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Anthrozoology

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Anthrozoology Human–Animal Interactions in Domesticated and Wild Animals ED I T ED BY

Geoff Hosey and Vicky Melfi

1

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1 Great Clarendon Street, Oxford, OX2 6DP, United Kingdom Oxford University Press is a department of the University of Oxford.

It furthers the University’s objective of excellence in research, scholarship, and education by publishing worldwide. Oxford is a registered trade mark of Oxford University Press in the UK and in certain other countries © Oxford University Press 2019 The moral rights of the authors have been asserted First Edition published in 2019 Impression: 1 All rights reserved. No part of this publication may be reproduced, stored in a retrieval system, or transmitted, in any form or by any means, without the prior permission in writing of Oxford University Press, or as expressly permitted by law, by licence or under terms agreed with the appropriate reprographics rights organization. Enquiries concerning reproduction outside the scope of the above should be sent to the Rights Department, Oxford University Press, at the address above You must not circulate this work in any other form and you must impose this same condition on any acquirer Published in the United States of America by Oxford University Press 198 Madison Avenue, New York, NY 10016, United States of America British Library Cataloguing in Publication Data Data available Library of Congress Control Number: 2018959590 ISBN 978–0–19–875362–9 (hbk.)

ISBN 978–0–19–875363–6 (pbk.)

DOI: 10.1093/oso/9780198753629.001.0001 Printed in Great Britain by Bell & Bain Ltd., Glasgow Links to third party websites are provided by Oxford in good faith and for information only. Oxford disclaims any responsibility for the materials contained in any third party website referenced in this work.

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This book is dedicated to Erin and Jemima, who have given the two of us such wonderful HARs.

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Preface

It is likely that nearly everyone in the world encounters animals on a regular basis. Many of us own pets, who may be companions in our homes, or else we have friends or family members who have pets. Then there are people who work in animal-related occupations, such as farmers, zookeepers, ­researchers and vets, who encounter animals daily in their jobs.

Finally, we might encounter animals around town, or in our gardens or on trips into the countryside; we might even deliberately seek them out, through wildlife tourism or visits to the zoo. In all of these scenarios we have some sort of interaction with those animals, and in time these interactions might develop into Human–Animal Relationships. And, it seems, the effect of those relationships is often to change our lives and those of the animals we have relationships with.

Over the past four decades there has been increasing interest in exploring just what those relationships are like, and what sorts of effects they have on the interactants’ lives. At first this interest was driven primarily by researchers studying companion animals or agricultural animals, but more recently the field has expanded to include research in other contexts as well: in laboratories and zoos, and in the wild. What this research is telling us is that the lives, the well-being and the welfare of both humans and animals can be affected by whether these relationships are good and positive, or poor and negative.

Alongside this growth in research there has been an accompanying growth in courses at colleges and universities, where relationships between humans and animals can be studied from a variety of perspectives. As a discipline, this area of study is sometimes referred to as ‘Anthrozoology’, and sometimes

as ‘Human–Animal Studies’. Contributions to this discipline can come from a variety of perspectives: biological, psychological, sociological, anthropological, economic, philosophical . . . and more. It is truly multidisciplinary. And it can focus on a variety of animals which have different roles within our society: pets, farm animals, laboratory animals, ­animals in zoos and animals in the wild.

Until now, however, there has been very little crossing of boundaries by people working in these different contexts and with these different perspectives.

There has been some borrowing of concepts between different areas, but often the research from a particular concept is published in journals and disseminated in conferences which are not routinely seen by workers within other contexts. Because of this, we thought it would be fruitful to collect together reviews of the current state of knowledge in each of these different contexts, written by leading authorities in the field, and this book is the result. The aim of this is not just to summarise how much we know about human– animal relationships in these different contexts, but also to try to identify whether there are any common underlying concepts and principles, what the implications for humans and animals are and what research ­priorities we should have in future, across the whole span of our relationships with animals.

Writing about such a wide field requires expert input from a number of different authors, and we are grateful to the contributors who have supplied us with the chapters that make up this book. We would like to thank Bethany Kershaw, our editor at Oxford University Press for her support and her endless patience with us, and also Ian Sherman at OUP, who encouraged us to do this in the first place.

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P r e fa c e

We would also like to thank Andrew Walmsley for allowing us to use one of his wonderful photos for the front cover; the photo captures the critically endangered Sulawesi crested black macaques in their native habitat being viewed by wildlife tourists.

Wildlife tourism is just one of the threats to the future survival of this species, which the conservation programme Selamatkan Yaki are working to mitigate. On a personal note, Vicky Melfi would like to thank Edward and Isabel, for their support.

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Contents

Contributors 1

xiii

Introduction Geoff Hosey & Vicky Melfi

1

1.1 Introduction 1.2 Defining what we mean 1.3 What is the distribution of HARs through the animal kingdom?

1.4 Why do we care about HAI, HAR and HAB?

1 1 5 8

2. Companion animals James A. Serpell 2.1 What is a companion animal?

2.2 A brief history of companion animals 2.3 Companion animals today 2.4 The benefits of companion animal ownership 2.5 Indirect benefits of companion animals 2.6 The costs of companion animal ownership 2.7 Conclusions and future areas of research 3. Agricultural animals Susanne Waiblinger 3.1 Historical and present role of agricultural animals for humans 3.2 Human–animal interactions and human–animal relationships in agriculture 3.3 Effects of the HAR on animal and human welfare and on productivity 3.4 Wider ranging implications for society and environment 3.5 Future areas for research 3.6 Concluding remarks Box 3.1 Animals, humans and the environment Werner Zollitsch 4. Human–animal interactions in the research environment Kristine Coleman & Allison Heagerty 4.1 Introduction 4.2 Animals in research facilities

