Stress and Animal Welfare: Key Issues in the Biology of Humans and Other Animals [2nd ed. 2019] 978-3-030-32152-9, 978-3-030-32153-6

Table of contents :
Front Matter ....Pages i-xix
One Welfare, One Health, One Stress: Humans and Other Animals (Donald M. Broom, Ken G. Johnson)....Pages 1-13
Adaptation, Regulation, Sentience and Brain Control (Donald M. Broom, Ken G. Johnson)....Pages 15-48
Limits to Adaptation (Donald M. Broom, Ken G. Johnson)....Pages 49-70
Stress and Welfare: History and Usage of Concepts (Donald M. Broom, Ken G. Johnson)....Pages 71-97
Assessing Welfare: Short-Term Responses (Donald M. Broom, Ken G. Johnson)....Pages 99-130
Assessing Welfare: Long-Term Responses (Donald M. Broom, Ken G. Johnson)....Pages 131-172
Preference Studies and Welfare (Donald M. Broom, Ken G. Johnson)....Pages 173-191
Ethics: Considering World Issues (Donald M. Broom, Ken G. Johnson)....Pages 193-210
Stress and Welfare in the World (Donald M. Broom, Ken G. Johnson)....Pages 211-216
Back Matter ....Pages 217-230

Citation preview

Animal Welfare

Donald M. Broom Ken G. Johnson

Stress and Animal Welfare

Key Issues in the Biology of Humans and Other Animals Second Edition

Animal Welfare Series Editor Clive Phillips School of Veterinary Science University of Queensland Gatton, QLD Australia Advisory Editors Marieke Cassia Gartner Atlanta, GA, USA Karen F. Mancera Mexico City, Mexico

More information about this series at http://www.springer.com/series/5675

Donald M. Broom • Ken G. Johnson

Stress and Animal Welfare Key Issues in the Biology of Humans and Other Animals

Second Edition

Donald M. Broom Department of Veterinary Medicine and St Catharine’s College University of Cambridge Cambridge, UK

Ken G. Johnson School of Veterinary Studies Murdoch University Perth, WA, Australia

ISSN 1572-7408 Animal Welfare ISBN 978-3-030-32152-9 ISBN 978-3-030-32153-6 https://doi.org/10.1007/978-3-030-32153-6

(eBook)

Originally published by Kluwer Academic Publishers, Dordrecht, 1993 © Springer Nature Switzerland AG 1993, 2019 This work is subject to copyright. All rights are reserved by the Publisher, whether the whole or part of the material is concerned, specifically the rights of translation, reprinting, reuse of illustrations, recitation, broadcasting, reproduction on microfilms or in any other physical way, and transmission or information storage and retrieval, electronic adaptation, computer software, or by similar or dissimilar methodology now known or hereafter developed. The use of general descriptive names, registered names, trademarks, service marks, etc. in this publication does not imply, even in the absence of a specific statement, that such names are exempt from the relevant protective laws and regulations and therefore free for general use. The publisher, the authors, and the editors are safe to assume that the advice and information in this book are believed to be true and accurate at the date of publication. Neither the publisher nor the authors or the editors give a warranty, expressed or implied, with respect to the material contained herein or for any errors or omissions that may have been made. The publisher remains neutral with regard to jurisdictional claims in published maps and institutional affiliations. This Springer imprint is published by the registered company Springer Nature Switzerland AG. The registered company address is: Gewerbestrasse 11, 6330 Cham, Switzerland

Animal Welfare Series Preface

Animal welfare is attracting increasing interest worldwide, and the knowledge and resources are available to, at least potentially, provide better management systems for farm animals, as well as companion, zoo, laboratory and performance animals. The key requirements for adequate food, water, a suitable environment, companionship and health are important for animals kept for all of these purposes. The increased attention given to animal welfare in recent years derives largely from the fact that the relentless pursuit of financial reward and efficiency, to satisfy market demands, has led to the development of intensive animal management systems that challenge the conscience of many consumers, particularly in the farm and laboratory animal sectors. Livestock are the world’s biggest land users, and the farmed animal population is increasing rapidly to meet the needs of an expanding human population. This results in a tendency to allocate fewer resources to each animal and to value individual animals less, for example in the case of farmed poultry where flocks of over twenty thousand birds are not uncommon. In these circumstances, the importance of each individual’s welfare is diminished. Increased attention to welfare issues is just as evident for zoo, companion, sport and wild animals. Of growing importance is the ethical management of breeding programmes, since genetic manipulation is now technically advanced, but there is less public tolerance of the breeding of extreme animals if it comes at the expense of animal welfare. The quest for producing novel genotypes has fascinated breeders for centuries. Dog and cat breeders have produced a variety of deformities that have adverse effects on their welfare, but nowadays the breeders are just as active in the laboratory, where the mouse is genetically manipulated with equally profound effects. In developing countries, human survival is still a daily uncertainty, so that provision for animal welfare has to be balanced against human welfare. Animal welfare is usually a priority only if it supports the output of the animal, be it food, work, clothing, sport or companionship. However, in many situations the welfare of animals is synonymous with the welfare of the humans who look after them, because happy, healthy animals will be able to assist humans best in their struggle for v

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survival. In principle, the welfare needs of both humans and animals can be provided for, in both developing and developed countries, if resources are properly husbanded. In reality, the inequitable division of the world’s riches creates physical and psychological poverty for humans and animals alike in many parts of the world. The intimate connection between animals and humans that was once so essential for good animal welfare is rare nowadays, having been superseded by technologically efficient production systems where animals on farms and in laboratories are tended by increasingly few humans in the drive to enhance labour efficiency. With today’s busy lifestyles, companion animals too may suffer from reduced contact with humans, although their value in providing companionship, particularly for certain groups such as the elderly, is beginning to be recognised. Animal consumers also rarely have any contact with the animals that are kept for their benefit. In this estranged, efficient world, people struggle to find the moral imperatives to determine the level of welfare that they should afford to animals within their charge. A few people, and in particular many companion animal owners, strive for what they believe to be the highest levels of welfare provision, while others, deliberately or through ignorance, keep animals in impoverished conditions in which their health and well-being can be extremely poor. Today’s multiple moral codes for animal care and use are derived from a broad range of cultural influences, including media reports of animal abuse, guidelines on ethical consumption and campaigning and lobbying groups. This series has been designed to contribute towards a culture of respect for animals and their welfare by producing learned treatises about the provision for the welfare of the animal species that are managed and cared for by humans. The early species-focused books were not detailed management blueprints; rather they described and considered the major welfare concerns, often with reference to the behaviour of the wild progenitors of the managed animals. Welfare was specifically focused on animals’ needs, concentrating on nutrition, behaviour, reproduction and the physical and social environment. Economic effects of animal welfare provision were also considered where relevant, as were key areas where further research is required. In this volume the series again departs from the single vertebrate species model to address the connections between animal welfare and stress. Donald Broom, the architect of so much of what we now consider to be animal welfare science, has comprehensively revised his earlier edition of Stress and Animal Welfare that was first published with Ken Johnson in 1993. The book refers extensively to human stress and welfare, not just to non-humans. The foundations of this topic are laid with carefully constructed definitions of the main terminology, which is fundamental to the subsequent detailed consideration of how stress in humans and other animals is connected to their welfare. Furthermore, Donald Broom discusses animal welfare issues in the context of other topical concerns, about the environment, as part of social change, and in the light of diminishing antimicrobial efficacy. Throughout, he uses his considerable experience in animal welfare science to introduce new material about sentience, brain function and stress measures. How individuals adapt to situations and respond to pain and other stress-inducing concerns in both the short

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and long term is all covered in depth in this book. The end result is a fascinating union of two topics—stress and animal welfare—that are fundamental to understand if we want to make decisions about how we should manage our lives and look after other animals. A key to this decision-making process to measure responses accurately, this book describes the rapidly changing situation in relation to monitoring animals’ welfare, never forgetting that it is an individual animal that is at the heart of the process, not a group of several thousand farm animals. It is over a quarter of a century since the first edition of this book was published, but I believe this edition will be providing us with valuable discussion on stress and welfare in humans and other animals for a very long time indeed. School of Veterinary Science University of Queensland Gatton, QLD Australia

Clive Phillips

Preface to Second Edition

This book is about the science underlying stress and welfare in humans and in other animals. The progress in this area of science since the first edition of this book has been remarkable. We now have a much better understanding about the role of different brain and body mechanisms in coping with our everyday environment. Psychiatry and ideas about human welfare are more closely linked to general human medicine and animal welfare more closely linked to veterinary medicine. The links between stress research and welfare research have become ever stronger and the dramatic results of epigenetic and other research have changed our ideas about how life is controlled. The idea that many characteristics of humans and other animals are solely genetic was eroded by the 1990s, but recent research shows it to be false. Every characteristic of every animal is affected by both genes and environment. As explained in Chap. 1, it now seems that no stage of gene expression is unaffected by environmental factors. No behavioural, physiological or anatomical character is genetically determined, instinctive or innate, where these terms mean independent of environmental effects. Of course, some characteristics are more likely to be modified by environmental factors than others, but no person can say that their anti-social behaviour, or other unwanted quality, is solely caused by their genes. The welfare of parents during sperm and egg development is now known to have wide-ranging effects on their own functioning and to affect the functioning of the offspring. Stressed parents have less viable offspring and some effects continue in the subsequent generations. The mechanisms of the effects of stressful environments are much better known now, as are the links between welfare, immune system function and likelihood of disease. The ideas of one health and one welfare, emphasising that each term means exactly the same for humans and non-humans and that health is an important part of welfare, are now widely accepted. Animal welfare science has developed at a rapid rate with at least fifty times more publications on the subject now than 30 years ago. The new scientific discipline was developed and made applicable to everyday life by establishing key concepts and

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developing methods for evaluating welfare in a scientific way. There have also been parallel and overlapping developments in human stress and welfare studies. The use of the term stress has been refined and methodologies in human and veterinary medicine further developed. The concepts provide the basis from which deductions can be made, and structures to which emerging ideas can be attached. The upsurge of public interest in the welfare of animals and the demand for precise information so that proper action can be taken has occurred in all countries of the world. Psychiatry and other treatment of people with stress and depression have gradually become more mainstream subjects in human medicine. Teaching and a need for knowledge about stress and welfare are now widespread in human medicine, psychology, animal biology, veterinary medicine and animal production. There are also close links with ethics and other areas of philosophy, as well as with relevant areas of law and social science. Associated with the identical use in humans and other species of concepts such as health, welfare, stress and pain, function in non-human species has been demonstrated to be closer to that in humans than was once thought. In recent years, evidence for the similarities between humans and many non-human species in cognitive ability and capacity for having emotions and feelings has become stronger. The very small genetic differences between humans and other species also reinforce the idea that humans are not unique or special and that an understanding of function in one species is often helpful in others. Studies of animal welfare science and stress impacts in non-humans can greatly help solve problems in humans and vice versa. The principles presented in this book are structured to refer to all animals, both human and non-human. In Chap. 1, the need for careful scientific study of stress and welfare is explained. The reasons for some of the problems in understanding the concepts are discussed, and it is argued that there is a requirement for further analysis of the concepts, and especially for an effective synthesis of current ideas. The use of the terms stress and welfare is clarified by deriving definitions for them related to the functioning and efficacy of the biological systems that animals use to both regulate their lives and deal with difficulties. These systems include a wide range of biological components including the feelings of the animals. This derivation is explained in Chaps. 2 and 3. The definitions, based on established biological concepts and consistent with similar ideas in other disciplines, are described in detail in Chap. 4. From this theoretical base, sound and practical approaches for assessing welfare are outlined. Chapter 5 provides an account of the responses of individuals to shortterm disturbances, while the responses to long-term disturbances are documented in Chap. 6. In Chap. 7, the use of preference studies to provide information relevant to the assessment of welfare, especially that of animals that we use, is discussed. The question of how great a disturbance of homeostasis, or what level of stimulation an animal should be subjected to, is partly a matter of biological judgement, since animals may manage better if exposed to a moderate level of stimulation, even if it is aversive, rather than being protected from stimulation entirely. But ethical considerations obviously also dictate that there must be a limit. A survey of the ethical

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issues involved and a guide to making ethical decisions about animal stress and welfare and putting it in a world context are presented in Chap. 8. Finally, the major arguments presented in the book are summarised in Chap. 9. The meanings of terms used in this book are listed in the Glossary, the references used in each chapter are listed at the end and a subject and author index is included. As human society continues to evolve it changes the relationship between humans and other animals, but too often this has been to the detriment of those animals. Fortunately, biological studies are uncovering ways of identifying, assessing and alleviating poor welfare. With this information, strategies can be developed to avoid unreasonable impositions on animals, as well as properly considering all other aspects of sustainability. One of the goals of the book is to help establish a biological base from which can be developed codes of living in a modern and compassionate society. Cambridge, UK

Donald M. Broom

Acknowledgements

For the first edition of this book, Don Broom and Ken Johnson thank Caroline E. Manser, Georgia J. Mason, Mike T. Mendl, Erina Kirby, Jane Blackburn, Sally E.M. Broom and the editorial staff at Chapman & Hall for their help in the preparation of the book, including contributions to the collection of material, and help in the formulation of ideas and comments on the manuscript for this book. Caroline Manser’s report on stress assessment measures was of particular value. For the second edition, prepared by D.M. Broom, thanks are offered to all those who have been members of the Centre for Animal Welfare and Anthrozoology in the Department of Veterinary Medicine, Cambridge University (1986–2019), and many members of the International Society for Applied Ethology for helpful discussions. In the preparation of this book, I expected to have help from the late Dr Fiona Lang and I shall remember interesting discussions with her. I thank Professor Clive Phillips for many helpful comments on the draft chapters and the editorial staff of Springer International for their assistance. Donald M. Broom

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Contents

1

One Welfare, One Health, One Stress: Humans and Other Animals . . 1.1 The Terms Animal, Welfare, Health and Stress . . . . . . . . . . . . . . 1.2 Animal Welfare and Social Change . . . . . . . . . . . . . . . . . . . . . . 1.3 The Debate About Animal Usage . . . . . . . . . . . . . . . . . . . . . . . . 1.4 Genetics, Epigenetics and What the Environment Can Change . . . 1.5 The Challenge Ahead . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

1 1 5 7 9 10 11

2

Adaptation, Regulation, Sentience and Brain Control . . . . . . . . . . . . 2.1 Adaptation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.2 Homeostatic Control . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.3 Sentience and the Role of the Brain in Coping . . . . . . . . . . . . . . 2.4 Habituation and Sensitisation . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.5 Motivational State . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.6 Outputs from Decision Centres . . . . . . . . . . . . . . . . . . . . . . . . . 2.6.1 Neural and Muscular Outputs . . . . . . . . . . . . . . . . . . . . 2.6.2 Hormonal and Neurohormonal Outputs . . . . . . . . . . . . . 2.7 Control Systems and Needs . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.7.1 Simple Models of Control . . . . . . . . . . . . . . . . . . . . . . . 2.7.2 Motivational State as the Determinant of Action . . . . . . . 2.7.3 Other Concepts that Have Been Used to Explain Motivation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.7.4 The Concepts of Needs and Freedoms . . . . . . . . . . . . . . 2.7.5 Motivational Dilemmas and the ‘Trade-off’ Concept . . . 2.8 Types of Control . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.8.1 Rates of Neural and Hormonal Response . . . . . . . . . . . . 2.8.2 Feedback and Feedforward Controls . . . . . . . . . . . . . . . 2.8.3 Predictability of Stimulation . . . . . . . . . . . . . . . . . . . . . 2.9 Pain . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

15 15 16 18 19 20 23 23 24 26 26 29 30 31 33 34 35 35 37 39

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2.10 2.11

Other Feelings and Emotions: Positive and Negative . . . . . . . . . Development of Regulatory Systems . . . . . . . . . . . . . . . . . . . . 2.11.1 Early Abilities, Preferences and Experiences . . . . . . . . 2.11.2 Learning and Memory . . . . . . . . . . . . . . . . . . . . . . . . 2.11.3 Lifetime and Evolutionary Changes . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3

4

. . . . . .

