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An Analysis of Geographic Variation in the Antipredator

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An Analysis of Geographic Variation in the Antipredator AN ANALYSIS OF GEOGRAPHIC VARIATION IN THE ANTIPREDATOR ADAPTATIONS OF THE GUPPY, POECILIA RETICULATA by BENONI HENDRIK SEGHERS B.Sc, University of British Columbia, 1967 A THESIS. SUBMITTED IN PARTIAL FULFILMENT 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 January, 197 3 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, t 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 Vancouver 8, Canada ABSTRACT The main objective of this study was to describe and explain several features of geographic variation among isolated and semi-isolated populations (Trinidad, West Indies) of the guppy, Poecilia reticulata. Three main aspects of geographic variation were considered: (i) sex ratio, (ii) body size, and (iii) antipredator behavior. (i) . Extreme deviations (favouring females) from a theoretical Mendelian sex ratio were correlated with the presence of dense populations of a small cyprinodontid predator, Rivulus hartii. Laboratory experiments revealed that this variation was not caused by genetic differences in the sex determination system. In addition, sex ratios were not correlated with sexual dimorphism in colour. Predation experiments with Rivulus demonstrated that male guppies were not selectively attacked but were less adept at avoiding capture. Size-selective predation by Rivulus also placed males at a selective disadvantage. Whether conspicuous coloration increases the liability of males to predation has yet to be demonstrated unequivocally. (ii) Populations of guppies sampled in 1967 and 1969 showed a stable pattern of variation in body size; differences of over 41% in body length and 200% in weight ii iii were discovered. In compliance with Bergmann's Rule there was a significant negative correlation between body size and stream temperature. Though a substantial portion of the size variation can be explained as a direct phenotypic response to environmental differences, there is also good evidence for microevolutionary differences. Of a multitude of potential selective factors that might be responsible for this genetic diversity, only one, size-selective predation, was investigated. Field and laboratory evidence supported the hypothesis that large guppies enjoy an advantage with respect to Rivulus predation but are more vulnerable to large characid and cichlid predators such as Hoplias malabaricus and Crenicichla alta. In the laboratory, size-selective predation appeared to be caused by differences in the handling efficiency of the predators, however, in nature the interaction of several other factors must be considered. (iii) Field observations revealed that where characid and cichlid predators were present (and Rivulus absent) guppies, (a) were more restricted to the stream shore, (b) showed a greater tendency to school, (c) avoided a potential predator at a greater distance, and (d) had a lower alarm threshold. To assess the functional and evolutionary significance of this behavioral variation, predation experiments were conducted with samples of wild-r caught and predator-naive (laboratory-bred) guppies iv originating from 5 natural populations. These tests demon^- strated that fish either taken, or descended, from populat• ions exposed to characids and cichlids were relatively less vulnerable than those exposed to Rivulus. To determine why the predator-naive guppies were selected non-randomly, a comparison wa,s made of their habitat preferences, schooling behavior, reaction distance, and escape motor patterns. Significant interpopulation differences were found for several of the measures; gener• ally, these were consistent with the field observations. In addition, it was hypothesized that certain populations may learn to avoid predators more rapidly. It was concluded that much of the geographic varia^ tion in antipredator behavior is caused by genetic differences attributable to differential predation pressures. In some cases, these microevolutionary differences are apparently maintained without a major barrier to gene flow. ACKNOWLEDGEMENTS This thesis was supervised by Dr. N. R. Liley. I extend sincere thanks to him for introducing me to the problem considered in this study and for critically reading the manuscript. I am also grateful to my research committee, Drs. A. B. Acton, C. S. Holling, and J. D. McPhail for guidance and comments on the thesis. For hospitality in the Zoology Section, Department of Biological Sciences, University