in, 176 Vertical migration, zooplankton, 441, 442

Vertical tmnsfer, heavy metals, 441, 442

detritus sinking, by, 444, 445, 446 zooplankton activity, by, 443 Vitamin B,,, 407 Volatile hydrocarbons (C, to C8), 299, 302

Von Bertalanffy’s growth equation, 177

w Washington State waters, 208 Water clearance rate copepode, 436 ctenophores, 271,279 Water masses, Paeudocalanua distribution in, 15-16

568

SUBJEOT INDEX

Water solubility, aromatic hydrocarbons, toxicity relationship, 330 Water-soluble fraction (WSF), oil 317, 318, 363 eco-system, effect on, 333 hydrocarbon contents, 318 lethal concentrations, 354 phytoplankton toxicity studies, in, 319-327 zoopIankton toxicity studies, in, 354-356, 358-361 Weak migrants, PeewEocalanw, 165 Weather, short term changes, 243 Weight -length relationship, copepods, 127-128, 185 production estimation, in, 189 Welsh coast, 205 West African coastal waters n-alkane levels in, 294, 298 hydrocarbon levels in, 299, 302 West Greenland, 506 Wet weight ctenophores, 269 Pseudocalanw, 124, 186, 187 Whales, 239 White sea, Pseudoca2anus in, 8, 18, 23, 81, 127, 167, 188 Whiting, 204 Winter migration, Pseudooalanw, 162 Winton Bay, B a n Island, Pseudocalanua in, 10, 123, 138 Woods Hole, Massachusetts phytoplankton in, 307 Ps&ocaZanua in, 24, 40, 41, 99 World distribution, Pseudocalanira. 11-16 World’s oceans annual hydrocarbon input, 310 crude oil imputs, 309, 310 phytoplankton hydrocarbon input, 310 Wrasse, 246

X Xmthophyceae, 306, 307, Xenobiotics, 346, 356, 365 Xylenes, 302, 322, 324, 330

308

Y Yatsushiro-kai, Japan, 498, 601, 502 Year -to-Year abundance, Pseudocalanus, 19-20 York River estuary, Virginia, 279 Yucatan Strait, non-polar hydrocarbon levels in, 292, 294, 297

Z zinc ocean residence time, 446 surface layers, removal from, 443 vertical transport, 444, 445, 446 Zinc turnover, zooplankton, 429, 430, 433, 434, 437, 439, 442, 460, 462, 463, 500, 507-508 chemical form effects, 439, 440 growth and development, effect on, 452,454 Zinc uptake, phytoplankton, 384, 385, 386, 387, 427, 497 diffusion controlled transport, 391 driving concentration, 388 extracellularly bound, 387 intracellular, 390 mechanism, 390 metabolic control, 389 primary production, effect on, 396, 41 7 radioactive tracer investigations, 394 synergistic effects, 41 1 Zirconium surface layers, removal from, 443 turnover, zooplankton, 435 uptake, phytoplankton, 435 Zooplankton, 20, 23, 26, 202, 205, 249, 262, 290 aromatic hydrocarbon hydroxylation, 343, 346 aromatic hydrocarbon metabolism. 342-348 arsenic content, 460, 461, 506 assimilation efficiency, 350 biomass, 317 caromsea, 440 chromium content, 500, 506 development, 450-456

SUBJECT INDEX

Zooplankton-continued development rate, 176, 451-455 digestive efficiency, 271, 360 diurnal vertical migration, 441 egg production, 431, 451, 464 environmental stress resistance, 456-457

excretion rate, 43, 45, 47, 49, 51 faeces, 272, 295, 348-351, 363, 430, 431,432,433,440,449,450,455, 459 fecundity, 454-455 food ingestion rate, 439, 448-450 generation time, 135 grazing rate, 436 growth rate, 132, 134, 277, 450-455 heavy metal turnover, 428 et seq hydrocarbon biosynthesis, 305, 311-317 hydrocarbon fate in, 335-351 hydrocarbon levels in, 3 11-31 7 hydrocarbon metabolism, 342-348 hydrocarbon retention, 292,336-339, 340 ingestion rate, 448-450, 459

labelled hydrocarbon retention, 335-344, 348, 349

lipid levels in, 313, 315,316, 317, 364 metabolic activity, 447-448 metabolite retention, 343, 344 moulting, 430, 431, 433, 440, 442 naphthalene metabolism, 336, 337, 350

nickel content, 462, 463, 499, 603 nitrogen excretion, 273, 280 oil ingestion, 295

569

Zooplankton-continued oxygen consumption, 37, 447 parasitized, 196 particulate heavy metal elimination, 430, 431

phototactic response, 455-456 phytophagous, 188 phytoplankton consumption, 188 population data, 279, 281 predation, ctenophores by, 262, 264, 279, 280

production estimates, 187, 188, 278 radioactivity elimination, 428, 429, 430,433

reproduction,hydrocarbon effectson, 356-357

respiration rate, 39, 447 seasonal variations, 227 seIenium content, 431, 433, 434,439, 503

silver content, 455, 460, 462, 463, 499, 503

soluble heavy metal elimination, 430, 431, 433, 436

specific food ingestion rate, 439 steroid metabolism, 356, 357 strontium content, 438 sub-tropical, 449. 455 succinic dehydrogenase activity, 37 swimming rates, 456 toxicity studies, 351-362 vertical distribution, 265 vertical migration, 173,179,441,442 water soluble fraction (WSF) of oil, susceptibility to, 333 zirconium content, 435


