MECHANISMS OF FOOD RESOURCE PARTITIONING AND THE FORAGING STRATEGIES OF RAINBOW TROUT (Salmo gairdneri) AND KOKANEE (Oncorhynchus nerka) IN MARION LAKE, BRITISH COLUMBIA
by
KIM D. HYATT
B. Sc. UNIVERSITY OF WINDSOR, 1971
A THESIS SUBMITTED IN PARTIAL FULFILLMENT OF
THE REQUIREMENTS FOR THE DEGREE OF
DOCTOR OF PHILOSOPHY
in the Department
of
ZOOLOGY
We accept this thesis as conforming to the required standard
THE UNIVERSITY OF BRITISH COLUMBIA
June 1980 0 Kim D. Hyatt In presenting this thesis in partial fulfilment of the requirements for an advanced degree at the University of British Columbia, I agree that the Library shall make it freely available for reference and study.
I further agree that permission for extensive copying of this thesis for scholarly purposes may be granted by the Head of my Department or by his representatives. It is understood that copying or publication of this thesis for financial gain shall not be allowed without my written permission.
Department of
The University of British Columbia 2075 Wesbrook Place Vancouver, Canada V6T 1W5
Date 0J- )H/g* ABSTRACT
This study was conducted to satisfy three objectives. The first was to provide a detailed description of the differences between the prey contents of rainbow trout ( Salmo qairdneri ) and kokanee ( Oncorhynchus nerka ) compared either to each other or to the prey contents of the natural environment. The second was to determine how elements of anatomy, physiology and behaviour interact to promote the acquisition of species specific diets by trout and kokanee. The third was to precisely identify the foraging strategies of the two predators by assessing how different anatomical and behavioural characteristics serve as interrelated adaptations that suit each species to effectively use a specific habitat-prey complex. Matched samples of trout and kokanee from Marion Lake exhibit only modest A dietary overlap ( mean of CX= .462, range.136 to .881 ). Although kokanee appear to track the environmental abundance of prey more closely than trout, both predators exhibit pronounced patterns of "density independent" acquisition of prey from the total complex of prey that is apparently available in the lake. To test hypotheses about the factors that control these dietary patterns, I conducted a series of studies concerning where trout and kokanee choose to forage, when they choose to forage, how they search for prey, how they attack prey, and how experience in encountering various prey alters the predator's foraging behaviour. Temporal segregation of trout and kokanee foraging activities is not well- developed under field conditions and appears unlikely to promote strong patterns of food-resource partitioning. By contrast, spatial segregation is well-developed and clearly plays a major role in promoting the acquisition of relatively large numbers of nearshore benthic prey ( eg. planorbid snails or odonates ) by trout and of relatively large numbers of offshore, water-column prey ( eg. chironomid pupae ) by kokanee. Close inspection of the details of predator and prey distributions indicates that many aspects of food-resource partitioning are not logical out• comes of spatial segregation.
ii iii
Differences in predator search-techniques do not determine the presence or absence of various prey types in predator diets, however, differences in predator search behaviours do bias them to obtain different quantities of particular classes of prey. Kokanee search procedures allow them to detect prey in both exposed and concealed locations while trout detect only exposed prey. While searching for benthic or lake-surface prey, kokanee maintain search positions which allow them to detect prey of smaller sizes than trout. This clearly favours the trend for kokanee to include greater quantities of small prey ( eg. Hyalella sp. ) in their diets than trout. Differences in search procedures do not explain why kokanee obtain a greater proportion of their diet than trout from small zooplankton ( £ 1 mm ) in late summer or why kokanee seldom exploit any of the relatively large ( > 4 mm ), armoured prey that are common in the diet of similar sized trout. Differences in both behavioural and morphological characteristics involved in the attack phase of foraging by trout and kokanee serve as the basis for explan• ations of a number of differences between the diets of free-ranging predators. These differences include: the greater utilization of aerial prey by trout, the inclusion of large numbers of copepods in the diet of kokanee but not of trout, the generally greater utilization of zooplankton by kokanee compared to trout, and the relative- scarcity of large ( > 4 mm ), armoured prey, in the diet of kokanee. A series of laboratory experiments was used to examine the extent to which short term experience might influence food-resource partitioning by trout and kokanee. These experiments offered convincing evidence that differential effects of experience will amplify the trends in resource partitioning already set in motion by differences in habitat selection, search procedures, and attack procedures. I argue that the morphological and behavioural traits that control food "selection" by trout and kokanee in Marion Lake are a consequence of the evolution of mutually exclusive foraging strategies. Trout are portrayed as D-strategists that concentrate on relatively large, dispersed prey for the bulk of their energy requirements. Adaptations which enable trout to differentially exploit large prey include: procedures for area-extensive search; a predisposition to attack relatively large, armoured-prey; large mouth- size; and persistent responses to opportunities to attack large prey. An inability to sustain high attack rates on small prey ( < 1 mm ) at high density ( 35 per liter ) and a tendency to ignore or reject such prey suggest that trout are not well-adapted to exploit relatively small, morphologically-uniform,prey. iv
Kokanee are portrayed as C-strategists which concentrate on relatively small, contagiously-distributed prey for the bulk of their energy requirements. Adaptations which enable kokanee to differentially exploit small prey include: procedures for area-intensive search; a predisposition to attack relatively small, morphologically- uniform prey; small mouth-size; well-developed gill-rakers; and an ability to sustain high attack rates on small planktonic prey. Low ingestion success with a variety of large benthic prey and a tendency to ignore or reject such prey under laboratory conditions where they serve as the sole source of food are evidence that kokanee are not well adapted to exploit large, armoured-prey. Adaptations associated with the search, capture, manipulation and ingestion phases of the foraging cycle appear in each instance to be evolutionary responses to specific features of a given habitat-prey complex. C-selected or D-selected foraging strategies appear to be mutually exclusive evolutionary avenues down which trout and kokanee have been directed by the fundamental nature of a given habitat-prey complex. ACKNOWLEDGEMENTS
I was initially attracted to U.B.C. by the ideas and approach to ecology of a group of biologists engaged in studying the Marion Lake ecosystem as part of Canada's contribution to the
International Biological Program. Although this group had largely dissolved by the time rny study was begun, the legacy of their efforts is clearly apparent in the present work.
Financial support came from the Canadian International
Biological Program, the National Research Council of Canada and the University of British Columbia, Department of Zoology.
Drs. I.E. Efford, C.J. Walters, T.G. Northcote and
N.R. Liley advised me during the early stages of the research while Drs. Walters, Northcote and Liley reviewed the thesis and provided helpful criticisms of early thesis drafts.
Dr. J.D. McPhail graciously assumed the task of research supervisor after the departure of Dr. Efford from U.B.C. He provided not only a kindred spirit but also a mixture of advice, criticism, healthy doses of encouragement and an incredible amount of patience to let me find my own way.
I profited greatly from the stimulation and good cheer of a succession of graduate students who broadened my understanding of approaches to both science and living. Conversations and shared experiences with Ben Seghers, George Calef, Wren Green, Mike Swift and Rick Charnov were especially influential.
v vi
Throughout this study I have relied on the unquestioning support of my parents who were in large part responsible for nourishing my early curiosity about the behaviour of animals.
Finally to my wife, Annice, my thanks for encouragement and understanding without which this study might never have been completed. TABLE OF CONTENTS Page
ABSTRACT ii
ACKNOWLEDGEMENTS V
LIST OF TABLES xiii
LIST OF FIGURES XVi
CHAPTER 1
GENERAL INTRODUCTION, GENERAL METHODS AND MATERIALS
INTRODUCTION 1
GENERAL METHODS AND MATERIALS 9
CHAPTER 2
THE SPECIES SPECIFIC DIETARY PATTERNS OF TROUT AND KOKANEE IN MARION LAKE
INTRODUCTION 17
METHODS 17
RESULTS 19
Comparisons between prey contents of trout and kokanee 19
Comparisons between prey contents of predators and the environment 31
DISCUSSION 39
SUMMARY 44
vii vi ii
Page CHAPTER 3
THE RELATIONSHIP BETWEEN SPATIAL SEGREGATION, TEMPORAL SEGREGATION AND DIETARY PATTERNS OF TROUT AND KOKANEE
INTRODUCTION 46
METHODS 48
RESULTS 52
Depth distribution 53
Distribution with area 55
Diel activity patterns of predators 57
The relation between diurnal activity and food search . 62
Activity patterns of emerging chironomids 63
DISCUSSION 64
The role of spatial and temporal segregation in producing dietary differences between trout and kokanee 64
The role of spatial and temporal segregation in producing differences between the prey contents of predators and the environment 69
Unexplained dietary patterns 71
SUMMARY 73
CHAPTER 4
THE RELATIONSHIP BETWEEN FOOD-SEARCH BEHAVIOUR AND DIETARY PATTERNS OF TROUT AND KOKANEE
4-A. FIELD DESCRIPTIONS
INTRODUCTION 75 Page
METHODS 78
RESULTS 79
Search techniques 79
Search positions 90
DISCUSSION
The potential effects of search techniques and microhabitat-specific search on dietary patterns 93
The potential effect of search positions on dietary patterns 96
4-B. LABORATORY COMPARISONS
INTRODUCTION 97
METHODS 99
RESULTS 103
Experiment 4.1 - reactive distance and prey density .... 103
Experiment 4.2 - reactive distance, trout versus kokanee 105
DISCUSSION 107
The role of search positions in producing dietary dif• ferences between trout and kokanee 107
The role of search techniques and search position in producing differences between the prey contents of predators and the environment 109
Unexplained dietary patterns Ill
SUMMARY 112 X
Page CHAPTER 5
THE RELATIONSHIP BETWEEN ATTACK BEHAVIOURS, MORPHOLOGICAL CHARACTERISTICS AND DIETARY PATTERNS OF TROUT AND KOKANEE
5-A. FIELD DESCRIPTIONS
INTRODUCTION 115
METHODS 117
RESULTS 119
Techniques of approach and capture 119
Comparisons of predator morphologies 123
DISCUSSION 127
The capture - success hypothesis 128
The gill-raker, prey-size hypothesis 129
The attack-rate hypothesis 130
The mouth-size, ingestion-success hypothesis 131
5-B. LABORATORY TESTS OF ATTACK HYPOTHESES
METHODS 132
RESULTS 137
Experiment 5.1, The capture-success hypothesis 137
Experiment 5.2, The attack-rate hypothesis 140
Experiment 5.3, The gill-raker, prey-size hypothesis ... 142
Experiment 5.4, The mouth-size, ingestion-success
hypothesis 147
DISCUSSION 150
Explanations of dietary differences between trout and kokanee 150 xi
Page
Explanations of differences between the prey contents of the predators and of the environment 155
SUMMARY 156
CHAPTER 6
THE ROLE OF SHORT TERM EXPERIENCE IN SHAPING THE RESPONSES OF TROUT AND KOKANEE TO PREY
INTRODUCTION 158
METHODS 160
RESULTS
Experiment 6.1, The effects of experience with Chaoborus 165
Experiment 6.2, The effects of experience with benthic prey 171
Experiment 6.3, The habituation hypothesis 182
Experiment 6.4, The success and strength-of-response
hypothesis 186
DISCUSSION 191
The range of responses by trout and kokanee to prey ... 191
Species specific effects of experience with prey 196
Consequences for patterns of prey acquisition 198
SUMMARY 200
CHAPTER 7
TROUT AND KOKANEE FORAGING, THE STRATEGIC POINT OF VIEW
INTRODUCTION 202
The environmental context for trout and kokanee foraging strategies 208
The role of prey size, relative abundance, and physical features of the environment in promoting C-selected or D-selected foraging strategies 217 The role of prey distribution in shaping search and attack components of trout and kokanee foraging strategies 220
The role of temporal patterns of prey renewal in shaping search components of trout and kokanee foraging strategies 229
The role of prey size and abundance in shaping morphological and behavioural elements that function during the attack phase of C-selectedor D-selected foraging strategies 232
SUMMARY 242
REFERENCES 244 LIST OF TABLES
Food overlap calculations for trout and kokanee from Marion Lake.
Seasonal exploitation of chironomid pupae by trout and kokanee.
Taxonomic composition of food items from predators used in food-size determinations.
The relative level of exploitation of Hyalella azteca and Crangonyx richmondensis by trout and kokanee.
Taxonomic composition of prey eaten by small trout and kokanee collected September 7, 1974. 2 Mean number of amphipods per m versus the mean number per predator in different months of the year. Depth-distributions of trout and kokanee under early summer and late summer conditions in Marion Lake.
North-trap versus south-trap captures of trout and kokanee 1974-75.
A comparison of the relative abundance in early summer (April-June) of prey at inshore (depths £2m) and offshore (depths ~>3m) locations in Marion Lake.
A comparison of the swimming velocities of trout and kokanee actively searching for prey in a variety of sub-habitats.
Residence time and the total number of attacks initiated by five trout using the hover and search technique.
A summary of the differences in search techniques employed by trout and kokanee foraging in the field. Reactive distance of trout to targets of known size at the lake surface on two occasions.
xiii XIV
Page
14. The seasonal exploitation of chironomid larvae 94: by trout and kokanee.
15. Distributions of reactive distance of kokanee to 103 stationary ephemeropteran (mayfly) nymphs in low -density and high-density experiments.
16. Head capsule widths (in mm) of larval 108 trichopterans consumed by trout and kokanee.
17. Techniques of approach and capture used by trout 119 and kokanee during attacks on prey in the field.
18. A list of prey types observed to evoke specific 124 approach and capture techniques in the laboratory and in the field.
19. Characteristics of predators and prey used in 134 experiments to determine the attack success of trout and kokanee on a variety of prey.
20. A comparison of capture success and ingestion 138 success of"size-matched" trout and kokanee in attacks on small, agile prey.
21. Species composition of small zooplankton used in 144 experiment 5.3 with trout and kokanee.
22. Means and 95% confidence limits of the maximum 145 attack rates per minute achieved by trout and kokanee exploiting small zooplankton at various densities.
23. Means and 95% confidence limits of the total 145 attacks per .5 hours completed by trout and kokanee exploiting small zooplankton at various densities.
24. A comparison of capture success and ingestion 148 success of "size-matched" trout and kokanee in , attacks on different species of invertebrate prey.
25. The effect of experience with prey in successive 166 feeding trials on attack success of trout and kokanee
26. A comparison of the time to first attack and of 170 total attacks by experienced and naive predators on chaoborus larvae. Characteristics of prey used to predict the expected order of times to first attack.
Characteristics of prey species used and the number of predators involved in trials from which TFA values have been derived.
A summary of the elements which define the foraging strategies of trout and kokanee.
A summary of the adaptive complex that has evolved with respect to foraging by trout and kokanee. LIST OF FIGURES
Figure Page
1. Study organization 8
2. A comparison of the relative proportions of 20 various prey types in the diets of trout and kokanee from Marion Lake, B.C.
3. A comparison of the proportions of trout 24 and kokanee that contain different quantities of chironomid pupae in their diets.
4. A comparison of the size-frequency distribution 26 of all prey eaten by size-matched trout and kokanee.
5. A comparison of the size-frequency distributions 29 of amphipods (Crangonyx sp. and Hyalella sp) eaten by size-matched trout and kokanee.
6. A comparison of the size-frequency distributions 30 of molluscs (Pisidium spp; planorbid snails, Helisoma spp and Menetus sp.) eaten by size-matched trout and kokanee.
7. A comparison of the size-frequency distributions 33 of water column prey exploited by size-matched trout and kokanee.
8. A comparison, on an annual basis, of the relative 35 proportions of prey in the environment and in the diet of trout from Marion Lake, B.C.
9. A comparison, on an annual basis, of the relative 36 proportions of prey in the environment and in the diet of kokanee from Marion Lake, B.C.
10. A comparison of the size-frequency distributions 38 of amphipods in the environment and in the diets of the predators.
11. A contour map.of Marion Lake indicating the 49 locations of both trap and observation sites.
12. A comparison of the relative proportions of trout 56 and kokanee observed at onshore and offshore locations in Marion Lake.
xvi xv ii
Page
13. A comparison of the relative proportions of 59 trout and kokanee netted at two hour intervals, over twenty-four hour periods at various times of the year.
14. A comparison of the relative numbers of trout and 61 kokanee observed at two hour intervals, over sixteen- hour periods at various times of the year.
15. The mean number of chironomid pupae obtained in 65 surface net-hauls taken between early afternoon and late evening on three separate dates.
16. The relative proportions of trout and kokanee 91 that maintain specific search positions while visually scanning the bottom sediments for prey.
17. The relative proportions of trout and kokanee 92 that maintain specific search positions while visually scanning the lake surface for prey.
18. The minimum prey size required to elicit an 98 attack by trout in search positions at various distances from the substrates on which prey are located.
19. Frequency distributions of reactive distances 104 of kokanee responding to either stationary or moving mayfly nymphs.
20. A comparison of the frequency distributions for 106 reactive distance of trout and kokanee to large and small prey types.
21. The relationship between fork length and wet weight 125 of trout and kokanee from Marion Lake.
^22. The relationship between standard length and jaw 126 gape of trout and kokanee from Marion Lake.
23. The relationship between the density of 141 small zooplankton and the maximum attack rates of trout and kokanee.
24. The size-frequency distribution of prey 143 used for the small-plankton, feeding-trials with trout and kokanee.
25. The relationship between consecutive feeding 167 trials with chaoborus larvae as prey and the total number of attacks that trout and kokanee initiate in a given trial. The relationship between consecutive feeding trials with chaoborus larvae as prey and the time to initiate the first attack by trout or kokanee in a given trial.
The effects of changes in experience and prey density on the total number of attacks that kokanee initiate on particular prey types in a given trial.
The relationship between the level of attack success that individual kokanee have with specific prey types and the total number of attacks that individual kokanee initiate on these prey types over four consecutive trials.
The effects of changes in experience and prey density on the time that individual kokanee take to initiate their first attack on specific prey types in a given trial.
The relationship between % attack success of individual trout and kokanee and their variability of response as indicated by the standard deviation of the time to first attack over the last three trials of ex• perience with specific prey types.
The relationship between consecutive trials of exposure to a constant density of no- tonectids and the total number of attacks that trout and kokanee initiate in a given .5 hour trial.
The relationship between consecutive trials of exposure to notonectids and the time to first attack of individual predators in a given trial.
The relationship between consecutive trials of exposure to a constant density of Diaptomus kenai and the total number of attacks that trout and kokanee initiate in a given trial.
The relationship between consecutive trials of exposure to Diaptomus kenai and the time to first attack of trout and kokanee in a given time. The effect of a predator's vertical distance from the lake surface on the diameter of the circular area within which surface prey may be detected. The effect of a predators search position on the size of selected portions of the instantaneous field of search.
An outline of the interactions between the basic structure of the habitat and the stra• tegies which organisms evolve in response to food, predators and competitors. 1
CHAPTER 1
GENERAL INTRODUCTION, GENERAL METHODS AND MATERIALS
Biologists have long been intrigued by differences in morphology and habit among closely related species, for to comprehend the manner and extent of such differences is to comprehend much of the natural control of organic diversity.
T.W. Schoener, 1974.
INTRODUCTION
All organisms are faced with the common challenge of acquiring and processing nutrients and energy in the form of already synthesized high energy compounds or else the raw materials from which they and new protoplasm can be synthesised.
This resource acquisition is never a random process and a great deal of research in the biological sciences may be interpreted as a search for general rules governing nutrient and energy acquisition at levels of organization from the cell to the ecosystem.
Ecologists usually work at or above the level of the whole organism and are concerned with the study of "inter• actions that determine the distribution and abundance of organisms" (Krebs, 1972). A large number of these interactions fall into the category of nutrient and energy acquisition.
Thus, ecologists too are interested in identifying patterns of nutrient and energy acquisition as well as in explaining . the nature of the biological interactions that are responsible for producing the patterns (for example , see discussion in
Paine, 1969 or Schoener, 1971, 1974).
-Most vertebrates and many, invertebrate predators are euryphagic (see De Ruiter, 1967 and Emlen, 1973 for reviews that is, they eat mixed diets containing a number of different types of food organisms. In their search for patterns of nutrient or energy acquisition by animals, ecologists have conducted a great many studies either comparing the dietary habits of closely related species of predators which occur sympatrically or comparing the abundance of food types that are apparently available in the habitat of a predator to the abundance of food types present in the predator's diet. These studies have shown repeatedly that (1.) closely related species of predators acquire different sets of food items, even in
instances where great care has been taken to obtain the pre• dators from the same habitats where they potentially have had access to an identical set of foods (Root, 1967;Pulliam
and Enders, 1971; Schoener, 1974; Paine, 1963; Brown and
Lieberman, 1973; Gwynne and Bell, 1968; Heinrich, 1976; Tyler,
1972; Keast and Webb, 1966) and (2.) each species of predator
exhibits what appears to be density independent exploitation
of foods from the total complex of foods that is apparently
available in a given environment (Root, 1967; Hespenheide,
1975; Gerking, 1962; Levings, 1972; Costa and Cummins, 1972;
Efford and Tsumura, 1973; Moore and Moore, 1976). 3
The types of predators examined in some of the best of these studies include birds (Tinbergen, 1960; Root,
1967; Orians and Horn, 1969; Hartwick, 1973; Hespenheide,
1975)/ fish (see Hyatt, 1979 for review), mammals (Estes and
Goddard, 1967; Gwynne and Bell, 1968; Schaller, 1972; Kruuk,
1972; Brown and Liebermann, 1973; Reichmani 1977), and in• vertebrates (Paine, 1963; Menge, 1972; Fedorenko, 1975).
Having demonstrated differences in the prey contents
of predators compared either to each other or to the natural
environment, an ecologist is faced with the problem of pro•
viding answers to questions about why food resources are
acquired in the way they are. Historically ecologists have
split into groups which have used either a mechanistic or
an evolutionary approach to provide answers for such questions
(Birch and Ehrlich, 1966; Holling, 1968).
The mechanistic or reductionist approach (Emlen,
1973; Horridge, 1977) involves a search for explanations of
dietary patterns in terms of the operation of proximal mech•
anisms. The work of both Holling (1964; 1966, 1968) and Ware
(1971, 1973) exemplifies this approach. To these authors
explanations for specific dietary patterns lie in an analysis
of how behavioural, anatomical or physiological characteristics
of predators influence the probability that they will acquire
some food items more often than others. For example, by
analysing the forces that operate in a mantid's forearm,
Holling (1964) predicted the size of prey that could be grasped 4 best. He then showed in behavioural experiments that the largest number of feeding responses were displayed to prey of just this size. Similarly Ware (1973) explored several visual "mechanisms" that operate during search and detection of prey by rainbow trout in the laboratory and then used these results to explain a number of patterns of prey intake ex• hibited by trout that had been foraging for benthic inverte• brates in the field.
Studies in which a mechanistic approach has been used have often avoided any attempt to provide insights into the nature of the evolutionary forces that have acted to shape the overall "design" of an organism. Accordingly a second group of ecologists has attempted to resolve questions about patterns of food acquisition by employing an evolutionary or "strategic" approach (Schoener, 1971). The work of Schoener
(1965, 1971), MacArthur & Pianka (1966), Emlen (1966), MacArthur and Levins (1967), Root (1967), Royama (1970), MacArthur
(1972), Hespenheide (1975), Diamond (1975), and Pianka (1975), to cite but a few, characterizes this approach to studies of food resource division by predators. To these authors explanations of specific dietary patterns lie in an analysis of how agents of natural selection, operating within a parti• cular environmental context, have acted to shape the foraging strategies of predators as adaptive (or optimal) solutions to problems of energy arid nutrient acquisition. 5
Although mechanistic or strategic approaches to answer questions about the significance of a given dietary pattern have generally been used in a mutually exclusive fashion, they need not be since studies of the proximal mechanisms which promote resource division will often provide information containing a variety of clues that may be used in the search for answers to evolutionary questions dealing with why re• sources are currently partitioned by predators in the way that they are. Indeed the. recent application of a combination of the two approaches in studies of "optimal foraging" by predators has begun to reveal how important the selective pressure to maximize the net energy return from foraging has been in shaping the behaviour of a variety of animals (see examples cited in Pyke, Pulliam and Charnov, 1977: Krebs,
Erichsen and Webber, 1977; Goss-Custard, 1977 or Zach, 1979).
In the present study I have used both mechanistic and strategic approaches in attempting to provide explanations for the
species specific diets of two fishes inhabiting a small fresh• water ecosystem.
The stimulus for the initiation of this study
originated from observations by Efford and Tsumura (1973)
that two similar species of fish (rainbow trout, Salmo gairdneri;
kokanee, Oncorhynchus nerka) inhabiting a small, subalpine
lake in British Columbia displayed substantial differences
in the proportions of various prey types found in their diets
when compared either to each other or when compared to the 6
relative abundance of prey apparently available in the lake
environment. Although differences in the prey contents of
closely related predators or of predators and the natural
environment have been described in numerous field studies
(see references cited above), it is often not clear what it
is precisely that favours-the acquisition of a particular
set of prey items by a given species of predator. This is
certainly true for the dietary patterns exhibited by the trout
and kokanee studied by Efford and Tsumura, thus one of- the
major goals of the present study is to determine how elements
of anatomy, physiology and behaviour interact as proximal
mechanisms which favour the acquisition of species specific
diets by trout and kokanee in the field.
Both Holling (1966) and De Ruiter (1967) have
emphasized that the predation process which generates dietary
patterns has a limited number of simple behavioural components
that serve as the common denominators linking all animals
in their quest for food. Thus, the behavioural chain that
leads from search and detection to final ingestion or rejection
of food items provides a convenient framework around which
to organize studies aimed at revealing the origins of diverse
.dietary patterns. However, few studies have attempted to
explore how morphological, behavioural or physiological charac•
teristics operate to shape dietary patterns over the entire
sequence of foraging events for single species of predators.
Rather the general trend has been to attempt explanations 7 of dietary patterns of predators from the field as a consequence of biological mechanisms that operate during only a single phase of the foraging cycle (eg. during food handling, Rear,
1962; Werner, 1974; Heinrich, 1976; during prey detection,
Murton, 1971;. Ware, 1973; Zaret, 1972; Zaret & Kerfoot, 1975).
This trend is unfortunate since the morphological, behavioural and physiological characteristics that interact at each stage of the foraging cycle are commonly asserted to form part of an adaptive complex that defines the foraging strategy of a given predator (Klopfer, 1973) yet there are few experimental studies which examine how interrelated sets of adaptations influence the range of prey that predators can effectively exploit. Indeed, there are few studies available which define the foraging strategies of predators more precisely than to label them as either energy maximizers or time minimizers
(Schoener, 1971). Consequently, the second major goal of this study is to provide a systematic assessment of the inter• related adaptations that define the foraging strategies of trout and kokanee. To do this requires an assessment of the nature of the "match" between the predator's structures and behaviours on the one hand and their chosen habitat and prey combinations on the other.
The thesis is organized into seven chapters (Fig.
1). The remainder of this chapter deals with general methods and materials used throughout the study. In chapter two I provide detailed comparisons of the dietary patterns exhibited STUDY ORGANIZATION
CH. 2
DIETARY PATTERNS DESCRIPTIONS
CH. 3 Y
THE ROLE OF SPATIAL OR TEMPORAL SEGREGATION
CH. 4 1 CH.7 Y THE ADAPTIVE NATURE THE ROLE OF PREDATOR OF TROUT AND KOKANEE SEARCH BEHAVIOUR FORAGING STRATEGIES A
CH. 5
THE ROLE OF ATTACK BEHAVIOUR AND PREDATOR MORPHOLOGY
CH. 6
THE ROLE OF SHORT TERM EXPERIENCE 9
by free ranging trout and kokanee in the lake environment.
In chapters three through six I use a strictly mechanistic approach to test hypotheses about how proximal factors shape the dietary patterns that trout and kokanee exhibit under natural conditions. This series of chapters is organized along the same lines as the series of "decisions" each predator must make while foraging. Thus, chapter three deals with where and when the predators, choose to forage, chapter four deals with how the predators search for prey, chapter five deals with interactions between morphological and behavioural characteristics during the attack phase of foraging and chapter six deals with the role of short term experience with prey in altering predator responses to prey. Finally in chapter seven, I use a strategic approach to reassess results from the preceding chapters in an attempt to precisely define the foraging strategies of trout and kokanee in terms of inter• related sets of morphological and behavioural adaptations addressed to specific habitat-prey combinations.
GENERAL METHODS AND MATERIALS
The Study Area
Populations of rainbow trout (Salmo gairdneri) and kokanee (Oncorhynchus nerka) in Marion Lake, British Columbia formed the focus for the present study. Marion Lake (also known as Jacob's Lake) is situated approximately 50 kilometers east of
Vancouver in a research forest operated by the University of British Columbia (latitude 49° 19° N, longitude 122° 33' W). For ten years (1964-1974) the Marion Lake ecosystem was the focus of intensive study sponsored by the National Research Council of
Canada, the University of B.C. and by the Canadian section of the International Biological Program. Efford (1972) reviewed the general objectives of the program and a number of authors
(Efford, 1972; Hall & Hyatt, 1974) have reviewed the progress of research directed towards these objectives.
The basin of Marion Lake is 800 m long and about 200 m wide at its maximum. The major inlet stream enters from the north. During the dry summer season, when the present study was conducted, the lake has a maximum depth that varies from 5 - 6 m, a mean depth of 2 - 2.5 m and is approximately 10 hectares in area.
The lake margin along the eastern shore is ill-defined and consists of a boggy zone in which the water level varies considerably. Vegetation in this zone is dominated by sedges, the small shrub Myrica gale, and other shrubs and small trees such as salmon berry (Rubus spectabilis) and alder (Alnus rubra).
The western shoreline has a steeper slope and is covered by stands of red cedar (Thuja plicta), western hemlock (Tsugo heterophylla) and willow (Salix spp.) to. the waters edge. There are only four types of rooted aquatic plants that are abundant. These cover
22% of the lake area (Davies, 1970; Neish, 1971) and include
Potomageton natans, P_. edihydrus, Isoetes occidentalis and
Nuphar polysephala. Dense beds of Chara globularis are found in association with a large spring at the south end of the lake. 11
Isoetes occidentalis occurs in water deeper than 2 m but 80% of the macrophytes occur in water less than 2 m deep.
Approximately 78% of the lake bottom consists of open mud (a deep flocculent ooze known as gyttja). The surface of shallow water sediments (depths less than 2 m) is covered by litter composed of leaves, needles, twigs and branches derived from weed beds and emergent vegetation around the lake. There is a gradual shift to much finer sediments covered by less litter in the deeper areas of the lake. During the summer a sparse cover of filamentous algae and diatoms occurs on the surface of open mud areas in water deeper than 1 meter. At depths of less than 1 meter there is often a thick mat of benthic algae composed of single celled and filmentous forms.
Marion Lake contains five species of vertebrate predators that are resident. These include three fishes (rainbow trout,
S_. gairdneri; kokanee, O. nerka; three spine stickleback,
Gasterosteus aculeatus ) and two salamanders (Pacific coast newt,
Taricha granulosa; the neotonous form of the Northwestern salamander,
Ambystoma gracile). In addition to the present dissertation, studies of the predators that have been completed or are in progress include; population dynamics of the salmonids, salamanders and sticklebacks (Sandercock, 1969; Neish, 1970; McPhail, in progress); predatory behaviour of rainbow trout, salamanders and sticklebacks under laboratory conditions (Ware, 1971; Neish, 1970;
Burko, 1975); and dietary habits of salamanders, salmonids and sticklebacks in the field (Efford & Tsumura, 1973; Hyatt, in progress). 12
Characteristics Of Trout And Kokanee
Rainbow trout and kokanee are both members of the
family Salmonidae which is composed of freshwater and anadromous
fishes that range widely in the waters of the northern hemisphere.
It is the dominant family of fishes in the northern waters of
North America, Europe and Asia (Scott & Crossman, 1973). Both
species are of great importance as commercial or recreational resources, and the rainbow trout is a standard laboratory animal
for a wide range of physiological investigations. The literature dealing with various aspects of the biology of these two species
is massive and I will not attempt to summarize it here.
Key references that may be consulted for additional background on rainbow trout may be found in Scott & Crossman,
1973 (general review of life history characteristics); MacCrimmon,
1972 (review of native and present global distribution); Neave,
1944; Hartman and Gill, 1968 (habitat associations); Jenkins, 1969;
Newman, 1960; Slaney and Northcote, 1974 (social organization and behaviour); Ware, 1971; Bryan, 1972 (feeding behaviour).
Key references that may be consulted for additional background on kokanee or sockeye salmon (the two are taxonomically
indistinguishable) include: Foerster, 1968; Scott and Crossman,
1973 (general review of life history characteristics); Nelson,
1968 (natural distribution); Vernon, 1957; Northcote, 1973; Lorz
and Northcote, 1965; Beach, 1974; Irizarry, 1975 (characteristics of lake dwelling populations); Foerster, 1968; Behnke, 1972,
Hartman and Burgner, 1972; Goodlad et al., 1974 (habitat 13 associations); Newman, 1960; Hoar, 1976 (social organization and behaviour); Rankin, 1978; Eggers, 1978 (feeding behaviour);
Hoar, 1976 (evolution and phylogentic affinities).
Study of trout and kokanee in the Marion Lake ecosystem offered many advantages for the pursuit of knowledge about foraging behaviour. The two species constitute self sustaining populations which are genetically isolated and complete their life cycles within the confines of the watershed of which Marion
Lake is a part. The absense of both extensive migrations by
Marion Lake fish and of gene flow from other populations potentially reduces the uncertainty, encountered in other studies, about whether particular traits are locally adaptive or related to some other habitat (Morse, 1971; Birch and Ehrlich, 1967; Van
Balen, 1973). Growth rates of both species in Marion Lake are among the lowest recorded across their geographic range and there
is little doubt that this is related to a limited food supply
(see Hall & Hyatt, 1974 for details), thus selection for a locally adaptive foraging strategy should be rigorous. Detailed analysis of the dietary habits of the predators (Sandercock, 1969; Efford
& Tsumura, 1973 and Hyatt, unpublished data) and extensive data on the distribution, abundance and production levels of their prey
(Hamilton, 1965; Hargrave, 1969; Mathias, 1971; Winterbourn, 1971;
McCauley, unpublished data) provided an almost unprecedented opportunity to relate details of dietary patterns and foraging behaviour to a known ecosystem context.