40 41 41 42 43 44

Limits to Adaptation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.1 Limitations of Timing and Temporal Aspects of Stimulus Modality . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.1.1 Changes in Frequency . . . . . . . . . . . . . . . . . . . . . . . . . 3.1.2 Changes in Duration . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.1.3 The Impact of Novelty . . . . . . . . . . . . . . . . . . . . . . . . . 3.1.4 The Value of Forewarning . . . . . . . . . . . . . . . . . . . . . . 3.2 Limitations of Intensity as an Information Basis for Adaptation . . . 3.2.1 Changes in Intensity . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.2.2 Hazard Avoidance and Lethal Limits . . . . . . . . . . . . . . . 3.3 Variation in Adaptation Has Consequences for Responses to Stimulation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.4 Integrating Time, Intensity and Mode of Stimulation . . . . . . . . . . 3.5 The Concepts of Tolerance and Coping . . . . . . . . . . . . . . . . . . . 3.6 Variations in Patterns of Adaptation . . . . . . . . . . . . . . . . . . . . . . 3.6.1 Differing Rates and Methods of Adaptation . . . . . . . . . . 3.6.2 Hypersensitivity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.6.3 Hyposensitivity and Stress-Induced Analgesia . . . . . . . . 3.7 Other Factors Affecting Adaptation and Coping . . . . . . . . . . . . . 3.7.1 Lack of Stimulation . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.7.2 Unpredictable Stimulation . . . . . . . . . . . . . . . . . . . . . . 3.7.3 Frustration of Behavioural Output . . . . . . . . . . . . . . . . . 3.8 Effects of Human Selection of Animals on Their Ability to Adapt . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

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Stress and Welfare: History and Usage of Concepts . . . . . . . . . . . . 4.1 Stress . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.2 Welfare . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.3 Welfare Assessment . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.4 Welfare in Relation to Stress . . . . . . . . . . . . . . . . . . . . . . . . . . 4.5 Welfare in Relation to Naturalness . . . . . . . . . . . . . . . . . . . . . . 4.6 Welfare and Well-Being . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.7 Welfare and Quality of Life . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.8 Welfare and a Life Worth Living . . . . . . . . . . . . . . . . . . . . . . . 4.9 Welfare in Other Languages . . . . . . . . . . . . . . . . . . . . . . . . . . 4.10 Welfare and Sentience . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

. . . . . . . . . . . .

49 49 52 54 54 55 55 55 57 58 60 62 62 63 63 64 64 65 66 67 68 71 71 81 87 91 92 93 93 93 94 94 95

Contents

5

6

Assessing Welfare: Short-Term Responses . . . . . . . . . . . . . . . . . . . 5.1 Behavioural Measures of Welfare . . . . . . . . . . . . . . . . . . . . . . 5.1.1 Orientation and Startle Responses . . . . . . . . . . . . . . . . 5.1.2 Individual Differences in Behavioural Responses . . . . . 5.1.3 Measures for Assessing Pain . . . . . . . . . . . . . . . . . . . . 5.2 Physiological Measures of Welfare . . . . . . . . . . . . . . . . . . . . . 5.2.1 Heart Rate and Heart Rate Variability . . . . . . . . . . . . . 5.2.2 Rate of Breathing, Breathlessness and Body Temperature . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.2.3 The Adrenal Axes . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.2.4 Other Hormones . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.2.5 Enzymes, Other Proteins and Metabolic Products . . . . . 5.2.6 Blood, Muscle and Other Carcass Characteristics . . . . . 5.3 Using Indicators to Evaluate Welfare . . . . . . . . . . . . . . . . . . . . 5.4 Short-Term Welfare Problems and Concepts of Stress . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

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99 101 101 103 103 106 106

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109 110 116 117 118 120 121 123

Assessing Welfare: Long-Term Responses . . . . . . . . . . . . . . . . . . . . 6.1 Direct Measures of Good Welfare . . . . . . . . . . . . . . . . . . . . . . . 6.2 Cognitive Bias and Other Indirect Measures of Good Welfare . . . 6.3 Qualitative Behavioural Assessment . . . . . . . . . . . . . . . . . . . . . . 6.4 Reduced Reproductive Success . . . . . . . . . . . . . . . . . . . . . . . . . 6.5 Reduced Life Expectancy . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6.6 Weight, Growth and Body Condition . . . . . . . . . . . . . . . . . . . . . 6.7 Cardiovascular and Blood Measures . . . . . . . . . . . . . . . . . . . . . . 6.8 Adrenal Axes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6.8.1 Sympathetic Nervous System and Adrenal Medulla . . . . 6.8.2 Hypothalamic-Pituitary-Adrenal Cortex . . . . . . . . . . . . . 6.9 Measures of Immune System Function . . . . . . . . . . . . . . . . . . . . 6.9.1 Measuring White Cell Numbers . . . . . . . . . . . . . . . . . . 6.9.2 Antibody Production . . . . . . . . . . . . . . . . . . . . . . . . . . 6.9.3 T-Lymphocyte Function . . . . . . . . . . . . . . . . . . . . . . . . 6.9.4 Other Body Defences . . . . . . . . . . . . . . . . . . . . . . . . . . 6.10 Bone Strength, Muscle Strength and Injury . . . . . . . . . . . . . . . . . 6.11 Disease Incidence Measures . . . . . . . . . . . . . . . . . . . . . . . . . . . 6.12 Brain Measures . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6.13 Behavioural Measures . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6.13.1 Problems with Movement . . . . . . . . . . . . . . . . . . . . . . . 6.13.2 Behaviour Associated with Lack of a Resource . . . . . . . 6.13.3 Behaviour Associated with Lack of Social or Sexual Partners . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6.13.4 Consequences of Inability to Perform a Behaviour . . . . . 6.13.5 Sickness Behaviour and Physiology . . . . . . . . . . . . . . . 6.14 Other Consequences of Frustration and Lack of Control . . . . . . . 6.14.1 Aggression . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6.14.2 Stereotypies . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

131 132 133 134 136 137 139 140 141 141 141 142 143 143 144 146 147 148 149 150 151 153 154 155 156 157 157 157

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6.14.3 Depression, Apathy and Unresponsiveness . . . . . . . . . . . Lack of Stimulation and Overstimulation . . . . . . . . . . . . . . . . . . 6.15.1 Lack of Stimulation . . . . . . . . . . . . . . . . . . . . . . . . . . . 6.15.2 Overstimulation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6.15.3 Problems Caused by Specific Localised Stimulation . . . . 6.16 Interrelationships Among Measures and Welfare Outcome Measures . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

160 162 162 162 164

7

Preference Studies and Welfare . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7.1 Time and Energy Allocation in a Rich Environment . . . . . . . . . . 7.2 Experimental Studies of Animal Preferences . . . . . . . . . . . . . . . . 7.2.1 Assessing the Importance of Preferences . . . . . . . . . . . . 7.2.2 Operant Techniques in the Assessment of Preferences . . 7.3 Environmental Enrichment . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7.4 Do Preference Studies Tell us What Is Important for Animals? . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

173 174 176 176 178 185 187 188

8

Ethics: Considering World Issues . . . . . . . . . . . . . . . . . . . . . . . . . . . 8.1 World Problems . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8.2 Value Systems . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8.3 Anti-Microbial Resistance . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8.4 Climate Change . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8.5 Sustainability . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8.5.1 Adverse Effects on Human Welfare, Including Human Health . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8.5.2 Poor Welfare of Animals . . . . . . . . . . . . . . . . . . . . . . . 8.5.3 Unacceptable Genetic Modification . . . . . . . . . . . . . . . . 8.5.4 Harmful Environmental Effects . . . . . . . . . . . . . . . . . . . 8.5.5 Inefficient Usage of World Food Resources . . . . . . . . . . 8.5.6 Not “Fair Trade”: Producers in Poor Countries Do Not Receive a Fair Reward . . . . . . . . . . . . . . . . . . . 8.5.7 Not Preserving Rural Communities . . . . . . . . . . . . . . . . 8.6 How Humans Impose on Other Animals: And Vice Versa . . . . . . 8.6.1 The most Successful Animals . . . . . . . . . . . . . . . . . . . . 8.6.2 Numbers of Animals Kept by Humans in Relation to Welfare Problems . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8.6.3 Ethics of Killing and Welfare . . . . . . . . . . . . . . . . . . . . 8.7 Setting Ethical Limits to Assessed Welfare . . . . . . . . . . . . . . . . . 8.7.1 Animals in a Natural Environment . . . . . . . . . . . . . . . . 8.7.2 Humans under the Same Strain . . . . . . . . . . . . . . . . . . . 8.7.3 The Informed and Compassionate Arbiter . . . . . . . . . . . 8.8 Food Production Systems for the Future . . . . . . . . . . . . . . . . . . . 8.8.1 Sustainable Animal and Forage Plant Systems . . . . . . . . 8.9 Stress and Welfare in the General Ethical Framework . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

193 193 194 196 197 197

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198 198 199 199 199 200 200 201 201 201 203 204 204 205 205 206 208 208 208

Contents

9

Stress and Welfare in the World . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9.1 Studying Stress and Welfare . . . . . . . . . . . . . . . . . . . . . . . . . . . 9.2 Using the Term Stress Scientifically . . . . . . . . . . . . . . . . . . . . . . 9.2.1 Avoidance of Stress . . . . . . . . . . . . . . . . . . . . . . . . . . . 9.2.2 Reduction of Stress and Improvement of Welfare . . . . . . 9.2.3 Monitoring Welfare . . . . . . . . . . . . . . . . . . . . . . . . . . . 9.3 Welfare in the Moral World . . . . . . . . . . . . . . . . . . . . . . . . . . . .

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211 211 212 213 214 214 215

Glossary . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 217 Index . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 225

Chapter 1

One Welfare, One Health, One Stress: Humans and Other Animals

Abstract In this chapter, the need for scientific study of stress and welfare is explained. The imprecise use of terms, especially stress, is described and reasons for some of the problems in understanding the concepts are discussed. It is argued that there is a requirement for further analysis of the concepts, and especially careful synthesis of current ideas. The use of the terms stress and welfare is clarified by deriving definitions for them related to the functioning and efficacy of the biological systems that animals use to regulate their lives and deal with difficulties. These systems include a wide range of biological components including the feelings of the animals. Terms defined include: animal, welfare, coping, health, stress and domestication. Attitudes to the animals that humans use and views about the treatment of such animals are considered. Major recent changes in ideas about genetic and environmental influences on humans and other animals are explained. Keywords Welfare · Stress · Health · One welfare · One health

1.1

The Terms Animal, Welfare, Health and Stress

The idea that humans are animals and share a very high proportion of genes and characteristics with other species has been a fundamental concept for biologists and people with medical, veterinary and agricultural training for many years. However, many other scientists and members of the general public still think of humans as special in some way. Whilst it is not surprising that humans favour their own species, the concept of humans as fundamentally different from all other animals is scientifically unsound. This subject, and ideas about human dominion, are revisited in Chap. 8. The main biological concepts discussed in this book will refer to a wide range of animal species including humans. As pointed out by Carr and Broom (2018) and by many others, biologists use the term ‘animal’ to mean a living being with a nervous system and other complex mechanisms for obtaining energy, using energy, and reproducing. Animals survive by consuming, and hence utilising the energy, of plants, other animals and bacteria. Most animals have an effective means of locomotion and a range of sense organs. © Springer Nature Switzerland AG 2019 D. M. Broom, K. G. Johnson, Stress and Animal Welfare, Animal Welfare 19, https://doi.org/10.1007/978-3-030-32153-6_1

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1 One Welfare, One Health, One Stress: Humans and Other Animals

They range in size from microscopic protozoans, worms and insects to animals that can be very much bigger than humans such as squid, sharks, elephants and whales. Other living beings also have some of these mechanisms but only animals have a true nervous system. Despite this scientific meaning of ‘animal’ to include insects, fish, snails, spiders, monkeys etc., many people have erroneously limited the meaning to farmed animals, owned animals, mammals, or warm-blooded animals. Hence, the word ‘animal’ elicits different images and concepts for different people, most of them biologically much too narrow. Humans have always had great interest in other species of animals, especially because of their diverse, brain-controlled behaviour. However, people have also used the word ‘animal’ with the implication that it is a being that is more aggressive, less controlled, or more subject to lust than the average human. The idea that humans control their emotions but non-humans never do is now known to be quite wrong. Many newspapers, magazines, internet sites and novels, as well as numerous academic journals and texts use the words stress, welfare and health. The terms are sometimes used in a general way in order to avoid being too specific about the nature of particular difficulties during life. General difficulties, that are of current concern to the public because of their social and ethical implications, where the terms may be used include: over-worked people, the dangers of novel diseases, antimicrobial resistance and cruelty to or close confinement of farm or other animals. However, a broad use of the words tends to result in less precision in the meanings attached to them. Precise, universally usable definitions of the terms are needed and should be born in mind when speaking about the subject areas. The terms stress, welfare and health strike responsive chords in all of us, perhaps because they relate to our concerns about our own welfare and that of individuals of importance to us. As discussed further in Chap. 8 and by Broom (2003, 2014) our concerns extend to other people, other species and, for more and more people, to all sentient beings. We have a vested interest in the stresses imposed on us, and their effects on our welfare. Many environmental impacts have consequences that benefit us, sometimes because we learn from the experience and cope better in future, but other impacts may have long-term detrimental effects, even into the next generations. We need to know how best to react to any period of poor welfare but also to distinguish effects that are permanently deleterious from those that are not. Whilst the central concepts of this chapter will be further explained and discussed in later chapters, they will be defined here in order that their meanings will be clear. The welfare of an individual is its state as regards its attempts to cope with its environment. Feelings are a part of coping mechanisms and health refers to coping with pathology so both feelings and health are important parts of welfare. The term welfare refers to living animals, including humans, but not to plants or inanimate objects. Coping means having control of mental and bodily stability so coping requires nervous system function. Hence, since plants do not have a nervous system, they do not have welfare. Plants can show differential growth in response to environmental variation, and mechanisms like the closing of a venus fly trap plant (Dionaea) are impressively fast, but the absence of a central nervous system means that the responses of plants are not behaviour controlled by nervous mechanisms.

