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Behavioral Ecology of Wasp-Spider Interactions: the Role Of BEHAVIORAL ECOLOGY OF WASP-SPIDER INTERACTIONS: THE ROLE OF WEBS, CHEMICALS, AND DECEPTION A Dissertation submitted to the Faculty of the Graduate School of Arts and Sciences of Georgetown University in partial fulfillment of the requirements for the degree of Doctor of Philosophy in Biology By Divya Bellur Uma, M.S. Washington, D.C. April 14, 2010 Copyright 2010 by Divya Bellur Uma All Rights Reserved ii BEHAVIORAL ECOLOGY OF WASP-SPIDER INTERACTIONS: THE ROLE OF WEBS, CHEMICALS, AND DECEPTION Divya Bellur Uma, M.S. Dissertation Advisor: Martha R. Weiss, Ph.D. ABSTRACT Predator-prey interactions are integral to the maintenance of community structure and function. Predators and prey use multiple cues to detect and assess each other, and identification of these cues is necessary to understand how selection operates to shape predator-prey interactions. Mud-dauber wasps (Sphecidae), one of the main predators of spiders, prefer araneids (two-dimensional web-building spiders) over derived araneoids, (three-dimensional web-building spiders). Predation pressure by spider-hunting wasps is considered a key factor in the evolution of 3D web-building spiders. However, the proximate basis of such preference was not known. By conducting behavioral and chemical assays I have determined that Sceliphron caementarium wasps recognize araneids as potential prey due to the presence of chemicals present on their silk and cuticle. By analyzing cuticular extracts of spiders in several families, I have shown that all spiders that are taken by wasps have similar cuticular chemistry; however, all spiders that have that similar chemistry are not taken by iv wasps. Indeed, spiders’ antipredator behavior, morphology and web architecture are important factors that influence prey capture by wasps. Though not captured by S. caementarium , derived araneoids are readily captured by another sphecid, Chalybion californicum . Examinations of the hunting behavior of C. californicum towards Achaearanea tepidariorum (cobweb spider, Theridiidae, derived araneoid) reveals that the antipredator behavior of the cobweb spider changes over its ontogeny. Whereas small-sized spiders drop off their webs (i.e., seem to treat wasp as predators), medium and large-sized spiders attempt to warap wasps in silk (i.e., seem to treat wasps as prey). Besides araneids, Sceliphron also capture jumping spiders: however, they do not capture Peckhamia picata , a jumping spider that mimics ants. Chemical analyses demonstrate that ant mimics lack the chemical signature of a typical jumping spider but they chemically resemble their model ant, Camponotus sp. My results suggest that P. picata uses visual mimicry to avoid predatory jumping spiders, and employs chemical information to elude wasps and perhaps ants. Thus P. picata uses different sensory modalities to deceive multiple audiences. My study highlights the importance of spider webs, chemistry and behavior in shaping interactions between wasps and spiders, and contributes to our understanding of the use of multimodal cues in predator-prey interactions. iv To amma and ajji v ACKNOWLEDGEMENTS I am grateful to a number of people who have encouraged me and stood by my side during several years of grad school life. Honestly, I do not have words to thank my advisor, Martha Weiss. She has been a wonderful mentor, friend, and a source of inspiration. I am grateful to Martha for allowing me to explore the world of spiders, an area which was not related to her own research. Working in Martha’s lab was a pleasure, as I could learn and participate in numerous on-going projects in the lab, which allowed me to broaden my horizon and to appreciate biology in a more holistic manner. I feel proud to say that I was of her student. By interacting with her, I have also developed a deep appreciation towards plants around me. I will miss the summer days spent on the Observatory hill, where we were always exploring something new, designing experiments or coming up with a new arts and craft project. This dissertation would not have been possible without Martha’s constant encouragement, her brilliant thoughts, and her help with writing proposals and papers. I hope, one day I could write as beautifully as you do. Besides my advisor, I am indebted to Todd Blackledge, my committee member for being my wasp and spider guru. Thank you for providing several insightful inputs through these six years, for giving critical feedback on papers and proposals and for helping me in collecting spiders. Only after following your own PhD work on wasps and spiders, I learnt the tricks of the trade in working with solitary sphecid wasps! vi I would not have known that spider-hunting wasps existed but for a conversation I had with my other committee