The nature of the questions asked in this study required a combination of laboratory and field investigation. I carried 14 out the bulk of the quantitative field observations during the summers of 1971 and 1972. Results from this work helped shape the laboratory experiments to examine the fine scale details of food gathering and responses of the predators to some major seasonal changes. I completed most of the laboratory work during the summers of 1974 and 1975.
Collection Techniques
Trap nets, gill nets, seine nets and a wire cylinder were used to obtain fish for various purposes. I used the wire cylinder exclusively to obtain uninjured fish for laboratory experiments. At night, from a boat equipped with auto head• lights, it was possible to locate trout and kokanee in shallow water. Because both species exhibit very low activity under conditions of darkness it was possible to place a wire cylinder
(diameter 1 m, depth 2 m) over them, dipnet them into a holding container, and carry them uninjured to the laboratory.
Laboratory Animals and Standard Experimental Procedures
Trout and kokanee used in laboratory experiments were captured, handled and maintained under identical conditions unless otherwise specified. Fish were housed individually in
40 - 80 liter glass and stainless steel aquaria at a lakeside site. Each aquarium received natural illumination and a constant supply of cold (10°C + 2), spring-fed water. Fish were main• tained on a diet of chicken liver when not involved in experiments.
A series of 200 liter aquaria (dimensions: L=92 cm,
W=48 cm, D=46.5 cm) in a nearby laboratory building served as experimental "arenas" for the majority of feeding trials. All laboratory experiments were conducted under conditions of constant light and temperature (10°C +2). Illumination was provided by a bank (seven 100 watt bulbs) of incandescent lights mounted 30 cm above the water surface. A sheet of white, translucent, plastic; positioned between the lights and the arena, served as a diffuser.
Flat-white partitions, arranged around the sides of the arena provided a constant background against which prey were presented.
During a pre-experimental period, each predator was conditioned to feed freely after transfer from its home aquarium to the arena. This process usually required one to two weeks following capture from the field. The hunger level of trout and kokanee was standardized before all experiments by depriving the predators of food for 48 - 72 hours. Results from other studies
(Ware and Hyatt, unpublished results) indicated that fish required
40-60 hours at 10° C to completely digest a satiation ration.
The standard procedure for experiments consisted of gathering the required number and type of prey from Marion Lake and holding them in plastic containers, without food, for up to
48 hours. The prey were introduced to the experimental arena and allowed 30 minutes to disperse before the introduction of a predator. Specific aspects of the predator's feeding behaviour were recorded chronologically on a Rustrac, 4 channel, chart recorder. Single feeding trials usually lasted 30 minutes at which
time the predator was returned to its home aquarium. The arena was drained and cleaned following each trial to facilitate
recovery and counting of remaining prey. 16
Measurements On Predators And Prey
During the pre-experimental period trout and kokanee were anaesthetized with MS-222, weighed to the nearest gram, and measured for total length to the nearest mm. jaw measurements were obtained from preserved samples of predators by using sliding vernier calipers. Live invertebrates used in each feeding trial were photographed before and after each trial, in a white enamel pan, containing a mm rule for reference. Body lengths or widths, where required, were obtained at a later date with calipers
from the image of the prey projected onto a screen. Measurements on very small prey such as zooplankton were obtained from preserved samples by using a dissection microscope (Wild M-5), equipped with an ocular micrometer. 17
CHAPTER 2
THE SPECIES SPECIFIC DIETARY PATTERNS OF TROUT AND KOKANEE IN MARION LAKE
To do science is to search for repeated patterns, not simply to accumulate facts. Repetitions of patterns in nature are usually imperfect and this gives us the means of making comparisons which may then serve as the seeds of testable hypotheses.
R. MacArthur, 1972.
INTRODUCTION
Two types of comparisons have frequently been used to draw inferences about the foraging behaviour of predators.
The diets of similar species are compared to each other, or the dietary composition of a particular predator is compared to the apparent availability of prey in the environment. In this section I will deal with both types of comparisons and comment on the nature of the inferences that they allow.
METHODS
Initial analysis of trout and kokanee diets from
1963-1966 (Efford & Tsumura, 1973) indicated substantial differ• ences in their patterns of food exploitation. The original analysis was based upon trout of 10-25 cm in length while kokanee were generally less than 15 cm long. Thus, I was interested in determining whether the species specific dietary patterns were primarily a consequence of differences in the average size of 18 predators included in the original analysis or if the differences would persist given comparisons limited to predators of similar size. Therefore, I analyzed some "size-matched" predators obtained from either the 1963-66 collections or from new collections taken between 1972-76. The new collections allowed me to extend the comparisons to fish of smaller body size than those examined by Efford & Tsumura.
Details concerning the times, locations and techniques of capture for the 1963-66 collection are available elsewhere
(Efford & Tsumura, 1973). Specimens from the 1972-76 collection, used in the present analysis, were collected by dip-netting at night from a boat equipped with lights. This ensured that trout and kokanee were matched not only for size but for location
(within an area of a few hundred square meters), and time of
capture (between 11 P.M. and 1 A.M.) as well. The majority of
fish in the 1972-76 collection were taken from depths of less
than 2 m in the northeast corner of Marion Lake. Freshly sampled
fish were immediately killed in 70% ethanol and then transferred
for longer term storage to 10% formalin.
To obtain size-frequency data on prey, I used a
dissection microscope (Wild M-5) equipped with an ocular micro• meter. Three measurements (length, head width, maximum body
width) were taken from each prey. Size frequency distributions
of prey are based on either body lengths or area (area = length
x maximum width). Frequency distributions are based upon length
when prey are of reasonably uniform shape. In order to provide
greater accuracy, distributions are based upon area when prey 19 include a variety of shapes (tubular, spherical, pentagonal etc...).
To construct representative size-frequency distributions of food items in the diets of trout and kokanee, I sorted fish, matched as closely as possible for size, from collections taken on May 26/64, June 10/66 and August 11/63. Prey measurements were taken from a total of 41 predators, with no fewer than 5 fish of each species from each month. Because the total number of food items in a sample of fish for any month varied considerably (range 213-1228), I applied a weighting factor to each month's samples. This guarantees that the food items from any month's samples have an equal influence on the shape of the size-frequency distribution constructed from data pooled for the three months.
RESULTS
Between Predator Comparisons
Examination of the taxonomic composition of the diets by weight or by numbers (Fig. 2a & b) indicates that over the course of a year trout and kokanee exploit significantly different proportions of each major prey type. There are numerous examples of prey types exploited extensively by one predator but barely utilized by the other. The four prey types (Trichoptera,
Amphipoda, Odonata and planorbid snails) that make up 69% (by weight) of the diet of trout contribute only 17% of the weight of prey in the diet of kokanee. Over the course of a year, chironomid larvae, pupae, and cladocerans were more important dietary items for kokanee (48% by weight) than for trout ( 8% by weight). 20
FIGURE 2. A comparison of the relative proportions of various
prey types in the diets of trout and kokanee from
Marion Lake, B.C. (a) Diet as % by weight (b) Diet
as %. by numbers. Data pooled from samples of fish
collected in the months of Nov., Feb., April, June
and Aug. Trout and kokanee were not rigorously size-
matched for analysis. All tests for significant
differences in exploitation of single prey types
by predators are based upon the normal approximation
to the binomial distribution (Siegel, 1956).
++ w = .01, + ^ = .05. Data adopted from Efford and Tsumura, 1973. KOKANEE TROUT
yo OF Dl ET BY WEIGHT Notonect ids Cor i x i d s Neuropteran larvae Pi s i d i u m S i mul ium larvae Copepods J Ephemeropt'eran larvae Plecopteran larvae Aquatic beetle adults Planorbid snaiIs Odonate larvae C ladocerans Chironomid larvae Amphipods Chironomid pupae Terrestrial insects Trichopteran larvae 40 30 20 10 10 20 30 40
© °/Q OF Dl ET BY NUMBERS
Aquatic beetle adul ts ++ N = 4430 N=3038 Ephemeropteran larvae ++ Simulium larvae++ Terrestrial insects++ . P i s i d i u m+ Odonate larvae + + Copepods Trichopteranlarvae ++ Planorbid snai Is++ Amphipods++ Chironomid larvae+ + Cladocerans Chironomid pupae,'+ + 50 40 30 20 10 10 20 30 40 50 The degree of dietary similarity between trout and kokanee fluctuates substantially from month to month. For com• parisons of monthly changes in the degree of food similarity I have used the overlap measure of Morisita (1959) and Horn (1966).
The overlap coefficient CX varies from zero when the samples are completely discrete to one when the samples are identical.
where: s is the total number of food categories s 2? _ , x.y. x^ is the proportion of the diet
1 = ^"'i=. l~ i=i of predator x taken from the i t 2 y . fooisd the proportion of the diet T x±+ z . y± 1 of predatocategorr yy taken from the i th. food category
Although no statistical method is available to test the signif- icance of CX , other authors (Zaret & Rand, 1971; Fedorenko,
1975) have assumed that values equal to or greater than .60 represent significant overlap. In comparisons of food overlap
in birds it is not unusual for all values to be greater than .60
(Orians & Horn, 1969; Pulliam & Enders, 1971) . By this criterion trout and kokanee exhibit close overlap in only one month df the year (Table 1). 22
TABLE 1. Food overlap calculations for trout and kokanee from Marion Lake. Numbers in brackets indicate the year in which the sample was taken.
Overlap by weight Feb.(64) April(66) June(66) Aug. (63) Nov.(63) Pooled
.018 .474 .463 .201 .736 .443
Overlap by numbers
.440 • 462 .243 .245 .881 • 136
Some prey types such as chironomid pupae are eaten in large numbers by both trout and kokanee over the course of a year. Because of individual variability in the number of pupae eaten, the means of the number of pupae eaten in any given month by the two predators are not significantly different (Table 2.).
However, this does not signify that trout and kokanee are equally likely to exploit chironomid pupae. Indeed the variance around the mean number of pupae eaten by trout or kokanee tends to obscure the fact that individual kokanee are more likely to contain relatively large numbers of pupae than are individual trout. For example, data pooled from an equal number of trout and kokanee captured between 1963 and 1974 indicates that kokanee eat significantly larger numbers of chironomid pupae (Kolmogorov-
Smirnov two-sample test, X = 27.03, degrees of freedom = 2,
p <.001) than trout (Figure 3). Although only 6% of 163 trout
examined contained more than 40 chironomid pupae in their guts,
28% of 163 kokanee examined contained 40 or more pupae. Further•
more, 75 of the 163 trout examined contained no pupae at all TABLE 2. Seasonal exploitation of chironomid pupae by trout and kokanee. N is the sample size and S.D. the standard deviation of the means.
Mean number of Mean number of Month pupae per trout S.D. pupae per kokanee S.D. N
February 0.00 .58 1.0 12 April 10.14 17.4 56.86 36.3 7 May 93.75 181.5 274.93 246.0 16 June 19.62 22.2 50.71 55.9 21 July 1.82 3.2 17.09 21.0 11 August 7.35 9.5 19.85 32.6 40 September 1.20 1.8 16.53 19.8 15 October .31 .9 27.77 22.0 13 November 3.92 9.2 13.00 21.4 24 December 0.00 - 0.00 - 4
Data pooled from predators collected between 1963 and 1974 by Hamilton (unpublished results), Sandercock (1969), Efford and Tsumura (1973) and Hyatt (present study). 24
FIGURE 3. A comparison of the proportions of trout and kokanee
that contain different quantities of chironomid
pupae in their diets. Data pooled for equal numbers
of trout and kokanee captured in various months (see
Table 2) between the years 1963 and 1974. N = number
of trout or kokanee examined. TROUT KOKANEE
CO X N = 163 N = 163 o < 100 + o 9 I -100
81 - 90 cwo 71 - 80 Uorl a UJ 61 -70
51 - 60
5 O 41-50 z o D£ 31-40 X o O 21 - 30 a: UJ co I I - 20 5 r 0 - 10
80 70 60 50 40 30 ; 20 10 0 10 20 3 0 4 0 50 60 70 80
% OF PREDATORS EXAMINED
to 0) while only 40 of 163 kokanee examined failed to contain
chironomid pupae.
Size-frequency Distributions of Food Items
The size-frequency distributions of prey from size- matched trout and kokanee are similar (Fig. 4), however, this may be misleading. Numerically trout obtain 8% of their diet
from the largest size-classes of prey while kokanee take only
1% of their diet from prey of these sizes. Efford and Tsumura have indicated that items constituting only 8% of trout diet by number may form as much as 50% of the total food intake by weight. Thus, small differences in numbers at this end of
the prey size-distribution may have considerable significance
for energy intake. Trout undoubtedly obtain a greater proportion of their diet from large size classes of prey
(terrestrial insects, snails, odonates, trichopterans) while kokanee exploit the smallest size classes (zooplankton) more
intensively (Table 3) .
Differences in the sizes of prey exploited by trout
and kokanee are not entirely due to differences in the type of prey exploited. Within a category of prey there are frequently differences in the size-distributions of individuals consumed.
A sample of size-matched trout and kokanee (Table 4) from June,
1966 was examined for the size-distributions of amphipods
exploited. Relative to kokanee, rainbow trout consume greater
proportions of the large size-classes of amphipods (Fig. 5). A 26
FIGURE 4. A comparison of the size-frequency distributions of
all prey eaten by size-matched trout and kokanee.
N = the total number of prey items measured and
pooled from all predators examined. Data pooled from
samples of fish collected in the months of May, June,
and August. KOKANEE N = 1765
~~i r~ 1 1 1 1 1 1 r 40 30 20 10 0 10 20 30 4(
% OF FOOD ITEMS EATEN TABLE 3. Taxonomic composition of food items from predators used in food-size determinations.
Trout Kokanee
No. examined 25 16
Mean length (cm) 14.8 14.0
Range 11.5-17.5 12.0-15.8
% No. %
Chironomid larvae 744 31.6 370 9.6
Chironomid pupae 954 40.5 2,797 72.3
Chironomid adults 278 11.8 97 2.5
Zooplankton 76 3.2 511 13.2
Pisidium sp. 37 1.0
Terrestrial insects 125 5.3 23 .6
Mollusca (snails) 52 2.2
Trichoptera 46 2.0
Amphipoda 27 1.2 22 .6
Odonata 20 .9
Other 34 1.4 13 .3
Total items 2,356 3,870 28
closer examination of the data reveals that this difference originates largely from differential exploitation of a small
species of amphipod (Hyalella azteca, sizes to 4 mm) by kokanee, and of a larger amphipod (Crangonyx richmondensis,
sizes to 10 mm) by trout (Table 4). Similarly, because kokanee
consume primarily the small bivalve Pisidium spp. (generally
less than 2 mm) and trout concentrate on pulmonate molluscs
(Helisoma and Menetus spp., sizes to 10 mm), the size-
frequency distributions for molluscs eaten by the predators are
significantly different (Fig.5). Winterbourn*s (1971) examination
of trichopterans, exploited by trout and kokanee, revealed that
trout exploit the largest size classes of caddis larvae available
(sizes to 20 mm) at all times of the year. The caddis larvae
present in trout stomachs accurately reflected the succession of
species moulting to the final instar during the year. Kokanee
exploited very few caddis larvae and those that were taken
belonged to the smallest species in the lake (Oecetis inconspicua,
body lengths to 4 mm)..
TABLE 4. The relative level of exploitation of Hyalella azteca and Crangonyx richmondensis by trout and kokanee.
Trout Kokanee No. examined 12 9 Mean length (cm) 14.9 15.1 Range 10.5-16.7 12.8-16.5 No. of Crangonyx 96 21 sp. eaten No. of Hyalella 89 77 sp. eaten Hyalella/Crangonyx 1.0/1.1 3.7/1.0 29
FIGURE 5. A comparison of the size-frequency distributions of
amphipods (Crangonyx sp. and Hyalella sp.) eaten
by size-matched trout and kokanee. N = the total
number of prey items pooled from all predators
examined. Data obtained from samples of fish collected
in the month of June.
30
FIGURE 6. A comparison of the size-frequency distributions of
molluscs (Pisidium spp.; planorbid snails, Helisoma
sp. and Menetus sp.) eaten by size-matched trout
and kokanee. N = the total number of prey items pooled
from all predators examined. Data obtained from
samples of fish collected in the months of May, June
and August. KOKANEE N = 41
i 1 1 r- —r- 60 40 20 20 40 60 80
% OF MOLLUSCS EATEN
CO o 31
Results presented so far have dealt mainly with trout i and kokanee between 10 and 17 cm in length. However, dietary
differences are not restricted solely to predators within this
size range. Size-matched, young-of-the-year trout and kokanee
collected in Sept./74 exhibit interesting differences in diet
composition in spite of the fact that animals of both species
obtained greater than 95% of their diet from just two prey groups
(zooplankton and dipterans). Small trout (average length 5.6 cm)
intensively exploited the cladoceran Sida crystallina, a
significant number of dipterans, terrestrial insects and a
few water mites (Table 5). By contrast, small kokanee (average
length 7.9 cm) exploited a greater diversity of zooplankton,
larger numbers of dipterans and almost no terrestrial insects.
These differences are surprising since the fish were sampled
within 2-3 hours of each other from virtually the same micro-
habitats .
Results of size-frequency analysis of prey (Fig.7),
reveal that kokanee, in spite of their larger size in this
sample, intensively exploit smaller size classes of prey
(primarily small cladocerans such as Bosmina sp. and copepods
such as Cyclops sp.) than trout do.
Comparisons of the Relative Proportions of Various Prey Types in the Natural Environment and in the Diets of Trout and Kokanee.
The dietary differences between trout and kokanee are
closely paralleled by differences between the apparent availability
of prey in Marion Lake and the prey exploited by each species of 32
TABLE 5. Taxonomic composition of prey eaten by small trout and kokanee collected September 7, 1974.
Trout Kokanee
No. examined 9 9
Mean length (cm) 5.6 7.9
Range 4.3-6.6 6.9-8.5
Zooplankton No. % No. %
Sida sp. 1,219 90.2 184 19.7 Bosmina sp. 2 .1 166 17.8 Chydorus sp. 1.1 Leptodora sp. 5 .5 Ceriodaphnia sp. 1 .1 Polyphemus sp. 1 .2 2 .2 Alona sp. 2 .2 Cyclops sp. 291 31.2 Mites sp. 9 .7 5 .5 Ostracods 2 .2
Diptera
Chironomid larvae 31 2.3 103 11.0 Chironomid pupae 16 1.2 124 13.3 Chironomid adults 39 2.9 24 2.6
Other
Amphipoda 9 1.0 Trichoptera 6 .4 3 .3 Odonata 2 .2 Ephemeroptera 3 .2 1 .1 Terrestrial insects 18 1.3 2 .2
Total 1,345 933 33
FIGURE 7. A comparison of the size-frequency distributions of
water column prey (primarily zooplankton and chironomid
pupae) exploited by size-matched trout and kokanee.
N = the total number of prey items pooled from all
predators examined. Data obtained from samples of
fish collected in the same microhabitats and at the
same time of day during the month of September. 3200 + TROUT KOKANEE N= 1345 N= 933
2560-2720
3> 1920-2080 >- UJ cr a. o 1280-1440] x —t o UJ 640-800
1 0-160 u" T i 1 1 r ~~T~ "T 40 30 20 30 40 10 0 10 20 % OF PREY EATEN
Ul u> 34
predator. On an annual basis, a large proportion of the diet of
both trout and kokanee consists of a relatively small number of prey types. Furthermore, when compared to the proportions of prey
apparently available in the lake, it is clear that each predator does not exploit the full range of prey in proportion to either
their weights or numbers (Figs. 8 and 9). There are numerous examples of intense utilization of poorly represented prey types and of failures to use other numerically abundant prey present in
the lake. The same situation prevails with respect to utilization of individual species within major prey groups. Out of nearly
100 species of chironomids found in Marion Lake, only 19 have been found in the diets of trout and kokanee (Efford & Tsumura,
1973) . Some of the most abundant species by volume or by number do not appear in the diets of fish at all (e.g. Pegastiella sp.A,
23% by no.; Phaenospectra protextus & Polypedelium spp.,
29% by vol.).
The utilization of many prey types bears little relation to seasonal changes in their apparent availability. The intense utilization of amphipods by trout in Aug. coincides with their greatest abundance (Table 6) but trout exploit equally large numbers in the month of June when amphipod numbers are at their lowest levels. Kokanee display similar discrepancies in intensity of amphipod use as compared to apparent amphipod abundance. The peak utilization of chironomid pupae occurs in May and June for fish and by July-August the mean number of chironomid pupae per stomach in fish is less than one tenth the May-June value (see data in Table 2). However, all the available evidence indicates 35
FIGURE 8. A comparison on an annual basis of the relative
proportions of prey in the environment and in the diet
of trout from Marion Lake, B.C. (a) % by number,
(b) % by weight. Note the changing scale along the
abscissa. Data modified after Efford and Tsumura
(1973) plus unpublished records of relative prey
abundance. 35a
ENVIRONMENT TROUT
1. SIALIS 2. EPHEMEROPTERA 2.
3. ODONATA 3.
4. OLIGOCHAETES
5. TRICHOPTERA 5.
6. CERATOPOGONIDS 6.
7. HIRUDINEA .
8. PLANORBIDAE 8. 9. PIS1DIUM 9. 10. CHIRONOMID PUPAE 10.
11. AMPHIPODA II.
12. CHIRONOMID LARVAE 12. 13. MEIOFAUNA 13. r 100 10 10 loo % BY NUMBER
1. CHIRONOMID PUPAE
2. PISIDIUM 3. MEIOFAUNA 4. CERATOPOGONIDS
5. EPHEMEROPTERA
6. OLIGOCHAETES
7 AMPHIPODA
8. SIALIS
9. ODONATA
10. TRICHOPTERA
11. PLANORBIDAE 12. CHIRONOMID LARVAE
13. HIRUDINEA li i till 60 40 20 40 60
% BY WEIGHT'
NOTE: LOG SCALE ON ABSCISSA 36
FIGURE 9. A comparison on an annual basis of the relative
proportions of prey in the environment and in the
diet of kokanee from Marion Lake, B.C. (a) % by
number, (b) % by weight. Note the changing scale
along the abscissa. Data modified after Efford and
Tsumura (1973) plus unpublished records of relative
prey abundance. 36a
ENVIRONMENT KOKANEE
1. SIALIS 2. MAYFLY
3. ODONATES 3.
4. OLIGOCHAETES 4.
5. CADDIS 5.
6. CERATOPOGONIDS 6.
7. LEECHES 8. PLANORBIDS
9. PISIDIUM 9. 10. CHIRONOMID R • 10.
11. AMPHIPODS II.
1.2. CHIRONOMID L. 12.
13. MEIOFAUNA 13. "T T ~T~ 10 "ioo 100 10 % BY NUMBER
1. CHIRONOMID P.
2. PISIDIUM 2.
3. MEIOFAUNA 3. 4. CERATOPOGONIDS
5. EPHEMEROPTERA 5.
6. OLIGOCHAETES 6.
7. AMPHIPODS
8. SIALIS
9. ODONATES 10. 10. CADDIS II. 11. PLANORBIDS 12. 12. CHIRONOMID L. 13. 13. HIRUDINEA l l' I l I TT II Hill I T—l I | 60 40 20 10 I I 10 20 40 60 % BY WEIGHT
NOTE •• LOG SCALE ON ABSCISSA 37 that the number of chironomids pupating and emerging in July and
Aug. is as great or greater than that recorded in May and June
(Efford & Tsumura, 1973; Hamilton, 1965; McCauley, pers. comm.).
Many of the differences between prey included in the diet and those randomly sampled from the lake are related to organism size. I have already mentioned that when caddis larvae are abundant as small, early, instars; trout continue to exploit the large fourth and fifth instar stages of less abundant species.
The same pattern emerges from a comparison of the amphipods exploited by trout compared to those present in the environment
(Fig. 10a). During June, the largest size classes of amphipods are many times more abundant in the stomachs of trout than expected from their relative abundance in the lake population. For kokanee the pattern is different (Fig. 10b) and includes a higher proportion of small amphipods.
TABLE 6. Mean number of amphipods per m versus the mean number per predator in different months of the year.
Feb. April June Aug. Nov.
Amphipods 1594 1724 1100 2478 1657
Amph ipods/Trou t .25 2.79 5.69 5.67 .50
Trout examined 12 14 24 45 18
Amphipods/Kokanee .38 2.14 1.92 .28 2.58
Kokanee examined 18 7 12 24 19 38
FIGURE 10. A comparison of the size-frequency distributions of
amphipods in the environment and in the diets of the
predators. Data for sizes of amphipods present in
the environment were obtained from samples taken
during June of 1969. Data for sizes of amphipods in
the diets of predators were obtained from samples
taken in June of 1966. 38a
ENVIRONMENT TROUT N = 560, 1969 N = 209 ,1966
E E
o c
—
>> O X)
LU N CO
Q O Q. X 12 H CL
I0H
T—i—i—i—r "i—i—i—r 10 20 30 40 50 % OF TOTAL AMPHIPODS PRESENT 39
DISCUSSION
A variety of comparisons presented above indicate that the individual "sampling" activities of trout, kokanee and scientists in Marion Lake each result in the acquisition of different sets of invertebrate "prey". Ultimately such differences must be related to differences in when, where, and how inver• tebrates are obtained from the lake environment by each of these
"predators".
It should not be particularly surprising that the relative abundance of invertebrate prey types in the diets of trout and kokanee do not closely follow the apparent abundance of these same invertebrates in the lake environment given that the characteristics of the "sampling gear" and procedures used by scientists and predators are inherently so different. For example, it is most often the case that man-made sampling devices are designed and employed to obtain samples of a wide range of invertebrates in proportion to their actual densities in the natural environment. Thus plankton nets or benthic grabs used in lakes are relatively non-selective in that they tend to acquire the majority of organisms within the space sampled by the device. By contrast predators such as trout and kokanee have been "designed" through natural selection to exploit a relatively limited portion of the total range of invertebrate prey that reside in a given environment and may frequently acquire some prey items rather than others due to subtle differences in characteristics such as prey size, colour, escape responses, armour, texture or taste. Furthermore, while the sampling protocol 40 used by scientists is often arbitrarily fixed, that of any predator will shift continuously in response to slight changes in general environmental conditions or prey characteristics. Thus, it is important to keep in mind that the apparent availability of prey types as measured by a scientist using a particular mechanical device will often constitute a poor index of the availability of prey to a given predator.
Because there are so many obvious differences between the design and operation of man-made sampling devices and the
"design" and sampling procedures of predators, it is possible to predict with some certainty that differences in the prey sets acquired by scientists and predators will be the result of a variety of predator characteristics that function during each stage of the foraging cycle from search to final ingestion of prey. By contrast, differences in the "design" and operation of trout and kokanee as predators are not at all obvious and thus there is considerable uncertainty about the identity and relative importance of various predator characteristics which will promote the acquisition of species specific diets. For example, it is not clear whether trout and kokanee in the field acquire species specific diets because they search for prey in different locations, search for prey at different times, search for prey by using different techniques, respond to different prey once detected, approach or capture prey by using different techniques, or choose to ingest or reject different prey once captured. The potential exists for any one or all of these factors to contribute to the observed patterns of prey acquisition, 41
thus any attempt to truly understand the basis for the different prey sets acquired by these predators in the field must entail a systematic enquiry into the role that each of these factors play.
The need for a systematic approach to assess the mechanisms that favour differential acquisition of prey by predators has not been generally recognized by field ecologists studying the dietary habits of animals. Having established the existence of a particular dietary pattern many ecologists have relied upon one or two simple hypotheses as explanations for the pattern. The most common of these are (1) that availability (in the sense of physical proximity) is the main factor which determines the set of prey obtained and implicit in this that predators are incredible generalists that simply accept food items as they appear or (2) that active selection and avoidance of food items by predators controls the set of prey acquired. This implies that predators are phenomenally choosy about the items that they eat in an environment where a great diversity of prey are simply there for the taking. By themselves, neither of these views has much scientific merit and their repeated expression without qualification (Allan, 1942; Houde, 1967; Siefert, 1968;
Hutchinson, 1971; Cody, 1974 and Engel, 1976 to name but a few) has accomplished little other than to obscure the nature of the actual range of mechanisms that do control the non-random acquisition of prey by predators in the field.
In previous work (Hyatt, 1979), I have stressed that each phenomenon of non-random exploitation of prey should be considered to be a function of several potential mechanisms 42
operating alone or in concert. Here the pattern of predator specific exploitation of prey by size will serve as an example.
Caddis larvae (Trichoptera) found in the diet of trout are considerably larger than those exploited by kokanee. The simplest inference to make is that trout are capable of handling larger prey than kokanee. This inference receives circumstantial support from the fact that to all outward appearances trout are heavier- bodied and have larger jaws than kokanee of similar length. How• ever, other hypotheses provide competing explanations for the same dietary pattern. For example, not only are the caddis larvae that trout obtain larger than those obtained by kokanee but they also belong to species which live primarily in weed beds along the lakeshore (Winterbourn, 1971) . The species exploited by kokanee are restricted to open sediment areas throughout the lake. Thus, the pattern described above may be explained by invoking differences in habitat selection by the predators which in turn exposes them to different distributions of prey. Similar competing hypotheses are applicable as explanations for the species-size patterns of mollusc exploitation by trout and kokanee. Various authors have suggested that the sampling of both predators and prey from identical locations eliminates this problem but this will only be the case where predators and prey are relatively immobile over a period of time that includes the most recent foraging bout. In the present study, as well as in many others, this assumption is seriously violated. Predators such as trout and kokanee are highly mobile, thus, capture at a particular location does not guarantee that food items they 43 contain were also obtained from that location.
The difficulty of competing hypotheses as explanations for a given dietary pattern is by no means unique to this study.
Tinbergen (1960) explained the non-random acquisition of prey by insectivorous birds in pinewoods as a consequence of the formation of a "specific search image" for particular prey. By this he meant that birds might learn the key visual characteristics of a prey after several encounters with it and then begin to search exclusively for those cues. By concentrating on one prey they would tend to overlook other foods, especially when they were relatively rare. Royama (1970) pointed out that on the basis of his observations certain features of the birds behaviour were inconsistent with the search image hypothesis and that identical dietary patterns could be produced if the birds possessed particular foraging movements which would result in a concentration of their search efforts in particular locations (see Krebs, 1973 for discussion).
From these few examples, it should be clear that field descriptions of dietary patterns are most valuable as sources of hypotheses about the biological mechanisms that are involved in controlling prey acquisition. However additional observational and experimental studies must be the major sources of critical evidence to test the merit of particular explanations or interpretations of a pattern. To some it may seem a tedious process to eliminate or identify the biological mechanisms actually responsible for specific patterns of prey exploitation, but unless we understand the underlying mechanisms it will be 44
impossible to predict patterns in many instances or to understand their significance in others.
In order to test hypotheses about the factors that control the dietary patterns exhibited by trout and kokanee in
Marion Lake I will, over the course of the next few chapters, examine where trout and kokanee choose to forage, when they choose to forage, how they search for prey, how they attack prey and how experience in encountering various prey alters the predators foraging behaviour on subsequent occasions.
SUMMARY
1. Trout and kokanee exhibit species specific dietary patterns on both an annual and a seasonal basis, even though the predators were collected simultaneously from the same habitats and apparently had access to an identical set of food items (Fig. 2).
2. Patterns of prey exploitation that are specific to either trout or kokanee are frequently related to differences in morphology and especially to differences in the sizes of prey (Figs. 4 to 7).
3. Predator specific dietary patterns persist even with respect to prey types that have many features in common (e.g. the two species of amphipods, Table 4, Fig. 5; various species of molluscs, Fig. 6; the many species of chironomids). 45
4. Dietary differences between trout and kokanee are not simply related to differences in the relative sizes of the predators.
5. Trout and kokanee exhibit pronounced patterns of
"density independent" exploitation of prey from the total complex of prey that is apparently available in the natural environment
(Figs. 8 and 9).
6. Field descriptions of dietary patterns are most valuable as sources of hypotheses about the biological mechanisms that are involved in controlling prey acquisition.
7. Because each pattern of non-random, prey-acquisition may be favoured by a variety of biological mechanisms that may act alone or together, there is generally a need to systematically assess the identity and relative importance of the particular mechanisms that are responsible for promoting a given dietary pattern. CHAPTER 3
THE RELATIONSHIP BETWEEN SPATIAL SEGREGATION, TEMPORAL SEGREGATION, AND DIETARY PATTERNS of TROUT AND KOKANEE IN MARION LAKE
INTRODUCTION
Schoener (1974) has suggested that separation by habitat is the most frequent form of ecological segregation in terrestrial communities and he pointed out that relatively little data are available to reach firm conclusions about patterns of ecological segregation in aquatic communities.
Some authors (Larkin, 1956; Chapman, 1966) have stressed that freshwater fishes of the north-temperate zone exhibit relatively wide tolerance of habitat type and thus should display extensive overlap while others (Nilsson, 1960, 1967;
Keast, 1970; Moyle, 1973; Werner et al., 1977) have observed well developed spatial segregation along gradients of depth, vertical height in the water column, and vegetation structure.