1.1 The Terms Animal, Welfare, Health and Stress

3

Similarly, a simple avoidance response to a toxic chemical by a bacterium is not coping and the term welfare is not used for bacteria. Animals, plants and bacteria can show adaptation by individuals to changed circumstances (Broom 2006a) but whilst adaptation occurs without nervous system involvement, coping usually does involve the nervous system so is limited to animals. Welfare refers to a wide range of coping systems, it can be measured scientifically and it varies over a range from very good to very poor (Broom 1986b, Broom and Fraser 2015). Welfare means the same as well-being, although the word welfare is often thought of as more precise, and welfare is used more often in scientific writing and in laws. Quality of life also means welfare, so it can be measured, although the concept of quality of life is not normally used for short periods of life (Broom 2007). The similarities in physiological, immunological and clinical research on stress and welfare in humans and a range of other species are widely discussed now but were considered in detail some years ago at a Dahlem Conference entitled “Coping with Challenge: Welfare in Animals including Humans” (Broom 2001). It was clear that human psychiatry and medicine could learn from farm animal and other welfare research and vice versa. More recently, the one welfare approach has emphasised that the concept of welfare is identical when applied to humans or to non-human animals (Colonius and Earley 2013; García Pinillos et al. 2015, 2016; García Pinillos 2018; Broom 2017). When the welfare of individual humans or non-human animals is poor, there is increased susceptibility to disease. As a consequence, improving welfare generally reduces disease. Those with a medical background and those with a veterinary or other biological background benefit from exchanging information, in particular because of the similarities in disease and in other causes of poor welfare in humans and other species. Care for people and care for animals used by people is generally better if all are considered as individuals. Colloquial use of the term health has sometimes been too general and the statement about health by the World Health Organization (1948) “health is a state of complete physical, mental and social well-being and not merely the absence of disease or infirmity” did not take account of the use of other scientific terms, did not distinguish health from welfare, and was too broad to be a meaningful definition. Health, like welfare, can be qualified as good or poor and varies over a range. It refers to body systems, including those in the brain, that combat pathogens, tissue damage or physiological disorder so health is the state of an individual as regards its attempts to cope with pathology (Broom 2006b). The concept of health is not exactly the same for plants and so the definition refers to “adapt to” rather than “cope with” pathology, the difference being explained above. For a plant, health is the state of an individual as regards its attempts to adapt to pathology. In all animals, health is a key part of welfare, not something separate from it, so it is not logical to refer to “health and welfare”. Instead we should say “welfare including health”. The One Health concept explains that health means the same for non-human animals as it does for humans. One Health is a worldwide strategy for expanding interdisciplinary collaborations and communications in all aspects of health care for humans, non-human animals and the environment. The impact of the environment on health is a very important topic in human and veterinary medicine but it is not scientifically

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1 One Welfare, One Health, One Stress: Humans and Other Animals

correct to refer to the health of the environment because the environment is not selfregulating. A resolution promoting the similarity of human and non-human animal health and the need for collaboration between the human medical and veterinary researchers and practitioners was adopted in 2007 by the American Medical Association and the American Veterinary Medical Association. The concept is further explained by Monath et al. (2010) and Karesh (2014). How well is the term stress understood? Can anyone say with confidence exactly when an animal, or even when they themselves, are stressed? Consider a situation in which human or animal athletes run to the limit of their capacity. Are they stressed? Perhaps so, but if that effort improves subsequent performance, was the first exhausting run ‘stressful’, or was it ‘training’, or was it both of these? Consider the case of an animal that is so protected from the physical and social challenges of the environment that subsequent exposure to the natural world causes it to collapse. Has the animal benefited, or suffered, from the lack of environmental buffeting? Has the isolation itself been a stress? A usable concept of stress must take account of such questions. Analysing what biologists mean by stress is a logical place to begin a study of animal welfare. The task undertaken in this book is to define and relate stress and welfare, and to review ways of measuring and using them. Most people who speak of stress refer to a situation in which an individual is subjected to a potentially or actually damaging effect of its environment. However, the usage of the term has often been confusing, as it has been used to mean three different things: (i) an environmental change that affects an organism; (ii) the process of affecting the organism; or (iii) the consequences of effects on the organism. Some people have used stress to refer to mental rather than physiological responses. Many others have limited stress to one kind of physiological response mechanism, hypothalamic–pituitary–adrenal cortex (HPA) activity. However, it was demonstrated by Mason (1971) that cortisol and corticosterone production occurs in many circumstances and the hormones are involved in several physiological systems. HPA activity is temporarily increased during courtship, mating, active prey catching and active social interaction, none of which would be considered to be stressful or otherwise harmful by the majority of the general public or by most scientists. For example, courtship and preparing for courtship in male and female humans involves increases in cortisol (Roney et al. 2003, 2007; López et al. 2009). To equate stress with HPA axis activity renders the word redundant and is considered unscientific and unnecessary by most scientists working in the area. Another use of the word stress is for any a situation that involves some difficulty for the individual, even if the consequence is positive. This use makes stress largely synonymous with stimulation and renders the term useless. If every impact of the environment on an organism is called stress, then the term has no value. Many stimuli that affect individuals in beneficial ways would never be called stressors by most people. A usable definition of stress presented in the first edition of this book (Broom and Johnson 1993) is slightly modified from Broom (1985). Stress is an environmental effect on an individual which overtaxes its control systems and results in adverse consequences and eventually reduced fitness. The ultimate measure of fitness is the number of offspring that are produced, that survive and that are

1.2 Animal Welfare and Social Change

5

reproductively successful so that their offspring reach future generations. There are many different ways in which challenges overtax control systems and have such effects. If stress is defined in this way, stress always involves poor welfare and no stress is beneficial. There has been an enormous amount of scientific and social study of human stress and welfare and also much work on laboratory, farmed, companion and wild animals. A key point, emphasised by the heading of this Chapter, is that the terms welfare, health and stress mean exactly the same whether applied to humans or non-humans. Stress and welfare, in people and in various managed or exploited animals, need to be understood in order that people can increase happiness, solve a range of human problems and use scientific information so that animal welfare requirements can be prescribed in legislation.

1.2

Animal Welfare and Social Change

The rise in public interest in animal welfare during the past four decades has been dramatic. Concern for animals is evident throughout society in many countries and is invisible only to those who do not want to see. Some of those who are passionately opposed to killing animals for any purpose have used a variety of methods to draw the attention of other people to actions that cause animal death. A high proportion of people in the world object to any action that causes poor welfare in animals and hence condemn and protest about any cruelty to animals. For example, 90% of respondents to a MORI Poll in China agreed that we have a moral duty to minimise animal suffering as much as possible (Podberscek 2005) and 94% of E.U. citizens thought that it is important to protect farm animal welfare (EU D.G. Health and Food Safety 2016; Broom 2017). Particularly loud have been claims that some or all of what is being done to animals is unjustified. The wide disparity in people’s views on how humans should treat other animals has led to social polarisation in a debate about the morality of various human interactions with other animals. An examination of the controversy may help us to understand its significance and contribute to resolving it. There have always been many kinds of interactions among animal species and those involving humans are as old as mankind. From earliest times, one-sided interactions have occurred when non-human animals were killed by man to provide a resource of some kind, commonly food. Conversely, humans have been prey of other species. For many thousands of years, humans have managed populations of animals, not just in relation to food but also for transport, recreation, companionship, or protection. Like humans, ants manage the populations of different animal species that are a resource for them whilst many animals manage prey animal or plant populations. For human convenience and ease of management, several species of animals have been kept in or near human dwellings, and their genotype modified by selective breeding. Perhaps the longest relationship has been with wolves, or dogs as we now call one form of the Middle-Eastern grey wolf (Clutton-Brock 1999; von

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1 One Welfare, One Health, One Stress: Humans and Other Animals

Holdt et al. 2010). This relationship, and we may speak of wolves domesticating humans just as correctly as humans domesticating wolves (Broom 2006a), seems likely to have been mutually beneficial to both species. The wolves were good at chasing prey at high speed for a short time, whilst the humans were able to continue a chase for longer distances and were better able to deal with some prey that were large, or which could climb. Price (1984, 2002) defined domestication as ‘that process by which a population of animals becomes adapted to man and to the captive environment by some combination of genetic changes occurring over generations and environmentally induced developmental events recurring during each generation’. However, the developmental events may not be the same during each generation. Wild animals vary in their potential to adapt, some being unable to do so and others having more or less ability to adapt, so there is likely to be much variation in chances of surviving and breeding when animals are first brought into captivity. In some species all will die, while in others a few will survive and breed in captivity. A clearer definition of domestication is: the process, occurring over generations, by which a population of animals becomes adapted to man and to the captive environment by some combination of genetic changes and environmentally induced developmental events. The animals which have been domesticated, or which have allowed themselves to be domesticated, or which have domesticated humans, are social species, that have always lived in groups. These are generally the animals with the highest levels of cognitive ability and are those in which the father plays an unusually small part in parental care (Broom and Fraser 2015). This latter fact has led to the unbalanced view that in most animals parental care is almost entirely maternal care. In reality, in many animal species the father has a substantial role in protecting and caring for the young (Elwood 1979; Kvarnemo 2006; Fernandez-Duque et al. 2009). Domesticated animals are certainly exploited by man, but to some extent they have also exploited the human ecosystem (Budiansky 1992). The domestic fowl, by providing a food source for man and adapting to human conditions, has so encouraged human care that it has become the commonest bird in the world (Broom 1986a). This is a successful species that has exploited an ecological niche, a major component of which is the availability of human care. As far as individual chickens are concerned, however, the majority derive much less benefit from humans, in terms of their welfare, than humans derive from them. Food animals, pet animals, and animals that race or perform in other ways for human entertainment may be common, and arguably biologically successful, but all are exploited to some extent within human society. With passing centuries, the nature of many interactions between humans and other species has changed. Some activities involving animals, that were once forms of daily business, such as riding horses and driving pony traps, are now mainly leisure activities or competitive sports. Others, like poultry raising, that were previously part of life on an average farm, and involved daily contact with, and knowledge of, each hen or cockerel, are now aggregated into commercial enterprises in which there is little concern for individual animals. Even the keeping of family pets is affected by fashion and business. Some pets are bred, purely as a human whim,

1.3 The Debate About Animal Usage

7

with characteristics of supposed cosmetic appeal that impair their ability to cope with everyday life. Many people consider immoral the selection as companion animals of dogs with inevitable respiratory problems like Pugs, French Bulldogs or English Bulldogs. Human attitudes to animals change with time, as do other characteristics of an evolving society. In one era people derive enjoyment from the spectacle of animal fights, in another they collect animals in zoos or museums, and in another, with the aid of technology, they seek to maximize animal production, consider animals as tourist attractions (Carr and Broom 2018), or use animals to find cures for diseases. Perceived values of individual humans or other animals are undoubtedly major determinants of what is acceptable. Sections of society in one generation attach great significance to hunting wild animals and in another to conserving them in their natural state. As ideological and economic priorities change, so does society’s regard or disregard for animals. But are there absolute standards to which these attitudes should conform? Some attempt is being made here to answer this question.

1.3

The Debate About Animal Usage

There are many human actions that affect much of life on the planet but the interests of non-human animals are widely neglected and the moral obligation to consider these interests is often forgotten. In order to be able to respond rationally to these concerns, two specific steps are essential. The first is to formulate an ethically and scientifically defensible philosophy about all animals, including humans. The second is to develop specific animal management and interaction practices consistent with this fundamental philosophy. Interested people have found it relatively easy to criticise particular areas of current animal usage, but it has been more difficult to develop a convincing philosophy about the place of humans in the animal world and hence to decide how we should all act. A central issue is what should be done to improve animal welfare? Some of our problems in trying to understand what to do are compounded by ignorance about our own species. How distressing are different sorts of human suffering? What can we measure to identify good welfare in humans? How can people regulate their lives so as to minimize adverse environmental effects? Should we avoid all potentially harmful stimuli, or is that unwise? The scientific investigation of human and non-human welfare can use much of the same methodology. Moral judgements about what should be done to improve welfare are also structured in very similar ways. Since many biological systems are common to both humans and non-human animals, we can learn about human systems for coping with adversity by studying similar systems in other species. Likewise, many ways of improving human welfare are undoubtedly appropriate for the animals that we keep. Contributions to the current debate about obligations to animals, animal usage, and animal welfare come from various community groups, ranging from critics who oppose virtually all animal use to defenders of every current practice involving

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1 One Welfare, One Health, One Stress: Humans and Other Animals

animal exploitation. Some of those espousing extreme positions are philosophers and biologists, but an increasing number in these groups are members of the public with more moderate positions, and there has been increasing discussion of concepts amongst those with differing views. Prominent groups in the debate include vocal critics who vigorously denounce some or all use of non-human animals. Their views vary from beliefs that humans should try to live in such a way that no animal is ever killed, to more practical commitments to finding homes for stray cats. Although some will not listen to the views of others, there are many who are receptive to different thinking. They contribute to the debate by identifying areas of concern, and indicating the extent of disquiet within the community. Their role in lobby groups has dramatically influenced the political position of animal welfare in human society. Defenders of the present situation with regard to the ways in which animals are treated generally insist that humans should always come before animals. This anthropocentric insistence is often not convincing, especially when some of these defenders, keep pets in better conditions than humans are forced to endure elsewhere in the world. Many defenders of animal exploitation are unaware of the worst conditions in which animals are kept or ways in which they are treated. Some hardly understand the link between food and animals. Many are reluctant to think about the ways in which animals’ conditions have been so strikingly altered from the relatively tranquil conditions that often prevailed during their own or their parents’ childhood. For many people in this group, to hear an account of the less savoury current animal practices is unsettling. Others know about the science and ethics of animal welfare, and are convinced that present laws and practices are adequate in protecting animals. Another group of contributors are the philosophers, of whom Singer (1995), Regan (2001) and Rollin (1989) are perhaps the best known. The conceptual analyses and soul-searching of these thinkers have clarified some of the fundamental issues. However, the theoretical problems have never been entirely solved. Serpell (2004) points out that some people think of other species only in relation to their utility to humans whilst the attitudes of others are dominated mainly by affect, the positive and negative feelings that different animals evoke. Philosophers explain that there is variation within communities of people and variation amongst different nationalities and religions in attitudes to animals. Representatives from almost all religions make statements urging that the welfare of animals be considered, but practising members of those religions adopt a wide range of positions concerning what that entails. Philosophical analysis must be reconciled with biological reality as there are currently major disparities in approach between philosophy and biology. For example, in emphasising the importance of rights with little consideration of welfare, in understanding the biological significance of pain (Chap. 5) and in appreciating the distribution of sentience in the animal kingdom. Neither philosophers nor biologists and veterinarians alone will solve problems about animal welfare. They will need to collaborate, to discuss the issues and subsequently take action to inform the public and legislators (see Chap. 8). All must be willing to reconsider their opinions in the light of new information and new arguments. The process of greatest importance in solving welfare problems will be

1.4 Genetics, Epigenetics and What the Environment Can Change

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education, both of oneself and of the community. Philosophers and biologists must analyse their disciplines in relation to animal welfare so as to understand better the nature of the problems, especially those aspects extending across disciplines. More than either group seems to realise, philosophical propositions can be reduced to nonsense by biological misunderstandings, and biological pronouncements wrecked by logical inconsistencies. Integration of the disciplines is essential. The results of dialogue must percolate into the community and become part of public education. When political advisors can be given reliable information there is a chance that governmental, public, commercial and private actions concerning animals will be widely approved by society. The most conspicuous contributors to the animal welfare debate, the activists and lobbyists, will be evident as long as there is a need for them. They will continue to function as barometers of welfare problems. Critics will be muted only when there are no further grounds for criticism and society has accepted the prevailing level of animal welfare.

