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Open Venable Dissertation__2019 Final The Pennsylvania State University The Graduate School Eberly College of Science THE EFFECTS OF INVASIVE PREY ON NATIVE PREDATORS A Dissertation in Biology by Cameron P. Venable © 2019 Cameron P. Venable Submitted in Partial Fulfillment of the Requirements for the Degree of Doctor of Philosophy May 2019 ii The dissertation of Cameron P. Venable was reviewed and approved* by the following: Tracy Langkilde Professor and Head of Biology Dissertation Advisor Committee Co-Chair Stephen W. Schaeffer Professor of Biology Associate Department Head of Graduate Education Committee Co-Chair Rudolf Schilder Assistant Professor of Entomology and Biology Nancy Ostiguy Associate Professor Emeritus of Entomology *Signatures are on file in the Graduate School iii ABSTRACT Invasive species are a growing threat to ecosystems worldwide. They can act as competitors, predators, and prey of native species, which may need to adapt in order to survive. Research on this topic usually focuses on the first two of these roles as they involve dramatic effects of invasive species killing or displacing natives. However, the role of invasive species as prey can have important effects that cascade down food chains, affecting entire ecosystems. My dissertation research focuses on the role of invasive species as prey and their influence on native predators. I use a well-studied system of the native eastern fence lizards (Sceloporous undulatus) that act as both predators and prey of the toxic invasive red imported fire ant (Solenopsis invicta). The ability to differentiate between toxic invasive and palatable native species is imperative for animals to be able to avoid a potentially lethal encounter. I tested whether fence lizards differentially consume native versus invasive ants as juveniles and adults. Despite being more vulnerable to lethal effects of fire ants, hatchling lizards consumed similar numbers of both ant species whereas adults consumed nearly three times as many native ants as invasive fire ants. This shift towards increased consumption of fire ants in adulthood could be the result of lifetime experience, an innate ontogenetic shift in the ability to distinguish between ant species, or a reduced risk for adults. Avoiding toxic invasive species can have important fitness advantages. I tested whether juvenile lizards would learn to avoid eating fire ant with repeated exposure. Lizards were exposed to different relative numbers of fire ants and native ants. Juveniles displayed a clear aversive behavior when given the highest exposure to fire ants, iv consuming nearly two-thirds fewer fire ants after the first day of consumption. Juveniles exposed to fewer fire ants showed similar aversion learning, but reverted to initial levels of consumption after 5 days. Juveniles that were exposed to native ants only did not alter their ant consumption. Juveniles showed a species-specific aversion to fire ants, which should allow them to preferentially avoid eating these toxic invaders, but this was dependent upon stimulus strength. In order to see if juveniles show a generalized aversion response of invasive ants that carries over to native ants, I tested whether prior exposure to (and subsequent avoidance of) invasive fire ants would reduce the subsequent consumption of a palatable native ant species. Lizards that were initially exposed to fire ants were less likely to subsequently consume palatable native ants. These results suggest that eating invasive prey can lead native species to avoid similar palatable native species, limiting their prey pool, and potentially destabilizing trophic interactions via the resulting cascading effects throughout the ecosystem. Finally, I determined the possible ways lizards may distinguish between a native and invasive prey species. My data shows that lizards do not seem to use chemical cues to differentiate these species but encounter more of the native species in controlled experiments and when given the option to consume or reject ants, they reject invasive ants three times more than native ants. My thesis research illuminates how native species can respond to invasive prey, revealing that they can learn to avoid toxic prey and preferentially consume palatable native species, but that this ability differs across life history. In addition, my work suggests that animals that are exposed to toxic prey may subsequently avoid palatable v native species which could dramatically limit their prey options. By examining interactions between native predators and invasive prey, this work provides insight into how native species are adapting to novel prey sources in their environment. Understanding the fitness consequences of different strategies to deal with noxious invasive prey and the potential trophic level consequences are vital in examining the long-term community level effects of invasive species. vi TABLE OF CONTENTS List of Figures .............................................................................................................. viii Acknowledgments........................................................................................................ x Chapter -1- Introduction .............................................................................................. 1 Ontogenetic shift in diet and learned avoidance ................................................... 2 Stimulus strength .................................................................................................. 3 Native predators distinguishing between alternative prey .................................... 4 Generalized/ Carry-over effects ............................................................................ 5 Study System and Research Objectives ................................................................ 6 References ............................................................................................................. 8 Chapter -2- Lizards display an ontogenetic shift in relative consumption of native and invasive prey .................................................................................................. 12 Abstract ................................................................................................................. 13 Introduction ........................................................................................................... 14 Methods ................................................................................................................ 17 Animal Collection and Husbandry ................................................................ 17 Lizard feeding trials ...................................................................................... 19 Statistical analysis ......................................................................................... 19 Results ................................................................................................................... 20 Discussion ............................................................................................................. 21 Acknowledgments ................................................................................................ 25 Figures .................................................................................................................. 26 References ............................................................................................................. 27 Chapter -3- Aversion learning in response to an invasive venomous prey depends on stimulus strength .............................................................................................. 32 Abstract ................................................................................................................. 33 Introduction ........................................................................................................... 34 Methods ................................................................................................................ 37 Animal Collection and Husbandry ................................................................ 37 Lizard feeding trials ...................................................................................... 38 Statistical Analysis......................................................................................... 39 Results ................................................................................................................... 41 Discussion ............................................................................................................. 42 Acknowledgements ............................................................................................... 47 vii Figures .................................................................................................................. 48 References ............................................................................................................. 50 Chapter -4- Eating toxic invasive ants reduces subsequent consumption of native ants by a lizard ...................................................................................................... 54 Abstract ................................................................................................................. 55 Introduction ........................................................................................................... 56 Methods ................................................................................................................ 58 Animal Collection and Husbandry ...............................................................
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