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New Reports That Monarch Butterflies BEHAVIORAL ECOLOGY OF PARASITOID DIET BREADTH AND INSECT DEFENSES A DISSERTATION SUBMITTED TO THE FACULTY OF THE GRADUATE SCHOOL OF THE UNIVERSITY OF MINNESOTA BY CARL MATTHEW STENOIEN IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF DOCTOR OF PHILOSOPHY ADVISOR: DR. KAREN S. OBERHAUSER JULY 2017 i © Carl Stenoien 2017 ii Acknowledgements I am deeply gracious for the contributions of many people to my graduate studies and this dissertation. First and foremost, thank you to Karen Oberhauser, who gave me all of the trust and freedom I could handle, yet was always there to help when I asked for it. You were incredibly generous with your time and provided me with many valuable opportunities, including conferences, travel, and colleagues. Thank you to my committee, George Heimpel, Emilie Snell- Rood, and Marlene Zuk. You provided feedback on my ideas, welcomed me into your lab groups, lent me space and equipment, and helped me to learn and grow as a scientist. I’ve been lucky to be a part of several intellectually stimulating communities. Within the Monarch Lab, thanks to Kelly Nail and Eva Lewandowski for lighting the way, to Patrick Pennarola, Julia Leone, Ami Thompson, Laura Lukens, and Kyle Kasten for friendship and productive conversatopms and to Wendy Caldwell, Katie-Lyn Bunney, Sarah Weaver, and Cora Ellenson-Myers for bringing balance to our group our research efforts to new audiences. Thank you to my peers and friends in EEB, especially members of Behavior Group, the Snell-Rood Lab (Meredith Steck, Megan Kobiela, Sarah Jaumann), and benevolent post-docs (Eli Swanson, Eric Lind, Heath Blackmon). Thank you to my external collaborators, especially Shaun McCoshum, Myron Zalucki, Stephen Malcolm, Dara Satterfield, Dan Papaj, and all the citizen scientists who contributed data and insights to my work with Pteromalus cassotis. Finally, thank you to reviewers of my manuscripts and grant proposals, especially Lincoln Brower and Michelle Solensky (Chapter 1) and Georgiana May (DDF proposal). Maintaining several colonies of plants, caterpillars, and parasitoid wasps simultaneously requires more time and resources than I could muster, and my deepest gratitude goes to all the undergraduates and volunteers who kept our little zoo alive: Rebecca Meyer, Joe Miller, Lauren Henrich, Laura Lukens, Dane Elmquist, Peter Xiong, Giulia DeLuca, John Lundquist, Charlie Jackson, Bradley Kelly, Sophia Crospby, Teal Johannson, Sylvia Durkin, Douglas Ayega, Andrea Gruver, Cameron Swenson, Olivia Fitch, Fiona Lennox, and Kadie Gullickson. This work would not have been possible without various funding sources. I am incredibly thankful for the National Science Foundation, the University of Minnesota, the EEB Grad Program, the Bell Museum of Natural History (Florence Rothman Fellowship, James W. Wilkie Fund for Natural History Fellowship, Richard and Judi Huempfner Ruffed Grouse Fellowship, iii Dayton Bell Museum Fund Fellowship), the Animal Behavior Society, and the Howard Hughes Medical Institute for believing in my work and providing the means to accomplish it. Finally, thank you to my family and friends, many of whom helped with field and lab work and many more who caught the monarch bug, so to speak. Thanks to my parents for showing me the beauty in nature, the value of grit, and teaching me that the quality of an answer received is proportional to the quality of the question proposed. Finally, thank you to Karen Stenoien, who provided encouragement, patience, critical feedback, and many hours in the lab and field as the self-appointed unpaid intern. Thank you all! iv Dedication To the most rarely-observed, under-appreciated, and misunderstood creatures inhabiting this pale blue dot. I hope that revealing your stories will bring out the best in us. v Abstract One of the primary challenges animals face is consuming enough nutrients of sufficient quality that they might realize their reproductive potential. In response to this challenge, many strategies have evolved, varying in the types and specificity of the foods consumed. Why do some animals consume a variety of foods (generalists), while others have extremely narrow diets (specialists)? What causes these divergent strategies to evolve? These questions form a central, yet unresolved theme of biology. To address them, I’ve used comparative studies rooted in behavioral ecology, chemical ecology, and natural history to better understand how physiological and behavioral trade-offs might limit a species’ diet breadth. My work utilizes two closely related parasitoid wasps that attack butterfly pupae: Pteromalus puparum, reported to attack over forty hosts in the field, and P. cassotis, an apparent specialist on monarch butterflies. Parasitoid wasps are an ideal