Advances in Ecological Research, Volume 4

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ECOLOGICAL RESEARCH VOLUME 4

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Advances in

ECOLOGICAL RESEARCH Edited by

J. B. CRAGG Enviroiintental Sciences Centre (Kananaskis) University of Calgary, Calgary, Alberta, Canada

VOLUME 4

1967

ACADEMIC PRESS London and New York

ACADEMIC PRESS INC. (LONDON) LTD. BERKELEYSQUHOUSE BERKELEYSQUARE LONDON,W.l

U.S. Edition published by ACADEMIC PRESS INC. 111 FIFTHAVENUE,NEW YORK10003, NEW YORK

Copyright @ 1967 by Academic Press Inc. (London) Ltd.

All rights reserved NO PART OF THIS BOOK MAY BE REPRODUCED I N ANY FORM BY PHOTOSTAT, MICROFILM OR ANY OTHER

MEANS,

WITHOUT WRITTEN PERMISSION FROM TEE PUBLISHERS

Library of Congress Catalog Card Number: 62-21479

Printed in Great Britain by W. S. Cowell Ltd, at the Butter Market, Ipswich

Contributors to Volunie 4 F. J. EBLINO, Department of Zoology, The University, Shefield, England. J. A. KITCHINO, School of Biological Xciences, University of East Anglia, England.

RICHARD S . MILLER,Department of Biology, University of Saskatchewan, Saskatoon, Canada.

N. W. MOORE, Monks Wood Experimental Station, Abbots Ripton, Huntingdon, England. B. STONEHOUSE, Department of Zoology, Canterbury University, Christchurch, New Zealand.

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Preface Man, not for the first time in his existence, must come to terms with his environment. I n the past it has been relatively small groups who have wasted the habitat around them and have either managed to move on to fresh areas or have died from hunger and thirst. Mankind, through the population and technological explosions, is now faced with major problems of adaptation on a global scale. No longer are the soils, waters and atmosphere of the world capable of sustaining indefinitely the products which he thrusts into them. Yet, in spite of his vast knowledge and notwithstanding the biological advances surrounding the letters D.N.A., man is woefully ignorant of how complex natural systems of organisms work. It is on the working of these systems that the capacity of the biosphere to deal with man’s food problems, and not least the waste materials of his industrial civilization, depends. Ecology must play a central role in rescuing man from some of his errors. Its importance has been recognized by at least one member of a major government. Mr. Stewart L. Udall, U.S.A. Secretary of the Interior, has said “Our time has already been labelled the Atomic Age and the Space Age. To my way of thinking it will more likely be known as the Era of Ecology. As history moves on our time will be known as the age in which man learned to admit that he is part of the balance of nature.” In Advances in Ecological Research an attempt is being made to see that a wide range of ecological viewpoints are expressed and that whilst advances are recorded, the blank areas where more attention is needed are also exposed. In this volume, four very different themes are presented. Dr. Richard S. Miller of the University of Saskatchewan, who has a wealth of experience of ecological thinking on both sides of the Atlantic, presents a refreshing analysis of the meaning of competition: “Why should several species share a common energy source if one species could take all the energy?’’is one of the questions which he poses. Professor J . A. Kitching and Dr. Ebling have, for many years, led parties of students to a delightful marine area on the coast of Ireland-Lough Ine. Here, for the first time, is a comprehensive review of their work. It demonstrates the extent to which student parties can be utilized to gather basic ecological information and it shows the knitting together of community analysis and experimental studies to explain why particular vii

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organisms occur where they do. Dr. Bernard Stonehouse of the University of Canterbury, New Zealand, reviews the biology of penguins from long experience of field work in the Antarctic. Penguins are among the most successful of bird species and in their land phase constitute ideal material for a range of studies on population dynamics and behaviour, particularly social behaviour. I n spite of the attention they have already attracted it is clear from Dr. Stonehouse’s review that they are a group which deserve very much more study than they are at present receiving, and that studies on them can provide information of great usefulness to students of population dynamics. Dr. Norman Moore, Head of the division concerned with toxic chemicals at the Nature Conservancy’s Station, Monks Wood, England, reviews pesticides as an ecological problem. A considerable amount has been written about the dangers from pesticides but most publications have been concerned with pesticides in specific cases. Dr. Moore makes the case that pesticides are a new ecological factor and that their influence within total ecosystems must be investigated. I n looking at their effects from the ecologist’s point of view, he exposes only too clearly the serious gaps in our knowledge. All four contributions form part of the framework of modern ecology. The accumulation of facts is necessary in order to understand, from the practical point of view, the working of ecological systems. At the same time, there must be a search for theoretical concepts which can be applied generally to communities and to ecosystems. We are still a long way from providing an adequate theoretical framework for explaining the mode of functioning of ecosystems. It is hoped that this series, by exposing both progress and areas of ignorance, will help to bring a more general theoretical ecology into being. J. B. CRAW February, 1967

Contents CONTRIBUTORSTO VOLUME 4 -ACE

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V

vii Pattern and Process in Competition

RICHARD S. MILLER I. Introduction 11. The Nature of Competition A. The Process of Competition B. Component Elements of Competition 111. The Ecological Niche A. Historical Development of the Niche Concept B. Niche Relationships IV. Competition in Nature A. Distribution Patterns B. Community Composition C. Species-Abundance D. Character Displacement E. Invasions V. Conditions of Coexistence VI. Conditions of Competitive Exclusion A. Mammals B. Birds C. Amphibia D. Crustacea E. Insects VII. Species Diversity References - -

1 6 7 8 15 15 17 20 21 26 28 30 31 33 48 49 65 57 58 60 65 69

A Synopsis of the Pesticide Problem N. W. MOORE I. Introduction - A. Definitions B. The Study of Pesticides aa an Ecological Problem 11. The Nature of the Pesticide Problem and the Types of Research Necessary for Studying It - 111. Pesticides as an Ecological Factor: Its Development and Present Magnitude IV.The Main Characteristics of Pesticides as an Ecological Factor A. Common Characteristics B. ToxicityC. Persistence and Solubility .. - D. Interaction of Pesticides - - A*

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CONTENTS

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V. Ecological Effects on Single Species A. Introduction B. Toxic Effect on a Species-Direct Effects C. Toxic Effect on a Species-Delayed Effects D. Reduction of Food Species E. Reduction of Habitat F. Removal of a Competitor G. Removal of a Predator VI. Effects on Ecosystems A. Introduction B. Effects on Diversity C. Effects on Production D. Effects on Succession VII. Pesticides and Evolution VIII. Application of an Ecological Approach to Pesticides A. Control of Pests and Pesticides B. Pesticides as Tools for Ecological Research IX. Conclusions on Pesticide Effects A. Comparisons with other Factors B. Pesticides as Part of a Developing System X. Summary Acknowledgments References -

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104 104 105 106 107 108 108 110 110 110 111 114 115 116 117 117 121 121 121 122 125 125 126

The General Biology and Thermal Balance of Penguins

B. STONEROUSE

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I. Introduction 11. TheEnvironment A. Species Distribution and Numbers B. Sea Temperatures and Terrestrial Climates C. Food, Nest Sites and Predators 111. Morphology, Metabolism and Heat Balance A. Form and Metabolism B. Heat Balance: Some Conclusions Acknowledgments References -

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131 136 136 158 165 173 173 188 191 192

Ecological Studies a t Lough Ine

J. A. KITCHINQ and F. J. EBLING I. Introduction 11. The Topography of Lough Ine 111. Hydrography A. Introduction B. Tides C. TheRapids D. TheLough IV. Inf3uence of Current A. Distribution in relation to Current B. Mode of Action -

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198 201 205 205 205 207 213 222 222 227

CONTENTS

V. Distribution in relation to Shelter and Wave-exposure A. Introduction B. The Littoral Region C. The Sublittoral Fringe D. The Sublittoral Region E. Wave Action in Comparison with Current F. The Fauna of Laminarian Algae VI. Zonation A. Introduction B. The Distribution and Characteristics of Patella Species C. Sublittoral Distribution in the Lough VII. Predation and Grazing A. Introduction B. Mytilzcs edulis C. Thais (Nucella)lap&a D. Paracentrotzcs and Predatory Crabs E. Paracentrotus and Algae F. Distribution of Crabs G. Conclusions VIII. Synecology Acknowledgment References AUTHORINDEX

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Pattern and Process in Competition RICHARD S

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MILLER

Department of Biology. University of Saskatchewan. Smkatoon. Canada I. Introduction ......................................................... I1. The Nature of Competition ............................................ A The Process of Competition......................................... B. Component Elements of Competition................................ I11 The Ecological Niche ................................................. A . Historical Development of the Niche Concept......................... B Niche Relationships............................................... I V Competition in Nature ................................................ A Distribution Patterns .............................................. B. Community Composition........................................... C Species-Abundance................................................ D Character Displacement ............................................ E Invasions ........................................................ V Conditions of Coexistence.............................................. V I Conditions of Competitive Exclusion.................................... A Mammals......................................................... B Birds ............................................................ C Amphibia........................................................ D Clustacea ........................................................ E Insects ........................................................... V I I . Species Diversity ..................................................... References...............................................................

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I. INTRODUCTION The development of competition theory has traditionally included three stages: (1) inferences drawn from observation of natural populations. (2) construction of mathematical models and (3) laboratory experiments designed to test elements of competitive interactions in controlled environments. Unfortunately. even though competition has occupied the minds of scientists in various biological disciplines for many years and is presumed to be a dominant force in biological evolution. remarkably few testable hypotheses have emerged and almost all of our conclusions about the importance of competition in natural systems are still based on speculation and inference. Darwin (1859) assigned a major role to competition between closely related species in the process of natural selection. He wrote. “As the 1

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species of the same genus usually have, though by no means invariably, much similarity in habits and constitution, and always in stmcture, the struggle will generally be more severe between them, if they come into competition with each other, than between the species of distinct genera.” He cited examples of the increase of the missel-thrush at the expense of the song-thrush in Scotland, invasions in which one species of rat has displaced another, the spread of the Asiatic cockroach a t the expense of a cogener, and the extermination of the native stingless bee of Australia by the imported hive bee. Darwin also stated one of the central problems of competition theory, which exists today as it did then, when he said “We can dimly see why the competition should be most severe between allied forms, which fill nearly the same place in the economy of nature; but probably in no one case could we precisely say why one species has been victorious over another in the great battle of life. ’’ The well-known mathematical models that were subsequently developed by Volterra, Lotka and Gause from extensions of the logistic theory, to describe population growth in single- and two-species systems, were attempts to state in mathematical terms the events that naturalists such as Darwin had recorded from field observation. I n logistic theory, each individual that is added to a population N reduces the growth capacity of the population by a constant increment. Population growth is thus described by a sigmoid curve in which N approaches an upper asymptote K , which represents the carrying capacity of the environment. If two species with carrying capacities K , and K , comPete for the same resource in the same environment, and if an individual of either species reduces the growth capacities of both populations, the growth of the two species can be represented by the following equation system :

where N , and N , are the numbers of each species, r1 and rz are their respective rates of increase, and K , and K , are carrying capacities or saturation values determined by growing each species alone in this environment. The term B/K2is the inhibitory effect of N , on the growth of N , and a/K, is the reciprocal effect of N , on N,. The outcome of competition will then depend on the inequalities tc > K,/K, and B > K,/Kl.

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Volterra (1926) and Lotka (1932) used this equation system to demonstrate that two species using the same resources cannot coexist indefinitely in a limited environment, and Gause (1935) confkmed this conclusion experimentally. The competitive exclusion principle that emerged as a result of this research has become known variously as the “Gause Hypothesis”, “Gause’s Law”, the “Volterra-Gause Principle”, etc. The verbal statement of this principle has also taken several forms. Crombie (1947) states, “. . . it can be demonstrated by simple argument that species with identical needs and habits cannot survive in the same place if they compete for limited resources - a t least if their needs and habits remain identical.” Hardin (1960) presents the case more simply by saying “complete competitors cannot coexist.” He defines the principle in the following terms: (1) if two non-breeding populations occupy the same niche, and (2) if they are sympatric, and (3) if A multiplies faster than B, then ultimately A will replace B and B will become extinct. Hardin notes that in practice we remove the hypothetical character of (3) because we subscribe to the “axiom of inequality” which states that “no two things or processes, in a real world, are precisely equal.” If, for example, two populations are sufficiently distinct morphologically to be recognized as species, they differ to some degree in their genetics, physiology and ecology as well. There is therefore an a priori assumption that no two species are ecologicallyidentical. This introduces a circularity, which has been discussed by Gilbert et al. ‘ (1952), such that the competitive exclusion principle can neither be proved nor disproved. If one species excludes another we say the principle is “proved”, but if they coexist we conclude that they differ ecologically and therefore occupy different niches. What importance can we assign to this axiom as a conceptual model of competition? Can we justifiably claim that the competitive exclusion principle is “perhaps the most important theoretical development in general ecology”, or that it is “one of the chief foundations of modern ecology”? (Hutchinson and Deevey, 1949). As it is usually stated, it cannot be used to either confirm or deny the existence of competition as a natural process and, as Cole (1960) has noted, it is in danger of becoming dogma. He points out that the doctrine of competitive exclusion contains a device which may be used to avoid Hardin’s (1960) admonition that “every instance of coexistence must be accounted for”, for it is easy to dismiss observations of apparent coexistence by merely saying “they obviously have to occupy different niches or they couldn’t exist.” The laboratory experiments that followed the initial research of Volterra, Lotka and Gause have not been particularly instructive insofar as competition in natural communities is concerned. The tendency

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has been to reconfirm one case of the Volterra-Gause model, namely that competitive exclusion can be demonstrated, and to ignore the more interesting fact that coexistence for many generations has been repeatedly observed in highly simplified laboratory environments. After showing that Drosophilafunebris and D . melanogaster were able to coexist in population cages where the only noticeable variable was a periodic alteration in the freshness of the food medium, Merrell (1951) stated that these results do not contradict the Gause hypothesis, because the two species were shown to have different responses to the character of the medium. Merrell chose to devalue the important result that, in an otherwise constant environment, a minor change in one variable was sufficient to permit coexistence of the two species for almost two years, after which the experiment was terminated. I n their anxiety to “prove” the competitive exclusion principle, ecologists have repeatedly ignored the important fact that many, if not most, laboratory studies of competition have provided better evidence of coexistence than they have of competitive exclusion. While competition between and within species has unquestionably been an important force in the evolutionary history of natural communities and is presumed to be a major factor in the organization of modern ecosystems, there is still no satisfactory explanation for the tremendous diversity of species that is observed in natural systems. When we consider the relatively low ecological efficiencies of animals, and the fact that a classical food chain is limited for this reason to about 4 or 5 direct links, we can understand why there is “room” for a certain variety of forms. It is surprising, nevertheless, that discrete biotopes such as small ponds or grasslands, with relatively uniform structural characteristics, support the number of speciesl they do, especially large numbers of closely related species. During four years of light trap collections at Rothampsted Experimental Station, 154 to 198 species of lepidoptera were recorded each year (Williams, 1964). Kontkanen (1950) collected 4 288 individuals of 56 species of leafhopper in one day at a locality in North Karelia, Finland. I n three summers he never collected fewer than 37 species in any sample during the months of July and August, and the mean per sample was 2 374 individuals representing 48 species. The H.M.S. Challenger expedition collected 4 248 species of benthic animals, representing 1 438 genera, from 70 stations less than 180 metres deep (Williams, 1964). Mitchell (1964) asks, “Why should several species share a common energy source if one of the species could have become adapted to take all of the energy?” Biotic communities are unquestionably the most highly organized of natural systems. There is a high degree of interrelationship among different parts, self-regulation maintains a more or

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less constant ratio of components in a continuous flow of materials, and the system returns to a steady state after a disturbance of stimulus (Bray, 1958). Nevertheless, is the amount of diversity that exists in ecosystems essential to the orderly function of its component parts, and what mechanisms make the diversity possible? It is often observed that older ecosystems such as those in the tropics are richest in structural and species diversity, even though the differences in primary productivity between comparable tropic and temperate systems is not great and may, in fact, be greater in the temperate ecosystem type (Odum, 1959). Bray (1958) advances the hypothesis that re-utilization efficiency may offset the reduced primary productivity that occurs in the succession from simple to more complex communities. Re-utilization efficiency reduces the relative loss that may occur through production of nonavailable energy forms and is a function of the number and kinds of organisms and their ability to create new energy niches and thus increase the number and pathways of energy exchange (Bray, 1958). The diversification of animal food chains is regarded as an example of this function. The most obvious source of species diversity among closely related forms, or within the assemblage of organisms a t one trophic level, is through specialization (Klopfer, 1962). Any natural community contains large numbers of specialists as well as more widely adapted nonspecialists, and it is worth noting that this kind of division seems to be an almost universal phenomenon in every taxonomic group, even within genera. Curiously enough, the more ubiquitous species have asserted themselves to only a limited extent. How then does specialization confer a competitive advantage? Even though we tend to accept the premise that specialization leads to competitive superiority, we lack empirical evidence to show how this occurs. There is no clear reason why the widely adapted wood mouse (Apodemus sylvaticus) has not entirely replaced its cogener, the yellow-necked mouse (Apodemus Jlavicollis), in Britain, or why Peromyscus maniculatus is not the only member of this genus in North America. A. sylvaticus would appear to be able to inhabit every woodland habitat in Great Britain, and there is no evidence to show that A . Jlavicollis is a more efficient or more productive species. I n the absence of competition from its cogeners the least chipmunk (Eutamias minimus) can apparently inhabit any environment in which western chipmunks are found, yet there are 16 species of this genus in North America and this more widely adapted species seems, usually, to be displaced by its cogeners (Sheppard, unpublished). It is obvious that genetic systems allow a rather wide range of adaptation - most taxonomic groups contain a complement of species that are capable of inhabiting a variety of habitats, in addition

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to a closely related group of more specialized forms -yet adaptability does not seem necessarily to be correlated with competitive superiority. MacArthur and MacArthur (1961) examine two ways in which species may share the resources of a community: (1) each species may have strict habitat preferences, feeding throughout its particular habitat on all kinds of food, or (2) all species may share the same habitat, each species feeding on a different food or in a different situation within the habitat. The first alternative violates the “jack of all trades - master of none” principle that natural selection favors the increased efficiency of a certain amount of specialization; in the second alternative specialization has proceeded so far that time and energy are wasted travelling from one point to another, where the particular food item or requirement is located (MacArthur and MacArthur, 1961). These authors note that it is difficult to determine where the balance of these opposing requirements is reached. As long as specialization leads to increased efficiency, it will be favored by natural selection, but only up to the point where time and energy are not wasted. While ecologists subscribe to the general proposition that evolution proceeds as a product of diversity and that diversity is accompanied by homeostatic mechanisms that promote stability, considerable development and modification of conventional competition theory will be required before species interactions can be described in terms that can be incorporated into testable hypotheses, and which will lead to a clear understanding of the exact nature of the mechanisms of competition and species diversity. 11. THE NATUREOF COMPETITION In dictionary usage “competition” is defined simply as “a contest between two rivals for the same object.” This definition is not sufficiently precise for ecological use and various attempts have been made to qualify biological competition with respect to ( 1 ) the nature of the contest, (2) the object of the competition and (3) the characters of the rivals. The inconsistencies in the literature regarding the meaning and significance of competition have been reviewed by Crombie (1947), Solomon (1949), Birch (195T), Milne (1961) and others. I n the discussions that follow I will simply employ a modified version of the definition proposed by Clements and Shelford (1939), namely, that “biological competition is the active demand by two or more individuals of the same species population (intraspecies competition) or members of two or more species a t the same trophic level (interspecies competition) for acommonresourceorrequirement that is actually or potentially limiting.” Questions that arise in any consideration of the nature of competition are: What precisely is the form of the competitive process and what

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are its component elements? What constitutes a common resource or ecological requirement that can legitimately be considered the object of the competitive process? Is competition limited to interactions between individuals and species at the same trophic level, or is any interaction which has a deleterious effect on the existence or increase potential of another individual or species a form of competition? How can the action of competition be detected and evaluated in natural situations, and what constitutes adequate proof of competition? A. THE PROCESS O F COMPETITION Because most of our knowledge of competition has come from laboratory studies designed to test the outcome of a competitive interaction, there has been a tendency to ignore the fact and nature of the process and to view competition almost entirely in terms of its end result of selective elimination. It is perfectly legitimate to design an experiment in which competition is defined as the elimination of one species by another, as in Park’s atudies of competition in Tribolium, but one must also recognize that this design imposes an artificial criterion which is merely a condition of the experiment. Thus, in describing one such series of experiments, Park (1954) writes, “. . . for the purposes of this paper only I shall refer to competition merely as those new events which emerge when two species co-associate and which lead to the persistence of one species and the elimination of the other.” Park cautions, however, that this is not advanced as a general definition of competition, but is merely a sct of ground rules he has selected for a particular purpose. Considerable ambiguity and misunderstanding has resulted from attempts to define the competition process according to its consequences, and through failure to establish a common resource as the object of competition. There may be distinct component elements within the competition process, associated for example with the ecological characteristics of particular taxonomic groups, but these may not be readily discernible in the outcome of the interaction and their considerable theoretical significance may therefore be ignored. For this reason, arbitrary schemes for classifying species interactions in terms of their positive, negative and neutral effects may be quite misleading. According to Burkholder’s (1952) system of classification, predator-prey and parasite-host interactions both have f values and may therefore be classed together. Such a classification ignores their separate ecological characteristics and requires that we view such interactions entirely as abstract energy transformations. There may be valid theoretical reasons for considering the energy flow between all primary and secondary

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consumers as a single set of interactions, but this need not disguise the fact that an array of distinctive phenomena, each with unique ecological and evolutionary properties, has produced the observed results. Birch (1957) has reviewed several cases in which various authors have described interactions such as predation and parasitism as forms of competition (cf. Nicholson, 1933), regardless of the fact that the species interaction did not involve a common resource. Thus, Nicholson (1937) states that “. . . competition for food and space, and the interaction of natural enemies and their hosts, can both be represented by the same fundamental formula and its corresponding exponential curve. . .” so that the criterion of competition is merely that survival decreases as density increases. There is a substantial body of literature and theory pertaining strictly to interactions between members of the same species or between species at the same trophic level, in which the interaction is directed toward a resource which is a common requirement for both members of the interaction. There is no conceptual problem in delineating the phenomenon of competition in these terms, nor is there any obvious theoretical advantage in considering competition to be more than an ecologically qualified “contest between two rivals for a common object.”

B. COMPONENT

ELEMENTS O F COMPETITION

Elton and Miller (1954), Park (1954) and others distinguish between interference and exploitation as component elements of the competition process. While the general consequences of a competitive interaction may be the same in either case (e.g. elimination of one species from a niche), the process leading to this result may involve one or both of these elements. “Interference” refers to any activity which either directly or indirectly limits a competitor’s access to a necessary resource or requirement. It usually operates in a spatial context, as in the case of territoriality, and assures possession of some minimum requirement by one individual or species. It may involve a structural resource such as a nest site or song post, or it may be a space containing a requisite amount of food or nutrients. The term “interference” has been used in somewhat different ways. It is broadly synonymous with the term “contest” as used by Nicholson (19!55), in that a contest in this sense invariably involves interference. Brian (1956) refers to interference and exploitation as “isolated components of the dual competition concept” and concludes that the Lotka-Volterra model involves competition by interference alone while the Windsor (1934) model involves only exploitation. An objection to the Lotka-Volterra model put forth by Andrewartha and

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Birch (1953) also states that it includes no differential exploitation, merely interference between species. I n this connection, they assert that there is no competition unless a common resource is involved and unless one species seeks power over this resource a t the expense of another, and seem therefore to imply that interference is not a sufficient mechanism for this purpose. This objection seems, however, to have no real connection with either the Lotka-Volterra model or the question of interference or exploitation. As long as competition is defined in terms of a limiting resource, which is clearly contained in the term for carrying capacity ( K )in the model, “seeking power” in its broadest sense could be accomplished either by interference or exploitation -in fact interference would appear to be the more effective mechanism for gaining power over a resource at the expense of another species. Some authors have introduced special terms to distinguish between interspecies and intraspecies interference or territoriality (cf. Frank, 1952; Simmons, 1951), but the evidence that is available supports the view that mechanisms such as interspecific territoriality do not differ from those involved in intraspecies relationships (Hinde, 1956) and it is doubtful that such mechanisms will be evolved unless they have first arisen among members of the same species. Indirect interference through chemical repellents may constitute a class of exceptions, although this is by no means certain. Wilson and Bossert (1964) list several examples of territory and home range marking by chemical secretions in different taxonomic groups. They state, “There is no reason to doubt that the essential characteristics of intraspecific communication . . . are also true of interspecific chemical communication.” The evidence they give also suggests that most chemical repellents that act as isolating mechanisms between closely related species may act as interspecies interference mechanisms as well, and have their origins in intraspecific relationships. The spatial organization and requirements of animal populations are usually discussed in relation to territory, but attempts to assign common origins and functions to the territories of different species have led to considerable disagreement and misunderstanding among ecologists (cf. Lack, 1954; Hinde, 1956). Wynne-Edwards (1962) has compiled an impressive number of examples that are presumed to show that animal dispersion is mostly in relation to an optimum food supply and that competition for territory or individual rank and dominance is the proximate agent limiting numbers for this purpose. This is supposed to provide an effective proximate buffer to limit density near the optimum for that species, in relation to the ultimate agent of food. Unfortunately, Wynne-Edwards attempts to categorize all species in the same way, limited proximately by territory and ultimately by food,

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and this weakens his argument. He does not define “optimum” and it is therefore impossible to test this critical hypothesis, but a more serious objection is the lack of evidence for food as an ultimate limiting factor in many populations (Andrewartha and Birch, 1954). While we must accept the fact that territories are rendered incompressibleat some point by psychological factors (Klopfer, 1962) and that competition for space is a form of limiting convention, it cannot be assumed that all species require space for the same reasons or that they are ultimately limited by the same factor. There are numerous examples among birds to show that territory is related to factors other than food (cf. Hinde, 1956). The principal area of defense among hole-nesting birds is usually the immediate vicinity of the nest hole, and the density of breeding pairs can be increased in most natural habitats by providing artificial nest boxes (Von Haartman, 1956). Intraspecific and interspecific territorialism exists among closely related species of plovers, but these birds, as do many others, feed outside the limits of their territories. Simmons (1956) suggests that the most important function of territory in these species is the spacing of nests and eggs, as Tinbergen (1956) has shown for other ground-nesting birds. Hartley (1949) found that the only common requirement among the territories of mourning chats (Oemnathe lugens) in their wintering quarters in the African deserts was a measure of shade. This could be provided by broken ground or some artificial counterpart such as a scar in a hill or hutments of a camp. A structural feature which is required for breeding or shelter may be more limiting than food in the habitats of some species, and it is frequently observed that the limits of population in territorial species are well below the ultimate limit of food supply, even in years of food scarcity. However, if we define “territory” simply as any “defended area or space”, regardless of its origin or function, it is evident that territorialism exists both within and between some species, and leads to competitive exclusion from particular habitats and niches. This concept can be accommodated within the broader term “interference”, which may be direct, as in the case of territoriality or overt aggression, or indirect chemical communication. I n each case the effect of interference is to ensure possession of a particular array of resources at the possible expense of other individuals or species. There is an apparent evolutionary tendency toward more formalized mechanisms of territorial behavior, with greater emphasis on display and correspondingly less on physical contact. Wynne-Edwards (1962) uses the term “epideictic display” to denote conventions that have evolved away from the direct, primitive contest and have come to assume a symbolic quality, not even directly implying threat in some cases, but which nevertheless serve to interfere with intrusion into a

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territory or defended space. A question pertinent to this discussion is the extent to which such behavior is effective between species, as well as within species, and how interspecific dominance is established and maintained. Direct, physical contests require no special methods of species recognition in order to be effective. The barnacle Balanus balanoides merely overruns its competitor Chthmalus stellatus, crushing or grinding its way into the niche space it seeks to occupy (Connell, 1961). Taxonomic aEnity in such cases functions mainly to bring two species into competition, in that closely related species are more liable to have similar niche requirements. When more elaborate behavioral mechanisms are present, however, taxonomic affinity assumes greater importance. The meadowlarks Sturnella magna and S. neglecta tolerate intrusion into their territories by species outside this genus, but defense and display between these two competing species are as frequent and intense as within species, resulting in complete segregation of their territories (Lanyon, 1956). Where the plovers Charadrius dubius, C. hiaticula and Leucopolius alexandrinus occur together they defend and maintain distinct territories, spaced in such a way that they occupy three contiguous areas (Sluiters, 1954; Simmons, 1956). Territory is advertised by the patrolling behavior of the male as he curves in a “butterfly” display flight, slowly backwards and forwards, singing all the while. These display flights obviously require that visual and song signals be recognized in order to be effective interference mechanisms, and it is evident that relatively elaborate behavior elements that are found in one species are present in, and recognized by, closely related competitors. Moore (1964) also notes that interspecific encounters are more frequent and are more effective between dragonflies that resemble each other, e.g. he found that Anax irnperator invariably drove Aeshnu juncea from small ponds but the presence of other, less similar species did not provoke aggressive attacks. Interestingly enough the motivation for interspecific encounters among dragonflies might be aggressive or sexual, e.g. an attacking male might assume a copulatory position on contact with another male, but the result is the same in that interference is successful and only one male remains within the territory. In each of these and other examples, interference between species almost invariably involves a behavioral element that is present and effective within the species. Thus, if intraspecific mechanisms are lacking, it is unlikely that competitive exclusion will operate through interference between species. Closely related species are not only more likely to have similar ecological requirements and, hence, overlapping or included niches, but are also more able to evolverecognizable, formalized mechanisms of interspecific interference with less dependence on harmful physical contests.

12

RICHARD 9. MILLER

“Exploitation” is the utilization of a resource once access to it has been achieved. Two individuals or species with unlimited access to a common source of food or nutrients will frequently have different abilities to exploit the available supply. This form of competition is referred to by Nicholson (1955) as a “scramble”, in that the most efficient competitor is the one that can obtain and utilize the greatest amount. Elements of both interference and exploitation are undoubtedly present in almost any competitive interaction, but we may inquire whether their relative values in any particular interaction are such that there are distinct theoretical consequences. Interference seems, for example, to be especially well developed among certain of the higher vertebrates, especially birds, and is often so effective that direct exploitation is a relatively unimportant element of competition. Conversely, exploitation seems to be characteristic of simple metazoans in which the populations are more directly controlled by factors in the physical environment apd social interactions are simple. I n other words, exploitation seems to be the dominant form of competition whenever interference mechanisms are poorly developed. If this is indeed the case, it implies that competition by direct exploitation is a primitive and unstable form of interaction, and that interference mechanisms such as territoriality represent evolutionary advances toward more effectivebiotic control of population interactions and numerical stability, as partly suggested by Wynne-Edwards (1962). Wynne-Edwards (1962) states “The substitution of a parcel of ground as the object of competition in place of the actual food it contains . . . is the simplest and most direct kind of convention it is possible to have.” Such an arrangement implies interference with access to a resource, which Wynne-Edwards assumes is a property of all species; buti for many species such conventions have not evolved and direct exploitation of food resources is a characteristic form of competition. Examples of competition through exploitation are found in laboratory studies of insects which spend all or part of their life cycle within their food medium, and there is evidence that similar interactions occur under certain circumstances in natural environments. Such species seem, generally, to be limited by absolute amounts of food or nutrients and there is little evidence of spatial organization in their populations. As the level of population increases relative to the volume of food and space available, there tends to be a non-linear increase in mortality which may ultimately result in the complete extinction of all members of a population. During artificially induced crowding in larval populations of Drosophila (Sokoloff, 1955; Robertson, 1960; Mishima, 1964; Miller, 1964b), moderate increases in density relative to available food and space cause

PATTERN AND PSOUESS IN COMPETITION

13

an increase in the length of the larval period and a corresponding decrease in final body size. Because of the correlation that exists between adult body size and fecundity (Chiang and Hodson, 1950),these physiological adjustments produce a somewhat lower potential rate of increase for the populations, but they also allow the larvae to compensate for the effects of moderate crowding without a significant increase in mortality (Miller, 1964b). Figure 1 shows the changes in larval period +0.3 ,

BODY S I Z E -05

10

I

I

I

I

20

4G

60

80

INITIAL LARVAL DENSITY

FIG.1. Deviation in larval period and adult body size, with larval crowding in Drosophiln 1964b).

melanogaster (After Miller,

and adult body size that occurred in populations of Drosophila melanogaster when the larval density was increased from 10 to 80 per 5 cc of medium (Miller, 1964b). Over this range of density the larval viability remained the same and there was only a slight increase in pupal mortality. With further increases in larval density these compensatory mechanisms lose their effectiveness and the flies reach what Sang (1949) refers to as “a minimum survival size”, after which further crowding is reflected in greater larval and pupal mortality (Fig. 5). In spite of the extremely high densities that were reached in these experiments, it can be shown that the limits on survival were due primarily t o food quality rather than food volume or space. The larvae were cultured in 8-dram vials containing 5 cc of a synthetic medium which acted as a substrate for a live yeast population. I n later studies it was found that a banana-agar medium enriched with dead yeast allowed much greater survival. The numbers of adults of D. melanogaster

RICHARD S. MILLER

14

and D. simulans produced from initial larval densities of 20, 40, 130, 120 and 160 per 5 cc of each medium are compared in Table I. Survival was nearly equal at densities of 20 and 40. At a density of 160 larvae per vial survival of D. melanogaster was reduced to 39.2% in Kalmus medium as compared with 72.1% in the banana-agar medium. Likewise, survival of D. simulans was only 18.1% at this density in the Kalmus medium compared with 70.6% in the banana-agar. Bakker (1961) has shown that competitive exploitation of food in D. melanogaster is controlled by subtle differences in (1) rate of feeding, (2) duration of the molting periods, (3) food requirements, (4)initial larval weight and (5) resistance to disoperative effects of crowding. There .is no evidence in these or other studies of larval competition in Drosophila of an allocation of space such that a relatively fixed number of larvae survive to pupate and produce adults. Given the constant physical environment of these experiments and the apparent absence of spaceregulating mechanisms, competition seems instead to be a process of selective elimination through direct exploitation of food resources. TABLEI Production of Adult Drosophila melanogaster and D. simulans in Different Food Media (Kalmus and Banana-agar) Adults Produced

D.sirnulam

D.n i e l a i t o p q t e r Kalmii 8

Initial Larval Density

(Mean

20 40 80 120 160

17.0 33.6 58.8 74.6 62-7

Banana-agar

* S.E.) (Mean i. 0.29 f 0.58 f 2.28 f 6.46 f 6.68

& S.E.)

16.2 Jr 0.34 32.2 f 0.54 66.0 f 0.69 95.9 + 1.14 115.4 3.74

*

Kalmus

Banana-agar

(Mean f S.E.) (Mean & S.E.) 15.9 33.6 54.4 69.0 29.0

& 0.47 f 0.79 2.16 f 3-89 f 2.52

16.5 f 0.32 32.3 f 0.42 70.6 0.62 89.2 j= 1-56 112.0 f 2.37

+

Studies of competition in daphnids also show competition through a process of selective elimination based on differential rates of exploitation among different species or age classes within the populations. Slobodkin (1954) has shown that growth, reproduction and the size of Daphnia obtusa populations is linearly dependent on food supply, and suggested that the same was true in Pratt’s (1944) studies of Daphnia obtusa. Frank ( 1952) concluded from his experiments with competition in Daphnia pulicaria and Simocephalus vetulus that absolute food shortage

PATTERN AND PROCESS IN COMPETITION

15

and chemical conditioning by nonvolatile substances were not limiting factors in these populations, and suggested that lack of oxygen or repeated physical contact might depress the feeding rate, or that food quality might be a limiting factor (P. W. Frank, personal communication), but there was no evidence of interference with access to a resource. Ullyett (1950) found no evidence of aggressive activity in competition among larvae of the sheep blowflies Lucilia sericata and Chrysomyia chlorophyga. They feed on the same food and compete only through exploitation of the same resource. Ullyett regards competition in these species in terms of “the provisions of nature rather than in the light of a specific ‘struggle’. The phenomenon which really acts as the controlling agent is basically sheer starvation.” It is in this sense that Nicholson used the term “scramble” to distinguish between this and a form of competition in which “each successful individual lays claim to a supply of requisites sufficient to maintain it and to enable it to produce offspring. The unsuccessful individuals are denied access to the critical requisites by their successful competitors” (Nicholson, 1955). In each of these examples the populations were directly limited by absolute amounts of food, food quality, or by a factor which affected their abilities to exploit their food resources. There is the suggestion, in other words, that food becomes limiting unless (1) some form of interference acts as a regulating mechanism relative to the space that contains a supply of resources, or (2) extrinsic factors such as climate prevent the level of population from reaching a critical value. The crowded populations and variations in body size that are commonly observed in natural populations of some dung, carrion and log-dwelling insects may reflect events similar to those observed in laboratory studies, in which exploitation is the principal form of competition. But there remains the question of how often natural populations are in fact directly limited by a resource such as food, or how frequently they are forced into a competitive interaction dominated by exploitation.

111. THEECOLOGICAL NICHE A. HISTORICAL DEVELOPMENT O F THE NICHE CONCEPT Elton and Miller (1954) have noted that the “ecological niche” is a far more elusive concept than was supposed by either Elton or Grinnell when they introduced the term into the literature. Elton (1927) observed that although there may be a difference in species composition between one community and another, there is usually an obvious similarity in their “ground plans”. We can expect to find groups of herbivores, predators, parasites and scavengers in every animal community, even though these roles may be filled by different species.

16

RICHARD S. MILLER

Elton proposed the term “niche” to describe this status of an animal in its community and spoke of the niche in the sense of an animal’s “profession” rather than its “address”. A reconnaissance of woodland bird communities in England and Wales (Elton, 1935) showed, for example, that “woodland birds in Britain form a clear-cut and ancient community that is much the same in different woodland types. . . It forms part of a life-zone widely spread over Europe.” Also, in a table of comparisons between comparable plant communities in California, Finland and Britain, Elton (1935)observed that “there is a high degree of resemblance in the structure of such bird communities right around the world.” Elton’s use of the niche concept was therefore primarily one of function, emphasizing that the same niches exist in each community, regardless of what species fill these roles. Udvardy (1859) attempts to establish that Elton and Grinnell used the term “niche” in the same way and that their concepts are therefore compatible, but it is obvious that Grinnell’s emphasis was on the “address” of a species, rather than its functional role. Grinnell (1917a) listed three facts of distribution: (1)that each animal has a habitat or range which is distinctive enough to be included among the characters used to describe a species, ( 2 )that some species range widely and others are restricted, and (3) that groups of species nearly or entirely coincide in range so that realms, zones, faunas, and other units can be easily recognized. These and similar observations laid the basis for his later development of the niche as “the ultimate distributional unit” (Grinnell, 1924, 1928).He also stated that it is axiomatic that no two species in a single fauna can occupy precisely the same niche (Grinnell, 1917b, 1924). Dice (1952) follows Grinnell’s usage to define the niche as all of the features of the ecosystem that a species utilizes and states that “The term does not include, except indirectly, any consideration of the functions that a species serves in the community.” He also emphasizes the distinctness of the niche of each species. It is in this and Gause’s sense that Hutchinson (1944) described the ecological niche as “the sum of all the environmental factors acting on an organism; the niche thus defined is a region of n-dimensional hyper-space, comparable to the phase-space of statistical mechanics.” A difficulty with the Grinnellian concept is that it cannot be used to define the conditions of competition without considerable modification. The broader concept, in which the niche is the functional status of an animal in the trophic system, clearly implies that this function may be filled by any of several species and that competition is not only possible within this context, but is also highly probable. This concept also provides for the possibility of “vacant niches”, in that a functional role

PATTERN AND PROCESS IN COMPETITION

17

may exist to be occupied by subsequently invading species (cf. Darwin, 1859; Elton, 1958). It is in this connection that Weatherly (1963) defines a niche as the nutritional role of an animal, existing to be occupied in widely separated ecosystems. However, while the broad functional concept of the niche allows us to describe the composition of a community in such a way that particular roles can be occupied by different species, it does not at the same time allow us to define degrees of overlap in the ecological requirements of species competing at the same trophic level. Obviously the value of the niche concept as a theoretical tool is as a means of describing environmental relationships in such a way that the conditions of competition or coexistence can be defined and evaluated. As Crombie (l947), Hutchinson (1957) and others have pointed out, the degree of similarity that leads to competition or, conversely, the ecological differentiation that is necessary for coexistence, can only be defined empirically. Thus we require a conceptual model for this purpose which will accommodate both the functional and distributional concepts of the niche (cf. Lack, 1944). B.

NICHE RELATIONSHIPS

Elton and Miller (1954) recognized certain of the difficulties inherent in using the niche concept to define competitive interactions when they pointed out, “There is no difficulty in seeing the reality of a very broad distinction of ecological function, such as between herbivore and carnivore. The distinctions get a bit blurred if we divide up carnivores into separate niches, since a carnivore may in fact ‘belong’ to more than one consumer layer. At the other end of the scale, each species has a unique ecological niche in the sense that its particular mosaic of abilities and habits is unique. I n between the broad consumer type and the species,. one may create any number of ‘niches’, by choosing some well-marked type of habit: ‘mouse-eater’, ‘conifer-needle feeder’, ‘bark.-beetle’ and so on. What ecologists usually imply by such groupings is that within them interspecific competition occurs or may occur. But when one considers an actual example like the grain-beetle Rhizoperth dominica competing with the grain-moth Sitotroga cerealella (in laboratory culture), it is seen that the similarities of habit (larvae feeding inside wheat grains for example) that bring about competition can be matched by other differences in properties of the species (they will have different parasites; they have different life spans; they presumably have Werent tolerance. . .) We think, therefore, that analysis of communities should pay attention more to tracing the consequences af one species in a key position being replaced by another, rather than trying to classify all the functions of species into a few niches.”