17 17 17 19 22 25 26 27 32 32 35 41 48 49 51 33

59 59 60

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Contents

4.3 Implications of human–animal interactions 4.4 Wider implications of human–animal interactions 4.5 Future areas for research 5. Zoo animals Samantha Ward & Sally Sherwen 5.1 Context 5.2 Implications of HAI in this context 5.3 Wider ranging implications for society and the environment 5.4 Future areas for research 5.5 Conclusions 6. Wild animals and tourists Ralf Buckley 6.1 Introduction 6.2 Species and roles 6.3 Human–animal interactions 6.4 Social and environmental implications 6.5 Conclusions and future research priorities Box 6.1 Local private tourism contributions to conservation of wild animals Box 6.2 Global contributions of park tourism to threatened species populations Box 6.3 Population viability analysis to calculate net outcomes of ecotourism on threatened species Box 6.4 Key factors in tourist experiences during encounters with wild animals Box 6.5 Some examples of close-range tourist encounters with wild animals 7. Human–animal relationships in the urban wild Seth Magle 7.1 Introduction 7.2 Animals in urban areas 7.3 Types of human–animal interactions 7.4 Implications of human–urban wildlife interactions 7.5 Wider implications of urban wildlife–human interactions 7.6 Future areas for research Box 7.1 Human–macaque interactions Anne Kwiatt

67 73 74 81 81 84 93 95 98 104 104 104 106 114 114 107 108 109 111 112 119 119 119 123 128 133 134 124

8. The importance of HAIs, HARs and HABs Vicky Melfi & Geoff Hosey

142

8.1 Introduction 8.2 The HAR: a single phenomenon?

8.3 The costs and benefits of HARs 8.4 Building a HAR

142 142 146 148

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Contents

8.5 The HAB: why would animals form bonds with humans?

8.6 What can HARs tell us about society?

8.7 Dominion: duty of care or a resource for our use?

Box 8.1 Starlings: friend or pest?

Index

xi

150 153 155 143 163

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Contributors

Ralf Buckley holds the International Chair in Ecotourism Research at Griffith University, Australia, and is also Distinguished Visiting Professor at the Institute for Geographical ­Sciences and Natural Resources Research of the Chinese Academy of Sciences. He is a natural and social scientist, focussing on practical mechanisms for conservation of biodiversity, and has published twelve books and more than 300 journal a­ rticles.

Kristine Coleman is an Associate Professor and Head of the Behavioral Services Unit at the Oregon National Primate Research Center. After receiving her PhD in Behavioral Ecology at Binghamton University, she went to the ONPRC for her postdoctoral training and has been there since. She has been studying the behaviour and welfare of nonhuman primates for over twenty years.

Allison Heagerty received a BS in Biological Anthropology and PhD in Animal Behavior at the University of California, Davis. She has been working with nonhuman primates in the research environment since 1998. She is ­currently a Senior Research Associate at the Oregon National Primate Research Center, where she manages social housing of rhesus macaques.

Geoff Hosey was Principal Lecturer in Biology at the University of Bolton until his retirement in 2005, and is now Honorary Professor there. His experience of undertaking research and ­supervising students has mostly been in ­behavioural biology, animal welfare and ­primatology, and he is still involved in research on zoo animal welfare, particularly about ­human–animal relationships in the zoo. He is

a member of the BIAZA Research ­Committee and is one of the authors of the textbook Zoo Animals:Behaviour, Management and Welfare (Oxford University Press, 2nd edition 2013).

Anne Kwiatt is an anthropologist and primatologist, interested in socioecology and behaviour, urban wildlife ecology and the application of cross-disciplinary methods to research. ­During her undergraduate and graduate training at the University of Notre Dame, New York ­University, and University of Texas at San ­Antonio, she ­researched the impact of u ­ rbanisation on macaque diets in Singapore and Gibraltar.

Currently, Anne is the research coordinator of the Lester E. Fisher Center for the Study and Conservation of Apes at the Lincoln Park Zoo in Chicago, where she manages the behavioural research programmes for the ape, chimpanzee and Japanese macaque populations.

Seth Magle is an urban wildlife ecologist who has studied animals living in cities for more than fifteen years. He has a Master’s degree from the University of Wisconsin and a ­Doctorate from Colorado State University. He currently directs the Urban Wildlife Institute at the Lincoln Park Zoo in Chicago, and serves as the executive director of the Urban Wildlife ­Information ­Network, a global initiative to study wildlife in cities around the world. His vision is to help to create a planet on which urban ­areas are a valuable resource for the ­conservation of biodiversity.

Vicky Melfi is currently the Principal Lecturer in Human–Animal Interactions at Hartpury University, Gloucestershire, UK. She has gained almost thirty years’ experience working professionally

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C o n t r ib u to r s

in animal welfare and conservation, in the UK at Drusillas Zoo Park, Whitley Wildlife Conservation Trust, in Ireland at Dublin Zoo, in Australia at the Taronga Conservation Society and finally founding the conservation programme Selamatkan Yaki in Sulawesi, Indonesia. She has also held various academic appointments, notably at the Universities of Exeter, Plymouth and Sydney.

Vicky is a passionate ­advocate of professional/ academic collaborations to gather data which can underpin evidence-based practice, to better understand human–­animal interactions, which will lead to great animal welfare and conservation outcomes.

James A. Serpell is the Marie A. Moore Professor of Animal Ethics & Welfare at the School of Veterinary Medicine, University of Pennsylvania, USA. His research and teaching focus on veterinary ethics, the behaviour and welfare of dogs and cats and human–animal interactions.

He has published more than 170 articles and book chapters on these and related topics, and is the author, editor or co-editor of several books, including Animals & Human Society (1994), In the Company of Animals (1986, 1996), Companion Animals & Us (2000) and The Domestic Dog: Its Evolution, Behavior & Interactions with People (1995, 2017).

Sally Sherwen is an animal welfare scientist based at Zoos Victoria (Melbourne Zoo, Werribee Zoo and Healesville Sanctuary in Australia). There, she develops and coordinates research programmes to facilitate evidence-based management in animal welfare at the organisation. A particular area of interest for Sally is the field of Human–Animal Relationships in zoo-housed species. Her PhD focussed on better understanding the visitor effect in previously unstudied groups of animals, including meerkats, penguins and kangaroos. In addition to human–animal relationships in zoos, other areas of research ­interest include investigating novel approaches to animal welfare assessment, evaluating cognitive enrichment programmes and the use of technology to advance animal welfare science.

