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Avian Diet and Visual Perception Suggests Avian Predation Selects for Color Pattern Mimicry in Bumble Bees

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Avian Diet and Visual Perception Suggests Avian Predation Selects for Color Pattern Mimicry in Bumble Bees AVIAN DIET AND VISUAL PERCEPTION SUGGESTS AVIAN PREDATION SELECTS FOR COLOR PATTERN MIMICRY IN BUMBLE BEES BY JOHN M. MADDUX THESIS Submitted in partial fulfillment of the requirements for the degree of Master of Science in Entomology in the Graduate College of the University of Illinois at Urbana-Champaign, 2015 Urbana, Illinois Master’s Committee: Professor Sydney A. Cameron, Chair, Director of Research Professor Andrew V. Suarez Assistant Professor Michael P. Ward ABSTRACT Mimicry theory was developed by H. W. Bates and F. Müller based on their observations of similarities among butterflies, and since publication their theories have been used to explain numerous other mimicry systems. Bumble bees can be found in throughout the temperate parts of the word, as well as the high mountains and polar regions. In any given area, the local bumble bee species tend to share the same color patterns. Statistical confirmation of these trends has resulted in the hypothesis that these similarity groups are Müllerian mimicry rings. Bumble bee color patterns are thought to convey protection from avian predators, thus creating selection for fewer, more effective color patterns. Evidence for birds as predators of bumble bees primarily comprises logical arguments bolstered by only a few laboratory studies and empirical accounts. Although the hypothesis that birds are bumble bee predators driving the evolution of Müllerian mimicry is well reasoned and has some evidential support, strong experimental data are lacking. To test the effects of bumble bee color pattern on avian attack frequency, I created bumble bee models from soft plasticine with local, novel, and non-aposematic color patterns. I then presented these models to birds in the field using presentation apparatus to simulate bumble bees in flight and foraging on flowers; despite numerous attempts to optimize the apparatus, however, models were not effectively engaged by birds and statistically significant trends were not detected. A larger sample size may be needed, or the presentation system may require further modification. Requisite to birds displaying preferences with regard to bumble bee color patters, is that birds are major predators of bumble bees in nature, which has not been conclusively shown. To investigate this premise, I recruited the assistance of bird banders from across the country as collaborators in the collection of dietary samples from a large number of birds representing ii multiple species. I then designed and conducted a PCR assay to detect the presence of bumble bee tissue in the samples. Samples yielding electrophoresis bands were sequenced for verification. My results indicate widespread bumble bee predation across multiple bird species. Many of these birds have large populations and distributions, suggesting that they are able to exert significant selective forces on bumble bee populations. The large number of individual birds and bird species found to consume bumble bees provides strong affirmative evidence for the claim that birds are bumble bee predators and possible participants in the evolution of mimicry groups. I found bumble bee predation to be more likely in older birds, contrary to what would be expected if learned avoidance of bumble bees was occurring. The relationships between birds and bumble bees appears to be complex and conform poorly to general trends such as “birds avoid bumble bees.” Mimicry theory has been applied to bumble bees to explain the observed color pattern similarities in species with overlapping geographical distributions. All research in this area is based on the human-centric observation that these similarity groups exist. Animals possess diverse visual systems, however, and it should not be taken for granted that predators of bumble bees, no matter what they are, see the same color pattern convergence that humans do. I asked the question of whether birds’ perceptions of bumble bee color patterns are likely to parallel our own. To test this, I used reflectance spectroscopy to measure bumble bee color patches and generated hue scores based on avian color perception. I then compared these scores to human- assigned color classifications and found strong statistical association between human and avian perception of bumble bee colors. I also found that white bumble bee color patches consistently display relatively high ultraviolet reflectance invisible to human, but not avian, eyes. Consistent association of ultraviolet reflectance with only white color patches suggests that this reflectance iii does not add variation to bumble bee coloration that humans cannot perceive. I conclude that existing studies indicating color pattern convergence in bumble bees based on human vision are likely valid from the avian visual perspective, as well. My analysis of bird dietary samples show that birds are eating bumble bees in large numbers sufficient to