1.4

Genetics, Epigenetics and What the Environment Can Change

Every characteristic of every animal, including of course every human, results from interactions between genetic and environmental information. Although this has been said for many years, for example Broom (1981, pp. 13–15) wrote about the “universality of environmental effects on behaviour”, some scientists and most of the general public still clung to the idea that some qualities of themselves and other individuals are independent of environmental effect. However research, especially that in the last 5 years, makes it clear that every step in the translation of genetic information into proteins and other products that define characteristics of individuals can be altered by environmental factors (Alexander 2017). Also, some characteristics are affected by epigenetic effects that can be passed from one generation to another by routes that do not involve DNA (Tatemoto and Guerrero-Bosagna 2018). As explained further below, this means that no aspect of anatomy, physiology or behaviour of an animal is genetically determined, instinctive or innate where these terms mean independent of environmental effects. Whilst all characteristics are affected by genetic information in the DNA, nobody can say, for example, “my anti-social behaviour is in my genes so there is nothing that could be done about it”. Similarly, no breed of dog is always aggressive. There are difference in probabilities of characteristics related to gene-complement but all qualities of individuals also depend on the environment during the expression of genes and some qualities are affected by non-genetic factors passed from one generation to another. A consequence of such mechanisms is that when parents are stressed, their offspring, and sometimes further generations, can be affected. Poor welfare resulting from difficult living conditions or treatment can have effects later in life and effects on offspring.

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1 One Welfare, One Health, One Stress: Humans and Other Animals

The conditions in which an embryonic animal develops can alter its adult phenotype. It is not surprising that starved embryos may not develop normally but embryonic conditions can alter growth and there may sometimes be “developmental origins of adult health and disease” (Hammond 1932; Gluckman and Hanson 2004; Gardner et al. 2009). Behaviour of offspring can also be affected, for example high fibre diet in mother pigs was associated with less aggressive behaviour in the offspring (Bernardino et al. 2016). Adverse or enriched conditions during sperm or egg production can also have effects on offspring. In utero exposure to adverse conditions can lead to DNA methylation and other epigenetic effects that affect offspring development, disease risk and brain pathology (Cao-Lei et al. 2017; Delgado-Morales and Esteller 2017). An epigenetic trait is a stably heritable phenotype resulting from changes in a chromosome without alterations in the DNA sequence (Berger et al. 2009). An interesting aspect of some recent work is that the effects on offspring of poor welfare during gamete production and early development can be as great, or greater, in fathers than in mothers. Semen quality in mammals is better if high temperatures and poor nutrition are avoided (Wilson et al. 2004; Kunavongkrit et al. 2005; Sinclair et al. 2016). Boars with a high fear of humans had worse growth, immune responses and reproductive performance (Patterson and Pearce 1992) whilst socialized boars with good welfare had better semen quality (Flowers 2015). Stressed male mammals had different DNA methylation that was preserved in the zygote, in the adult offspring and in the following generation (Jeong et al. 2007; Østrup et al. 2013). The occurrence of these paternal effects indicates epigenetic inheritance whereby epigenetic variation, mediated via DNA methylation, post-translational histone modifications, or small non-coding RNAs induced in the male germline is transmitted to subsequent generations with consequences for a broad range of phenotypes such as metabolism, behaviour and neurobiology (Braun and Champagne 2014; Bohacek and Mansuy 2015). Some of the effects on the fathers involve glucocorticoids which alter small RNA molecules in sperm and lead to increased anxiety or depression and effects on glucocorticoids in offspring (Dietz et al. 2011; Short et al. 2016; Chan et al. 2018a). The seminal fluid microbiome can also have an effect on offspring (Javurek et al. 2016). Effects such as these, involving male and female parents, are reviewed by Chan et al. 2018b).

1.5

The Challenge Ahead

In order that animal welfare science can develop further and its findings be used, it is essential to establish basic terminology and build logical arguments on it. The key terms stress and welfare are defined and explained within a logical and scientific framework and methods of measurement are reviewed in Chaps. 2–6. The groups pondering the complexities of animal welfare ask that society should have greater awareness of animals’ needs. This key area of animal welfare research will be explained in detail in Chap. 7. From this base and from the ethical positions explained in Chap. 8, practical guidelines can be proposed for recognizing,

References

11

measuring, avoiding and alleviating stress and its effects and improving the welfare of individuals. The ethical question of what is a justifiable imposition on an individual will finally be considered, and a guide given on how to answer such a question.

References Alexander D (2017) Genes, determinism and god. Cambridge University Press, Cambridge, p 376 Berger SL, Kouzarides T, Shiekhattar R, Shilatifard R (2009) An operational definition of epigenetics. Genes Dev 23:781–783. https://doi.org/10.1101/gad.1787609 Bernardino T, Tatemoto P, Morrone B, Rodrigues PHM, Zanella AJ (2016) Piglets born from sows fed high fibre diets during pregnancy are less aggressive prior to weaning. PLoS One 11:1–11. https://doi.org/10.1371/journal.pone.0167363 Bohacek J, Mansuy IM (2015) Molecular insights into transgenerational non-genetic inheritance of acquired behaviours. Nat Genet 16:641–652 Braun K, Champagne FA (2014) Paternal influences on offspring development: behavioural and epigenetic pathways. J Neuroendocrinol 26:697–706 Broom DM (1981) Biology of behaviour. Cambridge University Press, Cambridge Broom DM (1985) Stress, welfare and the state of equilibrium. In: Wegner RM (ed) Proceedings of the 2nd European symposium on poultry welfare. World Poultry Science Association, Celle, pp 72–81 Broom DM (1986a) Foreword; the products. In: Broom DM (ed) Farmed animals. Torstar Books, New York, pp 9–11 Broom DM (1986b) Indicators of poor welfare. Br Vet J 142:524–526 Broom DM (ed) (2001) Coping with challenge: welfare in animals including humans. Dahlem University Press, Berlin, p 364 Broom DM (2003) The evolution of morality and religion. Cambridge University Press, Cambridge, p 259 Broom DM (2006a) Adaptation. Berl Munch Tierarztl Wochenschr 119:1–6 Broom DM (2006b) Behaviour and welfare in relation to pathology. Appl Anim Behav Sci 97:71–83 Broom DM (2007) Quality of life means welfare: how is it related to other concepts and assessed? Anim Welf 16(Suppl):45–53 Broom DM (2014) Sentience and animal welfare. CABI, Wallingford, p 200 Broom DM (2017) Animal welfare in the European Union. European Parliament Policy Department, Citizen’s Rights and Constitutional Affairs, Brussels, p 75. https://doi.org/10.2861/ 891355. isbn:978-92-846-0543-9 Broom DM, Fraser AF (2015) Domestic animal behaviour and welfare, 5th edn. CABI, Wallingford, p 472 Broom DM, Johnson KG (1993. (reprinted with corrections 2000)) Stress and animal welfare. Springer (formerly Chapman and Hall), Dordrecht, p 211 Budiansky S (1992) The covenant of the wild. William Morrow, New York Cao-Lei L, de Rooij SR, King S, Matthews SG, Metz GAS, Roseboom TJ, Szyf M (2017) Prenatal stress and epigenetics. Neurosci Biobehav Rev. https://doi.org/10.1016/j.neubiorev. 2017.05.016 Carr N, Broom DM (2018) Tourism and animal welfare. CABI, Wallingford, p 173 Chan JC, Nugent BM, Morrison KE, Jašarević E, Bhanu NV, Garcia BA, Bale TL (2018a) Epididymal glucocorticoid receptors promote intergenerational transmission 1 of paternal stress. Nat Neurosci 21:1061. https://doi.org/10.1101/321976

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Chan JC, Nugent BM, Bale TL (2018b) Parental advisory: maternal and paternal stress can impact offspring neurodevelopment. Biol Psychiatry 83:886–894. https://doi.org/10.1016/j.biopsych. 2017.10.005 Clutton-Brock J (1999) A natural history of domesticated mammals. Cambridge University Press, Cambridge Colonius TJ, Earley RW (2013) One welfare: a call to develop a broader framework of thought and action. J Am Vet Med Assoc 242:309–310 Delgado-Morales R, Esteller M (2017) Opening up the DNA methylome of dementia. Mol Psychiatry 22:485–496. https://doi.org/10.1038/mp.2016.242 Dietz DM, LaPlant Q, Watts EL, Hodes GE, Russo SJ, Feng J, Oosting RS, Vialou V, Nestler EJ (2011) Paternal transmission of stress-induced pathologies. Biol Psychiatry 70:408–414 Elwood RW (1979) Maternal and paternal behaviour of the Mongolian gerbil: a correlational study. Behav Neural Biol 25:555–562 EU D.G. Health and Food Safety (2016) Special Eurobarometer 442 attitudes of Europeans towards animal welfare. European Commission, Brussels Fernandez-Duque E, Valeggia CR, Mendoza SP (2009) The biology of paternal care in human and non-human primates. Annu Rev Anthropol 38:115–130. https://doi.org/10.1146/annurevanthro-091908-164334 Flowers WL (2015) Factors affecting the efficient production of boar sperm. Reprod Domest Anim, Zuchthygiene 50:25–30 García Pinillos R (2018) One welfare: a framework to improve animal welfare and human wellbeing. CABI, Wallingford, p 112 García Pinillos R, Appleby MC, Scott-Park F, Smith CW (2015) One Welfare. Vet Rec 179:629–630 García Pinillos R, Appleby M, Manteca X, Scott-Park F, Smith C, Velarde A (2016) One welfare – a platform for improving human and animal welfare. Vet Rec 179:412. https://doi.org/10.1136/ vr.i5575 Gardner DS, Ozanne SE, Sinclair KD (2009) Effect of the early-life nutritional environment on fecundity and fertility of mammals. Philos Trans R Soc B 364:3419–3427. https://doi.org/10. 1098/rstb.2009.0121 Gluckman PD, Hanson MA (2004) Living with the past: evolution, development, and patterns of disease. Science 305:1733–1736. https://doi.org/10.1126/science.1095292 Hammond J (1932) Growth and the development of mutton qualities in the sheep. Oliver and Boyd, Edinburgh Javurek AB, Spollen WG, Mann Ali AM, Johnson SA, Lubahn DB, Bivens NJ, Bromert KH, Ellersieck MR, Givan SA, Rosenfeld CS (2016) Discovery of a novel seminal fluid microbiome and influence of estrogen receptor alpha genetic status. Sci Rep 6:23027 Jeong YS, Yeo S, Park J-S, Koo DB, Chang WK, Lee K-K, Kang Y-K (2007) DNA methylation state is preserved in the sperm-derived pronucleus of the pig zygote. Int J Dev Biol 51:707–714 Karesh WB (ed) (2014) One health. O.I.E. scientific and technical review, vol 38. O.I.E, Paris Kunavongkrit A, Suriyasomboon A, Lundeheim N, Heard TW, Einarsson S (2005) Management and sperm production of boars under differing environmental conditions. Theriogenology 63:657–667 Kvarnemo C (2006) Evolution and maintenance of male care: is increased paternity a neglected benefit of care? Behav Ecol 17:144–148. https://doi.org/10.1093/beheco/ari097 López HH, Hay AC, Conklin PH (2009) Attractive men induce testosterone and cortisol release in women. Horm Behav 56:84–92. https://doi.org/10.1016/j.yhbeh.2009.03.004 Mason JW (1971) A re-evaluation of the concept of ‘non-specificity’ in stress theory. J Psychiatr Res 8:323–333 Monath TP, Kahn LH, Kaplan B (2010) One health perspective. ILAR J 51:193–198 Østrup O, Olbricht G, Østrup E, Hyttel P, Collas P, Cabot R (2013) RNA profiles of porcine embryos during genome activation reveal complex metabolic switch sensitive to in vitro conditions. PLoS One 8(4):e61547. https://doi.org/10.1371/journal.pone.0061547

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Patterson AM, Pearce GP (1992) Growth, response to humans and corticosteroids in male pigs housed individually and subjected to pleasant, unpleasant or minimal handling during rearing. Appl Anim Behav Sci 34:315–328 Podberscek AL (2005) The consumption of dogs and cats in China, South Korea and Vietnam. Report of Cambridge University Animal Welfare Information Service Regan T (2001) Defending animal rights. University of Illinois Press, Urbana and Chicago Rollin B (1989) The unheeded cry: animal consciousness, animal pain and science. Oxford University Press, Oxford Roney JR, Mahler SV, Maestripieri D (2003) Behavioral and hormonal responses of men to brief interactions with women. Evol Hum Behav 24:365–375. https://doi.org/10.1016/S1090-5138 (03)00053-9 Roney JR, Lukaszewski AW, Simmons ZL (2007) Rapid endocrine responses of young men to social interactions with young women. Horm Behav 52:326–333. https://doi.org/10.1016/j. yhbeh.2007.05.008 Serpell JA (2004) Factors influencing human attitudes to animals and their welfare. Anim Welf 13: S145–S151 Short AK, Fennell KA, Perreau VM, Fox A, O’Bryan MK, Kim JH, Bredy TW, Pang TY, Hannan AJ (2016) Elevated paternal glucocorticoid exposure alters the small noncoding RNA profile in sperm and modifies anxiety and depressive phenotypes in the offspring. Transl Psychiatry 6: e837. https://doi.org/10.1038/tp.2016.109 Sinclair KD, Rutherford KMD, Wallace JM, Brameld JM, Stöger R, Alberio R, Sweetman D, Gardner DS, Perry VEA, Adam CL, Ashworth CJ, Robinson JE, Dwyer CM (2016) Epigenetics and developmental programming of welfare and production traits in farm animals. Reprod Fertil Dev 28:1443–1478 Singer P (1995) Animal liberation. Random House, London Tatemoto P, Guerrero-Bosagna C (2018) Biological dogmas in relation to the origin of evolutionary novelties. In: Pontarotti P (ed) Origin and evolution of biodiversity. Springer, Cham, pp 317–330. https://doi.org/10.1007/978-3-319-95954-2_17 von Holdt BM, Pollinger JP, Lohmueller KE, Han E, Parker HG, Quignon P, Degenhardt JD, Boyko AR, Earl DA, Auton A, Reynolds A, Bryc K, Brisbin A, Knowles JC, Mosher DS, Spady TC, Elkahloun A, Geffen E, Pilot M, Jedrzejewski W, Greco C, Randi E, Bannasch D, Wilton A, Shearman J, Musiani M, Cargill M, Jones PG, Qian Z, Huang W, Ding Z-L, Zhang Y-P, Bustamante CD, Ostrander EA, Novembre J, Wayne RK (2010) Genome-wide SNP and haplotype analyses reveal a rich history underlying dog domestication. Nature 464:898–902 Wilson ME, Rozeboom KJ, Crenshaw TD (2004) Boar nutrition for optimal sperm production. Adv Pork Prod 15:295–306 World Health Organization (1948) Preamble to the constitution of the World Health Organization. In: Official records of the World Health Organization, vol 2. WHO, Geneva, p 100