Susanne Waiblinger is a veterinarian specialising in ethology, animal husbandry and animal wel-

fare science (Dipl. ECAWBM – AWSEL).

She is Associate Professor at the Institute of Animal Husbandry and Welfare of the ­University of ­Veterinary Medicine in Vienna, leading the group of human–animal relationships, ruminant behaviour and welfare, and started to work in these fields more than t­ wenty-five year ago. Besides human–farm ­animal relationships, her research also focusses on the interactions of ­environment, social behaviour and welfare in dairy cows and goats, including ontogenetic aspects, as well as on on-farm assessment of animal welfare in ruminants.

Samantha Ward is a Senior Lecturer in Animal Science at Nottingham Trent University. Previously, Sam worked as a zoo animal keeper of various hoofstock, primate and macropod species.

Sam then went on to an MSc in Animal Behaviour and then a PhD in Animal Behaviour and Welfare. Following this, she was a zoo conservation and research manager with animal record (ZIMS), animal transportation and studbook responsibilities. Sam’s research has focussed on animal behaviour and welfare, with particular focus on zoo animals and the impacts of human–animal interactions (HAI), human–animal relationships (HAR) in zoos and zoo animal husbandry and management techniques, to investigate impacts and improve captive welfare.

Werner Zollitsch is Professor for Sustainability of Animal Production Systems and current Head of Department of Sustainable Agricultural Systems at BOKU-University of Natural ­Resources and Life Sciences, Vienna. He has twenty years of research experience in studying effects of feeding strategies on various aspects of different animal production systems, including organic and low input systems. His main research interests include analysis and ­optimisation of livestock systems, with a focus ­on ecological indicators of sustainability and their interactions with farm characteristics and other elements of sustainability. He is also involved in research and teaching organic livestock production with a focus on sustainability and feeding strategies.

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C H A PT ER 1

Introduction Geoff Hosey & Vicky Melfi

1.1 Introduction Where do we start to investigate and describe Human–Animal Relationships? With a current world human population of 7.3 billion (United Nations 2015), and 83% of the total land surface directly influ­ enced by human activities (National Geographic News 2002; see Figure 1.1), there can be few animals who have not interacted with people at least once during their lives. And these animals cover a multi­ tude of different species with different behaviours and different ecologies. We have also brought many millions of animals into captivity, in agriculture, laboratories and zoos, as well as to live with us as companion animals. Different species of animals living in these varied contexts may have different experiences of humans; the people who interact with these animals may also have different experi­ ences in these varied contexts. But it is ­legitimate to ask whether there are any underlying commonalities or general principles which can help us to explain and understand the processes and consequences involved when animals and people regularly inter­ act with each other. This search for commonalities is a major theme of this book. But firstly we should consider exactly what we mean.

1.2 Defining what we mean Perhaps the first thing to say is that we are very aware that humans are animals too. But repeated use of ‘nonhuman animals’ is cumbersome, and the phrase

‘human–nonhuman animal interaction’ is even more cumbersome. Furthermore, there is something of a divide between human and nonhuman animals in terms of the relationships described here. If it were up to the animals it’s likely that most of the interactions and relationships described in this book would not happen; in a sense they are forced on animals by our behaviour, and it’s i­ mportant for us to determine how our contact with animals affects their lives. For these reasons we will continue to use the terms ‘human’ and ‘animal’ as the two components of these relationships.

1.2.1 HAS, HAI, HAR and HAB Study of the interface between humans and animals is truly interdisciplinary, and can involve a variety of approaches including ethological, psychological, anthropological, sociological, historical, ethnograph­ ical, economic, legal and philosophical. Collectively, these approaches constitute the field of Anthro­ zoology defined as ‘the scientific study of human– animal interaction (de Mello 2012). The area of Human Animal Studies (HAS) ‘explores the spaces that animals occupy in human social and cultural worlds and the interactions humans have with them’ (de Mello 2012). An alternative but similar definition is that HAS ‘embodies a sustained ­interest in understanding and analysing how we humans relate to and make sense of other species’ (Birke & Hockenhull 2012). Often used synonym­ ously, these terms to some degree reflect a discipline bias; Anthrozoology more commonly used in the

Hosey, G. and Melfi, V., Introduction. In: Anthrozoology: human–animal interactions in domesticated and wild animals.

Edited by Geoff Hosey and Vicky Melfi: Oxford University Press (2019). © Oxford University Press.

DOI: 10.1093/oso/9780198753629.003.0001 1

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ANTHROZOOLOGY

Figure 1.1 Most the Earth’s surface is impacted by humans; with a large proportion being used for agriculture (WWF 2016; CC-BY-SA Hannah Ritchie & Max Roser).

natural sciences and HAS in the humanities. By this definition anthrozoology is a more restricted field than HAS, and corresponds more closely to the approach taken in this book. There is less about the wider approaches to human–animal relationships in this book; rather our authors have concentrated on what Birke & Hockenhull (2012) have referred to as a ‘micro-level’ approach, describing and analys­ ing interactions and relationships at the level of individual dyads, or in cases where this is unfeas­ ible, at a group or population level.

There has been a long tradition, dating back to the 1970s, of using this micro-level approach to investi­ gate relationships between companion animals and their owners (Hosey & Melfi 2014), and much of this research has been concerned with the benefits pet owners accrue from interaction with their animals, spawning a new sub-discipline of Animal Assisted Intervention (Griffin et al. 2012). Since the 1980s

there has also been a substantial research effort into understanding the relationships between animals kept for agriculture and their stockpersons, and a major goal of this research has been to determine how these relationships affect the welfare, and in turn the prod­ uctivity, of the animals (Hosey & Melfi 2014). So these two major approaches have different preoccupations and largely different goals; they are also different from each other in their use of terminology. A survey of the literature showed that 49% of agricultural papers in this field used the term ‘human–animal rela­ tionship’, whereas only 5% used the word ‘bond’.