Because many of the prey exploited by trout and kokanee exhibit close associations with specific habitats in Marion Lake (eg. water column, deep -water-sediments, shallow-water sediments, weed beds), habitat segregation by the predators is the first mechanism which may operate to produce species specific dietary patterns. Therefore the first hypothesis that I have attempted to test is that spatial segregation (between depths or sub-habitats) is 47 responsible for the species specific patterns of prey exploitatation exhibited by trout and kokanee.
Park (1941) first developed the idea that activity peaks occurring at different times of a 24 hour day can produce a type of symmetry in animal communitites, some species being nocturnal, some diurnal, and others crepuscular. Temporal patterns of activity are known to vary widely for both marine (Hobson, 1972) and fresh• water fish (Carlander & Cleary, 1949; Keast, 1970; Emery, 1973;
Engel & Magnuson, 1976). Aquatic invertebrates also exhibit con• siderable variability in diel activity patterns (Moon, 1940; Waters,
1962; Elliot, 1968) . Work with predatory vertebrates in terrestrial systems (Bider, 1962) indicates that they have activity cycles which coincide with those of their major prey.
A study by Baumann & Kitchell (1974) leaves no doubt that the timing of predator and invertebrate activity cycles can influence the patterns of prey acquisition by fish. They found that no Ephemeroptera (mayfly nymphs) were present in samples of bluegills
(Lepomis macrochirus) taken at 1600 hours but that the nymphs had become the most important food item in bluegills obtained at 0700 hours. This pattern corresponded to the observation that mayfly nymphs found in the lake were predominantly active at night. Because of the potential importance of activity cycles, the second hypothesis considered in this chapter is that differences in the temporal sequence of predator and prey activities produce differences in the food items found in trout, kokanee and the environment. METHODS
Patterns of Habitat Occupation
Depth Distribution
I recorded the distribution of fish in Marion Lake in 120 hours of diving during the months of May, June, July and August of 1971 and 1972. Salmonids in Marion Lake generally avoid an actively moving diver but ignore a stationary one, thus, most diurnal observations were carried out at specific stations (Fig. 11). I made observations throughout the day
(0500-2100 hours) and each station received equal effort during any one series of observations.
Each station was equipped with horizontal and vertical plastic, reference-markers graduated at 5 cm in• tervals. Horizontal markers enclosed a one square meter area and a four square meter area on the lake bottom. Vertical markers extended from diagonally opposed corners of this bottom grid to the surface. A diver positioned at the surface could estimate the size, species identity and vertical position of those fish passing between and over the various markers.
Stations included depths of 1, 2, 3, and 4 m of water and therefore encompassed 4, 8, 12 & 16 cubic meters of water.
The dimensions of the largest station (2 X 2 X 4 m) were small enough that under the most unfavorable conditions of low light and high turbidity, all fish passing over and between the reference markers could be counted and identified A contour map of Marion Lake indicating the locations of both trap and observation sites.
A, B, C and D represent the 1, 2, 3 and 4 meter observation stations respectively.
H and I represent surface observation grids.
N and S represent north and south trap-net locations respectively. Lake Outlet
vo 0» to species. This ensured that the visual sightings would
not be influenced by diurnal or seasonal changes in the
detectability of fish.
The observation procedure consisted of a diver
moving into position at the surface, above a station, then
waiting for . five minutes to compensate for any disturbance
of animals in the vicinity, and then recording a standard
set of observations for twenty minutes. I recorded observa•
tions by hand on a plexiglass slate in 1971 and used a four-
channel event recorder (Rustrak) modified for underwater
operation, for a continuous record of observations, in 1972.
I scored the vertical position of each fish sighted in 1971
to the nearest 5 cm interval, while in 1972 I designated
animals as surface (within 50 cm of the water surface),
bottom (within 50 cm of the bottom), or midwater.
Distribution With Area
The location of underwater stations made it possibl
to detect some changes in the depth-habitat distributions
of fish over the course of the summer. Two traps (fyke nets
with 6mm mesh and 17 m leads) were operated at intervals
through the period May,1974 - May,1975. One trap was located
in 1-2 m of water at the south end of the lake and the other
in 1-2 m of water at the north end of the lake (Fig 11).
, The traps were identical in every respect of construction
and operation. Thus, I accepted differences in the propor•
tions of animals caught at the two locations as indicative 51
of differences in spatial distribution.
In addition to the trapping and underwater observations,
I spent in excess of 100 hours in a boat equipped with lights, collecting fish from all areas of the lake at night. Although these observations are not quantitative, my general impression of the distribution of the predators at these times is in agreement with the distributions indicated by quantitative sampling techniques.
Patterns of Activity
Two conditions must be met before activity cycles will strongly influence differential prey exploitation by
trout and kokanee. Trout and kokanee must exhibit markedly different activity patterns (eg. nocturnal vs diurnal) and
the activity of some prey groups must coincide with the
activity of one species of predator more closely than with
the other. Because there was no information concerning the activity cycles of either fish or invertebrates in Marion
Lake, it was most efficient to test for differences in the activity patterns of the predators as a prerequisite to any examination of prey activity cycles.
I analyzed data from gill-net captures of fish
completed between 1963 and 1966. Monofilament gill-nets had been placed in 1-4 m of water near the eastern edge of
the lake to catch fish. The nets contained sections of three mesh sizes (2.5, 3.75 and 5.0 cm). The nets were examined every two hours for a twenty-four hour period so that changes 0 in "activity" could be detected. A twenty-four hour set was completed for each of February 1964, April 1966, May 1964,
August 1963 and November 1963.
Direct visual observations from fixed stations in the lake provided data to check that activity as measured by vulnerability to gill-nets is a reflection of foraging activity rather than of some other factor (eg. changes in ability to visually detect and avoid gill-nets under conditions of changing light) .
Prey
Preliminary examination of data from gill-net captures indicated a tendency for kokanee to be more active than trout during the late evening and night. This suggested that differences in activity cycles might well produce some of the differences in prey exploitation by fish if activity levels of some prey groups paralleled that of either trout or kokanee more closely. Chironomid pupae are an important item in the diets of trout and kokanee and they are obtained by the predators during times of adult emergence from the lake. The emergence of adults from pupae seemed to exhibit pronounced diel variations, thus, differences, in ex• ploitation of pupae by trout and kokanee (Table 2.) seemed a likely pattern to be produced by asynchronous activity cycles. To test this possibility, I took samples to document the temporal sequence of pupal emergence on selected dates during 1972. A bow-amounted net (opening 1 m X lm, mesh size
200ym) was pushed along just below the surface in front of a boat for 1 minute. Three replicate hauls were taken at each time. Samples were preserved in 70% ethanol and sorted at a later date.
RESULTS
Depth Distribution
I completed six sets of observations on the depth distributions (bottom, midwater, surface) of fish during
1971-72 (Table 7). Because temperature strongly influences habitat selection by the predators (Hyatt, Ms), I have de• signated observations as either early summer or late summer based upon the range of surface temperatures encountered.
The depth distributions of trout (Table 7a & b)
are significantly different between all sets of observations
(p<.001, df = 2, X for two independent samples, Siegel,
1956) while the depth distributions of kokanee are not signi•
ficantly different within either early or late summer observa•
tions, but are signifantly different between these periods
( \, , P < .001, df = 2). Due to the small numbers of kokanee
sighted during some sets of observations, I pooled the data
obtained under early summer conditions and those for late
summer conditions to test for differences in depth distri•
butions of trout compared with kokanee. Depth distributions TABLE 7. Depth distributions of trout and kokanee B = bottom, M = midwater, S = surface and N = the total number of sightings.
a. Early Summer
Date and Range Trout Kokanee of surface temperature ; B % M % S N % B % M % S N
May 26-July 6/71 73 23 4 306 9 24 67 303 10-17 °C
May 24-31/72 12 44 44 363 17 50 33 6 10-16 *C
June 8-28/72 43 35 22 113 13 17 70 23 2 12-17 °C
All dates pooled 41 34 25 782 9 24 67 332
b. Late Summer
July 29-Aug.l/71 89 10 1 582 74 25 1 276 23-27 °C
July 18-28/72 31 60 9 233 100 19-25 °C
Aug.3-11/72 62 28 10 1189 72 24 4 25 19-23 °C
All dates pooled 66 26 8 2004 76 23 1 316 of trout and kokanee differ significantly (X2, p <.001, df
=2) under both early and late summer conditions. In early summer kokanee occupy primarily surface habitats while trout occupy bottom ones. In late summer there are more trout than kokanee in surface habitats although qualitatively trout and kokanee exhibit similar depth distributions (Table 7b).
Distribution With Area
Proportions of trout and kokanee observed at under• water stations were not equal (Fig .12). Under early summer conditions in both 1971 and 1972 I observed the majority of trout at shallow (1-2 m) , inshore stations, while the greatest number of kokanee were always observed at the deep
(3-4m) stations farthest offshore. Thus, trout and kok.anee exhibit a remarkable degree of segregation. An increase in overlap of areas occupied by the two species under late summer conditions (Fig. 12c) is largely the consequence of a pronounced seasonal change in areas occupied by trout.
Under early summer conditions, fewer than 30% of all trout observed occurred at offshore stations but under late summer conditions 48% of all trout occurred there (compare fig.
12a with 12c).
Differences in the proportions of fish detected at various locations were not restricted only to stations
in different depths of water. The north and south trap-nets were located at similar depths (1.5m) and there were signi•
ficant differences in the proportions of predators captured 56
Figure 12
A comparison of the relative proportions of
trout and kokanee observed at onshore (stations
A and B) and offshore (stations C and D) locations
in Marion Lake. N = the total number of fish
observed during a given set of observations.
Numbers in brackets indicate the range of
lake surface temperatures attained during
each observation set. OBSERVATION STATION LOCATIONS AND THEIR ASSOCIATED WATER COLUMN DEPTHS (m)
> co o o > CO o o I i i i I I I I - . ro OJ - ••".M.». o CD CD O O H 33 Z —I O II CD 33 co OJ p c ro Ul co -5i o o
ro ro O' o
2
*_ o s? z ro o c ->i - 1 cr
CD CD CD rn -M" w ro oro
2 Z X £ »• 5 o CD £ o * i o m m m m
o o
Ul
CO co o o in these nets during a number of sampling intervals (Table
8a & b). In general kokanee were more abundant at the north
end of the lake. The single exception to this trend occurred
under late summer conditions when the south net captured
more kokanee than the north net. I attribute this to the
presence of a few hundred kokanee at this time, in a spring
less than 50 m away from the south net. Patterns for trout
are not as clear. On two occasions there were more trout
captured at the north net and on two others there were no
significant differences (Table 8b).
Diel Activity Patterns of Predators
Gill-net captures over 24 hours suggest that neither trout or kokanee are strictly nocturnal, diurnal or crepuscular
(Fig. 13). When captures are summed over all seasons, there is clearly a trend for kokanee to be most "active" at night and for trout to be most "active" in the day. Between season comparisons (Fig. 13a & b) suggest similar activity patterns for kokanee but a shift from morning to late afternoon in peak activity by trout.
It is necessary to examine two critical assumptions before attempting any interpretation of the significance of these results for patterns of prey acquisition. These are that vulnerability to capture during the daylight hours is similar to that under nocturnal conditions and that "activity" as measured by gill-net captures is a reflection of foraging activity rather than some other type of activity. 58
TABLE 8 North trap (Nth) versus South trap (Sth) Captures of trout and kokanee 1974-75
Interval June 14 July 17 Oct. 19 May 5 July 17 - July 30 -Nov..6 - May 26
Range of surface 10-17 19-23 6-11 5-12 temperatures C
No of trapping days 29 13 18 20 a. Kokanee Nth Sth Nth Sth Nth Sth Nth Sth
No. captured 69 29 6 41 83 34 25 6
% captured 70 30 13 87 71 29 81 19
Z (binomial 3.98 - 5.00 - 4.44 -3.21 test, Siegel, ** ** ** ** 1956)
b. Trout Nth Sth Nth Sth Nth Sth Nth Sth
No. captured 383 257 96 41 131 136 82 72
% captured 60 40 70 30 49 51 53 47
Z statistic - 4.96 4.58 -0.24 - 0.73 ** ** NS NS
** significant at the .01 level
NS not significant A comparison of the relative proportions of trout
and kokanee netted at two hour intervals, over
twenty-four hour periods during (a.) early summer
(b.) late summer and (c.) pooled over all dates.
A netting series was completed during each of Feb.
1964, April, 1966; May, 1964; Aug., 1963; and
Nov., 1963. N = the total number of trout or
kokanee captured during a particular netting
series. 59a
O KOKANEE N = I30 a. EARLY SUMMER (MAY-JUNE) © TROUT N = I36
Q LxJ 2- \- UhJ- z: O N=277 b. LATE SUMMER 26 - CO © N =58 (AUGUST) L±orJ 22- m 18- Z> z
10- A L h- O 6 - h- u_ 2 - o —1 1 1 1 1 T i 1 r O N = 6 11 22 - c. TOTAL OVER ALL SEASONS @ N = 284 18-
14-
10-
6 -
2 -
—i 1 1 n 1 1 1 n 1 r 1 r 4-6 8-10 12-2 4-6 8-10 12-2 -A. M- P.M. A. M. If differences in day and night vulnerability are related to some factor other than fish activity (eg. the ability to visually detect and avoid the nets), I expected that more individuals of both species would be captured at night than in the day. Since this is not the case, I suggest that captures do reflect diel changes in activity. I can not immediately confirm the second assumption and a study of fish by Darnell and Meierotto (1965) suggests that it may be incorrect. They found that feeding activity, as measured by the volume of food present in the gut, did not coincide with the periods of maximum "swimming" activity " as measured by the vulnerability of fish to capture in traps.
The data collected by direct observation of trout and kokanee activity are limited to only a portion of the diel cycle, but they are less subject to the assumptions that limit the usefullness of gill-net, capture data. Because
I wished to test the hypothesis that differences in the temporal sequence of foraging activity alone could affect prey exploitation, the results presented here concern only trout and kokanee that were observed in the same sub-habitats.
Therefore comparisons are limited to trout and kokanee foraging in offshore-surface, habitats during early summer (Fig. 14 a)i and in offshore-bottom, habitats during late summer (Fig.
14b) .
Direct observations indicate that in early summer both trout and kokanee exhibit maximum activity levels in .61
Figure 14.
A comparison of the relative numbers of trout
and kokanee observed at two hour intervals over
sixteen hour periods. (a.) trout and kokanee
observed in offshore-surface habitats during early
summer (b.) trout and kokanee observed in offshore-
bottom habitats during late summer. Vertical bars
indicate + one standard error of the means. 61a
5^7 7-9 9-11 11-1 1-3 3-5 5-7 7-9 A M — —- P M 62
early morning followed by lower levels for the remainder of the day. In late summer there are short intervals during the day when kokanee are more active than trout but, with the exception of the early evening peak in activity by kokanee, the activity patterns of the predators are similar.
The Relation Between Diurnal Activity and Food Search
There is often some uncertainty in the assessment of whether a predator is actively engaged in searching for prey (Beukema, 1968; Murdoch et al. 1975). This is because some of the motor patterns exhibited by actively searching animals are also incorporated into non-search activities
(Curio, 1976) and because predators engaged in non-search activites are often instantaneously receptive to opportunities for capture of prey (eg. Schaller's observations of lions,
1972) .
Although it was impossible in the present study to always distinquish clearly between search and non-search behaviours, I contend that much of the diurnal activity of trout and kokanee in Marion Lake was directed towards prey search. This contention is based upon various types of evidence.
Laboratory work by Beukema (1968) on sticklebacks and my own laboratory observations indicate that fish exhibit a readiness to search for and attack prey items as long as their stomachs are not filled to capacity. Trout and kokanee in Marion Lake seldom obtain as much as 50% of the daily ration they are capable of consuming (Sandercock, 1969; Hyatt, unpublished data). Thus, hunger (operationally equals full• ness of the gut) should serve as a strong motivation for the predators to search continuously for prey. Certainly trout and kokanee in the field appeared to be receptive throughout the daylight period to opportunities to attack food items.
Selective responsiveness to stimuli is often the most important feature by which different types of "goal oriented" behaviours such as food search can be categorized
(Hinde, 1966) . On this basis too, daylight activities of trout and kokanee in Marion Lake seemed to be related pri• marily to food search since overt responses by fish in the field were generally directed towards stimuli presented by potential food items. During daylight hours, direct obser• vations at underwater stations failed to reveal more than a negligible investment of time in activites that were not related to food search (eg. resting, territorial defense, agonistic interactions, predator avoidance). This was not due to an inability to recognize such behaviours since non- search activities were observed to involve large investments of time by trout and kokanee during other portions of the diel cycle, at other locations in the lake, or at other times of year.
Activity Patterns of Emerging Chironomids
Results of surface-net hauls reveal that chironomid pupae display distinct intervals for maximum emergence on any given date, but considerable variability in times of maximum emergence on different dates (Fig. 15 a, b, c).
In the May, 18 and June, 1 samples, the peaks of emergence
activity occurred from late evening to night. The peak of
activity for the much smaller June, 9 emergence occurred
in late afternoon.
DISCUSSION
I have previously established that trout and kokanee
exhibit only a modest degree of dietary overlap (Chapter
2) and that major differences exist between the apparent
availability of prey in the lake and their utilization by
predators. Given the patterns of habitat occupation and
activity of trout, kokanee and some of their major prey, it
is apparent that spatial segregation and to a lesser extent
temporal segregation may play a role in shaping the observed
patterns of prey exploitation.
The Role of Spatial and Temporal Segregation in Producing Dietary Differences Between Trout and Kokanee
Larval odonates, ephemeropterans and snails con•
stitute major foods of trout in early summer (37% by wt.
in April and 12% by wt. in June/66), but are barely repre•
sented in the diet of kokanee (absent in April and only 2%
by wt. in June/66) at this time (Efford & Tsumura, 1973).
Because the majority of these prey are found at depths of
less than 2 m in Marion Lake (Table 9), I suggested that
differential exploitation by trout and kokanee might be based 65
FIGURE 15.
The mean number of chironomid pupae obtained in surface net hauls taken between early afternoon and late evening on three separate dates. Numbers in brackets indicate the range of three replicate samples. AVERAGE NUMBER OF CHIRONOMID PUPAE OBTAINED PER NET HAUL 66
TABLE 9 A comparison of the relative abundance in early summer (April-June) of prey at inshore (depths <2 m) and offshore (depths >3 m) locations in Marion Lake
Abundance expressed as % of total numbers on a m basis
Prey Group Inshore Offshore Data Source
Chironomid pupae 70 0 303 1* Hamilton, 1965
Chironomid larvae 50-60 40-50 Hamilton, 1965 McCauley, pers. comm. Amphipods 82-90 10-18 Mathias, 1971 Efford, unpubl. Trichopteran larvae 50 50 Winterbourn, 1971
Planorbid snails 80 20 Delury, 1971. 2 Odonate larvae 87 13 * Inferred from the distribution Ephemeropteran larvae 87 13 of suitable cover
I have considered only the more abundant species of chironomids which have completed 50% of their emergence by the end of May and/or all emergence by the end of June. Hamilton's data for 0 - 1.9 m and 4-6 m were used to represent inshore and offshore areas respectively.
^* There are no good quantitative data concerning the distribution of immature odonates or ephemeropterans. However, both of these groups are most abundant in close association with the cover offered by weed-beds (Pearlstone, 1971 and personal observations). Therefore, I have used the patterns of weed-bed, depth-distribution (Davies, 1970; Neish, 1971) to infer the abundance of these two groups. in part upon some form of habitat segregation between the predators. Results from this study lend strong support to this hypothesis. Undoubtedly the occupation of offshore areas by the majority of kokanee and of inshore areas by trout creates different opportunities for exploitation of these prey. Even for those few kokanee that do forage in inshore areas, the occupation of primarily midwater and surface habitats (Table 7) will reduce the probability of encountering bottom prey such as odonates and snails. By contrast, the concentration of trout in positions close to the bottom will favour detection and exploitation of these prey types in early summer.
The occupation of offshore areas by kokanee and of inshore areas by trout provides a resonable explanation for significant differences in exploitation of other prey types as well. Over the course of the year trout exploit more terrestrial insects than kokanee (Fig. 2, Tables 3 and
5) and trout alone exploit notonectids (backswimmers) and corixids (water boatmen). Notonectids and corixids are known to be restricted to inshore habitats in the lake (Lovely,
1972) and it is likely that terrestrial insects will be most abundant there. Diets of the smallest trout and kokanee examined in this study contained large numbers of zooplankton
(Table 5) but trout exploited the cladoceran Sida crystallina almost exclusively. Kokanee took relatively modest numbers of Sida sp. along with many other species of zooplankton such as Leptodora sp. This difference may be traced to the close association of Sida sp. with littoral zone beds of lilypads while species such as Leptodora sp. are found only in the water column of offshore areas (Hyatt/ unpublished data).
Some differences in the size-frequency distributions of prey used by trout and kokanee most likely have their source in habitat segregation. For example, kokanee likely exploit the smaller species of molluscs (Pisidium spp.) rather than larger planorbid snails because the latter are not found
in appreciable numbers in the offshore locations occupied by kokanee (Delury, 1971) .
Since the majority of trout and kokanee that I observed during the day were continuously engaged in searching
for prey (see descriptions in chapter 4), it is unlikely
that differences in the presence or absence of particular
prey species in fish diets are due to differences in diurnal
activity levels of the predators or their prey. However,
asynchronous activites may combine with patterns of habitat
segregation by the predators to produce some dietary diff•
erences. For example the greater exploitation of chironomid
pupae by kokanee as compared to trout (Fig. 3) is consistent
with the former predators greater occupation of midwater
and surface habitats where pupae are most vulnerable to
detection during emergence. In addition the tendency for kokanee to exhibit higher activity levels than trout in the late evening and at night combined with emergence peaks by chironomid pupae at these times (Fig. 15) could certainly contribute to the greater exploitation of pupae by kokanee during some months of the year. However, in general the evidence supporting the idea that asynchronous foraging activites by trout, kokanee and their prey play a major role in controlling dietary differences exhibited by the predators is much less convincing than the evidence suggesting habitat segregation as a major mechanism favouring food resource partitioning.
The Role of Spatial Segregation in Producing Differences Between the Proportions of Prey Types Observed in the Natural Environment and in the Diets of Trout and Kokanee
Comparisons of the proportions of prey in the diets of trout and kokanee with the relative abundance of potential prey in the lake (Chapter 2, Figs. 8 & 9) revealed major diff• erences between the apparent availability of prey in the lake and their utilization by the predators. Results obtained in this chapter provide evidence that a likely reason these differences occur is that trout, kokanee and scientists each implement sampling schemes which exhibit differences in spatial coverage.
In order to characterize the species composition of the invertebrates that occupy an average square meter of lake 70
bottom, scientists (Hamilton, 1965; Efford and Tsumura, 1968-69, unpublished data; Bryan, 1971) employed stratified random sampling schemes in which the number of benthic stations within each depth zone was approximately proportional to the total lake area covered by that zone. Thus, of the 9 stations .sampled and averaged on a twice monthly basis by Hamilton (1965), 5 were located at depths of less than 2 m while the remaining 4 were located at depths between 2 m and 6m. Similarly, of the 25 benthic grabs taken on a monthly basis over a two year interval by Efford and Tsumura,
17 on average originated from depths of 2 m or less while the remaining 8 originated from depths between 2 m and 6 m. Although when averaged these data are likely to indicate the relative densities of each type of benthic invertebrate present in the lake as a whole, they are unlikely to indicate the relative densities of benthic invertebrates encountered by trout or kokanee while foraging. For example, over the course of a year scientists applied between 32 and 44% of their sampling effort to obtain prey from depth zones greater than 2m. By contrast, kokanee searching for benthic invertebrates spent between 65 and 88% of their time foraging in this zone. Thus, the set of benthic invertebrates acquired by scientists is biased towards those species that are most abundant in shallow (< 2 m) water habitats (eg. amphipods, snails, odonates) while the set of invertebrate prey acquired by kokanee will be biased towards those species that are most abundant in relatively deep (> 2 m) benthic habitats (eg. chironomid larvae). 71
The spatial pattern established by scientists for
sampling benthic invertebrates coincides more closely with
that used by foraging rainbow trout than by kokanee, however differences in where "samples" of invertebrates were taken within a given depth zone probably bias the sets of invertebrates obtained by scientists and trout in different ways. For example,
Hamilton as well as Efford and Tsumura obtained all grab samples within a give depth zone from open mud locations. They avoided obtaining samples from weed-beds that occur along the shoreline
because the plants interfered with the operation of the sampling gear. By contrast , rainbow trout observed in this study often
searched in and around submerged weed-beds located along the
lakeshore. This difference may be important given Winterbourn's
(1971) observation that many species of caddis larvae are particularly abundant in weed-beds. Thus, the apparent over-
representation of caddis larvae in benthic grab samples may also be partially based upon differences in areas sampled by
trout and scientists.
Unexplained Dietary Patterns
Although availability, in the sense of spatial proximity, plays a major role in the differential acquisition of prey, there are many trends which are not accounted for by spatial segregation.
Under late summer conditions, there is a decline in diet overlap between trout and kokanee (Chapter 2, Table 1.) despite a considerable increase in spatial overlap. For fish greater than 10 cm
in size, the exclusive use of trichopteran larvae by trout and of 72
cladocerans by kokanee contributes to the decrease in diet overlap and is not a logical outcome of the observed patterns of habitat segregation.
Despite the greater proportion of time spent foraging in bottom habitats, trout exploit substantially fewer chironomid larvae than kokanee. These largely benthic prey do not appear to be present at higher densities in inshore than in offshore hab• itats (Table 9), thus, some other mechanism must operate to produce the difference.
Spatial segregation offered an explanation for the observation that kokanee exploit smaller molluscs than trout do, but it is not an adequate mechanism to produce the general trend for exploitation of larger prey by trout. This is especially clear given that the trend applies to both a broad range of aquatic invertebrates (Chapter 2, Fig. 2) and to more limited groups such as zooplankton (Chapter 2, Fig. 5).
Habitat segregation and timing of activities are only a limited success in explaining the non-random exploitation of prey from the lake environment. Many of the observed differences still have no explanation. In the next chapter, I have combined observations of foraging behaviour in the field with selected laboratory experiments to test the general hypothesis that differences in how trout and kokanee search for prey will account for some of the as yet unexplained patterns of non- random, prey-exploitation. 73
SUMMARY
1. Trout and kokanee exhibit well defined patterns of spatial segregation (Tables 7 & 8, Fig. 12).
2. In early summer kokanee occupy primarily surface habitats while trout occupy mainly bottom ones (Table 7).
3. In late summer there are more trout than kokanee in surface habitats although the majority of individuals of both species are associated with midwater and benthic habitats (Table 7).
4. Kokanee exhibit a consistent trend to occupy offshore
( > 2 m) habitats (Fig. 12).
5. Trout exhibit a consistent trend to occupy inshore
( < 2 m) habitats (Fig. 12).
6. Activity patterns of trout and kokanee indicate relatively little temporal segregation. Neither species can be classed as strictly nocturnal, diurnal or crepuscular (Fig 13 & 14).
7. Spatial segregation between trout and kokanee in
Marion Lake plays a major role in producing predator-specific dietary patterns.
8. A number of differences between the apparent availablity of invertebrate prey in the lake environment and their utilization by trout and kokanee may be attributed to the fact that the relative proportions of prey obtained by scientists sampling all areas of the lake are not the proportions that trout and kokanee encounter when foraging in more restricted areas (eg. weed-beds, offshore benthic habitats) of the lake.
9. Many of the dietary differences described earlier
(Chapter 2) are not accounted for by either spatial or temporal
segregation between trout and kokanee. 75
CHAPTER 4
THE RELATIONSHIP BETWEEN FOOD-SEARCH BEHAVIOUR AND DIETARY PATTERNS OF TROUT AND KOKANEE IN MARION LAKE
4-A. FIELD DESCRIPTIONS
INTRODUCTION
I have previously established (Chapter 2) that trout and kokanee in Marion Lake display species specific diets and that spatial segregation (on a scale of meters) plays an important role in shaping the patterns of prey exploitation observed (Chapter 3). However consideration of only spatial and temporal segregation by fish in Marion Lake left many dietary patterns unexplained. This implies that differences in the foraging behaviour of the predators must play a major role in shaping their diets.
De Ruiter (1967) has divided the foraging behaviour of animals into four phases: search, approach, capture, and ingestion.
Events that take place during any one of these phases may have a profound influence on the diet of a predator. In this chapter,
I have set out to test the general hypothesis that differences in search behaviour will account for differences in the types of prey acquired by trout and kokanee. To demonstrate this requires an assessment of whether there is a "match" between the- predator1s search behaviours and specific characteristics (locations, sizes, behaviours) of their prey.
Food search by predators may be considered from many different aspects. A variety of studies indicate that microhabitat 76
specific search, the use of specialised search techniques, and
interactions between sensory perception and prey detection are particularly important in determining dietary patterns of free
living predators (MacArthur, 1958; Root, 1967; Baker, 1972; Ware,
1973). I have divided this chapter into two sections. The first deals with the food-search behaviour of trout and kokanee under natural conditions. The second deals with the relative abilities of trout and kokanee to detect various natural prey in the
laboratory. The implications of results on search behaviour and prey detection, for dietary patterns are discussed.
Microhabitat Specific Search and Specialized Search Techniques
There is no standard definition for what constitutes a habitat, a sub-habitat or a microhabitat and from a variety of studies it is clear that they are not absolute but rather relative units most commonly distinguished by differences of biophysical scale. In the majority of studies, dealing with the foraging behaviour of free-ranging vertebrates, habitats and sub-habitats are biophysical units which cover many square meters of space
(eg. forest floor, forest canopy, littoral zone, benthic sediments).
Microhabitats by contrast are biophysical units in which at least some dimensions are measured on a scale of cm or mm (eg. cracks
in tree bark, the undersides of leaves, the exposed layer of sediment as compared to the sub-surface sediments on a lake bottom). Within this context each sub-habitat generally consists of an aggregate of microhabitats, which may contain different assortments of food. Specialised search techniques which result in micro-
habitat specific search by vertebrate predators have been
identified as the basis for the occurrence of differences
between the diets of similar predators searching for food in
the same habitats (MacArthur, 1958; Root, 1967; Baker, 1972),
as well as the reason for why a particular predator fails to
take potential prey in proportion to their relative abundance
in the environment (Royama, 1970; Ware, 1973; Moore and Moore,
1976).
Root (1967) and Baker (1972) in particular emphasized
that differences in microhabitats searched by sympatric species
of birds served as the basis for their differential exploitation
of invertebrates in forest and mud-flat habitats respectively.
For example, Root found that Western flycatchers (Empidonax
difficilis) search a large area for prey from a "sentinel"
position on an exposed perch. He suggested that this search
technique biased flycatchers to exploit large, active insects
either in the air or from the surface of foliage. A high
proportion of large Hymenoptera and Diptera in the diet of
flycatchers supported his prediction. In contrast to flycatchers plain titmice (.Parus inornatus) often searched for prey
by pulling apart flowers and foliage as well as by probing
beneath foliage. Consequently, their diets contained a high proportion of small insects which were concealed in these microhabitats. These insects did not appear commonly in the diet of flycatchers. Similarly, Baker (1972) noted that some
species of shorebirds (eg. short billed dowagers) searched 78
for prey by probing deeply into the substrate with their bills, while others (eg. lesser yellowlegs), searched exclusively
for objects exposed on the mud surface. He presented evidence
that this difference in search procedure served as the basis
for differential detection and acquisition of prey by the predators.
Since many of the species of prey exploited by trout and kokanee exhibit microhabitat differences (eg. epibenthic or sub-benthic), I hypothesized that specialised search techniques
in concert with microhabitat specific search might form the basis for some differences in the dietary patterns of trout and kokanee. To provide data to test this hypothesis, I con• ducted observations of trout and kokanee foraging under natural conditions.
METHODS
Locations, times and general techniques of obtaining observations have been described elsewhere (Chapter 3). Locations at which observations were conducted differed both with respect to depth and distance from shore. Although I did not obtain observations of foraging behaviours of trout and kokanee associated with the entire range of microhabitats present in Marion Lake, locations at which observations were conducted contained a variety of microhabitat features (eg. open sediment, brush deposits, accumulations of litter, clumps of water lilies).
I recorded the search techniques and positions of actively foraging predators in great detail because I wished to detect any consistent differences between trout and kokanee 79 which would promote access to different portions of the food supply present in different microhabitats. When fish swam into view standard observations recorded were; the species identity, the number of individuals present, the specific substrate that individuals were oriented to, the water column position of each animal (expressed in cm from the nearest substrate), the cruising velocity of randomly selected animals, the "search techniques" employed by individual fish, the relative sizes and identities of items that fish attacked and the sequence of events surrounding an attack. To record those events requiring an estimate of time, I used either a four channel event recorder or a stopwatch.
Because individual fish at underwater stations remained within view for only 15 seconds to three minutes, it was impossible to determine exactly how many different individuals my observa• tions involve. However, I could often recognize individual trout due to differences in size or markings (scars, colour patterns, 200 to 300 trout carried colour coded tags) and kokanee frequently appeared in groups containing up to a few hundred individuals, thus it is likely that the data collected involve several hundred individuals of each species and that the behaviours observed are representative of those generally employed by trout and kokanee in Marion Lake.
RESULTS
Search Techniques
When particular behaviours are associated with specific environmental conditions and are repeatedly followed by attempts at prey capture, it is likely that such behaviours are part of the process of prey search. In the present study, prey detection and attack by fish commonly occurred within a series of recognizably different behavioural and environmental contexts.
For convenience, I have arbitrarily designated each of these behavioural-environmental associations as separate types of search.
1. Cruise and Search
Trout use this technique to locate prey in the water column, at the sediment surface and at the lake surface. Kokanee exhibit this form of prey search only when they are foraging in the water, column. Cruise and search is the most ambiguous of the behaviours classified as search and to the untrained eye there is little to differentiate the technique from general swimming activity. The key combination of characteristics that identify the technique is that the predators are mobile and their responses are restricted to recognizable prey items.
