And the Naked Mole-Rat (Heterocephalus Glaber)
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ASPECTS OF OLFACTORY COMMUNICATION IN THE DWARF HAMSTER (PHODOPUS SUNGORUS) AND THE NAKED MOLE-RAT (HETEROCEPHALUS GLABER) A Dissertation Presented to the Faculty of the Graduate School of Cornell University In Partial Fulfillment of the Requirements for the Degree of Doctor of Philosophy by Frank Robert Castelli December 2017 © 2017 Frank Robert Castelli ASPECTS OF OLFACTORY COMMUNICATION IN THE DWARF HAMSTER (PHODOPUS SUNGORUS) AND THE NAKED MOLE-RAT (HETEROCEPHALUS GLABER) Frank Robert Castelli, Ph. D. Cornell University 2017 Olfactory communication is an understudied phenomenon, likely due to human bias against this modality of communication. I expanded our knowledge of olfactory communication by testing the following hypotheses: self-grooming is a form of olfactory communication in the dwarf hamster Phodopus sungorus; naked mole-rats (Heterocephalus glaber) are capable of social-dominance-based discrimination of odor; and rolling behaviors of naked mole-rats function as a form of scent-marking. Self-grooming is ubiquitous among mammals, yet our knowledge of the functions of this behavior beyond cleaning the body surface is limited. Dwarf hamsters were exposed to cotton nesting material scented by same-sex and opposite-sex conspecifics, as well as an unscented control. As predicted, subjects self-groomed more in response to conspecific odor than unscented controls, an important first step in demonstrating communication. Furthermore, self-grooming in response to opposite- sex odor was higher than same-sex odor and unscented controls, which did not differ from each other, suggesting that its communicative function is to attract a mate. Naked mole-rats live in underground eusocial colonies in which social dominance plays important roles in their reproductive division of labor, cooperation, mate choice, and access to food. Three colonies were tested using a T-choice apparatus in which each stimulus arm contained the whole-body odor of one of two fellow colony members that differed in dominance rank. Subjects were tested with several pairs of stimulus odor donors that varied in dominance status, sex, breeding status, and body weight, and subjects were analyzed separately according to sex, breeding status, absolute dominance rank, and relative dominance rank. The overall results were consistent: naked mole-rats mostly preferred to enter the arm containing dominant odor. Naked mole-rats perform rolling behaviors in which an individual’s dorsum contacts the floor, and these behaviors may function in scent-marking. A plastic tube in each of three test colony tunnel systems was replaced on alternating days with a clean tube, to stimulate scent-marking, or a “dirty” tube that had been part of the colony tunnel system for 24 h prior. For both sexes, rolling behaviors were more frequent in the clean than the dirty stimulus tube condition within 2.75 h of tube replacement. BIOGRAPHICAL SKETCH Frank Robert Castelli has a deep passion for nature and the scientific method. He is particularly interested in animal social behavior and evolution. His academic interests have been shaped by many influential educators throughout his life. Frank was born and raised on the border of Brooklyn and Queens, NY by Robert Castelli and Kim Castelli along with his younger brother, Robert. He developed an interest in science in elementary school and became aware that becoming a scientist was a possible occupation in large part due to his love for the Ghostbusters, particularly the character Egon Spengler. He attended high school on Long Island where he developed a more specific interest in biology. During the summer before his senior year of high school he worked in the laboratory of Ivan Chace at SUNY Stony Brook studying winner and loser effects in cichlid fish. He continued to work with Dr. Chase on a project investigating ant foraging and recruitment to food sources which won Honorable Mention at the Long Island Science Congress. Soon after high school graduation, he was living in Nevada collecting stickleback fossils in the desert with SUNY Stony Brook researcher Michael Bell. In the fall he matriculated into the Honors College of SUNY Stony brook and worked on fossilized bird regurgitations in Dr. Bell’s lab. During his sophomore year, he worked in the lab of Douglas Futuyma rearing beetle and moth larva on plants with photosynthetic mutations. In the following summer, Frank took a rainforest biology course in Costa Rica and a primate biology course in Nicaragua in which he studied iii howler monkeys. In the fall of 2002, Frank transferred to the College of Agriculture and Life Sciences at Cornell University where he first studied naked mole-rats in the lab of Paul Sherman. The following summer, Frank studied