In contrast, 53% of companion animal papers used the word ‘bond’, and only 14% used the term ‘human– animal relationship’ (Hosey & Melfi 2014). Indeed, throughout the whole of anthrozoological research there is inconsistency and ambiguity in the use of terms, and it has been suggested that this hinders progress in this field (Griffin et al. 2012).

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INTRODUCTION

(a)

3

(b)

Figure 1.2 Similar positive interactions with different animals: a zoo keeper and pet owner initiating positive brushing with white rhinos and cats (a) Photograph from Katharina Herrmann, and (b) photograph from ID 84287241 © Vladans, Dreamtime.com.

Three widely used terms in particular would ­ enefit from pinning down to hard definitions: b human–animal interactions (HAIs), human–animal relationships (HARs) and human–animal bonds (HABs).

These words are often used vaguely in the literature, with HARs and HABs frequently being used as though they are interchangeable. Furthermore, all three are used to describe phenomena at the macro level (i.e. population, group, species or society level) as well as the micro level (individual animals and people), even though they likely mean something dif­ ferent at each of these levels. The most fundamental of these terms is the HAI, as these effectively form the units out of which HARs and HABs are constructed.

A human–animal interaction (HAI) is a dyadic event in its most basic form, that is, it’s an event between two individuals, one an animal the other a human. A good starting point is Hinde’s (1974, 1976) work on human–human interaction, which can eas­ ily apply to human–animal interaction too. His con­ ception of an interaction is ‘a sequence in which individual A shows behaviour X to individual B, or A shows X to B and B responds with Y’ (Hinde 1976).

An advantage with this definition is that as well as being conceptual (defining the phenomenon), it is also operational in that it helps us to identify interactions in our research by drawing attention to the outcome of the interaction (i.e. behaviour Y, B’s response). Thus we need not be unduly concerned about whether behaviour X was intentional or not (always a prob­ lem in describing animal ­communication), neither

should we worry too much about what X was (if we missed it), because Y identifies and quantifies the interaction for us.

At the end of an interaction each member of the dyad is likely to have learned something about the other. We can thus envisage that if the same two interactants meet again, their responses to each other’s behaviours might be slightly different from their first meeting; and if they continue to have interactions with each other they might attain such familiarity that they can start to anticipate what the other is likely to do (e.g. Figure 1.2). They now have a relationship. Hinde, then, sees a social relation­ ship as the consequence of ‘a series of interactions over time between two individuals known to each other’ (Hinde 1987, p. 24). Again, this can apply to dyads where one interactant is human, the other an animal, in other words a human–animal relation­ ship (HAR). Many other descriptions of HARs follow this sort of reasoning; for example, Sanders (2003) says that relationships are composed of ‘routine and patterned interactions’. What if the two inter­ actants do not meet again, but continue to have interactions with others who are different each time?

Most animals, including humans, are able to gen­ eralise their knowledge about a variable stimulus by picking out the stimulus features which are sali­ ent to them. Thus we can envisage that an animal or person repeatedly encountering other animals or people of a general category will build up a gener­ alised ‘view’ of that category, and perhaps have a

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4

ANTHROZOOLOGY

characteristic response to members of that category.

Thus, those of us who don’t own a dog may never­ theless sometimes interact with other people’s dogs, and it may be that we gradually come to respond to them in a fairly consistent way because we have a generalised view of what dogs are like and what they do, based on the varied interactions we have had with them. Similarly, animals in a zoo interact with lots of different members of the public, and as a result have generalised expectations of what zoo visitors are likely to do, meaning that they can respond to these people in a consistent way (Hosey 2008). In these cases we can regard the individual as having a generalised HAR, but although this can be the result of interaction with lots of different individuals, the HAI is still the basic unit of the relationship. Going one rung up from the micro to the macro level, we can envisage that both interactants in a HAR are cat­ egories which generalise; this, for example, might describe the relationship between crop farmers and the elephants who raid their crops, or the way sub­ urban commuters view urban fox populations.

What, then, is a human–animal bond (HAB)?

Hinde (1974) defined a social bond as a ‘mutual, affective, emotional attachment between two indi­ viduals that is relatively long lasting and survives temporary separations’. This sort of definition is also appropriate where one of the individuals is an animal, and this has been formalised for a HAB in a frequently used definition from the American Veterinary Medical Association (AVMA 1998): ‘The human–animal bond is a mutually beneficial and dynamic relationship between people and animals that is influenced by behaviors that are essential to the health and well-being of both. This includes, but is not limited to, emotional, psychological, and phys­ ical interactions of people, animals, and the envir­ onment’. The main characteristics of the HAB have been identified by Russow (2002) as (i) that it is a relationship between two individuals, (ii) that it is reciprocal and persistent and (iii) that it promotes a feeling of well-being in both parties. Conceptually this is straightforward; you can’t have a generalised HAB, it has to be between one animal and one person, and both must experience the feelings of well-being that go with it. Practically it is far from straightforward. Most studies assume the presence of a bond from human behaviour, without explicitly

testing for it in the animal (Hosey & Melfi 2014).

Emotional attachment and feelings of well-being can be measured without too much difficulty in human subjects, but showing them in an animal is a differ­ ent matter entirely. But this is something which needs to be addressed if anthrozoology is to be truly scien­ tific (see Figure 1.3).

It might be asked, does it matter? Is there any real reason why we need to distinguish HARs from HABs? We believe it does matter, for a number of ­reasons. Firstly, it is important in science to be explicit and precise in our use of terminology, as this is how people know exactly what it is we’re referring to.

Secondly, our use of words can influence our percep­ tion of the world; in this case our descriptions of our relationships with animals can affect our ethical stance towards them as well as our perceptions of them as social partners (Anthony 2003; Boivin et al. 2003). For example, we might view HAB forma­ tion as desirable between companion animals and

Figure 1.3 Though it might be difficult to empirically determine a reciprocal human–animal bond, there are many relationships which, qualitatively, appear to fit the definition. Photograph from Jane Williams.