However, in addition to the initiation of attacks directed towards prey, there are other clues which suggest that the predators are actively searching for prey.
The first clue is that the predators maintain a fixed orientation to certain "substrates" where prey are likely to be found. When trout employ this technique to search for benthic prey, they assume positions that vary from 0 - 50 cm above the substrate, but orient downwards to face it. Ware 81
(1971) suggested that this characteristic incline (about 10 to 20°) serves to direct the predator's visual a.xis onto the sediment. In support of this, when trout were very close to an observer in the field it was possible to see that the fish effect continuous eye movements as if "scanning" the sediment surface. When using cruise and search at the lake surface, trout maintain a horizontal posture and make frequent attack's on prey from 45 to 100 cm below the air-water interface.
The second clue that cruise and search is related to the process of prey detection is that predator swimming velocities vary in a way that suggests they are visually scanning their immediate surroundings for food. Swimming speeds are similar for fish foraging at the lake surface or in the water column, but movement is substantially slower for fish oriented to benthic substrates (Table 10).
Trout and kokanee both rely on vision during food search (Ware, 1971; Ali, 1959), thus one obvious reason for this reduction in velocity is the relative level of substrate heterogeneity that water column and bottom sediments offer a predator using vision to locate prey. The more complex background of benthic substrates will require a longer interval of perceptual attention per unit of space scanned in order to detect prey
(eg. see Boynton and Busch, 1956), consequently search velocities must be lower here. 82
TABLE 10. A comparison of the swimming velocities of trout and kokanee actively searching for prey in a variety of sub-habitats.
a. Trout Mean (cm/sec) Range S.D. N
Water column & lake surface 27.7 11.1- 50.0 + 1.4 165
Sediment surface 8.6 4.2- 16.7 + 1.0 35 b. Kokanee
Water column & lake surface 18.2 10.0- 50.0 + 2.1 45
Sediment surface 6.6 5.0- 10.0 + 0.5 22
TABLE 11. Residence time and the total number of attacks initiated by five trout using the hover and search technique.
Time spent in a single Total number of location (minutes) attacks initiated
4 6 2 3 6 4 4 1 5 2 83
2. Hover and Search
Trout use this technique to locate prey on the sediment surface and at the lake surface. The key combination of characteristics that identify the technique is that the predator maintains a stationary position (10 to 20 cm above the bottom or 50 to 60 cm below the lake surface) and attacks only recognizable prey items. The long axis of the body may be horizontal or slightly tilted (10 to 20°) towards the substrate. The constant performance of slight reorientation movements to the substrate, scanning movements of the eyes and the initiation of a number of attacks on prey items that move, distinguish this search technique from rest postures. Prey may be attacked within an arc centered between the predator's eyes and subtending 310 to
320°.
Trout rarely use this tactic for searching at the lake surface. Sixty of the seventy trout I have observed using this tactic were searching for benthic prey. Trout spend no more than a few minutes in a single location and there is considerable variability in their success at locating prey (Table 11). On a number of occasions, I have followed the activities of individual fish from an above surface location and have found that they will use the technique consecutively, in several locations, within a 25 to 50 square meter area, over 20 to 30 minutes intervals.
No kokanee used this technique during any of the field observations. Kokanee characteristically use only search techniques which involve constant swimming activity. 3. Test and Search
There is little doubt that both trout and kokanee use this technique as a means to locate food items. The key combination of characteristics that identify the technique is that the predators are mobile and they initiate many attacks on items that are not prey organisms. For example an individual trout will orient to, rapidly approach, grasp and then reject a small wood chip lying on the sediment surface. Attacks on this item may be repeated several times and each time the object is mouthed and then rejected. Finally the predator will abandon the item, however it may move only a short distance before making an attack on another. The specific items attacked are usually within the size range of prey items that will normally be consumed by fish in the lake. Trout use this technique occasionally at the lake surface but more frequently when searching for prey on the lake bottom. Search positions and swimming velocities are indistinguishable from those described above for trout employing cruise and search.
Kokanee use test and search exclusively when they forage at the lake surface. In contrast to the cruise and search technique that trout use most often at the surface, the test and search technique of kokanee is performed from a shorter distance below the lake surface (usually 5 to 30 cm) and at significantly lower velocities (mean 18.2 cm per second,
Table 11). The lower velocities are probably a consequence of the tendency for kokanee to momentarily grasp every prey-size object (range 1 mm to 15 mm) floating on the surface. A subtle 85
difference in this technique, as practised by trout and kokanee,
is that kokanee foraging at the surface usually test an item
only once before moving on. This may be a consequence of their
foraging in close association with other kokanee, while trout
are often solitary (see discussion in Chapter 7).
~ 4. Grab and Search
This technique was used only by kokanee searching for
prey at the sediment surface. The predator moves along very
slowly (6.6 cm per second - Table 10) right at the sediment
surface. The fish takes a mouthfull of sediment and leaf
litter, vigorously mouths it, and forcefully ejects the material.
The forward motion of the predator quickly carries it through
the small cloud of suspended material and at this point the
predator may take another mouthfull of sediment or turn through o
180 to reexamine the settling debris. By using this technique
kokanee detect prey that are exposed on the sediment surface
and prey which become exposed as a consequence of the substrate
disturbance. When I have observed this technique used under
laboratory conditions, prey often escape because the predator
fails to discriminate successfully between prey and falling
debris.
I have never observed rainbow trout employ this
technique to search for prey, although, on very rare occasions,
and only in the laboratory, I have observed them disturb
sediments by body movements reminiscent of redd digging. To briefly summarize the differences in search techniques between the two species, trout alone use hover and search while grab and search is a technique used exclusively by kokanee. Although two of the techniques (cruise & search, test & search) are shared by trout and kokanee, they are not practised with equal frequency and the same techniques are not always employed to locate prey in the same sub-habitats (Table
12). Search techniques employed by kokanee are more sub- habitat specific than those used by trout.
An Examination of the Distribution of Search Positions of Trout and Kokanee in Relation to Lake Surface and Bottom Sub-habitats
Direct observations suggested that the majority of prey discovered by trout and kokanee occurred either at the
lake surface or lake bottom. Several of the search techniques
used by the predators involved a different range of search positions with respect to the surface being scanned for prey.
Thus, I expected that the use of different search techniques
as well as differences in the frequency of use of the same
techniques might result in different distributions of search
positions of trout and kokanee when they searched for prey
located at the lake surface or bottom.
. In the field, trout and kokanee occupied a continuous
range of search positions extending from the lake surface,
through the water column to the sediment surface at the lake
bottom. In order to detect differences in the distributions
of search positions assumed by the predators, I first had to 87
TABLE 12. A summary of the differences in search techniques employed by trout and kokanee foraging in the field.
Level of Occurrence Sub-habitats Searched
Technique Trout Kokanee Trout Kokanee cruise & search +++ + S,W,B W hover & search ++ N S,B - test & search + +++ S,W,B s,w grab & search N +++ - B
+++ very common S - lake surface ++ common w - water column + occasional B - lake bottom N never observed 88
define which portions of the entire range of search positions were related to search for prey located in association with benthic substrates and lake surface respectively. To do this
I relied on observations of the maximum reactive distance
(Ware, 1971) of predators to benthic and surface prey in the field.
Reactive Distance to Potential Prey and the Spatial Limits on Benthic and Surface Search
In the field, a sudden change in the direction, velocity or form of swimming behaviour of a searching predator was usually followed by an attack on a prey organism. Because the coincidence of an attack occurring in the immediate vicinity of the bottom or water-column reference markers was relatively rare, and because predators always approached prey at an oblique angle to the substrate, I did not obtain many precise estimates of reactive distances to prey. However I did observe that fish maintaining positions further than 50 cm from the sediment surface (measured as the perpendicular distance between the sediment surface and the head of the predator) never attacked benthic prey, but predators closer than this frequently made attacks.
Laboratory studies have revealed many of the variables that influence the distance at which fish, as visual predators, react to prey. Size, contrast and movement of prey (Protasov,
1968; Ware, 1971); experience and size of the predator (Beukema,
1968; Ware, 1971); and complexity of the background environment 89
(Ware, 1971) , all have a substantial influence on reactive distance. These variables appear to interact in the field in a way that limits the search for benthic prey to predators that maintain positions of less than 50 cm from the sediment surface. The maximum reactive distance to benthic prey was greater than 50 cm on some occasions, since trout and kokanee always approached prey at an oblique angle to the substrate.
The maximum reactive distance of trout and kokanee to prey located at the lake surface was much greater than to prey on benthic substrates. Fish maintaining positions as much as 85 cm below the surface initiated attacks on prey.
On two occasions I obtained samples for size measurements of the targets trout were attacking (Table 13); thus I am certain that they are capable of responding from positions that are 80-85 cm below the surface to targets no larger than
6-10 square millimetres. The maximum reactive distance to prey of this size was modestly greater because of the slightly oblique angle at which attacks on surface prey occurred.
TABLE 13. Reactive distance of trout to targets of known size at the lake surface on two occasions
Reactive Distance Target Size (cm)
Mean Range No. of Maximum surface No. Target attacks area (mm2 ) measured identity
70 65-85 5 10 20 Nuphar seeds 50 30-80 10 64 40 adult Diptera 90
Under natural conditions, trout and kokanee never
initiated attacks on lake surface or benthic prey from distances greater than 100 cm below the lake surface or 50 cm above the lake bottom. Therefore, by definition, only predators within these distances were considered as actively searching lake surface and benthic substrates respectively. Given these restrictions, it is now possible to compare the distributions of trout and kokanee search positions with respect to lake surface and benthic sub-habitats.
The Distribution of Predator Search Positions
While foraging for prey at the lake surface or bottom, trout and kokanee exhibit different distributions of search positions. The results presented here are pooled from all observations carried out in both early and late summer intervals
(see Chapter 3).
The majority of kokanee search for benthic prey from positions that are within 5 cm of the sediment surface while trout are most often observed searching from positions some
15 to 30 cm off of the bottom (Fig. 16). This species-specific pattern is maintained when trout and kokanee search for lake surface prey as well. Here kokanee are most frequently observed searching for surface prey from positions that are 5 to 30 cm below the lake surface. By contrast, the majority of trout search for these prey from positions that are 45 to 100 cm below the lake surface (Fig. 17). 91
FIGURE 16. The relative proportions of trout and kokanee that
maintain specific search positions while visually
scanning the bottom sediments for prey. N = the
total number of trout or kokanee observed.
The sequence of solid spheres indicates the size
of the smallest prey that trout or kokanee can
detect from a given position. Sizes were estimated
on the basis of data presented in Fig. .18 (see
discussion for explanation). MINIMUM DETECTABLE PARTICLE SIZE (mm2)
vo I—1 92
FIGURE 17. The relative proportions of trout and kokanee that
maintain specific search positions while visually
scanning the lake surface for prey. N = the total
number of trout or kokanee observed.
..The sequence of solid spheres indicates the relative
size of the smallest prey that trout or kokanee may
detect from a given position. Sizes were estimated
on the basis of data presented in Fig. .18 (see
discussion for explanation).
93
DISCUSSION
The Potential Effects of Search Techniques and Microhabitat Specific Search on Dietary Paterns
Trout and kokanee share some techniques of search but others are used by only one of the predators. The question of whether a particular search technique biases a predator to locate some food items but not others can only be answered if search techniques are considered in relation to the prey contents of the predator's diets and known characteristics of the prey.
Differences in the search techniques of trout and kokanee result in some degree of microhabitat specific search but are not easily related to any qualitative differences in the composition of the predator's diets. For example, grab and search as practised by kokanee, opens up possibilities for prey location in microhabitats that are not open to trout ie. prey may be located by "flushing" them from concealed positions, beneath benthic sediments. By contrast the search techniques used by trout (Table 12) restrict them to the detection of prey in exposed positions. In spite of this difference, the two major classes of prey known to spend most of their time concealed beneath the sediment surface (amphipods and chironomids) are well represented in the diets of both trout and kokanee
(Chapter 2). This simply emphasizes that although differences in foraging behaviour will frequently result in differences in the kinds of foods consumed by predators, they may also result 94
in the acquisition of the same foods from slightly different microhabitats.
Kokanee acquire prey from both concealed and exposed positions while trout obtain them from only exposed positions.
This apparently does not result in any qualitative differences in the diets of the predators but may serve as the basis for certain quantitiative differences. For example, chironomid larvae are an. important component of the diets of both trout and kokanee, but kokanee exploit significantly more larvae than trout in four out of five months of the year (Table 14),
including the month of August when both predators are normally closely associated with benthic sub-habitats (Chapter 3).
Coarse-scale habitat segregation failed to explain this difference since chironomid larvae are no more abundant in offshore than in onshore locations in Marion Lake (Chapter 3).
TABLE1 14. The seasonal exploitation of chironomid larvae by trout and kokanee
Probability that Trout Kokanee trout exploit Sample Larvae Larvae Larvae Larvae more larvae than Date exploited expected exploited expected kokanee do
Nov. 10 131 252 131 p < .00003 Feb. 11 30 64 45 p <,. 00003 April 14 7 5 12 N.S. June 233 406 382 209 p < .00003 Aug. 131 246 247 132 p < .00003
Normal approximation to the binomial distribution, one tailed test, Siegel, 1956. The expected frequencies are derived from the number of trout and kokanee present in each months sample and assuming that each predator should consume an equal number of larvae. Data from Efford & Tsumura (1973). 95
On the lake bottom, chironomid larvae are the most abundant prey type to regularly reach sizes greater than 2 mm.
Because the majority of larvae are sub-benthic, tube-dwellers, trout, using hover and search or cruise and search techniques, will frequently fail to detect them. However given the great 2 abundance of larvae (5 to 10 per cm in late summer, McCauley, unpublished data), I suggest that a kokanee (12 cm in length) with a 6-8 mm mouth gape (see Chapter 5) and engaged in repeatedly grabbing mouthfulls of sediment, will experience a high probability of disturbing larvae. These may be then be detected visually or perhaps with the aid of chemosensory detectors in the mouth.
It is clear from the work of Ivlev (1961) that the concealment of chironomid larvae under silt has different consequences for different species of predators. His experiments indicated that the presence of silt on the bottom of an aquarium did not substantially alter the availability of chironomid larvae to carp (Cyprinus carpio), but drastically reduced the consumption of larvae by roach (Rutilus rutilus), when compared with the no-silt controls.
The observations of Schutz and Northcote (1972) are especially relevant to my suggestion that different search techniques result in differential exploitation of chironomid larvae by trout and kokanee. Their descriptions leave no doubt that other pairs of salmonids, existing in sympatry, use the techniques of grab and search, hover and search or cruise and search as species-specific adaptations for locating benthic 96 prey. Furthermore, in two sets of laboratory experiments, they demonstrated that grab and search (as practised by Salvelinus malma) was greatly superior to hover and search (as practised by Salmo clarki) as a technique for locating either chironomid larvae under a sand and leaf litter substrate, or, Tubifex worms under a sand substrate. This evidence offers strong support for my contention that the different search techniques used by trout and kokanee constitute a likely reason for the greater exploitation of chironomid larvae by kokanee compared with trout in Marion Lake.
The Potential Effects of Search Positions on Dietary Patterns
The use of different search techniques and differences
in the frequency of use of the same techniques leads to differences
in the distributions of search positions of trout and kokanee when they forage at the lake surface or bottom. What effect will this have on dietary patterns? A general answer to this question relies on the potential interaction betwen the search positions of the predators and visual detection of prey.
Visual predators like trout and kokanee display attack responses that are dependent on prey size (Ware, 1971; Hyatt,
this study). On the basis of laboratory observations, Ware
suggested that when trout search for benthic prey they maintain
a fixed search position and that this functions to create a
refuge from detection for prey that are below a specific size
limit. Adapting Ware's results to the present study, it is
apparent that the, further a predator's search position is
from the location of the prey, the larger the prey must be to 97 elicit an attack (Fig. 18). If these results are used to predict the minimum sizes of prey that the predators may detect at the lake surface or bottom it becomes apparent that the minimum prey sizes detected by kokanee should be considerably smaller than those detected by trout (Figs. 17 & 18). This inference will be misleading in the event that trout possess greater visual acuity than kokanee and respond to the same range of prey sizes from a greater distance. For example
Protasov (1968) reported that mullet reacted visually to 15 mm prey at a distance of 25 cm while horse mackerel reacted to identical prey at 65 cm. To test for possible differences in the abilities of trout and kokanee to detect similar prey
I conducted a number of laboratory experiments.
4-B. LABORATORY COMPARISONS OF PREY DETECTION
INTRODUCTION
I have suggested that trout and kokanee will often detect a different range of prey sizes in the field because they maintain different search positions at the lake surface and bottom. A second possibility is that trout and kokanee exhibit differences in their abilities to visually detect prey and that both species will detect the same range of prey sizes in the field despite the maintenance of different search positions.
To test this hypothesis I conducted laboratory experiments to compare the reactive distance (RD) of trout and kokanee where RD is defined as the distance between the fish and prey when the predator initiates an attack. 98
FIGURE 18 The minimum prey size required to elicit an attack
by trout in search positions at various distances
from the substrates on which prey are located.
Adapted from data in Table 1. (p. 95) of Ware, 1971. -i i 1 1 1 1 r 20 40 60 SEARCH POSITION (c .Like other investigators (Holling, 1966; Beukema,
1968), I have assumed that RD to food items is a function of the predator's ability to visually detect food items. For fish, this assumption is amply supported by Ware's extensive experiments (1971) which demonstrated that RD is controlled by prey characteristics such as size, contrast and movement but not by predator characteristics such as hunger (= degree of gut fullness).
METHODS
In experiments conducted to assess the reactive distance of fish, the methods of prey presentation may have an important effect on the results obtained. In most studies, the prey are introduced one at a time, at one end of a long, narrow tank, and out of sight of the predator (Ware, 1971;
Werner & Hall, 1974; Confer & Blades, 1975). Because of the dimensions of the experimental tank, the predator must swim in one direction only and will inevitably approach the prey.
The advantage of this technique is that it guarantees that each attack by the predator is a controlled event (unless the prey are "detected" with the aid of stimuli unintentionally provided by the experimenter when introducing the prey to the tank). The disadvantages are that a great deal of time is required to obtain replicate observations, the predators are often disturbed by handling between single attacks, and the shape of the tank forces the predator to detect prey along 100 only the axis of the visual field in which binocular vision functions.
In order to allow prey detection along all axis of of the visual field, I used an experimental arena (92 x 47 x
45 cm) which did not force the fish to respond in only one direction. To reduce the time required to obtain replicate observations, I introduced single predators into the experimental arena when it contained a population of well dispersed prey. I then recorded the reactive distances of fish in consecutive attacks on prey.
The front and bottom of the experimental tanks were marked off in a numerical and alphabetical lattice of
2.5 cm squares. By recording a coordinate from each of these at the beginning and end of an attack, I could measure the reactive distance involved in each attack, at the end of an experimental session. A number of features aided in an accurate determination of the coordinates. The discovery of a prey item was always clearly indicated by a sudden change of velocity or of both velocity and orientation by the predator. Because the fish were highly conditioned to the presence of an observer it was possible to follow their movements from a position as close as the front of the tank would allow. This along with the modest dimensions of the experimental tank (92 x 47 x 45 cm) allowed the observer enough freedom of movement to visually track the fish and avoid problems of parallax. Finally, the shadow caste on the tank bottom by the moving or stationary fish served as a useful cue in determining- its true position 101
with respect to the bottom coordinates. Preliminary trials
with an independent observer produced acceptable estimates of the
coordinates indicating the initial and final positions of an
artificial . predator (a piece of hose) moving at velocities
equivalent to those exhibited by trout and kokanee in the
experiments.
It is critical to the interpretation of the results
that the distribution of reactive distance values (DRD) exhibited
by fish in the arena is a consequence of prey detection taking
place as a series of separate events. However, there is an
alternate interpretation that must be dealt with. Since the
predators were hunting in an arena that contained more than one
prey item, it was possible for them to detect more than one
prey item at a time (ie: consecutive responses to prey may
not represent separate incidents of prey detection). In this
event, DRD would simply represent an index of the distance
between consecutive prey locations and not a measure of the
. distance at which the fish detect prey. To distinguish between
the alternatives that DRD serves as an index of the predator's
ability to detect prey or of prey spacing, I examined the effect
of prey density changes on DRD.
.Experiment 4.1 Reactive Distance and Prey Density
If DRD is an index of prey spacing, there should
be a significantly greater frequency of long reactive distances
in experiments conducted at low prey densities compared to 102
high density experiments (ie: closer prey spacing). This will not occur if the detection of prey proceeds as a series of separate events in the arena. I recorded DRD in separate trials with each of three kokanee (130-150 mm long) foraging for mayfly
(Ephemeroptera) larvae. In the arena I used prey densities of 20, 40, 100 and 200 per .42 m . All predators were maintained and handled in a standard fashion before experimental trials
(Chapter 1, general methods).
Experiment 4.2 Reactive Distance, Trout vs. Kokanee
Experiment 2.1 indicated that DRD will serve as a measure of the ability of the predators to detect prey (see results) rather than as a measure of prey spacing. Therefore,
I proceeded to use DRD in comparing trout and kokanee for differences in perceptual sensitivity to prey. Three rainbow
trout and three kokanee, obtained from Marion Lake were used
in these experiments. They ranged in length from 130-160 mm.
I conducted separate experiments for both species with two different prey types. The large and small prey types used
(16 mm damselfly larvae and 3 mm Daphnia) span a range of prey size similar to that normally encountered by the predators
in Marion Lake. 103
RESULTS
Experiment 4.1 Reactive Distance and Prey Density
The DRD of kokanee, responding to mayfly larvae,
in low-density experiments, did not exhibit a greater frequency
of long reactive distances (p 5>.98, Kolmogorov-Smirnov, one-
tailed-test, Siegel 1956) than in high-density experiments
(Table 15). Thus it appears that the detection of prey items proceeds as a series of separate events in spite of the presence
of numerous prey in the experimental arena. The substantial difference between DRD of kokanee responding to either
stationary or moving nymphs (Fig. 19) constitutes a second line of evidence supporting this conclusion. If DRD were simply measures of prey distribution, they should have been dramatically different in the low and high-density trials and identical
for moving and stationary prey. Thus, I conclude that DRD
is a legitimate index of the predator's abilities to detect prey.
TABLE 15 Distributions of reactive distance of kokanee to stationary ephemeropteran (mayfly) nymphs in low density (20 & 40 prey/.42 square meters) and high density (100 & 200 prey/.42 square meters) experiments.
Reactive Distance (cm) 0-5 6-10 11-15 16-20 21-25 26-30 31-35 36-40 N Density Number of Responses
Low 7 16 15 5 1 2 0 0 46
High 0 7 15 8 2 0 11 34 104
FIGURE 19 Frequency distributions of reactive distance of
kokanee responding to either stationary or moving
mayfly nymphs (Ephemeroptera, Centroptilum
sp.). N = the total number of observations.
105
Experiment 4.2 Reactive Distance-Trout vs. Kokanee
Comparisons of DRD (Fig. 20) indicate that trout do not respond more often to prey at greater distances than kokanee (All comparisons p>.95, Kolmogorov-Smirnov, one-tailed- test). They also indicate that large prey are at greater risk of detection than small prey (compare 3mm Daphnia to 16 mm odonates) and that moving prey are at greater risk of detection than stationary prey of identical size (compare stationary odonates to moving ones).
Because trout and kokanee consistently maintain different search positions in the field and respond to identical prey at similar distances in the laboratory, I conclude that they will experience different probabilities of detecting the same sizes of prey in the field. For instance , trout usually maintain search positions that are further than 20 cm. away from the sediment and consequently should seldom detect 2 benthic prey as small as 3mm (the approximate size of the small prey used in experiment 4.2). Conversely, kokanee should frequently detect prey in these small size classes.
It is wise to exercise some caution in the application of laboratory determinations of reactive distance to the field situation. Although the laboratory data clearly indicate that both trout and kokanee should occasionally attack prey the size of larval odonates, from distances greater than 50 cm.,
I never observed attacks on benthic prey in the field from distances greater than 50 cm. Similarly Ware's (1971) deter• minations of reactive distance in the laboratory suggest that 106
FIGURE 20 A comparison of the frequency distributions for
reactive distance of trout and kokanee to large
and small prey types, (a.) reactive distance of
kokanee to large prey (16 mm odonates, Enallagma
sp.) that are moving or stationary (b.) reactive
distance of trout to large prey that are moving or
stationary (c.) reactive distance of kokanee to
small prey (3 mm zooplankton, Daphnia sp.) that
are moving (d.) reactive distance of trout to small
prey that are moving. ^90T 107
very high contrast targets (white cylinders of liver offered against a black background) of approximately 15 mm are seldom detected from greater than 70 cm by trout, while my field 2 observations indicate that targets of only 10 mm may be detected at distances greater than 85 cm. This simply emphasizes the difficulty of exactly duplicating field conditions in the laboratory, and warns against the expectation that laboratory determinations of reactive distance, combined with field estimates of search positions, will lead to predictions of the absolute minimum size of detectable prey in the field.
DISCUSSION
The Role of Search Positions in Producing Specific Dietary Differences Between Trout and Kokanee
There is a general trend for trout from Marion Lake to include a greater proportion.of large prey in their diets than kokanee of comparable sizes do (Chapter 2, Fig. 4). This trend is in part related to the fact that for many prey types eaten by both.trout and kokanee, trout consume a higher proportion of large individuals than kokanee (eg. amphipods-
Fig . 5, molluscs-Fig. 6, zooplankton-Fig. 7). Results presented in this chapter help explain why this trend occurs.
Laboratory evidence (Experiment 4.2) suggested that trout are unable to detect small prey at greater distances than kokanee, yet in the field trout consistently assumed search positions that were further away than kokanee from the locations of prey at the lake surface or bottom. Therefore, 108
a given size class of a single prey type must experience different probabilities of detection by trout or kokanee and,
in general, the minimum sizes of benthic or surface prey detected by kokanee will be much smaller than those detected
by trout. Thus, it is no longer surprising that small
Hyalella sp. (3-4mm) make up a greater proportion of the
benthic amphipods in the diet of kokanee, while large Crangonyx
sp. (7-10mm) are more abundant in the diet of trout (Chapter 2,
Fig. 5 and Table 4).
The interaction between visual detection of prey
and search positions of predators may also account for differences
in patterns of exploitation of other benthic prey types.
Small molluscs such as pisidium spp. are often absent from
the diet of trout but are usually present in the diet of
kokanee (Sandercock, 1969 and Chapter 2, Fig. 5). Similarly,
the majority of caddis larvae (Trichoptera) in the diet of
kokanee are from small size classes (as indexed by head capsule
width), while trout exploit a greater proportion of large
caddis larvae (Table 16).
TABLE 16. Head capsule widths (mm) of larval trichopterans consumed by trout and kokanee. Data from Winterbourn, 1971.
Head Width (mm) 0.4-0.8 0.8-1.2 1.2-1.6 1.6-2.4
No. eaten by trout 39 151 232 265
No. eaten by kokanee 8 13 109
The Role of Search Techniques and Search Positions in Producing Differences Between the Proportions Of Prey Types Observed in the Natural Environment and in the Diets of Trout and Kokanee
Knowledge gained concerning search techniques and search positions not only provides insights into the reasons
for dietary differences between the predators but also contributes to a greater understanding of why discrepancies may exist between the apparent availability of potential prey
in the lake environment and in the diets of trout and kokanee
(Chapter 2, Fig's. 8 & 9).
In essence, the discrepancies exist because the sampling devices (eg. Ekman dredge, Kajak core, Hargrave sampler) used by scientists to determine the relative abundance of invertebrates in the lake do not remove samples of prey from the environment in the same way that either trout or kokanee do. For example, an Ekman dredge removes samples of benthic prey without distinguishing whether they are exposed on the mud surface, concealed just beneath the surface or buried under several mm of sediment. By contrast, search techniques of trout allow them to obtain only those benthic prey that are exposed on or above the sediment surface and search techniques of kokanee prevent them from gaining access to prey buried more than a few mm beneath the sediment. Since there are regular patterns in the vertical distribution of different prey types within benthic sediments (Burgis et al. 1973),
the depth of penetration of sampling gear and predators biases them to obtain some prey but not others or to obtain 110 different proportions of the same prey types. This may explain why the single most abundant species of chironomid larvae
(by numbers or by volume) present in Marion Lake has never been recorded in the diets of the fish (Efford & Tsumura, 1973).
Trout not only exploit a greater proportion of large prey than kokanee, but also overexploit large sized individuals of a given prey type relative to their abundance in the environment. Amphipods (Chapter 2, Fig. 5) and caddis larvae
(Winterbourn, 1971) are two prey types which demonstrate this pattern.
Winterbourn (1971) found that 72% of the caddis eaten by trout in Marion Lake belonged to the last or second from last instar of each species. He concluded that trout were "selecting" the largest sizes of caddis available at all times of year.
This was especially apparent when the species composition of caddis eaten each month was related to the life histories of each of the species. Different species of caddis were preyed upon sequentially as their last instars appeared in the lake.
In late summer and early fall, caddis larvae were of least importance in the diet of trout, although they were present at maximum abundance for the year as small, early-instar stages.
If the distribution of search positions observed for trout are representative of the times of the year when observations were not carried out (evidence that this is likely will be presented in a later chapter), then seasonal changes in the probability of detection of single prey species (eg. caddis) will occur as changes in sizes of prey occur at different developmental stages (Ware, 1973) . This is a plausible explanation to account for the seasonal and apparently size-dependent exploitation of both caddis larvae and amphipods by trout.
Unexplained Dietary patterns
Knowledge about search techniques, search positions and microhabitat-specific search in the field has improved my ability to explain the basis for differences in the prey
contents of predators and environment, but a number of
significant dietary patterns continue to resist my attempts
at explanation.
If trout and kokanee obtained all of the small-prey
component of their diets from surface or bottom sub-habitats,
then search positions alone would generate the observed
differences in the size-frequency distributions of prey that
they obtain. However, many of the small prey that trout and
kokanee exploit originate from the water column. In the later
summer months, kokanee of average size obtain a large proportion
of their food (48% by weight in Aug.) from small (usually
less than 1 mm body length) cladocerans and copepods found
in the water column (Efford & Tsumura, 1973). Although in
late summer trout spend at least as much time as kokanee in
the water column, zooplankton never contribute more than 0.5%
(by weight) of their diet. For the smallest trout and kokanee
which at times obtain virtually all of their food from the
water column (CHapter 2, Fig. 7 & table 5), there are major
differences in the species and size-class composition of zooplankton exploited. No mechanism proposed thus far will satisfactorily explain these differences.
The maintenance of species-specific, search positions by trout and kokanee will clearly favour the detection and exploitation of a greater proportion of small caddis larvae by kokanee than by trout but it does not offer a ready explanation for why kokanee exploit so few caddis larvae in all size classes relative to trout. In the next chapter, I will address the general hypothesis that differences in morphology and the behaviour of trout and kokanee during approach, capture and ingestion of prey will account for some of these unexplained dietary diferences.
SUMMARY
1. Trout and kokanee exhibit some species specific search techniques (Table 12).
2. The search techniques that trout and kokanee share are not practised with the same frequency and are not always employed to locate prey within the same sub-habitats.
3. Search techniques employed by kokanee are more sub- habitat specific than those used by trout (Table 12).
4; The majority of kokanee search for benthic prey from positions that are within 5 cm of the sediment surface, while trout are most often observed searching for benthic prey from positions some 15 to 30 cm off of the bottom (Fig. 16). 113
5. The majority of kokanee search for lake surface prey from positions that are 5 to 30 cm below the lake surface, while trout are most often observed searching for these prey from positions some 45 to 100 cm below the surface (Fig. 17).
6. Differences in the search techniques of trout and kokanee result in some degree of microhabitat specific search but are not easily related to any qualitative' differences in their diets.
7. Differences in search techniques likely account for certain quantitative differences in the diets of the predators such as the greater utilization of chironomid larvae by kokanee than by trout.
8. Trout and kokanee consistently maintain different search positions in the field and respond to identical prey at similar distances in the laboratory (Fig. 20), therefore they must experience different probabilities of detecting the same sizes of either benthic or lake surface prey in the field.
9. The sampling devices used by scientists to determine the relative abundance of benthic invertebrates in the lake do not discriminate between "prey" exposed on the mud surface, located just beneath the mud surface, or located several mm under the mud surface. When searching for benthic prey, trout and kokanee undoubtedly do discriminate in this fashion.
Therefore some discrepancies will exist between the apparent availability of prey in the lake (as measured by scientists) and patterns of prey utilization by trout and kokanee because
scientists and fish do not use the same procedures to detect prey sampled from the lake environment. 10.) Differences in prey-search behaviours of trout and
kokanee do not provide a ready explanation for why kokanee obtain a greater proportion of their diet than trout (by no. or by volume) from relatively small ( <1 mm)water-column prey or for why kokanee obtain so few caddis larvae of all sizes
in their diet relative to trout. 115
CHAPTER 5
THE RELATIONSHIP BETWEEN ATTACK BEHAVIOURS, MORPHOLOGICAL CHARACTERISTICS AND DIETARY PATTERNS OF TROUT AND KOKANEE IN MARION LAKE
5-A. Field Descriptions
INTRODUCTION
Each successful attack on prey by predators usually
involves a series of behaviours which include orientation, approach, contact, capture, manipulation and ingestion of the prey. Predators cannot successfully approach and capture every prey item they detect nor can they successfully manipulate and
ingest every prey item they capture. Interactions between the
behaviour and morphology of a given predator determine whether
an attack is successful or not. Consequently, differences
between predators in both attack behaviours and morphologies
may promote divergent dietary patterns. Morphological
differences and their relationship to resource partitioning by
predators have been studied more extensively than behavioural
differences.
