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Vocalization As an Indicator of Individual Quality in the Rock Hyrax

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Vocalization As an Indicator of Individual Quality in the Rock Hyrax Vocalization as an indicator of individual quality in the rock hyrax THESIS SUBMITTED FOR THE DEGREE "DOCTOR OF PHILOSOPHY" BY Lee Koren SUBMITTED TO THE SENATE OF TEL-AVIV UNIVERSITY October 2006 This work was carried out under the supervision of Dr. Eli Geffen and Dr. Ofer Mokady Abstract Vocal communication is used in various systems within and between species. Animals may vocally communicate such messages as an imminent danger, or advertise their social or mating status. Song is almost synonymous with birds and is rarely linked to mammals. In a variety of birds, anurans, insects and a few mammals, different elements of singing have been linked to hormonal levels, social status, body condition, and with reproductive success. Various models have addressed risk taking, decision making and hierarchy formation in social groups. Singing involves high costs in terms of time, energy and predation risk, warranting consequent rewards, such as social status and ultimately reproductive success. The rock hyrax ( Procavia capensis ) is an ideal model to test theories regarding honest signaling and advertising, since hyraxes live in multi-male and female social groups, with polyandrous mating and a low female reproductive skew. Hyraxes are also diurnal, facilitating behavioural observations, and in the Ein Gedi Nature Reserve can also be studied in their natural habitat, which includes predators, competitors, diseases and harsh weather conditions. Acoustic communication constitutes a widely used means of information transfer amongst hyraxes. Both males and females produce alarm calls, yet only some sexually mature males sing. Singers sing almost year round in individually distinct voices, and often counter-sing with neighbours. The purpose of this research was to investigate the relationships between male hyrax songs and individual attributes, such as survival, body condition, hormonal state and social status. This research includes data I have collected over five years of observations and experiments in the field and in the laboratory. I used an interdisciplinary approach, which involved physiological, behavioural and ecological tools to assess the above relationships. Over two hundred and thirty animals were captured and individually marked. Each animal was measured, weighed, and photographed. Hair samples were cut for the hormonal analysis. Field observations of agonistic interactions allowed me to rank animals in terms of social status in five groups. Surprisingly, results showed that in most groups, the most dominant members of the group were females. Females also ranked on average higher than males, and they lived longer than them. Despite that, adult male hyraxes were bigger and in a better physical condition than adult females. Hormones were extracted from hair samples. I essayed the levels of two androgens (testosterone and androstenedione; 'male' hormones), estradiol (a 'female' hormone) and cortisol (a stress hormone). I discovered that females had similar levels as males of both androgens tested. This result is the first of its kind, since female mammals usually have significantly lower testosterone levels than males. The elevated levels in female hyrax may be associated with the female-dominated social organization. Hyraxes seem to defy most mammalian hormonal and social rules, challenging perceptions and necessitating new explanations. Adult cortisol levels were found to be higher in females than in males, perhaps due to the extensive reproductive efforts, which include approximately 230 days of gestation each year. Female social ranks were positively related to cortisol levels, and negatively related to androgen levels and to body condition. Intersexual differences in hormonal strategies arise in pups. Pup mortality in Ein Gedi hyraxes is high for both sexes, yet male pups that survived their first year of life had lower cortisol levels, while females had higher cortisol and testosterone levels, than those who died. Both low male cortisol levels and high female testosterone levels are related to subordination in adults. It is possible that pups, in order to survive, need to signal subordination. Only a third of adult males sing. Singers are on average older and more dominant than non-singers. Singers also have higher testosterone levels and lower estradiol levels, than non-singers. Their cortisol levels, which were related to their social status, were also higher than in non-singers. High ranking singers had higher cortisol levels, similar to the case in females and to other social mammals, possibly due to the risk and stress involved with increased agonistic interactions. I recorded songs from 17 males. Songs