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INTRODUCTION

their owners, because some might consider that the whole point of pet ownership is to enhance wellbeing (Serpell 1986); but we might also think that HABs between zookeepers and their animals should be discouraged because an emotional distance might be seen as desirable between people and ‘wild’ ani­ mals (Hosey et al. 2018).

1.2.2 Relationship quality We can, then, envisage the HAI, HAR and HAB along a quantitative dimension (time) and also a qualitative dimension which encapsulates those feelings of attachment and well-being, and this is illustrated diagrammatically in Figure 1.4. HARs result from an accumulation of HAIs over time, but whether a HAR needs time to develop into a HAB is unclear, so the two have been drawn at similar places on the time axis. Good quality HAIs (e.g. friendly, calm and gentle interactions, or rewarded interactions) result in a good quality HAR, as meas­ ured both by its inputs (those good quality HAIs) and also by its consequences (e.g. more relaxed, less stressed interactants). But Figure 1.4 could also be drawn as a mirror image, with a descending nega­ tive qualitative axis. Some HAIs are negative (e.g. aggression, violence) and can lead to negative

5

HARs. The quality of the HAR is thus the conse­ quence of the net quality of preceding HAIs. Finally, the quality of HAIs is itself influenced by a number of variables, including the perceptions and attitudes of the person or animal, and their previous experi­ ence of interacting with that or similar interactants.

This is summarised in Figure 1.5, which shows that the positivity or negativity of an HAI changes the perceptions and attitudes of the recipient of that interaction, with the result that their response to it may similarly become more negative or more posi­ tive. In Figure 1.5 the dark arrows show the inter­ actants moving towards a negative HAR, while the pale arrows show them forming a positive HAR.

1.3 What is the distribution of HARs through the animal kingdom?

A number of interesting questions arise about HARs and possibly other inter-specific relationships and their distribution in the animal kingdom. Are there limitations about which kinds of animals are capable of HAIs, HARs and HABs? And do inter-specific relationships similar to HARs occur between nonhuman species, and if only with humans, why should that be?

+ve

HAB

HAR

Qualitative measures

HAI Neutral Quantitative measures Figure 1.4 Hypothetical relationship between human–animal interactions (HAI), human–animal relationships (HAR) and human–animal bonds (HAB). ‘Quantitative measures’ is a time axis, showing repeated contact between interactants. ‘Qualitative measures’ is meant to represent an increase in well-being or emotional attachment. So repeated HAIs, if they are positive, lead to the formation of a positive HAR. If this HAR eventually involves increased well-being and emotional attachment in the interactants, we can regard it as a HAB.

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ANTHROZOOLOGY

Attitudes, perceptions and experience

–ve effect

+ve effect

Human

Behaviour

+ve HAI

–ve HAI

Behaviour

Attitudes, perceptions and experience

Animal

Figure 1.5 Summary of how reciprocal HAIs of different quality lead to different quality HARs. The positivity or negativity of a HAI influences the attitudes and perceptions, and hence the behaviour, of the recipient, such that positive HAIs are likely to generate reciprocal positive HAIs, leading to the establishment of a positive HAR, and likewise for negative HAIs.

1.3.1 Distribution of HARs among animals It seems reasonable to assume that for interactions and relationships to develop between humans and animals, animals need to be sufficiently similar to and share some commonalities with humans, if for no other reason than that social interactions and relationships need to be communicated and under­ stood by both parties. The extent to which these com­ monalities extend within the animal kingdom is not clear, because it is unclear what these commonalities need to be. It seems reasonable to suggest that a shared geography is a pre-requisite, as both parties need to meet in order to interact and meet repeat­ edly for a relationship to develop. As already men­ tioned, repeated interactions might occur between

the same person and the same animal, or the same person and different animals (of the same species), or the same animal and different people, as we would expect the outcomes of the repeated interactions to be generalised by species and a HAR formed on the basis of these.

Aside from shared geography and the creation of opportunities for these interactions to occur and relationships to develop, what other commonalities might be needed? The animals need to be receptive to initiating, receiving and responding to social cues with humans. Communication can operate on many different levels and use different modalities. For example, human communication is often categorised as visual, auditory and kinaesthetic (­tactile); describ­ ing modalities that people are often more receptive

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INTRODUCTION

to and fluent in. Other species can often communi­ cate using modalities or ranges we can’t appreciate, i.e. using colours we can’t see, like ultra-violet vision in some bird and fish species (reviewed, Land 2018), vocalising in sounds outside of our hearing range or using magnetic fields in sensory communication (Hill et al. 2017). There are, however, many species who use communication cues which we are able to appreciate, such as vocalisations which can be detected by human ears and behavioural changes we can see. We can also detect more subtle com­ munication cues, including changes in skin colour­ ation, respiration rate and body posture shown by different species. When we consider the many dif­ ferent species with whom we can communicate, it becomes apparent that the scope for interactions and relationships between humans and animals is quite vast.

Alongside the need to be able to communicate effectively, animals need to have sufficient cognitive agility to recognise individual humans and/or generalise different people as humans. This task has been demonstrated in many different nonhu­ man species (reviewed, Smith et al. 2016). Cheney & Seyfarth (1992) explored how vervet monkeys Chlorocebus pygerythrus were able to categorise, and adjust their behaviour accordingly, to different threats in their environment, i.e. snakes and eagles.

And these capabilities are not just the domain of primates, farm animals have also been demonstrated to show cognitive categorisation skills, e.g. dwarf goats Capra hircus (Meyer et al. 2012). However, for a HAB to develop the animal would also need the capacity for experiencing emotion, as the definition of a bond requires that both parties experience a posi­ tive affective state resulting from their HAR. Until recently, the concept of animal emotion has been debated with some scepticism (Wemelsfelder 1997).

But more and more empirical studies are demon­ strating that animals have emotions like us, or a similar phenomenon which functions in the same way (Mendl et al. 2010). For example, rats have been shown to giggle when t­ickled (Panksepp & Burgdorf 1999).