the Utah prairie dog with John Hoogland of the University of Maryland, College Park. Frank graduated magna cum laude with a Bachelor of Science in Biology and helped the Cornell Men’s Fencing Club win the national club championships. After graduating from Cornell, he continued to work with naked mole-rats in Dr. Sherman’s lab and did a small project on tailless whip scorpions with Linda Rayor in the Entomology Department. Dr. Rayor taught him to become a passionate outreach speaker of spider biology which helped him overcome his arachnophobia. Frank went on to study prairie voles in the lab of Nancy Solomon at Miami University in Ohio where he learned to trap rodents in the field and genotype in the laboratory. He returned to Cornell for graduate school as a Sage Fellow and joined the lab of Robert Johnston where he earned a Masters in Psychology and a Psychology Department Teaching Award on his way to finishing his Ph. D. in Behavioral Evolutionary Neuroscience. Subsequently, Frank has joined the lab of Catherine Marler in the Psychology Department of the University of Wisconsin-Madison studying the social behavior of California mice. iv In memory of Robert E. Johnston, supportive mentor and kindred spirit. v ACKNOWLEDGMENTS I foremost thank my parents for supporting my academic pursuits throughout life. From making sure my homework was done to paying for field courses in foreign countries, my parents have nurtured my interests and lovingly supported my endeavors. I posthumously thank my original committee chair, Robert E. “Bob” Johnston for his encouraging support. Bob was one of several great professors who helped shaped my thinking about evolution and animal behavior and one of the people who influenced me to become an academic and pursue a Ph. D. I sincerely thank my special committee: Thomas A. Cleland, Paul W. Sherman, Robert A. Raguso, and David A. Pizarro. I am appreciative of Thom Cleland for taking me on as a student after Bob’s passing and for the support, encouragement, and mentorship necessary to help me through to completion. I am especially thankful to Paul W. Sherman for contributing to my inspiration to be a scientist, for introducing me to naked mole-rats, for passing down his lab to me, and providing support and mentorship so that I could finish my research and degree. I am thankful to Rob Raguso for helping to steer my ship steadily forward, for providing mentorship and valuable feedback for my research. I thank David Pizarro for his advice, help, and support. I thank Linda S. Rayor and Cole Gilbert for being wonderful unofficial advisors and friends. I am grateful for the emotional support provided by my friends at Cornell, including Joan Johnston, Marcela Vargas-Peters, Kristina O. Smiley, Matt Herndon, SiWei Luo, Marissa Rice, Ramon Velazquez, Tali Iwanir, and many others. vi I thank Alex G. Ophir for advice and unofficial mentorship, and I thank his entire lab for advice, training, and support. Many undergraduates have assisted my research over the years and I am very thankful to them all. I am grateful to Alaina Uhouse, Adefolakanmi Adenugba, and Zach Lodato for assisting with the work presented in this dissertation. Fantastic statistical training from Françoise Vermeylen was heavily applied in this dissertation, but any possible errors are solely attributable to me. I am thankful to many for logistical support. Ned J. Place and Leann Kanda provided dwarf hamsters and Rochelle Buffenstein traded naked mole-rats. Wendy O. Williams and the Cornell veterinary staff helped to keep my animals healthy. Tim L. Van Deusen, the Uris Hall and Mudd Hall animal care staff provided excellent service. John C. Howell was patient while helping to maintain the naked mole-rat colony environmental controls. Gary L. Oltz was incredibly helpful with designing and creating behavioral apparatuses and training in workshop and tool use. I thank the faculty and staff of the Psychology and Neurobiology & Behavior Departments who have helped in so many ways. I am very grateful to all those who influenced me to pursue a career in academia, especially the Cornell Fall 2002 Animal Behavior BIONB-221 lecturers: Elizabeth Adkins-Regan, Jack Bradbury, Thomas Eisner, Stephen T. Emlen, H. Kern Reeve, Thomas D. Seeley, Paul Sherman, Sandra Vehrencamp, and Charles Walcott. vii TABLE OF CONTENTS Biographical Sketch ....................................................................................................... iii Dedication ....................................................................................................................... v Acknowledgements ....................................................................................................... vi Table of Contents .......................................................................................................