of the West Indies, St. Augustine, Trinidad, I am indebted to Dr. B. D. Ainscough, Prof. F. G. Cope, Dr. J. S. Kenny, and Mr. R. L. Loregnard. Senator Jeffrey Stollmeyer kindly permitted me to collect fish on his estate and Mr. Hugh Wood, Chief Fisheries Officer, Ministry of Agriculture, allowed me to maintain fish at the Freshwater Fisheries Research Station, Bamboo Grove. Miss Shireen Imam and Mr. Robert W. DeForest gave freely of their time to help with the field work. I profitted greatly from the advice and good humour of my fellow students, especially Mr, Peter J. Ballin, Mr. Kim D. Hyatt, and Dr. Donald L. Kramer. Finally, I thank my parents for their patience, v and cheerful encouragement throughout this study. This investigation was financed by the National Research Council of Canada through operating grants to Dr. N. R. Liley and postgraduate scholarships to myself. TABLE OF CONTENTS Page Abstract . , ......... ii Acknowledgements , v List of Tables , xii List of Figures xiv Chapter 1. Introduction. 1 Main objectives of the study. ....... 3 The biology of Poecilia reticulata: relevant literature ........... 7 2. Materials and Methods . , , . , 10 Introduction. ............... 10 Collection techniques ........... 10 Laboratory populations at Vancouver .... 12 Maintenance of fish 13 Observation and recording methods ..... 14 Ecological measurements .......... 15 Measurements on guppies 17 3. The Environment 19 Introduction 19 Classification of streams 20 Geographic distribution of fish species . 20 vii viii Chapter Page Predators of the guppy. .......... 23 Distribution and natural history of the main predators .......... 31 Migration and dispersal of guppies. .... 35 Summary of Chapter 3........... 39 4. Geographic Variation in the Sex Ratio, .... 41 Introduction. • 41 Sex ratios of natural populations ..... 42 Sex ratios of laboratory stocks ...... 46 Relationship of predation to variation in the sex ratio. ............ 49 Size hypothesis .............. 57 Behavior hypothesis ...... 58 Relative survival of the sexes in predation experiments .......... 59 A. Experiments with wild-caught fish, . 60 B. Experiments with laboratory stocks , . 64 Procedure for standard survival test. 64 Discussion of survival experiments, ... 71 Tests of the behavior hypothesis. ..... 75 Discussion of sex differences in behavior. 82 Conclusion and general discussion of geographic variation in the sex ratio , . 83 Summary of Chapter 4........... , 89 ix Chapter Page 5. Geographic Variation in Body Size ...... 92 Introduction. ............... 92 Body size variation in natural populations .......... 95 Relationship of body size and temperature . 97 Relationship of body size and predation . 103 Evidence from the field for size selection ...... 104 Experimental analysis of size selection . 107 Mechanisms of predator selection for size differences in prey. ........ 112 Conclusion and general discussion of geographic variation in body size .... 123 Summary of Chapter 5........... 129 6. Geographic Variation in Behavior. 131 Introduction. , . 131 Field observations of behavior f . 132 Distribution of guppies in the stream environment. .......... 133 Schooling behavior 137 Reaction distance to potential predators ............... 141 Motor patterns used in antipredator behavior 143 X Chapter Page Population differences in escape motor patterns 148 Summary of the field observations of behavior .............. 150 Survival value of behavioral differences in wild-caught fish 151 Conclusion for survival experiments with wild-caught guppies , . » 159 Relative survival of laboratory stocks. , 161 Discussion of results of survival experiments ............... 166 Geographic variation in the antipredator behavior of laboratory stocks ...... 169 (a) Microhabitat selection. 170 (b) Reaction distance to predators. 182 (c) Escape motor patterns of individual fish 188 (d) Schooling behavior. 208 Conclusion and general discussion of geographic variation in behavior. .... 217 Summary of Chapter 6........... 226 7. General Discussion and Conclusions. ..... 231 The environment 231 Coloration and the sex ratio, ....... 232 Body size 234 xi Chapter Page Antipredator behavior , 235 Suggestions for future research 239 Literature cited , 244 Appendix 261 LIST OF TABLES Table Page 1. Classification and physical features of streams in the Northern Range (March-June, 1969).,...,.,.,., . 21 2. Natural history of the main fish predators 32 3. The principal fish predators occurring at the main study areas. ..... 36 4. Site attachment of guppies in the Petite
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