18

RICHARD S. MILLER

As long as the phenomenon of competition is described only by its outcome and in the abstract language of the Lotka-Volterra equations, we are liable to overlook the important fact that any interaction between two individuals or populations is an event which has dimensions of both space and time. Neither the broad, functional classification nor the total ecological characterization into mutually exclusive niches is capable, without modification, of expressing these properties of competition. A partial solution was offered by Elton and Miller (1954)when they proposed the term “arena” to describe a locus “within which some temporary relation between the species of animals is arrived at, by a combination of mutual opposition and various degrees of symbiosis”. This was an attempt to define species interactions in such a way that the total ecological characterizations of species express potentials which may overlap in time and space, leading under appropriate conditions to interspecies competition. A more satisfactory, formal description of the relationships between the ecological niches of potential competitors has been developed by Hutchinson (1957)using conventional notations of set theory. This approach allows us to define a niche in terms of all variables relative to the species, regardless of their exact nature or quality, and we may at the same time follow the usual set-theoretic practice of representing an infinite number of variables in a restricted number of dimensions. Hutchinson’s formalization also includes both the fundamental niche that might be expressed in the absence of competitive interactions and the realized niche that is occupied when competition restricts the expression of the total species potential. If we consider the total array of variables which limit the survival of a species S,, we may define an n-dimensional hypervolume N, which is the fundamental niche of that species. The fundamental niche, as so defined, may be regarded as a set of points in an abstract N space which will completely define the ecological properties of S,. Secondly, if B is a limited volume of physical space comprising the biotope of a collection of species S,, S,, . . . S,, the biotope is complete relative to S, if all the points in N, are represented in B. If N, and N, are two fundamental niches they may have no points in common and are therefore separate, or they may have points in common and are said to intersect. N,.N, is the subset of points common to N, and N, and is their intersection subset. The following restrictions apply to this mode of expression: (1) It is assumed that all points in each funda.menta1 niche imply equal probability of survival, and all points outside the niche imply zero survival of the relevant species. (2) It is also assumed that all environmental variables can be linearly

PATTERN AND PROCESS IN COMPETITION

19

ordered, even though this is obviously not possible with our present state of knowledge. (3) The model refers to a single instant in time. (4) Only a few species can be considered at once, even though all other species in the community are regarded as part of the coordinate system. As Hutchinson (1957) points out and earlier discussions have also shown, some of the confusion surrounding the “Volterra-Gause Principle” has arisen from the concept of two species not being able to co-occur when they occupy identical niches. This problem was dealt with in detail by Gilbert et al. (1952). According to the set-theoretic formulation of niches, identity of fundamental niche would imply N, = N,, that is every point of N, is a member of N, and vice versa. It is axiomatic that this is impossible (Hardin, 1960; Cole, 1960). Omitting this quasi-tautological case, Hutchinson ( 1957) distinguished two cases of intersection between fundamental niches: (1) N, is a proper subset of N, (N, is “inside” N, and is therefore a smaller niche) and (2) N,-N, is a proper subset of both N, and N,. These relationships are illustrated by Euler diagrams in Fig. 2 for two independent variables

CASE 1

CASE 2

FIQ.2. Relationships between fundamental niohes (N, and N,) defined by two variables (z and y) in a biotope ( B ) .

x and y which can be measured along ordinary rectangular coordinates. In the first case N, coincides with the intersection subset N,.N, and is included within N,, while in the second case the intersection subset N,.N, is formed by the “overlap”. between the two niches.

20

RICHARD S. MILLER

The case of an “included niche” is particularly interesting, as it imposes strict conditions for the outcome of competition and, especially, for the survival of S,. I n the simplified, two-dimensional relationship shown in Fig. 2 (Case l), the niche N, is described by the coordinates x, - x3 and y, - y3 and is included within the total niche N,, which is in turn described by the coordinates x, - xpand y, - ya. The following outcomes of competition are possible under the conditions of Case 1: ( a ) competition proceeds in favor of S , in all the elements of B corresponding to N,.N, and, given adequate time, only S , survives; or ( b ) S , survives in all elements of B corresponding to some part of the intersection subset and both species survive. The first alternative (a) implies that S , is the superior competitor and, with its greater ecological amplitude, will eliminate S , from all parts of the fundamental niche N,. Coexistence of S, and S, is impossible under the conditions of an included niche when S , is the superior competitor. The second alternative ( b ) requires that S , be the superior competitor, in spite of its narrower ecological tolerance. Under these conditions, S, will be excluded from N, but will survive in the parts of N, that lie outside the intersection subset. The realized niche of S, will therefore be the difference subset N, - N, (N, - N, N,). As long as the niche space N, - N, is sufficient to allow the survival of S, there will be coexistence of both species within the total biotope B . The conditions described by alternative ( b ) of an included niche would seem, at first glance, to contradict conventional theories of competition. We do not ordinarily expect a species with a relatively narrow range of tolerance to be superior in competition with a closely related species with greater ecological amplitude, yet later examples will show that the approximate conditions of an included niche are relatively common in species relationships, and that Case l ( b ) may in fact explain some of the species diversity that exists in natural communities.

-

IV. COMPETITION IN NATURE It is difficult to identify the actual process of competition in nature, either as an active or historical factor, although certain patterns of geographical or habitat distribution and niche relationships between species are often thought to reflect competitive exclusion. When a species occupies a broader niche in the absence of a closely rela.ted species than it does when the two species are sympatric, competitive exclusion is often inferred (Lack, 1944); contiguous allopatry can only be explained by a consistent environmental discontinuity or by a competitive interaction which maintains the pattern along a line of contact (Miller, 1964a); character displacement is usually explained as a product

PATTERN AND PROCESS IN COMPETITION

21

of competition (Brown and Wilson, 1956; Hutchinson, 1959;Mayr, 1963); the species composition of natural communities may reveal fewer repre sentatives of a genus than would otherwise be expected in the absence of competition (Elton, 1946); and MacArthur’s (1957) model of nonoverlapping niches has been advanced as a test for competitive exclusion (Hutchinson, 1957; Slobodkin, 1961). I n each case we are left, however, with the question of whether the observed phenomena are in fact due to competitive exclusion, or whether they cannot be explained instead by ecological differences which have arisen through some other agent of natural selection (Elton and Miller, 1954).

A. DISTRIBUTION PATTERNS Figure 3 shows the relationships that may exist in the spatial distributions and fundamental niches of two populations. For simplicity SPATIAL DISTRIBUTION

FUNDAMENTAL NICHE

1 A llopat ry

B N1

Syrnpatry

C N1

Contiguous Allopatry

FIU.3. Distribution patterns of two species (S, and S,) and their possible niche relationships (N, and N2).

the niches are represented by single variables. They illustrate (A) non-intersection; (B) intersection corresponding t o Case 2, Fig. 2; (C) intersection corresponding to Case 1, Fig. 2; and (D) contiguous nonintersection. Even though it is unlikely that the critical variables in B

22

RICHARD 5. MILLER

two niches would be precisely contiguous and non-intersecting (D), this is a theoretical possibility which must at least be considered as a possible cause of observed cases of contiguous allopatry in spatial distributions. The terms allopatry, sympatry and contiguous allopatry are conventionally used to describe geographic distributions, but analogous patterns occur at all levels of distribution and it is not always possible to distinguish between ecological events which affect geographic, habitat or microhabitat distributions (Miller, 1964a). The related questions of spatial distribution and coexistence are relative terms, depending on the level of spatial distribution chosen as a criterion and the sensitivity of sampling procedures in relation to this criterion. For this reason, it seems advisable to consider the general phenomenon of spatial distribution as a single event which can be qualified according to specific circumstances. When it is stated, according to the Gause axiom, that no two species can coexist indefinitely in the same locality, we beg the question of what is meant by “locality”. Populations which appear to be sympatric in their geographic distributions may diverge ecologically so that they are effectively allopatric in their local distributions, even in the absence of a competitive interaction. We know that closely related species frequently coexist in the same habitats, but there is usually some level of spatial distribution at which they are separate. What is required is a critical comparison between the spatial distributions of two supposed competitors and the amount of intersection in their fundamental niches. Unless it can be shown that their spatial distributions, at any level, reflect realized niches which are less than what would be expected from an unrestricted intersection of their fundamental niches, there is no reason to infer that competition is a contributing factor. Although there is no opportunity for competition to occur between allopatric populations, this situation illustrates the difficulty of drawing conclusions about niche relationships from observed distribution patterns. Allopatry may be due to an intervening barrier to dispersal or habitat occupation, in spite of intersection between two fundamental niches (Fig. 3 B); or the allopatric distribution may reflect a difference in fundamental niches (Fig. 3 A) such that N, and N, are separate sets, or at least do not intersect in the niche elements that affect spatial distribution. The Grst of these relationships is shown in the distribution of two races of song sparrow (Passerella melalia) in the San Francisco Bay area. One race occupies tidal marshes and the other is confined to nearby fresh-water habitats (Marshall, 1948). The intervention of unsuitable environments forces them to behave like allopatric species, but there is hybridization between them wherever there is contact between

PATTEI~NA N D PR(W;SS I N

coairim~~w~

6)

Y

3

the two habitats. The fundamental niches of the two populations intersect but their realized niches are expressed in allopatric distributions because of ecological barriers. In the absence of barriers to dispersal and habitat occupancy, intersection in the spatial elements of two fundamental niches will be expressed in various dimensions of sympatry, depending on the nature of the competitive interaction that results from intersection and the spatial requirements of the species concerned. There is considerable evidence showing that competitive exclusion at the level of broad habitat or geographic distributions is invariably accompanied by competitive interference. Species which compete primarily through exploitation are more often controlled by physical factlors which affect their distribution and abundance and are less likely to be spatially exclusive, except at the level of mxrohabitat distribution. They are also more likely to show complete differentiation in some critical element of their fundamental niches. Townes and Townes (1960) remarked on the apparent coexistence of three species of ichneumon wasp (Negarhyssa atrata, M . macrurus and M . greenei), all of which parasitize the same host, the wood-boring larva of the pigeon tremex (Tremex columba). A female Megarhyssa detects a host larva or pupa in a dead log or stump and inserts her ovipositor full length into the wood to deposit an egg on the host. The ovipositor is directed a t a right angle to the surface of the wood and all ovipositions require the complete insertion of the ovipositor (Heatwole and Davis, 1965). Tremex larvae occur a t various depths in the wood, but once established an individual larva tends to remain a t a constant depth. Thus the larva to be parasitized must be at a specified depth corresponding to the length of the extended ovipositor of the female wasp. Figure 4 shows a comparison of the ovipositor lengths of these three species of Megarhyssa. There is no overlap in the range of ovipositor lengths for M . atruta and M . macrurus and only a slight overlap between M . macrurus and M . greenei. There is a significant statistical difference in their means and standard deviations (Heatwole and Davis, 1965) with respect to this structural feature, and it is evident that they do not compete for the same larvae but parasitize different segments of the total host population. I n spite of their apparent sympatry, even to the extent of the adults using the same foods, resting places and oviposition sites and the larvae using the same resource in the same habitat, there is no intersection with respect to the critical factor of ovipositor length. The relationship between the fundamental niches of pairs of these three species is described by Fig. 3 A or D. It is possible that competition w-as a historical factor in the ecological differentiation that now exists anioiig these three species, but its action

RICHARD S. MILLER

24

is now negligible if it occurs at all. If the tremex larvae are uniformly or randomly distributed at different depths in the logs and do not alter their distributions as a result of the relative effects of the three species of parasite upon their numbers, each species of Megurhyssa will continue to utilize a separate portion of the total resource regardless of the activities or effects of the other two species, and changes in the abundance of tremex larvae at different depths will not lead to inter-specific interactions between the wasps. Thus, three apparently sympatric species which use the same habitat in the same ways are in fact allopatric at the level of their larval distributions and therefore do not compete.

+ t 0

u:13

N-SO

N:18

atrata

macrurus

greenei

FIG.4. Ovipositor lengths of Megarhyssa atrata, M . macrurus and M . greenei. Horizontal line, mean length; vertical line, range; rectangle, fS.D. (After Heat,wole and Davis, 19661.

Contiguous allopatry is a particularly interesting phenomenon which has received very little attention from ecologists, in spite of the fact that it seems by its nature to indicate a strong element of competition. It is unlikely that the fundamental niches of two species would be entirely separate but contiguous (Fig. 3 D) over any appreciable area. Nevertheless, such a'distribution pattern could be produced by a sharp environmental discontinuity, and there is nothing in the pattern itself which immediately reveals whether it is controlled by environmental factors or competitive exclusion. The geographic and habitat distributions of the four species of pocket gopher (Beomyidae)that occur in Colorado show a pattern of contiguous

PATTERN A N D PROCESS IN COMPETITION

25

allopatry between the ranges of adjacent species (Miller, 1964a). There are a t least three possible explanations for this rather striking distribution pattern. Each species could be so highly adapted t o some critical factor such as soil type that the relationship between their fundamental niches is that shown in Fig. 3 D; their fundamental niches may intersect but some intervening barrier, such as a discontinuity between soil types or a physical barrier such as a river, might prevent the intersection from being expressed in their realized niches; or, in the absence of effective geographical or habitat barriers, the intersection in their fundamental niches might be controlled by competition so that only one of any species pair can occupy the niche space corresponding to the intersection subset. This example will be discussed in R later section when the evidence for competition will be examined in more detail, but suffice to say it can be shown that there is intersection in the fundamental niches of all four species. I n fact, the relationship between their fundamental niches is essentially a system of included niches as illustrated in Fig. 3 C , and competitive exclusion is the most reasonable explanation of the distribution patterns shown by these species. A similar relationship is illustrated in Fig. 5, which shows the spatial distributions of two species of triclnd when they occur separately and together in highland brooks and streams (Beauchamp and UllyBtt, 1932). The distributions of fresh-water triclads are governed primarily by the temperature and rate of flow of springs and streams. Both of these species were found to exist alone in several springs where the water temperature was 6.5 to 8.5"C, but Planaria montenegrina can only tolerate temperatures up t o 16 or 17°C while P. gonocephala inhabits waters as warm as 23°C. Their fundamental niches therefore intersect (Fig. 3 C) in the range ofnpproximately 6.5 t o 1 G or 17°C with respect to this critical factor. \4heu the two species are sympatric in the sense that they both occur in the same stream, P. gonocephala is excluded from the spring head t o a point where the temperature reaches 13 to 14"C, below which P. nronteticgrina is absent and P . gonocephala is the only species present. It is interesting to note that competitive exclusion does not occur a t the extreme of the fundamental niche of P . montenegrina, but that there is a shift of 3 or 4 degrees to the exclusion point of 13 to 14°C. Andrewartha and Birch (1954) contend that this is not necessarily an example of Competitive exclusion, and that other selection processes could have produced the same result. They offer no alternative t o what seems a clear case of exclusive realized niches between two species whose fundamental niches intersect; the most reasonable explanation of this phenomenon is that competitive exclusion operates predominaiitly in favor of 1'. rnontenegrina, the more specialized species.

26

RICHARD S. MILLER

B. C O M M U N I T Y C O M P O S I T I O N Elton (1946) analysed published ecological surveys of 55 animal communities and 27 plant communities and concluded that the number of species present in any given community is less than would be expected from chance. He found a constantly high percentage of genera represented by only one species (86% for animal and 84% for plant communities) and average numbers of species per genus of 1.38 in STREAM FLOW

MONT€N€GRINA

4

I

GONOCEPRALA

I 6.5-8.5

D! c

-I 23’

16-17’

MONTENEGIINA

u_

t

t

4

z

5

GONOCEWALA

I-

w

-I

11 14”

I

I

I

FIQ. 5. Distributions of Planaria montenegrina and P . gonocepknla when they occur separately (allopatric) and together (sympatrir) in streams (Data froin Beauchamp and Ullyett. 1932).

animal communities and 1.22 in plant communities. These figures were found to differ considerably from those of faunal lists for large regions. For example, only 50% of the genera in 11 large groups of British insects contain one species and the average number of species per genus for all British insects is 4.23. Elton (1946) attributed the difference in species/genus frequencies between ecological surveys of relatively small habitats and those from faunal lists for large regions to “existing or historical effects of competition between species of the same genus,

PATTKRN A N 0 I’KOCESY 1N COI\1PETITLON

27

resulting in a strong tendency for the species of any genus to be distributed as ecckypes in different habitats, or if not, t o be unable to coexist permanently on the same area of the same habitat.” Williams (1947) argues that it is insufficient to show that the species per genus is smaller in smaller communities than in larger, as this is a mathematical result of taking a smaller sample from a larger group. It is necessary to show that the species/genus frequency in the smaller communities is different from expectation in a randomized sample of the same number of species, selected without reference to generic relationships from the smaller or larger fauna. Using an index of diversity Williams (1947) conc~ludcdthat Hlton’s data could have been obtained from a random sample and that the cvidcnce in fact indicates natural selection in favor of more rather than fewer species in the same genus in small communities. Williams ( 1951) reiterated his earlier conclusions after analysing Moreau’s (1948) records of East African bird communities. He showed an excess of‘congeneric groups with two or more species above what would be expected by selection without reference t o generic relationships, and further that the excess seems to increase as the number of congeneric species increases. Williams ( 1951) concluded from this analysis that (1) competition between closely related species is probably on the average greater than between less closely related species, and (2) that closely related species are probably more suited t o similar physical environments and, therefore, similar extra-generic competition. Bagenal (1951) examined the evidence presented by Elton and Williams and concluded that many of the communities analysed by Elton (1946) were unsuitable Serause they were often very heterogeneous, were sampled by a variety of methods and the community was often sampled over a long period of time. Hutchinson’s (1957) distinction between homogeneously dicerse and heterogeneously diverse environments implies that we cannot expect species-abundance distributions to behave in the same way under both conditions, a fact which is relevant t o community surveys. As this classification is related to the free paths of animals in relation to the mosaic of structural and microenvironmental features of a habitat, it follows that comparisons between species with different powers of dispersal and daily activity will also be suspect. Elton and Williams gave different meanings to “habitat” and the term is used especially broadly by Williams. Bageiial (1951) states “From this standpoint &Iton’s conclusions appear t o be correct, though based on unsuitable data, and Williams, far from contradicting Gause and Elton, has provided the corollary that related species are more likely t o occur in similar, though not identical, habitats than are unrelated ones.”

28

RICHARD S. MILLER

What these analyses do not, and cannot, show is any actual relationship between fundamental and realized niches, and therefore empirical evidence of either competitive exclusion or coexistence at the level of species interactions. I n order to verify or deny the possibility that competition affects community composition, we must first know how many species are geographically and ecologically available to the community and whether there is intersection in their fundamental niches. As Elton and Miller (1954) have noted, there is very little empirical evidence that gives satisfactory proof of interspecific competition in natural communities, “most of that adduced being equally explicable by selective processes acting through other density-dependent population pressures.” This distinction was not clearly realized by Elton (1946) in his analysis. We have not, therefore, answered the question of whether competition is a daily occurrence in the lives of many animals, or whether it has occurred in their evolutionary histories, even though laboratory evidence and some competition theory “is so strong and persuasive that it must be taken into account in theories about community ecology” (Elton and Miller, 1954).

c. SPECIES-ABUNDANCE When the MacArthur (1957) model of species-abundance is used to demonstrate competitive exclusion, it suffers from the same inadequacies as other inferences predicated on the a priori assumption that mutually exclusive distributions are invariably the product of competition. Of the three alternative situations considered in this model, the one based on non-overlapping niches most nearly fits the conditions of competitive exclusion. This case assumes that the Gause hypothesis is universally valid and that all species in the community are mutually exclusive, i.e. that each species in the community “utilizes the environment in some way so as to make it completely unavailable to the other species in the community” (Slobodkin, 1961). If we consider the total community environment to be a line of finite length, we may divide it into n random parts by throwing (n - 1) random points onto the line. The abundance of each species in the community will have the same distribution as the length of parts of the line. Under these conditions the expected distribution of the rth rarest species is given by:

in which there are S species and N individuals. There is a limitation on this theory such that the ratio of total numbers of individuals to

PATTERN AND PROCESS IN CORIPETITION

29

total number of species must remain constant. Hutchinson (1957) notes that this is likely in a homogeneously diverse environment, in which the mosaic of structural features (e.g. logs, stones, bushes, etc.) is small compared with the free paths of the organisms concerned, but is less likely in a heterogeneously diverse environment where, for instance, stands of woodland may be separated by areas of grassland. Two examples of a correspondence between observed species-abundance distributions and the predictions of this case of the model have been cited as evidence of competitive exclusion. MacArthur (1957,1958) obtained a reasonable fit t o the model when he plotted data for birds in the Quaker Run Valley of New York from component habitats (pasture, orchards, mature oak-hickory forest) which were homogeneously diverse; and Kohn (1959) found a remarkably good correspondence for some of his samples of snails (Conus)in Hawaii. However, these studies would appear to involve two quite different kinds of interaction. The birds studied by MacArthur are mostly territorial, they are relatively uninfluenced by minor variations in environmental factors, particularly microenvironment, and interfere with each other sufficiently to suggest that competitive exclusion is a t least a distinct possibility. Kohn (1959), however, found that the adult ecological niches of each species of Conus differ significantly with respect to a t least two of the following characteristics: nature of the food, nature of and relation to the substratum, and zonation of the marine environment. Kohn (1959) stated, “These differences are concluded to be the primary factors by which the ecological niches of species of Conus are differentiated. This is the mechanism which enables the maintenance of populations of large numbers of closely related, sympatric species of Conus in tropical regions.” I n other words, the fundamental niches of birds are large and, for the most part, independent of close environmental control, and the results obtained by MacArthur (1957) may reflect a series of nonoverlapping realized niches determined by competitive exclusion. But there is no evidence of territoriality or interference among different species of Conus (A. J. Kohn, personal communication). They are so sensitive to variations in the microenvironment that their fit to the MacArthur model probably reflects a condition of specialization with respect to food and substrate and mutually exclusive distributions that are controlled by environmental discontinuities and not competition. Correspondence with the predictions of the MacArthur model of nonoverlapping niches can be produced by (1) separate realized niches due to competitive exclusion of one species from the intersection subset of two intersecting fundamental niches (Fig. 3 B or C), (2) separate realized niches due to environmental discontinuities that are greater than the amount of intersection between fundamental niches, or (3) B*

30

RICHARD S. MILLER

non-intersecting fundamental niches (Fig. 3 A). Only the first of these alternatives requires the action of interspecies competition.

D.

CHARACTER DISPLACEMENT

Brown and Wilson (1956) proposed the term “character displacement” to describe a situation in which, when two species become sympatric, the differences between them are accentuated in the zone of overlap and are weakened or lost entirely in the parts of the range outside this zone. Any of a variety of morphological, ethological, ecological or physiological characters may diverge in this manner and they are assumed to have a genetic basis. While the most obvious function of character displacement may be to reinforce existing isolating mechanisms, it is usually thought to reflect a competitive interaction which has led also to niche differentiation (Brown and Wilson, 1956; Kohn and Orians, 1962; Mayr, 1963). Once a secondary contact between two cognate populations has been established, the species may interact in two ways to augment their initial divergence: (1) if inbreeding occurs, hybrid sterility or non-viability will lead to the reinforcement of reproductive barriers, and natural selection will favor a reduction in “gamete wastage” and further ethological or genetic divergence, and ( 2 )ecological displacement and a reduction in competition will also be favored by natural selection if the ecological characteristics have a genetic basis (Brown and Wilson, 1956). According to this theory interspecies competition leads initially to ecological divergence in the physical space of the intersection between the two fundamental niches. Ecological divergence is accompanied by character divergence, reduced competition, and reinforcement of ethological and ecological isolation. This theory describes a positive feedback mechanism which will continue to increase diversity, as long as it has selective value and hybridization does not intervene at an early stage disrupting the process. The adaptive differences between two sympatric species of nuthatches (Sitta) have been cited as a particularly clear example of character displacement (Brown and Wilson, 1956; Mayr, 1963). Xitta neumayer and X. tephronota largely replace one another in eastern and western Eurasia but overlap broadly in Iran. Vaurie (1951) showed that the two species are nearly identical in areas outside the zone of overlap, and in fact can only be distinguished by an experienced taxonomist; but where the two species occur in more or less equal numbers in the zone of sympatry in Iran, S. neumayer shows a marked reduction in bill length and overall bill size, and in the width, size and distinctness of the facial stripe. Conversely, S. tephronota shows a positive augmentation of all these characters in specimens from the zone of sympatry.

PATTEKN \ N I ) L’RO(‘I1;SS I N (”OIIII’HTITJON

31

Vaurie (1951) surmised that differences in bill size and shapr are correlated with different food habits and constitute a basis upon which the two species can avoid competition where they are sympat,ric, although he presented no evidence that would substantiate this conclusion. Unfortunate]y character divergence has received very little serious attention as an ccological phenomenon and there is only indirect evidence to support the view that it is related t o competition, attractive as this theory may be. Mayr (1963) has correctly emphasized the need for more quantitative analysis in the evaluation of character divergence. Sonie of the examplcs cited by Brown and Wilson (l95G) may illustrate hybridization rather than character displacement. There are cases in which species differences arc reduced in a region of sympatry, and there are also cases where the ovcrlap seems to have no effect on the phenotypes of the sympatric populations (e.g. sibling species). As Mayr (1963) points out, “Only a statistical analysis can bring out the facts needed for valid generalizations.”

E. I N V A S I O N S Elton (1958) has documented examples of changes in distribution resulting from the invasions of species into the geographic ranges of their cogeners, or of species which in some way require similar resources and become displaced in the resulting interaction. Thus the persistent spread of the ubiquitous European starling (Sturnus vulgaris) in North America has occurred at tlie expense of species such as the bluebird (Sialia sialis) and the flicker (Colaytes nztmtus) which have been forced to compete for a limited supply of the nest holes which they require for breeding. An overwhelming amount of evidence exists to show that when plants or animals invade a new area, they seldom do so without disrupting the ecological balance that existed before they arrived (Elton, 1958). The effect of competition in nature is perhaps best demonstrated by such invasions. Island faunas are especially vulnerable to invasion by new competitors (Mayr, 1963) and there are many well-documented examples. Greenwap (1958) has shown that most of the species of birds that have become extinct during the past 200 years have been island birds. However, as Mayr (1963) points gut, sweeping generalizations that attempt to predict the outcome of invasions from one fauna to another are not entirely reliable. There are exceptions, both in the fact that species native t o the larger more diversified areas are not necessarily superior competitors, and t o the assumption that such invasions inevitably lead to competitive exclusion. Moreover, there is indirect

32

RICHARD 9. MILLER

evidence that suggests that many of the birds that became extinct in New Zealand and the Hawaiian Islands were the victims of diseases introduced by the invaders (Mayr, 1963). Again, it is necessary that successful invasions and the extinction of members of the native fauna be carefully documented with supporting evidence of niche relationships before they are classed as evidence of competition. I n summary we may assign the Werent types of evidence for competition in nature to four principal categories, all of which contain elements of spatial relationships: 1. Mutually exclusive spatial distributions without supporting evi-

dence of a competitive interaction. 2. Mutually exclusive spatial distributions with supporting evidence of a competitive interaction. 3. Observed or inferred ecological displacement (usually correlated with character divergence) in sympatric populations. 4. Induced changes in distribution pattern. Udvardy (1952) and Andrewartha and Birch (1954) are critical of the use of competition to explain any aspect of variation and distribution of animals. After a review of examples from Lack’s (1944) article on species formation in passerine birds, Andrewartha and Birch (1954) concede that closely related birds either seem to live in different places or use different foods, but they note that “this is true, only more so, of distantly related species; but no one seriously suggests ‘competition’ as a cause for this.” They ask “Why then should it be necessary t o invoke competition to explain the same phenomenon among closely related species, especially when there is no empirical evidence for it?” Brown and Wilson (1956) agree that the evidence for competition in nature is scanty indeed, but they also suggest that Andrewartha and Birch (1954) have failed to appreciate the amount of evidence that does exist. The tendency for closely related species to inhabit different areas or to exploit different niches may in many cases originate from causes quite different from competition (Elton and Miller, 1954), and careful analysis of the critical variables in fundamental and realized niches is an obvious requirement in evaluating the role of competition in species interactions, as the preceding examples have shown. Statistical tests such as those for specieslgenus frequency, index of diversity, or species abundance distributions provide estimates which are more quantitative but are not necessarily more informative than direct observation, and they cannot be used to either prove or disprove the existence of competition in nature. Mutually exclusive distributions do not necessarily depend on competition, even when this seems to be the most immediate explanation. It is unfortunate, in this connection, that Mayr (1963)

PATTERN AND PROCESS IN COMPETITION

33

has chosen to use the term “exclusion” as though it were synonymous with competitive exclusion. It is obviously necessary to distinguish between observed patterns of mutual exclusion in spatial distributions and the cause of the distribution, which may or may not be competition. The correct alternative is not usually evident in the distribution pattern alone, but requires supporting evidence which will reveal the relationship between the fundamental niches of potential competitors. Nevertheless, there is also a growing body of evidence that establishes competition as an active force in species relationships in nature. When ecological displacement occurs in the realized niches of sympatric species that occupy broader niches outside the zone of sympatry, competition is clearly implied. If these observations are supported by accurate descriptions of the intersection of their fundamental niches with respect to critical factors which control their survival and habitat occupancy, a stronger case for competition is established. This is especially true when there is a strong element of interference in the interaction between the two species, as later discussions will show. It would be more convincing to be able to show, with appropriate controls, that the experimental addition or removal of a species affects the realized niche distribution of another. This has seldom been attempted, in spite of the potential value of such experiments.

V. CONDITIONSOF COEXISTENCE

It was stated earlier that the outcome of competition according to equations (1) and (2) depends on the inequalities a > K , / K , and fl > K,/K,. By reversing the aigns of the inequalities one by one it can be shown that there are four possible outcomes of competition in this model. Gause and Witt (1935) analysed the properties of this equation system to consider the essential types of competition that might exist between species. Two of the cases included in their analysis are of particular interest: Case 1 : a > K J K , and j? Case 2 : a < K , / K , and j?

> K2/Kl < K,/K,

(4)

(5) These cases are illustrated diagramatically in Fig. 6. In the diagrams, neither species can increase above its saturation line K,/a, K , or K , , RI/fland below its saturation line each species will tend to increase. I n the first case either N , or N , will be the sole survivor, depending on the initial concentrations of each species. I n the second case competition will lead to a stable, mixed-species population, regardless of the initial concentration of each species. An important feature of the second case is that there is homeostatic regulation of the composition of the stable

34

RICHARD S. MILLER

two-species population; disturbance of the balance in numbers will. lead automatically to re-establishment of the stable combination. Lotka (1932) and Windsor (1934) also recognized the theoretical possibility of infinite survival of both species in a mixed population. Windsor put the conditions in the form: up < 1. This requires that a singular point exists which is a “knot” on the surface of N , N , . This is guaranteed by the conditions u < K , / K , and p < K , / K , . The stable equilibrium will inevitably arrive a t the “knot” represented by point E (Fig. 6, Case 2) regardless of the initial concentration of the two species.

Care 1

Core 2

FIQ.6. Casen 1 and 2 for the outcoine of competition in the TAotke-Volterramodel (After Gause and Witt, 1935).

Gause and Witt (1935) assumed that the conditions of Case 2 would apply only when there was slight mutual depression of species, which might occur when two species belong to different niches in the same microcosm. They cited the example of Gause’s (1935) experimental demonstration of coexistence of stable, mixed-species populations of protozoans. Paramecium caudatum and P. aurelia are effective consumers of bacterial components suspended in the upper surface layer of a medium, while P. bursaria feeds on yeast cells sedimenting on the bottom of the experimental microcosm. Combinations of P . caudntum and P. bursaria, or P. aurelia and P . bursaria, can coexist because of this niche differentiation. Hutchinson and Deevey (1949) dismiss the possibility of coexistence in this case because they feel, as Gause and Witt (1935) assumed, that i t “implies that the ecological niches of the two species do not overlap completely.” There is nothing in the logistic theory that requires or supports this assumption, although it is presumably a corollary of the

PATTERN A N D PROCICSS IN COMPETI‘CION

35

axiom of inequality. Kostitzin (1939), who also dismisses the case of coexistence, reaches the further conclusion that intraspecies competition should be less violent than competition between two allied species. This statement introduces a curious mystique whereby speciation involves not only the evolution of normal isolating mechanisms, but also the sudden emergence of a competitive antagonism. Interspecies competition is assigned an arbitrary force which is presumed not t o exist within species. Cole (1960) finds no basis for these pronouncements and notes that Darwin not only referred to the fact that competition between closely related species will be more severe than between more distant relations, but that “the struggle will almost invariably be most severe between the individuals of the same species.” Cole (1960) states, “If Darwin was right the Volterra-Lotka analyses predict not competitive exclusion but coexistence.” Let us accept the proposition that some degree of ecological differentiation is one condition that will permit coexistence, provided the differentiation is great enough. The species diversity of any self-sustaining ecosystem, no matter how small, is sufficient t o substantiate this conclusion. We generally assume that the different species in such an ecosystem have distinct adaptations and requirements and are therefore compatible to this extent. It is also evident, at the other end of the scale of species difference, that members of the same species are able to coexist, even tbough their individual requirements are nearly identical. As they will also exhibit approximately identical responses to factors affecting their distribution and abundance, competitive advantage should be least pronounced among members of the same species. Or, stated in another way, the individual interaction values that comprise u or /3 should be nearly equal. Following this line of reasoning further, the degree of similarity between two species should also be reflected in the species interaction values u and /3. It is quite conceivable, in fact, that less competitive advantage ( u - /3) might exist between two sibling species than between the individuals of a highly polytypic species. Competitive exclusion, in such a case, would depend on the extent to which critical resources were limiting (e.g. the size of the total two-species population that the environment could support) and the constancy of the environment. Miller (1964b) examined the case of competition between larvae of the sibling species Drosophila melanogaster and D . sirnulam. These species are sympatric and apparently coexist in similar habitats throughout most of the temperate and tropic regions of the world. An initial assumption in the experiments was that these sibling species, because of the genetic similarity that underlies “their unusual morphological similarity (Moore, 1952; Miller, 1964b), are not only likely to

36

RICHARD S . MILLER

have similar geographic distributions and occupy similar niches in nature, but are also more likely than most species to have competitive interactions which are comparable. We might logically expect that the more nearly the ecological requirements of two species are alike and the greater the amount of intersection in their fundamental niches, the higher the probability their species interaction values will be the same. The experiments consisted of placing early first instar larvae in vials containing 5 cc of a standard medium to which was added 1/20 cc of a 15% yeast solution (Miller, 1964b).The cultures were allowed to develop a t 25OC and the production of pupae and larvae was recorded. In singlespecies cultures the larvae responded to increased crowding by extending the larval period and by progressive reductions in the final adult body size without significant increases in mortality. As noted earlier, this compensatory mechanism seems to occur in species which live in their food medium and compete mainly through direct exploitation of their food resources. There is, however, a minimum survival size which marks the limit of compensation for the effects of crowding, and both species showed a pronounced increase in mortality between formation of the pupa and emergence of the adult when the initial larval densities were raised above 120 per 5 cc of medium (Fig. 7). As maximum numbers of adults were produced when the initial larval density was 120 in single-species populations, this was defined as the “saturation density”. A t densities up to 120 larvae there was no significant difference in IS0

0 0

0

D.mdonogartbr D.rimulans

100

I

a

;

“3

5 0

a 50

0 I

100

200

300

lNlTiA1 LARVAL DENSITY

FIQ.I. Mean numbers of adult Drosophila melanogaster and D . sirnulam produced at different initial larval densities (After Miller, 1964b).

PATTERN AND PROCESS IN COMPETITION

37

the numbers of adults or pupae produced by the two species, although D. melanogaster had a higher production than D. simulans when the initial larval density was increased above this value. During interspecies competition between equal numbers of the two species at combined densities of 10, 20, 40, 80 and 120 larvae there was also no significant difference in the numbers of adults of each species produced. If we allow K , and K , to stand for the maximum production of adults of D. melanogaster and D . simuluns respectively at each experimental density up to saturation in single-species cultures, and consider N , and N , to be the number of adults of each from mixed populations, we can make the comparison shown in Table I1 and can test for the values of the interactions between them at each of the five density levels. TABLEI1 Numbers of Adult D. melanogaster (K, and N,) and D. simulans (K, and N,) in Single-Speciesand Two-SpeciesCultures (From Miller, 19643) Initial

Single-species

2-species

Larval Density

K,

Ka

Nl

N,

10 20 40 80 120

7 -8 17-0 33.6 58.8 74.6

7.9 16.9 33.6 54.4 69.0

4.3 8 -7 15.8 28.2 32.3

4.1 7 *7 14.3 28.2 37-2

Analysis of variance for the values of K,, K , , N , and N , at the five levels of density permitted the following conclusions: (1) K , N K , : the conditions of the experimental environment had the same survival value for both species at the density levels tested. (2) N , NN,:the total resources of the environment were shared equally between the two species. (3) ( K , - N , ) N , : the effect of N , on N , was the same as the effect of N , on members of its own species and therefore a = 1. (4) ( K , - N , ) N , : the effect of N , on N , was the same as the effect of N , on members of its own species and therefore /3 = 1. (6) a /3: the effect of N , on N , was the same as the effect of N , on N,. To test for differences in the values of a and /3 the logarithms of ( K , - N , ) , ( K , - N , ) and the observed values for N , and N , were andysed for variance. The comparison log a log /3 given by: N

N

N

Clog ( K , - N , ) - 1%

N 2 1

-

-

[log (K2- N , )

- 1%

N 1 1

(6)

38

RICHARD 9. MILLER

was seen to have an insignificant mean square, so that the values of a and fl may be considered equal. A considerable amount of ambiguity exists in interpretations of the results of interspecies competition. It is necessary to distinguish between two considerations: (1) maximum exploitation of the available resources by one species, or (2) equitable utilization of the resources and possible coexistence in a mixed species system. As most of the emphasis in competition experiments has been on the extent to which a population N , reduces the resources available to its competitor N , , there has been a tendency to ignore the far more interesting fact that the resources may be shared in such a way as to support two species. Terms such as “degree of interference” or “intensity of competition” may be completely misleading in this respect (cf. Merrell, 1951; Moore, 1952; Sokoloff, 1955). It is usually assumed that when the ecological requirements of two species are similar or nearly identical, the “intensity of competition” will be high and coexistence impossible; when their requirements are dissimilar they will compete less with each other and, therefore, may coexist. As noted earlier, this was assumed by Gause and Witt (1935) in their case for a stable equilibrium in mixed populations. The relationship between the sibling species Drosophila persimilis and D. pseudoobscura is remarkably like that between D. melanogaster and D. simulans. Their ecological requirements are almost identical and competitive superiority is only shown at extremely high densities. Sokoloff (1955) concluded that when these two species comPete with each other there is intense “interference”, even though adult survival is nearly the same for both species. When they compete with D. miranda, a more distantly related species, interference with the stronger competitor is not so great, even though the weaker competitor may be eliminated entirely. These results pose an apparent contradiction to the Gause principle, in that coexistence is usually more successful between closely related species than between more distant relatives. The expression ( K , - N , - aN,) merely implies that two species which compete with each other cannot each survive at the same density levels that are possible when only one species is present. Obviously N , cannot attain its maximum density K , when it shares the resources with N,. This refers to the exploitation of the total resources by two species, but does not exclude the possibility of coexistence, which depends on the relative values of cc and 8. Analysis of the results of the experiments with D. melanogaster and D. simulans showed that the values of K , and K , were not significantly different and we may therefore assume that K , = K , . It was also shown that a = 1 and fl = 1 and a and fl were not significantly different, and we may conclude that the competitive interactions between species were the same as those

PATTERN AND PROCESS IN COMPETITION

39

within species and a = jl = 1. This means that K , = K,/a and K , = Rs/Band the isoclines in Fig. 6 (Case 1) coincide. We may now state the general case for this relationship as follows: N , and N , will coexist at equilibrium densities which depend on initial concentration when : a = K,/K, and /3 = K , / K ,

(7)

These experiments were designed so that the initial concentrations of the larvae were always equal. The predictability of this model for different concentrations of the two species was not tested. However, equilibria occurred at points along the line 0s which corresponded to the density levels in the design of the experiments, and to this extent the data for N , = N , confirm the prediction of the general case for a two-species equilibrium. As this study only considered the case of competition during the larval stages of the Drosophila life cycle, there remained the possibility that factors affecting fecundity and fertility and the selection of oviposition sites will alter the course of competition by varying the initial concentrationsof the two species in this system. A series of experiments waa therefore designed to test competition between these two species for one complete life cycle (Miller, 1964~).Controls consisted of two pairs of adults of one species in each vial containing the same food medium used in the larval experiments; the experimental vials contained one pair of each species. The adult flies were allowed to lay eggs for 6 days and were then removed and the subsequent production of F, adults recorded. A total of 3 705 flies was produced from 111 competition replicates. The ratio of D. melanogaster to D. simulans F, adults was 51.1 to 48.9, which was not a significant difference. However, each replicate was a self-contained population in which the course of events had no direct relation to events in other replicates, and it was noted that there was marked dominance of one species or the other in individual populations. As competition was confined to a single generation and the total elimination of one species or the other was not a criterion of the experiments, there were two measurable categories of species dominance or competitive superiority: (1)the number of replicates in which a species waa the more successful (between-replicate dominance) and (2) the numerical dominance of one species over the other in individual replicates (within-replicate dominance). The lack of competitive advantage shown in the total numbers of each species produced was also reflected in the relative numbers of replicates in which each species was the more successful. D. melanogaster produced greater numbers in 51-4% of the 111 Competition replicates and D . simulans was dominant in 46.8%

40

RICHARD S. MILLER

with the numbers of each species equal in only 1 4 % . Table I11 shows the within-replicate dominance that existed in the competition cultures and Table I V shows the numbers of each species produced in control cultures. Three important facts emerge from these data: (1) the total numbers of adults produced in both the experimental and control replicates was well below the numbers that would be expected if the initial numbers of eggs and larvae were at the saturation densities established previously (Miller, 1964b); (2) total numbers of F, adults were not significantly different in the control and experimental populations; and (3) there was a distinct tendency for one species or the other to establish strong numerical dominance in each mixed-species population. A quantitative estimate of the species interactions within replicate populations was obtained by calculating the numbers produced by one species at each density level of the other. This relationship showed a general decrease of X2 ( D . simulans) with each increase in N , ( D . melanogaster)and vice versa. The rate of change of N , with each change in N , and the rate of change of N , with each change in N , was as follows:

With these and other data (see Miller, 1964c for details) it is now possible to construct a revised model of competition for one generation between D. melanogaster and D. simulans. This model (Fig. 8) shows that the numbers of F, adults that would be expected from the saturation densities established for larval populations of these species (Miller, 1964b) are not obtained when production depends on eggs oviposited by adult females. Secondly, when within-replicate dominance strongly favors one species over the other, the total numbers produced are higher than would be expected by chance; when the numbers of each species are nearly equal, the total numbers in each replicate are less than expected. I n what way can these data be used to explain the possible consequences of interactions in natural populations? There are two stages in the Drosophila life cycle that might be affected by competition: (1) the larval period when food quantity and quality might be critical and (2) the adult stage which is responsible for dispersal, habitat selection and reproduction. Larval competition, when it occurs, seems to consist of direct exploitation of the available food resources and will only be a

TABLEI11 .

Within-Replicate Dominance in Competition Cultures (FromMiller, 196aC) ~

~~

Females

Total

Mean & S.E. (Range)

Mean f S.E. (Range)

16.8 f 0-8 (5-30) 16.6 f 0.9 (5-35)

32.1 & 1.5 (12-53) 34.8 f 1.6 (13-60)

Males

D. sirnulana

D . melanogaster Dominant Species

Number of Replicates

D. melanogaster D . aimuluna

57 52

Mean f S.E. (Range) Mean f S.E. (Range) 13.7 f 0.8 (3-26) 2.9 f 0.5 (0-13)

1.6 f 0.4 (0-12) 15-3 f 0.8 (4-27)

T A B L EIV Number of Flies Produced in Control Cultures (From Miller, 1964-c) Males

Females

Mean f S.E. (Range)

Mean & S.E. (Range)

13.8 f 1.4 (0-30) 16.5 f 1.7 (0-28)

27.5 f 2.6 (0-48) 30.9 f 3.1 (0-52)

Species

Number of Replicates

Mean f S.E. (Range)

D. melanogaster D. aimulana

36 29

13.7 1.3 (0-24) 14.5 f 1.6 (0-27)

-+

Total

RICHARD S. MILLER

42

factor when the population reaches a critical density in relation to the amount and quality of food. It is evident that species interactions at this stage need not lead to the selective elimination of one of the competing species. The interactions values ( a = fi = 1) may in fact allow complete coexistence of both species, except at extremely high densities. The results obtained by Sokoloff (1955) for larval competition between the sibling species D . pseudoobsczsra and D. persirnilis were not analysed in this way but suggest an identical relationship. It would appear therefore that the outcome of competition in this system depends primarily on genetic and environmental influences affecting fecundity and fertility of the parental generation.

