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Consequences of Omnivory and Alternative Food Resources on the Strength of Trophic Cascades

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ABSTRACT Title of Dissertation: CONSEQUENCES OF OMNIVORY AND ALTERNATIVE FOOD RESOURCES ON THE STRENGTH OF TROPHIC CASCADES Steven D. Frank, Doctor of Philosophy, 2007 Directed By: Associate Professor Paula M. Shrewsbury Department of Entomology & Professor Robert F. Denno Department of Entomology Omnivorous predators that feed on prey and plant resources are recognized as an important component of food webs but their impact on herbivore populations and trophic dynamics is unpredictable. Feeding on food items from multiple trophic levels increases the reticulate nature of food webs and the labile role of omnivores in promoting trophic cascades. Using carabid beetles in a corn agroecosystem, this research explored the interactive effects of predator guild (omnivore or carnivore) and the trophic origin of alternative food resources (seeds or fly pupae) on the control of herbivores (black cutworms) and plant survival. I demonstrated that the trophic guild and feeding performance of carabids can be predicted from their mandibular morphology. Carnivorous carabids, using mandibles with sharp points and a long shearing edge, kill and consume caterpillars more efficiently than omnivores that have mandibles with wide molar areas adapted for consuming prey and seeds. Omnivore preference for seeds and pupae further reduced their consumption of cutworms, which resulted in increased plant damage, ultimately dampening trophic cascades. In open field plots the abundance of omnivorous carabids and ants increased in response to seed but not pupae whereas neither subsidy affected the abundance of carnivorous predators. Pupae subsidies reduced predation of cutworms by carnivores and omnivores, consequently reducing seedling survival. However, in seed subsidized plots omnivorous predators switched from seeds to higher quality cutworm prey. Thus, predation of cutworms increased with cascading positive effects for seedlings. This research demonstrated that omnivorous carabids interacted more strongly with alternative food resources, particularly seeds, than carnivores. In addition, this difference can be linked to morphological differences that reduced omnivore efficiency as predators suggesting omnivores may be less effective agents of biological control. However, increased tenure time and aggregation to plant resources by omnivores helped restore trophic cascades, and should enhance biological control. Understanding the predacious behavior of omnivores in resource diverse environments is essential to predicting their role in trophic dynamics. I provide evidence that the trophic origin of alternative food drives the strength of this interaction and the extent to which omnivores promote trophic cascades. CONSEQUENCES OF OMNIVORY AND ALTERNATIVE FOOD RESOURCES ON THE STRENGTH OF TROPHIC CASCADES By Steven D. Frank Dissertation submitted to the Faculty of the Graduate School of the University of Maryland, College Park, in partial fulfillment of the requirements for the degree of Doctor of Philosophy 2007 Advisory Committee: Associate Professor Paula M. Shrewsbury, Chair Professor Robert F. Denno, Chair Professor Pedro Barbosa Professor Galen Dively Associate Professor Irwin Forseth © Copyright by Steven D. Frank 2007 Acknowledgements I would like to thank my committee members for their time, expertise, and guidance as my research came to fruition. I would particularly like to thank Galen Dively who always made time to offer advice on an experiment, solve a statistical crisis, or track down his homemade corn jigger. I also thank Mike Raupp who introduced me to entomology (and Paula) and has been a valuable mentor and colleague ever since. From Mike I learned that you can’t be an entomologist when you grow up. You have to pick one or the other. I am grateful to the numerous laboratory and field technicians who helped me accomplish this research. However, I am truly indebted to Steph Wyman who was always willing to get up early, forego lunch, or stay out late – usually all in the same day– to get these experiments accomplished. Without Steph’s undue loyalty (and organization) the world would have had to wait considerably longer to understand how omnivory and alternative food resources affect trophic dynamics. I benefited from having two phenomenal advisors. Bob Denno brought a new and exciting dimension to my research and my perception of the natural world. From Bob I have learned an extraordinary amount that will enhance my career and contribution to the field of ecology. I am grateful to Paula Shrewsbury who started my scientific career and taught me every step of the way. Upon learning about her research I knew immediately, and for the first time, what my life’s work would be. I am grateful for her support of my many interests and projects which have helped me develop as an independent and confident scientist. More importantly, Paula has always prepared me to achieve my goals after school. Therefore, confident and well- trained as I may be, I will also be able to get a job. I am grateful to members of the Shrewsbury and Denno labs for helpful comments on experiments and presentations. Ellery Vodraska has been a fun and patient officemate and was always willing to listen to my ideas and even got roped into a few. I want to thank Rob Ahern and Holly Menninger for their friendship and willingness to serve as adjunct lab members. I am particularly grateful to Rob Ahern for our regular discussions and diversions as we took this journey together. I would like to thank my family for their life long support and encouragement. I am grateful to my father who nourished my love of nature by taking me fishing or picking up dead raccoons which was my, but not his, ideal weekend. I cannot thank my mother enough for everything she has done for me over the years. Under her subtle guidance I chose to stop following the Grateful Dead, abandon my budding careers in the Arkansas crystal mines and as an herbalist’s apprentice, and go to college. She never told me what to do. Rather, she helped me realize what I actually wanted and made that path so enticing I couldn’t help but follow it. And here I am. Finally I want to thank Sarah, my best friend and wife. Sarah has been extremely supportive of my work and goals and very understanding of their unpredictable nature. I cherish our relationship and look forward to fulfilling our goals and our next, exciting chapter together. ii Table of Contents Acknowledgements....................................................................................................... ii Table of Contents.........................................................................................................iii List of Tables ................................................................................................................ v List of Figures............................................................................................................viii Chapter 1: Mandibular morphology predicts trophic guild and feeding performance in predacious carabid beetles ............................................................................................ 1 Abstract..................................................................................................................... 1 Introduction............................................................................................................... 3 Methods..................................................................................................................... 9 Study system ......................................................................................................... 9 Relationship between mandibular morphology and guild membership ............. 12 Handling time of active and passive prey by omnivorous and carnivorous carabids with differing mandibular morphology ................................................ 17 Results..................................................................................................................... 19 Relationship between mandibular morphology and guild membership ............. 19 Effect of mandibular morphology and food type on handling time and food preference............................................................................................................ 21 Morphological and handling time differences between omnivorous and carnivorous carabids ........................................................................................... 23 Discussion............................................................................................................... 24 Applied implications........................................................................................... 32 Tables...................................................................................................................... 34 Figures..................................................................................................................... 40 Chapter 2: Consequences of omnivory and alternative food resources for herbivore suppression and the strength of trophic cascades ....................................................... 51 Abstract................................................................................................................... 51 Introduction............................................................................................................. 53 Methods................................................................................................................... 57 Study system ......................................................................................................
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