result in powerful selection for color pattern convergence in bumble bees if foraging preferences based on color pattern exist. Additionally, reflectance data indicate that human-observed groups of bumble bees with similar color patterns are seen by birds, indicating that birds could be generalizing these patterns to create functional mimicry rings. The question remains, however, of whether birds learn to recognize and avoid bumble bees in the wild. My experiments were unable to demonstrate any effects of coloration on avian attack rates in the field, while my examination of the effects of age on the likelihood of finding bumble bee tissue in a birds’ diets showed a pattern inconsistent with that expected in a mimetic system. While I have shown that birds play a significant role in the ecology of bumble bees, and that putative bumble bee mimicry rings are visible to birds as well as humans, the role of birds in creating these mimicry rings remains uncertain. iv ACKNOWLEDGMENTS The first and most important person I want to thank is my advisor, Dr. Sydney Cameron, for her continued support and encouragement. Under her mentorship, I have transitioned from a novice biology student to a true scientist and naturalist. I appreciate her boundless patience, her honest criticism, and her sound advice, all of which she has given freely. As a role model, Sydney embodies what a scientist should be: informed, dedicated, driven, and ethical. But more than that, Sydney has shown me that creativity and imagination are integral to the scientific profession, and that studying the natural world is a human endeavor, one predicated on passion, curiosity, and insight. Many academics measure the success of their students in securing academic positions and research programs of their own. Although my own career follows a different path, Sydney has ever been supportive, developmental, and invested in my education. Sydney has been many things to me, including teacher, advisor, supervisor, and editor, and has been a major contributor to the high quality of my education at Illinois. For that she has my eternal thanks, and will forever be a mentor and a friend. My labmates deserve a special thank you as well. Over the past three years they have been the core of my professional community, supporting my work and encouraging my continued growth. Michelle Duenness has been a teacher, sounding board, and role model to me for the duration of my graduate education and merits a special mention for her patience and dedication. I also thank Kyle Parks, Charles Dean, Andrew Debevec, Dr. Diana Arias-Penna, Dr. Haw Chuan Lim, and Dr. Jim Whitfield. Thank you to my committee for sharing their time and expertise with me, and without whom this work would not have been possible. Dr. Mike Ward brought an ornithological v perspective that I severely lacked. Dr. Andy Suarez, on the other hand, is one of the most broadly knowledgeable ecologists I have ever known. Thank you both. Leah Benuska was my undergraduate laboratory assistant for the last year of my research, and I cannot convey how grateful I am for her assistance. Leah was as hard and diligent a worker as any graduate student I have known, though she did it all for no financial compensation and little academic recognition. The hundreds of hours she spent in the lab proportionally reduced my workload, and without her my research would not exist in its current form. I wish her the best as she moves into the professional field, and congratulate whoever employs her next. During the course of this project many people have offered their resources, expertise, and advice. I want to thank these individuals now: Drs. Becky Fuller, Sönke Johnsen, Paul Marek, Chia-Ching Chu, and Page Fredericks. The department staff have been an invaluable and unending source of support for my work, and also of friendship; thank you to Audra Weinstein, Adrienne Harris, and especially Kimberly Leigh. In turn, you have all been influential and wonderful parts of my time at Illinois; I only wish I could begin to repay you. My friends in the program have been a continual source of comfort, joy, and support, without which I would long ago have suffered a nervous breakdown. Thank you to Selina Ruzi, Tom Schmeelk, and Tanya Josek for reminding me to take time for fun. I also thank my wife, Whitney, for being an inexhaustible source of support and encouragement. She stood by my side as I moved us to Illinois, worked nights and weekends on research, and stressed and fretted about results. Her strength gave me strength, and I am fortunate to have found such a dedicated partner in this life. The Entomology Department at Illinois consistently enjoys national recognition, and it is not hard to see why. The intellectual atmosphere here is collaborative, innovative, and vi developmental. It is with total honesty that I tell prospective students that this is a wonderful place to study, and I feel so fortunate for ending up in this department for my graduate education. Thank you to Dr. May Berenbaum for her part in creating this academic environment, as well as for the personal support and encouragement that she shows to all of her students.
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