L

K1.5 a PIO.8. Model of competition between Drosophila melamqaater and D . tiimulans for one generation (After Miller, 1 9 6 4 ~ ) . Nc,

NoI

Competition could occur a t the adult stage between females that require access to a limited number of oviposition sites, or through interactions between larval and adult populations when the larvae alter the suitability of the medium as an oviposition surface (Sang, 1950; Miller, 196413). Interference apparently does occur among adults, or between adults and larvae, as shown by the exponential change of N , with changes in N , in the model in Fig. 8. Nevertheless, the potential fecundity of the adult females is not realized and the larval population never reaches saturation in this system. Chiang and Hodson (1950) have shown that the character of the surface of the medium changes rapidly as the numbers of larvae increase. These changes lead to marked

PATTERN AND PROCESS I N COMPETITION

43

reductions in realized fecundity and fertility after the first few days of cultures, so that the conditions suitable for a high rate of production are restricted to a very short period (Robertson and Sang, 1944). Natural breeding sites also deteriorate rapidly in relation to their suitability as oviposition surfaces (Carson and Stalker, 1951) and seldom contain more than a few eggs or larvae (cf. Gordon, 1942; Birch and Battaglia, 1957; Sokoloff, 1957). Harrison (1964) studied the factors affecting the abundance of four species of Lepidoptera that spend their life cycles on banana plants, and concluded that they are not affected by intra- or interspecies competition because they normally lay so few eggs per unit area that their population levels never reach critical densities in relation to the food that is available. Adult female Ceramidia butleri will lay far more eggs on banana plants in cages in an insectary than they will under natural conditions in plantations, and the larval densities required to produce a significant decrease in pupal weight and an increase in mortality in the laboratory are much higher than densities recorded in the field. Population control through limitations on realized fecundity is so effective that competitive exploitation does not occur (Harrison, 1964). An absolute shortage of food is probably a rare event in the lives of animals such as insects and other invertebrates that would normally compete through exploitation. I n spite of the tremendous increase potential these animals possess, their populations appear to be regulated quite strongly by climatic factors that tend to reduce fecundity, fertility and adult longevity t o values that are only fractions of those reached under optimum conditions (Birch, 1948). Birch (1945, 1963) has shown, for example, that the beetles Rhizopertha dominica and Calandra oryzae are extremely sensitive to temperature and moisture in their rates of development and in population characteristics affecting their intrinsic rates of increase. Data for other poikilotherms are less precise than those provided by Birch’s elegant studies, but it is well known that their population characteristics are affected in much the same ways by relatively slight changes in physical factors. If competition for food occurs in such populations, it is likely to be a transient phenomenon that occurs only infrequently. The fact that population irruptions or “outbreaks” are especially characteristic of certain insect populations and are seldom observed in homiotherms lends support to the view that the populations of most terrestrial insects are normally under climatic control. They only express rates of increase approaching their full potential when an unusual combination of optimum conditions occurs. I n species such as dung and carrion insects, on the other hand, in which the oviposition site and larval environment are less subject to the effects of physical factors and over-population is more liable to

‘

44

RICHARD S. MILLER

occur, there is often a strong interference component that limits the number of eggs laid, or a sequence of rapid sera1 changes in the oviposition site that restrict egg laying to a relatively short period. For example, several burying beetles (Necrophorus)may collaborate in the burial of a carcass, but aggressive interference ensures that only one pair of adults will finally remain in possession of it (Wynne-Edwards, 1962). Such interactions are not confined to intraspecific encounters, as I have witnessed the same thing among different species of Necrophorus. I n this example, competitive interference limits the size of the F, generation and consequently reduces the probability of heavy exploitation among the larvae. The ecological advantages of this arrangement are fairly obvious. Laboratory studies of competition have demonstrated that direct exploitation in crowded populations may lead to extremely high mortality of larvae and severe reductions in the size of the F, generation. If climatic or other environmental controls do not prevent the occurrence of potentially harmful rates of exploitation, there will be a selective advantage in the development of effective interference mechanisms within and between species populations. It was noted earlier that the traditional emphasis on selective elimination in laboratory studies of competition has tended to obscure the more interesting fact of extended coexistence that is frequently observed in these populations, even when the conditions of the experiment are designed to achieve maximum competition. The experiments with D. melanogaster and D. simulans adults and larvae (Miller, 1964c) established the fact that interactions between sibling species in a uniform environment can have equal value, but this series of experiments involved events in only one generation. Conventional competition theory would argue with some justification that a competitive advantage, however slight, is bound to accrue to one species or the other in a stochastic projection of a mixed-species system through several generations. If we grant this objection to the models developed earlier, we must then ask "What degree of species difference or environmental fluctuation would permit indefinite coexistence of the two species?" Moore (1952)found that D . melanogaster eliminates D. simuluns when they compete in population cages kept a t a temperature of 25"C, but the competitive advantage is reversed at 15°C. However, the progress of competition and its outcome depended partly on the age and quality of the food, which was a function of the rate at which the food medium was renewed. Conceivably coexistence could have been maintained indefinitely either by keeping the populations at some intermediate temperature between 15" and 25"C, by periodic fluctuations in temperature, or by selecting an appropriate program of food renewal. Even with the experimental design that was followed, D. melanogaster was

45

PATTERN AND I’RO(’ESS IN COMPXTITION

only reduced to 45% of the total population in one cage after 402 days at 15OC. I n a similar study of competition between D. melanogaster and D. funebris in population cages, it was found that fresh medium favored the production of D. melanogaster while D. funebris was more successful than D. melanogaster in older food (Merrell, 1951). I n an otherwise constant environment, periodic renewal of the food cups introduced environmental fluctuations that were sufficient to allow coexistence of these species for almost 2 years, after which the experiment was terminated. Table V shows the time required for extinction of either Tribolium castaneum or T . confusum in mixed-species populations in different volumes of flour a t 29°C and 65 to 70% relative humidity (Park, 1948). The populations were started with an equal number of adults of each species. The minimum time of 270 days required for extinction of T . castaneum in 8 grams of flour is equivalent to approximately 8 generations at 29”. The maximum time of l 470 days in 80 grams of medium is roughly equivalent to 42 genwitions of coexistence in a uniform environment. TABLEV Period Required for Extinction of Tribolium castaneum or T. confusum at 29°C and 65-70% R.H. (Datafrom Park, 1948) Initial Adult Population

Amoiint of Medium (grams)

8 40 80

8 40 80

ReplicaLcs

Days to Extinction Minimum Maximum Mean ~

15

0 2

270 300 840

_

780 1020 1470

_

_

_

_

_

548 513 1155

There are numerous examples in the literature showing that selective elimination of species through exploitation of food may require an extremely long time, even when food and space are artificially limited and the environment is kept as uniform as possible. The remarkable fact in these results is not the traditional observation that “there is some ecological difference between the two species that permits coexistence” -this much is axiomatic -but that coexistence even in crowded populations seems t o require such slight alterations in a single factor, especially in relation to event,s in natural environments. The restrictions mentioned previously on expressing niche relationships in terms of set theory included the assumption that the probability of survival is equal at all point,s within the fundamental niche. This, as

%

~

46

S l C I i A S U S . MILIJES

Hutchinsori ( 1 ! ~ 7 )points out, is highly unlikely and we ordinarily expect that there will be an optimal part of the niche with suboptimal conditions near its boundaries. This is reflected, of course, in the law of tolerance and is seen in the outcome of competition between T . cnstaneum and T . confusum under different conditions of temperature and moisture (Park, 1954). Table VI shows the percentage of replicates for each treatment in which T . castaneum or T . confusum eventually persisted and its competitor was eliminated (extinction of one species was a condition of the experiment). At high temperature and moisture T . castaneum persisted and T . confusum was eliminated in all replicates; a t low temperature and humidity the reverse occurred. I n the latter situation the failure of T . cnstaneum to survive was not due entirely to competition. In single-species controls T . castaneum had a mean life-duration of 350.0 f 34.1 days, but this was reduced to 27.15 f 18-1 days when T . confusum was present, so that the effect of the mixedspecies interaction was to hasten the elimination of T . castaneum which would have occurred in any event. The most interesting feature of these results is, however, the “indeterminate” outcome of competition when temperature and moisture were between these extremes. Thus, although T . confusum eliminated T . castaneum. in 71% of 28 replicates a t 24°C and 70% relative humidity, T . castaneum won in 29% of the replicates. The results were therefore “probabilistic” rather than “deterministic” (Park, 1054). TABLE

VI

Selective Eliminotion .f Triboliuin cavtaneum and T. confusuin in Relation to Temperature and Moisture. (Data front Park, 1954) Treatment Tempera,ture Moisture

34 34 29 29 24 24

Percent of Replicates in which Species Persists

(Percent R.H.)

T.castaneum

70 30 70 30 70 30

100 10 86 13

29 0

T.coi&wrn 0 90 14 87 71 100

This interaction has been analysed in detail by Neyman, Park and Scott (1968) and is discussed in terms of the Gause cases by Slobodkin (1961). The patterns of competition for each set of conditions (Table VI) can be represented by a series of empirical diagrams that effectively

PATTERN AND PROCESS IN COMPETITION

47

replace the diagram of Case 1 (Fig. 6). The diagram for 24OC and 70% RH is shown in Fig. 9. The line 0s (Fig. 6) becomes an indeterminate zone of possible initial numerical combinations of T . castaneum and T. confusum (Fig. 9) in which either species may eliminate the other. Outside this zone the outcome of competition is deterministic. Different combinations of temperature and moisture alter both the shape and the position of the indeterminate zone. Thus, a t the highest temperature and humidity T . castaneum invariably persists and T. confusum is eliminated in mixed-species populations, even though these conditions are within the fundamental niche of both species. I n other words, at high temperature and humidity the zone of indeterminacy disappears ; the lowest temperature and humidity created conditions outside the fundamental niche of T . castaneum.

T confusum

FIG. 9. Diagram of the outcome of coniprtition between Triboliirm cnslatiruni nnd 7'. confwum at 24OC and 70% H.H. (After Neyniaii, Park and Rrott. 1958).

Inasmuch as different parts of tho fundamental niche have different survival values, the same is true for points within the intersection subset of competing species. Slobodkin (1961) points out that if there is also differential survival of the two species in the zone of indeterminacy, as the analysis by Neyman, Park and Scott (1958) suggests, their diagrams become probability of outcome surfaces, introducing stochastic processes into the Gause case for this interaction. The indeterminate model for Triboliurn and the analogous model for Drosophila imply that a position may exist within the intersection subset of two fundamental niches corresponding to equal or nearly equal probability of survival of both species. Such a conditioii would only be I~elevitntto direct or

48

RICHARD S. MILLER

indirect exploitation of the resources contained within the intersection subset of their niches, and would not usually apply in the case of competitive interference with access to the resource. Chance oscillations in the environmental variables controlling the values of tc and /Imight pass back and forth through the equilibrium point for the two species, continually reversing the direction of competition and the probability of survival of one or the other of the competitors (Hutchinson, 1948). The theoretical possibility of a stable equilibrium is instructive, even though it could not be sustained in a naturally changing environment. Its principal value lies in the fact that it allows us to recognize conditions which would permit the coexistence of two species and to examine these criteria with respect to events in natural ecosystems. Thus, these analyses support Hutchinson’s (1948) observation that the rule of competitive exclusion need-not apply when (1) external factors act to rarefy the mixed-species population so that the required resources are not heavily exploited, or ( 2 ) when the values for tc and @ are under environmental control and chance oscillations prevent the establishment of a permanent equilibrium.

EXCLUSION VI. CONDITIONSOF COMPETITIVE The conditions of temperature and moisture in Park’s experiments with Tribolium confusum and T . castaneum may be viewed as a set of points in the intersection subset between two fundamental niches (Fig. 2, Case 2). It is evident from the data for control replicates that all points in the fundamental niche spaces N, or N, do not have equal survival value for the species, which in turn implies that the outcome of competition between two species with intersecting niches will not be the same at all points in their intersection subset N,.N,. This will be the case especially in interactions where the dominant form of competition is exploitation and the outcome of the interaction depends on (1) the ability of each species to survive, in the absence of interspecies competition, a t different points in the niche space of the intersection subset, and (2) their different exploitation and survival rates during interspecies competition. Park’s experiments provide an especially good illustration of the change in interaction values occurring at different points in the intersection subset, and of the fact that an indeterminate zone exists where the outcome of competition cannot be predicted with certainty. Rather than the strict system of fundamental and realized niches referred to earlier with reference to Case 1 and Case 2 (Fig. 2), the indeterminate zone is an area of probabilities in which both species may occur with changing frequency. However, when competition is chiefly through interference, there tends to be a more definite exclusion point corresponding to the

PATTERN AND PROCESS IN COMPETITION

49

combination of factors which represents the limits of niche space within which species S, is able to exert its competitive superiority and completely exclude S,, or vice versa. As long as interference prevents access to the resources contained within a niche space, the realized niches of the two species can be described in spatial terms relative to the environmental variables that control the interaction. The conditions of competitive exclusion through interference are particularly well-illustrated in the case of an “included niche”, in which the niche (N,) of species 8,is a proper subset of and is included within the niche (N,) of species S,. As noted earlier, this situation immediately imposes certain strict conditions on the interaction. I n order for S , to survive in an included niche, it must be competitively superior to S,, otherwise it would be completely eliminated from this biotope. This with its smaller niche space, is a more relationship also implies that AS,, specialized species with respect to the variables determining N, and N,. A system of included niches therefore offers an opportunity for coexistence within the total biotope B by means of specialization of S, and the ability of S, to survive within the difference subset N, - N,. It is of considerable interest that several examples of this relationship exist among different taxonomic groups. These examples will be reviewed in some detail in order to define their common properties.

A.

MAMMALS

It has often been noted that pocket gophers (Geomyidae) do not form mixed-species populations and are mutually exclusive, even in local habitats. Their geographic distributions reflect this intolerance, in that the ranges of two species may meet in contiguous allopatry but do not become truly sympatric. An investigation of the ecological relationships among four species of pocket gopher which are at or near limits of their continental distributions in Colorado showed that their habitat and geographic distributions are essentially governed by three factors: soil depth, soil texture and competitive exclusion (Miller, 1964a). All four species seem to prefer deep, sandy soils but, as illustrated in Fig. 10, they differ in their abilities to burrow in shallower and coarser soils. For example, Geomys bursarius is mostly confined to deep sand or sandy loam soils, while indurate soils such as compacted clays or coarse gravels are barriers to its habitat and geographic distributions. At the other extreme, Thomomys tdpoides also prefers deep, sandy soils but can burrow in extremely coarse soils and occurs throughout a great variety of soil types and habitats. Although the four species differ slightly in food habits and perhaps in other respects as well, these differences do not appear to be critical and their fundamental niches are essentially defined by their responses to the two variables of soil

50

RICHARD S. MILLER

FIQ. 10. Relative tolerances of pocket gophers to soil depth and soil texture (After Miller, 1964a).

depth and soil texture. Thus the relationships between the four species can be described as a system of included niches based on these two environmental variables. It was also shown in this study that when the ranges of two or more of these species meet, the species with the greatest range of tolerance to these factors tends to be excluded from the preferred habitat and is displaced to less favorable environments. Thus, for example, the range of Geomys bursarius interdigitates into the general ranges of T . talpoides and T . bottae along river margins where sandy soils occur. When T . bottae and T . talpoides meet along mountain slopes, T . bottae tends to occupy the deeper soils at lower elevations, while T . talpoides is displaced upslope into less favorable soils. Survival therefore depends on finding sufficient space in habitats outside the included niche of the superior competitor. The order of fundamental niche space occupied by the four species 8.6determined by soil depth and texture is: Geomys bursarius < Cratogeomys m t a m p s < Thomomys bottae < Thomomys talpoides. When competition occurs between any species pair in this group the one with the smallest niche space occupies the position of N, in the relationship illustrated for Case 1 (Fig. 2) and the other species is excluded to the difference subset N, - N,. The corresponding ranks of competitive ability are: G e m y s bursarius > Cratogeomys castamps > Thomomys bottae > Thomomys talpoides. Each case of competitive exclusion that was observed when the ranges of the two species met in Colorado, or has been reported for combinations of these species elsewhere, conformed to this general

PATTERN AND PROCESS IN COMPETITION

51

relationship (Miller, 1964a). We conclude from this that the superior competitor is in some way more specialized and that its distribution is governed solely by its relation to the variables of soil depth and texture. These four species show morphological differences in body size and fossorial development that correspond to their competitive rankings. Gemys bursarius is the most obviously fossorial, with a relatively massive skull that is flattened doro-ventrally, reduced eyes and ears, and large forefeet and claws. Because of the pronounced fossorial character of its claws and feet it walks with difficulty, with the feet splayed outward like those of a mole. Thomomys talpoides, at the other extreme, is a more generalized, mouse-like rodent. I n body size, C. castanops is somewhat larger than G. bursarius, T . bottae is next in size, and T . talpoides is the smallest. As there is a correlation between body size and soil type in pocket gophers, with the largest individuals and subspecies occurring in deep, sandy soils, it is difficult to judge the extent to which observed differences in body size are hereditary or phenotypic. On the one hand, large body size might confer an advantage in aggressive encounters, which undoubtedly occur between these highly territorial animals, but smaller size may be advantageous when an animal is forced to live in more indurate soils. Kennedy (1954, 1959) suggests that the relatively smaller size of (2. bursarius may have adaptive value, allowing it to survive in less favorable habitats when it competes with G. personatus. The ranges of the yellow-pine chipmunk (Eutamiasamoenus) and the least chipmunk (E. minimus) overlap narrowly in the eastern foothills of the Rocky Mountains in Alberta, where E. amoenus occupies the open forests and E . minimus is mostly confined to alpine slopes. Wherever other species of Eutamias occur, E. minimus generally seems to be displaced either to sagebrush desert or to alpine habitats, although in regions of North America where there are no other western chipmunks, E. minimus also occurs in forest habitats, suggesting that its fundamental niche is in fact relatively broad. In a study of the oompetitive relationships between Eutamias amoenus and E . minimus in their region of sympatry in western Alberta, Sheppard (unpublished) observed that the most consistent difference between the habitats of the two species is in the amount of vegetative cover present. Using the classification of vegetation layers proposed by Elton and Miller (1954), Sheppard recorded the percent occurrence of each type in vegetation samples from habitats occupied by each species. As shown in Table VII, the typical habitat of E. amoenus contained more vegetation of all types, especially shrubs and trees. Both species use shrubs and trees as “ewape routes” when alarmed, but E. minimus will apparently tolerate more open habitats in this respect, moving across

52

RICHARD S. MILLER

greater distances in the open and making greater use of alternate forms of cover such as fell boulders and logs. Other ecological differences such as food habits were not great, and could be explained by the frequency occurrence of particular food species within the different .habitats, rather than an expressed preference. There is, however, a difference in the body sizes of the two species and corresponding differences in aggressive behavior. TABLEVII Percent Occurrence of Vegetative cover in Habitats Occupied by E. amoenus and E. minimus in WesternAlberta Percent Occurrence E. amoenus E. minimus Habitat Habitat

Vegetation type -

Field layer Shrub layer Tree layer

.

~~

68.9 73.3 87.8

57 *8 14.4

31-1

Brown and Wilson (1956) suggest that character displacement reduces competition and increases isolation, and Kohn and Orians (1962) maintain that all instances of character displacement probably involve ecological displacement as well. Sheppard (unpublished) compared the body sizes of the subspecies Eutamias minimus listed by Hall and Kelson (1959). The largest subspecies in North America occur where this is the only representative of the genus, while in regions where there is potential or presumed competition with other species of Eutamias, the subspecies of E. minimus are smaller. Sheppard also compared the body lengths of E. amoenus and E. minimus from within his general study area in western Alberta where (1) the two species live in adjacent habitats and are potentially sympatric and (2) where they are sufficiently allopatric that there is little or no continued contact. This comparison is shown in Table VIII. E. amoenus is consistently larger and E. minimus smaller in areas of sympatry, although the withinspecies differences between sympatric and allopatric populations were only significant for male minimus (t = 2-57, P < 0.02). The values for female amenus (t = 1-73, P ca. 0.09) and female minimus (t = 1.82, P ca. 0.075) approach significance. While these data indicate a case of competitive exclusion, they do not show conclusively that E. minimus in this region can survive outside the habitats in which it is presently found, or that the observed distributions depend on more than different habitat preferences. Sheppard (unpublished) therefore removed resident populations of E . amoenus

PATTERN AND PROCESS IN COMPETITION

53

from two areas of typical forest habitat and introduced approximately equal numbers of E. minimus and, likewise, introduced E. amoenus into areas previously occupied by E . minimus. Introduced populations of 10 E. amoenus in each of two areas either failed to survive or dispersed away from the alpine habitats where E . minimus had lived before. On the other hand, of 15 E. minimus transplanted into E . amoenus habitat, 3 were recovered 1 year later, 1 was still present after 2 years, and an immature E . minimus captured 2 years after the original introduction was presumably the offspring of a pair of the introduced adults. Although the survival rate for the introduced E . minimus was not particularly high, this experiment did show that they are capable of living and probably reproducing in habitats from which they appear to be excluded. TABLEVIII Body Lengths ( m n ~of) Adult Eutarniits amoenus and E. minimus from Symputric and Allopatric Habitats Malcs Mean & S.E. (Range) -.

._

Females Mean & S.E. (Range) . .

Eutarnias amoenus Allopatric Sympatric

121.3 f 0.54 (102-127) 122.2 1.40 (113-130)

125.1 0.5G (114-132) 127.4 f 1.53 (111-138)

112.4 f 0.85 (105-118) 109.5 0.76 (102-115)

115.9 & 0.82 (106-127) 113.4 & 1.14 (103-120)

Eutarnias mininaus Allopatric Sympatric

+

Sheppard (unpublished)concluded from these and other data that the relationship between these two chipmunks is broadly similar to that described by Miller (19G4a) for pocket gophers. E. amoenus apparently occupies an included niche (N,) within the larger, fundamental niche (N,) of E . minimus, while E. amoenus is a superior competitor which in areas of sympatry displaces E. .minimus into the difference subset (N, - N,) of their two niches. To test this theory further Sheppard conducted a series of laboratory tests of the behavior of the two species during aggressive encounters. For example, for one set of experiments Sheppard constructed an apparatus consisting of a centrally located food chamber from which a screen tunnel ran for 6 feet in either direction to a pair of nest boxes. An individual E . amoenus was placed in one nest box and an E . minimus in the other and their behavior observed from be-hind a screen. In a total of 71 contests between individuals of the same sex and age group, E . amoenus won 672 aggressive encounters and lost only 23. I n 60 of C

64

RICHARD 9. MILLER

the 71 contests the E. amoenus individual was the first to emerge from the nest box; on 43 occasions an E . amoenus individual entered the central chamber and fed, while only one E . minimus did so; and the E . amoenus spent a total of 2 185 minutes outside the nest box while the E. minimus remained outside for a total of only 983 minutes. I n these and other experiments E. amoenus individuals were consistently more aggressive and demonstrated their competitive superiority in physical encounters. This model also seems to be the best method of describing the pattern of interaction between the black rat (Rattus rattus) and the brown or Norway rat (Rattus norvegicus). The earlier arrival of the black rat in Britain, with the return of the Crusaders during the middle ages (Matheson, 1939), allowed this species to occupy most of the British Isles. The subsequent arrival of the brown rat at the begiiining of the 18th century has apparently been responsible for the disappearance of the black rat from most of the areas it occupied previously. A similar replacement is occurring in U.S., where the brown rat replaced the black rat in an area of 1 0 0 0 sq. miles in southwest Georgia between 1946 and 1954 (Ecke, 1954). The black rat is often arboreal, however, and in urban areas this allows it to coexist to a limited extent with the brown rat -the black rat occupies the top stories of buildings, travelling along power lines and rafters, while the brown rat inhabits the ground level (Southern, 1964). Relationships between the wood mouse (Apodemus sylvaticus) and the yellow-necked mouse (A.Jlavicollis)and the wood mouse and the bank vole (Clethrionomys gkreolus) invite a similar explanation. The larger yellow-necked mouse occurs entirely within the range of the more widespread wood mouse, except in northern Europe, but is absent, from large areas (Southern, 1964). I n Britain A . Jlavicollis occurs in pockets throughout populations of A. sylvaticus, but is more strictly confined to woodland habitats while A. sylvaticus is also common in fields and scrub. The habitat preferences recorded for these species in Europe also confirm this relationship (Grodzinski, 1959). The bank vole has a much more restricted distribution than the wood mouge in British woodlands, especially in winter when the ground layer of vegetation disappears (Evans, 1942; Miller, 1955; Kikkawa, 1964). This seems to be related to the fact that the bank vole is more active during the day and would be exposed to greater risk of predation if it did not restrict its movements to the immediate vicinity of protective cover. There is thus a relatively large amount of intersection in the spatial elements of the fundamental niches of these two species in summer when ground cover is abundant and the bank vole can move more freely, but interference is alleviated by the fact that the two species have different

PATTERN AND PROCESS IN COMPETITION

55

activity rhythms and distribute their use of the environment over somewhat different times of the 24-hour cycle (Miller, 1955). I n winter, however, when movements of the bank vole are most severely restricted, food resources are less abundant, population numbers are high, and interspecies competition becomes more critical (Kikkawa, 1964). I n order for C. glareolus to survive as it does in a niche included within the larger fundamental niche of A . sylvaticus it must have some competitive advantage. Kikkawa’s observations on aggressive behavior and dominant-subordinate relations show that voles are especially aggressive and tend to form dominance hierarchies and probably do interfere with access by mice to areas occupied by the voles.

B.

RTRDS

In spite of a vast literature on birds it is difficult to find well-documented information on their habitat requirements and interspecies interactions. Nevertheless, certain observations suggest that included niches occur commonly between many species. Snow (1954) concluded that most members of the Poecile group of titmice in Europe are separated by habitat and that the local absence of one member of a closely related pair has not been found to affect the habitat preference or size of the other, except in the case of Parus palustris and P. atricapillus, which are more similar than are any other sympatric Palearctic species of this genus. There is evidence that P. palustris has replaced P. atricapillus in four out of five instances, while in three cases where P. palustris is absent and its habitat available P. atricapillus has not extended into it. This is in striking contrast to the situation in North America where, with the exception of P . hidsonicus which overlaps widely with P. atricapillus, all of the Poecile group replace one another geographically, with some rather narrow zones of overlap (Snow, 1954). The system of relationships among the Paridae of North America indicates a possible system of included niches. P. atricapillus has the widest range, across the whole of the northern part of the continent, but is replaced in the southeast by P . carolinensis, in the Rocky Mountains by P. gambeli, on the western seaboard by P. rufescens and in the mountains of Mexico by P. schteri. Detailed studies of competitive relationships among these species have not been made, but where the ranges of these forms are contiguous or overlap they are separated by habitat differences, and Snow (1954) concludes that “The fact that no two species of the same genus overlap widely, except for P. hudsonicus and P. atricapillus, suggests a more recent, less complex evolutionary history for the genus in North America, a suggestion which receives support from the fact that on the whole differences between species are not nearly so great

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RICHARD S. MILLER

as they are in the Palearctic.” These observations seem to suggest, in other words, that competitive exclusion may still be an active ingredient in the more recent evolutionary events affecting this genus in North America, and that P . atricapillus, with its broader geographic range and presumably greater tolerance to habitat variation, is only able to survive outside the included niches of its competitors. Thus, Snow seems to feel that the habitat differences that are observed among members of this genus in Europe, such as between the coal tit (Parus ater) which searches for insects on the trunks and larger branches of trees and the blue tit (P. caeruleus) which concentrates on twigs and leaves (Snow, 1949), are due to ecological differentiation and no longer involve competitive displacement. A more precise study of the relationships between two species of this genus in North America has been made by Dixon (1954). In the past two decades Parus rufescens has become established as a breeding bird in the district immediately east of San Francisco, but its spread is impeded by competition with its larger cogener, Parus inornatus. I n all cases where the two species come into contact, their breeding territories are mutually exclusive and, in the face of antagonism by the larger form, the adjustments permitting co-occupancyof the area appear at this stage to be made entirely by the smaller, less specialized species. These include the use of vacated or suboptimal nesting territories, modification of territorial behavior, and a more varied choice of food items. Thus, the recent entry of P. rufescens into the range of its larger cogener has been made possible by the availability of a niche space outside the more specialized, included niche of P. inornatus. The yellow-headed blackbird (Xanthocephlus xanthocephalus) is restricted in its nesting sites to emergent vegetation, e.g. bulrush (Scirpus), cattail ( T y p h ) or Phragmites in fairly deep water (Nero, 1964). The red-winged blackbird (Agelaius phoeniceus) occupies the same marshes as yellow-headed blackbirds but nests in a greater variety of situations. Most nests are located in cattails but redwings will also nest in low trees, shrubs or any weeds that will support a nest (Orians, 1961). Male redwings arrive on the breeding grounds and begin to establish territories somewhat earlier than yellow-headed blackbirds. I n the vicinity of Saskatoon, Saskatchewan the first recorded arrival of male redwings in spring was 7 to 20 days (average = 13 days) earlier than the first male yellow-headed blackbird during 6 years from 1960 to 1965 (J. B. Gollop, personal communication). I n 1964 and 1965 the author observed interspecific relationships between these two species on a small marsh near Saskatoon. Male redwings were engaged in territorial display throughout most of the marsh by the time the first yellow-headed blackbirds arrived, but within a few days the yellow-headed blackbirds had

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occupied the emergent vegetation in deep water near the center of the marsh, and had displaced the redwings t o more peripheral nest sites in spite of persistent harassment by the redwings. The territories established by the yellow-headed blackbirds in their first few days on the marsh remained intact throughout the remainder of the breeding season.

c. AMPHIBIA W. F. Blair (personal communication) has followed events for several years in a temporary pond containing populations of the bullfrog (Rana catesbiana) and leopard frog (Rana pipiens). R. catesbiana requires a habitat of standing water but R. pipiens can also live in more terrestrial environments. When drought reduced the pond to almost nil, R. catesbiana disappeared and only a few, scattered R. pipiens remained. When the pond refilled after a wet spring, the 12. pipiens population “exploded” to a very high density, far greater than the pond could normally sustain. Gradually, the numbers of R . catesbiana also increased and the numbers of R. pipiens declined. When R. pipiens was the only species present it filled the entire habitat, but when the R. catesbiana reappeared this species occupied the water environment and displaced R. pipiens t o drier sites near the edge of the pond. The salamanders Plethodon dunni and P. vehiculum are abundant in the rocky outcrop-talus slope ecosystem of the coast range of Oregon, where they occupy approximately the same habitats. P. dunni tolerates slightly lower temperatures and wetter substrates than P. vehiculunz while P. vehiculum is tolerant of lower relative humidities and higher temperatures than P. dunni, although their preferences for cool, humid conditions are not significantly different (Dumas, 1956). Although temperature does not significantly alter the humidity preference of the two species within the normal range of humidity encountered in their natural environments, there are specific differences in their substrate distributions which are apparently due t o the presence of P. dunmi ill the preferred sites and displacement of P. vehiculum t o lion-preferred but tolerated habitats. This interaction becomes especially critical in spring and fall, when the weather is variable and there is great risk of exposure to lethal environmental conditions, and when P. vehiculum is found far more often than P. dunni in suboptimal “transient habitats”. Dumas (1956) examined 36 filled stomachs of P. dunni and 37 of P. vehiculum to determine the extent of ecological differentiation in their food habits, because of the stress that is often placed on this factor in competitive interactions. He found that collembolans are the greatest food source for both species, but that P. dunni consumes a greater variety of foods than P. vehiculwm. There was a total of 39 types of food with a mean of 8.36 items per stomach in the P. dunni sample,

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and a total of 28 foods with a mean of 20.84 per stomach in the P. vehiculum sample. The greater number of individual items in the P. vehiculum stomachs is explained by the fact that the somewhat smaller salamander ( P . vehiculum, snout-vent length 46 to 57 mm) consumed far more small-sized forms such as mites than did the larger species ( P . dunni, snout-vent length 48 to 65 mm). When the foods were separated by frequency index into “primary” and “secondary” foods, it was found that of 16 primary foods 10 were shared by both species but P. vehiculum had fewer secondary sources (14) than P. dunni (27). The similarity of primary food sources might suggest rather strong competition for these items, but P. dunni has more secondary sources and would be better able to survive periods of food scarcity than P. vehiculum. Dumas (1956) concluded that foods acceptable to both species are sufficiently abundant that competition for this factor will rarely be critical, but that there is rather high mortality from adverse physical conditions and there is definite competition for sites with high humidities, with P. dunni excluding P. vehiculum. D. C R U S T A C E A Connell’s (1961) study of competition between the barnacles Chthamalus stellatus and Balanus balanoides defines both the fundamental and realized niches of these species. The center of distribution for C. stellatus is in the Mediterranean and it reaches its northern limit in the Shetland Islands. Balanus balanoides is a boreal-arctic species which reaches its southern limit in northern Spain. At Millport, Scotland where this study was done, the larvae of C. stellatus settle in the marine intertidal zone between the levels of mean high water of spring tides and the mean tide level, but few survive below the mean high water of neap tide (see Fig. 11). The larvae of B. balanoides settle throughout the range of all intertidal levels from mean low water to mean high water of spring tide, but poor survival between the mean high water of spring and neap tides restricts the adult distribution in this region. Connell showed that the upper limit of distribution of Balanus is determined by mortality from desiccation, competition for space and predation by the snail Thais lapillus, but C. stellatus can survive at all levels and increased time of submergence was not a factor in the elimination of this species at low shore levels. Thus, in view of its greater ability to withstand alternate submergence and desiccation at the higher shore levels, C. stellatus has a larger niche than B. balanoides. Intraspecies competition for space is rarely observed in Chtharnalus but is common among individuals of Balanus. Comparison of the survival of Chthamalus in the presence and absence of Balanus showed that Balanus could cause considerable mortality among the Chtha.m,alus;

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the Balanus settled in greater population densities, grew faster than Chthamalus, and direct observation showed that Balanus undercut or crushed individuals of Chthamalus and eliminated them from the area between mean tide level and the level of mean high water of neap tide (Fig. 11). Chthamalus which survived after a year of crowding by Balanus were much smaller than uncrowded individuals but even adult Chthamalus failed to survive when transplanted to low levels. BALANUS BALANOIDES

CHTHAMALUS STELLATUS

SPRING

=

L I

f

NtAl

-

0 I 2

5

MtAN 1 l D t L l V t l

I I c

3

I

s

NEAP

:

STRING

FIG.11. Distributions of adults and larvae of Balanus balanoides and Chthamalus stellatics in the marine intertidal zone (After Connell, 1961).

Similar evidence for competition in an included niche is found in competition between the crayfish Orconectes immunis and 0. virilis (R. V. Bovbjerg, personal communication). Laboratory tests have shown that both species can live in mud but prefer rock and gravel substrates when given a choice. 0. immunis is the better burrower, however, and also tolerates lower oxygen tensions than 0. virilis. Thus, ponds which are subject to summer drying, periods of low oxygen tension, and have soft mud substrates are least tolerated by the stream form, 0. virilis. Bovbjerg found large numbers of both species in oxbows after spring floods, but when the oxbows became stagnant and finally dry, the pond species 0. immunis was the only one that survived. Conversely, in spite of its demonstrated preference for rock and gravel substrates, the pond form is seldom found in streams. In one stream

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where both species do coexist, 0. virilis occupies rocks and 0. irnmunis is found on mud. More concrete evidence for interspecies competition was provided by laboratory experiments in which substrate preferences were tested with both species in the same tank. A series of contests took place in which the less aggressive individuals were evicted from the more desirable crevices between stones. The stream species, 0. virilis, eventually occupied the rocks, leaving the mud substrate to the pond species, 0. immunis. Thus, 0. virilis has a more restricted niche, by virtue of its inferior ability to burrow in mud and to tolerate low oxygen tensions, but it is the more aggressive species and survives by excluding 0. immunis.

E. I N S E C T S The ant's Messor barbarus and M . aegyptiacus are harvesters which make long processions from their nests to harvest grass seeds. Pickles (1944) studied the relationships between these two species in Algeria and found that the foraging territory of a nest of M . aegyptiacus was 2 348 yd2 (1 963 m2) with a foraging distance of 82 f t (25 m). This nest was within a larger space occupied by M . barbarus, which had a foraging territory of 7 857 yd2 (6 569 m2)and a foraging distance of 45 f t (14 m). Processions of M . aegy@iacus frequently led over the nest of the M . barbarus and beyond it, showing that the presence of M . barbarus did not deter M . aegyptiacus from foraging in this direction. On only a few occasions, however, did M . barbarus forage in the direction of the M . aegyptiacus nest, and then only a few single individuals were involved. Eventually a series of battles took place during which there was considerable damage to members of the M . barbarus population and they abandoned the old nest and constructed a new one farther away. These two species apparently eat the same foods and have very similar habit'at requirements. M . aegyptiacus can occupy areas within the foraging territories of M . barbarus because of its greater competitive ability, which in this case involves direct aggression. M . barbarus can, at the same time, survive outside the immediate foraging territory of M . aegyptiacus because M . barbarus has a greater foraging distance. This system of relationships therefore allows coexistence of both species within the same broad habitat. While it is unlikely that the niche of one species will be entirely contained within the niche of another, it is evident that the critical factors which affect the outcome of competition between two species can often be reduced to a few simple variables which do have this relationship. This would seem to be especially true for homiotherms which, because of their adaptations to climatic factors, are subject to fewer controls and are perhaps more likely to have evolved a strong

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interference element in their competitive interactions. The plains pocket gopher, Geomys bursarius, can subsist on certain grasses which will not sustain individuals of the mountain pocket gopher, Thomomys talpoides (Myers and Vaughan, 1963), so that what has been referred to as an “included niche” for G. bursarius contains elements outside the niche of T . talpoides; but both species can survive on such a wide variety of foods that it is unlikely that food is a critical factor in their habitat or geographic distribution or in competition between them (Miller, 1964a), and their aggressive, territorial behavior indicates that competition for space overrides this source of ecological differentiation. Thus the critical factors of soil depth and texture determine the suitability of such space for the different species, and therefore the outcome of competition between them. Similary, while the salamander Plethodon dunni can tolerate somewhat lower temperatures than P. vehiculum, the niche of P . dunni is included within the niche of P. vehiculum in the critical range of temperature and humidity between the preferred cool and humid conditions and the suboptimal conditions of high temperature and low humidity. Thus, the included niche is an adequate description of interspecies relationships as long as it accounts for the critical range of factors that govern competition and survival, and in this sense we should be prepared to accept reasonable approximations. It should also be emphasized, however, that we cannot assume that intersection between fundamental niches will inevitably lead t o competitive exclusion -this is an outcome which should first be demonstrated or, in the absence of direct evidence, only inferred when it is the most reasonable explanation of observed events. Given that the examples in this section are of competitive exclusion under the conditions of a n included niche in which N, is the proper subset of N, and the realized niche of 8, is the difference subset N, - N,, we can examine the properties of these interactions with respect to: (1)the characteristics of the competition process, (2) the factors which give the more specialized species S, its competitive advantage and (3) the factors which allow the less specialized species S, to survive competition from S,. I n each of the preceding examples the process of competition involved a form of interference which led to competitive exclusion within the niche space of the intersection subset, and the competition was for some kind of space or a structural feature within a given space. The space requirements of different taxonomic groups are obviously different, depending on their specific needs, and we may infer that the factors affecting the form of interference also were different or had different values, but whatever these factors and mechanisms may be they apparently lead t o comparable end results through a similar set of general conditions. O*

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The following table categorizes forms of interference and the factors which seem to be related to their effectiveness: Forms of Interference Related Factors I. Indirect 1. Chemical communication 11. Direct A. Physical Contact 1. Population growth B. Threat 2. Aggression C. Epidiectic Display 3. Territory 4. Body size 5. Coloration 6. Voice A requirement of indirect ipterference is that a signal be produced which will be effective in the owner's absence, and this will almost invariably involve some form of chemical communication. 'Wilson and Bossert (1964), as mentioned earlier, have surveyed this topic, mostly with respect to intraspecies relationships, but there is a need for research on how chemical signals are transmitted between species and how effective they are. Regardless of whether a chemical is produced to act specifically as a signal, or whether such chemicals as metabolic wastes inadvertently condition the environment, the effect in either case may be indirect interference with access to parts of the environment or the resources it contains. The simplest form of direct interference in the preceding examples was the physical destruction of Chthumalus stellatus by populations of Balanus balanoides. This was due to the greater rate of growth of the Balanus populations, greater tolerance of crowding and, eventually, the reduced size and efficiency of the crowded Chthumalus. Competitive superiority of the ant Messor aegyptiacus was also due to direct physical aggression and a relatively primitive form of territoriality. The chipmunks Eutamias amoenus and E . minimus showed a kind of interference intermediate between physical combat and threat. Chases resulted in the establishment of dominance of E . amoenus, but with no apparent physical harm to either animal. The larger titmouse Parus inornatus is the more successful aggressor in competition with the chickadee, P. rufescens (Dixon, 1954), and the red-headed woodpecker (Melanerpes erythrocephalus) excludes the smaller downy woodpecker (Dendrocopus pubescens) from desired nest holes (Schwab and Monnie, 1959). I n competition between the hummingbirds Calypte anna and Selasphorus sasin (Legg and Pitelka, 1956), the former exercises dominance by earlier breeding and territory occupation, more effective flight displays and larger body size (see also Hartley, 1950; Marler, 1956). If the process of interference consists of direct or overt aggression, body size would seem logically to be advantageofis, and this hypothesis is supported by

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numerous examples among competing species of vertebrates. Additional evidence is found in the fact that character displacement in the direction of greater difference in body size is pronounced in zones of overlap between closely related and presumably competing species (Brown and Wilson, 1956; Hutchinson, 1959). We may conclude that larger animals tend generally to be more aggressive and more successful in competition, although N. Tinbergen has pointed out in personal conversation that the universal tendency of animals to avoid aggressive encounters may be as important, or more so, in maintaining dispersion of individuals and species (see also Ripley, 1961). Klopfer (1962) also emphasizes that smaller size may have adaptive value in allowing the subordinate animd to escape the effects of competition and survive, as suggested by Kennerly (1959) to account for size difference between Geomys bursarius and G . personatus. The smaller titmouse, Parus caeruleus, can feed from the extremities of twigs that cannot be reached by its larger competitor, P . major (Snow, 1949), and (Klopfer, 1962) the shorter-billed downy woodpecker (D. pubescens) can deal with smaller branches than the more heavily-weaponed hairy woodpecker (D.villosus). I n fact, in the examples given for species pairs in included niches there was generally an inverse relation between body size and niche size, suggesting that ( 1 ) larger body size may confer competitive advantage but (2) animals with smaller body size are adapted to a wider range of ecological conditions and are better able to survive outside preferred habitats, often on smaller food particles. Miller (1964a) postulated a correlation between body size, Competitive ability or aggression, and territory size, assuming that a larger body. size would enable an animal to sustain its aggressive drive or to display over a greater area, thereby restricting the movements of its smallei competitors to smaller and perhaps less favorable areas. Unfortunately, territory is highly variable and difficult to measure. Territory size depends on topography and local habitat conditions (Beer et al., 1966), and accurate data relating territory to competitive ability are seldom available. What little information does exist shows that in some cases the animal with the larger territory is the superior competitor, while in others the opposite relationship exists. The crimson-crowned bishop (Euplectes hordeacea) has a relatively large territory which is not much affected by the abundance of breeding males, whereas its cogener the Zanzibar bishop (E. nigroventris) has a smaller territory which is highly compressible, according to population density (Moreau and Moreau, 1938). E. nigroventris occupies less favorable habitats and its smallest territories are often those with the most obvious digadvantages of lack of food and orowding by other species. Colonies of the tri-colored blackbird (Agehius tricolor) do not have territories (Orians, 1961) and are also

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interspersed in apparently less favorable nesting sites than those occupied by the territorial red-winged blackbird ( A .phoeniceus). Moore (1964) measured the steady densities of the territorial males of 15 species of dragonfly in comparable habitats and found that territory size, as reflected in density, was correlated with the size of the species. On the other hand, Pickles (1944) found an opposite relationship between territory and foraging distance and competitive ability in the ants Messor barbarus and M . aegyptiacus. Gibb (1956) states, “Specific differences in size of territory have never yet been satisfactorily explained in terms of any particular biological requirement”, and we must conclude at this stage that if territory size is significant in competitive interactions between species it does not have a value which is consistent for different taxonomic groups. I n the absence of interspecies competition the fundamental niche of each species will eventually be fully occupied as a result of the pressures of intraspecies population growth, with the more desirable parts of the niche space occupied by the stronger individuals of the population. In the case of an included niche, for example, intraspecies and interspecies population pressures will tend to oppose each other in the manner shown in Fig. 12. The most preferred space of the two fundamental

Case 1

FIQ.12. Forces of population pressure within and between species in their realized niches N, and N,.