Chapter 2

Adaptation, Regulation, Sentience and Brain Control

Abstract In this chapter, the central focus is on the mechanisms used by animals to control their interactions with all aspects of their world. In order to understand what is stressful and what situations lead to good or poor welfare, we need to know about the systems with which humans and other species regulate their lives. Research on motivation has long been a major aspect of animal welfare science. Since the brain is the source of control mechanisms its complexity of function is a key issue. Which animals are sentient and when during development do humans and other animals become sentient? What are the roles of the complex mechanisms that we call feelings and emotions? Terms defined in this chapter include: adaptation, homeostasis, sentience, causal factor, motivational state, gain, need, frustration, pain, feelings, emotion and suffering. Keywords Adaptation · Brain control · Motivation · Sentience · Feelings · Emotion

2.1

Adaptation

The study of stress and welfare is a key area of fundamental science concerned with: the stimuli that pose challenges, how humans and other animals deal with problems that might put present and future efficiency of functioning at risk and how benefits to the individual are maximised. In this chapter, some of these key mechanisms are explained. In order to ensure that welfare is good during everyday human life, or during the use of animals in a human-orientated environment, we need to know about the ability of humans and other animals to adapt. Human success is due especially to adaptability whilst the process of domestication depends upon the efficiency of adaptation by the animals concerned. However, “adaptation” has several biological meanings (Broom and Johnson 1993; Broom 2001a, 2006a). At the cell and organ level, adaptation is the waning of a physiological response to a particular condition. This includes the decline over time in the rate of firing of a nerve cell. At the individual animal level, adaptation is the use of regulatory systems, with their behavioural and physiological components, in order to allow an individual to © Springer Nature Switzerland AG 2019 D. M. Broom, K. G. Johnson, Stress and Animal Welfare, Animal Welfare 19, https://doi.org/10.1007/978-3-030-32153-6_2

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cope with its environmental conditions. In evolutionary biology, as a noun, adaptation is any structure, physiological process or behavioural feature that makes an organism better able to survive and to reproduce in comparison with other members of the same species. This definition, without reference to behaviour, also applies to plants. Also: the evolutionary process that leads to the formation of such a trait (Broom and Fraser 2015). Hence, adaptive behaviour in an individual could help the individual without increasing fitness but if it is adaptive behaviour in a species that is referred to, adaptive would imply increased fitness. In relation to the first definition of adaptation, neural mechanisms that sense the environment often decline in their response as they are exposed to continuing or repeated stimulation. For example most sensory receptors show more of a phasic than a tonic response to continuing stimulation in that the rate of firing in the axon from a sensory neuron reduces over time (Broom 1981b). Such changes in receptors may result in reduced imposition of the environment on the animal, information gain without energy wastage, efficient use of information channels, possibilities to distinguish stimuli, and avoidance of information overload. Sensory receptors adapt at different rates, for example vibration receptors in less than a second, touch receptors in a few seconds, temperature receptors in minutes, and blood pressure receptors over a number of days. Pain receptors adapt little and if there is adaptation, it is slow (Broom 2001b; Clarke et al. 2014). The adaptation in receptors often occurs in single cells or in a combination of receptor cell and sensory neuron. However, a change in the frequency or intensity of responses of animals to repeated stimulation is often a much more complex matter (see below).

2.2

Homeostatic Control

Life within a cell, tissue or body depends on a supply of essential nutrients, on mechanisms to process them, and on arrangements for disposal of waste. Just as importantly it requires a network of control systems that adjust the inputs and outputs to ensure that chemical transformations occur in an environment of relative constancy. The vitality of all animals, from single-celled protozoans to multi-celled whales, depends ultimately on the efficient operation of the regulatory systems that control the conditions within their bodies. In an animal, homeostasis is the maintenance of a body variable in a steady state by means of physiological or behavioural regulatory action. The steady state is that is maintained varies within limits that are tolerable for the individual. Regulatory systems which maintain homeostasis are referred to as homeostatic. If homeostatic mechanisms within a living animal were to operate with wheels and cogs, they would whirr continuously. At every instant of an animal’s life, when it changes position, when the light or temperature levels alter, or when food or other resources become available, adjustment of function is required so that the state of the

2.2 Homeostatic Control

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body remains stable. Stability of brain functioning is just as important as that of other parts of the body. Most alterations in the environment and the stimuli that result from them, elicit appropriate responses so that homeostasis is maintained. Sometimes adaptation to stimuli from the environment is not immediately possible because they are excessive in intensity or duration, or noxious, or they are novel so that no system yet exists for coping with them. Inadequacy of the regulatory systems then leads to a displacement of state outside the tolerable range. The animal’s attempts to adapt to its environment are inadequate, and the likely results are injury, poor health, suffering and reduced survival chances. Analyses of control systems consider inputs, the various kinds of information passing into the system, and outputs, the resultant responses arising from the system, as well as the processes that relate inputs to outputs. The most numerous inputs to an animal’s regulatory systems come via its sensory nerves. The light impinging on an animal, the temperature of its surroundings, and pressures on its surface, together with sound, smell, taste and other less obvious factors such as gravity, apprise an animal of its environment via neural sensory mechanisms. Animals, other than the simplest, collect both non-specific information about the environment, for example via proprioceptor inputs that tell the individual about the relative positions of its limbs, and specialised information, such as sound, via the cochlea and visual patterns from the retina. Even the simplest animals have sensory systems. These may respond to general environmental changes, or be specific, such as the sites receptive to calcium ions in the protozoan malaria parasite Plasmodium (Gazarini and Garcia 2004) and receptors to heat shock protein 90 in Plasmodium, Trypanosoma, Leishmania and Giardia (Roy et al. 2012). Small changes in inputs from sensors can have important influences on an animal’s activity, such as when the presence of specific molecules allows adaptive reactions to the environment, including host defences in protozoan parasites, or light intensity influences the laying patterns of birds. Although some regulatory processes in the body are affected by simple inputs, most involve responses to inputs that are multiple and complex. Even initially simple inputs may be interpreted in the light of previous experience and compared with other inputs so as to build up a more accurate and elaborate picture of the environment and of the relevance of changes in that environment for the individual. In addition to providing information about the environment outside an animal’s body, or the physical state of its body, some inputs to the system in the brain that controls behaviour and other interactions with the environment arise from the brain’s emotional system. The significance of fear, anxiety and pain in this respect is so important that it is considered separately in Sect. 2.7. At this stage of our discussion of control systems it is important to emphasise that a single simple sensory change, such as the sight of a potential predator or rival, can be processed so that the ultimate input is very complex. It could initiate not only complex responses dependent upon previous experience, but new bodily changes such as the release of adrenal hormones that will themselves have an important effect on functioning of the control systems.

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Sentience and the Role of the Brain in Coping

Some inputs to control systems are simple and some are complex but, in all animals with a central aggregation of neurons, the control of interactions with the environment is located in the brain. Behaviour, and some of the physiological functioning of the body, are controlled by the brain. An individual’s perception, cognition, awareness and feelings occur in the brain of that individual and are the consequence of, or cause of, the functioning of sensory mechanisms, muscular responses, glandular responses and other bodily changes. The organs of the body, for example the heart, will influence brain function but thoughts and feelings are in the brain and not in the heart or any other part of the body. Emotions are not located in the heart and it is incorrect and logically harmful to say “I know in my heart” or when referring to a feeling, “My heart told me...”. The analytical, thoughtful and emotional aspects of the functioning of the brain are closely intertwined so it is not useful for the concept of mind to be considered separately from the brain (Panksepp 1998, 2005; Broom 2003, 2014; LeDoux 2012) except perhaps where it means the same as soul, or a component of spirit, and refers to links among individuals. There is a stage of development in humans and in other more complex animals when they become aware of themselves (DeGrazia 1996) and of their interactions with their environment. This is the point when they have ability to experience pleasurable states such as happiness and aversive states such as pain, fear and grief, i.e. they become sentient. Kirkwood (2006) proposed that to have sentience, the individual must “have the capacity to feel”. This capacity involves awareness and cognitive ability so is principally in the brain. Sentience means having the capacity to have feelings. Kirkwood also said “to be sentient is to have a feeling of something”. Whilst sentience implies having the range of abilities that are required to have feelings, it does not mean actually having the feelings as an individual can be sentient when it is not having feelings. A sentient being is one that, in order to have feelings, has some ability: to evaluate the actions of others in relation to itself and third parties, to remember some of its own actions and their consequences, to assess risks and benefits and to have some degree of awareness. This definition is slightly modified after Broom (2006b). Various aspects of sentience are discussed by Broom (2014). More information about cognitive and emotional functioning of a wide range of animals is reported in scientific papers each year. We know that pigs, magpies and cleaner wrasse fish can use information from mirrors, crows and bees can count, young cows show emotional responses to having learned something new and very many non-human species recognise individuals of their own and other species (Hagen and Broom 2004; Broom 2014; Howard et al. 2018; Kohda et al. 2019). Human opinion about which individuals of our own and other species are sentient has changed over time, where people have access to factual information, to encompass, first all humans instead of just a subset of humans, and then: certain mammals that were kept as companions; animals that seemed most similar to humans such as

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monkeys; the larger mammals; all mammals; all warm blooded animals; all vertebrates; and now also some invertebrates. The general public has been ready to accept some guidance about evidence for sentience from biologists who have collected information about the abilities and functioning of the animals. Animals that are shown to be complex in their organisation, capable of sophisticated learning and aware are generally respected more than those that are not, and such animals are less likely to be treated badly. However, some people still view animals solely on the basis of their effects on, or perceived extrinsic value to, humans and have little concern for them as individuals.

2.4

Habituation and Sensitisation

A characteristic of nervous mechanisms as they sense the environment is the decline, or sometimes increase, in their response when they are exposed to repeated stimuli. If the response increases it is sensitisation, if it decreases it is habituation. Habituation involves complex processing and is very seldom the result of simple adaptation of receptors or of fatigue in muscles. It is often very specific (Sokolov 1960; Broom 1968, Chap. 3) so the brain processes involved must be as elaborate as those that occur during conditioning. When a stimulus signalling the need for action is perceived, the delay before the maximal response, whether physiological such as a heart-rate change or behavioural, varies according to the sensory modality and the context. Some of this variation is a consequence of the functioning of receptor cells and sensory neurons but sophisticated brain processing, including inhibitory effects on sensory cell functioning usually plays a major part. The neural response to a sudden event, such as a peal of thunder, reaches a peak in no more than a few seconds and behavioural changes are usually also brief. Orientation reactions are rapid and startle responses range from absent to substantial depending on sound level and degree of familiarity with thunder. Responses to painful or other noxious stimuli will also depend on magnitude of input and perceived risk of further problems. The peak response may be reached in seconds or may be delayed according to which other emergency physiological and behavioural processes are initiated. Once the peak response is passed, adaptation is occurring but may not be complete for some minutes or hours. Habituation occurs more readily to some types of stimuli than to others. The sound of a branch falling from a tree might elicit a startle response from a person or other animal in a wood the first time it is heard, but frequent recurrence of the stimulus with no adverse effects would result in habituation. However, the same individual would be unlikely to habituate to the sight of a hunting leopard. Similarly, birds feeding in fields may not readily habituate to a sight or sound similar to that of a potential predator. Some bird scarers are probably effective because the bird experiences some uncertainty about whether the object perceived is dangerous (Fazlul Haque and Broom 1985).

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If a disturbing environmental event is detected, such as the sight of a hunting leopard or a twig cracking as a large animal walks on it, the responses to repetition of this stimulus are likely to become greater rather than smaller. Such an increase in response to continuing or repeated stimulation is called sensitisation and may be thought of as a facilitation of the response. This learning process will tend to exaggerate responses. Another example of sensitisation is the increase in response to the light touch of a biting fly on the skin when this touch is repeated. The effect may also be seen when a dog or human child, presented several times to a veterinary or medical doctor for an injection, reacts more and more adversely, even though the stimulus situation is essentially constant.

2.5

Motivational State

The inputs which an animal receives as a consequence of changes in its world are interpreted in relation to previous experience. In other words, some event in the past has changed the brain in such a way that when a particular kind of sensory input is received, the information that it provides for the individual is different from that which such an input provided the first time that it was experienced. The brain receives, analyses and interprets inputs so that the animal has a perception of its environment which can be used when taking decisions about what action to carry out next. Each input which provides information to the decision-making mechanism of the brain about an aspect of the animal’s world can be considered a causal factor (McFarland 1971) for it may alter the animal’s future behaviour and physiology. The levels of some causal factors provide information about the world outside the animal, for example the brightness of light detected by the eye. Other causal factors reflect variables within the animal, such as blood glucose levels, the concentration of a steroid hormone in the blood, or the output from some internal time-clock. Each sensory signal or result of internal body monitoring is interpreted in the light of previous experience (Broom 1981a, b; Broom and Fraser 2015). Hence causal factors are defined as inputs to the decision-making system, each of which is an interpretation of an external variable or an internal state of the body. The internal state referred to includes that of systems in the brain as well as that of other body systems. The causal factors which emanate from within the brain include ‘ideas’ which are not an immediate consequence of input from sensors, for example in the case of a dog which stands up and goes directly to the site of a buried bone and unearths it. There are also causal factors which are the consequences of more general brain activity resulting from many kinds of input. If a dog is deprived of water, after some time there will be input to the brain from: (a) monitors of body fluid composition; (b) sensory receptors indicating a dry mouth; (c) probably from oscillators which have a regular output and might initiate drinking at particular times of day or after particular intervals; and (d) other brain centres which could make the animal aware that drinking has not been possible for some time. The change in the state of the animal arising from this group of causal factors is

2.5 Motivational State

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shown in Fig. 2.1. As the levels of these causal factors rise there will also be increases in the likelihood of drinking if the opportunity arises and in the extent of related activities that would promote water acquisition. The actions of an animal will depend upon the levels of many different causal factors. This can be represented in a diagram (Fig. 2.2) that depicts for a dog the

Fig. 2.1 Levels of causal factors that promote a particular action vary over a range, and the state of the animal can be described in terms of these (after Broom and Fraser 2015)

Fig. 2.2 Motivational state of animals A, B, and C in two-dimensional causal factor space. Animal A is most likely to drink, whereas animal B is most likely to eat. The changes in state of animal C are explained in the text (after Broom and Fraser 2015)

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interaction of two sets of causal factors: those resulting from, firstly water deficit and secondly food deficit, in what is known as ‘causal factor space’ (McFarland 1971; Sibly and McFarland 1974). The decision of an animal about what to do will depend upon its position in this causal factor space with respect to the two axes, that is, to the two sets of causal factors. In Fig. 2.2 a dog whose state has reached B is more likely to eat and to work in some way to get food than one whose state is at O, while an animal whose state is at A is more likely to drink than one whose state is at O. Plotting the state of the animal in this two-dimensional space allows interactions between the two sets of causal factors to become clear. When a dog is deprived of water its state moves up towards A on the state space plot but it also moves to the right because dogs given no water cannot eat as much. The change in state of the animal as a consequence of water deprivation is shown as a trajectory from O to C1. If this animal were then deprived of food as well as water, its state would move to the right and up further to C2. The behaviour of an animal that is given the opportunity to either eat or drink will depend upon its state as represented in Fig. 2.2. A dog whose state is at C2 is a little higher on the water deficit side so it might drink. This would bring its state down across the boundary line to C3 at which time it might switch to eating, thus lowering the causal factors resulting from food deprivation. An example of a possible course of the animal back to O is shown. The dog whose state is at C2 might drink enough to move its state to the O level and then eat. The position of the boundary line for switching from feeding to drinking could be altered by making the animal search harder for the food or use more energy to get the water (Larkin and McFarland 1978). In reality an animal’s decisions will depend also on many other causal factors, each with its own dimension. The motivational state of an individual is a combination of the levels of all causal factors in the brain, or more technically, its position in multi-dimensional causal factor space. Another way of explaining the changes in motivational state is that animals, including humans, are constantly under pressure to embark on various activities such as drinking, grooming, mating, etc. Which of these is undertaken will be determined by the strengths of the various sorts of biological and social pressure. The activity or activities finally pursued would be that, or those, for which the overall pressure is greatest at the time. The dog referred to in Fig. 2.2 might have recently eaten salty food and hence there would be causal factors resulting from the taste of the food, the concentration of blood or saliva, the delay since drinking last occurred and the visual cues from a water source, all of which would promote the likelihood of going to drink. However, drinking might be delayed because of other causal factors resulting from the approach of a person carrying a stick, or the odour of a bitch, or the detection of a very palatable food item. All of these causal factors are a part of the motivational state of the dog, and one or more of them will determine which action is taken next. In summary all actions, except for a small number of simple reflexes, are determined by an animal’s motivational state. An understanding of motivational processes is therefore fundamental to the assessment of animal welfare using behavioural and

2.6 Outputs from Decision Centres

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physiological measures. Links between motivation, control during life, stress and welfare are discussed by Shah and Gardner (2008) and Broom and Fraser (2015).