Cumulative Index of Titles Alimentary canal and digestion in teleosts, 13, 109 Antarctic benthos, 10, 1 Artificial propagation of marine fish, 2, 1 Aspects of stress in the tropical marine environment, 10, 217 Aspects of the biology of seaweeds of economic importance, 3, 106 Behaviour and physiology of herring and other clupeids, 1, 262 Biological response in the sea to climatic changes, 14, 1 Biology of ascidians, 9, 1 Biology of coral reefs, 1, 209 Biology of euphausiids, 7, 1 Biology of pelagic shrimps in the ocean, 12, 233 Biology of Pseudoca~anu8,15, 1 Biology of wood-boring teredinid molluscs, 9, 336 Blood groups of marine animals, 2, 86 Breeding of the North Atlantic freshwater eels, 1, 137 Circadian periodicities in natural populations of marine phytoplankton, 12, 326 Diseases of marine fishes, 4, 1 Effects of heated effluents upon marine and estuarine organisms, 3, 63 Estuarine fish farming, 8, 119 Fish nutrition, 10, 383 Floatation mechanisms in modern and fossil cephalopods, 11, 197 General account of the fauna and flora of mangrove swamps and forests in the Indo-West Pacific region, 6, 74 Gustatory system in fish, 13, 63 Interactions of algal-invertebrate symbiosis, 1 : l Habitat selection by aquatic invertebrates, 10, 271 Learning by marine invertebrates, 3, 1 Management of fishery resources, 6, 1 Marine biology and human affairs, 15, 233 Marine molluscs as hosts for symbioses, 5, 1 Marine toxins and venomous and poisonous marine animals, 3, 266 Methods of sampling the benthos, 2, 171 Nutritional ecology of ctenophores, 15, 249 661

562

CUMULATIVE INDEX OF TITLES

Parasites and fishes in a deep-sea environment, 11, 121 Particulate and organic matter in sea water, 8, 1 Photosensitivity of echinoids, 13, 1 Physiological mechanisms in the migration of marine and amphihaline fish, 13, 248

Physiology and ecology of marine bryozoans, 14, 285 Physiology of ascidians, 12, 2 Plankton as a factor in the nitrogen and phosphorus cycles in the sea, 9, 102 Pollution studies with marine plankton: Part 1. Petroleum hydrocarbons and related compounds, 15, 289 Part 2. Heavy metals, 15, 381 Present status of some aspects of marine microbiology, 2, 133 Problems of oil pollution of the sea, 8, 215 Rearing of bivalve mollusks, 1, 1 Recent advances in research on the marine alga Acetabularia;, 14, 123 Respiration and feeding in copepods, 11, 57 Review of the systematics and ecology of oceanic squids, 4, 93 Scatological studies of the bivalvia (Mollusca), 8, 307 Some aspects of the biology of the chmtognaths, 6,271 Some aspects of neoplasia in marine animals, 12, 151 Some aspects of photoreception and vision in fishes, 1, 171. Speciation in living oysters, 13, 357 Study in erratic distribution: the occurrence of the medusa Cfonionemucr in relation to the distribution of oysters, 14, 251 Taurine in marine invertebrates, 9, 205 Upwelling and production of fish, 9, 255

Cumulative Index of Authors Allen, J. A., 9, 205 Ahmed, M., 13, 357 Arakewa, K.Y., 8, 307 Balakrishnan Nair, N., 9, 336 Blaxter, J. H. S., 1, 262 Boney, A. D., 3, 105 Bonotto, S., 14, 123 Bruun, A. F., 1, 137 Campbell, J. I., 10, 271 Cerroz, J. E., 6, 1 Cheng, T. C., 5, 1 Clarke, M. R., 4, 93 Corkett, C. J., 15, 1 Corner, E. D. S., 9, 102; 15, 289 Cowey, C. B., 10, 383 Cushing, D.H., 9,255; 14, 1 Cushing, J. E., 2, 85 Davies, A. G., 9, 102; 15, 381 Davis, H. C., 1, 1 Dell, R.K., 10, 1 Denton, E. J., 11, 197 Dickson, R.R., 14, 1 Edwards, C., 14, 251 Evans, H. E., 13, 53 Fisher, L. R., 7, 1 Fontaine, M., 13, 248 Garrett, M. P., 9, 205 Ghirardelli, E., 6, 271 Gilpin-Brown, J. B., 11, 197 Goodbody, I., 12, 2 Gulland, J. A., 6, 1 Hickling, C. F., 8, 119 Holliday, F. G. T., 1, 262 Kapoor, B. G., 13, 53, 109 Loosanoff, V. L., 1, 1

Lurquin, P., 14, 123 McLaren, I. A., 15, 1 Macnae, W., 6, 74 Marshall, S. M., 11, 57 Mauchline, J., 7, 1 Mawdesley-Thomas, L. E., 12, 151 Mszza, A., 14, 123 Meadows, P.S., 10, 271 Millar, R. H., 9, 1 Millott, N., 13, 1 Moore, H. B., 10, 217 Naylor, E., 3, 63 Nelson-Smith, A.,8, 215 Nicol, J. A. C., 1, 171 Noble, E.R., 11, 121 Omori, M.,12, 233 Pevzner, R.A., 13, 53 Reeve, M. R., 15, 249 Riley, G. A., 8, 1 Russell, F. E., 3, 256 Russell, F. S., 15, 233 Ryland, J. S., 14, 285 Saraswathy, M.,9, 336 Sargent, J. R., 10, 383 Scholes, R.B., 2, 133 Shelbourne, J. E., 2, 1 Shewan, J. M., 2, 133 Sindermann, C. J., 4, 1 Smit, H., 13, 109 Sournia, A., 12, 236 Taylor, D. L., 11, 1 Verighina, I. A., 13, 109 Walters, M. A,, 15, 249 Wells, M.J., 3, 1 Yonge, C. M., 1, 209

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