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niches is in the region of the values x, and yl,and this space will be occupied by the strongest individuals of species S,, with pressure on other individuals of this species forcing them toward the less desirable regions of N,. Although S , may be forced by competitive exclusion to live in the niche space N, - N,, there will be pressure from within its own population to expand into the preferred space of N, as well as toward the region of lowest survival at the periphery of N, (Xg,y6). Presumably, according to this hypothesis, the weakest individuals of 8,will be most directly in competition with the strongest individuals of S,. Depending on the strength and effectiveness of interference from S,, the region of immediate exclusion may exist as a “tension zone” where the niche distributions are not clearly delineated. This may explain distributions of Planaria naontenegrina and P . gonocephala when they occur together in the same stream, as compared with the temperature tolerances they express when they live in separate streams. Rather than a clear separation of niches at the extreme limit of tolerance of P . motenegrina (16 to 17”C), population pressure from P . gonocephula shifts the point of demarkation in their realized niches to approximately 13 to 14°C. This problem, while vaguely defined at present, may have considerable bearing on the evolution of ecological differentiation and of ecological and ethological isolating mechanisms.

VII. SPECIES DIVERSITY Klopfer (1962) suggests the following ways in which it is hypothetically possible to increase the number of species in a fixed area: (1) by increasing the amount of time during which speciation can occur, (2) by increasing the “space” within which niches can be provided for different species, and (3) by reducing the size of niche required by each species. Niche size in this sense is the measurable range of conditions which determine the presence or absence of a species. Klopfer and MacArthur (1960) conclude that the increased faunal diversity of the tropics is a result of the time available for speciation and smaller niche sizes. One might also add that the other factor (2) of space is also important, in that the structural diversity of tropical habitats provides a greater amount of niche space in a given area. Klopfer (1962) carries this line of reasoning further to state that a reduction in the volume of the niche of a species also implies that the behavior of the animal has become stereotyped, as reducing the niche size also reduces the range of objects in the environment (or environmental variables) to which the animal responds by feeding, nesting, or taking shelter. Hence, if niche size is relatively large there is a wider range of behavior and a given area will support fewer of such species. Support for this argument is found in the relative abundance of passerine birds in temperate

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regions. Klopfer maintains that passerines have a wider behavior range than non-passerines and are therefore capable of occupying a greater range and less stable set of conditions, and that this is the reason that members of this group are relatively more common in temperate habitats. Simpson (1964) analysed the species density of mammals in terms of the number of species in areas of North America and found two major trends: the most dominant trend is an increase in number of species from north to south, with a lesser trend toward increase in species with altitude. He decided that niche size is not an important contributing factor, although no particular reason was given for this conclusion. Van Allen (1965) analysed morphological variation in six species of birds in relation to niche size. The niches of these species are known to be broader on some islands than on the mainland and in each case there is also greater variation in bill measurements in the island birds, with the exception of one species in which the niche on the Canary Islands is known to be smaller than on the mainland. Van Allen concludes that niches on the zoogeographic mainland are relatively tightly packed together by the action of stabilizing selection imposed, presumably through competition, by ecologically adjacent species. On the islands the available environment is partitioned into wider niches with weaker stabilizing selection. Thus, the wider niches on the mainland would permit greater phenotypic variation if phenotype is controlled to a significant extent by the adaptive diversity of the niche (Van Allen, 1964). I n examples of included niches, in which the niche size of the included species is smaller by definition, there is a corresponding trend toward greater specialization. This is especially evident among pocket gophers in which Geomys bursarius, the species with the smallest niche, is the most highly evolved in fossorial behavior and morphology (Miller, 1964a). It has also been noted that in these and other species in which interference probably takes the form of overt aggression or threat, there is a trend toward greater body size. It would be interesting to compare examples of this sort with the exceptions that are known to exist (e.g. burrowing rodents) to Bergmann’s Rule. As the realized niche of an animal is the phenotypic expression of its responses to both its biotic and physical environments, specialization for competition may to some extent explain exceptions t o rules based on physical factors. It is also interesting to note that, while the fossorial development of Geomys bursarius may make it more efficient in sandy soils, this specialization apparently makes it less well adapted than less specialized forms (e.g. Thomomys talpoides) to a wide range of soil types. Caution must be used, however, in forming generalizations about the

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causes and especially the mechanisms of species interactions. Attempts to derive general theories of population control have been seriously hampered by the indiscriminate application of results from studies of one taxonomic group t o observations of relationships in another, and the same can be said of competition theory. There is no reason to assume that all animals respond in the same way to the same factors and are, therefore, subject to the same laws of population growth or competition. Gammarus duebeni has a large amplitude with respect to abiotic factors but low productivity, while its competitors G. salinus and G. zaddachi have high productivities, faster development rates, higher growth rates and higher reproductive potentials within a narrower range of conditions (Kinne, 1954). On the basis of research with these and other marine organisms Kinne (1956) suggests that animals with a narrow range of tolerance to abiotic factors tend to have a high biotic potential. However, it would obviously be a mistake to assume that a high replacement rate is a universal criterion of biological success. I n species with ill-defined space requirements, competing mainly through exploitation rather than interference, replacement rate may have high value; but in species with strong interference elements in their competitive relationships and rather rigid dispersion mechanisms, it may be more advantageous to have a relatively low replacement rate and greater population stability. I n other words, animals living in restricted niches may be successful in maintaining their populations either through high biotic potential and exploitation or by competitive interference. This article suggests a t least two major sources of species diversity. When competition is primarily through exploitation and the system is under strong environmental control, it is likely that fluctuations in factors affecting reproduction and survival will continually alter the outcome of the competitive interaction, allowing coexistence of mixedspecies populations. If there is no interference, the more similar the species the more likely that their interaction values will be equal and correspondingly less environmental change will be required in order to allow coexistence. If there is a strong element of interference resulting in competitive exclusion, species diversity may still be increased if one of the species becomes specialized and, in so doing, reduces its niche size in such a way that both species are able to exist in the same biotope, e.g. when the more specialized competitor occupies an included niche which is small enough to allow the other species to survive in the difference subset of their niches. -4s noted earlier, coexistence is a, relative term depending on the size of area one chooses to measure. If there is a strong element of interference and the critical habitat features are uniformly distributed, competitive exclusion may operate over

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geographic distances, as it does with pocket gophers which can only be said to coexist within relatively large areas or at the point of disjunction between soil types. If, however, the competitors occupy small territories and the habitat is suitably diverse, coexistence may be possible within relatively small areas of habitat. Thus the area of minimum coexistence is proportional to the area of interference and varies inversely with habitat diversity -in the last analysis no two individuals or species can occupy precisely the same point and a t this extreme cannot coexist. The possible parallels between mechanisms of population control and of competitive interactions have received very little attention. Just as it is impossible to account for natural control of all populations with one general theory based on stress, food or climate, we cannot expect) that the mechanisms of interference or exploitation will be the same in every animal population. It would be interesting to know whether species whose numbers tend to be controlled by climate also, as was suggested earlier, tend to have weak interference elements and compete mainly through exploitation; or, conversely, whether a strong interference component also suggests intraspecies control based on similar mechanisms. Another parallel may also exist between different kinds of isolating mechanisms and forms of interference. We know, for example, that birds have evolved strong ethological isolating mechanisms based on auditory and visual stimuli (Sibley, 1961), which also seem to be important factors in territorial behavior and competitor interactions. It would appear that the mechanisms which function in reproductive isolation may be used also as interference mechanisms, and that in each case there is a common evolutionary history. I n certain fishes, on the other hand, ethological mechanisms are poorly developed and species isolation depends more on physical factors in the habitat. The breakdown of isolation and subsequent hybridization occurs rather frequently in these species - does this also mean that interspecies interference is uncommon in such groups? Many insects (e.g. Drosophila) have evolved pre-mating, ethological mechanisms of isolation but also seem to depend on successive post-mating mechanisms for complete reproductive isolation (Mayr, 1963). Species recognition in these animals depends entirely on the adults, which suggests that this is the only stage during which ethological interference mechanisms would be effective, but if species recognition is relatively weak, interspecies interference might also be weak even among adults. There is, in other words, a possible parallel between mechanisms of population control, interspecies competition and species isolation, all of which influence the species diversity of natural communities.

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REFERENCES Andrewartha, H. G. and Birch, L. C. (1953). Aust. J . 2001.1, 174-177. The Lotka-Volterra theory of interspecific competition. Andrewartha, H. G. and Birch, L. C. (1954). “The Distribution and Abundance of Animals,” 782 pp. Chicago: University of Chicago Press. Bagenal, T. B. (1951). J . Anim. Ecol. 20, 242-245. A note on the papers of Elton and Williams on the generic relations of species in small ecological communities. Bakker, K. (1961). “An Analysis of Factors which Determine Success in Competition for Food among Larvae of Drosophila melanogaster,” 281 pp. Groningen: J. B. Wolters. Beauchamp, R. S. A. and Ullyott, P. (1932). J . Ecol. 20, 200-208. Competitive relationships between certain species of fresh-water triclads. Beer, J. R., Frenzel, L. D. and Hansen, N. (1956). WiLon Bull. 68, 200-209. Minimum space requirements of some nesting passerine birds. Birch, L. C. (1945). Austral. J . Exp. Biol.a i d Med. Sci. 23, 29-35. The influence of temperature on the development of the different stages of Calandra oryzae L. and Rhizopertha dominim Fab. (Coleoptera). Birch, L. C. (1948). J . Anim. Ecol. 17, 15-26. The intrinsic rate of natural increase of an insect population. Birch, L. C. (1953). Ecology 34, 698-711. Experimental background to the study of the distribution and abundance of insects. I. The influence of temperature, moisture and food on the innate capacity of increase of three grain beetles. Birch, L. C. (1957). Amer. Nut. 91, 5-18. The meanings of competition. Birch, L. C. and Battaglia, B. (1957). Ecology 38, 165-166. The abundance of Drosophilu willistoni in relation to food in natural populations. Bray, J. R. (1958). Ecology 39, 770-776. Notes toward an ecologic theory. Brian, M. V. (1056). J . Anim. Ecol. 25, 339-347. Exploitation and interference in interspecies competition. Brown, W. L., Jr. and Wilson, E. 0. (1956). Syst. 2001.5, 49-64. Character displacement. Burkholder, P. R. (1952). Amer. Sci. 40, 601-631. Cooperation and conflict among primitive organisms. Carson, H. L. and Stalker, H. D. (1951). Ecology 32, 317-330. Natural breeding sites for some wild species of Drosophila in the eastern United States. Chiang, H. C. and Hodson, A. C. (1950). Ecol. Monogr. 20, 175-206. An analytical study of population growth in Drosophila melunogaster. Clements, F. E. and Shelford, V. E. (1939). “Bio-ecology,” 425 pp. New York: John Wiley and Sons. Cole, L. C. (1960). Science 132, 348-349. Competitive exclusion. Connell, J. H. (1961). Ecology 42, 710-723. The influence of interspecific competition and other factors on the distribution of the barnacle Chtlmmalus atellatus. Crombie, A. C. (1947). J . Anim. Ecol. 16, 44-73. Interspecific competition. Darwin, C. (1859). “On the Origin of Speciss by means of Natural Selection, or the Preservation of Favoured Races in the Struggle for Life.” London: John Murray. Dice, L. R. (1952). “Natural Communities”, 547 pp. Ann Arbor: University of Michigan Press.

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Dixon, K. L. (1954). Condor 56, 113-124. Some ecological relations of Chickadees and Titmice in Central California. Dumas, P. C. (1956). Ecology 37, 484-495. The ecological relations of sympatry in Plethodon dun& and Plethodon vehiculum. Ecke, D. H. (1954). J . Mammal. 35, 521-525. An invasion of Norway rats in southwest Georgia. Elton, C. (1927). “Animal Ecology”, 209 pp. London: Sidgwick and Jackson. Elton, C. (1935). J . Anim. Ecol. 4, 127-136. A reconnaissance of woodland bird communities in Englmd and Wales. Elton, C. (1946). J . Anim. Ecol. 15, 54-68. Competition and the structure of ecological communities. Elton, C. (1958). “The Ecology of Invasions by Plants and Animals”, 181 pp. London: Methuen and Co. Elton, C. and Miller, R. S. (1954). J . Ecol. 42, 46CL496. The ecological survey of animal communities: with a practical system of classifying habitats by structural characters. Evans, F. C. (1942). J . Anim. Ecol. 11, 182-197. Studies of a small mammal population in Bagley Wood, Berkshire. Frank, P. W. (1952). Physiol. Zool.25,178-204. A laboratory study of intraspecies and interspecies competition in Daphnia pulicaria (Forbes) and Simocephalw vetulus 0. F. Muller. Gause, G. F. (1935). “La thdorie mathdmatique de la liitte pour la vie”, 61 pp. Paris: Hermann et Cie. Gause, G. F. and Witt, A. A. (1935). Amer. Nut. 69, 59&609. Behavior of mixed populations and the problem of natural selection. Gibb, J. (1956). Ibis 98, 420-429. Territory in the genus P a m . Gilbert, O., Reynoldson, T. B. and Hobart, J. (1952). J . Anim. Ecol. 21, 310-312. Gause’s hypothesis; an examination. Gordon, C. (1942). Nature 149, 610. Natural breeding sites of Drosophila obscura. Greenway, J. C. Jr. (1958). Amer. Comm. for International Wildlife Protection, Spec. Publ. N o . 13. Extinct and Vanishing Birds of the World. Grinnell, J. (1917a). Amer. Nut. 51, 115-128. Field tests of theories concerning distributional control. Grinnell, J . (1917b). Auk 34, 427-433. The niche-relationships of the California thrasher. Grinnell, J. (1924). Ecology 5, 225-229. Geography and evolution. Grinnell, J. (1928). Univ. Calif. Chron. Oct. 1928. pp. 429-450. Presence and absence of animals. Grodzinski, W. (1959). Ekologia Polska 7, 83-143. The succession of small mammals communities on an overgrown clearing and landslip mountain in the Beskid Sredni (western Carpathians). Hall, E. R. and Kelson, K. R. (1959). “The Mammals of North America”, Vol. I. 546 pp. New York: Ronald Press. Hardin, G. (1960). Science 131, 1292-1297. The competitive exclusion principle. Harrison, J. 0. (1964). Ecology 45, 508-519. Factors affecting the abundance of Lepidoptera in banana plantations. Hartley, P. H. T. (1949). Ibis 9, 393-413. The biology of the mourning chat in winter quarters. Hartley, P. H. T. (1950). Symp. SOC. E z p . Biol. No. 4, pp. 313-336. An experimental analysis of interspecific recognition.

PATTERN AND PROCESS IN COMPETITION

71

Heatwole, H. and Davis, D. M. (1965).Ecology 46, 140-150. Ecology of three sympatric species of parasitic insects of the genus Megurhyssa (Hymenoptera: Ichneumonidae). Hinde,R.A. (1956).Ibis98,340-369.Thebiologicalsignificanceofterritoriesofbirds. Hutchinson, G.E. (1944).Ecology 25, 3-26. Limnological studies in Connecticut. VII. A critical examination of the supposed relationship between phytoplankton periodicity and chemical changes in lake waters. Hutchinson, G. E. (1948).Ann. N . Y . Acad. Sci. 50, 221-246. Circular causal systems in ecology. Hutchinson, 0. E. (1957). Cold Spr. Harb. Symp. quant. Biol. 22, 415-427. Concluding remarks. Hutchinson, G. E. (1959).Amer. Nut. 93, 145-159. Homage to Santa Rosalia, or why are there so many kinds of animals? Hutchinson, G. E. and Deevey, E. S. (1949). “Survey of Biological Progress. Vol. I”, 325 pp. New York: Academic Press. Kennerly, T. J. Jr. (1954).T e z w J . Sci. 6 , 297-329. Local differentiation in the pocket gopher (Geomys personatus) in soiithern Texas. Kennerly, T. J. Jr. (1959).Evolution 13, 247-263. Contact between the ranges of two allopatric species of pocket gophera. Kikkawa, J. (1964).J. Anim. Ecol. 33, 259-299. Movement, activity and distribution of the small rodents Clethrionomys glareolus and Apodemus sylvaticus in woodland. Kinne, 0. (1954).Interspezifische Sterilpaarung als konkurrenzoligischer Faktor bei Gammariden (Crustacea, Peracarida). Sonderbook aus die Naturwissenechaften 41, 434. Kinne, 0.(1956).tfber den Wert kombinierter Untersuchungen (im Biotop und im Zuchtersuch) fur die okologisehe Analyse. Sonderbook aus die Naturwissenschaften 43, 8-9. Klopfer, P. M. (1962).“Behavioral Aspects of Ecology”, 161 pp. Englewood Cliffs, New Jersey: Prentice-Hall. Klopfer, P. M. and MacArthur, R. H. (1960).Amer. Nut. 94, 293-300. Niche size and faunal diversity. Kohn, A. J. (1959).Ecol. Mongr. 29, 47--90.The ecology of Conus in Hawaii. Kohn, A. J. and Orians, G. H.(1962).System 2001.11, 119-126. Ecological data in the classification of closely related species. SOC. 2001. Bot. Fen. Vannma 13, 1-91. Kontkanen, P. (1950).A n n . (2001.) Quantitative and seasonal studies on the leafhopper fauna of the field stratum in open areas in North Karelia. Kostitzin, V. A. (1939).“Symhiose, parasitisme et evolution (Etude mathematique) Actualit& Scientifiques”. Paris: Hermann. Lack, D. (1944).Ibis 86, 260-286. Ecological aspects of species-formation in passerine birds. Lack, D. (1954).“The Natural Regulation of Animal Numbers”, 343 pp. Oxford: Clarendon Press. Lanyon, W. E. (1956).Ibis 98, 485489. Territory in the meadowlarks, genus Sturnella. Legg, K. and Pitelka, F. A. (1956).Condor 58, 393-405. Ecologic overlap of Allen and Anna Hummingbirds nesting a t Santa Cruz, California. Lotka, A. J. (1932).J . Wash. Acad. Sci. 22, 461-469, The growth of mixed populations, two species competing for a common food supply. MacArthur, R.H. (1957).Proc. iNat. Acad. Sci., U.S. 43, 293-295. On the relative abundance of bird species.

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MacArthur, R. H. (1958). Ecology 39, 599-619. Population ecology of some warblers of northeastern coniferous forests. MacArthur, R. H. and MacArthur, J. W. (1961). Ecology 42, 594-598. On bird species diversity. Marler, P. (1956). Ibis 98, 496-501. Territory and individual distance in the Chaffinch Fringilla coelebs. Marshall, J. T. Jr. (1948). Condor 50, 233-256. Ecologic races of song sparrows in the San Francisco Bay region. Part 11. Geographic variation. Matheson, C. (1939). J . Anim. Ecol. 8, 76-93. A survey of the status of Rattus rattus and its subspecies in the seaports of Great Britain and Ireland. M a p , E. (1963). “Animal Species and Evolution”, 797 pp. Cambridge: Belknap Press of Harvard University Press. Merrell, D. J. (1951). Amer. Nut. 85, 159-169. Interspecific competition between Drosophila funebris and Drosophila melanogaster. Miller, R. S. (1955). Proc. 2001. Soc., Lond. 125,505-519. Activity rhythms of the wood mouse, Apodemus sylvaticus, and the bank vole, Clethrionomys glareolus. Miller, R. S . (1964a). Ecology 45, 256-272. Ecology and distribution of pocket gophers (Geomyidae) in Colorado. Miller, R. S. (1964b). Ecology 45, 132-148. Larval competition in Drosophila melanogaster and D . simulans. Miller, R. S. (1964~).Amer. Nut. 98, 221-238. Interspecies competition in laboratory populations of Drosophila melanogaster and Drosophila simulans. Milne, A. (1961). Symp. Ezp. Biol. No. 15. pp. 40-61. Definition of competition among animals. Mishima, J. (1964). Sci. Rep., Tokyo Kyoiku Daigaku 11, 277-301. The influence of environmental temperature upon the interspecific competition in Drosophila larvae. Mitchell, R. (1964). Ecology 45, 546-558. A study of sympatry in the water mite genus Arrenurius. Moore, J. A. (1952). Evolution 6, 407-420. Competition between Drosophila melanogaster and Drosophila simulans. I. Population cage experiments. Moore, N. W. (1964). J . Anim. Ecol. 33,49-71. Intra- and interspecific competition among dragonflies (Odonata). Moreau, R. E. (1948). J . Anim. Ecol. 17, 113-126. Ecological isolation in a rich tropical avifauna. Moreau, R. E. and Moreau, W. M. (1938). J . Anim. Ecol. 7,314-327. The comparative breeding ecology of two species of Euplectea (Bishop Birds) in Usambara. Myers, G. T. and Vaughan, T. A. (1963). Colorado Cooperdive Pocket Gopher Project Annual Progress Report, January, 1963. Food habits of the plains pocket gopher in Eastern Colorado. Nero, R. W. (1964). Wilson Bull 75,376-413. Comparative behavior of the yellowheaded blackbird, red-winged blackbird and other icterids. Neyman, J., Park, T. and Scott, E. L. (1958). Gen. Systems 3, 152-179. Struggle for existence; the Tribolium model: biological and statistical aspects. Nicholson, A. J. (1933). J . Anim. Ecol. 2, 132-178. The balance of animal populations. Nicholson, A. J. (1937). J . Council Sci. Ind. Res. (Australia)10, 101-106. The role of competition in determining animal populations. Nicholson, A. J. (1955). Austral. Jour. 2001.2, 9-65. An outline of the dynamics of animal populations. Odum, E . P. (1959). “Fundamentals of Ecology”, 546 pp. Philadelphia and London: W. B. Saunders Co.

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73

Oriam, G. H. (1961). Ecol. Monogr. 31, 285-312. The ecology of blackbird ( A g e h i u s ) social systems. Park, T. (1948). Ecol. Monogr. 18, 265-308. Experimental studies of interspecies competition. I. Competition between populations of the flour beetles, Tribolium c o n j m m Duval and Tribolium cmtaneum Herbst. Park, T. (1954). Physiol. 2001.27, 177-238. Experimental studies of interspecies competition. 11. Temperature, humidity, and competition in two species of Tribolium. Pickles, W. (1944). J . Anim. Ecol. 13, 128-129. Territories and interrelations of two ants of the genus Measor in Algeria. Pratt, D. M. (1944). Biol. Bull. 85, 116-140. Analysis of population development in Daphnia at different temperatures. Ripley, S. D. (1961). A u k 78, 366-371. Aggressive neglect as a factor in interspecific competition in birds. Robertson, F. W. (1960). Genet. Re.?. Camb. 1, 288-304. The ecological genetics of growth in Drosophila. I. Body size and developmontal time on different diets. Lond. B., 132: 258-277. Robertson, F. W. and Sang, J. H. (1944). Proc. Roy. SOC. The ecological determinants of population growth in a Drosophila culture. I. Fecundity of adult flies. Sang, J. H. (1949). Physiol. 2001.22, 183-202. The ecological determinants of population growth in a Drosophila culture. 111. Larval and pupal survival. Sang, J. H. (1950). Bwl. Rev. Cambridge Phil. SOC.25, 188-219. Population growth in Drosophila cultures. Schwab, R. G. and Monnie, J. B. (1959). Wilson Bull. 71, 190. Strife over a nesting site between Downy and Redheaded Woodpeckers. Sheppard, D. H. (1964). “Ecology ofthe chipmunks Eutamias a m e n u s luteiventris (Allen) and E . minimus orocetea Merriam”. Ph.D. Thesis, University of Saskatchewan, 1964. Unpublished. Sibley, C. G. (1961). I n “Vertebrate Speciation” (W. F. Blair, ed.), pp. 69-88. Austin: University of Texas Press. Simmons,K. E. L. (1951). Ibis 92, 407-413. Interspecific territorialism. Simmons,K. E. L. (1956). Ibis 98, 390-397. Territory in the Little Ringed Plover, Charadrius dubiua. Simpson, G. G. (1964). System. Zool. 13,57-73. Species density of North American recent mammals. Slobodkin, L. B. (1954). Ecol. Monogr. 24,69-88. Population dynamics in Daphnia obtwa Kurz. Slobodkin, L. B. (1961). “Growth and Regulation of Animal Populations”, 184 pp. New York: Holt, Rinehart and Winston. Sluiters, J. E. (1954). Limosa 27, 71-86. Waarnemingen over de brie bij Amsterdam broedende pluviersoorten (Leucopolius a. alexandrinus, Charadriua dubius curonicus en Ch. h. hiaticula). Snow, D. W. (1949). Var Fagelwadd 8, 156-169. Jamforande studier over vara mesarters naringssokande. Snow, D. W. (1954). Ibis 96, 565-585. The habitats of Eurasian tits (Parus spp.). Snow, D. W. (1956). Ibis 98, 438-447. Territory in the blackbird Turdus nteruh. Sokoloff, A. (1955). Ecol. Monogr. 25, 387-409. Competition between sibling species of the Pseudoobscura group of Drosophila. Sokoloff, A. (1957). Cold Spr. Harb. Symp. qwznt. Biol. 22, 268-270. Discussion following paper by A. Milne: Theories of natural control of insect populations.

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Solomon, M. E. (1949). J . Anim. Ecol. 18, 1-35. The natural control of animal populations. Southern, H. N. (ed.) (1964). “The Handbook of British Mammals”, 465 pp. Oxford: Blackwell Scientific Publications. Tinbergen, N. (1956). Ibis 98, 401-411. On the functions of territory in gulls. Townes, H. and Townes, M. (1960). U.S. Nut. Mus. Bull. 216, 1-676. Ichneumonflies of America north of Mexico. 2. Subfamilies Ephialtinae, Xoridinae Acaenitinae. Udvardy, M. F. D. (1952). Oikos 3. 98-123. The significance of interspecific competition in bird life. TJdvardy, M. F. D. (1959). Ecology 40, 725-728. Notes on the ecological concepts of habitat, biotope and niche. Ullyett, G. C. (1950). Phil. Trans. B : Biol. Sci. 234, 77-174. Competition for food and allied phenomena in sheep-blowfly populations. Van Allen, L. (1965). Amer. Nut. 99, 377-390. Morphological variation and width of ecological niche. Vaurie, C. (1951). Proc. X Int. O m . Congr. pp. 163-166. Adaptive differences between two sympatric species of nuthatches (Sittu). Volterra, V. (1926). Mem. R . Accad. Lincei ser. 6, 1-36. Vartatzioni e fluttuazioni del numero d’individui in specie animali conviventi. Von Haartman, L. (1956). Ibis 98, 460-475. Territory in the pied flycatcher Mwcicapa hypoleuca. Weatherly, A. H. (1963). Nature, Lond. 197, 1 P 1 7 . Notions of niche and competition among animals, with special reference to freshwater fish. Williams, C. B. (1947). J . Anim. Ecol. 17, 11-18. The generic relations of species in small ecological communities. Williams, C. B. (1951). J . Anim. Ecol. 20, 24G253. Intraggeneric competition aa illustrated by Moreau’s records of East African bird communities. Williams, C. B. (1964). “Patterns in the Balance of Nature”, 324 pp. London and New York: Academic Press. Wilson, E. 0. and Bossert, W. H. (1964). Recent Progress 19, 673-716. Chomicel communication among animals. Windsor, C. P. (1934). ColdSpr. Harb.Symp.q m n t . Biol. 2,181-187. Mathematical analysis of the growth of mixed populations. Wynne-Edwards, V. C. (1962). “Animal Dispersion in Relation to Social Beheviour”, 653 pp. Edinburgh and London: Oliver and Boyd.

A Synopsis of the Pesticide Problem

. .

N W MOORE

Monks Wood Experimental Station. Abbots Ripton. Huntiqdon. England

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I Introduction ........................................................

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A Definitions ...................................................... B. The Study of Pesticides as an Ecological Problem .................... I1. The Nature of the Pesticide Problem and the Types of Research Necessary for Studying It .................................................... 111 Pesticides as a n Ecological Factor: Its Development and Present Magnitude IV The Main Characteristics of Pesticides as an Ecological Factor ............ A Common Characteristics ........................................... B Toxicity ......................................................... C. Persistence and Solubility ......................................... D Interaction of Pesticides ........................................... V Ecological Effects on Single Species.................................... A Introduction ..................................................... B. Toxic Effect on a Species - Direct Effects ........................... C Toxic Effect on a Species-Delayed Effects ......................... D Reduction of Food Species......................................... E . Reduction of Habitat ............................................. F Removal of a Competitor ......................................... G Removalofa Predator ............................................ VI . Effects on Ecosystems ............................................... A Introduction ..................................................... B Effects onDiversity.............................................. C Effects on Production ............................................ D Effects on Succession ............................................. VII . Pesticides and Evolution ............................................. VIII Application of an Ecological Approach to Pesticides ..................... A Control of Pests and Pesticides ..................................... B. Pesticides as Tools for Ecological Research IX Conclusions on Pesticide Effects ....................................... A Comparisons With Other Factors ................................... B Pesticides as Part of a Developing System ........................... X Summary ........................................................... Acknowledgments......................................................... References...............................................................

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80 85 88 88 91 97 104 104 104 105 106 107 108 108 110 110 110 111 114 116 116 117 117 121 121 121 122 125 125 126

I . INTRODUCTION A . DEFINITIONS

This review is about pesticides and ecology.Both terms need defining. The term pesticide. as employed here. means any chemical agent used 76

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to kill any living organism which is free-living or has a free-living stage in its life history. The term ecology raises important questions of methodology. One branch of ecology deals with the relationship between individual organisms and t,heir physical environment. Population ecology on the other hand is the study of groups of individuals rather than of separate organisms. I take the view that there is a fundamental difference between these two types of ecology. The h s t is an adjunct of other disciplines, e.g. of physiology, but population ecology is a scientific discipline in its own right. Unfortunately the terms autecology and synecology do not coincide completely with the two divisions of the subject; for population ecology includes the population aspects of autecology, as well as the synecological subjects of population ecology of groups of species, of community ecology and ecosystem ecology. Accordingly the term population ecology is used throughout the paper when reference is made to the study of groups of organisms, and the term ecology is retained as a general inclusive term, covering all relationships between organisms and their environment. I should state briefly my personal views on population control since they underlie some of the arguments in this paper but are not discussed in it. I believe a useful distinction can be made between density-independent and density-dependent factors (Howard and Fiske, 191 1, etc.). Experimental evidence is lacking to show which type of factor usually controls animal populations. Density-independent factors operate continuously and one or more of them may keep a population at a relatively low level for a long period of time, but in the long run it seems unlikely that they could produce the stability in populations which is observed in nature. Therefore I favour the thesis that ultimately populations are controlled by those factors in the total complex which are densitydependent. I believe that behaviour mechanisms control population density more often than is usually supposed.

B.

THE S T U D Y O F PESTICIDES AS AN ECOLOGICAL PROBLEM

The widescale use of chemicals to control plants and animals is a recent development: within the space of about twenty years a new type of ecological factor has come into prominence, which is likely to affect all the ecosystems of the world. The situation is potentially of extraordinary interest to biologists. Yet, while great interest has been shown in the use and abuse of pesticides, the fundamental and theoretical aspects of the problem have been given less attention. It is possible t o guess some of the reasons. The chemical revolution of agriculture has developed gradually from small beginnings and there has been no particular moment when it could be said that a qualitative difference in

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the situation had arisen. The new ecological factor may be ignored because it is technological. The medieval notion that man exists “outside” nature still survives; its unfortunate corollary is that manmade factors like pesticides are considered to be unsuitable subjects for fundamental study. The pesticide problem is essentially about population ecology, and the principal difficulties of pest control and the control of pesticides result from the lack of fundamental ecological knowledge. It is, therefore, particularly unfortunate that it has received relatively little notice from ecologists. On the other hand the general public has not been slow to grasp the s i m c a n c e of pesticides; it has taken an almost obsessional interest in the subject. Few technical problems have received so much attention in the press and elsewhere. One of the reasons for this state of affairs is simple; there is the fear of being poisoned. Others are more complex and deserve objective study. There is a widespread fear of too rapid technological advance and change in the environment. It appears that the killing of wildlife by pesticides has become symbolic of the modern predicament and as a result pesticides appear to have become a whipping boy for all modern changes. Public interest in the subject may have had the effect of frightening away some scientists in the same way that popular interest in certain taxa, notably birds and Lepidoptera, at one time reduced the amount of scientific work done on these groups which otherwise are particularly suitable for investigation. Despite the lack of theoretical interest a great deal has been published on pesticides, mainly by those concerned with crop protection and by those concerned with the harmful side effects to man, domestic animals and wildlife. Chemical firms are concerned primarily with making profits from the sale of pesticides, therefore most of their scientific resources go towards the discovery of new pesticides and towards testing them for short-term efficiency and safety. The emphasis in biological work is on field trials to discover the effects of new pesticides on pest species and on toxicological studies on laboratory animals to discover hazards to man and domestic animals. Very little of the work of chemical firms producing pesticides is ecological. Government agricultural research reinforces the work of the firms and extends it to cover some ecological aspects, but again the emphasis is on the immediate effects of chemicals on the pests and so there is relatively little work on population ecology. I n recent years concern with the side-effects of pesticides on wildlife species has led to numerous studies on this subject by both Government and private organizations, mainly in the U.S.A. and Great Britain. We have to conclude that most work on the effects of pesticides on living organisms does not progress further than toxicology or the field

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trial. The ecological aspects of the problem have been studied mainly by those working for agricultural advisory organizations and for conservation organizations. The former have been concerned largely with arthropods, the latter with vertebrates. Therefore we have a situation in which there are links between scientific discipline, taxonomic groups and organization; toxicological effects on vertebrates - chemical firms effects on arthropods in the field chemical firms and agricultural advisory organizations effects on vertebrates in the field - conservation organizations. Both specialization and group interest has helped to prevent a unified approach to the subject of pesticide effects. Pesticide research involves chemistry, biochemistry, physiology, ecology and related disciplines. Few workers are trained in more than two of these disciplines, and therefore it is not surprising that the divisions of science have divided the study of pesticides. For example, those trained in chemistry do not easily see the pesticide problem as one of population ecology. It is more surprising that the subdivisions of biology erect barriers to understanding. For example, work on the effects of pesticides on avian predators rarely takes into account the extensive literature on the effects of pesticides on invertebrate preylpredator relationships in crops. Since the pesticide problem involves several scientific disciplines and is very complicated, it is one in which it is extremely easy to miss seeing the wood for the trees. The aim of this review is to describe the nature of the wood. The picture given is a crude one; but I hope that the great need for a logical and total view of the pesticide problem will be accepted as an excuse for the detailed errors of commission and omission which it inevitably contains. In particular I hope that this review will help to clarify the problem to pesticide specialists who are not ecologists, and at the same time provide a rational introduction to the subject for ecologists who know little about pesticides. Accordingly the effects of pesticides will be classified and described in ecological terms. Mr. R. Crompton, who acted as Information Officer of the Toxic Chemical and Wildlife Division of the Nature Conservancy from 196165, estimated that about 300 papers relevant to the study of pesticides in the environment were published every month. I must emphasize that I have only read a small fraction of the vast literature on this subject and am in no position to attempt to assess it. Therefore this pa.per is not a review of the subject but of its nature. My only qualification for attempting the task is that over the last six years my work has given me an unusual opportunity to see it as a whole. I n this paper references to some important works are given but many others are omitted. I have

A SYNOPSIS OF THE PESTICIDE PROBLEM

79

not attempted to review the literature other than to mention some key reviews, books and papers, but have merely used examples of the literature to illustrate the themes. Wherever possible I have referred to the most recent work known t o me when this contains references to earlier publications. The reasons that have hindered a unified approach to pesticide problems have doubtless discouraged workers from writing general reviews of the subject. The nearest approach to an ecological review is R. L. Rudd’s valuable book “Pesticides and the Living Landscape”, 1964. There are many excellent works on the various subdivisions of the subject. Of the text books the following are particularly valuable: Brown (1951), Metcalf (1955) and Martin (1964). From the ecologist’s point of view Martin’s book is especially valuable for its summaries of the chemistry and mode of action and methods of application of pesticides, Metcalf‘s for the summaries of the mammalian and insect toxicology of insecticides, Brown’s for information on the older insecticides and on the physical aspects including aerial spraying. The volume on biological control edited by DeBach (1964) provides a n excellent introduction to the ecology of crop protection. More has been written about DDT than about any other pesticide: the volumes edited by Muller (1955, 1959) on DDT summarize the extensive literature on this insecticide and contain information which is particularly valuable towards understanding a pesticide which is of very great ecological significance. Useful and extensive summaries of the toxicological literature are provided in the handbooks of Negherbon (1959) and Rudd and Genelly (1956). Among review papers the following are particularly useful introductions to their subjects: Ripper (1956) on the effects of pesticides on arthropod populations, Stern et al. (1969) on integrated control, Cope (1966) on the special problems of pesticides in fresh water, and Butler (1966) on pesticides in the marine environment. The problems of interaction (“potentiation”) are reviewed by Dubois (1961) and pesticide resistance by Brown (1961) and Georghiou (1965a). Much valuable information is presented in the handbooks produced annually by such organizations as the British Insecticide and Fungicide Council and the British Weed Control Council. Many valuable papers on pesticides, including some of the reviews already mentioned, have been published in the annual series entitled “Advances in Pest Control Research” which is edited by R. L. Metcalf. The annual circulars of the United States Fish and Wildlife Service (United States Department of the Interior) provide useful progress reports of pesticide/wildlife research in that country. British work on this subject is described in the reports of Monks Wood Experimental Station. Several symposia have been held on the effects of pesticides and their

80

N. W. MOORE

proceedings published. The following are particularly relevant from the ecological point of view: 1. “The Ecological Effects of Biological and Chemical Control of Undesirable Plants and Animals”. I.U.C.N. Symposium, Warsaw 1960. Edited by D. J. Kuenen. (1961) Leiden. 2. “Chemicals and the Land in Relation to the Welfare of Man”. Proceedings of a Symposium held at the Yorkshire (W.R.)Institute of Agriculture, York 1965. Edited by F. M. Baldwin. (1965) Bradford and London. 3. “Research in Pesticides”. Proceedings of the Conference on research needs and approaches to the use of agricultural chemicals from a public health viewpoint. Held at the University of California, Davis, California, 1-3 October, 1964. Edited by C. 0. Chichester. (1965) New York and London. 4. “Pesticides in the Environment and their Effects on Wildlife”. Proceedings of an Advanced Study Institute sponsored by the North Atlantic Treaty Organization, Monks Wood, England 1965. Edited by N. W. Moore. (1966) J . appl. Ecol. 3 (Suppl.). Finally there is “Silent Spring” by Rachel Carson (1962): this is not a balanced view of the pesticide problem; it is an impassioned advocate’s plea for a more critical appraisal of pesticide use. I n that it has influenced the minds of many people, this famous book is itself an important “ecological factor’’ which has to be taken into account in assessing the effects of pesticides on living organisms.