Schoener (1974) has pointed out the convenience and
occasional necessity of estimating differences in resource
utilization of animals by using morphological characteristics
of species. The most common indicator is the size of the feed•
ing structure, which is usually correlated with mean food size,
hardness, or depth in some protective medium. Many experimental studies support the contention that correlations between morpho• logical features and food types do exist. Small heteromyid rodents appear to select seeds on the basis of ease of handling
(Rozenzweig & Sterner, 1970) . Overlap in nectar resource utilization by bumblebee species (Heinrich, 1976) is slight due to differences in tongue length. Numerous authors (Grant et al., 1976; Hespenheide, 1975; Willson, 1972; Rear, 1962) have presented evidence that birds with different bill sizes exploit foods that are different with respect to size (large vs. small) or texture (hard vs. soft).
Results from these studies are not without exceptions
Pulliam and Enders (1971) found that five species of finches in old-field habitats did not divide food resources by size, in spite of possessing a wide range of bill sizes (9.3-18.9 mm).
In Root's thorough study (1967) of five foliage gleaning birds, prey size was not closely related to either body size or bill size. Hespenheide (1975) has warned that many cases exist in which species are quite similar morphologically but exploit quite different dietary items due to behavioural differences.
Similarly, other species which possess striking differences in morphology, may not exhibit striking differences in diet, again for behavioural reasons. Field observations, complemented by experimental studies offer one of the best ways in which to assess the links between attack behaviours, morphological characteristics and dietary habits of predators.
I have identified a number of differences in the dietary patterns of trout and kokanee from Marion Lake (Chapter 117
Many of these differences have been accounted for on the basis of either predator spatial segregation (Chapter 3) or predator search behaviours (Chapter 4), however, the basis for other dietary differences remains unknown (see discussion, Chapter 4).
Therefore, the central focus of this chapter is to test the general hypothesis that differences in predator attack behaviours interacting with differences in predator morphologies will account for some of these unexplained dietary differences.
The chapter is divided into two sections. The first section is essentially descriptive. I will describe the techniques of approach and capture that are used by trout and kokanee during attacks on prey in the field. I will also des• cribe differences in morphological characteristics of the predators that may affect their attack success with prey. On the basis of these descriptions I will propose a number of hypotheses concerning the likely outcome of attacks on prey by trout and kokanee. The second section of the chapter consists of a series of laboratory experiments designed to test these hypotheses. Finally, I will discuss the significance of the
findings for explanations of patterns of food-resource partitioning exhibited by the predators in the field.
METHODS
Attack Techniques
Descriptions of the attack techniques of free ranging
trout and kokanee were completed at the same time as observations on their search behaviours. Details concerning specific locations, times, and techniques of obtaining observations can be found in this earlier work (see Chapters 3 and 4). One problem with direct observation in the field is that the finer details of attacks on prey items are seldom seen since the observer is usually no closer than .5 m to the predator. For this reason I will include some information obtained during preliminary laboratory observations of attack techniques of trout and kokanee exploiting a variety of prey.
Morphological Characteristics
Superficially rainbow trout appear to be stockier than kokanee of similar length. From a dorsal aspect, trout also appear to be less streamlined and to possess a more massive jaw musculature than kokanee. Thus, I anticipated that significant differences would exist in their body-length versus weight relationships as well as in the structure of their oral cavities.
I compiled length and weight data on fish taken from a summer trapping program. Trout and kokanee were removed from trap-nets (in which they had been captives for 24-72 hours) anesthetized with-MS 222, measured for fork length to the near• est mm, and then weighed on a gram balance. After tagging and recovery, fish were released to the lake. I determined the relationship between jaw width and standard lengths of predators from measurements taken on samples of fish that had been stored in 10% formalin. Jaw width was measured with Vernier calipers, as the horizontal distance (to the nearest .1 mm) between the 119
posterior tips of the premaxillaries. Gill-raker examinations were also conducted on preserved fish.
RESULTS
Techniques of Approach and Capture
Once a prey had been detected by a predator in the
field, I could distinguish between five techniques of approach
and capture that were used during attacks on prey (Table 17).
None of these approach and capture techniques were specific to only one search technique (Chapter 4) but some were used more
frequently by trout or kokanee.
TABLE 17. Techniques of approach and capture used by trout and kokanee during attacks on prey in the field.
Level of Occurrence Technique Trout Kokanee
Rush +++ ++ Stalk + ++ Dart N ++ Jump ++ N Scrape + +
+++ very common ++ common + occasional N never observed 1. Rush
After detection of a food item the predator orients briefly to face the target, accelerates to reach its location and just before the moment of contact opens its mouth to engulf the prey. Trout may rush prey while operating in hover-and
-search or cruise-and-search modes (Chapter 4). The rapid acceleration to reach invertebrate prey, which are generally detected from less than 80 cm away, is accomplished by several powerful strokes of the caudal fin. Rough estimates of times taken to cover the distance to prey suggest that trout attain velocities of 50 to 150 cm per second during a rush on invertebrate prey. An entire attack sequence (orient, approach, engulf) is usually completed within 2 to 3 seconds.
Because kokanee maintain search positions that are closer to the locations of prey, they have fewer opportunities to use this technique and when rushing prey they do not appear to attain the high velocities that trout do.
2. Stalk
After sighting a prey, a swimming predator typically decelerates by performing braking movements with both pectoral and pelvic fins. After a brief pause for orientation, a slow approach (1 to 5 cm per second) is accomplished with the aid of pectoral fin sculling. The predator may stop entirely before the final phase of the approach when either a rush (trout) or a dart (kokanee - see description below) will be used to cover the remaining distance (usually just a few cm) to the prey. 121
Trout do not use this technique of approach very often and I have only observed them use it in approaching vertebrate prey such as salamanders (Ambystoma gracile, Taricha granulosa) or sticklebacks (Gasterosteus aculeatus). Kokanee use this approach frequently when they are hunting for benthic prey in the field or for certain species of zooplankton in the laboratory.
3. Dart
After completing a stalking approach, kokanee employ dart to cover the final 2 to 5 cm between themselves and certain types of prey. Dart begins from a stationary position. The predator flexes its body into an exaggerated sigmoid posture and then rapidly thrusts forward with mouth agape to engulf the prey. The technique differs from rush or stalk in that the posture assumed to perform dart is well outside of the range of normal swimming movements, the distance covered by dart is always less than one body length of the predator, and the move• ment is completed within a fraction of a second.
In the laboratory this technique was predictably evoked by copepods (Diaptomus kenai) and less commonly by amphipods
(Hyalella azteca) which exhibit marked avoidance responses to approaches by predators. In the field kokanee commonly exhibited this movement while foraging for benthic prey.
I never observed trout use dart during attacks on prey in the field or in the laboratory. 122
4. Jump
This movement is only executed by trout when they detect
adult insects above the lake surface. The initial stages of
the attack are identical to rush, however the acceleration of
the predator allows it to break the surface of the water and to
continue into the air to contact and capture the prey. A small
trout (15 cm) which accelerates from a distance of 50 to 80 cm
below the lake surface may clear the water by more than a body
length when leaping for aerial prey such as caddis adults.
• 5. Scrape
While moving along a firm, smooth substrate, a fish,
with its mouth held flush to the substrate surface, carries
out repeated biting movements. Trout use this tactic to attack
small, sessile animals which are anchored to the underside of
lily leaves, plant stems, submerged logs and limbs. Trout and
kokanee most frequently use the technique to obtain prey from
lily leaves which may possess more than 25 cladocerans per
square cm in late summer (Starr, 1973). A predator typically
moves from the underside of one leaf to the next within a
single lily bed and may move directly from one bed to another
several meters away where it will continue to use this attack
technique.
Kokanee appeared to use this technique less frequently
than trout but this is likely because only a small proportion
of the total number of kokanee observed were in inshore areas
that have abundant weed beds and submerged snags (Chapter 3). From both field and laboratory, observations, I have summarized the prey types that are taken by the predators using different approach and capture techniques (Table 18). These observations are strictly qualitative and do not reveal how often the tactics are used or the full range of prey species that each predator exploits. However, it is apparent that different tactics are used with different prey and that trout and kokanee may use different techniques to attack the same prey.
Comparisons of Predator Morphologies
In spite of their stockier appearance trout are not significantly heavier than kokanee of equivalent length (Fig. 21) from Marion Lake. Therefore differences in appearance must be due to differences in the way that a given amount of weight is apportioned. The false impression that trout are heavier than size-matched kokanee is in part created by the less streamlined appearance of the head region of trout. In quantitative terms this difference is expressed clearly by differences in the jaw widths of trout and kokanee of equivalent size (Fig. 22). For predators spanning the size range of most interest in this study (120-160 mm) kokanee exhibit jaw widths that are 3-4 mm or approximately 30% smaller than trout of equivalent body size. It would be surprising if such differences did not have a major influence on the capture and handling success experienced by the predators when faced with a variety of prey. 124
TABLE 18. A list of prey types observed to evoke specific approach and capture techniques in the laboratory (L) and field (F).
a. Trout
Rush Stalk Jump Scrape amphipods salamanders chironomid cladocerans (L & F) (F) adults (F) Sida sp. (F) caddis larvae stickleback caddis adults (F) (F) (F) damselfly 1. damselfly (L) adults (F) gyrinids (L & F) gerrids (F) sticklebacks (F) aquatic insect pupae (L & F) notonectids (L) copepods & cladocerans (L) b. Kokanee
Rush Stalk Dart Scrape amphipods copepods copepods cladocerans (L & F) (L) (L) Sida sp.(L & F) mayfly nymphs amphipods amphipods (L) (L & F) (L & F) damselfly 1. (L) insect pupae (L & F) cladocerans Daphnia sp. (L) notonectids (L) 125
FIGURE 21. The relationship between fork length and wet weight
of trout and kokanee from Marion Lake. Note that
representative data points were randomly drawn and
plotted but N = the number of trout or kokanee
actually measured. 125a
o TROUT Log Y =- 1.928 +2.925 Log X N=I20
-1 r r-—i r 1 1 r~ 5 6 7 8 9 10 20 30
FORK LENGTH (cm) 126
FIGURE 22. The relationship between standard length and jaw gape
of trout and kokanee from Marion Lake, jaw gape is
taken as the horizontal distance between the posterior
tips of the premaxillaries. Note that representative
data points have been plotted but N = the number of
trout or kokanee actually measured. 9 TROUT, Y= - .5567 + .08388 x, N= 122
O KOKANEE, Y=-.5987 + .06234x, N=98
STANDARD LENGTH (mm) CTi 127
Ordinarily kokanee possess 28 to 40 long, serrated rakers on the first gill arch, while trout possess 17 to 21 medium length rakers (Clemens and Wilby, 1961). My examination of
25 kokanee and trout from Marion Lake indicates that kokanee have 28-32 gill rakers on the first gill arch and that trout have
17-21. Thus although kokanee from Marion Lake exhibit a reduct• ion in the range of gill rakers normally observed, they still possess many more than trout.
DISCUSSION
A single attack on a prey is a complex event that may proceed in stages from initial orientation through approach, contact, capture, manipulation and ingestion or rejection by a predator. A successful attack is one which results in the ingestion of the prey. In this study, I operationally define attack success as the proportion of prey ingested to prey detected and then approached. Although interactions between predators and prey during any stage of an attack may influence overall levels of attack success, the descriptions presented here were not intended to provide a detailed assessment of the influence of each attack stage on attack success (e.g.,
Beukema, 1968) , but rather to provide a basis on which to propose specific hypotheses concerning differences in the out• comes of attacks that trout and kokanee are likely to experience in encounters with a variety of natural prey. 128
The Capture-success Hypothesis
Capture success is operationally defined here as the proportion of prey that are grasped firmly or "secured" in the mouth of a predator relative to the total number of prey approached or pursued after detection and orientation. To derive the capture success hypothesis, I have relied on the observations that trout and kokanee sometimes use different approach and capture techniques on the same types of prey and that they individually use different approach and capture techniques with varying degrees of success on different types of prey (Table 18). For example preliminary laboratory obser• vations suggest that trout utilizing "rush" during attacks on copepods may experience lower levels of capture success than kokanee using "stalk and dart". Field observations also indicate that trout frequently miss when jumping to catch adult caddis and that successful capture never follows a "rush" on surface prey such as water striders (Gerridae), in spite of the initiation of numerous attacks by trout.
The observations above suggest that differences in the approach and capture techniques used by trout and kokanee in the field likely alter the overall success of attacks on prey that are relatively small, fast, or agile and which exhibit avoidance responses during attacks by fish. Such prey will tax the reflexes and maneuverability of a predator up to the point of capture, but once captured, are unlikely to present much difficulty during the manipulation and ingestion phases of 129 attack. Since a number of the prey types constituting signifi• cant proportions of trout and kokanee diets conform to these characteristics (e.g., zooplankton, amphipods, mayflies), I hoped that results confirming differential capture success might form the basis for explanations of some of the unexplained dietary differences between trout and kokanee. Therefore, the capture success hypothesis clearly stated is that "differences in the capture success of trout and kokanee during encounters with small prey in the field play an important role in shaping predator-specific, diets."
The Gill-raker, Prey-size, Hypothesis
Kokanee possess a greater number of long serrated gill-rakers than trout. Kokanee in Marion Lake consistently exploit larger quantities and smaller zooplankton than trout do
(Chapter 2, Figs. 2 and 7). These differences in diet occur throughout the geographic range of trout and kokanee. Thus, this species pair serves as another example of the observation by many authors that fish with well-developed and numerous gill-rakers rely on zooplankton to a greater extent as a source of food than species which possess fewer, shorter, gill-rakers.
Many authors have suggested that gill-rakers function much like a sieve or filter during feeding and thus control the size range of planktonic prey that predators retain (see Hyatt,
1979 for a critical review of this topic). I initially expected that kokanee in Marion Lake must obtain more zooplankton than 130
trout by filtering in response to high densities of small prey.
The movements that characterize filtering as an "attack" procedure include the maintenance of a fully-opened mouth for up to a few seconds at a time during passage by a fish through a concentration of small plankton. To my surprise neither kokanee or trout in the field exhibited the characteristic feeding movements associated with the tactic of "filtering" small prey. Instead, both species always operated in a
"raptorial" mode by pursuing and grasping individual prey items.
Apparently some plankton-feeding fish always operate in raptorial mode (Kjelson, 1971), while others can operate in either filtering or raptorial modes (Leong & O'Connell, 1969;
O'Connell & Zweifel, 1972). For the latter species, the choice of technique appears to be influenced by the absolute density of the prey and the relative proportion of large to small prey.
I did not take samples to determine the densities or sizes of zooplankton present in the field during any of the observation sets, consequently the hypothesis that kokanee exploit more and smaller zooplankton than trout by filtering on occasions when they encounter high densities of small prey remains to be tested under controlled conditions in the laboratory.
The Attack Rate Hypothesis
Although trout and kokanee often appear to use the
same attack techniques when foraging in the field, there are
frequently quantitative differences in the number of attacks
initiated. For example, when foraging in the water column, kokanee were observed to initiate as many as 15 attacks over a 2 meter distance while trout seldom initiated more than 5.
Given the velocities maintained by the predators at these times (Chapter 4, Table 10)/ kokanee must attain attack rates exceeding 1 per second while trout do not exceed 1 attack per
3 seconds. The difference in attack rates may be a consequence of either trout and kokanee consistently hunting for different types of prey or of kokanee achieving a higher rate of detection or shorter attack times than trout on the same planktonic prey. The "attack" rate hypothesis assumes the latter case to be true and that as a consequence kokanee may accumulate a greater quantity of zooplankton in their diet compared to trout.
The Mouth-size, Ingestion-success Hypothesis
Kokanee exhibit smaller mouth dimensions than trout of similar length and weight. Although this may be advantageous for the capture and retention of small, agile prey, it is also likely that it results in a greater degree of difficulty for kokanee compared to trout in successfully manipulating and ingesting large "armoured" prey once they have been captured.
If this proves to be the case it will help explain a number of the outstanding differences in the types of prey that are included in the diets of free-ranging trout and kokanee. 132
5-B. Laboratory Tests of Hypotheses Concerning Prey Attack by Trout and Kokanee
I have proposed four hypotheses concerning the relationships between attack behaviours, morphological character• istics and dietary patterns of trout and kokanee. This section consists of a series of laboratory experiments designed to test these hypotheses.
METHODS
Experiment 5.1 The Capture-success Hypothesis
This experiment consists of feeding trials in which trout and kokanee were given separate opportunities to attack small amphipods (Hyalella azteca), copepods (Diaptomus kenai), and cladocerans (Daphnia pulex). These prey were chosen so that differences in attack success by the predators would depend upon approach and capture techniques rather than on difficulties during manipulation or ingestion of prey. A second consideration was that all individuals of the smallest prey type selected for feeding trials (D_. pulex) had to be large enough to be visible in all locations within the experimental arena
(92 x 47 x 45 cm) to an outside observer.
I obtained H_. azteca fresh from Marion Lake. D_. kenai were obtained from nearby Eunice Lake and D. pulex were cultured in the laboratory specifically for these trials. I used a graded series of sieves to obtain prey of uniform sizes for introduction into the experimental arena. Trout and kokanee used in trials 133 with the above prey were size-matched. Table 19 lists the characteristics of both predators and prey used in this experi• ment. I followed standard procedures, outlined earlier (Chapter 1), for capture, handling and preparation of predators to take part in experiments.
To conduct a trial, I introduced a single predator into the arena when it contained a population of well dispersed prey. I then recorded capture success (CS = # of captures/ # of pursuits) and ingestion success (IS = # of prey ingested/ # of prey captured) of predators during encounters with prey.
Although multiple trials were performed with each predator- prey combination (see Chapter 6), results across all trials are pooled here.
Experiment 5.2 The Attack Rate Hypothesis
The majority of freshwater zooplankton have maximum body dimensions of less than 3 mm. Preliminary field observa• tions led me to suggest that kokanee might be capable of sus• taining higher attack rates than similar sized trout on concen• trations of small planktonic prey. To test this hypothesis,
I conducted trials with trout and kokanee foraging for
Daphnia pulex at different densitites under controlled conditions. I used a sieve to obtain a limited size range of
D. pulex (1-3 mm) from laboratory cultures. Prey removed by predators during a feeding trial were not replaced as the trial proceeded. TABLE 19. Characteristics of predators and prey used in experiments to determine the attack success of trout and kokanee on a variety of prey.
PREY KOKANEE TROUT
Mean NO. Mean No. Mean Identity Size Range Used Size Range Used Size Range (mm) ( cm) (cm) Zooplankton Daphnia sp. 1.5 1.0- 2.5 5 11.4 10 .3-12.7 4 11.2 9.2-13.1 Diaptomus kenai 2.0 1.0- 3.0 4 8.4 7.6- 9.3 4 8.9 7.7-11.4 Chaoborus spp. 10.0 7.5-14.5 4 16.4 15.6-17.7 6 16.4 14.9-21.6 6 * 8.7 7.7- 9.2 Amphipods Hyalella azteca 4.6 3.5- 6.0 4 13.0 12.0-13.5 4 15.2 13.4-17.0 Crangonyx richmondensis 8.3 8.0- 8.7 3 14.7 14.5-14.9 4 15.2 13.4-17.0
Others Notonecta undulata & Buenoa confusa 10 .5 6.5-14.0 4 16.4 15.6-17.7 4 12.1 11.8-12.4 Ephemeroptera (Centroptilum sp.) 11.8 10 .1-12.6 3 12.7 12.4-13.3 Not-tested Odonata (Enallagma sp.) 15.6 15.0-16.2 3 14u2 13.2-15.0 4 15.0 12.5-16.5 Trichoptera (species unknown). 15.0 10.0-16.5 8 14.8 13.4-16.0 Not tested
two groups of trout were used in the tests with Chaoborus spp. in order to examine the within species effect of predator size on capture and ingestion success. Any advantage that kokanee might display compared to trout in obtaining planktonic prey could result either from genetically determined differences in behaviour and phenotype or from differences in experience the two predators have had in foraging for zooplankton. To partially eliminate the influence of differences in foraging experience on results in this experiment, I collected juvenile trout and kokanee from the field in the fall of 1973 and provided them with an identic feeding regime in the laboratory until the time of the experi• ments in June of 1974.
During the laboratory conditioning period, trout and kokanee were fed exclusively either frozen brine shrimp or fresh zooplankton. All of these food items were relatively small and were obtained in the water column by the predators.
A forced air bubbler helped keep the brine shrimp suspended during the feeding periods. Thus, trout and kokanee used in experiment 5.2 were highly preconditioned to feed upon zoo• plankton.
Experiment 5.3 The Gill-raker, Prey-size Hypothesis
The observation that kokanee did not "filter" small prey in the field did not falsify the hypothesis that their more numerous gill rakers give them an advantage over trout in obtaining small prey. Field observations may not have coincided with the times or locations of high densities of small planktonic prey which are most likely to elicit the 136 technique. To provide a more critical test of the hypothesis,
I conducted trials with size matched trout and kokanee foraging for a mixture of very small zooplankton at densities ranging from 7 to 35 per liter. I obtained the zooplankton used as prey from Eunice Lake. Prey larger than 1.5 mm were excluded from the laboratory stocks by sieving. In each set of trials one replicate portion of the prey mixture was set aside and stored in 30% ethanol for determinations of species composition and size distributions of prey at a later date. The other portions were used in trials with individual predators.
Experiment 5.4 The Mouth-size, Ingestion-success Hypothesis
This experiment consists of feeding trials in which trout or kokanee were given separate opportunities to attack caddis larvae (Trichoptera), damselfly nymphs (Odonata), water boatmen (Notonecta), amphipods (Amphipoda), chaoborus larvae
(Diptera) and mayfly nymphs (Ephemeroptera). Specific iden• tities of prey, prey sizes and predator sizes are listed in
Table 19.
I selected the first four prey types for this experi• ment because they possessed combinations of characteristics
(large size, tough body coverings, or slow movements) which improved the likelihood that differences in attack success by the predators would depend on manipulation and ingestion rather than approach and capture techniques. The last two prey types were selected because they were well within the size range of 137 the first four prey types but they lacked their tough, body- coverings. I believed that results from trials with these prey might yield greater insight into the nature of interactions between prey size, prey "texture", predator mouth size and ingestion success of the predators. Multiple trials were com• pleted with each predator-prey combination (Chapter 6) but results across all trials have been pooled here.
In all trials except those dealing with caddis larvae, the species named was the only prey present. I obtained results on capture and ingestion success of kokanee on trichopterans from mixed prey trials in which equal numbers of odonates, ephemeropterans and amphipods were also present. This is not likely to have influenced the results reported here.
RESULTS
Experiment 5.1 The Capture-success Hypothesis
As expected, the overall attack success (prey ingested to prey attacked) of trout and kokanee with small prey (<5 mm long) was controlled primarily by interactions between predators and prey during the approach and capture phase of attack since, with one exception, the predators experienced
100 percent ingestion success with prey after capture (Table 20).
Trout and kokanee both used "rush" as the approach and capture technique in encounters with small cladocerans
(p. pulex). The absence of any avoidance response by these prey enabled both trout and kokanee to achieve 100% capture TABLE 20. A comparison of capture success (CS) and ingestion success (IS) of "size-matched" trout and kokanee in attacks on small, agile prey. TA = total attacks initiated. Data on CS and IS are expressed to the nearest percentage point.
No. of trials conducted with TROUT KOKANEE individual fish Mean size Prey Identity in mm CS IS TA CS IS TA Trout Kokanee
D. pulex 1.5 100 100 2,328 100 100 2,469 16 16
D. kenai 2.0 11 25 495 28 100 4,271 15 16
H. azteca 4.6 91 100 300 94 100 819 4 16 success. Both predators experienced the lowest levels of
capture success in encounters with copepods (I). kenai) . This may be attributed to the highly effective escape responses
exhibited by the copepods. "Rush" was the only approach and
capture technique used by trout, in encounters with copepods,.
.While kokanee shifted from "rush" during the first few attacks
on copepods to a combination of "stalk-and-dart" for the remainde
The greater capture success that kokanee, compared to trout,
experience with copepods is due to this shift of approach and
capture techniques. It is not clear at this point why trout
ingested only 25% of the copepods that they did capture. This
is especially surprising in view of the high ingestion success
that kokanee exhibited with these prey (Table 20).
Trout used "rush" while kokanee employed either "rush"
or "stalk-and-dart" as approach and capture techniques in
encounters with Hyalella sp. These prey exhibited avoidance
responses at the instant of physical contact with the predators.
The high capture success of trout and kokanee with the prey
indicates that the avoidance response of amphipods is not as
effective as that of copepods in promoting escape during attacks
by fish.
Results presented here indicate that attack success
is controlled by specific behavioural interactions between
predators and prey during the approach and capture phase of
attack. These results generally support the hypothesis that
such interactions may assume an important role in shaping
predator-specific diets in the field (see discussion). 140
Experiment 5.2 The Attack-rate Hypothesis
Trout and kokanee experienced identical levels of capture success in encounters with cladocerans (D_. pulex) , however, results from the present experiment indicate that the predators sustain different attack rates on these prey at various densitites. The means of the maximum attack rates achieved by kokanee at all prey densities are more than double those attained by trout of similar size (Fig. 23).
Kokanee pursued Daphnia sp. by tracing a smooth path that flowed from one capture to the next with little
interruption and with very precise changes of alignment from one attack to the next. Trout, by contrast, often sculled in midwater, sighted a prey, stopped and then rushed in to make a capture. After a capture trout often stopped abruptly "to search for and line up on" the next prey item. Thus, the higher attack rates of kokanee compared to trout are likely a consequence of interactions between a higher rate of prey detection and shorter attack times on prey. Since trout and kokanee used in this experiment were highly "preconditioned" to feed on zooplankton,
these differences are likely based upon genetically fixed morpho• logical and behavioural traits.
These results support the hypothesis that kokanee may accumulate a greater quantity of zooplankton in their diet compared to trout by sustaining higher rates of successful attack on such prey. 141
FIGURE 23. The relationship between the density of small zoo•
plankton (1.5 mm Daphnia sp.) and the maximum attack
rates of trout and kokanee. Vertical bars indicate
the 95% confidence intervals of the means. N = the
number of trout or kokanee used in trials at each
density.
142
Experiment 5.3 The Gill-raker, Prey-size Hypothesis
It is certain that some fish have the behavioural flexibility to exploit zooplankton one at a time or, depending on the densities and sizes of prey, to switch over to a mode of operation in which many prey are "filtered" from the water simultaneously. Fish attacking prey by the latter method exhibit a peculiar gulping action that resembles exaggerated respiratory movements.
In spite of the provision of very small prey (Fig. 24) at densities ranging from 7-35 per liter, neither trout or kokanee were induced to exploit zooplankton by "filtering". These results fail to support the hypothesis that kokanee with well developed gill-rakers exploit more zooplankton than trout do as as consequence of an ability to filter such prey from the water column. However, the results do offer striking testimony to the superior "ability" of kokanee in foraging for small zooplankton.
Kokanee attain maximum attack rates that are seven to ten times higher than those attained by trout (Table 22 ) and in a half hour feeding session average eighteen times as many attacks on small zooplankton (see Table 21 for species composition) as trout (Table 23). Given that kokanee can function continuously at the average of their maximum attack rate and assuming 100% capture success, they could obtain approximately 2600 small zooplankton per hour. However a limited amount of data suggests that capture success is about 70%, therefore the net intake per hour is likely closer to 1820 zooplankton. Trout in the same 143
FIGURE 24. The size-frequency distribution of prey used between
July 18 and July 26 for the small-plankton, feeding
trials with trout and kokanee. N= 300
0-0.9 .2-.29 .4-.49 .6-.69 .8-.89 1.0-1.09 12-1.29 1.4-1.49 BODY LENGTH OF PREY (mm) 144
TABLE 21. Species composition (as % by number) of small zooplankton used in experiment 5.3 with trout and kokanee.
Low Density Medium Density High Density Identity 7/1 iter 27/liter 35/liter
Diaptomus tyrelli 82 60 83
Bosmina sp. 9 17 9
Holopedium sp. 3 6 5
Polyphemus sp. 3 6 2
Daphnia sp. 0 0 1
Diaphanosoma sp. 2 10 1
Rotifers 0 1 0
Others 1 1 0
Sample size 1,552 1,908 3,466 145
TABLE 22. Means and 95% confidence limits of the maximum attack rates per minute achieved by trout and kokanee exploiting small zooplankton at various densities.
Density of prey Trout Kokanee per liter N N 7 49.5 + 2 .1 4 4.00 + 5.7 3 27 35.3 + 17 .2 3 5.30 + 3.2 4 35 40.5 + 2 4.00 + 4.7 4 Pooled data 42.8 + 7 .0 9 4.50 + 1.7 11
TABLE 23. Means and 95% confidence limits of the total attacks per .5 hours completed by trout and kokanee exploiting small zooplankton at various densities.
Density of prey Trout Kokanee per liter N N
7 43 + 83 3 875 + 211 4
27 49 + 33 4 735 + 760 3
35 36 ± 61 4 673 2 Pooled data 46 + 23 11 783 + 160 9 146
interval of time would exploit only 270 and 189 zooplankton if
I assume they attain 100% and 70% capture success respectively.
One problem with this conclusion is the implicit assumption that trout are putting out a maximum effort to attack plankton during these trials. An alternate interpretation is that trout could perform better but choose not to. Certainly in exploiting
Daphnia sp. these same trout averaged better than 30 attacks per minute, that is, almost 8 times their performance on the much smaller zooplankton. Given that trout can detect the smaller zooplankton, there is no reason for them to fail in attaining similar attack rates on them.
The evidence about the detectability of these prey for trout is conflicting. During most trials with small plankton it was difficult to confirm that trout directed attacks at individual plankters because their sizes are at the lower limit of a human observer's visual resolution. On some occasions when trout and prey were very close to the front of the arena, I definitely saw attacks directed at small zooplankton when they moved. This suggests that trout are capable of visually detecting these prey. Other observations suggest that there is some difficulty in this for trout. Many trout exhibited intense search behaviour throughout the half hour duration of trials conducted at high prey density
(35 prey per liter) but made few attacks. At the end of such trials when large zooplankton (eg. Daphnia sp., Chaoborus spp. etc..) were introduced into the arena, the trout continued to search in the same fashion but displayed a dramatic increase 147 in attack rate. These observations suggest that small prey used in the present experiment are at the margin of trout visual sensitivity but that they are well within the detection range of kokanee.
Regardless of whether trout could attain higher attack rates on small zooplankton, the point is that they don't, while kokanee do. Whether trout are choosing not to attack or are incapable of efficiently locating the smaller zooplankton due to properties of trout sensory capacities, the results will be the same, that is, kokanee will tend to exploit zooplankton and other small (<,1mm) food items to a greater extent than trout.
Experiment 5.4 The Mouth-size, Ingestion-success Hypothesis
Results from this experiment (Table 24 ) indicate that the overall attack success (proportion of prey ingested to prey attacked) of trout and kokanee during encounters with large, invertebrate prey is controlled by predator-prey interactions during the approach and capture phase as well as during the manipulation and ingestion phase of prey attack. When large, armoured prey are involved, events during manipulation and ingestion of prey play a greater role than those during approach and capture in determining attack success (compare IS to CS for trichopterans, odonates, notonectids and amphipods in Table 24).
When large, soft-bodied prey are involved, events during the approach and capture phase alone determine the different levels of attack success (compare CS to IS for dipterans and ephemeropterans in Table 24). TABLE 24. A comparison of capture success (CS) and ingestion success (IS) of "size-matched" trout and kokanee in attacks on different species of invertebrate prey. TA = total attacks initiated. Data on CS and IS are rounded to the nearest percentage point. 95% confidence limits are indicated and are based on the normal approximation to the binomial distribution.
No. of trials Mean conducted with Large, "Armoured", Length TROUT KOKANEE individual fish Prey Types in mm CS IS TA CS IS TA Trout Kokanee
Trichoptera (species unknown) 15.0 93-1-3 2+2 248 16
Odonata (Enallagma boreale) 15.6 67+5 68+7 273 72+4 28+4 618 12 15
Notonecta (Notonecta undulata, Buenoa confusa) 10.5 46+4 6+3 552 45+7 0+0 165 16 16
Amphipoda (Crangonyx richmondensis) 8.3 91+3 100+0 230 68+6 46+7 266 12
Large, Soft-bodied, Prey Types
Diptera (Chaoborus americanus, C. 10.0 93+1 100+0 1,934 86+2 100+0 1,990 18 18 trevittatus) * 80+4 100+0 441
Ephemeroptera (Centroptilum sp.) 11.8 60+3 100+0 794 13
* trout in this group were only half the size of trout and kokanee "matched" for size in the other groups that were tested with Chaoborus spp. See Table 19 for predator sizes. 149
I suggested earlier that because kokanee exhibit smaller, mouth dimensions than trout of similar length, they might experience a greater degree of difficulty than trout in manipu• lating and ingesting large, armoured prey. This hypothesis is firmly supported by the results presented here (Table 24 ).
Kokanee and trout exhibit similar levels of capture success in encounters with large prey, however kokanee experience substantially greater difficulty than trout in manipulating and ingesting many of these prey. This difficulty is not due to any simple relation between prey size and predator mouth size. For example kokanee experience relatively low ingestion success on
Crangonyx sp. (46%) as compared with the mayfly Centroptilum sp. (100%) even though the latter are 42% larger than Crangonyx
sp. This difference is most likely associated with the amount of
"armour" possessed by the prey. Crangonyx sp. possess a tough,
chitinous exoskeleton which must offer considerable resistance to
compression during ingestion. Centroptilum sp. by contrast is
relatively soft-bodied and flexible.