2.6

Outputs from Decision Centres

An understanding of the cause and nature of output responses from regulatory systems after the motivational state has been altered is essential for the study of stress and welfare. Such responses are not only indicators of the adjustment of an individual to its environment, but also potential indicators of maladjustment.

2.6.1

Neural and Muscular Outputs

In more complex animals, outputs from decision centres commonly appear as various forms of neural and muscular activity. These may be no more than an electrical spike in the brain waves, shown on an electroencephalogram (EEG), as the signal reaches another system in the brain and they may cause no other physical sign. Such a sensory perception committed to memory may scarcely be measurable, yet it may exert a profound influence on the shaping of future responses. Most of what we call responses, however, are changes in whole body position or pattern of locomotion brought about by nervous control of muscular movement. A slight change in posture might be a response to sensory signals from aching joints, whilst a jump to catch prey might follow the sight of a darting insect. Less complex animals have proportionally less machinery to handle outputs, though even the simplest have mechanisms to co-ordinate their physical activity and retain information about past events. Some neuromuscular responses are structurally coupled to input signals so that they almost always follow a particular stimulus so are reflex responses. They are of survival value in eliciting an instant response to a noxious stimulus, but an unvarying nature of the response introduces an inflexibility that can reduce an animal’s capacity to adapt. Responses described as monosynaptic reflexes can be inhibited or facilitated by central nervous action in some circumstances (Crone et al. 1990). Behavioural responses are generally subject to many possibilities for variation according to other environmental impacts and hence information available to the individual animal. Some responses may vary little whilst others are seldom the same from one occasion to another. Examples of behaviour that varies little are repetitive behavioural routines such as stereotyped bar-biting by individually stalled or tethered sows (see Chap. 6). Repetitive routines are coordinated muscle movements which arise from maladaptation to the environment or malfunction of the sensory, integrative, decision-making or motor system. In all of those, except the motor malfunction, we need to know about the motivational state in order to understand the behavioural abnormality. What can be changed in the animals or the environment to break this cycle of apparently inappropriate behaviour? These are the types of

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question one finds at the core of some psychiatric disorders and animal welfare problems.

2.6.2

Hormonal and Neurohormonal Outputs

Environmental events which should be activating a homeostatic control system may not always have consequences that are outwardly evident to a human observer. Many occasions arise in which a hormonal response is evoked but there is no immediate evidence of a change. As examples, eating a large meal induces insulin release from the pancreas, and decreasing air temperature triggers the release of metabolic hormones from the thyroid gland. Externally the effects are not visible for some time, if ever, yet the mechanisms contribute significantly to an animal’s adaptation. Because they can be measured, such hormonal changes can provide insights into the processes of homeostatic control and physiological adaptation. A response of particular significance when complex animals adapt during interactions with predators or social challenges is that described by Cannon as the ‘fight or flight’ reaction (Cannon 1935). This sympathoadrenal response involves both neural and hormonal outputs. The hormones are the catecholamines adrenaline and noradrenaline, called epinephrine and norepinephrine in North America. Excitement, anxiety or alarm, initiated either within the animal or from an external challenge, result in a coordinated response of the autonomic nervous system including the medullae of the adrenal glands. The sympathetic component includes postganglionic neurons that release noradrenaline. This noradrenaline acts directly in the tissue where it is released, rather than being carried in the bloodstream. The adrenal arm of the system involves the endocrine chromaffin cells in the adrenal medulla that secrete adrenaline and noradrenaline into the blood stream (Turner et al. 2012). The nerves, together with adrenaline and noradrenaline, increase cardiac output, increase breathing rate and redistribute blood flow to organs thus preparing the individual physiologically to cope with an emergency. This alarm reaction, while unquestionably a beneficial and sometimes life-saving output from control systems, is relatively inflexible and, like some nervous reflexes, may commit an animal to a response even when it is inappropriate. The adrenal cortex also has a central role in the hormonal response to disturbance of homeostasis. Following various types of both internal and external stimuli, these outer segments of the adrenal glands will release glucocorticoid hormones affecting energy and protein metabolism and immunological reactions, or in other circumstances, mineralocorticoid hormones affecting body fluid balance. The first stage of the response of the hypothalamic-pituitary-adrenal cortex (HPA) axis response is the activation of corticotrophin releasing hormone (CRH) production in specialised neurons in the paraventricular nuclei of the hypothalamus (Chrousos and Kino 2007). Vasopressin in mammals, or vasotocin in other vertebrates, may be produced by these neurons at the same time (Tilbrook 2007). The CRH results in the release of the peptide pro-opiomelanocortin from the adenohypophysis (anterior pituitary).

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The component parts of pro-opiomelanocortin include adrenocorticotrophic hormone (ACTH), endorphins and enkephalins. ACTH is transported in the blood to the adrenal cortex where cortisol and corticosterone production occurs. ACTH also regulates gene expression of noradrenaline synthetic enzymes in the superior cervical ganglia and locus coeruleus so there is interplay between the sympathetic and HPA systems (Serova et al. 2008). The spelling of corticotrophin releasing hormone and adrenocorticotrophic hormone should be “trophin/trophic”, which means affecting or determining growth, and not “tropin/tropic”, which means affecting or determining direction of movement or orientation, because the action of these hormones is not to determine direction. The glucocorticoid hormones cortisol and corticosterone circulate in the blood and facilitate the production of extra energy, to help cope with the emergency, before being broken down by enzymes after a period of many minutes. They stimulate proteolysis and gluconeogenesis and bring about anti-inflammatory effects. In some animals, only one of these glucocorticoids is produced and in others both are produced. The glucocorticoid cortisol is produced in many mammals, such as primates, carnivores and ungulates, and in other animals. Corticosterone has the same function, being produced in rodents and many birds, including poultry. The hypothalamic–pituitary–inter-renal response of fish that experience adversity involves inter-renal tissue whose cell functions are very similar to those of the mammalian adrenal gland and can be measured in the same way (Mormède et al. 2007). Maximal concentrations of cortisol are produced in a trout when it is removed from water, an extreme emergency situation that causes it to be deprived of oxygen. Glucocorticoids have widespread effects in the body and it is estimated that they influence the expression of approximately 10% of the genome with targets including genes controlling metabolism, growth, repair, reproduction and management of resource allocation (Ralph and Tilbrook 2016). A high proportion of cells in the human body have receptors for glucocorticoids. Hence changes in plasma concentrations of cortisol or corticosterone may be associated with many different body functions. Activities such as energetically searching for food, courtship and mating are associated with increases in plasma cortisol concentration. Glucocorticoids are synthesised in a diurnal pattern, affected by light and other factors, with the peak blood concentration in the morning in diurnal species and in the evening in nocturnal species (Mormède et al. 2007; Turner et al. 2012). The daily fluctuation in the secretion of cortisol and hence in plasma cortisol concentration, in humans begins with a distinct sharp rise of cortisol at the time of waking, followed by a steady decline over the course of the day, with the lowest levels in the early morning hours. The cortisol facilitates effective learning, via the functioning of the hippocampus, and maintains other normal functions in the body (Broom and Zanella 2004). Hippocampal cells actively take up cortisol in vitro. Extreme adversity can suppress the daily cortisol cycle in humans (Kivlighan et al. 2008) and lead to less effective hippocampal function and hence worse learning ability and memory. Glucocorticoid effects on memory depend on noradrenaline mediated activation of the amygdala in humans (van Stegeren et al. 2007). As a consequence of the many beneficial effects and functions of cortisol and corticosterone, changes in concentrations of these

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hormones are often not indicators of stress or poor welfare (Broom 2017). They are very useful indicators in some circumstances but the context of the observations is crucial in the interpretation of these measures. Cortisol and corticosterone in the blood are normally bound to globulin proteins for 80–90% of the time but, although only free glucocorticoids can enter cells and bind to receptors, it is widely assumed that glucocorticoids readily switch from the bound to the free forms (Ralph and Tilbrook 2016). Several factors, that can be relevant to function, affect the binding of the glucocorticoids to the binding globulin. The work of Kumsta et al. (2007) shows that, especially when glucocorticoidbinding globulin concentrations are high, there is some regulatory effect on the amount of available glucocorticoid. Hence glucocorticoid-binding globulin can have a regulatory effect on HPA axis response patterns. This finding requires further investigation and is relevant to women using oral contraceptives as these can alter glucocorticoid binding globulin concentrations. A further function-regulating mechanism in blood and other tissues is that active cortisol can be converted by the enzyme 11 β-hydroxysteroid dehydrogenase to inactive cortisone. The glucocorticoids act by binding to cells in what are usually called target tissues. After a period, cortisol and corticosterone are removed from the blood. The use of glucocorticoid measurement in blood, saliva, urine, milk and faeces as part of welfare assessment is discussed by Mormède et al. (2007). As Ralph and Tilbrook (2016) emphasise, glucocorticoid measurements can give a range of information about affective states in humans and other animals. The consequence of an animal receiving a sensory signal about its environment may be outwardly zero, or a reaction as simple as the flicker of an eyelid, or a complex reaction under the influence of catecholamines and glucocorticoids comprising physiological adjustments of the cardiovascular, respiratory, metabolic and hormonal systems, together with some integrated behavioural response. In the short term these responses usually serve the function of promoting homeostasis in the animal. Over longer periods such responses have further significance for any animal as they may be remembered. Actions with consequences that are pleasant, neutral, or unpleasant may therefore cause any subsequent response to be altered. The commitment to memory of the effects of a sensory experience may not be immediately evident, but the consequences for ensuing responses can be profound. The role of past experience in shaping responses of the regulatory system is of great importance in determining the impact of fear, loneliness, anxiety, aggression, commitment, satisfaction and so on, all of which have significant influences on welfare.

2.7 2.7.1

Control Systems and Needs Simple Models of Control

Control systems are functional mechanisms which receive inputs and determine outputs. They may be simple or complex, most involve the brain and in many

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there are hormonal components. The operation of nerve networks is often influenced by hormones while hormone secretion is usually affected by nerve activity. Simple controls operate within nerve fibres themselves, in that they either fire and carry an impulse, or they do not. A stimulus that does not bring a nerve to its firing threshold disappears, and is filtered out. A somewhat more complex control is exemplified by the reflexes that constantly modify input-output relations of skeletal muscle via neural links in the spinal cord and central nervous system. Contraction of skeletal muscle is induced by impulses arriving in motor neurons. The impulse output is modified by signals, reflecting the degree of muscle stretch, sensed by the spindle receptors in the muscle and by Golgi tendon organs that inhibit contractions which would approach the mechanical limit of the muscular system. Another complexity is that muscle actions are modified by the composition of the body fluids, for example by the concentration of thyroid hormones. The complications of this control are multiplied many times over when body functions depend on the processing of signals into and out of the brain. In such cases, numerous inputs, both facilitatory and inhibitory, converge on the control centres to determine the output. Furthermore, the output is influenced by the composition of the surrounding fluid, including its content of any cyclically changing sex hormones, as well as by previous experience through the influence of memory. Hormonal control systems can also operate in a simple fashion. Insulin, which reduces blood glucose concentration, is produced from the pancreas in proportion to rises in glucose concentration, and hence prevents large rises in blood glucose from occurring, for example after eating. The control of insulin secretion is via glucose and calcium ions together with metabolic and neurohormonal amplifying pathways (Henquin 2011). Thus hormonal control systems are subject to nervous influences, just as nervous control systems are affected by hormones. These two components of the response of an animal to its environment can be viewed as elements of a combined control system that determines the animal’s physiology and behaviour. Simplified physical models of the relations between inputs and outputs are depicted in Fig. 2.3a. Other systems relating inputs to outputs also occur, for example ‘on-off’ controllers, but the type shown in Fig. 2.3b with a proportional controller and adjustable set point is one that seems to occur widely. It will be used later as a model on which to base discussions of stress. The simplest proportional controller (Fig. 2.3a) can be drawn as a rigid rod pivoting on a fulcrum, linking inputs to outputs in direct proportion. A more refined version of this system (Fig. 2.3b) operates in the temperature controller of a domestic central heating system. The air temperature is sensed at various points in the house, causing heating to be adjusted so that the colder the house the more the heaters are activated. This is negative feedback control. The temperature signals entering the system are integrated, and collectively they control a heat output that varies in magnitude or duration so that it is proportional to the input error. The magnitude of the response for a given change in input is called the gain. In Fig 2.3a, the gain depends on where the fulcrum is placed under the lever. The gain may vary from one control system to another, and may change from time to time within one control system. The gain is therefore adjustable. Since the fulcrum under

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Fig. 2.3 Models of biological control systems. (a) rod pivoting on fulcrum (b) also a proportional controller but like that of a domestic central heating system in that it has an adjustable set point and gain (after Bligh 1973)

the rod linking input and output in Fig. 2.3a is closer to the input end than the output end, small changes in inputs bring about large responses; in other words this system as depicted has a high gain. The output, or response, in such a system is not simply turned on or off. It operates at an intensity dependent on the strength of the input signals. To achieve this, there must be within the regulator system (Fig. 2.3b), components that integrate the inputs, compare them with a set-point or optimal value, and co-ordinate the outputs. The output to effectors can change, either because the input has changed or because the set-point for control has altered. This last change is akin to turning the thermostat of a central heating system up or down. Many physiological mechanisms have the capacity to change as though the set-point was being altered. A control system of this type is described as being a ‘proportional controller with adjustable

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set-point and gain’. Examples will emerge in later discussions of an animal’s responses to incoming stimuli being varied by adjustments that appear to be due to alterations of the set-point or of the gain of the control system.