11. THE NATUREOF THE PESTICIDE PROBLEM A N D THE TYPESOF RESEARCH NECESSARY FOR STUDYING IT The word pesticide is a useful omnibus term which covers all chemical agents used by man to kill or control living organisms. It includes weed killers (herbicides), fungicides, insecticides, acaricides, nematicides, molluscicides and rodenticides, and is often held to include chemosterilants and growth retarders. Since no plant or animal lives in isolation, an application of a pesticide never results in a total reaction of the form

all pesticide applications in fact consist of the reaction

I

pesticides --f ecosystem in which the pest occurs

I

This is the only reality; it consists of a man-made factor impinging on a complex system made up of physical elements and interacting

A SYNOPSIS OF THE PESTICIDE PROBLEM

81

populations. The essence of all pesticide problems, therefore, is one of population ecology. All other approaches are simplifications imposed for the purpose of scientific analysis. This has the important corollary that the results of analysis are likely to be misleading unless they are related to the system as a whole: in other words resynthesis is essential. Of course this concept applies to all ecological work, but there is abundant evidence to show that it is frequently forgotten in pesticide research. For example, it is often thought that effects in the field can be reliably predicted from simple toxicity tests. Misunderstanding about the nature of pesticide problems is probably reinforced by the use of the term “side-effects”. For commercial and pest control reasons emphasis has to be made on the pesticide and the pest; as a result all other effects are thought of as “outside” the essential pesticide/pest relationship. It is then very easy to fall into the error of thinking that the actual reaction is pesticide --f pest ( f side-effects) _ _ _ _ _ ~ ~

~

I believe that many of the misunderstandings about the effects of pesticides stem from this way of thinking. It might be countered by the use of the term “biocide”, since this emphasizes the whole effect of the chemical agent, not just the intentional effect. On the other hand it could be argued that many factors other than pesticides are biocidal. Once it is recognized that all pesticide applications consist of a toxic factor impinging on a highly complex system, useful deductions can be made. 1. In studies on the effects of pesticides, a scientist is always dealing with the effects of a factor (which can be accurately described) on a system whose nature is scarcely understood at all. This is because the complexity of ecosystems is such that in no case have their workings been demonstrated. At best we have crude models illustrating what are believed to be salient features. 2. At any one time the population size of each species in an ecosystem is the result of a number of intrinsic and extrinsic factors. Therefore, even if the exact physiological response of a species to a pesticide can be predicted this will not necessarily demonstrate whether the species will increase or decrease as a result of the application of the chemical. 3. The pesticide will impinge at all levels of organization: at levels of the cell and the organ, and a t the levels of ihe individual, the population and the ecosystem. Therefore the most adequate explanation of pesticide effects consists of a synthesis of information

82

N. W. MOORE

from a wide range of scientific disciplines, notably from toxicology and population dynamics. 4. All possible effects cannot be foreseen from toxicological and autecological studies, therefore it is often desirable to carry out experiments on whole systems: to compare sprayed areas with unsprayed controls. Nevertheless, experiments of this type can never produce absolutely reliable predictions on effects on constituent species, because ecosystems change and so alterations in the system may result in alterations in the effects on constituent species. From all these considerations it will be seen that while we can accurately describe the pesticide we cannot accurately describe the system it affects. Its impact is on ill-defined complex interactions and on phenomena that are frequently continuous; therefore effects can only be predicted in terms of probability. Most ecological situations are multifactorial ; when discussing the increase or decrease of a population we should expect several causes. Relatively simple cause and effect relationships may be found but we should not expect them. A full study of the effects of a given pesticide on a given species requires assessment of all available information about the following: 1. The properties of the pesticide. 2. The manner of application of the pesticide. 3. Information on the extent to which the species comes in contact with the pesticide. This can be obtained from: ( a ) Details of application, see 2 above (e.g. amount of active ingredient per unit area). ( b ) The behaviour of the species in the sprayed area. 4. Response of the species to the chemical (data on acute and chronic toxicity). 5 . Information on the principal factors which control the population of the species in situations in which no pesticide is used. 6. Toxicological information on the eEects of the pesticide on other species which are principal controlling factors of the species studied (see 5 above). Consideration of ihformation of these types will suggest an hypothesis that the pesticide is likely to have a certain effect on the species (e.g. cause a decrease). This can be tested to a limited extent by performing a field experiment of the type mentioned above. I n no case known to the author has all the necessary information been available in any assessment of pesticide effect. The main gaps in information are in toxicology and population ecology. Frequently no toxicological data exist for the species concerned, and the assumption has to be made that it reacts in the same way as a related standard

A SYNOPSIS OF THE PESTICIDE PROBLEM

83

laboratory animal. Only very broad conclusions can be drawn from such assumptions because organisms react very differently to the same pesticide, see page 94 and Table 111. One of the most valuable by-products of the pesticide controversy is that it has shown how very few elementary ecological data are available, even in Britain where the flora and fauna have been more thoroughly studied than in most countries. I n this country only the distribution of flowering plants has been systematically studied and recorded (Perring and Walters, 1962). Until recently the distribution of lower plants, vertebrates and the more conspicuous invertebrates has not even been studied systematically. For most animal species even crude distribution maps could not be drawn. Except for a very few species of birds no attempt has been made to assess population numbers, but even in this group which provides more scope for census work than any other, population data are largely lacking: of the 200 or so species of breeding birds in Britain, population estimates based on total censuses or censuses of extensive sample areas have only been made for fifteen species. I n only four have population estimates been made in three or more years and in only two of three were the first censuses made before the large scale introduction of pesticides (Moore, 1965b).Therefore there is extremely little systematic knowledge about population fluctuations in the past, and so much discussion on the effects of pesticides rests on a posteriori arguments. Man is the only species for which population data are adequate. Many animals ingest pesticides through their food, therefore knowledge about their feeding habits is essential in assessing the effects of pesticides upon them. Lists of recorded foods are available for a number of organisms, mainly birds and the larvae of Lepidoptera. Enough is known to show that most animals ar0 not specific in their choice of food but are to a greater or lesser extent opportunists within varying limits. This is not to say that some species do not have preferences or that some do not show distinct patterns. For example several herbivorous birds initially feed their young on insects. I n a few cases feeding patterns of local populations have been studied systematically, for example, the Tawny Owls of Wytham Wood by Southern (1954). But for large populations of species which feed on several types of food, statistical information about the proportions of different types eaten is not available. Again we lack essential basic data. I n assessing the effects of a pesticide on a species, data on populations, residues, toxicology and feeding habits are required. A list of vertebrate species recently or currently being studied in Britain in ordex to determine the effects of organochlorine insecticides is given in Table I. A reasonable amount is known about the feeding habits of all these species. It will

TABLEI Inforniation Available on The Effects of Organochlorine Insecticides on Some Vertebrate Species Studied iu Britain Population

Species

Heron (Ardea cinerea) Great Crested Grebe (Podiceps cristatus) Peregrine (Palco peregrinus) Sparrow -Hawk (Accipiter nisus) Buzzard (Buteo buteo) Pheasant (Phasinnus colchicw)

Feral Pigeon (Columbus livia) Shag (Phalacrocornx oristotelis) ~

Systematic Systematic national national studies studies made made before 1940 after 1940

+

Residue Analysis Local studies made before 1940

Local studies made after 1940

+

0

+ + +

0

0

+

0

0

0

0

0

0

0

0

+

0

0

0

+ 0 0

I-

0 0

0

(Vulpea vu2pee)

0

0

0

Authorities

-

0

+

r)

0

No change Stafford, in prep.

0

f

0

0

Increase

Prestt (1966)

0

-

0

0

0

+

0

0

0

0

Ratcliffe, (1963, 1965) Prestt (1965 and in prep.) Prestt (1965)

-

+

Large decrease Large decrease Slight decrease No change

i

0

?

0

0

+

0

0 0

+ + + +

Increase

Genelly and Rudd (1956), DeWitt (1956), Szevedo et al. (1966), Taylor and Ash (1964) Turtle et al. (1963) Potts (unpub.)

(limited systematic)

~~

For

Recent Population Changes

Acute oral Sublethal Systematic Incidental toxicity effects on national national data reproduction available studied

+ + + + + +

+ +

Toxicology

.p

+

?

Blackmore (1963), Taylor and Blackmore (1961)

3

a

30 5a

1 ‘1

A SYNOPSIS O F THE PESTICIDE PROBLEM

85

be seen that in no case do available data approach what is required. For most other species both in Britain and elsewhere even less information is available. It might be thought from what has been said in this section that the study of pesticide effects contains so many unknown factors that evaluation is pointless. On the other hand the use of pesticides raises so many practical problems that we have to attempt to understand their effects. In the present state of ignorance we rarely expect to do more than bring a little order into chaos and to provide tentative answers.

111. PESTICIDES AS AN ECOLOGICAL FACTOR: ITSDEVELOPMENT AND PRESENT MAGNITUDE While difficulties in interpreting the effects of pesticides might be expected, the measurement of the pesticide factor itself might be thought to be a simple matter. I n practice it is not. For all studies on the effects of pesticide use it is essential to know the quantity of active ingredient and how and when it was applied. I n dealing with localized effects the minimal information (unit weight per unit area, type of spraying machinery and date) can be obtained from the farmer or contractor. However, studies on pesticide application show that even under ideal conditions spraying treatments usually result in an uneven distribution of the pesticide. The practical difficulties of determining the exact distribution of spray on the treated area are so great that this is rarely done. For an exception see Giles and Peterle (1963), who studied the distribution of malathion after spraying by labelling the material with 3%. Even when the average rate of application may cause little damage, localized concentrations of pesticide are likely to occur and these may be hazardous. In going from localized areas such as an experimental orchard or field to large parts of the earth surface, and from local populations to ranges of species, the same general categories of information on use are still required. Unfortunately they are rarely available because annual statistics for different types of pesticide use are not kept by any country. It is impossible to give accurate figures for present day use or to describe accurately the development of pesticide use during the last quarter of a century. However, from the evidence available, it is possible to give a general picture of the trend and the order of magnitude of pesticide use. The earlier history of pesticide use has been recorded by several authors, e.g. Metcalf (1955) and Martin (1964). Nicotine was used as an insecticide in the mid-18th century. By the end of the 19th century a number of substances in common use today we;e being used, for example Bordeaux mixture, lime sulphur and dinitrocresol. BHC and DDT were both synthesized in the 19th century but their insecticidal D

86

dj,

,

,

,

,

/.;-I

,

= 4

- 3 > 2 1

1920

1910

1930

1950

1940

1960

Date

FIG.1. The increasing use of herbicides in Britain - the progress of rheinical weed control in cereals 1911-65. After Woodford, 19G4. Note: Total acreage in 1963 = 7.934 million acres (3.172 million ha.). 180

.

I

I

160-

140-

120u)

U

5 100-

0

a

c

0 ._

f

I

I

80-

I

I ,

a , a .

,. S

.

.I

,, ... , *

I

i

6 0 :* *

,

I $I

*

I

,2.4-l

*0

i

.lo-;,

, I a*

,:

20 -\

\

0, 1940 I

1945

1950

1955

1960

FIG. 2. Changes in the productioii of pesticides in the U.S.A. 1939-63. (Data from agricultural statistics, USDA. U.S. Government Printing Office, Washington.) Note: The graphs for the inorganic insecticide lead arsenate, the synthetic organic insecticides DDT and dieldrin, and the synthetic organic herbicide 2,4-D are of production. Not all the pesticides produced were used in the U.S.A. I n 1963 101 955 000 lb of DDT, 803 000 lb of lead arsenate and 28 GOO 000 lb of herbicides inr.luding soine 2,4-D were exported. The graph of pyrethrum, an insecticide dwived from t,he plRnt C'li,!/suntl~e,,,ui,1 cineruriuefolium, is of imports. Earlier figures for dieldrin not availablc: it, was first, produced about 1950. 1963 figure for lead arsenate not available.

87

A SYNOPSIS O F THE PESTICIDE PROBLEM

properties were not known until very much later. Development of new pesticides and the increase in treated acreage was slow between the wars. The modern pesticide era began during and immediately following the Second World War with the invention of the organochlorine and organophosphorus insecticides and of the phenoxyacetic acid (growth regulator) weed killers. The development of herbicide use in cereal crops in Britain is shown in Fig. 1, and changes in the production of various pesticides in the United States is shown in Fig. 2. The two graphs demonstrate the rapid rise of modern synthetic pesticides. The gradual decline in the use of the inorganic insecticide lead arsenate and of the naturally occurring insecticide pyrethrum is shown in Fig. 2. It can be assumed that the amounts of pesticide used will continue to increase until nearly all crop land is treated. Detailed estimates on the relative amounts of different pesticides used in a country can be made when crop acreages and standard spraying practices are known. The recent estimates of Strickland (1966) for Britain are given in Table 11. Estimates of the world production and use of pesticides are necessarily TABLEI1 Estimattd Quantities of Pesticides Used Annually in Great Britain Estimated tonnages of active ingredients used annually (in round figures)

Materials

INSECTICIDES

Organochlorines Organophosphates Petroleum and tar oils Other insecticides and actlricides TOM

600 a00 100 60 960

FUNQIOIDES

Lime sulphur Other sulphurs, expressed as S Coppers, expressed IM Cu Mercuries, expressed as Hg Dithiocarbamates, including dithiocarbamatetype fungicides captan Other synthetic fungicides Total ( 1 ton = 1 016 kg)

(From Strickland, 1966)

500 900 470 20 320 330 120 2 660

88

N. W. MOORE

most imprecise but several have been attempted, notably by Arrington (1956). Rudd (1964) estimates that the total annual production of DDT approaches 225 000 000 Ib. The total amount of a given pesticide in the environment depends on its persistence in atmosphere, water, soils and living organisms. At any one time the tonnage of a persistent pesticide like DDT, which may take several years to disappear, will greatly exceed the amount derived from annual production figures. The total amount of DDT on the earth’s surface is perhaps of the order of 1 0 0 0 000 tons. Fifty thousand tons of insecticides are now used in malaria control and eradication schemes alone each year (WHO Report 1964). Useful estimates of pesticide imports into African countries etc. are reported from time to time in the Economics Section of “Pesticides Abstracts and News Summaries”, edited by G. Ordish and produced by the Department of Technical Cooperation, London. Since persistent pesticides become concentrated in surface films, muds and lipid material in organisms, the distribution of these substances is undoubtedly most irregular throughout the world; therefore estimates of mean concentrations derived for example by dividing the contents of the oceans by the tonnage of organochlorine insecticides are virtually meaningless.’ It should be noted that these pesticides will be concentrated in those places, e.g. surface waters, where they are most available to living organisms. This should be taken into account when considering the significance of residues in marine animals both in temperate and polar regions. We are very far from being able to measure the size of the pesticide factor on a global scale, yet this is an important requirement in all large-scale appraisals of pesticide effects. The participants of the North Atlantic Treaty Organization Advanced Study Institute on Pesticides in the Environment held in 1965 drew attention to this fact in their General Statement (see Moore, 1966). It is greatly to be hoped that the relevant national and international agencies will take the steps to make the information on pesticide use available to all concerned. OF PESTICIDES AS AN IV. THEMAIN CHARACTERISTICS

ECOLOGICAL FACTOR A.

COMMON C H A R A C T E R I S TI C S

1. General There are, very approximately, 200 pesticides in common use today, of which about 90% are synthetic organic compounds, 5% are inorganic compounds like mercurous chloride and 5 % are naturally occurring organic compounds like pyrethrum. Some of the latter are also synthesized. Pesticides can be classified according to their function (herbicides, insecticides, eto.), or their form of application (sprays, dusts, granules, seed dressings, etc.), or their chemical nature (organochlorines,

A SYNOPSIS OF THE PESTICIDE PROBLEM

89

carbamates, etc.). The chemistry of pesticides and their properties are described in a number of handbooks; particularly valuable are the works of Brown (1951), Metcalf (1955) and Martin (1964). The characteristics of some pesticides of probable ecological importance in Britain are given in Table 111. All except dalapon, which is included because it is much used in fresh water, have one or more of the following characteristics: (i) They are used on more than 100 000 acres each year in England and Wales (see Strickland, 1966). (ii) They are highly toxic (acute oral toxicity LD50 to rat is less than 20 mg/kg). (iii) They persist in soils for more than one year. Pesticides vary considerably in their nature but they share the following characteristics : (i) They are designed and used by man to kill some form of living organism. (ii) They are used against populations of organisms. (iii) The amount which has to be used is far in excess of the amount required to kill the pest. (iv) They are used against a very small proportion of the world’s species (less than 0.5%). (v) They are generally used when a population of at least one species (the pest) is present in abnormally high numbers. t (vi) They are non-specific in their effects. (vii) Their action on populations is usually density independent. t Some exceptions should be mentioned. Chemosterilants do not kill the organisms but prevent reproduction. Poisons are sometimes used against individual vertebrate animals, for example against a rogue predator. At least one specific pesticide is on the market; this is Norbormide, a rodenticide which appears to be specific to the genus Rattus. Some of these common characteristics and their effects are elaborated below. 2. Non-speci$city Pesticides have radical effects on ecosystems because they are nonspecific. The effect of a specific pesticide would be homologous to specific disease or selective predation by one species on another. Even so it could have important effects because the elimination or great reduction of any wild species is bound to affect others in the same ecosystem. If the species is an important or key species, determining major features of the ecosystem, its disappearance may have widespread effects. For example, the great reduction of the European rabbit in Great Britain which followed the introduction of the myxoma virus led to widespread

t Note that the applications but not the effects are density-dependent.

90

N . W . MOORE

changes in vegetation (Thomas, 1960) and some changes in animal populations (Moore, 1956). Yet this disease was virtually restricted to the rabbit. A specific pesticide which eliminated the grey squirrel, the woodpigeon, the grey rat or bracken, for example, would be likely to produce similar fundamental changes in Britain. These might be complicated. However, most pesticides are not specific: most of the pesticide problems of agriculture, conservation and medicine arise from this fact. The reasons for the rarity of specific pesticides are these. New pesticides are largely discovered by trial and error - by subjecting test organisms to a very wide range of chemical substances. The chances of specific pesticides being found in this way are very slight. The systematic discovery of specific pesticides would depend on knowing more about specific biochemical features of the pest species. In general such basic information is lacking and the cost of the necessary fundamental research would be considerable. The incentive to find specific pesticides may be slight because the profits resulting from the sale of specific pesticides are likely to be less than those from the sale of wide-spectrum ones. To conclude, non-specific pesticides are likely to be used for inany years to come and their effects are likely to be complicated. There is a complete range of type of effect from total to specific effect. A few pesticides kill virtually all living organisms in the area of application (e.g. DNOC); others kill all plants (e.g. paraquat, simazine) and hence have a severe secondary effect on animals. But most herbicides and most insecticides are more selective: they kill species of certain large taxa and have little or no effect on the species of other taxa. For example, dalapon kills most monocotyledonous plants but does not harm dicotyledonous species, whereas phenoxyacetic acid herbicides in general have an opposite effect. The insecticides in common use are far more toxic to arthropods than they are to mammals and birds (see Table 111).I n the case of DDT this is because it is much more rapidly absorbed through insect cuticle than through vertebrate skin. Some systemic organophosphorus insecticides (e.g.schradan)kill aphids and other plant-sucking species but not their insect predators, while others (e.g. demeton) kill both aphids and predators. Owing to differences in reactions to pesticides by different species (see p. 94 and Table 111), pesticides have differential effects on populations.

3. Density-Independent Effects Pesticides usually act independently of the density of the species they affect. However, in some circumstances they could have densitydependent effects. For example, a species living in an environment that was not normally sprayed might begin to increase and be forced to

A SYNOPSIS O F THE PESTICIDE I’ELOBI,EM

91

colonize an environment that was subject to spraying. As a result it would only be affected above a certain level - that at which the sprayed environment was colonized. This could happen on a large scale, for example when a bird species living in an uncultivated habitat colonizes agricultural land; or on a small scale, as for example when members of an insect species which normally lives in parts of plants untouched by sprays are forced by population pressure to live on the exposed parts of the plant. Despite these exceptions pesticides are essentially a densityindependent factor. Therefore they do not necessarily “control” pests in the biological sense of the word. They may only kill a proportion of the surplus which would bc eliminated in any case by a densitydependent factor (e.g. predators) (Nicholson, 1939; Stern et al., 1959). An important difference between the medical and agricultural use of pesticides should be noted. In many programmes done to control disease-carrying organisms the aim is to exterminate the vector: in agricultural programmes the aim is to reduce its numbers so that they are of negligible economic importance.

B. TOXICITY The only generalization that can be made about pesticide properties is that there is great variation. Toxicity and persistence are especially important ecologically and are discussed below; the range of effect is very great, for both. Pesticides may kill, have sublethal effects, or none at all; and whereas some remain active after several years, others are broken down or inactivated almost as soon as they are applied.

1. Acute Toxicity Pesticides affect organisms in many different ways. Despite a formidable amount of research the exact mechanisms are rarely understood, The phenoxyacetic acid group of herbicides, which make up the bulk of those used today, kill plants by interferences with growth processes (see, for example, Wain, 1958). The primary effect of most insecticides (organochlorine, organophosphorus and carbamate substances) is on the nervous system. The organophosphorus and carbamate insecticides inhibit the activity of cholinesterase. Many pesticides have more than one effect, for example DDT affects the central nervous system, met,abolicprocesses and reproduct,ion. In this case the effect on the nervous system appears to be primary but 111 others it is often difficult to define the most important effect, especially since systems interact. Pesticides of the same chemical group have the same general effect and yet vary greatly in their toxicity. For example, for rats there is nearly a 700-fold difference in acute oral toxicity between the two

TABLEI11 Characteristics of Some Pesticides of Probable Ecological Importance in Great Britain 1966* (see p . 89) Group and Chemical

function

Estimated agricultural use in England and Wales

Toxicity Soluble in water

Acreage Tonnage treated

Aldrin

Organochlorine insecticide

Azinphos Organophosphorus Methyl insecticide BHC (including Organochlorine Lindane) insecticide Captan Organic fungicide Copper salts

Inorganic fungicides

Dalapon

Trichloroacetic acid herbicide Organophosphorus insecticide Organochlorine insecticide Phenoxyacetic acid herbicide Organochlorine insecticide Organic herbicide and insecticide

Demetonmethyl DDT 2,4-D Dieldrin DNOC

225000

137

AS Dieldrin

57 200

10.1

(+)

2 539 000

117.0

(+)

424 000

332.6

170000 468.4 Elemental cu

375 900 262 000

97.5

12 OOO+

+

+ +

+ +

+

50.0 8-O+

(+)

10-67

e a ~ i - Fish B~~ &own form (TL,- (Acute t o have Bird 24 hrs) Oral effectson (Acute LD50) reproOral duction LDBO) atsublethal doses 4-4.5

16.4

+ +

262.0

(100 O O O + ) 490000

Persistent in Rat (Acute Oral LD50)

125200 9 00015 000 C. 140300

0.020.1

2.5

As dieldrin

0.13 60200

0.09

1949

Notes

I n animals epoxidized to dieldrin

1953

+

1.5

1942 1949

900

1885

6 590 -9 330

255

40-

9.6

6.4

0.010.4 125

4.6

0.13-

2.5

180 113800 400666 347 100 740

+

Residues Approxiof pestimate cjde Or date Of toxic meta- introbolite in duction predators or secondarJ' poisoning recorded

300

2043

1953 1951

+

1944 1942

0.24

+

+

1949 1892

2580

f

(+I

23

Used against aquatic plants Systemic

Dithio-

carbemates Ehdosulfan Endrin

--

i(

Heptachlor

Lead Arsenate Mercury salts

YCPA Paraquat

Simazine Strychnine Sulphur TDE

UlW8 Warfarin

Organic fungicides

Organochlorine insecticide Organochlorine insecticide rodenticide Organochlorine insecticide I

Inorganic insecticide Inorganic and organic fungicides Phenoxyacetic acid herbicide Quaternary Ammonium herbicide Triazine herbicide Plant-derived rodenticide Inorganio fungicide Organochlorine insecticide Substituted urea herbicide rodenticide

1 120 600

31t-1

+-(+)

866-

2 860

7 500 13000

6-0

40-60

2000

1.0

7-43

3-4-

1931

22.4

0~00002 70

3.5

1956

+

0.0015-

+

1951

Isomer of dieldrin

+

1951

Closely related to chlordane. In animals epoxidized to H. epoxide. H. epoxide more toxic than Heptachlor.

0.0003 115 000

5.0

15 100

30.3

6 048 100 20.9 Elemental Hg 5 890 000 4 750 7340+

3.3+

5000+

2.2+ 0 m U

Id J LL.

z In

J J

TIDES IN LOUGH.

0

1

2

3

4 5 6 7 8 TIME. I N HOURS.

9

1011

12

I3

FIG.6. Graphs showing the rise and fall of water level in Lough Ine and Barloge Creek. A. Tide levels for spring tide in Lough Ine and Barloge Creek on 19 July 1932. B. Tide levels for neap and spring tides in Lough Ine with the times of high water made to coincide. C. The same curves in B with the neap tide curve displaced t o the right so as t o superimpose the curves for about 6 h of outflow. (Figs. 6A and B are copied from curves published by Roes (1936, Graph 2), made from data originally provided by Prof. N. H. Walsh of the Engineering Department, University College, Cork. In order t o produce the complete curves in B and C it was necessary t o repeat part of Rees’s curves. These parts are shown by broken lines. The dotted parts were inserted t o give smooth curves.)

ECOLOGICAL STUDIES AT LOUGH I N E

209

level with Mark 7 on the quay (Fig. 4); to the north and south of this point the greatest speed attained falls off, and is less than 1 m sec-l in mid-channel at each end of the Rapids. The current is weak in places where the shore recedes from the main channel at either end of the Rapids - Renouf’s Bay, Eddy Creek, and off Nita’s Rock - and these places are occupied by eddies when their end of the Rapids is downstream. The bottom of the Rapids is covered by a forest of the large brown algae Saccorhiza polyschides and (over the Sill) Laminaria digitata (Fig. 7). The fronds of these algae form a canopy held up a little distance above the bottom and populated by a characteristic but limited fauna and flora (p. 222). The current speeds at the upper surface of the canopy at several stations are given in Fig. 8. They are little different from those at the surface of the water. The canopy partially protects the bottom from the current. The current speed, as measured with a Pitot tube, falls off rather steeply below the canopy. However, in the regions of fastest flow at the water surface, there is still a very appreciable pressure (indicating up to 1 m sec-l) when the Pitot tube is held in contact with the rock bottom (Fig. 9). There are no doubt pockets of relatively still water, as described by Ambiihl(l959; see also Macan, 1963), between the large boulders towards the northern end of the Rapids. Nevertheless the direction of the current and the turbulence change with the tide, and few places are likely to offer permanent shelter. Macroscopic organisms living on the Sill must be subject to a very considerable velocity gradient in the boundary layer over the rock surface, as discussed by Crisp (1955). Other physical and chemical conditions of the water and underlying substrate are considerably affected by the current. Rocks in the main stream have little sediment upon them, and those on the Sill are clean, although there are some broken shells in crevices between them. Rocks in the quieter areas-Codium Bay, Renouf‘s Bay, Harbour, Eddy Creek, and off Nita’s Rock - have a distinct deposit of fine sediment resting on their upper surfaces and among the algae and other organisms which grow upon them. The distribution of sediments on boulders throughout the Rapids area was investigated by means of a special box which acted as a miniature diving bell (Kitching et al., 1952). Each boulder was placed in the box under water and the water in the box was then displaced by air, to fix the sediment in position, before the apparatus was brought to the surface. The sediment was then washed separately from the top and the bottom of the boulder, graded by the use of wire sieves, dried, and weighed. The average density of sediment is shown in Fig. 10. On the tops of boulders the total amount is least on the Sill and continues low to the

210

J. A. KITCHING A N D F. J. EBLING

0 1

10m304050 1

METRES

1

I

I

I

Himanthalk elongata o Codium fragile 0 Saccorhiza polyschides B Laminarb digitato

8

Laminoria wccharima

7. The distribution of dominant sublittoral algae in the Lough Ine Rapids in September 1946. The C o d i u m fragile is subsp. tomentosoides.

FIG.

FIG.8. Water currents at level of the canopy. (a)Maximal currents in metres per second. (b) Mean total flow in kilometres per tidal cycle (based on average of figures for spring and n a p tides.)

211

ECOLOGICAL STUDIES AT LOUOH I N E

"4

2 hr. inflow

180

I 50

140-

3.5 hr. outflow

Surface STATION I 7 hr. outflow

Surface

0 canopy

W

>

I !-

5

u

70 60

1r

Surface

STATION 3 I60

6+

STATION

STATION 7

s hr. outflow Surface-

CanopyI I I

-Canopy

I I I

I

CURRENT IN CENTIMETRES PER SECOND

FIG.9. Current measured by Pitot tube in the Rapids.

north end of the quay. The highest amounts are a t Cadium Bay within the lough and at the north end of the Rapids on the Dromadoon side. There is much less sediment on the bottoms of the boulders than on the tops and the amount does not vary significantly from place to place. The largest fraction of the sediment, about half the" total amount at each station, is of the finest grade, passing a sieve of 200 meshes to the inch.

J. A. KITCHING AND F. J . EBLINO

212

TOPS v

u

u ....__ ............................................. ....... -..-'. ~

40

BOTTOMS 3

MARK OF SPRING TIDE

FIG. 10. Average dry weight of sediment, in grams per 1000 sq. cm of surface, on tops and bottoms of boulders.

I n places where the current is strong, the chemical conditions of the water are held fairly constant, although temperature fluctuates with inflow and outflow. We measured physical and chemical conditions a t a number of stations over a period of 24 h during fine weather, and the conclusions are summarized in Fig. 11 (Kitching et al., 1952). We found a fall in the percentage saturation with oxygen, and a rise in CO, concentration, 5 cm above the bottom in Codium Bay a t the time of low slack water (Fig. 12). There are slight indications of a similar change at other stations in quiet water. The mud no doubt has considerable reducing power, which can affect the overlying water when this becomes

ECOLOGICAL STUDIES AT LOUOH INE

213

FIG.11. Environmental conditions in the Rapids.

temporarily stagnant. Although no such effects were detected elsewhere, it is quite possible that some degree of stagnation may develop between the boulders at some of the other sheltered stations. One other feature marks off Codium Bay, and to some extent Renouf’s Bay, from the other sheltered stations. The fall in temperature brought about in summer by the inflow of cold water (Fig. 13) affects all other sheltered stations except these: they are protected from the inflow current by the South Basin vortex, which draws South Basin water across them throughout inflow. I n this respect these two stations belong to the South Basin rather than to the Rapids area, whereas Whirlpool Cliff, which is topographically well within the South Basin, has obvious affinities with the Rapids.

D.

T H E LOUGH

1. Currents The flow of water through the Rapids attains 50 m3 sec-l during inflow of an ordinary tide. This figure is derived from the area and tidal levels of the lough (Bassindale et al., 1948, p. 317) and independently from summated measurements of current in a section across the north end of the Rapids. The powerful inflowing stream sets towards Whirlpool Point a t about 20 m min-l and is mainly deflected to the northwest and west by the vertical cliff face. It sets the whole body of water in the eastern half of H

214

J . A. KITCHING AND F. J. EBLING

4

5

6

7

8

9 10 I1 12 13 14 I S 16 17 18 19 2 0 21 2 2 2 3 24 I

2

3

4

140-

60-

NITF'S

High Slack Water

ROCK ,

Low Slack

High Slack

Water

Water

low Slack Water

TIME IN HOURS FIQ.12. Oxygen saturation by Winkler's method at five stations off the west bank of the Rapids, 7-8 July 1949. 0 , surface; 0 . bottom.

ECOLOGICAL STUDIES AT LOUGH INE

215

CODIUM BAY

16 W

n 4

a

RENOUF'S BAY

(3 I-

z W u

In W W

a

s

0

z W

18-

Lr

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t-

4 16-

Lr W

a

I

IS-

W 14I-

EDDY CREEK

18-

1716-

15-

NITA'S ROCK

144

i k f

6 to 1'1 Low Tide in Sea

HighSlack Water

1'2

h h

1

1'5 1'6

15 18 lb

' I

HighTide in Sea LOW Slack High Sldck Water Water

d 0 dI 2 2 t r k

1 1 1

4

Low Tide

in Sea Low Slack Water

TIME IN HOURS FIQ.13. Water temperature at five stations off the west bank of the Repids, 7-8 July 1949. 0 , surface; 0 , bottom.

216

J. A. KITCHINO AND F. J. EBLING

the South Basin turning as an anti-clockwise vortex (Fig. 14). The inflowing water moves with ever-decreasing velocity towards the southwest corner of the lough, off the mouth of the Goleen, and displaces water northwards into the North Basin. The vortex is still active at a depth of 10 m, where we found speeds of up to 10 and 16 m min-1. We have reason to believe that the very turbulent inflow current mixes extensively with the whole body of water between the north end of the Rapids and Whirlpool Point. I n several experiments quantities of fluorescein were thrown into the Rapids (Bassindale et al., 1957) and the coloured water could be seen to move around the edge of the vortex along the route already predicted from observation of depth floats. The green colour appeared strong as seen from the cliff top, but could not be seen in samples of the water; no doubt it had been greatly diluted because mixing had occurred to a considerable depth. However, we were able to detect it in approximately equal concentrations at the surface and near the bottom in its passage between the north end of the Rapids and the Whirlpool Cliff. Additional evidence was obtained from measurements of water temperature. In summer the water flowing in

FIQ.14. Currents in the South Basin of Lough h e at a depth of 1 m during inflow. Each track represents the path of one depth float. Speeds are shown in metres per minute. (For this purpose sections of the track are delimited by arrowheads.)

ECOLOGICAL STUDIES AT LOUOH INE

EAST SHORE

WHIRL

POOL

MIDCURRENT

EDGE OF CURRENT

*C

OC

OC

217

WEST END

OF SECTION

OC

OC

0

5

10

15 20

AT LOW SLACK WATER

25

0 5

10

IS THREE HOURS AFT€ LOW SLACK WATER

20 25

;?

I

5

10

15

20

25

30

35

METRES

FIQ.15. Temperatures in section X (see Fig. 1 ) across the inflowing current in the region of the whirlpool, on the evening of 20 July 1954.

218

J. A. KITCHING AND F. J. EBLINO

through the Rapids is often much colder than the general body of water in the lough, and can thus be distinguished. I n these circumstances the strong thermal stratification which can be observed in the area north of Whirlpool Cliff during outflow becomes completely broken down during inflow, and the whole of the water along the route of inflow becomes uniformly chilled from surface to bottom (Fig. 15). The conclusion that water movement extends right down to the bottom is confirmed by the nature of the bottom itself -rocks and gravel rather than the mud which covers the rest of the lough bottom. During outflow water is drawn from the whole surface of the South Basin into the mouth of the Rapids (Fig. 16). There is little current at a depth of 10 m.

FIQ.16. Currents in the South Basin of Lough Ine at a depth of 1 m during outflow. Speeds are shown in metres per minute. (See Fig. 14.)

2.Stratijcution During summer the western trough becomes very markedly stratified with respect to temperature, pH, and oxygen saturation, with an epilimnion extending down to 20 m, and a hypolimnion from 30 m to the bottom (Fig. 17) (Bassindale et al., 1957). The epilimnion is relatively warm (13-16"C), well supplied with oxygen (80-100~0saturated), and

219

ECOLOGICAL STUDIES AT LOUBH INK

of the usual alkalinity for seawater (pH 8.8); the hypolimnion is cold (8.25-8.5O0C), deficient in oxygen (about 3% saturated in July 1962), and subnormally alkaline (pH 7.65). The thermocline is centred at about 25 m. I n the middle of the South Basin the depth barely exceeds 20 m, and near the bottom there is a sharp inflection in the curves for temperature, pH, and oxygen saturation, as though to begin a thermocline. A sharp fall in oxygen saturation was also found near the bottom in the North Basin. The salinity varies little with depth; all our readings in July 1952 fell between 34*90x0and 35.10%,,.

,

Y

7,7

pH7,6

7 R

Buoy

#

7,')

80

R I

82

83

0

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40

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#A

?

E f n

20

n

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/30

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Oxygen solurnlion

I

FCQ. 17. Temperature, pH and percentage saturation with dissolved oxygen (Alsterberg's modification of Winkler's method) in centre of Western Trough on 20 July 1952. Continuous line 11.11-11.40 h. Broken line 16.40-18.03 h. (High slack water about 06.20 and 18.40; low slack water about 14.45 h.)

We have no information about conditions a t other times of year, but we presume that there is complete mixing in winter. The temperature of water flowing in through the Rapids ranges in July between 11.5"C and 15OC; no doubt it depends on conditions in the sea outside. Presumably the surface waters of the lough are warmed

220

J. A. KITCHINB AND a. J. EBLINO

still further by the rays of the sun, so that a higher temperature is msintained there. It is to be expected that the deeper waters of the Western Trough will become better oxygenated with the postulated autumnal mixing, and that conditions may become much more favourable for animals in respect of oxygen than they were during the summer. We might expect a new onset of stagnation and oxygen depletion with the re-establishment of a thermocline in early summer. However, all this remains to be investigated.

3. Renewal of Water There are three different extreme situations which the South Basin might approach : (a) that all the water which comes in during inflow leaves again during outflow without mixing with the South Basin water; (b) that all the water which flows in remains within the South Basin, and that only old South Basin water flows out; (c) that all the water which comes in mixes with the South Basin water, and that mixed water flows out.

We have already provided evidence to suggest that the actual state of affairs approximates to (c),and we shall assume that (c) obtains. We must also assume that the hypolimnion of thc Western Trough, which in summer is at a temperature well below that of any inflowing water, is almost completely cut off during that season from the epilimnion. We may, therefore, regard the thermocline as forming a false bottom, as in some Norwegian fjords (Strom, 1936). Disregarding water below the thermocline, the average depth of the South Basin, including the south end of the Western Trough, is about 15 m. The surface area of the North Basin is about twice that of the South Basin, and the rise and fall of the tide in the lough is about 1 m. We shall express volumes of water in terms of the depth which they would occupy in the South Basin. During inflow 3 m of new water enter the South Basin from the Rapids, and 2 m of South Basin water are displaced into the North Basin, giving a general rise of 1 m. During outflow 3 m of water, again in terms of the South Basin, leave the lough, of which something less than 2 m come from the North Basin and something more than 1 m from the South Basin. I n effect, about 50% of the South Basin water is replaced by water from outside the Rapids in three tides; and there is also some exchange with the North Basin. Some of the water entering during the first hour of inflow may be old South Basin water, but it is

ECOLOQICAL STUDIES AT LOUQH INE

221

clear from the temperature of the inflow water (Fig. 13) that this amount will be relatively small. We have not studied the hydrography of the North Basin. The shortest possible time for complete replacement, on the assumption that there is no mixing and no loss of new (that is South Basin) water, is about twenty-two tides. With complete mixing about 90% of the North Basin water would be replaced by South Basin water in twenty-six or twenty-seven tides. It is possible that some parts of the North Basin may require much longer for a comparable renewal.

4. The Very Shallow Sub-Tidal Areas The investigation at Lough Ine is much concerned with the fauna and flora of the margins of the iough, from low water down to a depth of 1 or 2 m below that level, so that some consideration of the environmental conditions in the “shallow sublittoral” is needed. Unfortunately only preliminary studies are available. The quantity and nature of sediment on sub-tidal rocks has not been determined, although one can see without any precise measurement that rock surfaces on the open coast and in the mouth of Barloge Creek are clean, but that within the lough, except where there is appreciable current, they carry a film of fine sediment which becomes thicker with increasing depth until a t a depth of a few metres any rocks present are buried in mud. As in Codium Bay, stagnant conditions are likely to develop locally and in crevices between boulders over mud. Measurements of oxygen saturation made on a number of samples from positions 5 cm above the bottom, collected in July 1960, ranged from 78% to 122%. Goleen mud smells of H,S. Very little fresh water runs into the lough. Small streams enter a t the northwest corner, where a film of water of low salinity spreads over the surface, at Rookery Nook (northeast corner of lough), and near Whirlpool Cliff (drips only), and at the head of the Goleen. There is less opportunity for the fresh water to become diluted and dispersed in the enclosed Goleen, and after heavy rain we have found salinities as low as 3 4 ~ 0 % a t ~mid-Goleen, and 30.0%, at upper Goleen. I n other parts of the lough, in July and after heavy rain, salinities ranged from 3 4 ~ 3 % ~ to 34.9%,. Extremes of temperature also occur in the Goleen, especially when low water is in the afternoon. We have recorded 25°C in the shallow inter-tidal water of the upper Goleen, and 19-55OCsub-littorally at East Goleen. Under similar conditions the temperature sometimes rises above 16°C in the shallow waters at North Wall and along the north side of Castle Island. €I*

222

J. A. KITCHING AND F. J. EBLING

IV. INFLUENCE OF CURRENT A. DISTRIBUTION I N RELATION TO CURRENT Laminarian algae form a forest covering the whole Rapids area, and the plants and animals which inhabit the oanopy of fronds are more fully exposed to the current than are those living on the bottom. Moreover, most of the bottom is occupied by one species of laminarian alga, Succorhim polyschides, so that an extensive uniform substrate is provided for the population of plants and animals which live upon its fronds and stipes. Laminaria digitata is confined to the Sill and to the side of the quay. We have detailed information about the distribution within the Rapids area of several animals associated with Saccorhiza (Ebling et al., 1948). The numbers of Patina on Succorhim were counted at various stations in the Rapids - eight plants to each station. The results are shown in Fig. 18, where they are plotted against the maximum speed of the

-. 0

i

i sprrd d W

~

W . 1r-n

I-

3

inrn.tr.~ p~ -d

FIQ. 18. Population density of Patina pellucida on Saccovhiza polyschides (whole plant) in relation to the speed of current at fastest flow (inmetres per second). For position of stations see Fig. 4. September 1946. mean number of Patina per Saccorhiza plant; 0 number of Patina per 3 lb of Saccorhim.

current. Patina reaches its greatest abundance in moderate current, both above and below the Sill. It is rare on the Sill, where presumably the current is too strong, and almost absent from bays above and below the Rapids which are sheltered from the main stream. This conclusion is fully supported by much more extensive evidence for three selected stations.

ECOLOGICAL STUDIES AT LOUGH I N E

223

FIa. 19. Distribution of Membranipora membranacea, on fronds of Saccorhim polyschides, expressed as a percentage of total visible area of weed covered, as estimated from shore or boat. Current flowing out. September 1946.

The polyzoon Membranipora membranacea has a similar distribution. The percentage area of fronds covered by its colonies, as judged by an observer in a boat, is shown in Fig. 19. A very high proportion of the frond area was covered with this polyzoon at the optimum positions at the north and south ends of the Rapids. Two other Polyzoa, Hippothoa hyalina and Tubulipora plumosa, reach their greatest abundance on the fronds in the most sheltered places, and are almost absent from the fronds in the main stream. However, on the frilly margins of the stipes (Fig. 20), which are below the slippage plane formed by the canopy and which presumably also themselves provide some shelter, the last two Polyzoa are less abundant a t the most sheltered stations and reach their maxima a t stations in moderate current. The same pattern of distribution is shown by the spat of anomiid lamellibranchs. We investigated the fauna and flora associated with tufts of undergrowth-forming algae all along the west side of the Rapids. The weed was collected into bags held on the downstream side t o avoid loss of free-living organisms, although alert and active animals such as prawns and fish would have escaped. Although no preferences for particular species of algae were detected, there were distinct preferences in relation to water current. The species preferring strong current were the lamellibranch Mytilus edulis, to be discussed later (p. 258), two Polyzoa, Ebctra pilosa and Alcyonidium hirsutum, and two amphipods, Caprella acutifrons and Jmsa falcata, the last also inhabiting the frills of Saccorhiza in enormous numbers where the current is fast. Fifteen species preferred stations in quiet water, and others preferred intermediate stations (Sloane et al., 1961).

224

J. A. KITCHINQ AND F. J. EBLINQ

Fronds

Flats of stipes

U

l

l

l

U

W

l

f

I

t

50 I

Frills of stipes

FIa. 20. Average number of colonies of Hippothoa hyalina per plant, on fronds, flsts of stipes, and frills of Saccorhiza polyschidea in September 1946, a8 determined by counts from samples.

We collected boulders from all over the Rapids area as a means of sampling the bottom and studying the sessile fauna (Lilly et al., 1953). Of the species found attached to rocks, forty-eight were common enough for us to examine for preferences. Of these, eleven preferred stations in the strong current. For example, the anemone Metridium senile (Fig. 22)

ECOLOQICAL STUDIES AT LOUQH INE

226

and the mussel Mytilus edulis (Fig. 24) were almost confined to the Sill; the hydroid Sertularia operculata (Fig. 25) and the Polyzoa Hippothoa hyalina (Fig. 26) and Costazia costazii (Fig. 23) occurred on the Sill but also extended somewhat more widely throughout the Rapids. None of these species showed any preference for tops or bottoms of boulders, even though the water movement must be much less below. Indeed, of common species preferring current, only the hydroid Tubularia bellis (Fig. 27) and the limpet Patella aspera can be cited as preferring tops of boulders.

-

o

10

Metres

20

30

40

50

Q One

or only few seen

0 Moderote

in qumtity

FIG.21. Distribution of Gibbula cineraria on fronds of Sacwrhiza polyschides in September 1946 as seen from boat or quay.