As humans we are incredibly anthropocentric, a bias which influences which animals we prefer, as well as the scientific questions we ask, and how we determine to answer them (Fraser 2008; Batt 2009).

7

When we consider HAIs, HARs and HABs, most ­ eople start from a position where humans are p ­considered to have superior capabilities and/or skills to other animals (e.g. http://freakonomics. com/podcast/animal-economics/). These superior capabilities have historically been considered to set people apart and ahead of other animals (Suddendorf 2013). We revere capabilities which we believe ‘make us human’ and demonstrate that we are ‘more’ than animals. Interestingly, the list of capabilities which separates us from other animals has declined over time, as science has deepened our knowledge of animals’ capabilities. And this is despite scien­ tific endeavour being anthropocentric with regard to testing whether animals share the capabilities we revere, and if they do, to what extent; rather than testing to see what capabilities they have, which we might not. Language, tool use, culture and morality were all considered uniquely human traits. But increasingly, research on primates, birds and fish, as well as other species, has demonstrated that these and other capabilities are shared and expressed in our animal relatives (Suddendorf 2013). However, as this area is subject to continual debate, it may be easier to consider what capabilities are required in ‘other’ animals to interact, develop relationships and experience bonds with us humans.

When we think about the range of animals with whom humans might develop relationships, most people would probably consider these to be restricted to animals that are like us. And what animals are like us? Primates are often noted for their high degree of genetic relatedness to humans and commonalities in their social behaviour (de Waal & Ferrari 2012). It is not a big leap from this to consider other mammals and birds too, which have also been observed to show high levels of social and cognitive complexity, so maybe they are sufficiently similar to us for HAI, HAR and HAB too? And why stop there? Studies of reptiles, and to some extent amphibians, also find problem solving, parental care, play and complex sociality (Burghardt 2013).

1.3.2 Relationships between (nonhuman) animals As far as we can tell, humans are the only species which keeps other species as pets for companionship

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ANTHROZOOLOGY

or social support (see Chapter 2). And although apparent ‘friendships’, which we might regard as animal–animal relationships similar to HARs, do occur in both wild and captive animals, they are unusual and not part of any systematic speciestypical pattern (Dagg 2011). This raises a number of questions about the ontogeny or evolution of these behaviours in humans, which are not currently answerable, but which are best approached in a multi-disciplinary way.

As mentioned in Section 1.2.1, HAS are multidisciplinary for a very good reason: different discip­ lines can help us to understand different aspects of HAIs, HARs and HABs. There are different perspec­ tives we can use to understand why people develop HARs as a consequence of repeated HAIs. In psych­ ology, learning theory suggests that reinforced behaviours are repeated, whereas punished behav­ iours diminish over time. Adopting this psycho­ logical perspective, we might venture that HARs develop where repeated HAIs result in consequences (reinforcement); positive interactions result in posi­ tive relationships and potentially bonds, whereas negative interactions result in negative relation­ ships and no HAB. Considering this same issue from a behavioural ecological perspective, we might explore whether other animals engage in and experience inter-species interactions and relationships, and whether they experience bonds. And importantly, if these interspecies behaviours do occur, do they bestow an evolutionary advantage which might explain why we too engage in these behaviours? Or are they costly, making their evolution unlikely other than in particular circumstances?

An anthropological or sociobiological perspec­ tive might enquire whether humans are predis­ posed towards these inter-species interactions: are these HAIs, HARs and HABs intentional and sought out or a result of opportunistic interactions? The eminent sociobiologist E.O. Wilson suggested that people were especially drawn to nature, a phe­ nomenon he termed biophilia (Wilson 1984). And it certainly makes sense that this fascination and love of nature might include animals, which are part of nature, and thus we might expect people to be receptive to communicating with other animals.

1.4 Why do we care about HAI, HAR and HAB? HAS are multi-disciplinary because their ramifica­ tions are far reaching, and thus to fully appreciate their influence different metrics and perspectives are necessary. It is not surprising, therefore, that we should care about HAIs, HARs and HABs for many different reasons; and as humans, these centre on how interactions with animals affect our lives and the lives of other people. It is likely that there are few, if any, people whose lives are unaffected by interactions with animals, directly and indirectly. And it is true that few animals live without interaction with or con­ sequence from human actions and activity. HAIs, HARs and HABs are far from new. Unsurprisingly, HAIs are not new and can be seen in the earliest human historical records that exist, almost 40,000 years old, depicting animals and humans (the latter are mostly represented as hand prints) in rock paint­ ings in Sulawesi, France and Spain (Marchant 2016).

Subsequently, records of HAI are intertwined with our evolution and cultural development and stratifi­ cation (Serpell 1986; Encyclopedia.com 2018). An extreme example of this co-evolution can be found in our species relationship with dogs. The consequence of this species-level relationship appears to have resulted in humans and dogs being predisposed to relate to one another. Different mechanisms which support human–dog relationships include: dogs being especially good at reading human social ges­ tures (Hare & Tomasello 2005); they appear to under­ stand not only dog emotions but also human mental states and respond appropriately to them (Miklosi et al. 2000, 2004; Albuqerque et al. 2016); and import­ antly humans can interpret dogs’ emotions from their vocalisations (Faragó et al. 2017). With this shared history, it seems far from surprising that HAS has developed. What is peculiar is that this widespread interest in HAS seems to have recently risen substan­ tially; evidenced in the popular literature, emergence of new HAS courses, publication within peer review and changes in legislation which reflect and acknowledge both parties. This could represent a hopeful move towards people considering their rela­ tionship with animals and the world more generally; so that happy, healthy and sustainable HARs can be developed (Knight 2015; WWF 2016).

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INTRODUCTION

1.4.1 Financial incentives The interactions and relationships between humans and animals have been dynamic over time and by species, where animals represent food, religious idols, companions and much more. As previously mentioned, HAS spans many different academic disciplines, so establishing a focus can be complex.