2.7.2

Motivational State as the Determinant of Action

The notion that an animal acts to stabilise its internal environment via an assortment of homeostatic systems was introduced in Sect. 2.1. The proposal was then developed by reasoning that an animal achieves this by integrating a myriad of inputs, including those from sensors, which may be as simple as those resulting from changes in light intensity, or as complex as the recognition, following experience, that a certain site in a field will provide shelter. Inputs from external sensors, internal monitors or rhythm generators and from other brain centres are the causal factors that together make up the motivational state. It is this state which leads to an animal carrying out particular activities. Furthermore, changes in causal factors may modify not only the motivational state but also the set-point and the gain of an animal’s regulatory systems. As an example to illustrate this concept. Consider a sheep, at pasture in hot summer conditions, which has not drunk for 12 h. Its body fluids are becoming concentrated and several causal factors are becoming stronger and increasing the likelihood that the animal will drink. These may include inputs from monitors of body fluid concentration, mouth receptors, the memory of the time since the last drink, and temperature receptors. In other words, the sheep is becoming more and more thirsty. The more concentrated the body fluids, the stronger the animal’s interest in seeking water. If water were near, the animal would drink. But as other sheep in the flock have not yet moved to the water trough, the animal is disinclined to walk there alone. The normal motivational output from the body fluid regulatory system is outweighed by the causal factor resulting from the animal’s preference to stay with the flock. A body fluid concentration greater than that which usually occurs at this time of day is required to prompt this animal to drink. Gregariousness has raised the threshold that must be reached before the animal will drink. In control terminology, it is as if the set-point has been raised. Finally, other sheep begin to walk to the water and the constraint on the focal animal not to move alone is removed. The set-point returns to normal. At this stage, the same sheep has higher levels of causal factors promoting drinking than do other animals in the flock, and it runs faster than they do. A further control process now determines how much it will drink. Since the weather is warm causal factors resulting from this have some influence. The warmth indicates, perhaps without any higher level concepts being involved, that a greater water input than usual may be required. The animal uses the available information, predicts its future needs and drinks more water than usual for a given elevation of body fluid concentration. The drinking response is enhanced or, put another way, the gain of the

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control system is increased. This ability to change the gain so as to prepare for probable future needs is a form of (see Sect. 2.8.2) control. This example, despite its complexity, is still a simplification of the operation of the type of system believed to control animal behaviour. Nonetheless, it serves to illustrate the enormous variety of inputs, and how events might be interpreted in terms of alterations in stimulus input, set-point or gain. Every aspect of an animal’s life is under a control system as complicated as this, including simple responses such as standing, lying, scratching and chewing. Complex activities such as foraging, predation, mating, social bonding, responding to inappropriate or immoral behaviour, or aggression require even more complicated integration and processing.

2.7.3

Other Concepts that Have Been Used to Explain Motivation

When non-human animals were thought of as being largely automata, the term instinct was often used to explain how their behaviour was organised. It was assumed that some inherited property of an animal made it act in an automatic way in certain circumstances. As explained in Chap. 1, the idea that there can be development without environmental influence is now demonstrated to be wrong and detailed studies of both gene action and behaviour show that animals are far from being automata, so the terms instinct, innate and genetically determined are no longer used. Another term used in motivation research was drive. The idea of a thirst drive that caused drinking and an exploration drive that caused exploration was criticised by Hinde (1970), who said that ‘Drive concepts can be useful if defined independently of the variations in behaviour which they are supposed to explain’. Hinde followed Miller (1959) in suggesting that it could be useful to think of ‘thirst’ as an intervening variable between effects on animals (independent variables), such as water deprivation and amount of dry food eaten, and behavioural responses (dependent variables) such as amount of water drunk and rate of pressing a bar for a water reward. In reality, the drive concept is seldom useful and Toates (2002) emphasised the complexity of the relationships among all the dependent and independent variables, and hence of motivational systems. Toates explains that the defence of body fluid volume depends upon detection of interleukin concentration by neurons in the brain, release of the hormone vasopressin, action of this hormone in the kidney to conserve water, secretion of renin from the kidney and hence production of angiotensin, which acts in the hypothalamus to initiate drinking. A further, now discredited idea related to motivation is that there are often simple links between a stimulus and a response in determining which behaviour will occur. According to current theory, each animal is intrinsically active rather than passive, even in the absence of new stimuli and is goal-seeking, flexible; cognitively able and exploratory. An animal deprived of an important resource does not just wait for an

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appropriate stimulus so that it can respond. It will use its cognitive ability to attempt to prevent continuing deprivation using reward and incentive learning (Dickinson and Balleine 2002). One mechanism for an animal deprived of food or water may be to have lower perceptual thresholds for relevant stimuli (Aarts et al. 2001). The cluster of neuronal representations associated with particular food objects, positive tastes and the joy of eating may be activated by food deprivation (Ferguson and Borgh 2004). Other concepts formerly used but now largely replaced by ideas about cognition and emotion are conflict behaviour and displacement activity. Our domestic animals and their wild counterparts function by managing their lives using sophisticated control mechanisms. They assess potential risks and benefits and predict the future before acting (Forkman 2002; Raby and Clayton 2009, see Sect. 2.8.3 below). In order to do this and deal with potential problems they use their efficient brain mechanisms (Bagley 2005; Broom and Fraser 2015).

2.7.4

The Concepts of Needs and Freedoms

All animals, including humans, have functional systems, for example those controlling body temperature, nutritional state and social interactions (Broom 1981b; Broom and Fraser 2015) and there are inputs to these systems during much of life. By investigating functional systems and motivational mechanisms we can go some way towards identifying the resources or stimuli in the environment that are required by or important to animals, and so learn something about an animal’s needs. It is important for understanding animal welfare to consider the needs of animals, as proposed by Thorpe (1965). When do we say that an animal needs something? To need is to have a deficiency, often manifested as a homeostatic maladjustment. A need is a requirement, which is part of the basic biology of an animal, to obtain a particular resource or respond to a particular environmental or bodily stimulus. Some needs are for food, water or heat, but others are for a certain behaviour to occur e.g. grooming, exercising or nest-building. Control systems in animals have evolved in such a way that, in some circumstances, animals have a requirement to perform certain behaviours and their welfare is very poor if they are unable to carry them out. At any moment an individual will have a variety of needs, some of greater urgency than others. Each is a consequence of the particular motivational mechanisms of the individual. Some needs are simple, such as to escape the debilitating effects of high concentrations of body fluids or a high body temperature. Others are complex consequences of the mechanisms that promote survival and reproduction, for example, the need to circumvent the deficiencies in mental functioning that result from too little variety in sensory input or insufficient contact with other members of the species. Needs can be identified by studies of motivation and by assessing the welfare of individuals whose needs are not satisfied. The studies of motivation involve starting from either a known resource, or a known action by the animal, and finding out what are the causal factors influencing decision-making. When an animal has an unsatisfied need, its motivational state will usually elicit behavioural

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and physiological responses that remedy that need, so the individual will be able to cope with its environment. If a need cannot be satisfied, the consequence in either the short term or the long term will be poor welfare. Indications of the nature of the needs of a particular animal are often deduced from situations where there is some inadequacy in the environment. In fact, this is a way of investigating what constitute needs. Another way of finding out about the needs of animals is to examine what they do when they have some free choice of environment (Chap. 7). The individual’s need is a consequence of the motivational state that arises in given circumstances. This will depend on the biological functioning of such an animal. Most of the needs of animals of a certain species will be the same but there will be some inter-individual variation depending upon the experience during the development of each individual. However, the means of fulfilling some needs will vary greatly depending on the environment at the time and the capabilities and experience of the individual. Individuals often develop one or more particular strategies for achieving objectives. Some reports and legislation refer separately to physiological needs and to behavioural or ethological needs but the need itself is in the brain. Needs may be recognisable because of effects on the physiology or behaviour of animals, and animals may have a need to show a certain behaviour (Toates 2002; Broom and Fraser 2015), but the need is a requirement, usually to remedy a deficiency as explained above, and is not itself physiological or behavioural. Hence it is scientifically more precise not to qualify the term ‘need’ except with the word ‘biological’. It may be desirable in legislation and in advisory codes to place some emphasis on the existence of many needs that can only be satisfied if the individual is able to perform a particular behaviour. This can be done by defining biological needs as above, or by referring to ‘needs including those satisfied only by showing specific behaviours’. A problem associated with the use of the word ‘need’, especially in legislation, is that the deficiencies involved range from the rapidly life-threatening to those that are relatively harmless in the short term. If providing for the needs of an individual person or domestic animal were limited to those which are life-threatening, then the welfare of the individual would be poor indeed. Most of what is strongly avoided is harmful and most of what is strongly preferred is beneficial. However, some of what is wished for is not necessary, in the sense of essential for life, or it is harmful, so the reference to ‘part of the basic biology of the animal’ in the definition of need is valuable, as is the idea that to need is to have a deficiency. An earlier approach to consideration of what should be provided for individuals in order that welfare would be good was “the five freedoms”. This was first suggested in the Brambell Report in 1965 but it was not quite in line with Thorpe’s concept of needs. The freedoms provide a general guideline for non-specialists but animals have many needs that have been investigated for many species. As a result, the rather general idea of freedoms is now replaced by the more scientific concept of needs. A list of needs has been the first step in Council of Europe recommendations and E.U. scientific reports on animal welfare for over 30 years. The freedoms are not precise enough to be used as a basis for assessment of the welfare of a particular species or group of closely related species and are illogical in

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places. For example, “freedom from pain, injury and disease” for domestic animals is a desirable state and a worthy aim but it is not achievable. Animals might slip and fall or collide with something and be caused pain and injury. Freedom from disease is not achievable because some disease cannot be prevented. The fact that domestic and other animals often have fear of humans means that “freedom from fear and distress” cannot be achieved in some individuals. Unless food and water were available at all times, “freedom from hunger and thirst” would not be possible. “Freedom to express normal behaviour” would necessitate giving the animals the possibility to show aggression to others and other anti-social behaviours that are normal for the members of the species. The difficulties with the use of the term freedom are emphasised by Mellor et al. (2009). A final point is that unlimited freedom is harmful (Broom 2003, 2014) so for humans and domestic animals there are social limitations to individual freedom. These logical inconsistencies mean that some of those who use animals may say that they follow the five freedoms approach, knowing that they are not fully achievable and, as a consequence, not meeting the needs of the animals. A more useful general guideline is provided by the Welfare Quality project’s four welfare principles and 12 criteria (Blokhuis et al. 2010). However, these have some of the same disadvantages, for example they also include: “no disease”, “no injuries”, “expressing normal behaviour”, although normal behaviour is qualified by “non-harmful”. A limitation of these 12 criteria is that they are aimed at certain, housed land animals so some wording is difficult to apply to extensively kept or aquatic animals, e.g. “good housing” and “comfort around resting”. The five domains approach explained by Mellor et al. (2009), Mellor and Beausoleil (2015) is also a useful general guide. Whilst general guides, like these, can help in general planning, they are not specific enough to be used when deciding about how to keep a particular species. The best approach to a scheme for ensuring good welfare is to start with details of the needs of animals of that species, as determined from knowledge of their biological functioning and scientific studies of their preferences. Laws and guidelines for animal care, whose aim is to ensure good welfare, should refer to needs rather than to freedoms (Broom and Fraser 2015).

2.7.5

Motivational Dilemmas and the ‘Trade-off’ Concept

When the control systems affecting the various aspects of an animal’s life are examined in isolation, the outcomes of their operation are commonly predictable. But in most natural circumstances, two or more systems interact, often driving different variables towards independent goals, and the outcome of the interaction is then far more difficult to predict. Sometimes control systems function in harmony to achieve a common purpose, as when increased blood circulation in the skin and increased respiratory ventilation jointly serve to keep an animal cool on a hot day. On other occasions, the outputs of two separate control systems conflict. This occurs when the achievement of homeostasis requires two responses that cannot be pursued

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simultaneously. For example, an animal cannot both forage for food and escape from cold if food is available only in the cold (Johnson and Cabanac 1982). Other problems arise when one physiological apparatus services the needs associated with two physiological control systems. The cardiovascular system provides both skin vasodilation and muscle blood flow during exercise, and may be inadequate to provide both during exercise in hot weather. In such circumstances circulation will be compromised in both vascular beds (Johnson and Hales 1984). A wide range of motivation research analyses how individuals cope when faced with behavioural dilemmas. In simple terms, animals make choices that suggest that the costs and benefits of various behavioural options are evaluated, and certain options are ‘traded off, that is partially or totally abandoned, in favour of the option that offers greatest gains. Humans often face such situations. A simple decision, whilst in bed and wanting to sleep, is whether or not to get up and urinate. Somewhat more complex is the decision about going out to buy food in bad weather. We weigh up psychologically how strongly we crave the food and compare that with the discomfort that must be experienced to gain it. A decision is made by evaluating the relevant causal factors including those resulting from assessing what alternative food is in the larder, how effective is our overcoat, how hungry we are, and so on. Such dilemmas are also encountered by members of other species, sometimes with outcomes of relevance to animal welfare. In nature animals may be driven to tolerate unpleasant conditions while they pursue other goals. Newts, which court their mate underwater, face a dilemma during courtship between the need to come to the surface to breathe and the need to continue a sexual encounter (Halliday and Sweatman 1976). The extent of animals’ voluntary tolerance of unpleasant stimuli in such situations of conflict is surprising. Rats will make excursions into a very cold environment ( 15  C) to eat tasty food even when nutritionally adequate food is continuously available in unlimited amounts in warm conditions (Cabanac and Johnson 1983). We could interpret this as meaning that, in the pursuit of pleasure, animals will voluntarily tolerate considerable discomfort.

2.8

Types of Control

The impact of a disturbing stimulus on an animal is critically affected by how long the stimulus lasts, how often it occurs, and whether the animal was prepared for it in advance. Time is an important factor in the operation of control systems. A clap of thunder is a shock, not because it lasts for long, occurs often, or even solely because it is loud. It is alarming particularly because it is infrequent and unexpected. Yet the effect is brief and almost always harmless. A dog may be frightened by thunder and also be caused anxiety by the soft whirr of hair clippers if it is heard each time the animal attends a veterinary clinic for an injection. Many associations are not made because there is a high intensity stimulus but because of its timing.

2.8 Types of Control

2.8.1

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Rates of Neural and Hormonal Response

The neural response to a peal of thunder peaks in a few seconds. Signals pass to and from the control systems along nerve pathways in a matter of milliseconds. The muscular startle response occurs in the same instant as, or even before, human subjects report perception of the sound. So too might the outputs elicited in response to brief noxious stimuli, such as butts from an aggressive littermate or shocks from an electric stock prod. But not all nervous reflexes are so mechanical and rapid. Incoming stimuli undergo comparison with past experiences before being transformed into complex behavioural responses, and these responses may occur with considerably greater delay than the response to thunder. The co-ordinated response may be effected by the sympathetic rather than the somatic nervous system, for example when the heart rate is raised. In such a situation, the effect will last five to ten times longer, and additional tissues may be stimulated through the release of hormones from the adrenal medulla. All unpleasant stimuli, even if brief, are likely to elicit some hormonal response. Not only will the ‘alarm’ reaction release adrenaline and noradrenaline from the adrenal medulla, it may lead to the release of glucocorticoid hormones from the adrenal cortex. These hormones reinforce and extend the effects of the more rapid nervous reflexes. They do this partly by their slower release and especially by their slower turnover in the body. Adrenaline and noradrenaline take several minutes to disappear to half their initial concentration; glucocorticoids can take more than an hour. Consequences of noxious stimulation may thus last for hours. Other hormones such as prolactin, vasopressin, ß-endorphin and those from the thyroid may be mobilised, thereby further prolonging the effect (see Chap. 5).