It is apparent from feeding trials conducted with
damselflies and especially with notonectids (Nk undulata
and confusa) that prey armour is less of a deterrent to
successful attacks by trout. In the notonectid trials, I
purposefully selected particularly well armoured, large prey which
I thought would be unmanageable for both trout and kokanee. This
goal was completely realized with kokanee (0% IS) but less so with
trout (6% IS). This is all the more remarkable since the trout 150 used in these trials were appreciably smaller than the kokanee used (12.1 cm versus 16.4 cm) and had jaw widths that were virtually identical to those of the larger kokanee (Fig. 22).
Thus, smaller trout possessing equivalent jaw dimensions appear to have an advantage over kokanee in ingesting large, armoured invertebrates.
DISCUSSION
The relative vulnerability of a single prey type to different species of predators or of a variety of prey types to a single species of predator will often be determined by the
"match" or "mismatch" of predator and prey characteristics during the attack phase of the feeding cycle. Results from the present chapter may now be used to resolve the general question of whether differences in predator attack behaviours interacting with differences in predator morphologies are likely to account for specific patterns of food-resource partitioning exhibited by trout and kokanee from Marion Lake.
Explanations of Dietary Differences Between Trout and Kokanee
Both field and laboratory observations indicate that
some techniques of approach and capture of prey are specific to either trout or kokanee. This should lead to differences in dietary habits because specific approach and capture techniques give greater access to certain prey for one predator over
another. For example both trout and kokanee include large 151
numbers of the larval, pupal and adult stages of chironomids in their diets, but trout consume approximately twice as many chironomid adults as kokanee during the summer months (Chapter 2,
Table 3 ). This dietary difference is not obviously related to temporal segregation, spatial segregation (Chapter 3), or search behaviours (Chapter 4) of trout and kokanee, however evidence from the present chapter indicates it may be related to differences in their attack behaviours. I base this suggestion on the observation that trout frequently jump to catch a variety of aerial prey while kokanee apparently do not. This should allow trout to obtain greater quantities than kokanee of the adult forms of both aquatic and terrestrial insects which are much more abundant in flight a few cm above the lake surface than on it.
Differences in approach and capture techniques as well as quantitative differences in attack responses to small prey such as zooplankton in the laboratory form the basis for explana• tions of differences in the kinds and quantity of zooplankton obtained by trout and kokanee in the field.
Efford and Tsumura (1973) reported that cladocerans
(almost entirely Sida crystallina) were the dominant form of zooplankton found in the diet of moderate size trout (mean fork length 17.5 cm) from Marion Lake. By contrast they indicated that zooplankton in the diet of kokanee of comparable sizes
(mean fork length 14.0 cm) was composed of significant quantities of both cladocerans (primarily S^ crystallina) and copepods 152
(primarily Cyclops bicuspidatus). I have previously confirmed that this difference in the taxonomic composition of zooplankton is repeated in the diets of small trout (mean fork length 5.6 cm) and kokanee (mean fork length 7.9 cm) from Marion Lake (Chapter 2,
Table 5).
The dominance of cladocerans and the scarcity of copepods in the diet of trout relative to kokanee is likely based upon the interaction of several factors, however my data identify two specific reasons for why such a pattern should occur.
First results from experiment 5.1 indicate that a shift in approach and capture techniques (from "rush" to "stalk and dart") by kokanee allows them to attain greater capture success than trout in encounters with one species of copepod (EK kenai) which exhibits avoidance responses during attacks by predators.
Many species of copepods, including C_^ bicuspidatus, exhibit avoidance responses that are qualitatively similar to those performed by D.kenai, thus differences in approach and capture techniques may allow kokanee greater capture success and higher intake than trout of copepods in general.
The second explanation for the appearance of greater numbers of copepods (C^ bicuspidatus) in the diet of kokanee and the dominance of cladocerans (S^ crystallina
in the diet of trout is based upon the differences in the
interaction between the probability of attack and prey size for
trout and kokanee. I have demonstrated that trout of moderate
size (mean fork length 11.2 cm) exhibit weak attack responses to planktonic prey smaller than 1 mm in length but that size-matched 153
kokanee exhibit well developed attack responses to prey less than
1 nun long (Experiment 5.3). Since the maximum size of C. bicuspidatus in Marion Lake is less than 1.0 mm (Northcote &
Clarotto, 1975), it is no longer surprising that Cyclops is largely absent from the diet of moderate sized trout but relative• ly common in the diet of kokanee. By contrast the cladoceran
S. crystallina is commonly present in the lake at sizes to
1.8 mm and its dominance relative to other zooplankton in the diet of trout is undoubtedly due to the combination of large
size, local concentration on the underside of lily pads, and
the absence of any avoidance responses during encounters with vertebrate predators.
The evidence that trout exhibit a larger prey-size
threshold for an effective attack response than kokanee of
similar size may also explain why the zooplankton (largely
S. crystallina) that very small trout (mean fork length 5.6
cm) obtained on one occasion were largely from size-classes
composed of individuals greater than .6 mm in length while
a large proportion of the zooplankton (Sj^ crystallina, C.
bicuspidatus, Bosmina longirostris) obtained by small kokanee
(mean fork length 7.9 cm) on the same occasion were from size-
classes composed of individuals less than .5 mm in length
(Chapter 2, Fig. 7).
The foregoing discussion makes it clear that there
is no single explanation for why kokanee from Marion Lake
exploit greater quantities of zooplankton than trout do.
Indeed, this general trend is likely favoured by the small 154
sizes of most species of zooplankton present in the lake (Efford,
unpublished data), the higher levels of capture success that
kokanee may experience with copepods, and finally the greater
facility that kokanee have compared to trout in gathering large
numbers of small zooplankton within a specified time interval
(Experiments 5.2 and 5.3). Kokanee do not obtain more zooplankton
or smaller zooplankton than trout as a consequence of an ability
to filter these prey from the water column (Experiment 5.3).
Trout from Marion Lake include greater numbers of
large (>5 mm), armoured, prey types (caddis larvae, odonate
larvae, amphipods, planorbid snails) in their diet than kokanee
of comparable sizes do (Chapter 2). In previous chapters I
have pointed out how differences in both spatial segregation
(Chapter 3) and search behaviours (Chapter 4) of trout and
kokanee promote this pattern of food resource partitioning.
Results from this chapter indicate that interactions between
the predators and their prey during the attack phase of the
feeding cycle will promote this pattern as well. The larger mouth size and apparently more powerful jaw musculature of
trout relative to kokanee allow trout to achieve higher levels of manipulation and ingestion success with large, armoured
invertebrates (Experiment 5.4), thus, on average, kokanee will have to initiate many more attacks on such prey to achieve
the same levels of intake as trout. For prey such as large amphipods (Crangonyx sp.) or odonates (Enallagma sp.) the figure
is 2-3 times as many attacks while on prey such as notonectids or caddis larvae the figure will be even higher. Difficulties 155 during the manipulation and ingestion of large prey probably account for the virtual absence of the largest amphipods ( >
8 mm in length), molluscs (>5 mm in diameter), caddis larvae
(;>5mm in length) and larval odonates ( >6 mm in length) from the diet of Marion Lake kokanee (Chapter 2).
Differences Between the Proportions of Prey Observed in the Natural Environment and in the Diets of Trout and Kokanee
Ecologists concerned with describing the composition of the invertebrate community in Marion Lake have employed a variety of devices (Ekman dredge, Hargrave sampler, Kajak core, plankton pump, plankton net) to obtain samples. In
Chapter 2 I pointed out that trout and kokanee do not acquire prey from the natural environment in the same proportions as these other types of samplers do. Studies such as those reported here help to explain precisely why this is so. In general these man-made sampling devices were designed and employed to obtain invertebrates in proportion to their actual densities in the natureal environment, thus the samplers tend to "reject" or omit relatively'few species of aquatic invertebrates on the basis of differences in armour, size or escape behaviours.
By contrast trout and kokanee have been "designed" through natural selection to accommodate a relatively limited portion of the total range of potential invertebrate prey that reside in the lake and as this chapter shows may frequently fail to include items in their diets due to armour, size or escape behaviours. 156
Thus far I have examined in sequence the potential influence of spatial segregation, temporal segregation, search behaviours and attack procedures of trout and kokanee from
Marion Lake on the composition of their diets. This exercise has provided explanations of how specific mechanisms may operate to predispose the predators to accumulate species-specific diets. This does not mean that all of the interesting patterns of prey exploitation have been successfully linked to the mechanisms that produce them nor have I examined all of the major mechanisms involved in shaping dietary habits. For example, experience in dealing with various prey types is likely to have a profound influence on the responses of both trout and kokanee during all stages of the food gathering process.
In the next chapter, I will examine the influence of short term experience on the responses of trout and kokanee to prey.
SUMMARY
1. Trout and kokanee sometimes use different approach and capture techniques on the same types of prey and individually they use different approach and capture techniques with varying degrees of success on different types of prey (Tables 17 and 18).
2. Kokanee with well developed gill-rakers do not obtain more zooplankton or smaller zooplankton than trout as a consequence of any ability to filter such small prey from the water column
(Experiment 5.3).
3. Kokanee consistently exhibit either higher attack rates or greater attack success than trout in encounters with small 157
(<3 mm) zooplankton (Experiments 5.2 and 5.3).
4. Trout are either incapable of efficiently locating very small (<1 mm) zooplankton or they choose to ignore them (Experiment
5.3)/ while kokanee are quite adept at exploiting these small prey.
5. Experiments with trout and kokanee "preconditioned" to
feed on zooplankton suggest that advantages of kokanee over trout
in obtaining zooplankton are likely due to genetically fixed
morphological and behavioural characteristics (Experiment 5.3).
6. Kokanee exhibit jaw widths that are 30% smaller than
those possessed by trout of equivalent body size (Fig. 22).
7. Trout display a highly significant advantage over
kokanee in the ingestion of relatively large (>5 mm), armoured
prey (Experiment 5.4).
8. Experiments with both notonectids and odonates as prey
indicate that prey armour is less of a deterrent to successful
attacks by trout than by kokanee (Experiment 5.4).
9. Qualitative and quantitative differences in both
behavioural and morphological characteristics involved in the
attack phase of foraging by trout and kokanee serve as the basis
for explanations of a number of differences between the diets of
free ranging predators. These differences include: the greater
utilization of aerial prey by trout, the inclusion of large
numbers of copepods in the diet of kokanee but not of trout, the
generally greater utilization of zooplankton by kokanee compared
to trout, and the relative scarcity of large (>4 mm body length),
armoured prey in the diet of kokanee. 158
CHAPTER 6
THE ROLE OF SHORT TERM EXPERIENCE IN SHAPING THE RESPONSES OF TROUT AND KOKANEE TO PREY
INTRODUCTION
Predators are selectively attentive to stimuli that
are characteristic of different prey types. Selection of
information saves an animal from wasting time or energy on
stimuli which are unimportant and this will be adaptive no matter how limited the repertoire of response (Manning, 1972).
Directed attention in higher vertebrates is usually brought
about through the process of learning i.e., "a process that manifests itself by adaptive changes in individual behaviour as
a result of experience" (Thorpe, 1956) . A variety of studies
suggest that selective perception of responses resulting from
experience with various stimuli may influence patterns of prey
exploitation by predators. For example Bryan and Larkin (1972)
claim that experience has a long term effect (on the order of
weeks or months) on patterns of food specialization by trout.
Similarly experimental studies with birds suggest an important
role of learning in generating non-random patterns of prey
exploitation (Murton, 1971; Alcock, 1971; Kear, 1962; Rabinowitch,
1969) .
Experiments with three-spined sticklebacks (Gasterosteus
aculeatus) faced with different combinations of prey reveal that
experience with one prey simultaneously alters the risk of others 159
(Beukema, 1968). Sticklebacks faced with combinations of Tubifex sp. and Enchytraeus sp. as prey consistently rejected Tubifex sp. "on the expectation" of locating the more palatable
Enchytraeus sp., since at the moment of rejection of Tubifex sp., the fishes could not simultaneously perceive Enchytraeus sp. Therefore, predator experience with different prey types under natural conditions may commonly influence the prey's risk of exploitation.
Learning and habituation are involved in determining what an animal will or will not eat or avoid. Learning may indirectly affect the types of foods gathered through its influence on habitat selection, timing of activities, search techniques.
Learning may also directly affect the types of foods gathered by influencing the probability of attacks on prey that are discovered and by influencing the probability of rejection of prey after they have been captured. These direct effects of learning are the focus of the present chapter. I have already established that trout and kokanee from Marion Lake display considerable divergence in the ways that similar prey are located, approached, and manipulated (Chapters 3, 4 and 5). Because of these differences,
I am now interested in testing the general hypothesis that exposure to identical prey often constitutes a different experience for trout and kokanee and thus learned responses to prey as a consequence of this experience will serve as a powerful mechanism to produce predator specific patterns of prey exploitation in the field. 160
METHODS
Experiment 6.1 The Effects of Experience with Chaoborus spp. Larvae on the Predatory Responses of Trout and Kokanee
I designed this experiment to provide a number of pieces of information. First, I wished to determine how trout and kokanee would respond to repeated exposure to a prey type with which on first encounter they have high (>_ 80%) but far from total attack success (Chapter 5). I used two groups of predators (4 kokanee and 4 trout) captured fresh from the field.
All predators received identical treatment with respect to capture, handling and maintenance procedures. Seven days after capture from the field I conducted feeding trials with individual predators in 200 liter aquaria stocked with 400 late instar
Chaoborus spp. larvae. Additional trials took place every
72 hours until each predator had completed seven consecutive trials with chaoborus larvae as prey.
When wild caught predators are used in laboratory experiments, their responses will be affected not only by experience gained with particular prey types but also by the experience gained from exposure to an experimental procedure, which in this study included handling and transfer from a "home" aquarium to an experimental arena. I wished to observe the effects of experience with prey on predators rather than the effects of experience with other aspects of the experimental procedure. To minimize the latter, I took great care to standardize all aspects of predator handling and maintenance during this experiment. For example, the dip net, used to capture 161
fish for transfer, fit the home aquarium in a way that I could
always obtain individual predators without resorting to forced
pursuit. After gentle netting, individual predators were always
transferred from the home aquarium to the experimental arena in
a red plastic bucket. In order to assess the success of these measures I compared the responses on the first trial with
chaoborus larvae, of newly captured kokanee, to the responses
of experienced kokanee. The four animals in the experienced
group had previously participated in at least five feeding trials with small amphipods (Hyalella azteca) as prey.
As predators accumulate experience with particular prey,
they may exhibit changes in: capture success, frequency of prey
rejection, total attacks initiated, reactive distance or the time
taken to initiate the first attack in a given trial. Thus a variety of potential indices exist to document the influence of
experience with prey on predator responses. I relied on the
present experiment to provide information to assess the relative
sensitivity of these indices and their potential for application
in further experiments.
Experiment 6.2 The Effects of Experience on Responses of
Kokanee to a Variety of Benthic Prey Types
This experiment was designed to examine the effects of
changes in both prey density and predator experience on the
responses of kokanee to a variety of benthic invertebrates. I
carried out individual feeding trials with thirteen kokanee and
four species of benthic prey (Hyalella sp., Centroptilum sp.,
Crangonyx sp., and Enallagma sp.). The sizes of predators 162 and prey used in this experiment are recorded elsewhere (see
Table 19, Chapter 5). All predators used had completed at least
two identical pre-conditioning trials with mixed prey in the experimental arena and thus were quite familiar with the experimental procedures. Each predator received at least four consecutive feeding trials with specific prey types since results of experiment 6.1 suggested that the effects of experience on various predator responses were always apparent by this point. 2
I used prey densities of 20, 40, 70 and 100 per .42 m respectively in consecutive trials. In this way I could examine predator responses to changes in prey density from trial to trial and predators were presented with an equal opportunity to
accumulate equivalent levels of experience with the various prey types by the end of trial four. Thus, by pooling results
across all four trials, I was able to examine the response of kokanee to experience with prey, minus the influence of changes
in prey density between trials. I recorded number of prey eaten,
total attacks initiated and time to initiate the first attack
in a given trial as standard indices of predator responses to
experience with prey. Because time to first attack in a given
trial is likely to be affected by prey size and levels of
activity, I collected information on these characteristics of
prey types used in trials with kokanee. Experiment 6.3 The Habituation Hypothesis: Effects of Experience with Large, Armoured Prey on Trout and Kokanee.
Young or adult vertebrates which forage on their own must deal with many different food situations, therefore their responsiveness to prey must be broad. Inevitably this broad responsiveness will result in encounters with prey items that are unfit to eat. Repeated exposure of predators to such prey is commonly predicted to result in habituation, that is, a decrement in responsiveness to a repeated or constant stimulus (Thorpe,
1956). In previous feeding trials involving a variety of prey
(Chapter 5), trout and kokanee experienced the lowest levels of ingestion success (6% and 0% respectively) with large, armoured notonectids. I designed the present experiment to test the hypothesis that low levels of attack success will reduce the responsiveness of trout and kokanee to prey.
I conducted individual feeding trials with four trout and four kokanee (see Table 19 for sizes). Each predator used in this experiment had completed at least three pre-conditioning trials with chaoborus larvae as prey in the experimental arena, thus all predators were fully experienced with the standard laboratory procedures. At the beginning of each trial, 40 large notonectids (mean length 10.5 mm) were placed in the experimental arena. Each predator received four consecutive trials (each lasting .5 hours) of experience with notonectids in the arena.
Because these prey were seldom eaten and the fish did not receive a supplementary food supply at any time during the experiment, I conducted trials with individual predators every 24 hours for four days. This ensured that responses by the predators to the 164 prey would be a consequence of accumulated experience rather than a consequence of any long term effects of starvation. I recorded number of prey eaten, total attacks initiated and time to initiate the first attack in a given trial as standard indices of predator response to experience with notonectids.
Experiment 6.4 The Success and Strength of Response Hypothesis: Effects of Experience with Small Agile Prey on Trout and Kokanee
I have demonstrated previously that kokanee are more effective predators than trout in initial contacts with a variety of small planktonic prey (Chapter 5). Therefore, repeated exposure to such prey will constitute a different experience for trout as compared to kokanee. This experiment is designed to test the hypothesis that when such differences in success with small prey exist, kokanee will develop a stronger response than trout, upon repeated exposure to these prey.
I used Diaptomus kenai as the prey in this experiment because they are large enough (mean length in this experiment was
2 mm) to allow easy observation of predator success and because trout and kokanee experience different levels of capture success with these prey upon initial contact. In a single trial with these prey, trout achieved only 8% capture success while kokanee attained
18% capture success. The lack of total success by predators in these trials was clearly related to the pronounced avoidance response of p_. kenai when attacked by fish.
Eight size-matched trout and kokanee (mean lengths 8.9 and 8.4 cm respectively) served as predators. Up until the time 165 of the experiment all predators had received identical treatment with respect to capture from the field and subsequent handling and maintenance procedures in the laboratory. The initial density of p_. kenai in each trial was set at 100 per 200 liters. I conducted half hour trials with individual predators every 24 hours for four days. I recorded the number of prey eaten, total attacks, total rejections, and time to initiate the first attack in a given trial as the standard indices of predator response to experience with D_. kenai.
RESULTS
Experiment 6.1 Experience with Chaoborus Larvae
Trout and kokanee both attain high capture and ingestion success in initial trials with chaoborus larvae and there is no evidence for any significant improvement in their ability to capture or handle these prey as a consequence of repeated exposure to them (Table 25 a and b). This does not mean that "experience" has no effect on the predator's response levels since there is clearly an increase in the total number of attacks that trout and kokanee make from one trial to the next (Fig. 25). This trend may be a consequence of either an increased willingness to make attacks or a consequence of an increased ability to process chaoborus larvae. Both are possible.
Animals such as laboratory rats commonly exhibit an increased intake of novel foods as experience with these increases
(Rozin, 1969) . The gradually increased intake is presumably a 166
TABLE 25. The effect of experience with prey in successive feeding trials on attack success of trout and kokanee. Numbers in brackets indicate the total number of attacks for a particular trial. Attack success is the proportion of prey eaten to the number attacked. a. Trout Attack Success (as %) Mean Trial Trial Trial Trial Trials Prey Identity Size 1 2 3 4 > 4 mm Zooplankton Daphnia sp. 1.5 100 100 100 100 100 ( 404) ( 337) (668) (361) ( 558) Diaptomus kenai 2.0 8 12 18 8 - ( 231) ( 155) ( 97) ( 12) - Chaoborus spp. 10 .0 86 92 97 95 92 ( 85) ( 212) (305) (261) (1,071) Amphipods Hyalella azteca 4.6 91 - - - - ( 300) - - - - Crangonyx 8.3 91 - - - - richmondensis ( 120) — — — — Others Odonata 15.6 75 - - - - (Enallagma boreale) ( 100) — — — —
Notonectids 10 .5 4 8 2 7 — ( 79) ( 75) ( 42) ( 57) - b. Kokanee Attack Success (as %) Zooplankton Daphnia sp. 1.5 100 100 100 100 - ( 225) 859) (811) (574) - Diaptomus kenai 2.0 18 24 36 39 - (1,224) 1,262) (980) (805) - Chaoborus spp. 10.0 86 85 89 87 86 ( 308) 366) (449) (449) ( 867)
Amphipods Hyalella azteca 4.6 89 98 92 95 — ( 83) 133) (225) (378) - Crangonyx 8.3 63 16 60 43 78 richmondensis ( 49) 49) ( 20) ( 28) ( 27)
Others Odonata 15.6 49 26 31 43 38 (Enallagma boreale) ( 35) 84) (121) ( 75) ( 47) Notonectids 10.5 0 0 0 0 — ( 56) 8) ( 8) ( 2) — Ephemeroptera 11.8 75 60 56 61 54 (Centroptilum sp.) ( 59) 141) (197) (203) ( 71) 167
FIGURE 25. The relationship between consecutive feeding trials
with chaoborus larvae as prey and the total number
of attacks that trout and kokanee initiate in a
given trial. Trout used were 8.7 cm in mean length.
Kokanee used were 16.4 cm in mean length. H TROUT Y= 18.21 + 9.64x O KOKANEE Y= 82.98+ 15.25 x o
CONSECUTIVE FEEDING TRIALS WITH CHAOBORUS LARVAE 168
consequence of a "testing" procedure which allows the animals to run minimal risk of obtaining a lethal dose of a novel food that is toxic. It is most likely that the trend to increase attacks on consecutive trials with chaoborus larvae is related to parallel changes in some aspect of digestive tract anatomy or physiology.
I base this conclusion upon the observations that the predators had been starved for seven days prior to the initial trial with chaoborus and that the small trout (mean length 8.7 cm) used in the experiment exhibited fewer attacks which increased more slowly from trial to trial than was the case with the larger kokanee
(mean length 16.4 cm). The idea that the increase in total attacks from trial to trial is due to a gradual process of accomodating predator stomachs to larger volumes of food after a period of "starvation" is consistent with both of these observations.
The progressive decline in the time taken to initiate the first attack (TFA) on prey in the arena (Fig. .26) indicates that both trout and kokanee respond positively to the combination of a highly acceptable prey and standard laboratory procedures.
A comparison of values of TFA between laboratory experienced kokanee and inexperienced kokanee and trout (Table 26) indicates that most of the variability in TFA on the first trial is due to the response of the predators to the experimental procedure rather than due to responses to the prey. The similar values obtained for TFA of experienced predators on trial one (Group II kokanee,
Table 26) and of relatively inexperienced predators on trial two 169
FIGURE 26. The relationship between consecutive feeding trials
with chaoborus larvae as prey and the time to
initiate the first attack by trout or kokanee in a
given trial. Note the changing scale on the
ordinate. Curves fitted by eye.
170
(Fig. 26) suggests that the effects of the standard experimental procedure largely disappear by trial two with predators. Thus, changes in TFA after trial two are most likely a consequence of experience with prey alone.
TABLE 26. A comparison of the time to first attack (TFA) and of total attacks by predators on chaoborus larvae. Group I. predators were not familiar with the experimental procedure while Group II predators were.
Group I Kokanee Group I Trout Group II Kokanee
TFA (sec) Attacks. TFA (sec) Attacks TFA (sec) Attacks
416 96 290 36 26 ;89
223 102 720 36 9 141
*1800 9 800 44 20 94
686 95 660 35 65 103
X 781 76 617 338 30 107
S.D. 705 44 226 44 24 24
this is a minimum value since trials lasted only .5 hours.
The decrease in TFA from trial two through trial five indicates that chaoborus larvae are a highly acceptable prey to both trout and kokanee. Further, it appears that changes in TFA may serve as an especially sensitive indicator of the effects of experience with prey on predator response levels. 171
Experiment 6.2 Responses of Kokanee to Experience with a Variety of Benthic Prey Types.
Attack Success
In general kokanee do not gain an improved ability to capture or handle benthic prey types in consecutive trials
(Table 25b). Although mean ingestion success across all trials is more variable for kokanee exposed to Crangonyx sp. and
Enallagma sp. than for those exposed to Hyalella sp. and
Centroptilum sp. (Table 25b), attack success does not appear to be a particularly sensitive index of the effects of experience on predator responses to prey.
Total Attacks 2
At an initial density of 20 prey per .42 m all kokanee completed similar numbers of attacks on the four types of benthic prey. In subsequent trials, as prey density increases, there is a clearly defined increase in total attacks by kokanee on Hyalella sp. and Centroptilum sp. (Fig. 27 a and b), but a highly variable response to Crangonyx sp. and Enallagma sp. (Fig. 27 c and d). These rather different results could all be a consequence of responses to prey density, if the abilities of kokanee to process large Crangonyx sp. and Enallagma sp. are fully saturated at the lowest prey density, while those of kokanee, in trials with Hyalella sp. and Centroptilum sp., are not saturated even at the highest prey density. Various pieces of evidence suggest that this is not the case. First,
Kokanee generally were not consuming a maximum ration of either 172
FIGURE 27. The effects of changes in experience and prey
density on the total number of attacks that
kokanee initiate on particular prey types in a
given trial.
Crangonyx sp. or Enallagma sp. in these trials. The kokanee used in the Centroptilum sp. trials were smaller (mean length
12.7 cm) than those used in trials with Crarrgonyx sp. (mean length 14.7 cm) and therefore their total intake of prey (by volume) should have been less than for kokanee feeding on Crangonyx sp.
In sharp contrast to this expectation, many more large Centroptilum sp. (mean length 11.8 mm) than the relatively smaller Crangonyx sp.
(mean length 8.3 mm) were consumed by kokanee. Given the average ingestion success of kokanee with Crangonyx sp. and information on the number of Crangonyx sp. equivalents (as wet weight intake) consumed by the predators in two pre-conditioning trials with mixed prey I have calculated that kokanee in the Crangonyx sp. trials would have to have initiated 116 attacks to reach saturation (i.e. to fill their guts). It was also apparent that the time taken by kokanee to handle individual Crangonyx sp. and Enallagma sp. did not preclude their making additional attacks during the .5 hour period of single trials. The longest handling times on these prey were seldom greater than 15 seconds and were usually on the order of 2 - 4 seconds. In addition, kokanee in trials with Crangonyx sp. and Enallagma sp. spent a great deal of time engaged in seemingly "aimless" swimming about the aquarium. In some trials individual kokanee failed to exhibit any response to either Crangonyx sp. or Enallagma sp.
This was not due to any general lack of responsiveness to stimuli because at the end of trials in which there had been no response, the introduction of a few mosquito or chaoborus larvae was always 174 followed by immediate attack and ingestion. Therefore, it seems that kokanee are more strongly predisposed to attack some prey
(Hyalella sp. and Centroptilum sp.) than others (Crangonyx sp. and Enallagma sp.) and that possibly predator experience with some prey has a greater influence over response levels than changes in prey density do.
The Relation Between Total Attacks and Attack Success
I have argued above that the upper limit on total attacks made on prey by predators in these trials is not a consequence of saturation of either the predators abilities to handle prey in the amount of time available or of their gut capacities. The relevant question then is what does control the total number of attacks that these predators make on specific prey types? Results from a later experiment (see Experiment 6.3) suggest that when kokanee are repeatedly exposed to prey with which they have little capture or ingestion success they make very few attacks, thus, I suggest that the levels of attack success experienced by predators with prey may influence the total number of attacks that they are willing to make. To determine whether or not this is the case I have pooled the total attacks initiated by individual predators on single prey types
in four consecutive trials and plotted this value against % attack success experienced by individual predators over the same
four trials. Results from this analysis (Fig. 28) reveal that there is an unmistakable relationship between the level of attack success experienced by individual predators and the total attacks 175
FIGURE 28. The relationship between the level of attack success
that individual kokanee have with specific prey types
and the total number of attacks that individual kokanee
initiate on these prey types over four consecutive
trials. 1. Centroptilum sp. 2. Enallagma boreale,
3. Crangonyx richmondensis, 4. Hyalella azteca,
5. Notonecta undulata or Buenoa confusa. Note
that I have included results from trials with notonectids
(Experiment 6.3) because the response by kokanee to
these prey is basically independent of prey density. ARCSIN OF % INGESTION SUCCESS 176
that they make on specific prey types. My interpretation of
these results relies on the assumption that the predators do make
"choices" about whether or not to attack individual prey. A
particularly strong piece of evidence that this is the case
consists of the trends in time to first attack (TFA) by kokanee
on prey in consecutive feeding trials.
, Time to First Attack (TFA)
There is a progressive decline in TFA of kokanee exposed
to increasing densities of Hyalella sp. and Centroptilum sp.
on consecutive trials (Fig. 29 a and b). This supports the idea
that Hyalella sp. and Centroptilum sp. are highly acceptable
as prey by kokanee. There is no well developed decline in TFA
for kokanee exploiting either Crangonyx sp. or Engallagma sp.
(Fig. 29 c and d). TFA will be influenced by factors that affect
the probability of prey detection by predators. Initially the
absolute value of TFA is determined by prey characteristics such
as size, activity, colour and contrast. TFA will then be
further influenced by prey density, familiarity of the predators
with the experimental procedure and familiarity of the predators
with the prey. On trial one of this experiment all factors
except prey characteristics were held constant. By examining
specific prey characteristics it is possible to predict the
expected order of TFA from lowest to highest for the four prey
types. 177
FIGURE 29. The effects of changes in experience and prey density
on the time that individual kokanee take to initiate
their first attack on specific prey types in a given
trial. Note the scale differences between the
ordinates of a & b and c & d respectively. Curves
fitted by eye.
178
Prey used in this experiment were all of similar colour and low contrast, thus, these characteristics will contribute
little to the observed variability in TFA values. Because prey detectability increases linearly with an increase in prey size, kokanee should respond to Enallagma sp., Centroptilum sp.,
Crangonyx sp., and Hyalella sp. in order of increasing TFA.
Prey detectability is also enhanced by the proportion of time that prey spend moving and on this basis alone kokanee should respond
to Crangonyx sp., Hyalella sp., Centroptilum sp., and
Enallagma sp. in order of increasing TFA. To predict the order of TFA as a consequence of the combined effects of prey size and movement, I will assume that movement and size are equally important
in determining TFA and that their effects are additive (note that although a more sophisticated analysis is possible (see Ware, 1973),
its use would not alter the order of TFA on prey predicted here).
I have arbitrarily assigned the largest and the most active prey a value of 100. Next, I have awarded the remaining prey points
for size and movement relative to the largest and most active prey respectively. Finally, by adding the two values together I have produced an index which indicates the order of the four prey types according to increasing values of TFA (Table 27). 17?
TABLE 27. Characteristics of prey used to predict the expected order of TFA proceeding from smallest to largest. See text for explanation of points awarded.
Mean Proportion Total size Points of time Points points Prey Identity . mm awarded spent moving awarded awarded
Enallagma sp. 15.6 100 .01* 1 101
Centroptilum sp. 11.8 76 .05* 7 83
Crangonyx. sp. 8.3 53 .74** 100 153
Hyalella sp. 4.6 29 .26** 35 64
* values obtained in this study, prey observed at 10 C ** values obtained from extensive studies by Ware, 1971; prey observed at 10°C.
On the basis of total points accumulated, the predicted order of TFA, as a consequence of the interaction between prey size and movement, is Crangonyx sp., Enallagma sp., Centroptilum sp., and Hyalella sp. This is almost exactly the reverse of the order observed i.e., Centroptilum sp., Hyalella sp.,
Enallagma sp., and Crangonyx sp. respectively. Thus, TFA does not appear to be consistently influenced by factors related
to the detectability of prey.
By conducting a more elaborate analysis, Ware (1973)
indicated that individual Crangonyx sp. are seven times more vulnerable to attack by trout than Hyalella sp. because Crangonyx
sp. are larger and spend more time moving when exposed. Thus, he 180
successfully predicted that trout recognize Crangonyx sp. more easily, attack them from further away and attack them more often that they do Hyalella sp. For the same reasons
Crangonyx sp. should elicit a shorter TFA from kokanee than
Hyalella sp. do. Instead kokanee exhibit an average TFA to
Crangonyx sp. (673 sec) that is 84 times longer than their i
average TFA (8 sec) to Hyalella sp. on trial one. This
difference is maintained across all four trials. The inescapable
conclusion is that kokanee do not respond to Hyalella sp.
relative to Crangonyx sp. in the same way that trout do. The
results presented here not only indicate that kokanee are pre•
disposed to attack small Hyalella sp. and poorly armoured
Centroptilum sp. rather than large, well armoured Crangonyx sp.
and Enallagma sp., but that the effects of experience with
these prey intensify rather than reduce this tendency.
TFA and Attack Success
TFA does not appear to be consistently influenced by
factors related to prey detectability (e.g. prey density, prey
size, movement). Instead, it seems that predator experience with
some prey affects the "willingness" of the animals to initiate
attacks. The level of attack success experienced by the predators
in trials with various prey types may be particularly important.
It is not appropriate to compare predator TFA values and
attack success across all prey types tested on both trout and
kokanee because of the great differences in prey density and
characteristics of prey used in the various experiments (Table 28). TABLE 28. Characteristics of the prey species used and the number of predators involved in trials from which TFA values have been derived.