A historical review of HABs suggested that in the last couple of decades, funding, programmes and research have focussed on the importance of human– animal interactions on human health and well-being (Hines 2003). Hines (2003) suggests that this has resulted from funding from the pet industry. It is probably fair to say that an appreciation of the eco­ nomic consequences of interactions with animals has been responsible for stimulating different foci in HAS. HAIs, HARs and HABs all have direct financial costs associated with them; for instance, financial advantage, as well as improved well-being for people and animals, can be gained in agricultural produc­ tion when positive HAIs are applied (Waiblinger et al. 2006; reviewed Chapter 3). While it is difficult to estimate the direct financial implications of HAIs and HARs within agriculture and other contexts, they are embedded in the success of these industries; they would not operate without animals. Consideration of the financial worth of these industries, or aspects

9

of them, can provide an indication of the financial value of HAIs and HARs to them. For example: the global animal agricultural industry was estimated to be worth more than $3 trillion in 2016 (WHO 2018); sustainable wildlife tourism was estimated to gener­ ate more than $600 billion in tourism revenue in 2015 (Twining-Ward et al. 2018; see Figure 1.6); the pharma­ ceutical industry, which is one of several industries using laboratory animals, was valued at about $300 billion dollars in 2015 and predicted to rise to $400 billion dollars within three years (Peggs 2015); the pet food industry in the USA alone generates more than $100 billion annually (reviewed Chapter 2); and the financial contribution zoos made to the USA and Australia was estimated at $22.5 billion in 2016 and $434 in 2009, respectively (AZA 2018; Aegis 2009).

Certainly, there are many reasons why we should be interested in HAIs, HARs and HABs, not least that it could prove expensive not to be interested.

1.4.2 Improved quality of life Interactions with animals affect the physical, psy­ chological and emotional health of both parties (e.g. in human gerontology, Gee et al. 2017; also reviewed throughout this book). This can include the food people choose to eat, whether they keep a pet or are

Figure 1.6 Wildlife tourists getting opportunistic photographs of coatimundi crossing the road in Costa Rica. Photograph from Vicky Melfi.

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ANTHROZOOLOGY

exposed to other people’s pets or whether they choose to see animals in their native range, both at home or on wildlife holidays. It also includes the impact of animals which are considered to dele­ teriously affect human outcomes, both in an urban environment or the animals’ native range, when we confer on them the derogatory epithet of pest: ‘a species located where humans don’t want them’.

Recognition of the scope by which HAIs, HARs and HABs influence the quality of life for both parties, is increasing. It is probably fair to say that there is greater interest, at least within published empirical literature, in how animals can promote human quality of life compared to how we might improve animals’ quality of life (e.g. Bokkers 2006). Ser­ endipitously, there is evidence that benefits for both humans and animals can be positively cor­ related, and thus improvements for one are also seen to have positive ramifications for the other. For example, increased agricultural animal productivity is of benefit to people, and can be achieved when animal welfare is improved (reviewed Chapter 3; Zulkifli 2013).

1.4.3 To ensure scientific rigour Our society is increasingly recognising the need for evidence-based systems (EBS); a premise which uses reliable empirical data on which to make deci­ sions. Evidence-based medicine is probably a term and concept many are familiar with, so it is ­probably unsurprising that EBS have been applied to other medical disciplines e.g. psychiatry (Barron 2017), as well as other biological fields and indeed those which are multi-disciplinary, like conservation (Sutherland et al. 2004). The importance of using reliable and rigorous data is paramount to support these EBS. Animals have been, and still are, central in our understanding of many branches of science, includ­ ing pharmacology, toxicology, food safety, as well as behaviour and endocrinology and much more (Bottini & Hartung 2010). There is a long history of animal use in science, which has developed into modern animal laboratory science guided by three principles (the Three Rs): replacement, reduction and refinement, the aims of which are to use as few ani­ mals as possible (Baumans, 2005; reviewed Chapter

4). To ensure scientific rigour when animal models are used, contemporary research suggests that condi­ tions which promote animal welfare also promote good science; which can include a move away from standardisation and the promotion of good HAIs and HARs (Richter et al. 2009; Davis & Balfour 1992).

There are of course consequences for the health and well-being of both parties, and an almost incalculable financial consequence to industry and society.

1.4.4 To minimise human–animal conflict We have focussed on the benefits which can result for both humans and animals when there are posi­ tive HAIs and HARs. Similarly, negative HAIs and HARs are associated with costs for both parties; these are above and beyond the absence of the positive consequences of positive HAIs and HARs. Conflict arises between humans and animals when actions from either adversely affect the other (reviewed, Nyhus 2016). Most research conducted in this area has focussed on wildlife. According to definitions of human–wildlife conflict, the threat to human life/health/safety, economics, food or prop­ erty security, or recreation can be actual, potential or perceived (Treves & Karanth 2003; Peterson et al.

2011). This issue is complex, not least because we can perceive interactions differently, so some see conflict where others do not. Furthermore, our per­ ceptions of different species also affect how we per­ ceive risks of and conflicts with these animals; for example many people are concerned by the risks posed by apex predators, but not necessarily with smaller or seemingly insignificant wildlife which pose a significant disease risk (Soulsbury and White 2015; Chapron et al. 2014; Jones et al. 2008). Conflict can also arise between ‘human proxy animals’ (ani­ mals serving a role in society i.e. within agriculture and as companion animals) and native animals; a conflict can arise according to whichever animal people perceive to be ‘in the right’ i.e. endemic over introduced wild animals (Reidinger et al. 2013).