Eleven species preferred stations in quiet bays; they are well exemplified by the anemone Anthopleura ballii (Fig. 22) which occurred within the lough and sparsely below the Rapids, and the polyzoon Cellepora pumicosa (Fig. 23). Intermediate preferences are nicely demonstrated by the anemone Corynactis vividis (Fig. 22), which though plentiful above and below the Sill is uncommon on tops of boulders exposed to the maximum current and extends neither beyond Renouf's Bay into the lough nor below the Rapids area. The polyzoon Scrupocellaria reptans is not dissimilar (Fig. 23). Again none of these common species showed any preference for tops or bottoms. However, some such preferences were shown by a few less common species, for example by Acanthochitona crinitus for tops and by Serpula vermicularis and Bugula jiabellata (Fig. 28) for bottoms. A number of species listed in Table I and exemplified by Verruca stroemia (Fig. 29) showed no obvious preference in respect of current. Some of these, such as Escharoides coccineus (Fig. 30) were almost

J. A. KITCHING AND F. J. EBLING

226

restricted to bottoms and sides of boulders, but we found no ubiquitous species which strongly preferred tops with the exception of the limpet Acmaea virginea (Fig. 31). T A B L EI Distribution of Commoner Species on Sublittoral Boulders in the Rapids in J u l y 1948 and J u l y 1950 No obvious preference for tops or bottoms Haliclona indistincta Adocia cinerea Mycale rotalis Anthopleura ballii Caryophyllia m i t h i Cellepora pumicoaa

Preference for tops

Preference for sheltered bays Acanthochitona crinitus

Preference for bottoms

Serpula vermicularis Bugula jabellata Escharella varioloaa Membran iporella n itida

~~-

Preference for intermediate conditions of current Corynactis viridia Scrupocellaria reptans Sertularia operculata Balanus crenatus Costazia costazii Hippothoa hyalina Umbonula littoralis Sagartia elegans Metridium senile Mytilus edulis

Preference for whole main stream Tubularia bellis Phimularia setacea

Virtually confined to Sill Patella aspera

N o obvious preference for current or shelter Myxilla rosacea Acmaea virginea Haliclona limbata Amphilectia fucorum Scruparia chelata Leuconia n,ivea Halichondria bowerbair ki Hymedesmia bronsted? Pomadoceros triqueter Spirorbis spp. Balanus balanua Eseharoides coccineus Verruca stroemia Diastopora patina Schizoin avella spp Crisia eburnea Lichen opora hispida Tubulipora plumosa Muaculua m r m o r a t u s Hiatella arcticu Kellia suborbicularis Monia s q u a w Heteranomia squamula Didemnum maculosum

.

* Not on the Sill.

ECOLOGICAL STUDIES AT LOUGH I N E

B.

227

MODE O F ACTION

Water movement may affect an organism a t any or all the stages of its life, and it may act in various ways, beneficial or injurious. It may dislodge an animal or plant from its substrate; it may prevent settlement of sediment, including organic matter which might otherwise lead to a deficiency of oxygen; it may prevent the establishment of local extremes of oxygen or carbon dioxide concentration or of temperature; it may distribute food, or the organism’s own larvae. It is extremely difficult to distinguish between these possibilities in any particular case, although we may speculate with some degree of plausibility in a few instances. We have investigated experimentally the preference of t’hegastropod Gibbula cineraria for water sheltered from strong current and from waves (Fig. 21) (Ebling et al., 1948). In several tests a number of G. cineraria were suspended on fronds of laminarian algae both in the main stream of the Rapids (off Mark 3 on the Rapids Quay) and at nearby stations sheltered from current. The fronds were placed in position at slack water in order to give the snails the opportunity of adjusting themselves to the current as it increased. They were re-examined after some hours, and it was found that nearly all the Gibbula had disappeared from the fronds placed in the Rapids, while most remained on the fronds placed in quiet water. We may reasonably conclude that GibbuZu cineraria is unable to hold on in the current; nevertheless, we cannot conclude unequivocally that the absence of G . cineraria from Laminaria on the Sill is to be explained in this way. A t present we can only surmise that current may prevent the larvae from settling on algae on the Sill, and that in any case any growing or adult Gibbula which wander or are carried on t o the Sill will fail to hold on to the laminarian fronds there. The same explanation may account for the absence of G . cineraria from laminarian fronds on the open coast. Inability to hold on is the most likely explanation for the limitation of many species which inhabit the fronds of Laminaria spp. and Saccorhiza in more sheltered positions, but are scarcer in or missing from the Rapids. These include the Polyzoa Membranipora membranacea (page 223) and Tubulipora plumosa, and the gastropod Patina pellucida. We do not yet know whether the adults or the larvae are susceptible to dislodgement. We have attempted some preliminary investigation, by means of field experiments, of the distribution of two species which “prefer” places where a strong current flows but show no preference between the tops and the bottoms of boulders. When rocks bearing Shrtularia operculata were transferred from the

228

J. A. KITCHING AND F. J. EBLING

Sill to Codium Bay, a sheltered situation inside the lough, the Sertularia became clogged with fine sediment within a week, and most colonies died within nine weeks. A large population of diatoms settled on the perisarc; and the amphipod Caprella acutifrons, a normal inhabitant of the Sertularia and transferred with it from the Rapids, also became clogged with sediment and perished along with the Sertularia. Clogging with sediment is the most probable cause of death, both for the Sertularia and for the Caprella, but again it is not possible to exclude other agents. It is interesting that Sertularia on boulders raised up on spikes in Codium Bay, whether facing upwards or downwards, and even Sertularia suspended over relatively deep water from buoys, all rapidly became clogged and perished. These colonies must have been quite out of reach of any adverse chemical influence of the bottom mud. The branches of the hydroid filtered sediment from the water moving past in the South Basin Vortex, At the same time the water movement was insufficient to prevent the spread of diatoms upon the hydroid, and a considerable population of these developed during the course of a few weeks (Round et al., 1961). We have made similar investigations on the anemone Corynactis viridis, which is somewhat more tolerant of sheltered conditions than is Sertularia operculata. Rocks bearing this anemone were transferred from the Rapids to Codium Bay. Corynactis on rocks raised upon spikes, and mounted facing downwards, survived for two years and multiplied. On the other hand, Corynactis on rocks facing upwards, whether upon spikes or on the bottom, survived for only about one year or less. Settling of sediment upon Corynactis facing upwards might account for this observation. Nevertheless, there remains the possibility that full exposure to light, in the absence of a canopy of Saccorhiza fronds, might be deleterious, either directly or by the encouragement of competitive algae. Rocks with Corynactis were therefore transferred to floating wire cages, some open to the light and some covered, in the Rapids and in sheltered water. Corynactis tended to close and to remain closed when exposed to full daylight, but to open in covered cages or by night. The distribution of Corynactis in the Lough Ine area is consistent with the hypothesis that these animals require clean conditions and restricted illumination. We have not yet investigated any of the numerous species which prefer shelter from current. We do not know whether they are restricted by the mechanical effects of current or by some secondary effect.

ECOLOGICAL STUDIES AT LOUGH INE

229

V. DISTRIBUTION IN RELATION TO SHELTER AND WAVE-EXPOSURE

A.

INTRODUCTION

Most of the plant and animal species which are common in Lough Ine show a significant preference for only part of the area; only a few occur throughout. Many of these preferences appear to be related to wave action; some species favour shelter, others exposure to waves, others an intermediate condition. The information to be presented is based mainly on a survey of the occurrence or abundance in July 1955 of a limited number of common species at thirty-three stations, each extending 10 m along the shore (Ebling et al., 1960). The whole intertidal region of each station was searched, and the shallow sublittoral explored with a view box, by wading, and in a few cases by diving. Observations of the sublittoral region did not a t any station extend below 5 m, and at some stations not below 1-2 m; in most parts of the lough there is a thick deposit of mud at greater depths. We recognize that the distribution of organisms may fluctuate from season to season or change over a period of time. For example, the amount of Codiumfragile within Lough Ine is not constant from year to year; we noted slight differences between the years 1955 and 1958 in the occurrence of Clawa squamata; and many new patches of Paracentrotus appeared in 1964. Nevertheless, our common experience over many years in general confirms the conclusionsbased on the 1955 survey. B.

THE LITTORAL REGION

1. Species Preferring Open-sea Stat'z m 1

Several intertidal organisms which occur on the open coast do not penetrate the Bullock Narrows. Such are the alga Porphyra urnbi~icalis, common on exposed shores where fucoids are absent, and the anemone Actinia equina (Fig. 32); probably both require frequent splashing. Littorina neritoides penetrates the mouth of Barloge Creek (Fig. 33). The alga Lomentaria articulata (Fig. 34) penetrates as far as the Rapids, and Laurencia pinnatijda as far as the South Basin of Lough Ine (Fig. 35). Thais ( =Nucella) lapillus (Fig. 36) is abundant intertidally on the open coast, but is found only in small numbers throughout Barloge Creek and sparsely a t a few stations within the lough. Subject to the occurrence of suitable food, its distribution appears to be largely determined by predators; the problem is discussed in Section VII.

2. Species Preferring Intermediate Stations Pucus serratus (Fig. 37) is absent both from the open coast and from much of Lough Ine, but occurs throughout Barloge Creek and the

230

J. A. KITCHING AND F. J. EBLINO

Rapids, penetrating as far as the south-east corner of the South Basin.

It occupies the lowest fucoid zone and is covered by the sea for most of the time. Clava squamata (Fig. 38) was found in 1955 only in or near the Rapids (though small quantities were found elsewhere in 1958), even though its substrate Ascophyllum is widely distributed.

3. Species Preferring Stations Remote from Open Sea The intertidal fucoid algae, Pelvetia canuliculata, Fucus vesicubsus, F . spiralis and Ascophyllum nodosum (Fig. 39), are common around the shores of the lough and extend southwards as far as Bullock Narrows, but are absent from exposed seaward stations. It might be supposed that these fucoids are unable to endure powerful water movements, though it has been demonstrated a t Port Erin that removal of Patella may lead a growth of fucoids on a shore where they wese previously very scarce (Jones, 1948; Southward, 1956). P. vulgata and P. aspera are both very abundant intertidally at Carrigathorna and on the south shore of Bullock Island; both species are much less abundant within the lough, and P. aspera is entirely sublittoral. Polysiphonia lanosa, Dynamena pumila, Dymmene bidentata, Flustrella hispida and Littorina littoralis (Fig. 40) are associated with Ascophyllum and are found a t nearly all the stations where Ascophyllum occurs; only Clava, as already mentioned, is more limited in distribution than its normal substrate. Gibbula umbilicalis and Hydrobia ulvae are likewise found everywhere in the area except on the exposed coast. Littorina littorea (Fig. 41), however, present in the lough and Rapids, does not extend farther south than Southern’s Bay. 4. Species Found in All Parts of the Area Relatively few intertidal forms were of general distribution. Ulva Zuctucu occurred nearly everywhere, including South Bullock, though not Carrigathorna. Littorina saxatilis was found at all thirty-three stations, and the barnacles Chthamalus stellatus and Belanus balanoides were widely distributed. The distribution of Patella spp. has already been mentioned and will be considered in detail in a separate section. Mytilus edulis is common a t Carrigathorna, but occurs spasmodically in Lough Ine, being abundant in the Goleen and on the north-east shore; the evidence that its distribution is limited by predators will be discussed later.

c. THE SUBLITTORAL FRINGE Two large brown algae are characteristic of the subIittoraI fringe namely Alaria esculenta and Himanthalia elongata. Alaria (Fig. 42) is almost confined to the full sea stations and appears to require exposure

ECOLOGICAL STUDIES AT LOUGH INE

231

to wave action. Himanthalia (Fig. 43) replaces Alaria towards increasing shelter and may perhaps compete with it in the entrance to Barloge Creek; the two species overlap along the south-west shore of Bullock Island. Himanthalia itself grows only very sparsely in the lough, and looks unhealthy except where it is washed by the inflowing tide; it is absent from the North Basin. I n stations of moderate wave exposure Gigantina stellata and Chondrus crispus form an undergrowth in the sublittoral fringe; at this level within Lough Ine and extending the length of Barloge Creek but not into open sea, the brown bubbly vesicles of Leathesia difformis and Colpmenia sinuosa are found on horizontal or gently sloping rock surfaces.

D.

THE SUBLITTORAL REGION

1. Species Preferring Open-sea and Intermediate Stations Along the open coast the upper margin of the Laminaria forest is formed by Laminaria digitata, which can escape undue exposure to air a t low tides by lying flat; below the reach of all tides, however, it cannot compete with the erect L. hyperborea (Etching, 1941). Both species penetrate the Bullock Narrows, and Saccorhiza polyschides (Fig. 44) penetrates slightly further. L. digitata and Saccorhiza polyschides reappear to form a dense forest in the Rapids, where L. hyperborea is very uncommon; it appears that the two species with flexible stipes are superior in current. I n contrast, L. saccharina is found a t sheltered stations from Bullock Narrows to the South Basin, but is absent from most of the North Basin, even though the area includes seemingly suitable substrates. Experimental transfers carried out by Dr. E. M. Burrows and Dr. T. Norton indicate that the sea urchin Paracentrotus, which is abundant along much of the shore of the North Basin, readily destroys Laminaria saccharina; other factors also may operate against this alga. The laminarian seaweeds form the chief substrate for Patina pellucida and an important one for two other gastropods, Calliostoma zizyphinum and Gibbula cineraria. Patina (Fig. 45) is found at all seaward stations and extends up Barloge Creek to the Rapids, where i t flourishes in moderate current. It is almost absent from the lough, though occasional specimens occur in the Castle Narrows. Calliostma has a similar type of distribution, but not Gibbula cineraria which is discussed below.

2. Species Preferring Stations Remote from the Open Sen The most conspicuous algae of the shallow sublittoral within the lough are Stilophora rhizodes (Fig. 46), Enteromorpha clathrata, and Codium fragile subsp. tomentosoides (Silva, 1955), although there are

232

J. A. KITCHINO AND F. J. EBLING

0

up to 10 per 1000 rq.crn.

(c)

FIG. 22. Distribution of the sea-anemones Metridium senile, CorynactiS

ViTidi8

Anthopleura ballii on boulders throughout: he Lough h e Rapids in July 1948.

and

ECOLOGICAL STUDIES AT LOUGH INE

233

Metridiurn senile

0 up to 10 per 1OM)sq.cm. Bottoms

Corynactis viridis

(4 Anthopleura ballii

FIG.22 (Continued.)

234

J. A. KITCHING A N D F. J. EBLINa

Cortazia costazii

o

5 colonies per lo00 rq.crn.

(4

0 up to 5 colonler per 1 ~ r q . r m .

(el

FIG.23. Distributionof the Polyzoa, Coatazia costazii, Scrupocdlaria reptam and Cdepora pumicosa on boulders throughout the Lough Ine Rapids in July 1950.

235

ECOLOQICAL STUDIES AT LOUQH INE

5 colonles per 1000 rq.cm.

Metres 50. P

0

0 up to 1%coverage Bottoms

0

Metres

0 u p to 5 colonies per 1Wtq.cm.

FIG.23. (Continued.)

236

J. A. KITCHINO AND F. J. EBLINQ

0

B 1-10

Metres

per 1OOOsq.cm.

(b) FIQ.24. Distribution of Mytilus edulb on boulders in the Lough Ine Rapids in July 1950

(a) FIO.25. Distribution of Sertularia operculata on boulders in the Lough Ine Rapids in July 1948.

237

ECOLOGICAL STUDIES AT LOUGH INE

0 Absent 0 u p to 1% coverage

\

(> 2-10%

0

Over lo0;

Bottoms

~

(b) FIQ.25. (Continued.)

Bottoms

(b) FIG.26. Distribution of Hippothoa hyalina on boulders in the Lough h e Rapids in July 1948.

238

J. A. KITCHING AND F. J. EBLING

Bottoms (b) FIG.27. Distribution of Tubularia bellis on boulders in the Lough Ine Rapids in July 1948. 0, absent; present.

a,

FIQ.28. Distribution of Bugula&bellata on boulders in the Lough Ine R.apids in July 1948. 0, absent; present.

a,

239

ECOLOGICAL STUDIES AT LOUGH INE

FXQ.28.

(b) (Continued.)

Tops

0 Up to 50 per 1000rq.crn. Bottoms

(b)

FIG.29. Distrihution of Verrum stroemin on boulders in the Lough Ine Rapids in July 1948.

FIQ.30. Distribution of Eschuroidea wccinew on boulders in the Lough Ine Rapids in July 1948.

FIQ.31. Distribution of Acmaea virginen on boulders in the Lougli Ine Rapids in July 1948. 0, absent; a, present.

MORES 100

0

IW

2oc JW

FIQ.32 FIQ.32. Distribution of Actink cquincc in July 1955. 0. abmnt; @, present. FIQ.33. Distribution of Littorim neritoidea in July 1955. 0 , absent; @, present. FIQ.34. Distribution of Lomentaria articulata in July 1955. 0 , absent; a,present.

FIQ.34

FIG.36

F I ~36 .

FIQ.37

FIQ.36. Distribution of Lauren& p*nn&i&ia in July 1966. 0. absent; @, present. FIO.36. Diatribution of Thcrie (NuocUa)ZupiUau in July 1966. 0. absent; 6, up.to 10 per 89. m; @. 11-100; 0 , over 100.

Wa. 87. Diatribution of F -

88-

in July 1066. 0. abeent;

e,up to 6 % ;

c). 8-25; 0 , over

26.

FIQ.38 FIG. 38. Distribution of Clava squamata in July 1955. 0, absent; @, present. FIG.39. Distribution of Aecophyllum nodoeum in July 1955. 0, absent; 0 , up to 25%; C , 26-50; 0 , over 50. FIG.40. Distribution of Littorim liltoralis in July 1955. 0, absent; @, present.

FIG.40

FIG.41 FIG.42 FIG.41. Distribution of LiUorinu Zittoreu in July 1955. 0.absent; a,present.

FIQ.43

FIG.42. Distribution of AZararia eacubntu in July 1956. 0 , absent; e, up t o 6%; 0 , 8-25; 0 , over 26. Eko. 4% Dineribution of H i m c m t h l i o

i n July 1066. 0 . absent;

e, up t o

6%;

.).

6 - 2 5 ; 0 , over 26.

l4-11:.

46

FIG.44. Distribut,ion of Succorhizrs polydidea in July 1955. 0, ahsent; 0 , up t o 5ue,,t.: 0 . few; m. modnratnly plentiful; m, ah-dant,.

Fru. 47. Distribution of Oibh.idn cineraria in July 1066. 0. nlxwlt:

ECOLOQICAL STUDIES AT LOUQH INE

247

FIQ.51. The distribution of Tubularia bellis on Saccorhiza plyschides in July 1951. Quantities as percentage area covered. For position of stations see Fig. 2.

'1

248

J. A. KITCHINQ AND F. J. ERLING

FIQ.63. The distribution of Patinu pellucid48 on the fronds, flats and frills of the stipe, and the holdfasts of Sacewhiza polyechidee in July 1951. Quantities are numbers of individuals. For position of stations see Fig. 2.

ECOLOGICAL STUDIES AT LOUOH INE

249

large fluctuations in the amount of Codium present in successive years. Stilophora is confined to the lough; it is a weakly anchored form and is probably unsuitable for open waters. Gibbula cineraria (Fig. 47) occurs throughout the lough and Barloge Creek on laminarian fronds, where these are present, and on the shallow bottom when they are not, though it is absent from laminarian fronds a t open sea stations. Caryophyllia smithi, Marthasterias glacialis, Asterinu gibbosa and Paracentrotus lividus (Fig. 48) also prefer the lough, but are not confined to it; occasional specimens of all these animals occur in Barloge Creek, and Paracentrotus has been found in rock pools just inside Carrigathorna. As a speculation it seems possible that Paracentrotus requires a combination of virtually permanent immersion with safety from powerful predators. This would be afforded in rock pools and sublittorally in certain landlocked areas (see Section VII). Paracentrotus is indeed common in rock pools on the west coast of Ireland. It has also been suggested by Southward and Crisp (1954) that high summer temperatures are necessary for breeding. There is, however, an additional problem in that it is almost absent from Great Britain.

3. Species Found in All Parts of the Area Asterias rubens (Fig. 49) and Hiatella arctica occur commonly, both in Lough Ine and on the open coast.

E.

W A V E ACTION I N COMPARISON WITH CURRENT

Of the three intertidal species, Porphym umbilicalis, Actinia equina and Littorinu neritoides, which prefer open sea stations and penetrate only to Bullock Narrows, none reappears in current in the Rapids. On the other hand, all of the twelve species which prefer stations remote from the sea and are not found outside of Bullock Narrows are present in the Rapids. Thus the littoral species treat the Rapids as sheltered. This one might expect, since there is little splash in the Rapids to protect vulnerable species from desiccation, and the current a t the bank exerts much less mechanical pull than do the Atlantic waves on an open shore. Two of the sublittoral species which do not penetrate beyond Bullock Narrows, namely Laminaria digitata and Saccmhiza polyschides, also occur abundantly in the Rapids. As already stated, the third open coast form, L. hyperborea, which is virtually absent &om the Rapids, may be unable to compete there because of its stiff stipe. On the other hand, of the species favouring the lough, only Marthasterias glacialis occurs in the Rapids, and Stilophora rhizodes, Caryophyllia smithi and Paracentrotus lividus are all absent. Moreover, three species which occur both

250

J. A. KITCHING AND F. J. EBLING

intertidally and sublittorally within Lough Ine, namely Asterina gibbosa, CaEium fragile, and Gibbula cineraria, appear to be restricted to the littoral region in the Rapids. Thus to a great extent, in the sublittoral region, the Rapids provide conditions similar to those on the open coast; in both places there is powerful water movement which not only exerts a direct mechanical effect but also prevents settlement of sediment and the establishment of local extremes of temperature and oxygen tension.

F. THE

F A U N A O F LAMINARIAN ALGAE

The laminarian algae which occur on the open coast and in the Rapids provide a substrate for several epiphytic algae and a number of sedentary animals. The distribution and abundance of the animals, especially Patina pellucida, within the Rapids area have been shown to be related to current (Section 111).I n order to make a comparison of the relative effects of wave action and current, the faunas of laminarian algae at six stations (Fig. 2) on the open coast, within Barloge Creek and in the Rapids were compared (Sloane et al., 1957). The features of these stations are summarized in Table 11. TABLEI1 Conditions of Current and Wave-Actionat Six Stations (Fig.2 ) Used for a Comparative Study of the Flora and Fauna of Luminarian. Algae Station

Current.

Wave-action

North Rapids Sill South Rapids Barloge Point Cave Island South Bullock

Fairly strong Very strong Moderate Very slight Slight but probably continuous Slight

None None Almost n0n.e Slight Moderate Strong

Seven species of sedentary animals occurred frequently on Baccorhiza polyschides, namely the hydroids Obelia geniculuta and Tubularia bellis, the Polyzoa Hippothoa hyalinu, Membranipora membranacea and Tubulipora sp., the tube-building amphipod Jassa falcata, and the gastropod Patina pellucida. For two species, Hippothoa hyalina (Fig. 50) and Tubulipora sp., distribution at the seaward station appears to be related to wave-action just as the distribution in the Rapids area is related to current. It is interesting that of the seven common species, these are the only two which prefer weaker currents. I n the Rapids area both these species are much less abundant on the Sill than at North or South

251

ECOLOGICAL STUDIES AT LOUQH INE

Rapids, and on the Sill both are mainly confined to the frills and holdfasts. At the seaward stations both show a progressive and drastic de crease towards the open coast, and both show a similar restriction towards the frills and holdfasts as they die out. Possibly water movements either prevent the settling of larvae or dislodge the settled organisms. Three species, namely Tubularia bellis (Fig. 5 l),Membranipora membranacea (Fig. 52), and Jassa falcata, had a marked preference for the Rapids area but were absent from, or sparse at, all the seaward stations. As these are all species which have been shown to favour moderate or strong currents within the Rapids area, it seems either that the favourable effects of current are not produced by wave-action or that there is another over-riding factor which causes these species to prefer the Rapids area. For instance, it is possible that the continuous current of the Rapids area provides unusually favourable feeding conditions or that physical or chemical conditions resulting from the outflow of lough water are more advantageous. One species, Patina pellucida, has been treated more fully (Fig. 53 and Table 111). Account has been taken of variations in algal frond weight, which has an approximately rectilinear relation to frond area. T A B L EI11 Distribution of Patina pellucida on Saccorhiza polyschides, Laminaria digitata and L. hyperborea in July 1951 Number of plants

- -

Number of RegresPatina per plant sion coeffiMean Range Mean cient

Frond weight

(€9

Range

Standard error

~

Saccorh iza polyschides North Rapids Sill South Rapids Barloge Point Cave Island South Bullock

25 26 28 28 37 21

Laminaria digitata Sill 28 South Bullock 21

L. hyperborea Barloge Point South Bullock

21 12

735 60-2040 78-1 870 584 280-3400 1193 632 150-1800 134 10- 740 70- 900 423

1- 39 0- 10 0-264 8-180 0-829 6-621

14.5 2.7 118.7 60.6 264.3 212.1

0.0106 0.0024 0'0667 0.0767 1.0229 0.3145

0.0034 0.0026 0.0170 0.0136 0.1541 0.1430

50- 740 15- 400

357 161

0- 2 0- 33

0.2 10.3

0.0141

0.0205

220-1000 35- 480

585 269

8- 82 4- 75

37.7 30.4

0.0646 0.0202

0.0185 0.0419

252

J. A. KITCHING AND F. J. EBLING

Saccorhiza in fast current on the Sill is remarkably elongated (Ebling and Kitching, 1950), but this does not seriously affect this relation. Our information is summarized in Table 111. Patina pellucida had a marked preference for South Rapids and the three seaward stations to North Rapids and the Sill. The results confirm a previous conclusion (Section I V ) that in the Rapids area Patina prefers a moderate current. They add, however, the important fact that the numbers of Patina were much greater at South Rapids and a t all the seaward stations than a t North Rapids or the Sill. The greatest numbers were at Cave Island, so that moderate wave-action appears to favour Patina in the sea, just as moderate current does in the upper Rapids, but it also appears that some additional adverse factor supervenes from the Sill northwards. It is possible only to speculate what this may be. For instance, the current flows almost continuously on the Sill and at North Rapids, whereas a t South Rapids there are much longer periods of relatively quiet water with slow turbulent movement rather than continuous flow. Thus the opportunities for the settlement of Patina may be much more restricted at North Rapids and the Sill than anywhere else. The fronds of Succorhim proved a more favourable substratum for Patina than either Laminaria digitata or L. hyperborea (Table 111).

VI. ZONATION A. I N T R O D U C T I O N Restriction of each species to its own zone, extending horizontally a t a characteristic level, is the principal and most widely observed feature of the distribution of plants and animals in the tidal zone. The period of exposure to air is the obvious primary environmental cause of such zonation, though wave-action, substrate, aspect, climatic conditions, the time of low water of spring tides, and miscellaneous biological interactions may all be modifying factors (Lewis, 1964). Zonation continues below the limits of the lowest tides. I n the shallow sublittoral the intensity and quality of light change with depth, and there is no doubt that illumination is of cardinal importance in the distribution of algae. The decrease in water movement due to waveaction may also be important. For instance, the upper limit of Laminuria. sacchurina in the Sound of Jura is depressed by increased wave-action (Kitching, 1941), and this relationship has been confirmed by Kain (1962). As wave-action and current lessen, the bottom deposit also increases in amount and the quality may change. Many other factors may play a part. The existence during summer of a thermocline within Lough Ine involves the establishment between a depth of 20 and 30 ni of gradients of oxygen concentration and pH as well as of temperature.

ECOLOGICAL STUDIES AT LOUGH INE

253

Biotic factors may also be of great importance in determining sublittoral distribution. For example, in Lough Ine predation by crabs may determine the lower limits of Mytilus edulis (Section VII), and Herring Gulls may prevent the establishment of large Marthasterias glacialis in water less than 1 m deep and thus permit the survival of Anomia (Section VIII). Problems of littoral zonation (reviewedby Lewis, 1964) have received much attention from others; they have not formed any major part of our studies a t Lough h e . Nevertheless certain problems of particular relevance to the locality have interested us. We have, for example, made detailed observations on the comparative zonation and characteristics of Patella species within and without the lough which also have some taxonomic interest arising from the interplay of environmental and genotypic characters. We are now studying the distribution of organisms in the Western Trough in relation to the thermocline and chemocline.

B.

THE DISTRIBUTION A N D CHARACTERISTICS O F P A T E L L A SPECIES

1. Zonation Of the three species of Patella found in the British Isles, only two, namely P. vulgata L. and P . aspera. Lamarck, occur in the Lough Ine area or, indeed, anywhere on the Irish coast (Southward and Crisp, 1954; Crisp and Southward, 1958). Both these species are abundant on the open coast of Carrigathorna, and occur somewhat more sparsely throughout Barloge Creek and within Lough Ine (Ebling et al., 1962). We have made a detailed study of the limpet population of a section of coast exposed to the full tidal range and severe wave-action at Carrigathorna, and compared with it the population in Lough h e , where the tidal range is contracted and splash is negligible. The relative proportions of Patella vulgata and Patella aspera were determined from adequate samples at different levels in a section a t Carrigathorna and are shown diagrammatically in Fig. 54. Limpets were distributed fairly evenly throughout the intertidal region, although occasional specimens occurred above our highest sample in crevices and gullies outside the limits of the section. Samples were also taken from two rock pools at the level of the uppermost band. It is evident that P. aspera is t,he dominant species throughout the intertidal region, extending up to but not beyond high water of spring tides. P. vulgata exclusively occupies a narrow belt above this level, but below it forms only a minor constituent of the limaet population. In rock pools about 1 m above high-water mark the two species occur together in roughly equal proportions. These observations put the limits

J. A. KITCHING AND F. J. EBLING

254 METRE5

I

1E m

m

G 1H

-

1I

PATELLA 0 1 METRES

L I

2

3

*

VULGATA

0

5

PATELLA

ASRRA

FIG.54. Section at Carrigathorna showing tho relative proportions of Patella wulgata and P . aspern at different shore levels. The arrows show the approximate levels of high and low water on 20 July 1959, giving a tidal range of 3.9 m for a spring tide with a forecast height of 3-35 m at Baltimore.

of P. vulgata and the upper limit of P. aspera higher than those reported from elsewhere (Evans, 1947; Southward, 1953; Southward and Crisp, 1954; Southward and Orton, 1954). We ascribe the high limits of both species a t Carrigathorna to extreme wave-action. The vertical distribution of limpets within Lough Ine is exemplified in a section made at North Wall (Fig. 55) in September 1959, and the conclusions are supported by records for other parts of the north and

*90cm

]*m

......................

0

METRES

1

2

FIQ.55. Section at North Wall, Lough Ine (see Fig. 67), showing relative proportions of Patella vulgata and P. aspera at different levels, based on a sample of 105 limpets taken in September 1959. The maximum density was at 40-50 cm above standard level. Standard level is approximately that of low water; the level of high water is about 90 em higher, and this is exceeded at spring tides.

ECOLOGICAL STUDIES AT LOUGH I N E

255

south basins. P . vulgata does not occur above an average high water and is virtually the only intertidal species; P . aspera is almost confined to the sublittoral; the highest specimens recorded, in the South Basin, would have been exposed to air only a t low water of neap tides (which within the lough is lower than low water of spring tides). We have also found P . aspera on sublittoral rocks surrounded by mud; unless they can cross mud, they must have spent their whole lives below water. Distribution in the Rapids is much as in the lough. P . vulgata extends down to low water and very occasionally below it. P . aspera occurs on sublittoral boulders on the Sill.

2. Variation in Relation to Level and Habitat (a) Specijic characters. Both species of Patella are widely variable, and we examined a number of characteristics to see whether there were any consistent correlations with environment. Certain features, among which are the shape of the radula teeth and the nature of the marginal tentacles, are species diagnostic, as described by Fischer-Piette (1935). To these may be added the internal appearance of the shell which shows, when not obscured by nacre, a grey or white head scar with orangeyellow radiating ribs in P . vulgata, and an orange head scar with white or pale straw ribs in P . aspera. Nacre increases with size in both species, more quickly in P . aspera, to hide the original colour. It would be particularly interesting to know what are the relative advantages - if any - of these specific characters. For instance, differences in the structure of the radula might be associated with differences in the food at different levels on the shore. (b) Radula length. Other features, while having a species-characteristic component, also show varying degrees of environmental modification. Most important of these is the radula length. As radula length depends on the size of the limpet, the ratio radula length/shell length (termed the ‘radula ratio’) is frequently used for comparative purposes (FischerPiette, 1955). This is not entirely satisfactory for a critical evaluation of our samples because though the regressions of radula length on shell length are approximately rectilinear they do not for either species a t any level pass through zero. By analysis of covariance we have been able to show that, for each species, radula length, after correction for shell length, tends to decrease as level decreases, although the corrected mean radula length for P . vulgata is substantially greater than that for P . aspera a t all levels (see also Brian and Owen, 1952). The mean radula ratio for P . vulgata ranged from 1.66 at its highest level (A) to 1.30 a t its lowest level (G), and that for P . aspera from 1.17-at level E to 0.93 at level I ; individual values overlap for the two species, as already noted by earlier workers. I**

260

J. A. KITCHING AND F. J . EBLING

As on the open coast, the relative radula length of P. vulgata within Lough Ine decreases with decreasing level. The values of the radula ratio for P. mpera are very low, although a comparison between Lough Ine and Carrigathorna is complicated by a difference in range of shell length; the means for samples taken within Lough Ine run from 0.82 to 0.90. It remains to be seen whether this is related to longer periods of feeding associated with permanent immersion. (c) Foot colour. Foot colour appears to have two components, dark pigment which is species-characteristic, and orange pigment which appears to be environmentally acquired in relation to locality and level. P. vulgata has more dark pigment than P. aspera; thus in rock pools at Carrigathorna, where neither species has orange pigment, the foot of P. vulgata is dark grey and that of P. aspera white or pale grey. On open rock a t Carrigathorna P. vulgata has a foot of ochre or of a mixture of grey and orange; orange tends to increase towards the bottom of its zone. The foot of P. aspera has less grey colour. Towards the bottom of the zone a t Carrigathorna it becomes a clear orange; within Lough Ine and the Rapids it ranges from cream to apricot. We suspect a connection with food. (d) Shell form. The relative height of the shell is almost entirely related to level. The lower it is on the shore the more depressed is the shell, but there are no significant differences between the species at any one level. Within Lough Ine, sublittoral P. aspera has an extremely depressed and crenulated shell, as though a continuous state of relaxation allows the mantle margin to extend until it becomes wavy. On the Sill the shell is relatively taller, but is nevertheless substantially more flattened than on the open coast. It seems probable, therefore, that while exposure to air is the main environmental feature affecting tallness of the shell, exposure to wave-action and current also have some effect.

c. SUBLITTORAL DISTRIBUTION I N THE LOUGH We are at present only a t an early stage in the investigation of changes in the fauna and flora with increasing depth in the lough. The problem concerns not only the macroscopic benthos but also microscopic organisms such as diatoms on the surface of the mud and bacteria upon and within it. We cannot yet discuss the vertical distribution of algae in relation to illumination. The outstanding characteristic of the lough is the discontinuity -in summer - of temperature and of various chemical conditions at around 25 m. We have laid crab traps a t a range of depths leading down into

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the Western Trough, and we have failed to catch crabs below 25 m, although Carcinus and Portunus arcuatus occur where the bottom is not so deep. Portunus arcuutus extends down to 20 m over a muddy bottom apparently comparable in texture with that in the Trough. When this crab was placed in cages on the bottom below the thermocline, in experiments carried out in 1965 by Miss Jancis Betney, it became inert or died within 24 h, although when placed on the bottom above the thermocline it appeared unharmed. The most probable explanation is in terms of oxygen concentration, although confirmation is wanted by means of experiments in the laboratory. So far we have not found any animals below the thermocline in the Western Trough, although much more investigation is needed. The polychaete Pectinaria belgica, the decapod Calocaris macandreae and Priapulus caudatus (all found by Mr. John Heath and Mr. Colin Irwin while diving) extend to about that level. VII. PREDATION AND GRAZINQ A. INTRODUCTION The importance of predation in determining the distribution of marine organisms first became apparent from our studies on the mussel Mytilus edulis. The distribution of mussels presents a problem, since they occur plentifully only in what appear to be widely separated ecological sites, for example, on beds in the sheltered mouths of estuaries, on open rocky coasts exposed to wave-action, and generally on poles and other vertical surfaces. We were able t o show that mussels rapidly disappear when transplanted to sites where they are normally scarce, even though they readily survive when they are protected in cages. In such sites crabs were seen eating the mussels. The ability of crabs to break mussels was tested by placing the animals together in cages, and the feeding of crabs was observed in the aquarium. Finally, careful surveys by several methods of the occurrence of crabs showed that the distribution of competent predators was inversely related to that of mussels. The sea urchin Parmentrotus lividus also has two habitats in Ireland: intertidal rock pools along much of the west coast and the shallow sublittoral in certain sheltered localities. I n the Lough Ine area it occurs in small numbers in rock pools around Carrigathorna, and abundantly within the lough. The rock pool habitat is better exemplified in Connemara. Investigations similar to those described for Mytilus have created a chain of circumstantial evidence to explain the distribution of Paracentrotus in relation to its predators within Lough Ine. Moreover, it appeared that areas where Paracentrotus was plentiful were practically

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J. A. KITCHING AND F. J. EBLING

free from algae, whereas algae were abundant in areas where urchins were less plentiful. We were able to show that algal growth is limited by the grazing of Paracentrotus. Finally, during a study of the relationship of T h i s (Nucella)to its predators, we recognized the existence of two forms, one more resistant to predation and the other better able to adhere to wave-washed rocks.

B.

MYTILUS EDULIS

1. Distribution The distribution of mussels in the Lough Ine area resembles that in other places. Small mussels are abundant on the exposed Atlantic coast, where there is a continuous intertidal belt. Within Lough Ine mussels occur sparsely, except at the north end of the lough and in the Goleen; these populations, also intertidal, include many large specimens (Fig. 56). Mussels also occur sublittorally on the Sill in the Rapids, although their numbers fluctuate considerably from year to year. Straight and hooked forms (corresponding respectively to M . edulis L. and M . galloprowincialis Lmk. of Hepper (1957), though not, according to Lewis and Powell (1961), of two different species) are found in all these sites.

2. Transplantation Experiments The ability of Mytilus to survive a t various levels from the upper littoral to the shallow sublittoral in various parts of the Lough Ine area (Fig. 2) was tested by experiments involving small mussels from Carrigathorna and mainly large mussels from the north end of the lough (Kitching et al., 1959). Pieces of rock with Mytilus attached were removed from the shore with hammer and chisel, and after storage for about 24 h in an open crate in the shallow sublittoral were cemented with a quick setting mixture into their new positions. A t Carrigathorna, where there is severe wave-action, they were fixed to a 50-kg concrete block which was placed in a shallow depression in the Mytilus zone. Small mussels disappeared quickly from all stations except the open coast a t Carrigathorna (Figs. 57 and 58). Except a t the highest, levels, they all remained alive and appeared healthy up to the time of their disappearance. Undoubtedly they fell victim to predators; in general, those higher up survived longer, which suggests that the predators were mainly or entirely marine. Mussels placed in the Pelwetia zone, however, died, gaped and eventually were broken up, probably by birds. The small mussels replaced a t Carrigathorna survived much better than those transferred from there to other stations. Large mussels (from the north end of the lough) disappeared fairly quickly from all lough stations except in extreme shelter a t East Goleen

259

ECOLOGICAL STUDIES A T LOUGH INE

METRES

100

0

100

200

300

400

FIG.66. Distribution of Mytilus edulis in July 3955. plentiful; 0 , abundant.

0, absent; f), few; a, moderately

2G0

J. A. KITCHING AND F. J . EBLING

Mytilur from N end of Lough Ine

Mytilus from Carrigathorna

D(70)

.....

,_..... ....... .................

.'....

%,*

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30-

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20-

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10-

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3

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4

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14

Date

FIG.66. Survival of unprotected Thais ( N u c d l a ) in the Goleen. Fifty Thai8 of the Rapids type (0) and fifty of the Carrigathorna type ( 0 )mere .irt up for the start. of the experiment on 2 August, 1965.

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J. A . KITCHING AND P. J. EBLINQ

broken shells were found, and there is little doubt that Carcinus was responsible for this. We do not know whether Carcinus accounted for all the losses; it is possible that it may have carried off shells which it could not break open.

7. Conclusions Our results show that crabs selectively destroy Thais of the opencoast type in cages, and that water currents selectively remove Thais of the sheltered-coast type under experimental conditions of fast flow. When Thais of both types are transferred to either natural habitat, selection occurs in the expected direction with an intensity which would be sufficient to account for the suppression of the inappropriate type, should it occur. Moreover, there is evidence to show that the selective agents operating are, in fact, wave-action and predation. Our interpretation may be somewhat oversimplified in that it does not take account of possible differences in behaviour of the two types of Thais. Nevertheless we believe that we have substantially demonstrated the significance of these two types for survival. We do not know to what extent the existence of two types of Thais in the Lough Ine area depends on environmental modification of the developing organism, and to what extent the differences are genetic. Abundance of food, easily obtained, might produce a more rapid growth of the soft tissues in relation to the deposition of shell material. Nevertheless, the lack of a planktonic larval stage could encourage the establishment of local genetic types, and studies of chromosomes carried out by Staiger (1957) lend support to this interpretation. We think that it is the more likely explanation. We are a t present examining the region of transition between open coast and shelter, and we are undertaking studies 011 the growth of transferred individuals.

D. P A I t A CEN TI2 0T U S A N D P R E D A T O R Y C R A B S Paracentrotus lividus is common throughout Lough Ine, though it is more plentiful in areas of the North Basin than in the South Basin. During July 1962 all the boulders within a small selected area of the shallow sublittoral were removed and examined at each of seven stations in the lough (Muntz et al., 1965). The numbers of Paracentrotus per square metre at each of these stations are shown in Fig. 67. Small Paracentrotus, up to 10 or 25 cm diameter, were abundant on the bottom surfaces of upper layer boulders around the margins of the lough. Large Paracentrotus, up to 55 mm diameter, were found on the open sea bed only at North Wall and in Curlew Bay (Fig. 69), although they occurred in large crevices under boulders in the South Basin. One

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West

21

METRES

i00

0

100

200

300

FIG. 67. Population, as numbers per square metre, of Paracentrotus lividus at Seven stations in Lough h e in July 1962.

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276

possible explanation of this distribution is that larvae settle over the whole lough and that small Paracentrotus are able to survive as long as they are sheltered from predators underneath boulders. According to this view, emergence and subsequent growth were only possible in the North Basin, because in the South Basin the urchins were subject t o predation. We must admit, however, that there is another possibility, namely that the numerous small Paracentrotus resulted from an unusually successful settlement. I n order to test the first hypothesis, we investigated the ability of crabs to damage Paracentrotus. Individuals of various sizes of the three most important species of crabs (see p. 281) -Carcinus maenas, Portunus puber and Cancer pagurusm were tested in cages with batches of Paracentrotus of progressively increasing diameter. A period of three days was allowed with any one batch of Paracentrotus, and if the crab failed to break open any in that time, the test was considered to have reached end-point. Tests showed that end-point was not due to satiation. The largest Parmentrotus (by horizontal diameter) broken open by each crab is plotted against carapace diameter in Fig. 68. An arrow signifies

-

t 60-

A

v

C

dk 50II)

E

0

5 40-

A

c 4“

O ! 0

I

I

i

100 Width of carapace of crab (rnm)

150

200

FIG.68. Predation of crabs on Paraoentrotw, lividw in “progressive” tests in cages. The results show the largest Paracentrotw eaten against width of carapace of the crab. Arrows indicate thet the upper limit for the crab was not reached. Carcinus m e n a 8 ( 0 , a central point indicates two coincident results; a central point end a tag indicates three coincident results); Pmtunus puber (a);Cancer pagurus (A).