Mean Prey density in Number of predators size Other consecutive trials used Prey Identity mm characteristics T-l T-2 T-3 T-4 Trout Kokanee
Chaoborus spp."*" 10.0 stationary, transparent. 400 400 400 400 4 4 2 Hyalella sp. 4.6 active, low contrast. 20 40 70 100 0 4
Centroptilum sp. 11.8 stationary, medium 20 40 70 100 0 3 contrast. 2 8.3 active, low contrast. Crangonyx sp. 20 40 - 70 100 0 3 2 15.6 stationary, medium Enallagma sp. 20 40 70 100 0 3 contrast.
Notonectids spp. 10 .5 active, high contrast. 40 40 40 40 4 4 4 2.0 active, high contrast. Diaptomus kenai 100 100 100 100 4 4
1 Experiment 6.1 2 Experiment 6.2 3 Experiment 6.3 4 Experiment 6.4 182
However, it is worthwhile to examine how variable predator responses are to prey with which they have a given level of success. The standard deviation of TFA is used here as an index of this variability.- Because much of the variability in initial trials with prey is produced by the predator's lack of familiarity with the experimental procedure (Experiment 6.1), I have considered as replicates only responses recorded in the final three trials predators completed with any prey type.
The results from this analysis (Fig. 30) indicate that as long as trout and kokanee experience an attack success of 30% or better with prey, they will respond in a highly consistent fashion from trial to trial. However, if attack success falls much below 30% the predators display tremendous variability in their willingness to make attacks upon introduction to the experimental arena.
Experiment 6.3 The Habituation Hypothesis: Responses to Notonectids
Attack Success
In four consecutive trials with notonectids, small trout and kokanee fail to exhibit any improvement in their ability to successfully handle and ingest notonectids (Table 25).
Trout exhibit higher as well as more variable success with these prey than kokanee do, although even trout are only marginally successful at using these prey as a food source. Observations indicate that the low level of success is primarily a consequence of difficulties in manipulating these large, well-armoured, prey' 183
FIGURE 30. The relationship between % attack success of
individual trout and kokanee and their variability of
response as indicated by the standard deviation of
the time to first attack over the last three trials
of experience with specific prey types. Data derived
from trials with seven different prey types (see
Table 28). Curve fitted by eye. 183a
CO o IOOOH
UJ cr 900 H
< Q > 800-
O 700 H
O
600 A co or o 500H UJ y- 40oH Ll_ O
LZ 300- < > UJ Q 200 H
< o
loo H CO
T r~ T T" T I T T T 10 30 50 70 90 % ATTACK SUCCESS OF INDIVIDUAL PREDATORS 184
by relatively small predators. Casual observations on larger trout (21.6 cm) in the laboratory indicate that they experience no difficulty in ingesting notonectids in the size range used in this experiment.
Total Attacks
Trout exhibit higher levels of response to notonectids on trial one than kokanee do (Fig. 31). Therefore, they either have a greater predisposition to attack this prey type than kokanee do or within the short span of one trial there is a differential effect of experience with notonectids on the tendency of trout and kokanee to initiate attacks. Consideration of the responses of the predators over all four trials indicates that as
the amount of experience with notonectids increases the respon•
siveness of kokanee to these "prey" decreases. Thus, kokanee maintain the ability to recognize this prey over the 24 hour
interval between trials and are capable of reducing responses to
a very low level, given such unrewarding prey. This supports the
hypothesis that the process of habituation will operate to reduce
the probability of kokanee exploiting prey which are difficult to
handle and ingest.
The response of trout over the four trials is quite
unlike that of kokanee. In spite of an attack success that never
exceeds 8% and which may be as low as 2%, trout continue to respond
to notonectids at much higher levels than kokanee do. The failure
of trout to habituate to notonectids is surprising, especially
since Benfield (1972) has reported that rainbow trout quickly 185
FIGURE 31. The relationship between consecutive trials of
exposure to a constant density of notonectids and
the total number of attacks that trout and kokanee
initiate in a given .5 hour trial. N = number of
individual predators tested in consecutive trials.
Vertical bars indicate + one standard error of the
means. DU-1
CONSECUTIVE TRIALS WITH NOTONECTIDS 186
habituate to prey (Gyrinids, Dineutes discolor) that are
unpalatable due to defensive chemical secretions.
. Time to First Attack (TFA)
Although trout and kokanee vary dramatically in their
tendencies to attack large armoured prey like notonectids during
repeated exposure to them, there are some similarities in their
responses. Both trout and kokanee fail to exhibit any significant
reduction in TFA on notonectids over four consecutive trials (Fig.
32). This suggests that at the beginning of each trial both
predators are equally reluctant to attack notonectids. Certainly
the long TFA recorded for individuals on consecutive trials is
not a consequence of detection difficulties since prey such as
Hyalella sp. which are less than half the size of notonectids
and of lower contrast (Table 28) were always attacked in much
shorter times (Fig. 29 a).
Experiment 6.4 Responses to Diaptomus kenai: The Effects of Differential Success with Small, Agile Prey.
Attack Success
Kokanee are approximately twice as successful as trout
in capturing D_. kenai. In sharp contrast to the situation
observed for the majority of prey types tested, trout and kokanee
do display a consistent improvement through trial three in their
abilities to capture jD. kenai. Both predators more than double
their capture success by trial three (Table 25). In the case of
trout, this was accomplished through refinement of a basic pattern 187
FIGURE 32. The relationship between consecutive trials of
exposure to notonectids and the time to first attack
of individual predators in a given trial. The solid
line joins the means. Note the changing scale along
the ordinate.
188
of approach and attack while for kokanee the increased success relied on a complete change in the basic pattern of approach and attack between trial one and trial three. During trials with
D. kenai trout exhibited the same behaviour as they had in trials with Daphnia sp., that is, they scull in midwater, sight a prey, stop, and then lunge to make a capture after which they often stop abruptly "to search for and line up on" the next prey item (see Chapter 5). Although refinement of these tactics results in significant improvement in the ability of trout to capture D. kenai, the vast majority of JJ. kenai are still successful in evading capture. This is because JJ. kenai respond to the onrushing predator by darting rapidly to the side, thus successfully evading capture.
In previous experiments (Chapter 5) with other zoo• plankton (Daphnia sp., Diaptomus tyrelli etc ...), kokanee pursued prey by swimming in a smooth path that flowed from one capture to the next with little interruption and with very precise changes of allignment from capture to capture. With repeated exposure to JJ. kenai these tactics change drastically. After sighting a prey, a cruising kokanee typically decelerates and approaches slowly either by gliding or with the aid of gentle sculling by pectoral fins. When within 3 - 5 cm of JJ. kenai, kokanee stop, flex into a sigmoid posture, and then rapidly release to thrust forward and make the capture. This set of tactics is also far from completely successful but does allow kokanee to attain a level of success that is greater than double the maximum exhibited by trout (Table 25). 189
Total Attacks
Kokanee exhibit higher levels of response than trout to
D_. kenai on trial one (Fig. 33). Therefore, they either possess a greater predisposition to attack this prey type than trout or within the short span of a single trial there is a differential effect of experience with D_. kenai on the tendency of trout and kokanee to initiate attacks. Given the magnitude of the difference
(i.e. an average of 60 attacks versus more than 300 attacks by kokanee) the former seems more likely.
Over the course of four consecutive trials both trout and kokanee exhibit a tendency to reduce the total number of attacks initiated on D. kenai. However, I wish to stress that even on the last trial kokanee are highly responsive to kenai
(more than 200 attacks) while trout exhibit almost complete habituation and make few responses at all. Even on occasions when trout attack and successfully capture D_. kenai there is evidence that their response to the prey is different from that of kokanee. Out of a total of 55 D. kenai successfully captured, trout rejected 41. Kokanee never rejected any of the 1188 D. kenai that they managed to capture. The response of trout is particularly
surprising given that JJ. kenai were the only potential source of
food over the four day duration of the experiment. The results
from this experiment lend solid support to the hypothesis that an
initial difference in capture success of trout and kokanee
exploiting small, agile prey is accompanied by the development of
a more intense positive response by kokanee upon repeated exposure
to the prey. 190
FIGURE 33. The relationship between consecutive trials of
exposure to a constant density of Diaptomus kenai
and the total number of attacks that trout and kokanee
initiate in a given trial. N = number of trout or
kokanee tested on consecutive trials. Vertical bars
indicate + one standard error of the means. KOKANEE
1 I —I I 2 3 4 CONSECUTIVE TRIALS WITH D. KENAI AS PREY 191
Time to First Attack
Results from TFA for predators exposed to JJ. kenai generally reflect the patterns of response already indicated by total attacks. Kokanee exhibit a well defined decline in TFA over the four trials, a response which confirms the relative accept• ability of jp_. kenai as prey for kokanee. TFA of trout exhibits an initial decline (compare trials one and two of Fig. 34), followed by a dramatic increase, which suggests that as trout become more experienced with D. kenai, they become less willing to attack this prey.
DISCUSSION
The Range of Responses by Trout and Kokanee to Prey
There are numerous examples in the literature of papers dealing with questions concerning the relative accept• ability of prey to predators (see Edmunds, 1974 for references).
Most of these have concentrated on the effects of a single stimulus dimension (e.g. taste, colour, size) even though it is certain that many stimulus dimensions are "integrated and summated" by predators in the course of their inspections of prey items (Eisenberg & Leyhausen, 1972). The stimulus dimensions that represent a given prey are not of uniform significance to predators. Potential stimuli associated with each prey may elicit a range of response that varies from very positive to highly negative. It is the predator's assessment of the significance of the total stimulus set which will determine its ultimate response to a particular prey type. 192
FIGURE 34. The relationship between consecutive trials of
exposure to Diaptomus kenai and the time to
first attack of trout and kokanee in a given trial.
The solid line joins the means. Note the changing
scale along the ordinate.
193
In many cases the final assessment of prey by predators proceeds without difficulty. For example, many caged and wild predators learn after only a few trials to avoid attacking unpalatable insects or to pursue palatable ones. When this is the case, it is often possible to associate the predators response with particularly strong stimuli such as noxious chemical secretions and, secondarily, bright colours in the former or large size and "provocative" movements in the latter. On the basis of data on total attacks or time to initiate first attacks, kokanee develop reliable responses which indicate that prey such as
Chaoborus spp., Hyalella sp., Centroptilum sp., and D. kenai are easily discriminated as acceptable, while prey such as notonectids are just as readily identified as unacceptable. Strong, positive responses by trout suggest that they readily identify
Chaoborus spp., Crangonyx sp., and Hyalella sp. as acceptable prey.
A second situation encountered by predators is that in which the information content of the stimuli presented by prey is clear and results in the predators consistently making mistakes. The best known examples of this are cases in which palatable insects mimic the appearance and behaviour of highly unpalatable ones (Rettenmeyer, 1970; Brower, 1969) and thus escape high levels of predation because predators fail to differentiate mimics from their models (Sexton, 1960; Duncan &
Shepherd, 1965). Although seldom studied, it is just as likely that unacceptable prey items continue to elicit predator responses because these prey present stimuli that are similar to those 194
possessed by familiar and highly acceptable prey. For example, some birds learn to reject unpalatable prey that are novel more readily than they learn to reject those resembling familiar palatable prey (Brower, 1958; Shettleworth, 1972) . The continued response of trout to notonectids in spite of very low ingestion success may fall into this class of response, that is, notonectids present trout with stimuli which include large size, high visual contrast, and provocative movements. Many of these stimuli will be reliable indicators of a wide range of prey that are highly acceptable to trout, thus their continued response to notonectids may represent an unavoidable cost of maintaining a high state of
receptivity to stimuli ordinarily associated with such acceptable prey.
A final and rather poorly explored situation is that
in which prey present predators with particularly difficult
problems of discrimination which arise as a consequence of prey
stimulus sets that contain conflicting information content for
predators. It is difficult to know exactly how to study this
problem (see Sutherland, 1964), but information from the present
study as well as others suggests that it may be a fairly common
phenomenon. For example, the responses of kokanee to Crangonyx
sp. and Enallagma sp. are ambiguous at best. Similarly some
aspects of trout responses to notonectids are ambiguous. Their
TFA values suggest a continued reluctance to attack notonectids
upon repeated encounters, however, they inevitably do respond
with a large number of attacks on these prey within single half
hour trials. 195
Trout responses to D_. kenai are also ambiguous.
Initially, TFA values decline suggesting an increase in readiness to attack these prey, but then in later trials TFA values increase dramatically suggesting just the opposite. Upon initial exposure
to JJ. kenai, trout make numerous attacks and many successful captures; however these are not carried through to ingestion and many of the prey are rejected. These predator responses are not easily associated with strong stimuli from any of the prey, rather, given an appropriate predator-prey combination, these same prey evoke highly consistent responses. According to Ware (1971),
trout respond in a consistently positive fashion to Crangonyx sp.
and in the present study, kokanee registered unambiguous positive
and negative responses to D. kenai and notonectids respectively.
Stimuli that trigger and sustain attacks to completion
by other predators are by no means obvious. Schaller (1972)
reported that he was unable to discover the factors which triggered
sustained attacks on giraffes or buffalo by lions. Kruuk (1972)
reported that he could not detect any differences in animals of
one species that were attacked compared to those that were not
attacked by hyenas. Mech (1970) and Haber (pers. comm.) have
experienced similar difficulties in determining the critical
stimuli which lead wolves, holding prey such as moose at bay,
to abruptly cease attacks.
Predators receive and interpret a continuous stream of
stimuli associated with prey from the moment of detection until
at least the moment of ingestion. Many morphological,
behavioural or chemical characteristics of prey are undoubtedly 196 retained, in an evolutionary sense, because they serve as stimuli
that uncouple or dis-integrate an effective approach and attack procedure by predators. For example, Neil and Cullen (1974) presented evidence to suggest that schools of prey act upon ambush predators such as pike (Esox lucius) by interfering with the complex sequence of attack by causing avoidance reactions together with irrelevant behaviours that were inappropriate to the goal of
catching prey. For pursuit predators such as perch (Perca
fluviatilis) the schools appeared to disrupt the attack sequence
by forcing the predators to continually switch targets during pursuit. By extension to the present study it is not too difficult
to believe that prey texture or a slightly awkward handling
procedure will deter kokanee from effectively exploiting large prey such as Crangonyx sp. nor is it unlikely that stimuli from
small, agile prey types disrupt the behavioural chain that trout
ordinarily depend upon to exploit larger benthic prey or
terrestrial insects. Certainly it is clear that there are
predator specific differences in the readiness with which similar
stimuli acquire control of behaviour under similar conditions.
This suggests that there may be predator specific predispositions
to learn certain things and not others.
Species Specific Effects of Experience with Prey
In considering the effects of experience on closely
related predators in the present study, two extreme positions
are possible. These are that animals may have a highly
generalized ability to learn or that animals possess specialized 197
abilities to learn only certain things. Experimental psychol• ogists have historically stressed the former view, but from an ecological perspective the latter view makes more sense, that is, animals should be predisposed to learn things that it is important for them to learn under natural conditions especially well, while they may not learn other comparable tasks at all if these have no place in their lives in nature (Seligman, 1970; Rozin & Kalat,
1971; Shettleworth, 1972).
The differential effects of experience on responses by trout and kokanee to the same prey were surprising to me, but perhaps should not have been. Ethologists have pointed out that behaviour may be as species characteristic as any feature of morphology or physiology. This must be true of abilities to learn. Trout and kokanee learn not to attack some small, agile prey (such as D_. kenai) and some large, armoured prey (such as notonectids) respectively. The effects of experience seem to operate by amplifying an existing, although weak, predisposition not to attack or ingest these prey. These predispositions may be either a consequence of genetically determined differences or of differences in experience accumulated by the predators under field conditions prior to their capture and performance in the present experiments. The failure of trout to habituate to notonectids as objects for attack may indicate that responses to such prey are innate. Various authors (Hinde, 1966; Figler,
1972) have indicated that innate behaviour is highly resistant to habituation. Smith (1973) found that the attack responses of young shrikes to models did not habituate, even in the absence 198
of any tangible reward and she concluded that their attack responses were innate. The experiments conducted earlier
(Experiment 5.3 and 5.4) and involving preconditioning of juvenile trout and kokanee to zooplankton suggest that attack predispositions of trout and kokanee may be genetically determined, although I recognize that more critical experimental tests are required to establish this point.
The Consequences of Species Specific Effects of Experience for Patterns of Prey Acquisition by Trout and Kokanee
Many motor patterns involved in search, approach, attack and manipulation of prey may be common to the members of two closely related species, however, learning may lead to divergence
in the form of such patterns which then may generate substantial differences in patterns of prey exploitation by predators. There are no specific differences between the composition of trout and kokanee diets, or between the prey contents of these predators and the environment, which I can attribute solely to the effects of short term experience with prey. In general experience will operate to amplify dietary differences by altering the responsive• ness of predators to prey that are encountered. Thus, the differential effects of experience on responsiveness of trout and kokanee will amplify the trends identified previously for:
1) kokanee to exploit a greater quantity and a greater variety
of zooplankton than trout do, 199
2) trout to exploit more large, armoured prey types such as
caddis larvae (Trichoptera), dragonfly and damselfly nymphs
(Odonata), aquatic insect adults (e.g. notonectids), molluscs
(e.g. planorbid snails) and large amphipods (Crangonyx sp.),
3) trout to "overexploit" and kokanee to "underexploit" large
prey items relative to their environmental abundance,
4) trout to contain a disproportionate number of large prey
items and kokanee to contain a disproportionate number of
small prey items relative to their environmental abundance.
In an earlier review article (Hyatt, 1979) , dealing with fish dietary habits, I stressed the point that patterns of non- random exploitation of prey should be considered to be a function of several potential biological mechanisms which operate alone or in concert. This view was contrasted with the more common practise by various investigators of sponsoring one mechanism or another as the sole driving force behind particular dietary patterns.
In the present study it is apparent that some of the differences in dietary patterns between trout and kokanee are not the result of single mechanisms but rather are produced by entire sets of mechanisms which operate at each stage of the behavioural chain involved in food gathering. For example, the general trend for trout to exploit larger prey than kokanee of equivalent size do (Chapter 2) is favoured not only by differences in habitat selection (Chapter 3) and search positions (Chapter 4), but also by the inability of trout to effectively capture the smallest size classes of prey (Chapter 5), the inability of kokanee to effectively handle large, armoured prey (Chapter 5), and finally by the 200
differential effects of experience on the responsiveness of these predators to large and small prey respectively (this chapter).
SUMMARY
1. The effects of experience on subsequent responses of trout and kokanee to prey are similar for prey with which the predators attain similar levels of capture and ingestion success
(Experiment 6.1).
2. Both trout and kokanee develop and maintain relatively constant and usually high levels of response to single prey species with which the predators experience greater than 30% attack success. Lower levels of attack success result in highly variable levels of response by the predators to single species of prey (Experiment 6.2).
3. Trout and kokanee exhibit an initial reluctance to attack large, well-armoured notonectids. However, in any trial trout eventually respond to notonectids more strongly than kokanee do.
With repeated exposure, kokanee rapidly habituate to these unrewarding prey but trout do not in spite of very low attack success (Experiment 6.3).
4. In response to experience with small, agile, JJ_. kenai, kokanee exhibit a change in approach and capture tactics which improves their capture success. Trout refine their basis approach and capture tactics, but do not employ entirely new ones in response to experience with D. kenai (Experiment 6.4). 201
5. In general, trout exhibit a strong predisposition to attack relatively large, well-armoured, prey and to ignore or reject small, agile ones (Experiments 6.3 and 6.4). Kokanee exhibit a strong predisposition to attack small, agile prey and to ignore or reject relatively large, well-armoured ones
(Experiments 6.2, 6.3 and 6.4). The effects of experience act to intensify these differences. 202
CHAPTER 7
TROUT AND KOKANEE FORAGING - THE STRATEGIC POINT OF VIEW
Much of evolutionary biology is the working out of an
adaptationist program. Evolutionary : biologists assume that each aspect of an organisms morphology, physiology, and behaviour has been molded by natural selection as a solution to a problem provided by the environment. The role of the evolutionary biologist is then to construct a plausible argument about how each part functions as an adaptive device. In practise an adaptationist program is constructed by creating descriptions of the organism and of the environment and then relating the descriptions by functional statements.
Lewontin, 1978.
INTRODUCTION
Trout and kokanee from Marion Lake exploit
statistically different sets of food resources. In previous
chapters I have dealt with why this is so in terms of proximal
"mechanisms" but have ignored why this is so from an evolution•
ary point of view. Therefore, the purpose of this chapter is to develop a discussion which will place results from previous
chapters into an evolutionary context.
Each species possesses a variety of strategies (eg.
feeding, reproductive, antipredator) which consist of the sum of both the fixed and facultative adaptations that have been
shaped through natural selection to maximize the fitness of individuals. Environmental diversity is the essential
ingredient that favours the evolution of species specific
strategies. This is because the metabolic and genetic 203 resources that go into one set of adaptations, addressed to particular environmental characteristics, come at the expense of energy and information that could go into another set of adaptations addressed to different environmental characteristics,
(Cody and Diamond, 1975). Hence the benefits derived from any trait are weighed by natural selection against the costs of maintaining that trait and also against the "abandoned" benefits of alternative traits.
In this chapter my basic argument will be that the morphological and behavioural traits that control food "selection" by trout and kokanee in Marion Lake (summarized in Table 29 ) are a consequence of the evolution of mutually exclusive foraging strategies which suit these predators to gather food most effectively from two different environments. One consequence of this is that trout and kokanee are preadapted to gather different foods even in the same environment (eg. benthic and littoral habitats of Marion Lake).
I will develop the chapter in two parts. The first involves the identification of the general nature of the habitat-prey complexes that have shaped trout and kokanee foraging strategies. The second part consists of a discussion concerning the evolution and adaptive significance of specific elements of trout and kokanee foraging strategies. TABLE 29. A summary of the "elements" which define the foraging strategies of trout and kokanee.
SOURCE TROUT KOKANEE
Within lake distribution consistently Within lake distribution consistently • Table 7. skewed towards onshore and benthic skewed towards offshore and surface or and habitats water column habitats Fig. 12
Activity peaks in early morning after Activity peaks in early morning and late Fig's. 13 which foraging efforts assume lower afternoon. Foraging efforts are continuous and 14. but consistent levels throughout throughout the daylight hours. Relatively daylight hours. Relatively inactive inactive at night. at night.
Do not "track" the environmental .Track the environmental abundance of Fig's. 8 abundance of prey very closely potential prey much more closely than and 9 trout do
Greatest proportion of diet (by wt.) Greatest proportion of diet (by wt.) Fig's. 4, obtained from relatively large size obtained from relatively small size 5, 6, and classes of prey (eg. terrestrial classes of prey (eg. chironomid pupae, 7 insects, snails, odonates, caddis zooplankton etc...) and other fish)
Usually forage as solitary individuals Usually forage in groups except when Unpublished but may forage within groups on some searching in benthic habitats at which observations occasions time they are solitary
Vision used as the primary sensory Vision used as the primary sensory Ali, 1959; mode during food search mode during food search Ware, 1971; Hyatt, present study Table 29 - continued
Employ a variety of search techniques Employ a variety of search techniques Table 12. and which may involve constant or which always involve constant swimming text intermittent swimming activity activity
Area extensive searchers ie. maintain Area intensive searchers ie. maintain Table 10. relatively high search velocities, relatively low search velocities, "test" Fig's. 16 "test" relatively few inanimate large numbers of small inanimate objects and 17 objects for their "potential as prey" for their potential as food and maintain and maintain search positions that search positions that are relatively are at relatively great distance close to the substrates that are scanned from the substrates that are scanned (see text for further explanation)
Reactive distance to a variety of prey Reactive distance to a variety of prey Fig. 20 of different sizes (up to 16 mm) is of different sizes (up to 16 mm) is usually less than 70 cm usually less than 70 cm
Employ a variety of approach and Employ a variety of approach and capture Table 17. capture techniques to take benthic, techniques to take benthic, water column, water column, surface and aerial prey and surface prey but do not exploit aerial prey
Possess relatively large mouths (ie. Possess relatively small mouths (ie. jaw Fig. 22 and jaw widths are close to 7-8% of widths are close to 5-6% of standard text standard length) and poorly developed length) and well developed gill-rakers gill-rakers
Exhibit a predisposition to attack Exhibit a predisposition to attack Experiments relatively large, well-armoured prey relatively small, agile prey and to 5.2, 5.3 and tend to ignore or reject small, ignore or reject large, armoured ones and 5.4 agile ones Table 29 - continued
Exhibit relatively high levels of Exhibit relatively low levels of Table 24. manipulation and ingestion success manipulation and ingestion success with large, armoured and with large, armoured and morphologically morphologically diverse prey diverse prey
Exhibit variable attack and Exhibit generally high attack and Tables 20 ingestion success with relatively ingestion success with small, agile and 22 small, agile prey prey
Maximum attack rates on small, agile, Maximum attack rates on small, agile, prey at high densities are relatively prey at high densities are relatively Fig. 23 low (ie. average 1860 attacks per hour high (ie. average more than 3000 attacks on Daphnia at densities of slightly per hour on Daphnia). greater than 2 per liter)
Exhibit a relatively high prey-size Exhibit a relatively low prey-size Table 22 threshold for an effective attack threshold for an effective attack response on very small prey response on very small prey
Develop and maintain high levels of Develop and maintain high levels of Fig. 30 receptivity to prey with which they receptivity to prey with which they experience greater than 30% attack have greater than 30% attack success. success. Responses more variable at Responses are more variable at lower lower levels of success. levels of success
Maintain high levels of response to Habituate rapidly to large prey which some large prey in spite of low offer low net energy returns and/or Fig. 31 ingestion success possibly high risk of damage during ingestion Table 29 - continued
Habituate rapidly to some small prey Maintain high levels of response Fig. 33 in spite of a potential for positive to small prey in general net energy returns
o 208
THE ENVIRONMENTAL CONTEXT FOR TROUT AND KOKANEE FORAGING STRATEGIES
In each instance the foraging strategies of trout and kokanee must ultimately relate to a specific environmental context. What is this context? Behavioural and morphological characteristics related to the feeding behaviour of trout and kokanee observed in this study have evolved or at least been maintained most recently with respect to the habitats and prey that are found within Marion Lake. However, adaptations do not evolve from scratch (Lewontin, 1978, Horridge 1977), thus, the kinds of foraging strategies that trout and kokanee have evolved to exploit the food resources of Marion Lake will have been limited to ones that are extremely similar to those of their immediate ancestors. Consequently, the elements making up the foraging strategies of trout and kokanee in
Marion Lake must be related not only to specific characteristics of habitats and prey found within Marion Lake but also to habitat and prey characteristics that trout and kokanee have responded to in other ecosystems over evolutionary time. A brief summary of the habitat-prey features that trout and kokanee respond to in Marion Lake compared to those commonly considered to be important to the species across their geographic range will help identify the general characteristics of the habitat-prey complexes that have likely shaped and maintained the foraging strategies of trout and kokanee.
In spite of its limited physical dimensions (area
13.3 ha, maximum dept 6 m), Marion Lake and its 2-5 miles 209 of accessible tributary streams do not represent a single habitat-prey complex to rainbow trout or kokanee. Results presented in this study (Chapter 3) as well as additional observations (Hall & Hyatt, 1974; Hyatt, unpublished data) identify rainbow trout from Marion Lake as predators that most commonly use habitats found within small streams or the littoral zone of the lake. Outside of Marion Lake rainbow trout form self sustaining populations in a variety of locations including: brooks and rivers (Metzelaar, 1929;
Neave, 1944; Hartman & Gill, 1968; Rawstron, 1972), small ponds (Berst & McCombie, 1975), lakes (Larkin et al. 1956;
Cartwright, 1961; Tody, 1964), estuaries and the open ocean
(Hart, 1973). However behavioural responses of trout to habitat features such as overhead cover (Newman, 1960;
McCrimmon & Kwain, 1966; Jenkins, 1969) and physiological responses to both salinity (Hoar, 1976) and temperature
(McCrimmon, 1972) suggest that trout are primarily animals of streams, intermediate sized rivers and the littoral zone of lakes.
Benthic and littoral habitats of streams and lakes contain a diverse invertebrate fauna that may potentially serve as prey for trout. Some of the important groups include nematodes, oligochaetes, leeches, ostracods, amphipods, crayfish, molluscs and a variety of aquatic insecta (for reviews see
Hynes, 1970; Wetzel, 1975). This taxonomic diversity is reflected in the invertebrates by a wide range of body sizes however the various sizes of prey are not equally abundant. 210
For example, within the top cm of a "typical" square meter of sediment in the littoral zone of Marion Lake, there is an average (based upon monthly samples taken over a year, Hoebel, unpublished data) of approximately 300,000 potential prey
(rotifers, copepods, mites, cladocerans and nematodes) between
100 ym and 2 mm in size. For prey greater than 2 mm in size, the average numbers per square meter are generally less than
50,000 (based upon monthly samples taken over a year, Efford et al., unpublished data). Similar patterns of abundance versus size exist for the invertebrates present as drift in
streams. Bishop and Hynes (1969) sampled the invertebrate drift in a stream, on a 24 hour basis, once a month for a year and found that more than 96% of the prey present were
smaller than 5 mm in length.
Results from a host of studies make it clear that
the diversity of potential prey in benthic and littoral habitats
is reflected in the diet of rainbow trout. At various times,
locations or developmental stages trout diets may be dominated
by zooplankton (Johnson and Hasler, 1954; Antipa, 1974),
terrestrial insects (Swift, 1970; Northcote, 1973), aquatic
insect larvae (Tody, 1964; Crossman and Larkin, 1959; Tippets
and Moyle, 1978), large crustaceans such as crayfish (Metzelaar,
1929); molluscs, leeches, or fish (Leonard and Leonard, 1946,
Crossman and Larkin, 1959). Regardless of this dietary
diversity there are general trends in rainbow trout dietary
habits. For example as rainbow trout increase in body size,
they usually exhibit dietary shifts from small-bodied 211 invertebrates (trout less than 10 cm in size), to larger crustaceans or aquatic insecta (trout less than 20 cm in size), and finally to a diet dominated by large prey items such as fish, squid or crayfish (trout greater than 30 cm in size).
Thus, in spite of the preponderance of small-bodied prey
items present in benthic and littoral habitats, trout, over most of their developmental history, derive the bulk of their food from relatively large (greater than 4 mm) prey items.
Trout from Marion Lake conform to this pattern since they do not track the environmental abundance of prey very closely
(Chapter 2,) but rather derive the bulk of their food from relatively large (greater than 4 mm), armoured, benthic
invertebrates (eg. snails, caddis larvae, odonate nymphs and amphipods).
The details presented above indicate that the habitat-prey complex that trout respond to in the Marion
Lake system (stream and lakeshore habitats, relatively large prey such as benthic invertebrates and terrestrial insects)
is the same as that which has been important to the species
in general. Therefore, I suggest that the foraging strategy
of trout from Marion Lake is likely representative of that
of the species in general and that it has evolved primarily
in response to certain selective pressures characteristic
of the littoral and benthic regions of both rivers and lakes.
It is my contention that trout "see" an environment containing
low densities of large, energy-rich prey that are relatively 212
dispersed within a given foraging patch. I will argue that this type of environment has selectively favoured adaptations which enable trout to differentially exploit relatively large dispersed prey at the cost of their abilities to effectively exploit small, contagiously-distributed prey. Because prey that trout obtain most of their energy from are relatively dispersed (see discussion below), I will refer to the foraging strategy of trout as a D-strategy.
In sharp contrast to rainbow trout, Marion Lake kokanee are almost exclusively inhabitants of offshore, water- column and benthic habitats. In spite of the fact that less than 35% of the surface area of Marion Lake lies over bottom contours at depths greater than 2 m, kokanee are found largely in this area (Chapter 3). Outside of Marion Lake, kokanee and sockeye salmon (from which kokanee are taxonomically indistinguishable) occupy a limited range of habitats most commonly associated with large oligotrophic lakes and the open ocean. Within the confines of a lake, kokanee and juvenile sockeye usually occupy the offshore, upper and middle layers of water (Foerster, 1968; Hartman & Burgner, 1972;
Goodlad et al., 1974). Occasionally kokanee may be closely associated with benthic habitats (Northcote & Lorz, 1966;
Chapman et al., 1967) of offshore waters for short periods of
time, however there are few records of populations that make prolonged use of the littoral zone of lakes or of running waters
prior to maturation. Behavioural responses of 0. nerka to
habitat features such as cover (Newman, 1960) and physiological 213
responses to both salinity (Hoar, 1976) and temperature (Brett,
1952; Foerster, 1968; Hyatt, Ms. in prep.) suggest that outside of the breeding season 0. nerka is primarily adapted to the upper waters of large lakes and the open ocean.
The prey complex of the upper waters of lakes typically occupied by kokanee or juvenile sockeye salmon is dominated by just three major groups. These include rotifers, cladocerans and copepods (for reviews see Hutchinson, 1967;
Wetzel, 1975). The size-frequency distribution of invertebrate prey in the upper waters of lakes is severely truncated in comparison to that of the littoral and benthic habitats occupied by trout. For example, although more than 15% of the potential invertebrate prey (organisms greater than 100 m) in benthic habitats of Marion Lake commonly fall within sizes ranging from 2-30 mm, invertebrate prey larger than 2 mm are virtually absent from the water column. This same pattern is repeated for the majority of lakes. Freshwater invertebrates
(eg. Mysis relicta, Leptodora sp., Chaoborus spp. and pontoporeia sp.) which commonly exceed sizes of 4 mm and which may occur in the upper waters of lakes are clearly the exception, not the rule. Indeed such prey are largely absent from the lakes that kokanee and juvenile sockeye are found in. In cases where such prey are present in the upper waters of lakes, it is usually only for a short interval during the diel cycle when vertical migration from deep water occurs.