Consequences are significant in terms of impact on life, economy and the environment (Woodroffe et al. 2005; Nyhus 2016). Conflict can range in inten­ sity from minor (a nuisance) to severe (lethal), and in frequency from rare to common (see Figure 1.7,

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INTRODUCTION

Shark

11

Severe

IMPACT

Elephant

Negative

INTERACTION

Y

C EN

Positive

U

EQ

FR

Deer

Rare

Common

Minor

Peacock

Goose

Figure 1.7 A model which illustrates the different types of HAI that occur, along the x axis from negative to positive interactions, the impact of the interactions on humans is represented on the y-axis from minor to severe and the z-axis represents the frequency at which these interactions occur from common to rare (after Nyhus 2016, https://www.annualreviews.org/doi/full/10.1146/annurev-environ-110615-085634).

from Nyhus 2016). Direct or indirect consequences for humans can include: attack, which can be lethal and/ or transmit disease which can also be lethal (e.g. rabies transmission, Hughes & Macdonald 2013); vehicle collision with an animal (Olson et al. 2014); loss or damage to material goods (including prop­ erty, agriculture e.g. Waterfield & Zilberman 2012); and reduced well-being (e.g. when pets are killed by wildlife, Lescureux & Linnell 2014). Whereas direct and indirect consequences for animals can include: species extinction, of which there have been many (Woodroffe et al. 2005); death of indi­ viduals intentionally, through pest management which aims to exterminate a species (Bomford & O’Brien 1995), persecution and hunting, to acci­ dental collisions with vehicles (Olson et al. 2014), turbines, houses and other terrestrial objects (Calvert et al. 2013) and ships (van der Hoop et al.

2013); infection by human (or human animal proxy) carried disease (Messenger et al. 2014); contributing to and being negatively affected by reduced eco­ system services (Luck et al. 2003); as well as vari­ ous abuses inflicted on captive and wild animals (Maher et al. 2017).

Most of these conflicts arise through competition for resources. This competition can arise when: humans choose to live in areas that overlap the home ranges of native animals, which with increas­ ing populations and decreasing wilderness is an increasing likelihood; where animals choose to move into areas inhabited by people, i.e. polar bears moving into urban areas to exploit human refuse as a resource; and when people introduce animals which are then in competition with native animals, e.g. introduced mammals versus native mar­ supials in Australia (Woinarski et al. 2015). They can however also result from incompatible behav­ iours performed by either party. Measures taken to reduce human–animal conflict have included: legislation to outlaw attacks on and/or to protect species which have declined due to conflict, e.g. several European carnivore species (e.g. Chapron et al. 2014), and where killing is allowed, humane ­recommendations to be provided (e.g. HSA 2011); the creation of health and safety standards for work with captive animals (e.g. DEFRA 2012); training programmes to promote positive attitudes and empathy for animals in those working with them

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ANTHROZOOLOGY

(e.g. in agriculture, Coleman & Hemsworth 2014); compensation schemes to offset damages made by animals, stakeholder engagement and sustainable ecotourism (e.g. Madden 2004; Dickman et al. 2011; Twining-Ward et al. 2018). Some of the more ­imaginative solutions to conflict can be found in wildlife and urban ecology, where attempts are being made to find ways of coexisting with animals (Redpath et al. 2013).

1.4.5 To create a better world We are living in the Anthropocene, a period of time when our actions are changing our climate and destroying habitats so fast that these extraordinary events can be witnessed during a single human life­ time. Species extinctions are occurring on a scale and at a speed reminiscent of a mass extinction. The Living Planet Index, which measures biodiversity, has estimated that 58% of monitored species declined between 1970 and 2012 (WWF 2016). The main threat to species survival is habitat loss and degradation (Newbold et al.). Not only does our use of land directly endanger species with extinc­ tion, it also exacerbates the impacts of humancaused climate change (Mahowald et al. 2017). We currently live in a time when 40% of the Earth’s sur­ face has been converted for use in agriculture and a further 3% is used to house urban communities (Liu et al. 2014). Unsustainable agriculture and logging, as well as changes to ­freshwater systems, seem to be the main causes of habitat loss (Baillie et al. 2010).

Though habitat loss is the greatest threat to species globally, in Australia, which has experienced more than 10% extinction of its 273 terrestrial species, predation by introduced species, and changes to the fire management regime, seem to be the greatest threats (Woinarski et al. 2015). Introduced species not only predate other species but also cause environmental damage, like the feral camels in ­ Australia, the cost of which has been estimated to be $7.15 per annum (Zeng and Edwards 2010). Often not recognised as introduced species, our pets can have devasting effects on other species. Notably, domestic cats have been estimated to kill 1.3–4.0 bil­ lion birds and 6.3–22.3 billion mammals annually in the USA and are considered to have contributed to

at least sixty-three vertebrate extinctions world­ wide (Loss et al. 2012; Loss and Marra 2018). Pets have also been identified as threats to conservation programmes when housed within reserves or ecotourism facilities (Bessa et al. 2018).

But our interactions with animals globally and more locally are not all bad; in fact, there have been considerably positive HAIs initiated by people, to establish greater positive future HAIs and potentially HARs with animals. The Convention on Biological Diversity set ambitious targets of protecting 17% of terrestrial and 10% of marine regions by 2020; along with ‘bold science’ and strategic thinking, experts consider that this will ‘generate genuine benefits to biodiversity’ (Watson et al. 2016; Butchart et al.

2015). For example, it has been calculated that with­ out conservation efforts, including targeted interven­ tions and habitat protection, the status of the world’s 235 recognised hoofstock species would have been eight times worse than observed; it was estimated that at least 148 species would have dropped by at least one IUCN red list category, meaning some might have become extinct (Hoffmann et al. 2015). Avian conservation efforts implemented in the USA were also found to be successful, though funding alloca­ tion and population trend were positively associated; the more money that was spent seemed to ensure greater conservation success (Luther et al. 2016).

Furthermore, efforts are being made towards being creative in how to establish positive HAIs, through the a­ melioration of threats (e.g. the development of conservation physiology, Madliger et al. 2016).

Unthinking previous traditional agricultural ­methods, which have been ridiculed in the past for their detri­ mental impact on other animals and nature (Ripple et al. 2013), might also provide solutions for using cows and hoofstock in general to help to regenerate grasslands and stave off the devastation of desertifi­ cation, which is becoming more widespread (Savory & Duncan 2015). The Anthropocene has thus far been epitomised by negative HAIs and HARs, it doesn’t need to be. We can instead care more about issues relating to the environment, sustainability and con­ servation (Arias-Maldonado 2013; Knight 2015). And we can choose to work towards building positive HAIs and HARs, which will contribute towards a more resilient world (WWF 2016).

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INTRODUCTION

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