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Pan Paniscus) UNIVERSITY OF CALIFORNIA, SAN DIEGO Self-Directed Behaviors, Handedness & Lateralization in the Bonobo (Pan paniscus) A Thesis submitted in partial satisfaction of the requirements for the degree Master of Science in Biology by Elysa Anne Everson Committee in charge: Professor David Woodruff, Chair Professor David Holway Professor James Nieh 2011 The Thesis of Elysa Anne Everson is approved and it is acceptable in quality and form for publication on microfilm and electronically: ___________________________________________________________________ ___________________________________________________________________ ___________________________________________________________________ Chair University of California, San Diego 2011 iii This thesis is dedicated to Edna Everson, the best grandma in the world. Who gladly assisted in building a thousand birthday cakes out of sand, who makes the best Mac-N-Cheese on the planet, and who taught me never to give up... iv TABLE OF CONTENTS Signature Page.................................................................................... iii Dedication........................................................................................... iv Table of Contents................................................................................ v List of Figures.................................................................................... vii List of Tables...................................................................................... viii Acknowledgements.............................................................................. ix Abstract................................................................................................ x Introduction............................................................................................. 1 Methods………………........................................................................... 8 Figures................................................................................................... 14 Results.................................................................................................... 20 Discussion............................................................................................... 30 Appendix A [Review of Self-Directed Behaviors in Primates]............ 53 I. Self Directed Behavior Research in Nonhuman Primates.. 53 II. Rank and Dominance Patterns in Bonobos…………...…. 57 III. Captivity as a Source of Stress…………………………. 60 IV. Sex as a Mechanism to Diffuse Stress…………………. 63 V. Bonobo Tool Use and the Effect of Novel Enrichment on SDBs...67 VI. Self-Directed Behavior Research in Humans………..… 70 v Appendix B [Review of the Hypothesized Evolutionary Origins of Cerebrally Lateralized Behaviors........................................... 76 I. Handedness, Brain Lateralization, and Behavioral Response…...76 II. Cerebral Dominance and Functional Brain Asymmetries……… 83 III. Gender effects…………………………………………………... 88 IV. Measuring Handedness and Hemispheric Specialization……… 93 V. The Social-Learning Hypothesis……………………………….. 98 VI. The Prenatal Environment: Hormonal Regulation of Laterality…102 VII. Postural Origin (Bipedalism) Hypothesis………………………109 VIII. Genetic control over Handedness……………………………… 112 IX. Mother-Infant Interaction Asymmetries……………………….. 118 Appendix C [Data Archive Tables]............................................................... 125 References...................................................................................................... 128 vi LIST OF FIGURES Figure 1: San Diego Zoo Bonobo Enclosure........................................... 14 Figure 2: San Diego Zoo Bonobo Enclosure Floor-Plan.......................... 14 vii LIST OF TABLES Table 1: Subjects (Individual bonobo profiles).…………………………………… 12 Table 2: Self-Directed Behavior type definitions…………………………………. 18 Table 3: SDB Target Locations……………….………………………………....... 19 Table 4: Rough Scratches……….………………………………………………… 20 Table 5: Gentle Scratches………..……………………………………………….. 21 Table 6: Unilateral Rubs……….……………….………………………………… 22 Table 7: Bilateral Rubs……………...…………………………………………….. 23 Table 8: Picks………….………………………………………………………… 24 Table 9: Wipes…………….………..……………………………………………... 25 Table 10: Self-Grooming……………..…………………………………………… 26 Table 11: Individual Handedness Scores.…………….…………………………… 28 Table 12: Comparative Individual Handedness Scores….………………………... 29 Table 13: Directional Laterality Results……….….……………………………….. 29 Table 14: Five Levels of Laterality (Marchant & McGrew, 1997)………....….….. 80 Table 15: Extant Data on Hemispheric Functioning………………………………. 81 Table 16: Sexual Dimorphism in the Human Brain (Witelson, 1991)…………….. 92 Table 17: 1996-1997 Video Archive………………………………………….…. 124 Table 18: 2007-2008 Video Archive…………………..