Various studies indicate that kokanee and juvenile
sockeye salmon use small (less than 2 mm) crustacean zooplankton 214 as their major source of food. A number of studies (Narver,
1970; Woody, 1972; Horak and Tanner, 1963; Davis and Warren,
1970; McDonald, 1973) indicate that 80% or more of annual food intake (by volume) may consist of limnetic zooplankton.
Some studies (Chapman et al., 1967; Northcote and Lorz, 1966;
Goodlad et al., 1974) report that chironomid pupae make up a substantial proportion of the diet, however benthic invertebrates and terrestrial insects are seldom reported as significant in the diet of this species.
The pronounced dietary shifts that occur in rainbow trout as they increase in body size are largely absent in kokanee. Kokanee (or sockeye salmon) as large as 30 cm may still rely almost entirely on small (less than 3 mm) water column prey for the bulk of their food. A number of authors
(Hanamura, 1966; LeBrasseur, 1966) have indicated that even ocean dwelling sockeye at sizes between 30 and 50 cm consume mostly small amphipods and copepods from the water column.
At sizes greater than 30 cm, lake-dwelling kokanee may rely on relatively large water colmn prey such as Mysis sp. for food (sizes greater than 3 mm), however piscivory is rarely observed even in those freshwater populations containing individual kokanee which attain sizes greater than 40 cm
(Northcote, 1972; Irizarry, 1975) . In the open ocean, sockeye larger than 50 cm in length consume predominantly euphasiids, squid and small fish (LeBrasseur,1966 ). Thus, over most of their, developmental history, kokanee (and sockeye salmon) are pelagic predators that gather their food from relatively small-bodied prey found in the upper waters of lakes or the 215 open ocean. Kokanee from Marion Lake partially conform to this pattern since they derive much of their food from small, water-column prey (eg. chironomid pupae, zooplankton) however the inclusion of quantities of benthic invertebrates in their diet represents a significant departure from the general pattern.
The habitat-prey complex that kokanee are faced with in Marion Lake exhibits a number of features that differ from those normally encountered by the species. First less than 30% of the lake area can be classed as limnetic in character (ie. open water lacking cover such as logs, brush or weed beds). Next the zooplankton community in Marion Lake is ephemeral and is well developed only during a 2-3 month period in late summer (Efford, 1970). Finally Marion Lake exhibits a seasonal temperature regime which "forces" kokanee to abandon surface waters (Hyatt Ms. in prep.) and to forage in offshore (depths greater than 2 m), benthic-habitats in late summer (Chapter 3.). In spite of these differences, I believe that the responses of kokanee to the habitat-prey complex in Marion Lake suggest a foraging strategy which clearly bears the imprint of evolution in response to the habitat-prey complex that characterizes the offshore and upper waters of large lakes and in some cases the open ocean.
It is my contention that kokanee (and implicitly sockeye salmon) perceive an environment containing relatively high densities of small, low-energy, prey that are contagiously distributed within a given foraging patch. I will argue that this type of environment has favoured adaptations which enable 216
kokanee to exploit relatively small, contagiously-distributed
prey at the expense of their abilities to exploit large,
dispersed prey. Because prey that kokanee obtain most of
their energy from are contagiously distributed (see discussion
below), I will refer to the foraging strategy of kokanee as
a C-strategy.
It is important to note at the outset of this discussion
_that the concepts of C and D strategies are not absolute,
but are meaningful only by comparison. A given organism is
more or less of a D-strategist only by comparison with another
organism. Thus I will argue that rainbow trout as a species
possess adaptations which identify them as D-strategists relative
to the C-strategy of kokanee. The utility as well as the
weakness in applying this point of view exactly parallels
that in designating organisms as either r-strategists or K-
strategists with respect to their reproductive strategies
(reviewed in Stearns, 1976). By developing the concepts of
.C-selection and D-selection with respect to the foraging
strategies of kokanee and trout, I hope to demonstrate that it
is possible to recognize complementary associations of biological
traits which constitute foraging strategies addressed to
particular sets of environmental conditions. I will now
describe specific features of each habitat-prey complex in
greater detail and then attempt to show that morphological
or behavioural characteristics associated with foraging by
trout or kokanee are adaptations to these features. 217
THE ROLE OF PREY. SIZE,' RELATIVE ABUNDANCE AND PHYSICAL FEATURES OF THE ENVIRONMENT IN PROMOTING C-selected or D-selected FORAGING' STRATEGIES IN TROUT OR KOKANEE
In the upper waters of lakes containing fish, large, invertebrate prey (body sizes greater than 4mm) are scarce compared to the numbers found in benthic and littoral habitats, however small prey (body sizes between 100 ym and 2mm) are abundant. Kokanee as well as the majority of other freshwater fishes inhabiting the upper and offshore waters of temperate- zone lakes obtain the bulk of their diets from relatively small prey items (less than 2 mm body size). Due to the absence of any detailed analysis of the biological and physical conditions that control the evolution of successful foraging strategies, I can only suggest that this situation occurs because there are very few potential combinations of adaptations which provide a selectively advantageous balance of energy returned to energy expended for a predator searching open water habitats for large-bodied but extremely rare prey. Thus, it appears that the extreme scarcity of large-bodied prey consist• ently favours the evolution of C-selected strategies for predators
such as kokanee that must obtain their food from the habitat- prey complex associated with the open waters of temperate-
zone lakes.
In benthic or littoral habitats of lakes or streams,
large,invertebrate prey (body sizes greater than 4 mm) are
abundant compared to the numbers found in limnetic habitats.
Although large prey are still relatively scarce compared to the
numbers of small prey (body sizes less than 2 mm), many species 218
of freshwater fish that feed upon benthic prey obtain the bulk of their diets, over most of their developmental histories, from relatively large prey items. Thus, the greater abundance of large-bodied prey in benthic habitats has apparently expanded evolutionary "opportunities" to include D-selected foraging strategies (in which predators concentrate on exploiting relatively large, dispersed prey) in addition to C-selected foraging strategies. Because rainbow trout are among the species that include a disproportionately high number of large prey in their diets, I consider them to be D-strategists.
There may be any number of reasons for why conditions in the stream or lake habitats occupied by trout have tipped the balance of natural selection in favour of the evolution of a D-strategy. The one suggested here relies on the observation that trout always spend significant proportions or; in.many populations, their entire developmental history within running water habitats. These habitats often lack the crustacean zooplankton that characterizes the small-but-abundant end of the prey resource distribution in lakes. Although the presence of other small prey types still guarantees that the abundance of prey of different sizes in rivers is log normally distributed, the microfauna of rivers and streams is largely concealed beneath benthic substrates (Hynes, 1970) and thus is much less exposed than the microfauna of standing waters.
This likely reduces the probability that selection will favour the evolution of adaptations for the exploitation of relatively small prey by visual predators such as trout. Of course 219
significant quantities of this microfauna must still enter the drift of streams and trout do appear to frequently obtain the majority of their food supply in streams from drifting invertebrates (Jenkins et al., 1970), however review of a number of studies (references in Bishop and Hynes, 1969) suggests that small-bodied prey (less than 2 mm) are relatively inaccessible to trout even when suspended in the water column of a stream or river as drift.
The small size of individual prey, the difficulty of detecting them against a background of similar sizes of drifting detritus, and the short time available for response before currents carry prey out of attack range likely select against specialization on small prey by predators such as
trout. The alternative that natural selection will favour is
the retention of adaptations to exploit the large, relatively
rare prey items which characterize one end of the prey resource
distribution in flowing water habitats. Although the habitat-
prey complex of lakes is somewhat different from that of flowing
waters, I suggest that trout retain a D-selected foraging
strategy here because adaptations that favour the differential
acquisition of large dispersed prey within littoral and benthic
habitats of lakes are incompatible with those that favour
exploitation of small, contagiously-distributed prey (see
discussion below). 220
THE ROLE OF PREY DISTRIBUTION IN SHAPING SEARCH AND ATTACK COMPONENTS OF TROUT AND KOKANEE FORAGING STRATEGIES
In the upper waters of lakes, population densities of zooplankton commonly reach 200-300 animals per liter and occasionally exceed 5000 per liter. The density of zooplankton in lakes inhabited by O. nerka is usually reported as falling between 50-100 animals per liter (references in
Fo.erster, 1968). Unlike benthic prey, the majority of which are usually concealed, zooplankton are virtually always exposed within a foraging patch. Thus if the average density of zooplankton in a given foraging patch were 50 per liter, then the distance between sequential encounters by kokanee with prey would be on the order of a few cm (ie. 5 cm. or less). It is important to emphasize that this value likely represents the maximum within-patch distance between consecutive prey since fish will often encounter higher densities of prey
than limnetic sampling gear indicates. This is because sampling gear, moving linearly through many cubic meters of water, is not responsive to fine scale variations in prey density but
fish are. Thus at any instant, in limnetic habitats, multiple prey are likely to be within the reactive distance of a kokanee
(Chapter 4) searching within a patch (physical scale cm to m) containing prey.
On a per liter basis the densities of invertebrate
prey found within the top cm of benthic substrates of either 221
streams or the littoral zone of lakes may commonly exceed the densities of invertebrates present in the upper waters of lakes. For example, within Marion Lake there are on average 5 3.0-4.0x10 potential prey (organisms between 100 ym and -2
15 mm in size ) m and more than 80% of these are found within the top cm of sediment (Efford et al., unpublished data).
This is equivalent to 2.4-3.2x10 prey per liter. However, unlike the situation for limnetic prey, data on the density of benthic prey are not useful for even rough calculations of the distance between sequential encounters with benthic prey by predators such as trout. This is because the majority of benthic prey are normally concealed and thus are not subject to detection by visual predators such as trout.
Because the prey that are subject to detection are those suspended in the drift of streams or on the surface of benthic substrates in either streams or lakes, it is the densitites of these prey that will generally define the distance between potential encounters with prey by trout. Bishop and Hynes (1969) reported that although densities of benthic prey in the Speed River (southern Ontario, 5
Canada) were very high (average greater than 3.4x10 organisms m between July and Dec), only a small proportion of the benthos (.0002 - .004%) was present in the drift at any one
time. Therefore, densities of drifting invertebrates seldom
exceeded an average (taken over a 24 hour interval once per month) of one prey per 20 liters. Furthermore because only
3.5% of all prey were larger than 5 mm in size, the density 222
of larger prey was generally less than 1 per 500 liters. Since the Speed River flows through agricultural land and is relatively productive compared to streams inhabited by trout in the Pacific Northwest the above values are probably higher than the average densities of invertebrate drift encountered by trout throughout much of their native range. Translated into a spatial scale, these values suggest that on average the distance between potential encounters with prey by trout feeding on stream drift would be on the order of 14-20 cm. In addition if only large prey (sizes greater than 5 mm) are considered the distance between potential encounters would often be a meter or more.
Given the observations above, it is apparent that the distribution, abundance and sizes of prey in limnetic or flowing water habitats have provided rather different spatial scales for the evolution of search behaviours by trout or kokanee.
The relatively contagious distribution of prey within limnetic habitats, where there may be thousands of prey per cubic meter, should have"favoured the evolution and continued maintenance of area intensive search techniques by kokanee. By contrast the relatively dispersed distribution of prey within flowing water habitats, where there will generally be only a few prey m , should have favoured the evolution of area extensive search techniques by trout.
The characteristics that trout and kokanee exhibit while searching for prey in Marion Lake are highly compatible with this point of view. For example, trout and kokanee obtain 223
substantial quantities of prey from the lake surface, however, when foraging at the lake surface trout maintain search positions that are 45-100 cm below the surface while kokanee consistently search from positions that are only 5-30 cm below the surface
(Chapter 4, Fig. 17). The vertical distance of the predators below the lake surface affects the diameter of the circular area within which, on theoretical grounds, prey may be detected.
This is because beyond an angle of 97° 12' complete internal reflection of light occurs and the predators will see only this reflection (Fig. 35).
For predators foraging at the lake surface in very shallow water, the reflection beyond 97° 12' would consist of a distorted image of objects on the lake bottom, while in deeper water the reflection would include only objects found in the water column. The significance of this is that a trout, maintaining a search position 75 cm below the surface, searches a "window" with a diameter of 170 cm, while a kokanee at only
25 cm below the surface will experience a search window only 1/3 this diameter (Fig. 35). Thus, by maintaining positions that are further below the surface than those of kokanee, trout sacrifice the ability to detect small prey on the surface but they gain the capacity to search a much larger area of lake surface per unit time for relatively large prey.
This is especially apparent when it is recalled that trout maintain swimming velocities that are 55% greater than those of kokanee when searching in the water column (Table 10).
When combined, the effect of search position and velocity 224
FIGURE 35.
The effect of a predator's vertical distance from the lake surface on the diameter of the circular area within which, on theoretical grounds, surface prey may be detected. Beyond 97° 12' complete internal reflection of light occurs and the predators will see only this reflection. Search field diameters of 170 cm and 57 cm are reasonably representative values given the search positions that trout and kokanee usually assume when foraging at the lake surface (see Fig. 17).
The solid spheres indicate the relative sizes of the smallest prey that trout or kokanee could detect at particular locations within the instantaneous field of search, values of the minimum detectable target size for stationary prey were estimated by using Ware's results .on the reactive distance of trout to very high contrast prey (see Fig. 3, P. 104 of Ware, 1971). According to these results, a trout positioned at 75 cm below the lake surface would require a prey of at least 45 square mm in area to elicit a response at the edge of the instantaneous field of search, while a kokanee at only 25 cm from the surface would respond to prey of less than 3 square mm at the edge of the instantaneous field of search. KOKANEE-AREA INTENSIVE SEARCH
VELOCITY = 18.2 cm/s ^ ,
45 mm 2
VELOCITY = 27.7 cm/s
SEARCH FIELDS DRAWN TO SCALE 225
differences allow trout to search approximately 15 times the area that kokanee do in the same interval. Therefore at the lake surface the D-strategy of trout involves area extensive search for large prey while the C-strategy of kokanee involves area intensive search for small prey.
Unlike the situation at the lake surface, the search field at the lake bottom is theoretically greatest for a predator positioned right at or just above the substrate surface
(Fig. 36 a and b), however trout maintain search positions that are on average 30 cm away from the lake bottom when they forage for benthic prey, while kokanee generally maintain search positions that are only 5 cm away from the bottom
(Chapter 4, Fig. 16). Because trout swim approximately 30% faster than kokanee while searching for benthic prey (Table
10), trout will still scan a slightly larger area of lake bottom per unit time than kokanee however the distinction between area extensive search and area intensive search is hardly significant.
The near bottom search positions of kokanee are essential if they are to successfully detect prey as small 2
(ie. <1 mm ) as those normally exploited in limnetic habitats, but why should trout in Marion Lake maintain search positions such that they sacrifice the ability to detect small prey even though they do not gain the advantage of an enlarged field-of-search for large prey as was the case for the same behaviour at the lake surface? One key may lie in the assumption that the benthic search behaviour of trout has evolved in 226
response to relatively flat substrates. In lakes such as Marion this is a reasonable assumption, but in the flowing water habitats commonly occupied by trout the bottom is highly irregular due to the presence of rock-cobble substrates.
Bottom irregularities in flowing water habitats will block the search field of a predator that is close to the bottom more than for one that searches from a position further off the bottom (compare Fig. 36 c and d). An additional advantage for a predator assuming a higher position in the water column is that the search field may then take in both surface and benthic substrates, given an appropriate water depth (Fig.
36 d). Therefore in flowing water habitats which have played an important role in shaping the D-strategy of trout, the maintenance of search positions some distance away from the bottom could serve as an adaptation to favour area extensive search. Thus, trout in Marion Lake may respond to prey search on benthic substrates according to the same set of "rules" dictated by selection in flowing water habitats.
Certain specialized aspects of the spatial distribution of prey in flowing water or littoral zone habitats as compared to limnetic ones may also have influenced the evolution of attack procedures used by trout and kokanee. For example trout frequently leap distances of one to two body lengths above the lake surface as part of an attack procedure to capture aerial prey while kokanee do not appear to leap at all for prey (Chapter 5). The ability of trout to leap for aerial prey is highly advantageous in streams or the inshore 227
habitats of lakes where there will usually be many flying insects just above the water's surface throughout the summer.
This is especially apparent in Marion Lake which is small, shallow and surrounded by productive forest lands. Both terrestrial and aquatic insects are commonly in flight just above the lake's surface throughout much of the summer.
The failure of kokanee to leap for aerial prey does not appear to be very adaptive within the context of the
Marion Lake ecosystem. Although kokanee occupy offshore habitats in Marion Lake, the lake is small enough that large numbers of potential prey are in flight just above the surface even in these locations. The absence of well developed capture procedures for aerial prey is not surprising given that the usual habitat of kokanee is either the upper waters of offshore areas in large lakes or, as sockeye salmon, the upper waters of the Northeast Pacific. In these locations aerial prey are unlikely to have constituted an important enough prey resource to favour the evolution of such behaviour. 228
FIGURE 36. The effect of a predator's search position on the size of selected portions of the instantaneous field of search.
(a) Predator maintaining search position 5 cm off of lake bottom. Diameter of instantaneous field of search equals approximately 98 cm if the reactive distance to prey is assumed to be 50 cm.
(b) Predator maintaining search position 30 cm off of lake bottom. Diameter of instantaneous field of search is reduced to approximately 79 cm if the reactive distance to prey is assumed to be 50 cm.
(c) Predator maintaining search position of approximately 5 cm away from top of irregular, rock-cobble substrate within a stream riffle. Diameter of instantaneous field of search is only approximately 40 cm at the stream bottom and will not include the water surface in riffles deeper than 45 cm. Again the assumption is that the reactive distance to prey is 50 cm.
(d) Predator maintaining search position approximately 30 cm away from top of irregular, rock-cobble substrate within a stream riffle. Diameter of instantaneous field of search is approximately 76 cm at the bottom and 64 cm at the stream surface. Assumptions are that the riffle is approximately 65-75 cm deep and that the reactive distance to prey is 50 cm.
229
THE ROLE OF TEMPORAL PATTERNS OF PREY RENEWAL IN SHAPING SEARCH COMPONENTS OF TROUT AND KOKANEE FORAGING STRATEGIES
In addition to the spatial distribution of prey,
their temporal distribution within patches of water column or benthic habitats of lakes or streams will have acted to
shape and maintain some elements of the foraging strategies of trout and kokanee.
Within streams or rivers, flowing water provides
a mechanism for the continuous renewal of prey at any fixed
location. The rate of renewal will vary between locations
because of stream characteristics (eg. water velocity, stream-
bed morphology) as well as between times because of prey
behaviour (see Waters 1972 for review) however, the time scale
for renewal of drifting prey after removal by trout within
riffle habitats will generally be on the order of a few seconds
to a few minutes. As in streams, the within-patch renewal
rates of the prey of trout in the littoral zone of lakes may
be very fast (seconds to minutes) but highly variable in both
space and time. This is because the sources for prey renewal
at the lake surface (the vast "reservoir" of terrestrial and
airborne insects) and lake bottom (concealed benthic invertebrates)
are very close (distances of mm to a few m) to the locations
from which trout obtain their prey. Thus if trout deplete
the prey exposed on the sediment surface, prey renewal can
potentially take place almost instantaneously if prey concealed
a few mm beneath the sediment surface move into exposed positions. 230
Unlike the benthic invertebrates or terrestrial insects that trout commonly use as food, the zooplankton that kokanee commonly exploit in the upper waters of lakes are virtually always exposed within a foraging patch. Thus removal of prey from a foraging patch by kokanee can be relatively complete and prey renewal will have to depend upon both mass movements of surface waters and diel patterns of vertical migration by prey that are in deep water "compart• ments" some distance away (meters to hundreds of meters).
Due to the spatial and temporal scale of these events, prey renewal within a foraging patch in open waters is likely much slower (minutes to hours) than in the benthic and inshore-surface habitats of lakes, or the surface and water-column habitats of flowing waters.
If the inferences drawn above are generally correct, then different rates of within-patch prey renewal in limnetic, benthic and flowing water habitats may have acted to shape the evolution of some differences in trout and kokanee search behaviour.
For example, the foraging strategy of trout in streams frequently involves the selection of fixed locations from which the bottom, water-column or surface may be scanned for prey (Jenkins, 1969). Furthermore, laboratory studies on trout in artificial streams (Ringler, 1979) indicate that trout can distinguish profitable feeding positions from less profitable ones and tend to periodically shift locations to occupy the former (see Chapman & Bjornn, 1969). Trout in Marion Lake 231
exhibit the same behaviours since they frequently search for
lake surface or benthic prey by scanning the substrates from
a stationary position for intervals lasting up to a few minutes.
If few captures are made, trout resume mobile search (Chapter
4). Given that flowing water; nearshore, lake-surface; and
benthic habitats exhibit a potential for rapid but highly variable
renewal of prey, the maintenance of stationary search positions by trout may be viewed as an adaptive procedure to assess the
rate of within-patch prey renewal before the predators abandon
a given foraging location (eg. see Charnov, Orians and Hyatt,
1976).
The prey search behaviour of kokanee contrasts
sharply with that of trout since kokanee only employ search
techniques that involve continuous fixed-velocity swimming
(Chapter 4). Thus, kokanee in Marion Lake do not pause long
enough at the lake or sediment surface to obtain information
on the rate of within-patch prey renewal. This may be because
kokanee are adapted to forage primarily within limnetic habitats
where within-patch prey renewal is relatively slow and where
moving directly through a series of patches will always
result in a higher rate of prey discovery than waiting for
prey to recover within a patch where they have been recently
depleted. 232
THE ROLE OF PREY SIZE AND ABUNDANCE IN SHAPING MORPHOLOGICAL AND BEHAVIOURAL CHARACTERISTICS THAT FUNCTION DURING THE ATTACK PHASE OF C-selected or D-selected FORAGING STRATEGIES
If trout and kokanee really possess foraging strategies that have been shaped through evolutionary reponses to environments containing relatively large, dispersed prey and small, contagiously-distributed prey respectively, then the predators should not only exhibit adaptations which favour the detection of such prey but also should display complementary sets of adaptations for dealing with large and small prey respectively during the attack phase of food acquisition.
Results from previous chapters offer considerable support for this idea.
Trout possess relatively large mouths which are associated with high levels of success in the manipulation and ingestion of large, armoured or morphologically diverse prey. Trout also exhibit a predisposition to attack relatively large, well-armoured prey and to maintain high levels of response to large prey even when ingestion success is low. Persistent attacks undoubtedly pay off by ensuring that large but rare energy packages which require prolonged or vigorous handling are not abandoned prematurely by trout.
Adaptations which suit trout for acquiring large prey have apparently not been achieved without "abandoning"
the benefits of alternate traits. Accordingly trout possess relatively poorly developed gill-rakers which are often associated
in some way with an advantage in exploiting relatively small
prey (see Hyatt, 1979 for discussion). Trout also lack the 233
high degree of streamlined form attained by kokanee and this is accompanied by a relatively inferior maximum attack rate on small, agile prey. Finally trout exhibit a behavioural tendency to either ignore or reject many types of small planktonic prey that kokanee find highly acceptable. This behaviour appears even in situations when the prey are present at very high densities and represent the only obvious source of food.
As C-selected strategists in limnetic habitats, kokanee will have generally exploited a relatively narrow range of prey sizes (ie. usually between 100 ym and 4mm) and will seldom have experienced large prey-size as an obstacle to the successful capture or ingestion of prey. Difficulties
in handling prey are more likely to have been associated with an inability to retain the very small but abundant prey at
the "end" of the prey-size distribution. The relatively small mouth, well developed gill-rakers, and low prey-size threshold
for an effective attack response on invertebrates are logical outcomes of natural selection operating to favour adaptations
for exploitation of relatively small, morphologically-uniform prey by kokanee.
High densities of uniformly low-energy prey should also
have favoured the evolution of behaviours that promote high
rates of prey intake in order to meet the energy demands
of normal growth and metabolism. Kokanee do achieve high
maximum attack rates compared to trout when confronted with
high densities of small planktonic prey. High attack rates
may be achieved not only as a consequence of a more streamlined 234
body form and greater maneuverability but also through selection to favour: short decision times concerning whether or not to attack a given prey item, short handling times with individual prey and, as a corollory, short giving up times on individual prey that present any "difficulty" during manipulation. These characteristics are highly compatible with those traits known to constitute elements of the foraging behaviour of kokanee from Marion Lake (Table 29).
In many respects the adaptations that enable kokanee to effectively exploit small, contagiously-distributed prey are mutually exclusive of those which would allow them to exploit large, dispersed prey. The small mouth size of kokanee is clearly related to the relatively low levels of manipulation and ingestion success that they experience with large, armoured and morphologically diverse prey. Kokanee also appear to possess a behavioural predisposition to frequently ignore or reject even those large prey that laboratory experiments indicate they can handle. I suggest that this is logically an adaptive measure to reduce the risk of physical damage to the finely developed structure of gill-rakers which may be useful in exploiting very small prey.
FORAGING STRATEGIES AS COMPLEMENTARY COMPONENTS OF LIFE HISTORY STRATEGIES
A foraging strategy represents only a portion of
the adaptive complex that characterizes each species and it
is essential to remember that trends in the evolutionary
direction of any one component may influence the selective 235
advantages of many or all of the other components (Fig. 37).
For example, water column habitats, lacking cover, may favour an antipredator strategy that relies on the maintenance of large group size. Given that there is an overwhelming antipredator advantage to maintaining groups in the water column, then the elements of a species foraging strategy will evolve with reference to this selective pressure as well as to those exerted by the basic nature of the prey resource. Subtle differences in the reponses of trout and kokanee to "prey" are likely related to just such interactions.
Individual trout often orient to, approach, attack and then reject pieces of twig or armoured prey in the water column or on the sediment surface. Attacks upon a single item may be repeated several times until final rejection or ingestion takes place. When individual kokanee forage within groups in the water column, they too "test" objects for their food potential, however, they do not repeatedly attack single items.
Instead, after an initial rejection, they move on with the group and then test the next item encountered. The tendency to make only a single attack upon potential prey items in the water column is likely due to the "necessity" of maintaining contact with the main group as it moves. For. trout which forage alone most of the time, no such constraint applies. Single kokanee in the laboratory will repeatedly "test" prey just as trout do.
Because of the nature of the interactions between
the components making up the various strategies of a species, 236
FIGURE 37. An outline of the interactions between the basic
structure of the habitat and the strategies which
organisms evolve in response to food, predators
and competitors. -HABITAT • •^DISTRIBUTION AND FORAGING STRUCTURE ABUNDANCE OF •STRATEGIES FOOD
ANTIPREDATOR GROUP-*- STRATEGY SIZE
^ STRATEGIES FOR ' t SOCIAL ORGANIZATION 237
it is usually impossible to specify whether a particular element of a foraging strategy is the precedent for or the antecedent of a given pattern of social organization or a part• icular pattern of antipredator behaviour. In the example above,
I could have argued just as easily that water-column habitats favour the evolution of a prey complex, which in turn favours the evolution of foraging in groups by predators. Then, given that there was an overwhelming advantage to foraging as groups in the water column, the elements of a species antipredator strategy would evolve with reference to this selective pressure as well as to those exerted by the nature of the important predators.
Although the order for the evolution of a species strategies cannot be specified with any certainty, I believe that it is clear from the present study that the basic structure of the habitat determines the nature of the adaptive complex
(summarized in Table 30.) that evolves with respect to foraging by trout and kokanee. Cullen (1957) reached a similar conclusion concerning the adaptive complex that has evolved with respect to reproduction by cliff-nesting kittiwakes
(Rissa tridactyla). TABLE 30. A SUMMARY OF THE ADAPTIVE COMPLEX THAT HAS EVOLVED WITH RESPECT TO FORAGING BY TROUT AND KOKANEE.
PREDATOR CHARACTERISTIC ENVIRONMENTAL CHARACTERISTIC ADAPTIVE SIGNIFICANCE OF PREDATOR CHARACTERISTIC
DIET
TROUT Do not "track" the Wide range of invertebrate Large prey provide more environmental abundance prey sizes common in benthic favourable net return of prey very closely. and littoral habitats of of energy per unit foraging Bulk of diet over most flowing water or lakes. Small effort than small prey in of developmental history prey (<2mm) relatively unavail• flowing water habitats. composed of relatively able in flowing water. large (>4mm) prey.
KOKANEE Track environmental Narrow range of invertebrate Small but abundant prey abundance of prey more prey sizes commonly present provide a more favour• closely than trout do. (100.^m-3mm) in limnetic able net return of energy Bulk of diet over most habitats relative to benthic per unit foraging effort of developmental history or littoral zone habitats. than large prey in composed of relatively Large prey sizes (>3mm) limnetic habitats. small (<2mm) prey items. relatively unavailable due to virtual absence from plankton.
SEARCH BEHAVIOUR
TROUT Maintain relatively high Large prey are relatively Search procedures increase search velocities, "test" dispersed ie. on average the area scanned per unit relatively few inanimate distances between potential time and predispose the objects for their encounters with large prey predators to detect large "potential as prey" and (>2mm) may often be a meter but rare prey. maintain search positions or more. that are at relatively great distance from the "substrates that are scanned. Table 30.- continued
KOKANEE Maintain relatively low Small planktonic prey exhibit Search procedures favour velocities, "test" large relatively contagious the detection of large numbers of small distributions within a given numbers of small prey inanimate objects for foraging patch. On average through area intensive their potential as prey distances between sequential search. and maintain search encounters with small prey positions that are (<2mm) may be 5 cm or less. relatively close to the "substrates" that are scanned.
TROUT Stationary search Within-patch renewal rates of Procedure allows predator positions often benthic and terrestrial prey to assess within-patch, maintained as an highly variable in both space prey-renewal rates before alternative to mobile and time. Potential exists a "decision" is made to search. for very rapid (seconds to abandon a patch. minutes) prey renewal after depletion.
KOKANEE Search techniques Within-patch renewal rates of Continuous movement always involve planktonic prey relatively slow through a series of continuous, fixed- (minutes to hours) in both patches results in a velocity swimming. space and time. higher rate of prey discovery than waiting within a patch for prey to recover after depletion.
to to vo Table 30 - continued
ATTACK BEHAVIOUR
TROUT Commonly leap to capture Aerial prey frequently very Access to a source of aerial prey. abundant within a few cm of food that would be the water's surface in flowing unavailable otherwise. water or littoral zone habitats.
KOKANEE Do not leap to capture Aerial prey largely absent near aerial prey. the surface of the offshore waters of large lakes or the open ocean.
TROUT Possess relatively large Invertebrate prey span a wide Ensure relatively high mouths and a behavioural range of sizes and many possess levels ofsuccess during predisposition to attack tough chitinous body coverings. manipulation and ingestion relatively large, well- of large, armoured or armoured prey. morphologically diverse prey.
KOKANEE Possess relatively small Invertebrate prey span a Small mouth and gill- mouths, well developed narrow range of sizes and are rakers may aid in gill-rakers and a morphologically uniform capture or retention predisposition to attack relative to diverse of small, planktonic relatively small, invertebrates of benthic and prey. morphologically-uniform littoral zone habitats. prey. Table 30 - continued
TROUT Maintain high levels of Large, armoured prey may Persistence during response to large prey require vigorous or prolonged attacks on large prey even if ingestion success handling before ingestion but ensures that large but is low. Tend to ignore each prey represents a large rare energy packages or reject many types of quantity of energy. are not abandoned small planktonic prey. prematurely.
KOKANEE Maintain high levels of Small, morphologically uniform Ensures that predators response to small prey prey require very short maintain high rates of even if capture success "handling" times and each prey prey intake and a is low. Tend to ignore represents a small quantity of favourable net-energy or reject large, armoured energy. Large prey size should return. Rejection of prey upon initial seldom constitute a problem large prey may be an encounter and habituate during manipulation or inevitable consequence rapidly to stimuli ingestion of prey. of the set of "rules" presented by large prey kokanee use to assess upon repeated encounters. small prey (ie. minimize handling time) or a procedure which reduces the risk of damage to delicate structures such as gill-rakers. 242
SUMMARY
1. Trout are primarily adapted to the habitat-prey complex of flowing waters and of the benthic and littoral zones of lakes.
2. Conditions associated with flowing water habitats in particular have favoured the evolution of a D-strategy in which trout concentrate on relatively large, dispersed prey items for the bulk of their energy requirements.
3. Adaptations which enable trout to differentially exploit large prey include: procedures for area-extensive search; a predisposition to attack relatively large, armoured prey; large mouth size, and persistent responses to opportunities to attack large prey.
4. Trout are not well adapted to exploit relatively small, morphologically-uniform prey since the predators exhibit a tendency to ignore or reject such prey even under laboratory conditions where they serve as the sole source of food.
5. Kokanee are adapted primarily to the habitat-prey complex of the limnetic zone of large lakes and, as sockeye salmon, to the open waters of the Pacific ocean.
6. Conditions associated with open water habitats have favoured the evolution of a C-strategy in which kokanee concentrate on small, contagiously-distributed prey items for the majority of their energy requirements.
7. Adaptations which enable kokanee to differentially exploit small prey include: procedures for area-intensive search; a predisposition to attack relatively small, morphologically uniform prey; small mouth size; well-developed gill-rakers; and 243 an ability to sustain high attack rates on small, planktonic prey.
8. Kokanee are not well adapted to exploit large, armoured prey since the predators exhibit a tendency to ignore or reject such prey even under laboratory conditions where these prey serve as the sole source of food. 9-. Adaptations associated with search, approach or pursuit, and manipultation and ingestion phases of the feeding process appear in each instance to be evolutionary responses to specific features of a given habitat-prey complex. 10. C-selected or D-selected foraging strategies appear to be mutually exclusive evolutionary avenues down which kokanee and trout have been directed by the fundamental nature of a given habitat-prey complex. 244
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