were digitalized and analyzed. I focused on three main song elements: wails, chucks and snorts. All songs contained wails and all but one contained chucks, but only songs belonging to 11 (out of 17) males contained snorts. I measured time and frequency related parameters for each song and element. Using discriminate function analysis, each singer was individually recognized, based on these song parameters. I used multiple regressions in order to determine the relationship between specific song elements and male attributes. I found that one song component corresponded to every aspect of male quality I measured, possibly advertising it. For example, age, androgen levels and social ranks, were all related to the snort component. Body size and cortisol levels were associated with the chuck component. Formant frequencies, which are produced by the vocal tract, are associated in hyraxes with fur coverage and social ranks. Taken together, my results suggest that male hyraxes in Ein Gedi advertise their age, body size and condition, hormonal levels and social ranks using song. Singing is expensive in terms of time expenditure and predation risks, and factors that enhance it, such as high hormonal levels, are expensive as well. The benefits expected, in terms of reproductive success, have yet to be assessed, but they must be considered, as well as the potential audiences and their response to the singing. Acknowledgements Thank you To my supervisors: Dr. Eli Geffen and Dr. Ofer Mokady, who held my hand, lent a hand and let go when necessary. Who were brave and secure enough to allow me to find my own way. To my committee: Prof. Uzi Motro, Prof. Yoram Yom-Tov and Prof. Arnon Lotem for their support. To the project students (Liat, Gill, Nati, Modi and Leah), technicians (Beth, Itamar, Oren, Yotam and Enbal), field guides (Ynon, Dafna, Ta'ir, Shimi) and park rangers, for their help in the field. To friends who bravely restrained northern hyraxes (Anat, Tamar and Ofir). To the Israeli Nature and Parks authority for their permission to work in The Ein Gedi Nature Reserve. To the Ein Gedi Field School for their warm hospitality and logistic help. To the Ein Gedi Emergency Rescue Crew (Alon, Eran, and Yakov), for lending me carrying equipment and for securing my ropes. To the beautiful Ein Gedi and Mizpe Shalem women, who danced, shared their lives, friendship and support (especially to Rohik, Saraleh, Chaya and Orna). To Hanita and Yael, who babysat Nour. To Michal, Doron and Yael for their friendship and support while working in the field. To the molecular crew (Zlil, Michal, Ronit, Adar, Tamar and Haggar), for guarding the flame. To my friends in the lab (i.e. the salad club: Anat, Sigal, Sharon, Vered, Tamar, Inbar and Hagar). To Rachel Paz for the support, advice, help and chocolates (and reprimands for eating them). To members of the ex- Institute for Nature Conservation Research, especially to Prof. Dan Eisikowitch, who accepted me for a MSc, and to Dr. Sarig Gafni for the hospitality. To my dad, Prof. Gideon Koren for the help, advice, encouragement and the idea for the hormone analyses. To Tatyana Karaskov and Julia Klein, for their help with the hormone analysis and for teaching me the hair-testing protocol. To Dr. Yuval Zohar, who skillfully dissected the run-over hyraxes with me. To Dr. Noam Leader, Dr. Ofer Amir and Dr. Noam Amir, for their help diving into the acoustic world. To Dr. T. W. Fitch, for helpful formant analyses advice. To Dr. Hans deVries, for his generosity, patience and help with the rank determination, steepness and linearity testing. To Dr. Charlotte K. Hemerlijk, for sharing with me her Matrix Tester program. To my mother, for encouraging me to trust my intuition. To my wonderful sister Tal, who is always there for me, and to her partner Yuval, for all the help. To Amir, who came through whenever no one else could. To all of my extended family, especially to my grandmother who came out and helped me set up Nour in Ein Gedi, and to friends who are part of my family, especially to my 'sisters' Anat and Ronit and my teacher, friend and guide Fifi. To my partner, Avi, for the great love, for the help in the field, for the support at home, and for Nour. To my daughter Nour, who allowed me to work in the field throughout the pregnancy and during her first 2 years of life. Who shares my love of Ein Gedi, helped me capture pups, and asks good questions. To the hyraxes, who emit such funny, fun to work on vocalizations. Also to the leopards, wolves, and hyaenas, and to the floods, that helped make every day in the field a celebration… Thank you all! The extensive field work in this research was very logistically complex. Loads of help was extended to me in every junction. I humbly and truly apologize if I forgot to mention anyone who helped along the way…Thank you very much… Table of Contents Prelude
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