group for studying the evolution of diet breadth strategies because they are hyper-diverse, ecologically ubiquitous, and have enormously variable host ranges, even amongst closely related species. Individual endoparasitoids spend their entire larval development inside of a single insect host, almost always killing this host before emerging as free living adults. Therefore, a common measure of a parasitoid species’ diet breadth is its range of suitable host species. In Chapter 1, I provide the first detailed reports of parasitism of monarch butterfly pupae by P. cassotis. Using field experiments in the northern U.S. and observational data from wild- collected pupae in the southern U.S., we report occurrences and brood characteristics of this host- parasitoid interaction across a broad geographic area. I also discuss several lines of evidence which suggest that P. cassotis is a specialist on monarchs. This chapter serves as a starting point for conservation-related investigations of the potential impacts of P. cassotis on monarch populations, which have declined severely in recent decades. In Chapter 2, I test multiple hypotheses regarding the potential merits and trade-offs associated with the evolution of generalist versus specialist dietary strategies. Using no-choice trials, female P. cassotis and P. puparum were presented ten butterfly species as potential hosts. I measured each species preference for, and performance on each host. Our results supported the preference-performance hypothesis, but did not support the trade-off hypothesis. As predicted by the novel diet breadth mistakes hypothesis, the generalist was more likely than the specialist to accept unsuitable hosts, while the specialist was more likely than the generalist to reject suitable hosts. The frequency of these mistakes in nature is unknown. These findings suggest that foraging vi mistakes may not only be consequences of diet breadth strategies, could also reciprocally influence the evolution of such strategies. This research has implications for organisms in rapidly changing environments and parasitoid-based biological control because it demonstrates that specialist foragers may retain the physiological ability and evolutionary potential for host switches, while generalist foragers may cause difficult-to-measure non-target mortality. Not all hosts were found to be suitable for the development of a either parasitoid, and those hosts known to sequester plant defense compounds into their own bodies were especially likely to be unsuitable. In Chapter 3, I investigate the potential role of milkweed butterflies’ sequestered cardenolides as a defense mechanism against parasitoids by testing the preference and performance of P. cassotis and P. puparum on milkweed butterfly pupae containing high, low, or zero sequestered cardenolides. More toxic monarchs were more likely to survive encounters with the specialist, but only because this wasp was less likely to attack more toxic hosts. After attack, neither host survival nor the emergence of parasitoids was affected by host toxicity, although the specialist produced smaller broods and experienced lower survival on more toxic hosts. P. puparum was unable to develop in monarchs of high or low toxicity, and was also unsuccessful when attacking a cardenolide-free danaid butterfly, Euploea core, though it frequently killed both species. These findings do not rule out the possibility that sequestered plant toxins may be one mechanism preventing successful parasitism of monarchs by the generalist, but suggest that other mechanisms are also involved. The challenge of consuming an optimal diet inspired the first three chapters of this dissertation. In Chapter 4, I investigate the opposing side of this challenge: avoiding mortality caused by natural enemies. In conducting the work that makes up the first three chapters of this dissertation, I observed butterfly larvae and pupae performing behaviors that I hypothesized to be defensive in nature, such as choosing protected pupation sites, color matching, and vigorous wiggling when contacted by a parasitoid. Insect pupae are relatively immobile and are often presumed to be highly vulnerable to natural enemies. In fact, previous reviews of insect defenses had only briefly considered morphological and physiological aspects of pupal defense, but the role of behavior in pupal defense had largely been ignored. In Chapter 4, I attempt to fill this gap in the literature. By bringing together dozens of studies showing that insect pupae likely benefit from a variety of behaviors performed before pupation (by the larva or pre-pupa), behaviors of the pupa itself, and behaviors of conspecific and heterospecific individuals. Some of these behaviors include the construction of protective enclosures
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