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The Communicative Function of Self-Directed Behaviours in Macaques

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The Communicative Function of Self-Directed Behaviours in Macaques The communicative function of self-directed behaviours in macaques Jamie Whitehouse Thesis submitted in partial fulfilment of the requirements for the award of the degree of Doctor of Philosophy of the University of Portsmouth. July 2018 Abstract In humans and non-human animals, stress is often linked to observable behaviours (e.g scratching, self-grooming and other self-directed behaviour). The link between stress and these behaviours is widely accepted, but their adaptive value remains understudied and so, the reasons for their production is unclear. Stress behaviours are often highly visual (e.g. scratching, yawning, self-grooming), and so it has been hypothesised that these behaviours may provide information to others. In this thesis I explored the hypothesis that stress behaviours (e.g. scratching) have communicative function, using a non- human primate model genus, the macaques (Macaca). First, I consider how observers perceive the scratching of others, and more specifically, how they are perceived in comparison to neutral, non- communicative behaviour. Macaques attended to the scratching of others more so than neutral behaviours, with this shift in attention being modulated by the degree to which the subject is bonded with the actor. Second, I measured how the macaques responded to the stress of others, comparing social interactions with and without a preceding scratch. The findings of this study demonstrate that producing stress behaviour significantly impacted the likelihood of aggression from others, and led to more peaceful social interactions. Finally, I considered the function of scratching during two other contexts, preceding behavioural change, and as a signal during grooming interactions, however, I found no evidence for a communicative function of scratching in either of these contexts. Overall, this thesis supports the idea that stress behaviour is perceived and responded to by others, providing some of the first evidence to suggest that these behaviours may function communicatively. Ultimately, these data adds clarity as to why stress behaviours have evolved, and why they exist in the behaviour repertoire of many social animals (including ourselves). Contents list Acknowledgements _________________________________________________ 7 Dissemination of research from this thesis ______________________________ 9 List of tables ______________________________________________________ 10 List of figures _____________________________________________________ 11 Chapter 1. General Introduction ______________________________________ 14 1.1 Overview ____________________________________________________ 14 1.2 Stress in human and animal societies ___________________________ 19 1.3 Behavioural markers of stress _________________________________ 21 1.3.1 Form ___________________________________________________ 21 1.3.2 Function ________________________________________________ 24 1.3.3 Applications _____________________________________________ 25 1.4 Social communication ________________________________________ 27 1.4.1 The study of communication ________________________________ 27 1.4.2 Signal evolution and emergence _____________________________ 29 1.4.3 Signals vs. Cues. _________________________________________ 30 1.4.4 Comparative approaches to studying communication _____________ 31 1.5 The macaques (Macaca) ______________________________________ 33 1.5.1 Macaque ecology _________________________________________ 33 1.5.2 Macaques as a model to study stress and communication. _________ 34 1.5.3 An experimental and observational approach ____________________ 35 Chapter 2. Macaques attend to scratching in others. _____________________ 37 2.1 Overview __________________________________________________ 37 2.2 Introduction ________________________________________________ 38 2.3 Methods ___________________________________________________ 43 2.3.1 Subjects and housing ______________________________________ 43 2.3.2 Stimuli and apparatus ______________________________________ 44 2.3.3 Experimental Procedure ____________________________________ 45 2.3.4 Video coding _____________________________________________ 47 2.3.5 Measures of relationship quality ______________________________ 48 2.3.6 Data Analysis ____________________________________________ 49 2.4 Results ____________________________________________________ 50 2.4.1 Influence on rates of scratching ______________________________ 50 2.4.2 Influence on attention to the video ____________________________ 50 2.4.3 Influence on orientation towards group mates ___________________ 54 2.5 Discussion _________________________________________________ 54 Chapter 3. Stress behaviours buffer macaques from aggression. __________ 60 3.1 Overview ___________________________________________________ 60 3.2 Introduction ________________________________________________ 61 3.3 Methods ___________________________________________________ 65 3.3.1 Species and Study Site _____________________________________ 65 3.3.2 Data Collection ___________________________________________ 66 3.3.3 Measures of relationship quality ______________________________ 68 3.3.3 Statistical Analyses ________________________________________ 70 3.4 Results ____________________________________________________ 74 3.5 Discussion _________________________________________________ 81 Chapter 4. Scratching and behavioural transitions in a social primate ______ 85 4.1 Overview ___________________________________________________ 85 4.2 Introduction ________________________________________________ 86 4.3 Methods ___________________________________________________ 90 4.3.1 Subjects and Study Site ____________________________________ 90 4.3.2 Data collection ___________________________________________ 91 4.3.3 Defining behaviour transitions________________________________ 92 4.3.4 Statistical analyses ________________________________________ 93 4.4 Results _____________________________________________________ 94 4.4.1 Scratching around transitions ________________________________ 94 4.4.2 Behavioural contexts eliciting scratching _______________________ 96 4.4.3 Adaptive value of scratching before moving _____________________ 98 4.5 Discussion _________________________________________________ 102 Chapter 5. Exploring the function of grooming signals in a group of free- ranging macaques. ________________________________________________ 107 5.1 Overview __________________________________________________ 107 5.2 Introduction _______________________________________________ 108 5.3 Methods __________________________________________________ 113 5.3.2 Subjects and study site ____________________________________ 113 5.3.2 Data collection __________________________________________ 114 5.3.3 Video extraction and coding ________________________________ 114 5.3.4 Social relationships _______________________________________ 117 5.3.5 Data analysis ___________________________________________ 117 5.4 Results ___________________________________________________ 119 5.4.1 Descriptive statistics ______________________________________ 119 5.4.2 Tests for referentiality _____________________________________ 120 5.4.3 Benign signal hypothesis __________________________________ 122 5.5 Discussion _________________________________________________ 125 Chapter 6. General Discussion ______________________________________ 131 6.1 Overview __________________________________________________ 131 6.2 Main findings and implications _______________________________ 132 6.2.1 Stress behaviours as information ____________________________ 132 6.2.2 Stress behaviours as a signal or cue? ________________________ 134 6.2.3 The role of social relationships _____________________________ 135 6.2.4 Emotional signals within a predictive framework ________________ 137 6.2.5 Scratching as a marker of stress: a word of caution ______________ 138 6.2.6 Scratching outside of the context of stress _____________________ 139 6.2.7 Implications for a comparative approach ______________________ 140 6.2.8 Welfare ________________________________________________ 141 6.3 Future directions ___________________________________________ 142 6.4 Conclusions _______________________________________________ 144 References ______________________________________________________ 145 Appendices ______________________________________________________ 163 Declaration Whilst registered as a candidate for the above degree, I have not been registered for any other research award. The results and conclusions embodied in this thesis are the work of the named candidate and have not been submitted for any other academic award. Word count 37,340 Acknowledgements First and foremost, I would like to thank Prof Bridget Waller and Dr Jerome Micheletta for not only their continuous support and availability throughout my PhD as my supervisors, but for their friendships over the last 4 years. They both have made my time at the University of Portsmouth extremely enjoyable, and I consider any future students of theirs extremely lucky. I would also like to thank my third supervisor, Dr Juliane Kaminski, for her helpful comments and discussion at every stage of my research, and Dr Ed Morrison, Dr Paul Morris, Dr Marina Davilla-Ross, and Dr. Leanne Proops for their comments during annual and major reviews. I would like to thank the Primate Society of Great Britain, for the financial support from the Captive Care Working Party. I am grateful to Don Walser, Terri May, Lisa Simpkins, and the rest of the keepers and staff
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