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Cooley, J. R. 1999. Sexual Behavior in North American Cicadas of The Sexual behavior in North American cicadas of the genera Magicicada and Okanagana by John Richard Cooley A dissertation submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy (Biology) The University of Michigan 1999 Doctoral Committee: Professor Richard D. Alexander, Chairman Professor George Estabrook Professor Brian Hazlett Associate Professor Warren Holmes John R. Cooley © 1999 All Rights Reserved To my wife and family ii ACKNOWLEDGMENTS This work was supported in part by the Horace H. Rackham School of Graduate Studies, the Department of Biology, the Museum of Zoology (UMMZ), the Frank W. Ammerman Fund of the UMMZ Insect Division, and by Japan Television Workshop Co., LTD. I thank the owners and managers of our field sites for their patience and understanding: Alum Springs Young Life Camp, Rockbridge County, VA. Horsepen Lake State Wildlife Management Area, Buckingham County, VA. Siloam Springs State Park, Brown and Adams Counties, IL. Harold E. Alexander Wildlife Management Area, Sharp County, AR. M. Downs, Jr., Sharp County, AR. Richard D. Alexander, Washtenaw County, MI. The University of Michigan Biological Station, Cheboygan and Emmet Counties, MI. John Zyla of the Battle Creek Cypress Swamp Nature Center, Calvert County, MD provided tape recordings and detailed distributions of Magicicada in Maryland. Don Herren, Gene Kruse, and Bill McClain of the Illinois Department of Natural Resources, and Barry McArdle of the Arkansas State Game and Fish Commission helped obtain permission to work on state lands. Keiko Mori and Mitsuhito Saito provided funding and high quality photography for portions of the 1998 field season. Laura Krueger performed the measurements in Chapter 7. Artwork in Chapters 7 and 8 is by Melissa Anderson, Dan Otte, and John Megahan. iii I thank Charles L. Remington for introducing me to the complexities of Magicicada, Oren Hasson, Tom Moore, Mark O’Brien, and Dan Otte for helpful discussion, and Chris Simon, for her pioneering genetic surveys of 13- year cicadas and our conversations about cicadas. Andrew Richards has been instrumental in the project to map the distributions of periodical cicada broods in central Illinois. Although little of that information is included in this thesis, Andrew’s meticulous work and careful thinking have been an important component of all our various and ongoing cicada projects. My development and maturation as a graduate student were strongly influenced by the members of my doctoral committee, Richard D. Alexander, George Estabrook, Brian Hazlett, and Warren Holmes. None of this work could have been possible without the nearly 40 years of effort of Richard D. Alexander. I thank Dick for reigniting my early interest in periodical cicadas. Most of the techniques, approaches, and questions in this work can be traced back to Dick, and the discovery of the new Magicicada species and the female wing flick signal are the legacies of his pioneering bioacoustical studies and his admonition to watch and measure everything. It was at Dick’s suggestion that we followed the behaviors of individually marked females kept separate from males except while under direct observation, allowing us to observe the complete male-female rapprochement sequence. What makes Dick uniquely unique is that he has an uncanny ability, and a proven track record, for being right about how things work. Dick has been tireless in his support, profound in his suggestions, and unwavering in his commitment to seeing that this work meets high quality standards. My friends David C. Marshall and Deborah Ciszek have also provided irreplaceable support, input, and collaboration. The fieldwork in this thesis is the joint collaborative effort of David and myself. The pronoun “I” in this thesis is but a formality; all “I’s” are truly “We’s.” As a collaborative team, we have accomplished far more than we could have separately, and it has been a joy to work with as insightful, iv careful, and thorough a partner as David. This collaboration has been an important part of my own intellectual development. My thanks would not be complete without considering my family. I thank my parents, Rickie and Bill Cooley, for valuing education above all else, my brothers Bill and Jamie for their interest and technical expertise, my grandmothers, Frances S. Cooley for her determination, and Jane H. Yager for her creativity and patience, and my grandfathers, William H. Cooley for teaching me practical ways to construct things, and Richard S. Yager, for instilling in me a love of the strange, the natural, and the absurd. My wife, Louanne Reich Cooley, is a constant source of support. She designed an inexpensive and portable flight cage, contributed her knowledge of northern