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Identifying measures of emotion in dairy cattle Helen Susan Lambert “In partial fulfilment of its requirement for the award of the degree of Doctor of Philosophy by Publication of the University of Portsmouth” April 2018 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. Signature: 2 Acknowledgements Firstly, I would like to thank World Animal Protection for enabling me to carry out my research whilst under their employment, and for supporting my goals to undertake a PhD by Publication. I am particularly grateful to my co-author Gemma Carder for her support and hard work. I would like to thank all of the staff at Bolton’s Park Farm for their support during data collection. I would also like to thank all of the interns and volunteers who helped with data collection and coding; Dr Alma Massaro, Simone Foister, Lucy McCrae, Hilary Audretsch, Leonardo Rescia, Chanelle Andrenn, Amber Hatch, and Alexandra Thomas. I would also like to thank my supervisors; Dr Leanne Proops and Dr Marina Davilla-Ross for their advice and encouragement on the thesis introduction. Finally, sincere thanks to all of my family and friends for their undying support over the years, particularly my husband who has supported me through every stage, continuously believed in me, and given me the strength to keep going. 3 Abstract The following commentary discusses the six papers submitted for evaluation for the award of PhD by Publication (chapters 1-6). To give context to my contribution to the field of animal welfare science, I have also included several published reviews and extended abstracts as appendices (appendices 1- 6). The research considered in this commentary examined the potential of ear postures, eye whites, and nasal temperatures as measures of both positive and negative emotions in cattle. Three papers focussed on measuring a positive, low arousal emotional state. The paper; “Can ear postures reliably measure the positive emotional state of cows?” (chapter 1, page 44), which was published in Applied Animal Behaviour Science, demonstrated that cows perform two ear postures for significantly longer when they are in a positive, low arousal emotional state, compared with before and after. The second paper; “Nasal temperatures in dairy cows are influenced by positive emotional state” (chapter 2, page 53), which was published in Physiology & Behavior, showed that cow’s nasal temperature drops significantly when they are stroked to induce a positive, low arousal emotional state, compared with before and after. The paper; “Measuring positive emotions in cows: Do visible eye whites tell us anything?” (chapter 3, page 59), also published in Physiology & Behavior, revealed that the percentage of visible eye white is significantly decreased when cows are in a positive, low arousal emotional state, compared with before and after. Papers 4-6 focussed on measuring both positive and negative high arousal emotional states in dairy cows. The paper “Can changes in nasal temperature be used as an indicator of emotional state in cows?” was published in Applied Animal Behaviour Science (chapter 4), page 66), and showed a significant decrease in nasal temperature in cows, in response to stimuli intended to elicit positive and negative high arousal states, compared with a neutral stimulus. Paper 5; “Looking into the eyes of a cow: Can eye whites be used as a measure of emotional state?” (chapter 5, page 73), was also published in Applied Animal Behaviour Science, and found that visible eye white in cows increased significantly in response to the emotional states of excitement and frustration, compared with a neutral stimulus. Finally, paper 6; “Positive and negative emotions in dairy cows: Can ear postures be used as a measure?” (chapter 6, page 80) which has been submitted to Behavioural Processes, demonstrated that cows are more likely to perform certain ear postures in response to positive or negative, high arousal emotional states. Taken together, these findings show that there is potential for ear postures to be used as a measure of emotional state in cattle, although further research is required to explore the effects of other contexts and stimuli. In addition, nasal temperatures and eye whites are not purely the result of arousal levels, as they did not mirror the heart rate measurements, and so further research is needed to explore the complex relationship between arousal and valence. Throughout the whole of the commentary these papers will be referred to, and so it is recommended that the publications are read first. 