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that it was not possible to reach end-point in the test, either for lack of time, or, for some tests with Cancer, because the crab destroyed the largest Paracentrotus available. Carcinus, up to 6&60 mm carapace width, were able to destroy only very small Paracentrotus of 1&20 mm diameter, and some crabs failed to damage any at all. Portunus puber (up to 115 mm) destroyed Paracentrotus mare readily and up to 60 mm in diameter. Cancer of very moderate size (143 mm) destroyed Paracentrotus of the largest size available, even two in one night. One large Cancer destroyed eleven Paracentrotus in seven nights. The height of Paracentrotus is about one half its horizontal diameter. An analysis of all the measurements of shell diameter and shell height in centimetres gave the relation D = 1.93 H + 0.02, the constant having no significance. From measurements of the maximum gap of the chelae of all the test crabs it is evident that crabs can destroy Paracentrotus of a height greater than would fit within the tips of either chela. The predatory behaviour of five male Porturms puber (78-84 mm) was observed in running sea water in the Dromadoon Laboratory. On a number of occasions Paracentrotus small enough to be gripped within the chelae were quickly crushed and consumed except for spines and shell fkagments. Paracentrotus greater in height than the gaps of either chela were attacked on several occasions, and spines were broken off. I n one case the crab (the most aggressive of the five) pulled the Paracentrotus free, broke off a number of spines, and finally broke through the oral surface by pressing its chelae downwards into the upturned Paracentrotus. It proceeded to enlarge the hole with its right chela and was no longer disturbed by torchlight. A small Cancer pagurus (a 56 mm male) was observed to break up and clean out a Paracentrotus in the same way. I n several experiments a number of large Paracentrotus were collected in the North Basin and transported under water to sites in the South Basin. The transplanted Paracentrotus quickly diminished in numbers, no doubt partly because they walked away. Nevertheless, small groups of spines and pieces of broken shells showed that some had fallen victim to predators. Finally, attempts were made to identify the predators in two further experiments. I n one, carried out on 24 August 1963, one hundred large Paracentrotus were put in Renouf's Bay, one hundred off Harbour Wall, and eighty off Mermaid Rock, east of Glanna€eenBeach. A large Cancer was seen to eat one Paracentrotus and attack another off "Harbour Wall, and a Portunus puber was seen on the site at both Renouf's Bay and Mermaid Rock, though neither was seen to attack. I n the final transfer,

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in which twenty fairly large Paracentrotus ( 5 6 5 5 mm) and twenty smaller ones (30-35 mm) were deposited in a cleared area off Harbour Wall, the site was examined every 5 min for 12 h, including the whole night. Portunus puber destroyed four of the smaller Paracentrotus. A determined attack on a larger specimen failed, with no more damage to the Paracentrotus than the loss of some spines - a result in accord with the experiments on predation in cages.

E. P A R A C E N T R O T U S A N D ALGAE The most extensive beds of Paracentrotus are along the north shore of the lough, and on the north side of Castle Island. Most of these areas are practically free from obvious algal growth, whereas algae are abundant in places where Paracentrotus is less plentiful (Kitching and Ebling, 1961). During the summer of 1950 the innermost part of Curlew Bay, near the shore, was well populated by Paracentrotus and practically clear of algae. In the slightly deeper water, however, there was a very dense covering of algae, mainly Enteromorpha clathrata, but including also some Ceramium spp., Ectocarpus conferroides, Chlyocladia verticillata, Polysiphonia, and others. The boundary of this dense weed cover in that year is shown in Fig. 69. The population of Paracentrotus in relation to the occurrence of algae and the nature of the bottom was examined in a series of metre squares along each of two sections running out northwards into the bay from shore marks. As will be seen from Fig. 70, Paracentrotus stops where dense algal cover begins. On 7 July 1959, an area of Curlew Bay amounting to nearly 300 sq. m was completely cleared of Paracentrotus (Fig. 69); in all, 1 9 5 7 sea urchins were removed. By 23 July, the cleared area was about 10% covered by algae, by 10 August it had risen to 25%, and by 3 September to 50%, but the dry weight of alga/sq. m was much less than in the part of the bay normally dominated by Enteromorpha. Parts of the bay still occupied by Paracentrotus continued practically free of weed. The boundary between the Paracentrotus-freed sector and the uncleared areas on either side of it became irregular, but apart from this the Paracentrotus-freed sector remained completely clear throughout the summer. I n early July 1960, the area cleared of Paracentrotus in the previous year was thickly and completely covered with Enteromorpha and other algae. The area to the west, well populated by Parucentrotus, remained free of weed, but the area to the east of the cleared area, previously free of algal cover, carried some large dense patches of algae. The Paracentrotus collected during clearance of the area were transported to various sites in the lough. On 7 July 1959, 1 3 2 6 Paracentrotus were dropped in an elongated heap on the western section in

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FIG.69. Curlew Bay, showing the distribution of algal c o w r a i d the po4tion of the sector cleared of Pnrcccentrotitn in July 1959.

FIQ.70. Diagrams of the section at J and K (Fig. 6 9 ) showing (a)the number of P a w centrotus per square metre, (b) the percentage coverage of the bottom with algae, (c) the bottom profile, (d) the nature of the bottom expressed as the percentage area covered with boulders, gravel, or mud. Throughout the sections a t J t,he bottom consisted of shell gravel resting on mud.

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J. A. KITCHING A N D F. J. EBLING

Curlew Bay (Fig. 69), in an area densely covered with algae. On 15 July , the the Paracentrotus occupied an irregular area about 6 x 2 n ~ with central patch eaten clear; all appeared healthy. By 10 dugust the area had increased to about 6 m x 33 m; most of the Paracentrotus were around the edge of the area in contact with Enteromorphu (Fig. 71). A year later a wide area around the section, which had been covered with Enteromorpha in 1959, mas now free of weed and well populated with Pnrucentrotus.

FIG.7 1 . The distribution of Parace,rtro/its at transfer station K on 10 August 1959. Only one end of the oval patch is reprewnted. The positions of the Paracent+-ott~s have been traced from a colour photograph.

Smaller groups of Paracentrotus transferred to the middle of the Goleeii and to a site near its west shore also cleared areas of weed. Those near the shore disappeared but a few in the middle of the Goleen survived to July 1960. There is no doubt that in Lough Ine Paracentrotus grazes predominantly on algae; gut contents have been found to consist almost entirely of algal remains, though in one specimen a few copepod exoskeletons were found. To test the grazing capacity of Paracentrotus, we covered the floors of six galvanized wire cages, 32 x 64 x 43 em, with rocks and shells free from obvious algal growth. Six large Paracentrotus were put into one cage, three into a second, one into the third and none into the others. Two months later the cages were lifted for examination. I n the three cages without Paracentrotus the rocks and shells were lOOyo covered with algae. There was 33%-50y0 coverage in the cage with one

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Paracentrotus, about 30% in the cage with three Paracentrotus, and no growth of macroscopic algae in the cage with six Paracentrotus. These observations establish that there is an inverse correlation between the occurrence of Paracentrotus and algae. The field experiments involving clearance and transfer of Paracentrotus and the experiments with cages suggest that this inverse relationship in distribution arises because Paracentrotus destroys algae as fast as they grow. Examination of the sedentary fauna of Curlew Bay shows that the grazing activity of Paracentrotus also prevents the establishment of other parts of the fauna especially associated with algae, namely the gastropods Rissoa parva and Bittium reticulaturn, and the amphipod Caprella acanthifera.

F.

DISTRIBUTION O F CRABS

We have already seen that the distribution of intertidal mussels in a limited area of Lough Ine is negatively correlated with the distribution of certain crabs, and our observations and experiments on Thais and on Paracentrotus have suggested that crabs may play a similar part in determining their distribution. A necessary link in our chain of evidence is a knowledge of the distribution of crabs. We have investigated this in four ways (Muntz et al., 1965). First, we have used beds of intact or crushed mussels as ground bait at various selected stations and we have observed the visitors with a view box; second, we have fished from a rowing boat a t night, luring the crabs out of their crevices by dangling a crushed mussel on a string; third, skin diving has been carried out by day in a limited number of places; fourth, traps have been laid. The traps were of conventional design, but made of mesh polythene, and were baited with fresh fish, crushed mussels or tinned fish cat food. They were always put down in the afternoon well before dusk and taken up on the following morning long after dawn. The results of trapping are shown in Fig. ' i d ; these distributions are confirmed by the other methods which we used. C'arcinus maenas is common intertidally all around the lough. It is abundant sublittorally close inshore in the North Basin and in the Goleen. It is common intertidally among rocks at Harbour, but seems to be scarce sublittorally in the south-east corner of the lough. Portunus puber is not found anywhere in large numbers, but occasional specimens are taken in shallow water in many parts of the lough, and the crab was regularly found in small numbers at all stations in the south-east corner of the South Basin, where the Rapids join the lough. It is abundant in Barloge Creek, which possibly acts as a source of replenishment for the lough. Portunus puber is virtually absent from three much studied areas, namely North Wall, the Goleen, and the inner part of Curlew Bay. E

METRES 100

3

100

zoo 100

100

FIG.72. Total catch of crabs in eight pots placed overnight at each of twenty stations in July or August 1963. At seven stations pots were laid b0t.h in July and in August; the letter A indicates August. (a)Curcinus maenaa; (b) Portunus puber; (c) P . wrcuatus.

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Cancer p q u r u s L. is distributed much as Portunus puber but is apparently less common. It is fairly easily found in the south-east corner of the South Basin, and is seen sporadically in the lough, but not at North Wall or in the inner part of Curlew Bay or in the Goleen. Portunus arcuatus Leach is common all around the lough, but is found mainly on or near a muddy bottom. Portunus corrugatus, also abundant in Barloge Creek, has been found a little way offshore in Curlew Bay and North Wall, on a muddy bottom or on weed over mud (but was very local). Portunus depurator has not been seen in the shallow sublittoral, although it has been trapped in the middle of the South Basin. Maia squinado has been seen in the North Basin and a t the north end of the Rapide, but is not a t all common. Xantho incisus is widely distributed but not common; Xantho hydrophilus is even less common. Homarus vulgaris has been seen and captured occasionally, mainly in the Rapids area. The most important decapod predators in the shallow rocky sublittoral, which are powerful enough to break open prey protected by shells or tests, are thus probably Cancer pagurus, Portunus puber and Carcinus m e n a s . The eastern part of the South Basin, i.e. that part which is washed by the great vortex set up by the incoming tide, differs from the rest of the lough in the more frequent occurrence of the large crabs Cancer pagurus and Portunus puber. G. CONCLIJSIONS It is extremely difficult to be sure that the absence of an organism from any site is due to the activity of any particular predator. The fact that a predator can damage an animal under experimental conditions in cages or that it can be seen to do so in the laboratory does not establish that this is a normal event in the sea, where the chances of encounter may be very much less. Moreover, such an experiment takes no account of possible behavioural interactions between different predators, or between predators and other species which are not directly involved in the predator-prey relationship. Similarly the demise of an animal after transplantation is a contrived event, although there is a closer approach to natural conditions in such an experiment. A normal absence from che site in question, coupled with destruction on transplantation to it, does not in itself show that the predator concerned is the normal cause of the failure of the prey to establish itself there. This failure could be due to a variety of causes, biotic or otherwise, acting upon the younger stages. Equally, the survival of a mature sedentary animal after transplantation does not prove that it could have developed in situ. Nevertheless, if evidence from experiments on predation in cages and

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from transplantation is combined with a clear demonstration of an inverse correlation in distribution between predator and prey, it is a reasonable hypothesis that such a predator-prey relationship exists in nature. To support such a proposal, we suggest that the following criteria need to be fulfilled: (a) the organism does not survive when transplanted to a site where it does not normally occur, unless it is protected from predators by cages. (b) there is an inverse correlation between the distribution of the organisms and the suspected predator, or alternatively, in the places where it occurs the organism is inaccessible to the predator. (c) the suspected predator is able to inflict lethal damage on the prey in experiments in cages, or can be observed to do so in the laboratory. (d) there is direct evidence that the suspected predator is responsible for destruction of the prey in transplantation experiments. Our experiments on Nytilus, Paracentrotus and Thais have fulfilled all, or nearly all, of these conditions. There remains the possibility that in nature these organisms may fail, for quite different reasons, to develop in the situations from which they are missing, so that the opportunity for predation does not occur. Successful survival of a species in spite of predation does not require complete immunity for every individual. Production of a shell strong enough to guarantee survival of all individuals would involve other overriding disadvantages. All that is required is a sporting chance of survival. For this reason there are likely to be fluctuations both in time and space in the balance between predators and prey. This aspect of the relationship will be developed, for Paracentrotus, in Section VIII.

VIII. SYNECOLOGY As in other areas, it is possible to recognize a t Lough Ine a number of communities of animals and plants, each in its characteristic habitat. Naturally these communities are subject to local variation. It is the aim of an ecologist to describe the system of food chains which operates in each of these communities, to elucidate any changes, whether cyclical or casual, in the populations of organisms within these communities, and ultimately to describe the interactions of different species in quantitative terms. This last objective requires information as to the feeding, growth, reproduction, and mortality, of all the important members of a community over a range of conditions corresponding to those normally experienced throughout the year in the area under consideration. At present we do not know nearly enough about these matters, although

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we hope that in the end we shall be able to treat quantitatively at least one community at Lough Ine. So far we are only in a position to make qualitative suggestions about the food chains of the Paracentrotusdominated community of the shallow sublittoral, and to describe diurnal migrations which probably play an important part in controlling encounters with predators. A full account of this work is published elsewhere (Ebling et al., 1966). The ultimate source of food for the Paracentrotus community consists of algae growing upon the rocks and eaten by grazing animals, and of plankton eaten by filter feeders. The most important grazers are Paracentrotus and Gibbula cineraria, of which Paracentrotus undoubtedly determines the character of the community. It maintains the rock bare of algae by its constant grazing, and from observations of Paracentrotus transferred to new sites we infer that it spreads as far as is necessary for it to maintain itself on regenerating algal growth in the occupied area, supplemented by virgin growth cropped around the margins. The chief filter feeders are Anornia and Chlamys varia; both are plentiful in shallow areas of the North Basin, but the former is by far the more important. Small specimens of the starfish Marthasterias and Asterias reside within the Paracentrotus community in certain areas. They are found especially on shores which slope steeply and are heaped with boulders, including most of the areas newly dominated by Paracentrotus in 1964 (see below). The larger specimens of these starfish do not, within our experience, come up into the Paracentrotus community. The shore crab Carcinus inhabits the community in the North Basin, and Portunus puber and (less frequently) Cancer pagurus visit it mainly in the South Basin. Birds destroy some Paracentrotus and remove starfish in the shallowest part of the Paracentrotus-dominated areas. From the local abundance of Anoinia in areas of the North Basin free from starfish, it is likely that in the South Basin the numbers of Anomia are, in fact, controlled by predators and not by the supply of planktonic food. Similarly, from the density of Paracentrotus and Gibbula in shallow parts of the North Basin, where abundant algae surround the Paracentrotus-dominated areas, we may infer that food supply does not limit the population of grazers. Thus the numbers of these grazers are probably controlled by predators. The fragile young Paracentrotus develop under boulders around the margins of the lough, where presumably they find relative safety from predators. We believe that as they grow they emerge and spread downwards as far as their food requirements make necessary and predators permit. The larger they grow, the less vulnerable they become, but in venturing deeper they may expose themselves to greater danger. Areas dominated by Paracentrotus are almost bare of animal and plant

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growth. Paracentrotus is omnivorous, and its effect must be to eliminate a number of species from the community. I n so far as Paracentrotus is itself controlled by crabs and other predators, these predators must encourage the growth of algae and their associated fauna. It is interesting that another carnivore, the Pacific Starfish Pisaster ochraceus, is believed to encourage diversity of species within its community. According to Paine (1966), Pisaster reduces the competition for space, so that species survive which would otherwise be crowded out. Important constituents of the Paracentrotus community make diurnal migrations (Figs. 73 and 74). Paracentrotus and Gibbula cineraria come

FIG.73. Numbers of Paracentrotus and Marlhasterias visible in defined areas amounting to about 20 sq. m on the south shore of Lough Ine from 2 August to 4 August 1965, with parallel records of weather, percentage saturation with dissolved oxygen, tide level, and water temperature.

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FIQ.74. Numbers of Ctibbula cineraria visible in two separate metre squares in tho shallow sublittoral on the north side of Castle Island from 19-21 July 1966, with parallel records of weather, percentage saturation with dissolved oxygen, tide level, and water temperature.

out on to the tops of rocks by day, and Marthasterias and ophiuroids emerge by night. Not all members of the population come up on every occasion, and the smaller Paracentrotus and Gibbula stay below anyway. There is no evidence of an9 relation with tide, water temperature, or percentage saturation of the water with dissolved oxygen. Crabs inhabiting the intertidal and shallow Rublittoral regions of the shore hunt mainly by night, as already illustrated (Fig. 59). An. activity rhythm with peaks of activity at night has been demonstrated in Carcinus by

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J . A. KITCHING A N D F. J . EBLINQ

by Naylor (1958), and in the starfish Luidia sarsi by Fenchel (1965). These rhythms, in Lough Ine, appear to separate predator and prey, and may serve to prevent over-predation, and thus to stabilize the community (Fig. 75). There can be little doubt but that crabs and starTime of activity

DAY

NIGHT

DAY \

NONMIGRATORY

\/

cineraria

Attached algae

J

Anornia

/

Plankton

FIG.75. Uiagrarnmat,ic rol)rrscnLatiun of major food chains iii tho Paraccntrotrm cominunity in relation to tinios of daily activity.

fish benefit by keeping out of sight of birds. Without knowing what goes on under boulders we cannot tell to what extent the prey of crabs and of starfish may benefit from a periodicity out of phase with that of their predators. Clearly the population of Paracentrotus is subject to fairly long-term fluctuations. Ten thousand Paracentrotus were seen in Paracentrotusdominated bare patches in the South Basin in 1964 and 1965; no such patches had been seen in the few years before, although Paracentrotus was fairly common in crevices and under boulders. It is suggested (Ebling et al., 1966) that extreme fluctuations of the inanimate environment, such as an unusually cold winter or summer, might unbalance the steady state of production and death of Paracentrotus upon which the population depends. An external effect of this sort might act either directly upon the Paracentrotus or upon some other species ecologically linked with it, such as a predator. All this indicates the need for quantitative assessment of the number of the ecologically important

ECOLOGICAL STUDIES AT LOUGH INE

289

species and for records of environmental conditions extending over a number of years. It seems likely that another important feature contributing to the overall stability of the Paracentrotus and other communities is the existence of limited sites safe for otherwise susceptible species, from which repopulation of contested areas can occur from time to time. Finally, we must not expect to interpret the composition of benthic communities in terms of interactions involving only post-larval benthic stages. Larval mortality both in the pelagic phase and during settlement can be very high (Thorson, 1964, 1966), although in some cases there may be more than enough larvae to saturate a surface (Connell, 1959). Additional knowledge is also needed of the behaviour of larvae before and during settlement. We do not yet know to what extent there are topographical or annual differences in the survival and settlement of larvae, which could account for local or temporal differences in the composition of the benthic flora and fauna of the shallow sublittoral region of Lough Ine.

ACKNOWLEDGMENT Diagrams which have previously appea.red in our papers in the Journal of Ecology and the Journal of Animal Ecology are reproduced by the kind permission of the Editors and of Blackwell Scientific Publications.

REFERENCES Ambuhl, H. (1959).Schweiz. 2. Hydrol. 21,133-264. Die Bedentung der Stromung als okologischer Faktor. Bassindale, R., Ebling, F. J., Kitching, J. A. and Purchon, R. D. (1948). J . Ecol. 36, 305-322. The ecology of the Lough I n e Rapids with special reference to water currents. I. Introduction and hydrography. Bassindale, R., Davenport, E., Ebling, F. J., Kitching, J. A., Sleigh, M. A. and Sloane, J. F. (1957). J. Ecol. 45, 879-900. The ecology of the Lough Ine Rapids with special reference to water currents. VI. Effects of the Rapids on the hydrography of the South Basin. Battaglia, B. (1965). Advances and problems of ecological genetics in marine animals. I n “Genetics Today”, Vol. 11, 451463. (S. J. Cfeerts, ed.) Oxford: Pergamon Press. Brian, M. V. and Owen, G. (1962). J . Anim. Ecol. 21, 241-249. The relation of the radula fraction to environment in Patella. Connell, J. H. (1959). Studies of some factors affecting the recruitment and mortality of natural populations of intertidal barnacles: I n “Marine Boring and Fowling Organisms”, 226-233. (D. L. Ray, ed.) Univ. Washington Press, Seattle. K*

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J. A . KITCHING AND F. J. EBLING

Crisp, D. J. (1955). J . m p . Biol. 32, 569-590. The behaviour of barnacle cyprids in relation to water movement over a surface. Crisp, D. J. and Southward, A. J. (1958). J . mar. biol. Ass. U . K . 37, 157-208. The distribution of intertidal organisms along the coasts of the English Channel. Ebling, F. J. and Kitching, J. A. (1950). School Sci. Rev. 114, 222-229. Exploration of the Lough Ine Rapids. Ebling, F. J., Kitching, J. A., Purchon, R. A. and Bassindale, R. (1948).J . h i m . Ecol. 17, 223-244. The ecology of the Lough Ine Rapids with special reference to water currents. 11. The fauna of the Saccorhiza canopy. Ebling, F. J., Sleigh, M. A., Sloane, J. F. and Kitching, J. A. (1960). J . Ecol. 48, 29-53. The ecology of Lough Ine. VII. Distribution of some common plants and animals of the littoral and shallow sublittoral regions. Ebling, F. J., Sloane, J. F., Kitching, J. A. and Davies, H. M. (1962). J . Anim. Ecol. 31, 457-470. The ecology of Lough Ine. XII. The distribution and characteristics of Patellu species. Ebling, F. J., Kitching, J. A., Muntz, L. and Taylor, C. M. (1964). J . Anirn. Ecol. 33, 73-82. The ecology of Lough Ine. XIII. Experimental observations of the destruction of Mytilus edulis and Nucella lapillus by crabs. Ebling, F. J., Hawkins, A. D., Kitching, J. A., Muntz, L. and Pratt, V. M. (1966). J . Artim. Ecol. The ecology of Lough Ine. XVI. Predation and diurnal migration in the Paracentrotus community. Evans, R. G . (1947). Proc. zool. Soc. Lo?zd. 117, 411-423. Studies on the biology of British limpets. Part 1. The genus Patella in Cardigan Bay. Fenchel, T. (1965). Ophelia 2, 223-236. Feeding biology of the sea-star Luidia sarsi Diiben & Koren. Fischer-Piette, E. (1935). J . Corrch., Paris 79, 5-66. Systematique et Biogeographic: Les Patelles d’Europe et d’Afrique du Nord. Fischer-Piette, E. and Gaillard, J. M. (1959). J . Conch., Paris 99, 135-200. Les patelles, au long des c8tes atlantiques iberiques et nord-marocaines. Grubb, V. M. and Martin, M. T. (1937). J . Bot. 75, 89-93. The algal vegetation of a cave. Hepper, B. T. (1957). J . mar. biol. Ass. U . K . 36, 33-40. Notes on Mytilus galloprovincialis Lamarck in Great Britain. Jones, N. S. (1948). Proc. Truns. Lpool biol. SOC.56, 60-77. Observations and experiments on the biology of Patella wlgata at Port St. Mary, Isle of Man. Kain, J. M. (1962). J . ww.biol. Ass. U . K . 42, 377-385. Aspects of the biology of Laminaria hyperborerc. 1 . Vertical distribution. Kitching, J. A. (1941). Biol. Bull. mar. biol. Lab., Woods Hole 80, 324-337. Studies in sublittoral ecology. 111. Laminaria forest on the west coast of Scotland; a study of zonation in relation to wave action and illumination. Kitching, J. A. and Ebling, F. J. (1961). J . Amim. Ecol. 30, 373-383. The ecology of Lough h e . XI. The control of algae by Paracentrotus lividus (Echinoidea). Kitching, J. A., Lilly, Silvia, J., Lodge, Sheila, M., Sloane, J. F., Bassindale, R. and Ebling, F. J. (1952). J . Ecol. 40, 179-201. T h e ecology of the Lough Ine Rapids with special reference to water currents. 111.The effect of current on the environmental conditions. Kitching, J. A., Sloane, J. F. and Ebling, F. J. (1959).J . Anim. Ecol. 28,331-341. The ecology of Lough Ine. VIII. Mussels and their predators. Kitching, J. A., Muntz, L. and Ebling, F. J. (1966). J . A n i m Ecol. 35, 113-126. The ecology of Lough h e . XV. The ecological significance of shell and body forms in Nucella.

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29 1

Lewis, J. F. (1964). “The Ecology of Rocky Shores”, pp. 323. London: English Universities Press. Lewis, J. F. and Powell, H. T. (1961). Proc. 2001. SOC.Lond. 137, 583-598. The occurrence of curved and ungulate forms of the mussel Mytilus edulis L. in the British Isles and their relationship to M . galloprovincialis Lamarck. Lilly, Sylvia J., Sloane, J. F., Bassindale, R., Ebling, F. J. and Kitching, J. A. (1953). J . Anim. Ecol. 22,87-122. The ecclogy of the Lough Ine Rapids with special reference to water currents. IV.The sedentary fauna of sublittoral boulders. Macan, T. T. (1963). “Freshwater Ecology”, pp. 338. London: Longman Green & Co. Ltd. Muntz, L., Ebling, F. J. and Kitching, J. A. (1965). J . Anim. Ecol. 34, 315-329. The ecology of Lough Ine. XIV. Predatory activity of large crabs. Naylor, E. (1958). J . exp. Biol. 35, 602-610. Tidal and diurnal rhythms of locomotor activity in Carcinus maenas (L.). Paine, P. T. (1966) Am. Nut. 100, 65-75. Food web complexity and species diversity. Rees, T. K. (1935). J . Ecol. 23, 69-133. The marine algae of Lough Ine. Renouf, L. P. W. (1931). J . Ecol. 19, 410-433. Preliminary work of a new biological station (Lough Ine, Co. Cork, I.F.S.). Round, F. E., Sloane, J. F., Ebling, F. J. and Kitching, J. A. (1961). J . Ecol. 49, 617-629. The ecology of Lough Ine. X. The hydroid Sertularia operculata (L.) and its associhted flora and fauna: effects of transference to sheltered water. Silva, P. C. (1955). J . mar. biol. Ass. U . K . 34, 565-577. The dichotomous species of Codiuin in Britain. Sloane, J. F., Ebling, F. J., Kitching, J. A. and Lilly, 6. J. (1957). J . Anim. Ewl. 26, 197-211. The ecology of the Lough Ine Rapids with special reference to water currents. V. The sedentary fauna of the laminarian algae in the Lough Ine area. Sloane, J. F., Bassindale, R., Davenport, E., Ehling, F. J. and Kitching, J. A. (1961). J . Ecol. 49, 353-368. The ecology of Lnugh Ine. IX. The flora and fauna associated with undergrowth-forming algae in the Rapids area. Southward, A. J. (1953). Pvoc. Trans. Lpool biol. SOC.59, 1-50. The ecology of some rocky shores in the south of the Isle of Man. Southward, A. J. (1956). Rep. mar. bwl. Stn. Port Erin. 68,20-29. The population balance between limpets and seaweeds on wave-beaten rocky shores. Southward, A. J. and Crisp, D. J. (1954). Proc. R. Ir. A d . (B), 57, 1-30. The distribution of certain intertidal animals around the Irish coast. Southward, A. J. and Orton, J. H. (1954). J . mar. biol. Ass. U . K . 33, 1-19. The effects of wave-action on the distribution and numbers of the commoner plants and animals living on the Plymouth breakwater. Staiger, H. (1957). Annde biol. 6 1 , 251-258. Genetical and morphological variation in Purpura lapillus with respect to local and regional differences in population groups. Streni, K. M. (1936). Skr. norake I.7iderrsk-Akad.i l f a t . - N d . Kl., No. 7, 85 pp. Land-locked waters. Hydrography and bottom deposits in badly-ventilated Norwegian fjords with remarks upon sedimentation under anaerobic conditions. Thorson, G. (1964). Ophelia 1, 167-208. Light as an ecological factor in the disposal and settlement of larvae of marine bottom invertebrates. Thorson, G. (1966). Neth. J . Sea Res., 3, 267-293. Some factors influencing the recruitment of’ marine bonthic communities.

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Author Index Numbers in italics refer to the pages on which references are listed in bibliographies at the end of each article. A Aitken, T. H. G., 109,126 Albert, T. F., 96, 126 Ambiihl, H., 209, 289 Ameghino, F., 158, 192 Ames, P. L., 103, 126 Anderson, J. M., 97, 128 Andrewartha, H. G., 10, 25, 32, 69 Archey, G., 146,192 Ardley, R. A. B., 168,192 Arrington, L. G., 88, 126 Ash, J. S., 104, 126, 128 Azevedo, J. A., Jr., 106, 126

B Bagenal, T. B., 27, 69 Bagshawe, T. W., 162, 168, 192 Bailey, A. M., 171, 192 Baker, A. de C., 167, 192 Bakker, K., 14, 69 Barker, R. J., 99, 106, 126 Bartholomew, G. A., 187, 193 Bassindale, R., 205, 209, 212, 213, 216, 218, 222, 223, 224, 227, 289, 290, 291 Battaglia, B., 43, 69, 199, 289 Beauchamp, R. S. A., 25, 26, 69 Beer, J. R., 63, 69 Bernard, R. F., 101,126 Birch, L. C., 6, 8, 9, 10, 25, 32, 43, 69 Bischoff, A. I., 99, 102, 127 Blackmore, D. K., 84, 126, 128 Blandin Landivar, C. J., 142, 192 Blyth, C. S., 185, 194 Bonner, W. N., 171, 192 Borg, K., 99, 101, 126 Borgman, L., 96, 97, 129 Bossert, W. H., 9, 62, 74 Boubier, M., 159, 160, 192

Boyd, C. E., 116,126 Boyle, C. M., 116, 126 Brady, J., 104, 128 Bray, J. R., 5, 69 Brian, M. V., 8, 69, 255, 289 Brown, A. W. A., 79, 89, 116, 1 6 Brown, R. N. R., 192 Brown, W. L., Jr., 21, 30, 31, 32, 52, 63, 69 Bruce, W. S., 192 Budd, G. M., 154, 156, 157,192 Burdecki, F., 192 Rurdick, G. E., 95,126 Burkholder, P. R., 7, 69 Burstall, T., 157, 171, 194 Bushland, R. C., 96, 126 ButJer, P. A., 79, 96, 98, I26

C Carson, H. L., 43, 69 Carson, R., 80, 126 Cawkell, E. M., 147, 162, 170, 192 Chiang, H. C., 13, 42, 69 Chichester, C. O., 80 Clarke, W. E., 157, 192 Clements, F. E., 6, 61) Colby, D., 95, 126 Cole, L. C., 3, 19, 35, 69 Collyer, E., 110, 126 Connell, J. H., 11, 58, 59, 69, 289, 289 Coon, F. B., 102,127 Cope, 0. B., 79, 98, 126 Crawford, A. B., 148, 192 Crisp, D. J., 209,249,253,254,290,291 Crombie, A. C., 3, 6, 17, 69 Csordas, S. E., 171, 192 D Darwin, C., 1, 17, 69 Davenport,, E., 216, 218, 223, 289, 291

293

294

AUTHOR INDEX

Devies, D. H., 157, 192 Davies, H. M., 253, 290 Davis, B. N. K., 106,126 Davis, D. M., 23, 24, 7 1 Deacon, G., 134, 192 Dean, H. J., 95, 126 De Bacli, P., 79, 126 Deevey, E. S., 3, 34, 7 1 De Witt, J. B., 95, 126 Dice, L. R., 16, 69 Dixon, K. L., 56, 62, 70 Douglas, D. S., 160, 192 Downes, M. C., 154, 157, 192 Dubois, K. P., 79, 104, 126 Dnmas, P. C . , 57, 58, 70

E Ealey, E. H. M., 154, 157, 192 Ebling, F. J., 205, 209, 212, 213, 216, 218, 222, 223, 224, 227, 228, 229, 252, 253, 258, 264, 269, 274, 278, 281, 285, 288, 289, 290, 291 Ecke, D. H., 64, 70 Edwards, R. W., 109, 113, 126 Egan, H., 109, 113, 126 Eights, J., 154, 192 Elliott, H. F. I., 132, 147, 157, 1G0, 169, 192 Elton, C., 8 , 16, 10, 17, 18, 21, 26, 27, 28, 31, 32, 51, 70 Elton, C. S., 113, 126 Erne, K., 99, 101, 126 Evans, F. C., 64, 70 Evans, R. G., 264, 290 Evans, 8.A., 93, 129

F Fabricius, A. F., 153, 193 Falla, R. A., 149, 153, 157, 167, 170, 193 Farner, D. S., 131, 133, 187, 189, 194 Fenchel, T., 288, 290 Ferguson, D. E., 116, 126 Filhol, H., 180, 193 Finlayson, H. H., 158, 19.3 Fischer-Piette, E., 255, 290 Fiske, W. F., 76, 127 Fleming, C. A., 170, 193 Foxton, P., 168, 193 Frank, P. W., 9, 14, 70

Frear, I). E. H., 98, 103, 126 Frenzel, L. D., 63, 69 G Gaillard, J. M., 290 Gain, 168, 193 Gause, G. F., 3, 33, 34, 70 Genelly, R. E., 79, 95, 97, 126, 128 George, J. L., 98, 103, 126 Georghiou, G. P., 79, 95, 116, 127 Giban, J., 94, 127 Gibb, J., 64, 70 Gilbert, O., 3, 19, 70 Giles, R. H., Jr., 85, 127 Uodley, E. J., 144, 193 Gordon, C., 43, 70 Greenway, Jc., Jr., 31, 70 Grinnell, J., 16, 70 Grodzinski, W., 54, 70 Grolleau, G., 94, 127 Grubb, V. M., 199, 290 Gunther, E. R., 167, 193 Gwynn, A. M., 154, 157, 161, 171,192, 19J

H Hagen, K. S., 79, 91, 128 Hagen, Y., 167, 171, 193 Hall, E. R., 52, 70 Hamilton, J. E., 147, 161, 162, 170, 192,193 Hammell, H. T., 184, 193 Hanko, E., 99, 101, 126 Hannon, J. P., 131, 193 Hansen, N., 63, 69 Hanson, W. C., 122, 128 Hardin, G., 3, 19, 70 Hardman, J. A., 98, 129 Hardy, J. D., 185, 194 Harrington, H. J., 157, 193 Harris, E. J., 95, 126 Harrison, J. O., 43, 70 Hart, J. S., 187, 19.3 Hartley, P. H. T., 10, 62, 70 Hawkins, A. D., 285, 288, 290 Hayne, D. W., 106,128 Heath, R. G., 95, 127 Heatwole, H., 23, 24, 71 Heppcr, R. T., 258, 290 Herreid, C. F., 185, 196

AUTHOR INDEX

Hewlett, P. S., 116, 129 Hickey, J. J., 102, 127 Higgins, E., 122, 127 Hinde, R. A., 9, 10, 7 1 Hitchcock, S. W., 114, 127 Hobart, J . , 3, 19, 70 Hock, R., 187, 195 Hodson, A. C . , 13, 42, 69 Holdgate, M., 155, 193 Holgersen, H., 155, 193 Housse, E., 163, 193 Howard, L. O., 76, 127 Howell, T. R., 187, 193 Huffaker, C. R., 121, 127 Hunt, E. G., 99, 102, 106,126,127 Hutchinson, G. E., 3, 16, 17, 18, 19, 21, 27, 29, 34, 46, 48, 63, 71 Huxley, T. H., 158, 193

295

Knox, G. A., 145,194 Knutson, H., 95, 127 Koeman, J. H., 103, 127 Kohn, A. J . , 29, 30, 52, 71 Kontkanen, P., 4, 71 Kostitzin, V. A., 35, 71 Kuenen, D. J., 80, 110, 127 Kunze, F. M., 96, 127

Jeannel, R., 147, 193 Jefferies, D. J., 107, 127 Jessup, D. C . , 94, 127 Johnson, F., 187, 195 Jones, N. S., 230, 290

I, Lttck, D., 9, 17, 40, 32, 71 Laird, M., 115, 127 Lamb, H. H., 163, 194 Lanyon, W. E., 11, 71 Laiig, E. P., 96, 127 Lavalloe, A., 94, 187 Laverton, S., 114, 127 Law, P. G., 157, 171, 194 Laws, R. M., 171, 192 Learner, M. A., 109, 113, 126 Legg, K., 62, 71 LBv$que, R., 132, 142, 157, 172, 194 Lewis, J. F., 252, 253, 258, 291 Lilly, Silvia J., 209, 212, 224, 290, 291 Lindsay, C . , 146, 192 Lipkin, M., 185, 194 Lodge, Sheila M., 209, 212, %90 Lonnberg, E., 142, 194 Lotka, A. J . , 3, 34, 71 Lowe, P. R., 183, 193 Lu, F. C . , 94, 127 Ludwig, H. F., 96, 127

li Kain, J. M., 252, 290 Kanwisher, J., 187, 194 Kearton, C., 132, 145, 194 Keith, J. A., 95, 98, 102, 127 Kelson, K. R., 52, 70 Kennedy, T. J., Jr., 51, 63, 71 Kennett, C. E., 121, 127 Kikkawa, J., 54, 55, 7 1 King, J. R., 131, 133, 187, 189, 194 Kinne, O., 67, 71 Kinsky, F. C., 145, 194 Kitching, J. A., 205, 209, 212, 213, 216, 218, 222, 223, 224, 227, 228, 229, 231, 252, 253, 258, 264, 269, 274, 278, 281, 285, 288, 289, 290, 291 Klopfer, P. H., 5, 10, 63, 65, 71

M MacArthur, J. W., 6, 72 MacArthur, R. H., 6, 21, 28, 29, 65, 71, 72 Maca.n, T. T., 209, 291 McNab, B. K., 186, 194 Madsen, H., 184, 194 Maples, B. J., 158, 194 Maris, P. J., 109, 113, 126 Marler, P., 62, 72 Marr, J. W. S., 166, 194 Marshall, J. T., Jr., 22, 72 Martin, H., 79, 85, 89, 93, 1.27 Martin, M. T., 199, 290 Matheson, C., 54, 78 Matthewu, L. H., 167, 194 M a p , E., 21, 30, 31, 32, 68, 7%

I Ide, F. P., 114,127 Ingham, S. E., 171,192 Irving, L., 131, 187, 193, 195 Ise, G. A., 98, 128

J

296

AUTHOR INDEX

Menhinick, E. F., 111, 113, 127 Merrell, D. J., 4, 38, 45, 7 2 Metcalf, R. L., 79, 85, 89, 127 Miller, A. T., 185, 194 Miller, R. S . , 8, 12, 13, 15, 17, 18, 20, 21, 22, 25, 28, 32, 35, 36, 37, 39, 40, 41, 42, 44, 49, 50, 51, 53, 54, 55, 61, 63, 66, 70, 72 Mills, D. H., 128 Milne, A., 6, 72 Mishima, J., 12, 72 Mitchell, R., 4, 72 Mohn, M. H., 98, 128 Monnie, J. B., 62, 7 3 Moore, J. A., 35, 38, 44, 7% Moore, N. W., 11, 64, 72, 80, 83, 88, 90, 98, 99, 100, 102, 103, 104, 107, 120, 127 Moreau, R. E., 27, 63, 72 Moreau, W. M., 63, 72 Morrison, F. O., 94, 116, 128 Moseley, H. N., 147, 194 Mountford, M. D., 121, 128 Muir, R. C., 110, 127 Mulla, M. S., 101, 127 Muller, P., 79, 127 Muntz, L., 264, 269, 274, 281, 286, 288, 290, 291 Murphy, R. C . , 134, 141, 142, 144, 153, 161, 162, 163, 167, 168, 183,194 Murton, R. K., 128 Myers, G. T., 61, 72

N Naylor, E., 288, 291 Negherbon, W. O., 79, 9 3 , 1 2 8 Nero, R. W., 56, 72 Neyman, J., 46, 47, 72 Nicholson, A. J., 8, 9, 12, 15, 72, 128

0 O’Brien, P. J., 170, 194 Odum, E. P., 5, 72, 122, 128 Ogilvie, D. M., 97, 128 Oliver, W. R. B., 134, 146, 194 Olsen, S., 168, 194 Orians, G. H., 30, 52, 56, 63, 71, 7 3 Orton, J. H., 254, 291 Owen, G., 255, 289 Ozburn, G. W., 94, 116, 128

P Paine, P. T., 286, 291 Pantin, C. F. A., 134,195 Park, T., 7, 8, 45, 46, 47, 72, 7 3 Passel, C . F., 185, 195 Paulian, P., 147, 153, 158, 195 Peakall, D. B., 119,127 Pendleton, R. C., 122, 128 Perring, F. H., 83, 128 Peterle, T. J., 85, 127 Peters, J. L., 134, 195 Peterson, K. K., 96, 97, 129 Phillips, A., 132, 195 Pickles, W., 60, 64, 73 Pitelka, F. A., 62, 7 1 Post, A., 110, 127 Powell, H. T., 258, 291 Pratt, D. M., 14, 7 3 Pratt, V. M., 285, 288, 290 Prestt, I., 107, 109, 119, 127, 128 PrBvost, J., 132, 165, 172, 176, 180, 185, 186, 187,195 Prickett, C. S., 96, 127 Purchon, R. D., 205,213,222,227,289, 290 Pycraft, W. P., 183, 195 R Ramsay, L. N. G., 192 Rand, R. W., 145, 148, 158, 166, 195 Rankin, N., 153, 195 Ratcliffe, D. A., 97, 107, 113, 128 Rees, T. K., 199, 208, 291 Renouf, L. P. W., 199, 200, 201, 291 Reynoldson, T. B., 3, 19, 70 Richdale, L. E., 132, 146, 171, 176, 188, 195 Roughley, T. C., 168, 195 Round, F. E., 228, 291 Rudd, R. L., 79, 88, 95, 97, 106, 126, 128 S Sang, J. H., 42, 43, 73 Sapin-Jaloustre, J., 132, 180, 155, 186, 187,195 Satchell, J. E., 121, 128 Scheffer, V., 133,195 Schell, J., 134, 196 Schmidt-Nielson, K., 160, 195

AUTHOR INDEX

Schneider, F., 114, 128 Scholander, P. F., 133, 187, 195 Schott, G., 142, 145, 158, 159,195 Schwab, R. G., 62, 73 Scott, E. L., 46, 47, 72 Serventy, D. L., 148, 192 Shackleton, E. H., 163, 195 Sharpe, G. I., 104, 126 Sheldon, M. G., 98, 128 Shelford, V. E., 6, 69 Sheppard, D. H., 73 Sibley, C . G., 68, 73 Silva, P. C., 231, 291 Simmons, K. E. L., 9, 10, 11, 73 Simpson, G. G., 66, 73, 158, 159, 177, 195 Siple, P. A., 185, 195 Skea, J., 95, 126 Sladen, W. J. L., 138, 155, 157, 160, 176,195

Sleigh, M. A., 216, 218, 229, 289, 290 Sloane, J. F., 209, 212, 216, 218, 223, 224, 228, 229, 250, 253, 258, 289, 290, 291 Slobodkin, L. B., 14, 21, 28, 46, 47, 73 Sluiters, J. E., 11, 73 Smith, R. F., 79, 91, 128 Snow, D. W., 55, 56, 63, 73 Sokoloff, A., 12, 38, 42, 43, 73 Solomon, M. E., 6, 74 Solyanik, G. A., 155,195 Sorensen, J. H., 171, 192 Southern, H. N., 54, 74, 128 Southward, A. .J., 230, 249, 253, 254, 290, 291 Springer, P. F., 114, 128 Staiger, H., 274, 291 Stalker, H. D., 43, 69 Stern, V. M., 79, 91, 128 Stickel, L. F., 106, 127, 128 Stickel, W. H., 95, 106, 128 Stonehouse, B., 132, 134, 155, 165, 167, 168, 169, 171, 172, 173, 176, 188, 189,196 Street, J. C., 104, 128 Strickland, A. H., 87, 89, 93, 98, 128,