Michigan to the studies of Okanagana, and has been incredibly patient and understanding throughout this process. Last, I thank my study organisms. They lead bizarre lives—but then, so do we! v PREFACE Sexual behavior in North American cicadas of the genera Magicicada and Okanagana by John Richard Cooley Chairman: Richard D. Alexander. The dense, raucous, mass emergences of North American periodical cicadas (Magicicada spp.) have attracted scientific study since the 17th century. Periodical cicadas are unique in their combination of long life cycles (13- or 17- years) and synchronous development, leading to periodical emergences of adults. Although their long life cycles make it difficult to conduct a longitudinal study of any one periodical cicada population, because populations in different regions of eastern North America are divided into asynchronous “broods,” or year classes, in almost any year, it is possible to study Magicicada. Over four years, I collected natural history information and studied the mating behaviors of 13- and 17- year Magicicada and two species in a non-periodical genus, Okanagana. vi Chapter 1 is a review chapter, and it owes a major intellectual debt to my experiences as a co-author of a book chapter1 about the evolution of insect mating systems. As I became involved in that project, and as I started to construct my thesis, I realized that I would have difficulty discussing mate choice unless I clarified for myself, at least, the nature of mate choice. In this chapter, I review the reasons, starting with asymmetries in parental investment, why mates should be choosy. I continue with discussions of how sexual conflicts of interest shape mating systems, and the kinds of choice mechanisms and criteria invertebrates are most likely to employ. I conclude with some predictions about possible mechanisms and functions of mate choice in periodical cicadas. Chapter 2 is largely a methodological chapter. I present data demonstrating that the methods I used to mark and confine cicadas were not likely to cause mortality or behavioral changes that would bias my studies. Chapter 3 is a brief examination of “seminal plugs” in Magicicada. These structures are usually left behind in the female genital opening after mating. I demonstrate that these structures contain DNA and are likely composed of dried ejaculate, not other specially constructed or secreted materials. Seminal plugs do not prevent future mating attempts, but I suggest that they may be the products of antagonistic coevolution between females who are time-limited and males who can reduce threats to their paternity by imposing time-costs on females’ future mating attempts. 1 Alexander, R. D., D. C. Marshall, and J. R. Cooley. 1997. Evolutionary Perspectives on Insect Mating. Ch. 1 in B. Crespi, J. Choe, eds. The evolution of mating systems in insects and arachnids. Cambridge University Press. vii Chapter 4 tests two hypotheses for female multiple mating in Magicicada: Females remate either to replenish depleted supplies or to effect postcopulatory mate choice. I demonstrate that interrupting a female’s mating tends to promote remating, while matings with an inappropriate, conspecific mate do not. Further, mated females do not actively seek additional mating opportunities, nor are they sexually attractive to males. Interrupted females, however, solicit second matings. These results are most consistent with the hypothesis that females remate for replenishment, and they disprove the hypothesis that females use postcopulatory choice mechanisms to make species-level mating decisions. Chapter 5 documents a previously unknown female wing flick signal, used by females to signal sexual receptivity. No such signal has previously been reported in North American cicadas, although similar signals are known in some Australian and New Zealand species. This chapter documents the signal in different Magicicada species and also describes a bizarre effect (behavioral bisexuality) of a fungus disease in males, as well as a specialized, competitive signal males use to “jam” the acoustical signals of interloping rivals. The newly described behaviors allow formulation and testing of a hypothesis for the two-part calling songs of Magicicada species such as M. septendecim . The two-part structure of these songs facilitate female discrimination of an individual male’s call against a background chorus. Chapter 6 describes a new 13- year species, Magicicada neotredecim. M. neotredecim male calling songs and female mate acceptance criteria are distinct from those of the similar, synchronic and partially sympatric species, M. tredecim. Perhaps the most compelling piece of evidence that M. neotredecim and M. tredecim are separate species is that M. neotredecim has undergone reproductive
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