4 Table of Contents Publications and Presentations 7 Commentary: Identifying measures of emotion in dairy cattle 11 Introduction 11 Chapter 1. Can ear postures reliably measure the positive 18 emotional state of cows? Chapter 2. Nasal temperatures in dairy cows are influenced by 27 positive emotional state. Chapter 3. Measuring positive emotions in cows: Do visible eye 33 whites tell us anything? Chapter 4. Can changes in nasal temperature be used as an 40 indicator of emotional state in cows? Chapter 5. Looking into the eyes of a cow: Can eye whites be used 47 as a measure of emotional state? Chapter 6. Positive and negative emotions in dairy cows: Can ear 53 postures be used as a measure? Discussion of Studies 76 References for commentary 91 Appendix 1. Animal Sentience: Where Are We and Where Are We 99 Heading? Appendix 2: Searching for Animal Sentience: A Systematic Review 115 of the Scientific Literature Appendix 3: Report of an RSPCA / AHVLA meeting on the welfare of 140 agricultural animals in research : Cattle , goats , pigs and sheep 5 Report of an RSPCA / AHVLA meeting on the welfare of agricultural animals in research: cattle , goats, pigs and sheep Appendix 4: Report of the 2014 RSPCA/UFAW Rodent Welfare 145 Group meeting Appendix 5: What is Animal Sentience? 147 Appendix 6: Monkey say, monkey do, monkey grieve? 155 Appendix 7: Jointly Authored Outputs 157 Appendix 8: UPR16 Form 162 6 Publications and Presentations Peer-reviewed Lambert (Proctor), HS and Carder, G. (2016). Looking into the eyes of a cow: Can eye whites be used as a measure of emotional state? Applied Animal Behaviour Science, 186, 1-6. Proctor, HS and Carder, G. (2016). Can changes in nasal temperature be used as an indicator of emotional state in cows? Applied Animal Behaviour Science, 184, 1-6. Carder, G., Proctor, H., Schmidt-Burbacht, J. and D'Cruze, N. (2016). The animal welfare implications of civet coffee tourism in Bali. Animal Welfare, 25(2), 199-205. Proctor, HS and Carder, G. (2014). Can ear postures reliably measure the positive emotional state of cows? Applied Animal Behaviour Science, 161, 20-27. Proctor, HS and Carder, G. (2015). Nasal temperatures in dairy cows are influenced by positive emotional state. Physiology & Behavior, 138, 340-344. Proctor, HS and Carder, G. (2015). Measuring Positive Emotions In Cows: Do Visible Eye Whites Tell Us Anything? Physiology & Behavior, 147, 1-6. Proctor, HS, Carder G, Cornish AR. (2013). Searching for Animal Sentience: A Systematic Review of the Scientific Literature. Animals, 3(3), 882-906. Proctor, H. (2012). Animal Sentience: Where Are We and Where Are We Heading? Animals, 2(4), 628-639. Invited articles and reviewed by the Editor Proctor H. (2014). Animal Sentience. Commonwealth Veterinary Journal. 30(2): 22-26. Proctor H. (2016). Monkey say, monkey do, monkey grieve? Animal Sentience, 4(7). Published extended conference abstracts Proctor, H. & Carder, C. (2014). Measuring positive emotions in dairy cattle. Animal Technology and Welfare. December, 2014. Proctor, H. (2014). Animal sentience: what do we know and why does it matter? Animal Technology and Welfare. April, 2015. Conference proceedings Proctor, H. & Carder, G. (2016). Exploring whether ear postures are a reliable indicator of emotional state in dairy cows. Proceedings of the 50th Congress of the International Society for Applied Ethology 12-15th July, 2016, Edinburgh, United Kingdom. Editors: Dwyer, C., Haskell, M., & Sandilands, V. p180. Proctor, H. (2014). Do ear postures indicate positive emotional state in dairy cows? Proceedings of Measuring Behavior 2014, (Wageningen, The Netherlands, 27-29 August, 2014). Editors: Spink, AJ, Loijens, LWS., Woloszynowska-Fraser, M., & Noldus, LPJJ. p276 Proctor, H. (2014). Do ear postures indicate positive emotional state in dairy cows? Proceedings of the 48th Congress of the International Society for Applied Ethology (Vitoria- Gasteiz, Spain, 29 July- 2 August, 2014). Editors: Estevez, I., Manteca, X., Marin, RH., & Averos, X. p113. Proctor, HS., Carder, G., & Cornish, A. (2013). Looking back to map the future: The road ahead for animal sentience research. Proceedings of Science in the Service of Animal Welfare. Priorities around the world. UFAW, Barcelona, Spain, 4-5 July, 2013. Editors: UFAW. p.83. Proctor, HS and Carder, G. (2014). Do ear postures indicate positive emotional state in dairy cows? Proceedings of Recent advances in animal welfare science IV. UFAW York, UK, 26 June, 2014. Editors: UFAW. p.67. Proctor, HS, Carder, G., & Ribeiro, R. (2013) Looking back to map the future: A review of animal sentience research. Proceedings of the 47th Congress of the International Society for Applied Ethology, Florianópolis, Brazil, 2-6 June, 2013. Editors: Hotzel, MJ., & Fihlo, LCPM. p.123. Carder, G., Proctor, H., & Ribeiro, R. (2013) Animal sentience: Be part of the movement. Proceedings of the 47th Congress of the International Society for Applied Ethology, Florianópolis, Brazil, 2-6 June, 2013. Editors: Hotzel, MJ., & Fihlo, LCPM. p.123. Proctor, HS. (2012) Advancing understanding of animal sentience. Recent advances in animal welfare science III. UFAW, York, UK, 21 June, 2012. Editors: UFAW. p56. Other conference presentations (talks) Proctor, H. and Carder, G.
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