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Coversheet for Thesis in Sussex Research Online A University of Sussex DPhil thesis Available online via Sussex Research Online: http://sro.sussex.ac.uk/ This thesis is protected by copyright which belongs to the author. This thesis cannot be reproduced or quoted extensively from without first obtaining permission in writing from the Author The content must not be changed in any way or sold commercially in any format or medium without the formal permission of the Author When referring to this work, full bibliographic details including the author, title, awarding institution and date of the thesis must be given Please visit Sussex Research Online for more information and further details Social Communication In Domestic Horses: The Production And Perception Of Facial Expressions. Dissertation submitted to the University of Sussex for the degree of Doctor of Philosophy. Jennifer Wathan June 2015 2 I herby declare that this thesis has not been and will not be, submitted in whole or in part to another University for the award of any other degree. Signature……………………………………………………………………………… Jennifer Wathan 3 Acknowledgements First, I would like to thank my supervisor, Karen McComb, for offering me the opportunity to study for this PhD, and for her faith, help, and guidance throughout every stage of this process. I would also like to thank Katie Slocombe, without whom I may well never have begun the formal study of animal behaviour. Countless people assisted me with collecting the data presented in this thesis, including those who allowed me access to their horses - some of the most notable being the staff and volunteers at Albourne Equestrian Centre, Bowler’s Riding School, CHET Centre, Ditchling Common Stud, Glebe Field Equestrian Centre, Hope in the Valley Riding for the Disabled, Plumpton College, and The Diamond Centre. Charlotte Lillis, Becky Spooner, and Chris Wathan also helped considerably in the data collection. Anne Burrows and Bridget Waller were fundamental to the development of EquiFACS. I thank Bridget for her advice in adapting FACS for a non-human animal, and Annie for sharing her anatomical expertise. The school administration team and technicians were always willing to offer their assistance during my studies. My office mates, Thibault Chabert, Kate Grounds, Leanne Proops, Jordan Raine, Graeme Shannon, and Amy Smith offered me their friendship, and Kate, Leanne, and Amy have also provided valuable support in innumerable other ways. Thank you to all my friends and family for their love and support along the way. Emma Green deserves a special acknowledgement for her help in proof reading. Andy Bamford has contributed to greatly to this thesis through providing endless discussions and advice, practical help whenever I was short of assistance, and trips to Madagascar for cherished adventures, if not quite rest and recuperation. A final mention must be given to Barty - for his critical judgement on my experimental protocols, and for constantly reminding me of how much more there still is to learn about how horses think. This research was funded by a studentship from the Biotechnology and Biological Sciences Research Council and the School of Psychology, University of Sussex. A University of Sussex Alumni Travel Grant supported the collaboration with Anne Burrows, which contributed to Article I. 4 Author Contributions The thesis conforms to an ‘article format’ in which the empirical chapters consist of discrete articles written in a style that is appropriate for publication in peer-reviewed journals in the field. The first and final chapters present an introduction to and discussion of the field and the research undertaken. I am the principle author on the manuscripts that form this thesis, and have been responsible for all aspects of the design, implementation, analysis, and dissemination of this research. Karen McComb is listed as senior author on all of the articles to acknowledge the contribution of her expertise and advice to all stages of my work. Other specific author contributions are described below. Article I: Wathan, J., Burrows, A.M., Waller, B.M., & McComb, K. EquiFACS: The Equine Facial Action Coding System. PLOS ONE, in press. AMB contributed to the dissection and recording of the facial musculature of the horse, and identifying the muscular basis of horse facial movements. AMB also provided vital reagents and tools, and provided feedback on the manuscript draft. BMW provided feedback on the study design, assisted in identifying the muscular basis of horse facial movements and their relations to previous FACS, and the manuscript draft. Article IV: Wathan, J., Proops, L., Grounds, K., & McComb, K. Functional use of Facial Expressions in a non-primate: horses discriminate between differing emotions. In the Style of Proceedings of the Royal Society B: Biological Sciences. LP and KG contributed to the design of the experimental protocols, assisted with data collection and analysis, in particular the video coding and heart rate analysis, and provided feedback on the manuscript draft. 5 University of Sussex Jennifer Wathan Doctor of Philosophy Social Communication In Domestic Horses: The Production And Perception Of Facial Expressions. Summary Living in complex societies is thought to promote the development of sophisticated social, cognitive, and communicative skills. Investigating the extent of these skills across taxa is critical to understanding the evolution of the advanced abilities found in some species, including humans. Facial expressions are rich sources of social information for humans and some primates; however whether this is true for other animals is largely unknown. Horses are an ideal study species for these questions: they form valuable social relationships and display some advanced socio-cognitive skills, but are phylogenetically distant from primates and so might be expected to communicate quite differently. Here I present a method for quantifying and coding horse facial movements (EquiFACS), which reveals that horses have an extensive capacity for producing facial expressions. I then utilise EquiFACS to demonstrate that horses produce facial actions that mirror the emotional content of auditory stimuli, providing evidence for a perception-action representation of emotional information. Through my experiments on the perception of facial expressions in horses I show that these expressions display meaningful information to conspecifics, which influences their behaviour in functionally relevant ways. I also shed light on the physiological processes involved in the perception of emotional conspecific facial expressions, showing that viewing negatively valenced conspecific emotional expressions raises resting heart rate. This is indicative of emotional contagion, which may be a mechanism through which information is obtained and social interactions are regulated. Collectively, my research demonstrates the ability to produce and use complex facial expressions as a source of social information is not limited to primates, but is present in at least two phylogenetically distant groups. This suggests these skills may either be an evolutionarily conserved trait or have evolved under common selective pressures. As well as their scientific significance, these findings have implications for horse management and welfare. 6 Table of Contents Introduction ............................................................................................................................... 12 Social Cognition .................................................................................................................... 12 What is social cognition? ................................................................................................... 12 Living in a complex society ............................................................................................... 14 Studying social cognition and communication .................................................................. 15 Section summary ................................................................................................................ 17 Facial Expressions ................................................................................................................ 18 The evolution of facial expression ..................................................................................... 19 Section summary ................................................................................................................ 23 Sensitivity to the Attentional and Emotional States of Conspecifics ................................ 24 Attention ............................................................................................................................. 25 Sensitivity to others’ attention in primates ......................................................................... 26 Sensitivity to others’ attention in non-primates ................................................................. 29 Studying attention following .............................................................................................. 30 Section summary ................................................................................................................ 32 Emotion .............................................................................................................................. 33 Measuring emotional experience........................................................................................ 34 Emotion attribution ...........................................................................................................
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