129 Strem, K. M., 205, 220, 291 Sundnes, G., 187, 194 Swales, M. K., 132, 147, 157, 160, 163, 171, 712, 196

297

T Taljaard, J. J., 196 Tatton, J. O’G., 98, 103, 104, 127 Taylor, A., 104, 128 Taylor, C. M., 264, 290 Taylor, J. C., 84, 128 Taylor, 12. H., 157, 196 Templeton, W. L., 122, 128 Thomas, A. S., 90, 128 Thorson, G., 289, 291 Tinbergen, N., 10, 74 Tomes, H., 23, 74 Tomes, M., 23, 74 Trapido, H., 109, 126 Tregear, R. T., 184, 196 Turner, N., 98, 128 U TJdvardy, M. F. D., 16, 32, 74 Ullyett, G. C . , 15, 26, 74 Ullyott, P., 25, 69

V Van Allen, L., 66, 74 Van der Bosch, R., 79, 91, 128 Van Genderen, H., 103, 127 Van Mieghem, J., 134, 196 Van Oye, P., 134, 196 Vaughan, T. A., 61, 72 Vaurie, C., 30, 31, 74 Veghte, J. H., 185, 196 Viereck, E., 131, 193 Vinson, S. B., 116, 126 Vizoso, M., 128 Volterra, V., 3, 74 Von Haartman, L., 10, 74 Vowinckel, E., 196 W Wace, N. M., 147, 158, 196 Wain, R. L., 91, 129 Walker, C . H., 99, 127 Walker, T. M., 95, 98, 126 Walters, S. M., 83, 128 Walters, V., 187, 195 Wanntorp, H., 99, 101, 126 Warham, J., 132, 145, 171, 176, 196 Warner, R. E., 96, 97, 129 Watson, M., 180, 196 Weatherly, A. H., 17, 74 WVebster, C . G., 114, 128

298

AUTHOR INDEX

Wheatley, G. A., 98, 129 WHO Report, 88, 129 Williams, C. B., 4, 27, 74 Willis, A. J., 109, 111, 129 Wilson, E. A., 134, 196 Wilson, E. O., 8, 9, 21, 30, 31, 32, 52, 62, 63, 69, 74 Wilson, R. A., 98, 128 Wiman, C., 158,196 Windsor, C. P., 34, 74 Wingstrand, K. G., 184, 194

Winteringham, F. P. W., 116, 129 Witt, A. A., 33, 34, 38, YO Woodford, E. K., 93, 129 Woods, L. A., Jr., 106,126 Wynne-Edwards, V. C., 97, 129

Y Yemm, E. W., 109, 111,129 Young, E., 172, 196 Young, P. S., 154, 157, 192, 193

Subject Index A Acanthochitona crinitus, 225, 226 Acaricides, 80, 87 Accipiter nisus, 84, 119 Acmaeu v i r g i m , 226, 240 Actinia equina, 229, 241, 249 Aculus fockeri, 110 Addlie penguins, 132, 138, 139, 141, 154-157, 161, 165-168, 172, 174, 176, 179, 180, 182-191 Adocia cinerea, 226 Aerial spraying (Pesticides), 79, 91 Aeshna juncea, 11 Africa, 27, 131, 135, 136, 157, 160, 171 African coasts, 163 African countries, 88 African deserts, 10 Agelaiue phoeniceus, 56, 54 Agelaius tricolor, 63 Agulhas current, 160 Alaria esculenta, 230, 231, 244 Albany, 137, 143, 145 Albatross, 167, 187 Albemarle Island, 136, 142 Alberta, 51, 52 Alcyonidium hirsutum, 223 Aldrin, 92, 107 Algae, 108, 113, 199, 209, 210, 222, 223, 227, 229, 230, 250, 268, 278-281, 286, 288 Algeria, 60 Amanda, 140 America, North, 5, 31, 51, 52, 55,56, 66 America, South, 135

American Museum of Natural History, 191

American penguins, 132 American woodcock, 106 Amphilectie fucorurn. 226 Amphibia, 57-58, 116, 133 Amphipods, 167, 223, 228, 250, 281 Anax imperator, 11 Anemone, Sea, 224, 225, 229, 232

Anomia spp., 253, 285, 288 Anopheles hispaniola, 109 Anopheles labranchiae, 109 Anopheles mulipennis atroparvua, 116 Antarctic, 98, 103, 131, 132, 138, 140, 143, 152, 154, 155, 157-161, 163, 166, 166, 168, 169, 171, 172, 182, 184, 187, 188, 190, 191 Antarctic Convergence, 135, 136, 138, 139, 147, 148, 150, 153, 161, 167 Antarctic Peninsula, 136, 138, 139, 156, 157, 158, 161, 162, 168, 190 Antarctic, Sub-, 131, 132, 134, 136, 138, 139, 141, 143, 150, 152, 163, 157, 158,163,164,168,170, 172, 188 Anthopleura ballii, 225, 226, 232 Antipodes Island, 136-139, 143, 160, 152 Ants, 60, 62, 64 Aphids, 90, 107 Apodernw$avicolli, 5, 64 Apodemua qlvaticua, 5, 54, 55 Aptenodytes spp., 134, 140, 165, 180, 182, 191 Aptenodytea forstel., 174 Aptenodytes pakzgonica, 174 Aptenodytes patagonica halli, 134 Arctocephalus spp., 171 Arctocephalus forsteri, 171 Arctocephalus t . trop*caliS, 171 Arctomysis marina, 167 Ardeu cinerea, 84 Argentine, 135 Argentine Islands, 135, 150, 164 Arrhenathrum elatiua, 109 Arthropods, 78, 70, 90, 116, 121 Ascophyllum spp., 230, 260 Ascophyllum nodosum, 230, 243 Asiatic cockroach, 2 Asterim rubens, 246, 249, 285 Asterinu gibbosa, 249, 250 Atlantic Ocean, 146, 147, 159, 160, 201, 202, 249, 258

299

300

SUBJECT INDEX

Atlantic salmon, 97 Auckland Islands, 136-138, 143, 150152 Auster, 140

Austral Bay, 140 Australia, 2, 131, 132, 135, 136, 137, 143, 145, 146, 158, 159, 161, 163, 168, 171, 172 Azinphos methyl, 92

B Bacteria, 113, 256 Bahia Bianca, 135 Bdanua balanoides, 11, 58, 59, 62, 230 Balanua balunus, 226 Balanua crenatus, 226 Balleny Islands, 135, 136, 138, 154, 155, 163

Ballyisland, 204 Baltimore Harbour, 201, 254 Banana-agar medium, 13-14 Banana plants, 43 Bank vole, 54, 55 Banks Peninsula, 137, 138, 143, 146 Bantam, 94 Barloge Creek, Lough Ine, 201, 202, 204-206, 208, 221, 229, 231, 249251, 261, 269, 281, 283 Barnacles, 58, 230, 263, 269 Bass Strait, 137, 143, 145, 167 Bay of Islands, 137, 143, 145 Beaufort Island, 140 Bee, stingless, 2 Beetles, burying, 43-44 Behaviour, effects on (Pesticides), 9697 Benguela Current, 144, 160, 161, 166, 168, 172 Benthic animals, 4 Bergmann’s Rule, 66, 179 BHC, 85, 92, 94, 107 Biogeographic zones (Penguins), 134136 Birds, 55-57,77,83,90,94,98, 100,101, 104, 107, 114, 285, 288 Bittiurn. reticulaturn, 281

Blackbirds red-winged, 56, 67, 64 tri-colored, 63 yellow-headed, 56, 57

Blackfooted penguins, 136, 137, 141, 145, 157, 160, 166-168, 172, 174, 179, 181, 189, 190 Black rat, 54 Blackwell Scientific Publications, 289 Blepharidopterus angulatus, 110 Blowflies, 15 Bluebird, 31 Blue shark, 171 Blue tit, 56 Boobies, 166, 170 Bordeaux mixture, 85 Bounty Island, 136-139, 143, 150, 152 Bouvet~yaIsland, 135, 136, 138, 143, 154, 155 Brachypodiurn pinltatum, 121 Bracken, 90 Bransfield Strait, 166 Breeding cycles (Penguins), 132, 142, 145, 169 Breeding habitats, 169-171 Breeding habits, 142, 144, 145, 147, 165, 169-171 Britain, 16, 54, 83, 85, 86-90, 98, 104, 108, 119, 120

British Insecticide and Fungicide Council, 79 British Isles, 54, 98, 99, 253 British Museum (Nat. Hist.), 191 British South Georgia Expedition, 157 British Weed Control Council, 79 Brown or Norway rat, 54 Brussels sprouts, 107 Buckle-Sabrina Island area, 155 Bugula$abellata, 225, 226, 238 Bullfrog, 57 Bullock Island (Lough Ine), 202, 204, 205, 230, 231, 263

cave, 199, 202, 204, 251, 252 narrows, 229, 230, 249 Bulrush, 56 Buteo buteo, 84 Buzzard, 84 C

Caird Coast, 140 Calandra oryzae, 43 California, 16, 99, 102, 106 Callao, 142, 143, 161 Calliostowba zizyphinum, 23 1 Calocaris macandreae, 157

SUBJECT INDEX

Calypte anna, 62 Campbell Island, 136, 138, 139, 143,

Chile, 132, 135, 136, 142, 144, 159, 162, 163, 167-170, 172

Chinstrap penguins, 132, 138, 139, 141,

148, 150-152, 164, 171

Canada, North West Territories, 98 Canary Islands, 66 Cancerpagurus, 261,263,276,277,283, 285, 288

Canterbury, 146 Canterbury Museum, 192 Cape Crozier, 140 Cape D d e y , 140 Cape Frio, 144, 161 Cape Leeuwin, 145 Cape penguins, 136 Cape Royds, 138, 163, 172, 176, 186, 187

Caprella acanthifera, 281 Caprella acutifrons, 223, 228 Capricorn, Tropic of, 135 Captan, 87, 92 Carcinus spp., 257, 263, 270, 273, 274, 277, 285, 288

Carcinua maenas, 261-263,

301

269, 272,

276, 281-283

Carrigathorne, (Lough Ine), 202, 204,

153-157, 163, 168, 174, 179, 184, 189- 191 Chionis alba, 172 Chionis minor, 172 Chipmunks, 5, 51, 53, 62 Chlamys varia, 285 Chlyocladia verticillata, 278 Chondms crispua, 231 Chrysanthemum cinerariaefolium, 86 Chrysomyia chbrophyga, 15 Chthamlua stellatus, 11, 58, 59, 62, 230 Claoa squamata, 229, 230, 243 Clear Lake, California, 99, 102, 114 Clethrionomys glareolua, 54, 55 Climate, terrestrial (Penguins), 163-165 Clupea bassensis, 168 Coal tit, 56 Codium Bay (Lough Ine), 209,211-213, 221, 228 Codium fragile, 210, 229, 249, 250

Co-existence conditions (Competition), 33,48

230, 249, 253, 254, 256-258, 260, 261, 263-273 Caryophyllia m i t h i , 226, 249 Castle Island (Lough Ine), 200, 201, 221, 278, 287

Colaptes auratua, 31 Collembola, 57 Colloo, 137 Colorado, 24, 49, 50 Colpomenia sinuosa. 231 C a t h a r d skua, 170 Columbia coast, 141 Cats, 172 Columbua livia, 84 Cattail, 66 Community composition, 26-28 Cellepora pumicosa, 225, 226, 234 Competition Cephalopods, 165, 167 component elements, 8-16 Ceramidia butleri, 43 exclusion, 48-65 Ceramium spp., 278 in Nature, 20-33 Cetaceans, 171 nature of, 6-16 C h a e c h , 119 pattern and process in, 1-74 Chapman Memorial Fund, 192 process of, 7-8 Character displacement (Compet,ition), Competitor removal (Pesticides), 10830-31

Charadrim dubius, 11 Churadrius hiaticula, 11 Chatham Islands, 135, 137, 138, 142, 143, 146, 170

Chatham Island penguins, 137, 138, 174, 179, 181, 184, 189, 190

Chemosterilants, 80, 89, 96 Chesapeake Bay, Maryland, 103 Chickadee, 62

110

Concentration (Pesticides), 99- 101 Connecticut, 103 Connemara, 257 Control (Pesticides), 117-120, 123 C o n m spp., 29 Cook Strait, 138, 146 Cooper Bay, South Georgia, 157 Coosh (Lough Ine), 202, 204 Copepods, 167

302

SUBJECT INDEX

Coppers, 87, 92 Cork County, 201 Cork University College, 199, 208 Cormorants, 166, 170, 172 Coronel, 135 Corral, Chile, 163 C o r y w t k viridk, 225, 226, 228, 232 Costazia: costazii, 225, 226, 234 Coulman Island, 140, 157, 166 Crabs, 257,261, 263,268, 272,286, 287 distribution of, 281-283 predatory, 274-278 Cratogemys mtanops, 50-5 1 Crayfish, 59 Creek (Lough Ine), 198 CriSia eburnea, 226 Crow, carrion, 109 Crozet Islands, 135, 136, 138, 140, 143, 149, 169 Crusaders, the, 54 Crustacea, 109, 113, 165, 167, 168, 263 Culicids, 109 Curlew Bay (Lough Ine), 274,278,279, 281, 283 Currents (Lough h e ) , 213-218 d u e n i e ofY222-228 measurements, 211, 216, 218 mode of action, 227-228 D Dactylie glonterata, 109 Dalapon, 90, 92 Daphnia obtusa, 14 Daphnia pulimria, 14 Davis, 135, 151 Decapods, 257, 283 DDT, 79, 85, 86, 88, 90-92, 9696, 98, 99, 101, 104, 106, 107, 109, 110, 114-116, 120 Deer Flat, California, 102 Demeton, 90, 92, 107 Dendrocopus pubescens, 62, 63 Dendrocopua villoaua, 63 Department of Technical Cooperation, London, 88 Density-dependent factors, 76,90, 118, 121, 124 Density-independent factors, 76, 89, 90-91, 121, 124, 125 Devonian slates, 204 Dimtopma patina, 226

Diatoms, 256 Didemnum macculosum, 226 Dieldrin, 86,92,94-96, 98, 104, 107,121 Dinitrocresol, 85 Diomedea negripee, 187 Dion Islands, 140 Diquat, 97 Dispersal (Pesticides), 98-99 Distribution patterns, 2 1-25 Dithiocarbamates, 87, 93 Diversity, effects on (Pesticides), 111114, 125 DNOC, 90, 92 Dogs, 172 Dolphins, 171 Dominican gulls, 172 Dominion Museum, 192 Donovan Point (Lough Ine), Bti9 Downy woodpecker, 62, 63 Dragonflies, 11, 64 Dromadoon (Lough Ine), 199,200,202, 211, 277 Dronning Maud Land, 156 Drosophila spp., 12, 39, 40, 47, 68 Drosophih funebrie, 4, 45 Drosophila mlanogaater, 4, 13, 14, 3542, 44-45, 95 Drosophila miranda, 38 Drosophila persirnilis, 38, 42 Drosophila pseudoobscura, 38, 42 Drosqhda &mulans, 14, 35-42, 44 Dulupon, 89 Dynamena bidelztata, 230 Dymmerm pumila, 230 E Earthworms, 106, 113 East Anglie, 107 Ecological effects on single species (Pesticides), 104-1 10 Ecological niche (Competition), 15-20 Ecological studies at Lough Ine, 197290 Ecology, definition of, 75-76 Ecosystems, effects on (Pesticides), 110-116, 125 E c t o m r p conferroidee, 278 Eddy Creek (Lough h e ) , 209 E h t r a pilosa. 223 Elephant seals, 155, 163 Ellsworth, 135, 150, 164

SUBJECT INDEX

Emperor penguins, 132, 140, 141, 155157, 161, 163, 165-170, 172, 174, 176-189, 191 Endosulfan, 93 Endrin, 93 Energy exchange, 111 Energy niches, 5 England, 16,89,102, 103, 109, 119, 120 Engraulis anchoita, 168 Engraulk australis. 168 Engraulis japonicus, 168 Enteromorpha clathrata, 278, 279, 280 Eocene formations, 158 Equador coast, 141 Erect-crested penguins, 138, 139, 141, 152, 165, 174, 179, 181, 189-'191 Erskine Trust, 192 Escharella variolosa, 226 Escharoidea coccineus, 225, 226, 240 Eudypteespp., 138, 139, 145, 161, 165, 169, 180, 182 Eudyptes atr&us, 174 Eudyptes crestata, 174 Eudgptes crestatus Jilholi, 134 Eudyptes chrysolophus, 174 Eudyptes pachyrhynchue, 174 Eudyptes robusta, 174 Eudyptes robustus, 134 Eudyptes schlegeli, 174 Eudyptula spp., 134, 137 Eudyptula albaaignata, 174 Eudyptula m. iredalei, 174 Eudyptula m. minor, 174 Eudyptula m. novaehollandiae, 174 Euler diagrams, 19 Euphausia cryetallorophias, 167 Euphausia hemigibba, 167 Eupham'a recurva, 167 Euphausia superba, 166, 167 Euphausids, 166- 168 Euplectes h o r h c e a , 63 Eztplectes nigroventris, 63 Eurasia, 30 Europe, 16, 5 6 5 6 European rabbit, 89-90 starling, 3 1 E u t a m k amoenus, 51-54, 62 E u t a m k minimus, 5, 51-54, 68 Exclusion, competitive, 48-65 Exeter University, 201 Extinction (Pesticides), 113

303

F Fairy penguins, 136, 145, 177, 179, 180 Falco peregrinue, 86 Falco tinnunculus, 120 Falkland Islands, 135-140, 143, 147, 148, 156, 159-162, 164, 167-170, 172, 177 Farne Islands, Northumberland, 103

Fat solubility, effects of (Pesticides), 101-104, 125

Fens, 120 Feral pigeon, 84 Fe-stuca rubra, 109 Finland, 4, 16 Fish, 94,96,9&101,116,

165, 168, 171,

223

Fjordland penguins, 132, 138, 139,141, 146, 156, 165, 167, 169-171, 174, 179, 180, 189, 190 Flicker, 3 1 Flocking behaviour (Penguins), 165 Flustrella hispida, 230 Fold Island, 140 Food chains, 4, 5, 98, 101, 107, 121, 122, 125, 288 Foraminifera, 158 Form and metabolism (Penguins),173188 Fossil penguins, 158, 177 Foveux Strait, 138 Fowl, 96 Fox, 84, 96, 172 Franklin Island, 140 Fremantle, 137, 143, 145 Fringilla coelebs, 119 Frogs, 57 Fuoua serratue, 229, 242, 260 Fucue spiralis, 230, 260 Fucus veakulosue, 230, 260 Fungicides, 80, 87, 92, 107, 111 Fin seals, 155, 166, 171

G Galapagos Islands, 131, 135, 137, 141143, 159, 171

Galapagos penguins, 132,136, 137,141, 142, 157, 170, 172, 174, 177, 179, 182, 184, 189-191

Q a m W aflnis, 101 Garnwmrua duebeni, 67 Gammarue salinus, 67

304

SUBJECT INDEX

Clammarus zaddachi, 67 Gastropods, 227, 250, 281 Gause hypothesis, 3-4, 22, 28, 38,47 Gaussberg, 140 Gentoo penguins, 132, 139-141, 144, 147-149, 153-155, 157, 162, 165, 167-171, 177, 179, 182-184, 189 Geomyidae, 24, 49 Cleomys bursarius, 49-51, 61, 63, 66 Geornys personatus, 51, 63 Georgia, 54 Gibbula cineraria, 225, 227, 246, 249, 250, 285-288 Bibbuh umbilicalis, 230 Qigantinu stellata, 231 Glannafeen (Lough Ine), 199, 200, 202, 260-263, 269, 273, 277 Cllomeris spp., 121 Qlyphis ( = Prionace) ghucus, 171 Goats, 94, 169, 172 Goleen (Lough Ine), 200, 202, 204, 216, 221, 230, 258, 260-264, 272, 273, 280-283 Gophers, 24, 49, 51, 61, 66, 68 Gough Island, 132, 135, 143, 146, 147, 157,158, 163, 166, 169, 171, 172 Graham Land, 156 Grain beetle, 17 Great Britain, 6 , 77, 87, 89, 92, 249

Grebe Great Crested, 84 Western, 99 Greenland, 184 Grey rat, 90 Grey squirrel, 90 Growth retarders (Pesticides), 80 Grinnellian concept, 16 Guano, 142, 144, 145, 165, 170, 172 Gulf of San Matias, 144

H Hairy woodpecker, 63 Halichondria bowerbanki, 226 Hdiclona indiatinch, 226 Haliclonu limbatu, 226 Hallett, 135, 152 Halley Bay, 140 Haswell Island, 140 Hawaii, 29 Hawaiian Islands, 32 Hawthorn, 111

Heard Island, 135, 136, 138, 140, 143, 148, 153, 156, 164

Heat balance (Penguins), 188-191 regulation, 131-136 Heptachlor, 93, 94, 106 Herbicides, 80, 86, 87, 88, 90-92, 97, 107, 108, 111, 115

Heron, 84 Herring gulls, 95 Heteranomia squamula, 226 Hiatella arctica, 226, 249 Himanthalia elongata, 210, 230, 231, 244

Hippothoa hyalina, 223-226, 237, 247, 250

Homarus vulgaris, 183 Homeostatic mechanisms, 6 Hope Bay, 176, 187 Horseshoe Island, 135, 150, 164 House fly, 95 Humboldt penguins, 136 Hummingbirds, 62 Hydrography (Lough Ine), 205-221 Hydrobia ulvae, 230 Hydrurga leptonyx, 171 Hymedesmia bronstedi, 226 I Illinois, 99 Inaccessible Island, 146, 160 Indian Ocean, 147, 167 Insecticides, 79, 80, 83, 87, 88, 90-92, 96, 111. 122

Insects, 60-65 Insulation (Penguins), 183-186 Integrated control (Pesticides), 79 Interference factors, 62 Invasions (Competition), 31-33 Iran, 30 Ireland, 249, 257 Isolan, 95

J Jackass penguins, 136 Jassa falcata, 223, 250, 251 Journal of Animal Ecology, 289 Journal of Ecology, 289 Juan Fernandez Islands, 135, 137, 142, 143

Jura, Sound of, 252

SUBJE(JT INDEX

K Kalmus medium, 14 Karelia, North, Finland, 4 Kellia suborbicularis, 226 Kent, 111 Kerguelen Island, 135, 136, 138, 140, 143, 148, 153, 158, 164, 167, 169

Kestrel, 109, 120 Killer whales, 171 King penguins, 132,140, 141,144, 147149, 153-155, 157, 165, 167-170, 172, 174, 176, 177, 179, 182, 184, 18G188, 198-191 Kloa Point, 140

L Labhra (Lough Ine), 200, 204, 275 Lake Michigan, 95, 102 Laminaria spp., 227 Laminaria digitata, 209, 210, 222, 225, 249, 251, 252

Laminaria hyperborea, 249, 251, 252 Laminaria saccharina, 210, 252 Lanius colluria, 119 Lams dominicanua, 172 Laurencia pinnatifcda, 229, 242 Laurie Island, 157, 166 Lazarev, 140 Lead arsenate, 86, 93 Leaf-hoppers, 4 Leander aerratus, 262 Leathesia difformis, 231 Leopard frog, 57 Leopard seal, 171 Lepidoptera, 4, 43, 77, 83, 107, 199 Leeiconia nivea, 226 Leucopoliua alexandrinus, 11 Lichenopora hispida, 226 Life-cycle, Drosophila, 39-40 Lime sulphur, 85, 87 Limpet, 198, 225, 226 Lindane, 92 Little Blue penguins, 132, 136, 141, 171, 176, 182, 188

Littoral region (Lough Ine), 229-230 Littorina littorea, 230, 244 Littorina littoralis, 230, 243 Littorina neritoides, 229, 241, 249 Littorina saxatilis, 230 Lobster krill, 167 Lomentaria articulata, 229, 241

305

London, 88 Long Island Sound, Connecticut, 103 Lotka-Volterra model, 8, 18, 34 Lough Ine Ecological Studies, 197-290 geological map, 203 hydrography, 205-221 influence of current, 222-228 predation and grazing, 257-284 species distribution, 229-252 synecology, 284-289 topography, 201-205 water renewal, 220-221 zonation, 252-257 Lucilia sericata, 15 Luidia sarsi, 288 Lusitania Bay, Macquarie Island, 157

M Macaroni penguins, 132, 138, 139, 141, 147-149, 153-155, 157, 162, 163, 167-169, 174, 179, 180, 182, 184, 189-191 Mackellar Islets, 157 Macquarie Island, 135-140, 143, 148, 150-152, 156, 157, 161-164, 169171, 176, 179 Macronectes giganteus, 172 Magellan, 137, 143, 144, 167 Magellanic penguins, 132, 136, 137, 141-143, 147, 161, 162, 165, 167171, 174, 179, 181, 183, 189-191 Maia squinado, 283 Malaria, anti-, campaign, 109 Malathion, 85, 94 Mammals, 49-55, 90, 94, 98, 100, 101, 116, 131 Marie Byrd Land, 156

Marine Biological Station, Cork University College, 199 Marion Island, 135, 136, 138, 140, 143, 147-149, 156, 158, 164, 169

Marthasterim glacialis, 249, 253, 261, 285, 286, 288

Maryland, 103, 114 Mas a Fuera, 143 Mathematical models, 1-2 Mawson, 135, 152 McMurdo, Antarctica, 103, 135, 152, 164, 172

McNab’s curve, 186

306

SUBJECT INDEX

McNary, California, 102 MCPA, 93, 109 Meadowlarks, 11 Mediterranean, 58 Megadyptes spp., 137, 138, 145 Megadyptes antipodes, 174 Megarhyssa atrata, 23-24 Megarhyssa greenei, 23-24 Megarhyssa mcrurus, 23-24 Melanerpes erytltrocephulus, 62 Membraniporu membranaceu, 223, 227, 248, 250, 251 Membraniporella ~ritidu,226 Mercuries, 87, 88, 93 Messor aegyptiacun, 60, 62, 64 Messor barbarua, 60, 64 Metabolism (Penguins), 136, 173-188 rates, 186-188 Metridium senile, 224, 226, 232 Mexico, 55 Mice, 65, 94, 116 wood, 5 , 54 yellow-necked 5, 54 Midway, Island, 187 Migration (Penguins), 147 Millipedes, 121 Millport, Scotland, 58 Miocene period, 158 Mirids, 110 Riissel thrush, 2 Mocha Island, C'hilc, 162 ~ o i i ~ ~ sloo, c s , 101, ii:*,272 Molluscicides, 80 Mollymawk, 167 Monin squama, 226 Monks Wood Experimental Station, 70 Moroteuthis spp., 167 Morphology (Penguins), 131-133, 187 Mosquito, 109, 115, 116 Mourning chats, 10 Munida gregarian, 167 Munida 8Ubrugosa, 167 Murray and Rciillin Monoliths, 157 Musca domesticn, 95 Museum d'histoire neturellt~,19 I Mussels, 225, 257, 258, 260-263, 269, 273, 281 Mustelids, 172 Mutton birds, 146 Mycale rotatis, 226 Mysids, 167-168

Mytilus edulis, 223, 225, 226, 230, 236, 253, 257, 259-261, 263, 264, 272, 273, 284 Mytilus galloproai?bcia&?, 258 M y x i l h rosacea, 226 Myxoma virus, 89 N Nann,opterunz harrisi, 172 Narborough Island, 136, 142 Nature Conservancy, 78, 125 Necrophorus spp., 44 Nekton, 165, 199 Nematicides, 80 Netherlands, 103 Nettles, 111 New Amsterdam lslantl, 135, 138, 143, 146, 147, 167 New York, 29 New York Aquarium, 161 New Zealand, 32, 132, 136-138, 145, 149, 158, 167, 169, 171, 172, 187 Fjordland area, 137, 146 North Island, 135, 137, 146 South Island, 137, 138, 145, 156, 158, 159 Niche concept (Competition), 15-17 Niche relationships (Competition), 1720, 46-47 Nicotine, 85 Nightingnle Islantl, 148, 157, 160, 169 Norbormide, 89 Norfolk, 103 Norse1 Bay, 140 North Atlantic Treaty Organisation, 88 Northern Blue penguins, 136-137, 141, 145, 146, 156, 159, 168, 174, 177, 179, 181, 183, 184, 189, 190 Northern Gentoo penguins, 139, 140, 174, 177, 179, 182, 189, 191 North Karelia, Finland, 4 Northumberland, 103 Norway or brown rat, 54 Norwegian fjords, 206, 220 Notothenia rossi, 168 Notothenidae, 168 Nucella spp., 268, 270 Nuthatches, 30

0 Oak, 121 Obelia geniculata, 250

SUBJECT INDEX

Ocenebra crinacea, 269, 272 Oenanathe lugens, 1 Oligocene formations, 158 Onychoteuthia spp., 167 Oregon, 57 Orcinus orca, 17 1 Orconectes immun is, 59, GO Orconectes virilis, 59, GO Organochlorine insecticides, 83, 84, 87, 88, 91, 96-100, 104, 106, 107, 109, 113, 116, 119, 120, 125 Organophosphorous insecticides, 87,90, 91, 96, 101, 107, 114, llG Oryctolagus cutiiculus, 184 Otago, 137 Otago Museum, 192 Otariid seals, 134 Oxygen saturation (Lough Ine), 21 4, 219, 221, 252 Oysters, 96

P Pacific Ocean, 159, 161 Pacific starfish, 286 Palearctic, 55-56 Panonychus ulmi, 110 Papaver spp., 107 Paracentrotus spp., 229, 258, 274-281, 284-289 Parmentrotus lividus, 246, 249, 257 Paramecium aurelia, 34 Paramecium bursaria, 34 Paramecium mudatum, 34 Paraquat, 90, 93, 97 Parathion, 101 Paridae, 55 Partridge, 94, 108 Parus ater, 56 Parua atricapillus, 65-56 Pama caeruleus, 56, 63 Parua carolinensis, 55 Parus gambeli, 55 Pama hudsonicus, 55 Parus inornatus, 56, 62 Parua major, 63 Parua palustris, 55 parus rufescens, 55-56, 62 Parua sclateri, 65 Paaserella nzelodia, 22 Patagonia, 130, 144, 158, 101, 167, 168, 172

307

Patella spp., 198, 230, 253 distribution and characteristics, 253256

Patella aapera, 225, 226, 230, 253-256 Patella vulgatu, 230, 253-256 Patina pellucida, 222, 227, 245, 248, 250-252

Pectinaria belgica, 257 Pelicans, 170 Pelvetia spp., 258, 260, 261, 272 Pelvetia canaliculata, 230 Penguins, 98 environment of, 13G-I 73 food, 165-169 fossils, 158 gclneral biology with some considerntion of thcrmal balance, 131-196 InoThologY, md&ofism and heat balance, 173-191 nests and breeding habitats, 169-171 predators, 171-1 72 sea temperatures and terrestrial climates, 158-165 Peregrin falcon, 84, 97

Peromyscus nmniculatus, 5 Peruvian coast, 131, 136, 142 current, 161, 166, 168, 172 Peruvian penguins, 136, 137, 141, 161, 163, 165, 168, 172, 174, 179, 181184, 189-191 Pesticide Problem, 75-129 nature of, 80-85 types of research, 80 Pesticides and evolution, 116-1 17 application of an ecological approucli, 117-121 as an ecological problem, 70-80 tlehition of, 75-76 ec.ologica1 factor, 85-88 ecosystem effects, 110-1 16 interaction of, 79, 104 main characteristics, 88- 104 non-specificity, 89- 90 persistence of, 88, 91, 97-104, 125 resistance, 79 solubility, 97-104, 125 sublethal effects, 95-97, 125 tools for ecological research, 121, 125 toxicity, 91-97 P r t w Island Oy, 135, 13G, 138, 154, 155

308

SUBJECT INDEX

Petrels, 167, 170, 172 Petroleum and tar oils, 87 Phalacrocorax ariatotelis, 84 Phaaianw wlchicus, 84 Pheasant, 84, 94, 106 Phenoxyacetic weed killers, 87, 90, 9 1 Phocurctos hookeri, 17 1 Phodrin, 121 Phragmiterr spp., 5G Phytoseiids, 110 Pigeons, 23, 84 Pigs, 172 Pisaater ochraceus, 286 Planaria gonocephala, 25-26, 65 Planaria montenegrina, 25-26, 65 Plankton, 160, 165, 168, 172, 199, 285, 288

Plethodon dunni, 57-58, 61 Plethodon vehiculum, 57-58, 61 Plovers, 10-11 Plumularia setacea, 226 Poa pratensis, 109 Podiceps oristatus, 84 Pointe Geologie, 135, 140 Poisons, 89 Poleen (Lough Ine), 200, 202 Polychaetes, 257 Polysiphonia lanosa, 230, 278 Polyzoa, 223, 225, 227, 250 Pomatoceros triqueter, 226 Poppies, 107 Population dynamics, 82, 125, 199 Porphyra umbilicalis, 229, 249 Port Erin, 230 Portunus spp., 263 Portunus arcuatus, 257, 282, 283 Portunus corrugatus, 283 Portunus depurator, 283 Portunus puber, 261-263, 268, 269, 272, 276, 277, 278, 281-283, 285, 288

Predation and grazing (Lough Ine), 257-2 84

Predators (Penguins), 171-172 Predator removal (Pesticides), 110 Prey-predator relationships, 78, 12 1 Priapulw caudatus, 257 Prince Edward Island, 147 Probit analysis, 95 Production, effects on (Pesticides), 114-115, 125

Protozoa, 34, 116

Psychoteuthis glacialis, 167 Pufinus griseus, 146 P w a hispida, 133 Pygoscelis spp., 138, 139, 165, 180, 182 Pygoscelis adeliae, 174 Pygoscelis antarctica, 174 Pygoscelis papua ellsurorthii, 134, 174 Pygoscelis p . p a p , 174 Pygoscelk p . taeniata, 174 Pyrethrum, 86-88

Q Quaker Run Valley, New York, 29 R Rabbit, 89, 90, 184 Radioactive tracers, 121, 122 Rana catesbiana, 57 Rana pipens, 57 Rapids (Lough Ine), 198-202,204,205, 207-213, 216, 218-220, 225, 227, 229, 230, 249-252, 256, 264-270, 281 chart of, 206 current speeds, 207 water temperature, 215, 219 Rattus spp., 89 Rattus norvegicw, 54 Rattus rattus, 54 Rats, 89-91, 94, 104, 169, 172 Red-backed shrike, 119 Red-headed woodpecker, 62 Red spider mite, 110 Red-winged blackbird, 56-57, 64

Reduction of food species (Pesticides), 107-108

Reduction of habitat (Pestioides), 108 Renouf’s Bay (Lough Ine), 202, 209, 213, 225, 260, 277

Reproduction, effects on (Pesticides), 95-96, 101, 104

Rhizopertha dominim, 17, 43 Ringed seal, 133 Rio de Janeiro, 161 Rissoa parva, 2 8 1 Rockhopper penguins, 132, 138, 139, 141, 144, 146-149, 152-154, 157, 159, 160, 162, 166, 167, 169, 171, 172, 174, 176, 177, 179, 184, 189 Rocky Mountains, 51, 55

SUBJECT INDEX

Rodenticides, 80, 89, 107 Rookery Nook (Lough Ine), 221, 272, 283

Ross Island, Antarctica, 103 Ross Sea, 140, 155, 157, 167 Rothamsted Experimental Station, 4 Royalpenguins, 138,139,141,153,157: 163, 174, 179, 183, 189, 190

Royal Sound, 153

6 Sabrina Islet, 155 Sacwrhiza spp., 227, 228 Saccorhiza polyschides, 209, 210, 222, 223, 225, 245, 247-252

Saddle Island, 157 Sagartia elegans, 226 Salamanders, 57, 61 Saldanha Bay, 137, 143, 144, 145 San Ambrosio, 143 Sandwich Islands, 135, 136, 138, 140, 154, 155

San Felix, 143 San Francisco, 56 Bay, 22 Santa Maria Island, 144 Sardinops neopilchardue, 168 Sardinops ocellata, 168 Sardinops sagax, 168 Saskatoon, Saskatchewan, 56 Schizomauella spp., 226 Schradan, 90, 122 Scirpus spp., 56 Scolt Head, Norfolk, 103 Scopelidae, 168 Scotia Arc, 138, 139, 161, 166, 167, 190 Scotland, 2, 58 Scott Island, 135, 136, 138, 154, 155 Scruparia c h e h , 226 Scrupocellaria reptans, 225, 226, 234 Sea lions, 171 Seals, 98, 133, 134, 155, 163, 166, 171 Second World War, 87 Sediment (Lough h e ) , 212 Selaaphorus sasin, 62 Serpulu uermicularis, 225, 226 Sertularia operculata, 225-228, 236 Seymour Island, 158 Shackleton Barrier, 140 Shag, 84

309

Sharks, 171 Shawa, 135, 151 Sheathbills, 172 Sheep, 94, 169, 173 Shetland Isles, 58 Shrike, red-backed, 119 Shrimps, 262 Sialia sialb, 31 Simazine, 90, 93 Simocephalus vetulus, 14 Simuliids, 170 Sitotroga cerealella, 17 Sitta n e u m q e r , 30 Sitta tephronota, 30 Skuas, 98, 170, 172 Snails, 29, 58 Snares Island, 136, 139, 146 penguins, 138, 141, 169, 171, 174, 179, 180, 183, 184, 189

Song sparrow, 22 Song thrush, 2 South Africa, 143, 144, 166 South African Blackfooted penguins, 132, 161

South America, 141, 143, 161, 163, 171 South Equatorial current, 142 South Georgia, 135, 136, 138-140, 143, 148, 153, 154, 156, 157, 164, 167, 168, 169, 170. 176, 177, 188 South Orkney Islands, 135, 136, 138, 143. 149, 154, 155, 157, 164 South Pole, 138 South ShetJand Islands, 135, 136, 143, 149, 154, 164 Southern Blue penguins, 137, 138, 141, 146, 156, 169, 174, 179, 181, 182, 184, 189-191 Southern Gentoo penguins, 139, 140, 156, 174, 179, 189-191 Southern’s Bay (Lough Ine), 200, 202 Sow thistles, 111 Spain, 58 Sparrow hawk, 84, 97, 109, 110, 120 Species abundance (Competition), 2830 Species distribution (Lough Ine), 229252 relation to current, 222-229

Species distribution and numbers (Penguins), 136-158 Rpccies diversity, 65-68, 111

310

SIJBJECT INDEX

Spheniscidao, 131, 133, 160, 166, 179, 183, 184, 191 Spheniscua spp., 136, 137 Spheniscua demersus, 174 Spheniscus humboldti, 174 Spheniscus magellanicus, 174 Spheniscus mendiculus, 174 Spiders, 113 Spirorbis spp., 226 Squid, 167, 168, 171 Squirrel, Grey, 90 Starfish, 288 Starling, European, 31 Staten Island, 136, 138, 139, 144 Stevenson screen, I64 Stewart Island, 138, 139, 143, 145, 146, 160 Stilophora rhizodes, 245, 249 St. Paul Island, 135, 146, 147, 167 Stratification (Lough Ine), 218, 220 Strychnine, 93 Sturnella magna, 11 Sturnella neglecta, 11 Sturnua vulgaris, 31 Sublittoral region (Lough h e ) , 231-249 Sub-tropicalconvergence, 135,139,146, 147, 160 Succession, effects on (Pesticides), 115116 Sulphurs, 87, 93 Swedish birds, 101 Sydney, 137, 143, 145 Synecology (Lough Ine), 284-289 T Tasmania, 145, 137, 145 Tasman Sea, 145 Tawny Owls, 83 Taylor, 140 TDE, 93, 99, 101, 109, 114 Temperatures (Lough Ine), 217, 219 Temperatures (Penguins), 186-188 Temperatures, sea (Penguins), 159-163 Templebreedy (Loiigh Ine), 200, 202 Terre Addie, 176, 187, 188 TEPP, 94 Tertiary period, 158 Tetranychid mites, 110 Texel, The Netherlands, 103 Thais spp., 198, 281, 284 Thais lapillus, 58

Thais ( = h'ucella) lapillua, 199, 229, 242, 258 distribution and shell form, 263-274 Themisto gaudichaudi, 161 Thermal balance (Penguins), 131, 133, 163 Thomomys bottae, 50-51 Thomomys talpoides, 49-51, 61, 66 Thurston Island, 163 Tide levels (Lough Ine), 208 Tierra del Fuego, 136, 140, 141, 144, 160 Titmice, 55, 62 Topography (Lough Ine), 201-205 Tortrix spp., 121 Toxic Chemical and Wildlife Division, Thc Nature Conservancy, 78, 125 Toxic effects, 105-107 Toxicity (Pesticides), 81, 82, 91-97, 113, 125 Tranabo (Lough Ine), 202, 205 Tremex columba, 23 Tribolium spp., 7 Tribolium castaneum, 45-48 Tribolium confusum, 45-48 Triclads, 25 Tristan da Cunha, 132, 135, 138, 143, 146,147,159, 160,163, 167, 169 Trout, 95, 109 Tubularia bellis, 225,226, 238, 247,250, 251 Tubulipora spp., 250 Tubulipora plumosa, 223, 326, 227 Tule Lake, California, 102 Typha spp., 56 Typhlodromus p j r i , 110

U Ulva lactuca, 230 Umbonulu littoralh, 226 United States Department of Agriculture, 86 United States Department of the Interior, 79 United States Fish and Wildlife Service, 79 U.S.A., 54, 77, 86, 87, 95, 102, 103, 114 Urea, 93 Urchins, sea, 257, 276 Uruguay, 161, 162

311

SUBJECT INDEX

V Valdez Peninsula, 137, 143, 144, 161, 162

Valdivia, 137, 143, 144 Valparaiso, 137, 142, 143, 161 Verruca stroemiu, 225, 226, 239 Victoria, 145 Victoria Land, 156, 157 Voles, 54, 55 Volterra-Gause principle, 3, 4, 19 Volterra-Lotka analyses, 35 Vulpes vulpes, 84

W Wales, 16, 89 Walvis Bay, 137, 143, 145 Warfarin, 93 Wasps, 23 Wave action (Lough Ine), 249-250 Weddell Sea, 148, 149, 153, 156, 164 Weddell Sea Drift, 154, 164 Weed killers, 80, 121 Weight losses (Penguins), 186-188 West Australian Museum, 191-192 West Wind Drift, 142, 144-147 Whales, 163, 166, 171 Whelk, dog, 198 Whirlpool Point (Lough h e ) , 300. 213 White flippered penguins, 137,138,141, 145, 156, 170, 174, 177, 179, 182, 189, 190

Wilkes Land, 135, 140, 151 Winkler’s mctliod, 214 Wisconsin, 102 Woodcock, American, 106 Wood mouse, 5, 54 m’oodpecker downy, 63 hairy, 63 red-headed, 62 Woodpigeon, 90 World Health Organisation (WHO), 88 Wytham Wood, 83

s Xantho hydrop1i ilics, 183 Xantho inc is us , 283 Xunthoceplinlua ~cLiitliocpphalits,56

Y Ycllow-eyed penguins, 132, 137, 138, 141, 146, 152, 156, 167, 169, 170, 174, 176, 179-181, 183, 189, 190 Yellow-headed blackbird, 56, 57 Yellow-necked mouse, 5 , 54

z Zanzibar bishop, 63 Zonation (Lough Ine), 252, 257

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