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THE BEHAVIORAL DYNAMICS and TEMPORAL EVOLUTION of WALL- FOLLOWING BEHAVIOUR in BLIND and SIGHTED MORPHS of the SPECIES Astyanax Fasciatus

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THE BEHAVIORAL DYNAMICS and TEMPORAL EVOLUTION of WALL- FOLLOWING BEHAVIOUR in BLIND and SIGHTED MORPHS of the SPECIES Astyanax Fasciatus THE BEHAVIORAL DYNAMICS AND TEMPORAL EVOLUTION OF WALL- FOLLOWING BEHAVIOUR IN BLIND AND SIGHTED MORPHS OF THE SPECIES Astyanax fasciatus Saurabh Sharma A Thesis Submitted to the Graduate College of Bowling Green State University in partial fulfillment of the requirements for the degree of MASTER OF SCIENCE December 2008 Committee: Sheryl L. Coombs, Advisor Paul Moore Robert Huber ii ABSTRACT Sheryl L. Coombs, Advisor Mexican blind cavefish exhibit an unconditioned wall-following behavior in response to novel environments. Similar behaviors have been observed in a wide variety of animals, but the biological significance of this behavior and its evolutionary history are largely unknown. In this study, the behaviors of sighted river morphs and congenitally blind, cave-dwelling morphs of the same species, Astyanax fasciatus were videotaped during and after their initial introduction into a novel arena under dark (infrared) and visible light conditions. The swimming movements of fish in the experimental arena were tracked with an automatic image-tracking system to provide a post-hoc analysis of how the fish’s swimming speed and position (distance and orientation) with respect to the arena walls varied over time. In response to the novel environment in the dark, both sighted and blind morphs exhibited wall-following behaviors with subtle but significant differences. Blind morphs swam more nearly parallel to the wall, exhibited greater wall-following continuity and persistence and reached maximum and stable swimming speeds (~1.5 BL/s) much more quickly than sighted morphs. In contrast, sighted morphs placed in the same novel, but well-lit environment exhibited dramatically different behaviors that consisted of either holding stationary positions near the wall for long periods of time or moving in and around the central region of the environment without moving along the walls. These results are consistent with the idea that both blind and sighted morphs have inherited primitive wall- following behaviors from their common sighted ancestor that serve an exploratory function under visually-deprived conditions. Under well-lit conditions, the proclivity of some sighted morphs to remain motionless near the wall of a novel environment suggests that near-wall iii preferences may also serve a protective function under some circumstances. It appears that wall- following behaviors of blind morphs rely more heavily on active sensing by the lateral line and have become more finely honed for exploratory purposes than those of sighted morphs. iv DEDICATION To my teachers and parents who have always been my guiding light. v ACKNOWLEDGMENTS I would like to thank my advisor, Dr. Sheryl L Coombs for her guidance and support in my research endeavors. I would also like to thank Dr. Paul Patton for his extensive technical support and advice on experimental design, Dr. Tim Bonner at Texas State University, San Marcos, Texas for supplying the sighted Astyanax morphs, Dr. Theresa Burt De Perera and my committee members, Dr. Paul Moore and Dr. Robert Huber for their feedback on my thesis and for statistical advice. Finally, thanks to all my lab mates, especially Tristan Ula for taking care of the experimental animals for the major portion of my time as a graduate student. vi TABLE OF CONTENTS Page REVIEW OF LITERATURE ................................................................................................ 1 Introduction………………………………………………………………………… 1 Blind Mexican cavefish as models for studying wall-following behaviors ................... 6 The lateral line system and active hydrodynamic range ............................................... 9 Other non-visual sensory systems .............................................................................. 12 MATERIALS AND METHODS ........................................................................................... 14 Overview of experimental design .............................................................................. 14 Experimental animals................................................................................................. 15 Experimental setup..................................................................................................... 15 Behavioral procedures ............................................................................................... 16 Data analysis ............................................................................................................ 17 Statistical analysis ...................................................................................................... 20 RESULTS .............................................................................................................................. 22 Movement patterns, spatial distributions and body orientations of blind sighted morphs in the dark ......................................................................................... 22 Temporal development of wall-following behaviors of sighted and blind morphs in the dark ............................................................................................ 26 Behavioral results of sighted morphs in the light compared to sighted and blind morphs in the dark ..................................................................................... 29 The effects of swimming speed and fish length ......................................................... 30 SUMMARY OF RESULTS .................................................................................................. 32 vii DISCUSSION ………............................................................................................................ 34 Functional significance and evolution of wall-following behaviors in Astyanax fasciatus ...................................................................................................... 34 The role of active sensing by the lateral line in wall-following behaviors of blind and sighted morphs ...................................................................................... 37 Inter-individual variability within morphs ................................................................. 41 Alternative explanations for wall-following behaviors and observed population differences ................................................................................................ 43 Switching from visual to non-visual modes of processing information .................... 44 SUMMARY AND CONCLUSIONS ................................................................................... 46 LITERATURE CITED .......................................................................................................... 48 APPENDIX A. TABLES AND FIGURES .......................................................................... 56 viii LIST OF FIGURES Figure Page 1 Distribution of the lateral line system on blind cavefish .......................................... 56 2 Mechanism of active flow sensing in fish ................................................................. 57 3 Video frame record and digitized tracks of fish movements ..................................... 58 4 Conventions for measuring distance and orientation of the fish re: wall ................. 59 5 Swimming tracks of sighted and blind morphs in dark ............................................ 60 6 Frequency distributions of wall distances ................................................................. 61 7 Frequency distributions of angular compass positions .............................................. 62 8 Frequency distributions of body orientations ............................................................ 63 9 Wall distance, orientation, orientation vector strength and swimming speed as a function of time ................................................................................................... 64 10 Z statistic of angular compass distributions as a function of time ............................. 65 11 Illustrations of operational criteria for wall-following behaviors .............................. 66 12 Swimming tracks of two sighted individuals in the light .......................................... 67 13 The effects of time, morph type and light vs dark condition on key wall-following parameters ............................................................................................................ 68 14 Summary of temporal effects for sighted morphs in the light and sighted and blind morphs in the dark ..................................................................................................... 69 15 Temporal effects on the uniformity of angular compass positions for sighted morphs in the light and sighted and blind morphs in the dark. ................................................... 70 ix LIST OF TABLES Table Page 1 Significance levels (p values) for tests of population differences ............................ 71 2 k-stat values for tests of difference between observed and hypothetical uniform distributions of wall distances ...................................................................... 72 REVIEW OF LITERATURE Introduction Orientation is a critical and ubiquitous component of animal behavior that takes many different forms to function in many different behavioral and ecological contexts. As a consequence, orienting behaviors have been classified in many different ways (Fraenkel and Gunn 1961; Janders 1975; Schone 1984). Nevertheless, most orienting behaviors can be grouped into general categories based on stimulus and response
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