………………….....…... 125 viii ACKNOWLEDGMENTS I would like to thank, although I feel like even the most sincere words would only fall short, Dr. David Woodruff. I think I am not alone amongst the students and faculty of UCSD to be touched by David’s patience, humor, compassion, and hope for a better world. His words have reached into the lives of so many students all over the world, and inspired them to realize their own potential and to evaluate their role in this planet in a much more profound and meaningful way. I am just one of many in this respect, and it has been such an honor to work with such a legendary and inspirational man. As an advisor, David saw me through several years (what probably should have been months!) of project changes and edits- with lots of interesting surprises along the way. What I am most thankful for, other than for allowing me to operate a clandestine kitten nursery in his lab, is that David never lost faith in this project. Without David’s support, guidance, and friendship this project would have been as sad and lonely as all those sweet little kittens he refused to adopt. I couldn’t have made it here without him. I would also like to thank Dr. Christine Johnson for her valuable insight with regards to the mysterious eccentricities of bonobo behavior and for helping me set up and guide this project . I’d like to thank David Holway and James Nieh, for being on my committee, and acknowledge all my friends from all over the world who never failed to respond to my frantic e-mails regarding stats and graphics: Daren Eiri, Rebecca Dai, Meg Eckles, Matt Tucker, and Katie LeVan. ix ABSTRACT OF THE THESIS Self-Directed Behaviors, Handedness & Lateralization in the Bonobo (Pan paniscus) by Elysa Anne Everson Master of Science in Biology University of California, San Diego, 2011 Professor David Woodruff, Chair The bonobo, Pan paniscus, originated from central African chimpanzees (Pan troglodytes) 1–2 million years ago and has been used as a model for the ancestral human condition. This study focuses on the handedness and directional lateralization of a set of behaviors known as self-directed behaviors, which are often used as an index of emotional arousal with regards to the stress response. They arise from unconscious defense mechanisms that are thought to serve as arousal-inhibiting systems within the central nervous system during the stress response. This study was based on the nonintrusive videotaping of a group of 10 captive bonobos living at the San Diego Zoo during two periods about ten years apart. 1,174 self-directed behavior events were identified and micro-analyzed, in nearly 20 hours of recorded observation. The directional laterality and population-level handedness x for each self-directed behaviors were calculated, along with individual handedness scores for each bonobo, which were compared to the handedness scores reported previously by others for these same individuals. It was predicted that, on an individual level, there would be a shift away from symmetrical control in the brain of self-directed behaviors. This prediction was confirmed by the observation of several significant individual-level preference determinations in the execution of self-directed behaviors, presumably reflecting a corresponding asymmetrical functional lateralization in the cerebral management of stress. Significant population-level handedness was neither expected nor observed, confirming a lack of population-level bias in this species and supporting the idea that the alignment of lateralization may not be under selective pressure. xi Introduction In this thesis I explore the question of what we can learn from the study of the behavior of our sister taxon, the bonobo, that might enable us to better conserve these now endangered primates. The bonobo or pygmy chimpanzee, Pan paniscus, originated from central African chimpanzees (Pan troglodytes) 1–2 million years ago (Caswell et al., 2008) and has been used as a model for the ancestral human condition based on genomic, anatomical and behavioral evidence (Zihlman et al., 1978; de Waal and Lanting 1997). A few of the remaining 50,000 bonobo have been studied in their native Congo forests (Kano, 1992) but the species is better known from observations of the few hundred apes kept in zoos (Sandin, 2007; Woods, 2010). The well-being of these captive apes is of paramount concern and the focus of a Species Survival Plan organized by the Association of Zoo’s and Aquariums (Reinartz, 1994). Although the public’s imagination was captivated by the bonobos designation as the “make love, not war” species (de Waal, 1995), the welfare and sustainability of the captive populations hinges more on their adaptation to the stresses of confinement than their reproductive behavior.
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