Ecological Effects of Predator Information Mediated by Prey Behavior
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ECOLOGICAL EFFECTS OF PREDATOR INFORMATION MEDIATED BY PREY BEHAVIOR Tyler C. Wood A Dissertation Submitted to the Graduate College of Bowling Green State University in partial fulfillment of the requirements for the degree of DOCTOR OF PHILOSOPHY May 2020 Committee: Paul Moore, Advisor Robert Green Graduate Faculty Representative Shannon Pelini Andrew Turner Daniel Wiegmann ii ABSTRACT Paul Moore, Advisor The interactions between predators and their prey are complex and drive much of what we know about the dynamics of ecological communities. When prey animals are exposed to threatening stimuli from a predator, they respond by altering their morphology, physiology, or behavior to defend themselves or avoid encountering the predator. The non-consumptive effects of predators (NCEs) are costly for prey in terms of energy use and lost opportunities to access resources. Often, the antipredator behaviors of prey impact their foraging behavior which can influence other species in the community; a process known as a behaviorally mediated trophic cascade (BMTC). In this dissertation, predator odor cues were manipulated to explore how prey use predator information to assess threats in their environment and make decisions about resource use. The three studies were based on a tri-trophic interaction involving predatory fish, crayfish as prey, and aquatic plants as the prey’s food. Predator odors were manipulated while the foraging behavior, shelter use, and activity of prey were monitored. The abundances of aquatic plants were also measured to quantify the influence of altered crayfish foraging behavior on plant communities. The first experiment tested the influence of predator odor presence or absence on crayfish behavior. Crayfish spent more time foraging and less time in shelter in the presence of predator odor cues compared to predator absent controls. The crayfish also consumed greater quantities of two macrophyte species in the presence of threatening odors. In the second experiment, crayfish were exposed to odors from predators that were fed four different diets and varied in their size iii relative to the size of the crayfish. The crayfish responded to the relative size ratios between themselves and their predators, but the direction of the response was determined by the predator’s diet. The third experiment exposed individual crayfish to odors from individual predators which varied in gape size relative to the body size of the crayfish. The crayfish responded along a gradient of relative risk by foraging more and using shelter less in the face of greater threats. Crayfish that were not as threatened foraged less and spent more time in shelter. The results obtained across all three experiments were largely consistent and indicate that crayfish can extract detailed information from predator odor cues. Further, crayfish incorporate multiple types of predator information into threat assessments as they make resource use decisions. Subtle differences in predator odor cues alter crayfish behavior which mediates the influence of predatory fish in freshwater communities. iv This dissertation is dedicated to… Mom, for urging me to chase butterflies and my dreams; Dad, for leading me into the forest and the fields; Gram, for inspiring my passion for living things; Poe, for teaching me the faith of a fisherman; Ali, for the chance to learn how to lead; And Sarah, for being my partner in crime. I love and thank you all. I could not have come so far without all your support. v ACKNOWLEDGMENTS First, I want to thank my advisor, Dr. Paul A. Moore for his guidance and wisdom over the last four years. His approach to graduate training provided the bootcamp experience that I have long sought to test myself against. Under his tutelage, I learned more philosophy than I ever thought I would know, but more importantly I learned how to think and how to teach. Thank you to my committee members, Robert Green, Shannon Pelini, Andrew Turner, and Daniel Wiegmann for the inspiration of your work and for your comments on my research along the way. I appreciate your willingness to take me on as a mentee. To the past and present members of the Laboratory for Sensory Ecology, thank you for the solid foundation laid by those who came before, for the support given by those who were here, and for all the cinderblocks hauled, cold-wet nights collecting crayfish, tedious writing edits, and stimulating conversations whether scientific or pedestrian. Thank you to Bowling Green State University for financial and infrastructural support over the last four years. Thanks to the Department of Biological Sciences and Graduate Student Senate for providing travel funding which has allowed me to attend many conferences at locations across the United States. Thank you also for supporting my research with the Barbara Long-Masters Biological Sciences Research Award. I would also like to thank the University of Michigan Biological Station for the use of facilities and funding through the Marian P. and David M. Gates Graduate Student Endowment Fund. My three summers at the station were an amazing opportunity to network with world class scientists while exploring the natural wonders of northern Michigan. Finally, I would like to thank The Crustacean Society for supporting my research with their Fellowship in Graduate Studies. vi TABLE OF CONTENTS Page CHAPTER I: INTRODUCTION ........................................................................................... 1 CHAPTER II: FEEDING IN FEAR: INDIRECT EFFECTS OF PREDATORY FISH ON MACROPHYTE COMMUNITIES MEDIATED BY ALTERED CRAYFISH FORAGING BEHAVIOUR ........................................................................................................................ 12 Methods...................................................................................................................... 15 Collection and Housing of Crayfish, Bass, and Aquatic Plants ..................... 15 Experimental Design and Arenas................................................................... 16 Experimental Protocol ................................................................................... 18 Data Collection .............................................................................................. 20 Statistical Analysis ......................................................................................... 21 Ethical Approval ............................................................................................ 22 Results ........................................................................................................................ 25 Macrophyte Consumption .............................................................................. 25 Crayfish Behavior .......................................................................................... 26 Discussion .................................................................................................................. 31 Effect of Predator Odor on Macrophyte Consumption by Crayfish .............. 31 Consequences for Aquatic Systems ............................................................... 32 Conclusions ................................................................................................................ 35 CHAPTER III: BIG AND BAD: HOW RELATIVE PREDATOR SIZE AND DIETARY INFORMATION INFLUENCE CRAYFISH BEHAVIOR AND RESOURCE USE DECISIONS ........................................................................................................................... 36 vii Methods...................................................................................................................... 41 Collection and Housing of Animals and Plants ............................................. 41 Experimental Design and Arenas................................................................... 43 Experimental Mesocosms .............................................................................. 43 Diet Production .............................................................................................. 45 Experimental Protocol ................................................................................... 45 Data Collection .............................................................................................. 47 Ethical Approval ............................................................................................ 48 Statistical Analysis ......................................................................................... 48 Results ........................................................................................................................ 51 Macrophyte Consumption .............................................................................. 51 Foraging Effort............................................................................................... 51 Shelter Use ..................................................................................................... 52 Transitions...................................................................................................... 52 Discussion .................................................................................................................. 58 Chemical Components of Threat ................................................................... 58 Conclusions ................................................................................................................ 63 CHAPTER IV: FINE-TUNED RESPONSES TO CHEMICAL LANDSCAPES: CRAYFISH USE PREDATOR