member, Jonathan Coddington. I am grateful to you for allowing me to spend time looking through the spider collection at the Natural History museum. Thanks also to Janet Mann, my other committee member who graciously agreed to be on my PhD committee, and for her inputs on my dissertation. This work would not have been possible without the collaboration with Larry Phelan, chemical ecologist at Ohio State University. I owe my deepest gratitude to Larry Phelan, Rodrigo Chorba and Jenny for helping with the chromatograms. I am also grateful to Gudrun Herzner, and Erhard Strohm from University of Regensburg for their help with the ant mimicry project, and their hospitality while I visited Regensburg. I also sincerely thank Catalina Estrada and Johannes Kroiss for your guidance with the chemical analysis. Much appreciation goes to John Lill and Shannon Murphy and other members of the D.C. Plants Insect Group (DC PIG) for their excellent inputs while I was working on the manuscripts. I would like to thank Peter Armbruster for being always available to talk about ideas, and Edd Barrows, for sharing his vast natural history knowledge about anything we saw out in the Observatory garden! My deepest gratitude to Jeremy Miller who taught me how to identify spiders, and Fernando Pallida, Lara Lopardo and G. B. Edwards for identifying spiders. This research would not have been possible but for the timely statistical help from Gina Wimp and Aaron Howard, who devoted much time with me to answer my naïve questions. My earnest thanks to a number of others with whom I corresponded via emails to learn about different aspects of wasps and spiders. These vii include Michael Greene, Mark Elgar, Gudrun Herzner, Allan Hook, Stefan Schulz and James Pitts. I would not have enjoyed being in grad school but for my wonderful lab mate Heather Mallory. Thanks Heather for all your help, your insights about anything I wanted to know, for your company, and for your efforts to expose me to the American culture and way of life!—I will truly miss you. I owe you a big treat for helping me format the page numbers on the last day—I could not have done this without your help! I was lucky to have very good lab mates and fellow graduate students throughout these six years in Georgetown- Thank you Aaron Howard, Caitlin Durkee, Karin Bothwell, Doug Blackiston, Dani Rodrigues, Sheena Pooter, Eric Oberdorf, Jean Tsai, Debbie Ladner, Dan Kjar and Tenley Archer and many more. I would not have survived graduate school without interactions with a number of dear friends, most of who do not live in the DC area, but kept in touch through emails! Thank you, Srini, Smita, Roy, Daniel, Avanti, Tanu, Anju, Swati, Rhitu, Manu, Elu, Suneela and Vivek for being available when I needed you most. Thanks to Raghvendra who did not think I am crazy, but cheerfully to part in collecting spiders in India. I am also grateful to a number of close friends in the area with whom I have explored the multicultural events that DC has to offer. Thank you Agomoni, Isha, Srinjoy, Shailaja, Krishna, Kirk and Alpa for your wonderful company and friendship. I am indebted to my housemate Alpa, who cooked for me, and took care of things during the stressful times before my defense. I would not have pulled through the last few months before my defense but for the viii affection, friendship and solid support of my dear friend Kirk—thanks for just being there for me. Most importantly I would like to thank my close friend and husband Sayantan, without whom I would not have joined grad school in the first place! Thanks for believing in me, sharing my excitement about new ideas and for showing me that the only way to see whether something works is to try it! I would also like to thank my in-laws for their love and support. My love for nature comes from having spent many hours during my childhood in the backyard of my home in Shimoga, India, either attempting to feed Ashy Wren Warbler babies, watching ant trails, or shooing monkeys that came to eat guava fruits! I feel proud and privileged to have grown up in such surroundings, and I owe it to the love of my mom and grand mother, without whom I would not have come so far. This research has been supported by funding from Georgetown University, American Arachnological Society, Washington Biologists’ Field Club, Sigma Xi, Animal Behavior Society student grant, American Museum of Natural History (Theodore Roosevelt award) and a NSF dissertation improvement grant, and travel grants from the Center for Environment, Georgetown University. ix TABLE OF CONTENTS Introduction ………………………………………………………………………………1 Chapter 1: Chemical mediation of prey recognition by spider-hunting wasps …….23 Methods…………………………………………………………………………..26 Results…………………………………………………………………………....33 Discussion………………………………………………………………………..36
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