2.8.2

Feedback and Feedforward Controls

Homeostatic mechanisms control the essential variables of the body, minimising deviation of their levels from the optimal range. Where this is achieved by a response after the changes in the variable, it is called feedback. If the response counteracts a disturbance to an individual, and can thus be considered to be opposite in sign to the displacement, it is negative feedback. If the response increases the displacement, this is positive feedback which is not homeostatic. In negative feedback the disturbance to the body occurs before a counteractive response begins. If the disturbance is very great or rapid in onset, substantial disruption may occur to the animal before the disorder is corrected (Fig. 2.4). Feedforward controls also operate in many homeostatic systems, presumably due to their capacity to reduce system disruption. In these cases, an anticipatory mechanism induces a change in the homeostatic control system before a disruption actually occurs. The disturbance, when it comes, thus causes less upset to the animal

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Fig. 2.4 In negative feedback control a correction is made after the state of the animal has changed, and this restores the state to the former condition. A drop in body temperature is detected, and corrective behavioural or physiological action is taken at the point marked by the arrow. The dotted line shows how the state would change if no correction occurred (after Broom and Fraser 2015)

Fig. 2.5 In feedforward control a change in state is predicted and corrective action taken before it can occur, so that the state changes little from its former condition. Above, a drop in body temperature is predicted and behavioural or physiological action is taken at the point marked by the arrow. The dotted line shows how the state would change if no correction occurred (after Broom and Fraser 2015)

(Fig. 2.5). How does an animal anticipate a disturbance? One means is via a signal, indicative of a potential change, coming from a sensory input that is peripherally related. The sight of snow outside a window of a house will be sufficient to alert a person to put on a coat before venturing into the cold. It may even reduce the rate of cooling by limiting skin blood flow, before there is any lowering of body temperature. Research on animal behaviour is providing more and more evidence of feedforward control in operation (e.g. Tolkamp et al. 2012). Other environmental challenges come on a regular daily or seasonal basis, so may be signalled by day-night changes or by changes in day length. By such means, an animal can prepare for the predators of the impending night, or the heat of the approaching summer. Any changes that constitute a threat to an animal’s life will be particularly effective in alerting it to the possibility of that threat being repeated. A hunted species may be physiologically prepared for flight by a distant gunshot or the sight of fleeing prey. One of the first detailed studies showing non-human animals preparing for future needs was that of Metz (1975). He measured food intake and

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inter-meal intervals in cattle given food ad libitum and with regular periods of night and of milking at which food was not provided. He found that the amount eaten in a meal was related more closely to the interval before the next meal than to the interval after the last meal. Similar results have been found in other species. The animals did not accumulate a nutritional deficit and then rectify it, but rather ate a meal in order to prepare for a period when they would not eat. Another example is drinking during or soon after a meal which occurs prior to the dehydrating effects of food in the gut resulting in water being taken from the tissues by osmosis. There are many cases of animals behaving in a way that prepares them for future events rather than responding to previous occurrences. The effects are that many predictable changes in state are minimised or prevented. Understanding the nature and causes of feedback and feedforward controls is important in studies of stress and animal welfare for two reasons. First the characteristics of negative feedback mechanisms determine the extent of disruption to an animal brought about by an environmental imposition. Inability to correct displacements of state from the tolerable range will usually be disturbing and will sometimes be damaging: we shall propose in Chap. 4 that an animal has a limited capacity to cope with such disruptions. Second, feedforward mechanisms, being anticipatory, tend to minimise the degree of disruption. Study of them should provide clues to the nature of successful adaptation. An inability to carry out feedforward control because of conditions imposed on an animal by man may be a source of particular frustration.

2.8.3

Predictability of Stimulation

As mentioned above, since we now realise that our domestic animals and their wild relatives often predict likely changes in body temperature, body nutrient levels or social actions, our view of animals has changed to consider them as cognitive beings aware of the complexities of their environment. Each animal has an expectation of what input it will receive when it performs a certain action. It is essential for simple movement control for animals to have a model of the expected input so that, following actions, they can compare this with the actual input (Broom 1981b). With more complex actions too, the animal is continually predicting changes in input and comparing actual and expected input. The idea that animals have a ‘should-be value’ or Sollwert for each important aspect of their environment and that they compare this with an ‘actual value’ or Istwert was presented by Wiepkema (1985, 1987). The Sollwert is the animal’s neural construct of the tolerable range. When an animal is exposed at constant intervals to stimuli that are not noxious or excessive, its response to them progressively wanes as it habituates (Sect. 2.4). This too depends on the animal having a should-be value. Cattle grazing beside a road, although initially interrupted by passing vehicles, soon cease to show a response. However, if stimulation occurs irregularly, or with widely varying intensities, each stimulus continues to elicit a response. The progressive decrease in concern about a

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regular harmless stimulus may depend on feedforward control; the animal is prepared for the rumble of a passing vehicle and pays it no heed. But when the next stimulus is unpredictable either in time, intensity, or both, yet is certain to arrive sometime, the animal can prepare only by being constantly ready. The anticipation in such circumstances engenders a state of anxiety, and heightens the reaction when the stimulus is eventually perceived. In extreme circumstances an animal may even respond to its uncertain situation by showing learned helplessness. Many responses to perceived environmental changes are not related just to the detected change, but also involve predictions about what will happen next. Animals in learning situations have been shown to not only associate successive events, but also assess the probability that events will occur (Dickinson 1985; Dickinson and Balleine 2002; Raby and Clayton 2009). Rats running in a maze show clearly their expectation of a food reward at the end if that reward is not present or inadequate. Pigs fed at a particular time of day change their behaviour in the hour before feeding and cattle show responses if their feed gate does not work. Previous unpleasant experiences also result in expectation, so that a cow that has experienced unpleasant veterinary treatment in a crush may be unwilling to enter it later. Rushen (1986) showed that a sheep that had been roughly or painfully treated at the end of a race was difficult to move into and along that race on subsequent occasions. Previous experience with stockpersons can substantially alter later farm animal behaviour and ease of management by people (Hemsworth and Coleman 2010). If animals live in a world that they organise so that many of the events in it are predictable and the state of the animal is closely regulated, then it is logical to ask whether unpredictability is especially aversive to those animals as it usually is to humans. It has been known for a long time that rats and dogs show a clear preference for prediction and control over unpredictability and lack of control. Predictable shocks cause fewer ulcers in rats than do unpredictable shocks (Weiss 1971; Overmier et al. 1980), while unpredictability in feeding after previous regular feeding led to increases in adrenal cortical activity in pigs (Carlstead 1986). Animals can prepare for predictable aversive events, and for events that are not aversive. Body regulation and coping are more difficult if there is unpredictability and the consequence is usually poor welfare. One kind of situation where there is no match between expected and actual input leads to frustration. If the levels of most of the causal factors that promote a behaviour are high enough for the occurrence of the behaviour to be very likely, but because of the absence of a key stimulus or the presence of some physical or social barrier the behaviour cannot occur, the animal is said to be frustrated (Broom 1985). For example, Duncan and Wood-Gush (1971, 1972) thwarted hens about to feed by covering their food dish with a transparent perspex cover. The hens showed stereotyped pacing and increased aggression. Feeding is often frustrated by the presence of stronger rivals in group-housing situations. Whilst some frustration is trivial, other frustration can be so frequent and involve so fundamental an activity that the fitness of that animal is impaired.

2.9 Pain

2.9

39

Pain

Pain is one of the primary sensations that result directly from the activity of sensory receptor cells, either specialized for this function or for other functions. However, there are important differences between pain and other sensations because a large proportion of the impact of pain on the individual is a result of high-level function in the brain. Pain is associated with some substantial stress and is particularly significant in animal welfare studies. Public concern about welfare has been greatly influenced by the widely held conviction that many non-human animals experience pain much as humans do, and that pain is probably as distressing for other animals as it is for humans. First we must consider what pain is. People who are asked this question firstly describe pain as something that they feel. There is always the qualification that the sensation is unpleasant. A useful way to recognise or measure unpleasantness is to examine the extent of withdrawal from, or avoidance of, unpleasant stimuli. Pain is only one unpleasant feeling, for example fear also elicits strong avoidance. When pain has been discussed or defined, processes in non-humans have sometimes been ignored because the writer has been thinking only about humans, and sometimes the wording has been chosen in order to exclude non-humans. Pain receptors are often called nociceptors and, in humans, nociception is considered by some to be the physiological relay of pain signals; an involuntary, reflex process not involving awareness. Some authors have distinguished pain, as a mechanism in humans, from nociception, as the only mechanism in non-humans. The distinction between nociception and pain is largely a relic of attempts to emphasise differences between humans and other animals or between “higher” and “lower” animals. The visual and auditory systems involve receptors, pathways and high-level analysis in the brain but the simpler and more complex aspects are not given different names. A perception of pain can exist without the involvement of pain receptors, but so can visual or auditory perceptions exist without their receptors being involved. Wall (1992) said that the problem of pain in man and animals was “confused by the pseudoscience surrounding the word nociception.” While the word nociceptor is useful as the sensory cell receiving the input, the use of the term nociception, which separates one part of the pain system from other parts, should be discontinued. The system should be considered as a whole (Wall 1992; Broom 2001c, 2014). Given that pain has sensory and feeling components and leads to aversion, Kavaliers (1989) suggested, based on the International Association for the Study of Pain definition (Iggo 1984), that for non-humans, pain is ‘an aversive sensory experience caused by actual or potential injury that elicits protective motor and vegetative reactions, results in learned avoidance and may modify species specific behaviour, including social behaviour’. However, the IASP and Kavaliers definitions are inadequate because a definition of pain should refer to both sensory and emotional aspects and the reference to function and consequences is not needed as it may unnecessarily restrict its meaning. A definition should exclude fear and other feelings and take account of phenomena such as phantom-limb pain. Accordingly,

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Broom’s (2001b, c) definition was: pain is an aversive sensation and feeling associated with actual or potential tissue damage. Animals differ in their responses to painful stimuli (see Chap. 5), for example dogs and humans make much noise but sheep do not, because loud vocalisations may elicit help from social group members in dogs and humans but just attract more predator attention to an injured sheep. Hence different responses are adaptive in different species. The feeling of pain may be the same even if the responses are very different. The behavioural responses may vary but avoidance of the painful stimulus, and the effects on subsequent responses of learning to avoid such stimuli, should be observable in any animal that feels pain. In considering how we decide whether or not an animal can feel pain, Bateson (1991) proposed that an animal showing behaviour and physiology homologous with humans undergoing pain and suffering should be treated as suffering unless there is evidence to the contrary. Such use of the precautionary principle is like that for wider areas of animal ability proposed by Bradshaw (1998) and others. The occurrence of pain in a wide range of animals is discussed by Braithwaite (2010), Broom (2014, 2016) and Sneddon et al. (2014). The conclusion of these studies is that there is good evidence at present that all vertebrates, cephalopod molluscs and decapod crustaceans have pain systems, including the sophisticated brain system necessary for this function. For example fish are capable of learning about spatial relationships (Odling-Smee and Braithwaite 2003), using information about sequences of spatial information (Burt de Perera 2004), recognising social companions (Swaney et al. 2001), and learning to discriminate reliable from ephemeral food sources (Salwiczek et al. 2012). They have two types of nociceptor, A-delta and c fibres, the transmitter substance P, the analgesic opioid enkephalins and β-endorphin, and specific responses to painful stimuli that stop when the analgesics are given (Sneddon et al. 2014). The parts of the brain that process pain information vary amongst animals but the functioning of the cell systems in the brain is extremely similar. Pain detection and analysis is valuable for all of these animals and the systems arose during evolution before much of the differentiation of the major animal groups.

2.10

Other Feelings and Emotions: Positive and Negative

The concept of affect concerns emotions, feelings, moods and affective dispositions (Fox 2008; Sander 2013). Paul et al. (2005) state that “affect involves: behavioural and physiological responses (and in conscious beings, feelings) that can vary both in terms of valence (pleasantness/unpleasantness) and also intensity (arousing/ activating qualities)” so the term is not limited to animals that can have feelings (Broom 2010). A feeling is a brain construct involving at least perceptual awareness which is associated with a life regulating system, is recognisable by the individual when it recurs and may change behaviour or act as a reinforcer in learning (Broom 1998). In relation to this definition, emotions are considered to be similar but

2.11

Development of Regulatory Systems

41

physiologically describable (Broom 2007). Rolls (1999) considered feelings to be the subjective consequences of emotions involving consciousness or awareness. Emotion can be defined as follows: an emotion is a physiologically describable component of a feeling characterised by electrical and neuro-chemical activity in particular regions of the brain, autonomic nervous system activity, hormone release and peripheral consequences including behaviour. These concepts and their physiological basis are discussed further by Boissy et al. (2007) and Broom (2014). Feelings are adaptive mechanisms that have evolved and that include: pain, fear, anxiety, sexual pleasure, eating pleasure, exhilaration, achievement pleasure, other sensory pleasure, social affection, guilt, anger, rage, malaise, tiredness, hunger, thirst, thermal discomfort, grief, frustration, depression, boredom, loneliness, jealousy and lust (Broom 1998, 2014). Suffering is one or more bad feelings continuing for more than a few seconds or minutes.

2.11

Development of Regulatory Systems

2.11.1 Early Abilities, Preferences and Experiences Mammals at birth and birds and reptiles at hatching have an impressive repertoire of capabilities. One of the least developed of mammalian young, the new-born kangaroo, has the capacity to sense its environment and make its way through smoothed fur to its mother’s pouch. Precocial species such as lambs, foals or domestic chicks attempt a range of behaviours within minutes of birth. Newly hatched domestic chicks can stand, walk, preen, peck, vocalise in several ways, approach visual or auditory stimuli and respond to contact with a brooding hen (Broom 1981a, b). As explained in Chap. 1, all characteristics are affected to some extent by environmental variables. Domestic chick responses to flashing lights or sounds, or to the voice of the mother, are affected by specific pre-hatching sensory experiences (Vince 1966). The new-born animal faces a profusion of sensory experiences, from which it begins to establish responses to the pleasant and the unpleasant, the vital and the irrelevant. Influenced particularly by its mother, father and siblings, if present, and others of its species in the vicinity, the young animal begins developing its survival and social skills. Stimuli during the sensitive neonatal period have a substantial effect on later development and various movements and social relationships are developed and refined as a consequence of stimuli received. The progress of these developments can have a profound influence on an animal’s success in adapting to conditions in later life. During the period of socialisation of puppies, between about 4 and 10 weeks after birth, exposure of pups solely to dogs leads to poor subsequent rapport with humans, while exposure solely to humans can lead to poor relationships with other dogs, to which the pup may show excessive timidity or aggression. In principle, the raising of chicks without hens, or of puppies in pet shops, or of various types of animals in zoo enclosures would be expected to influence the later responses of those animals. Some evidence is now available about the effects of early

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stimulation on gene function and other changes in animals in these contrived environments where animal welfare problems commonly occur (Bernardino et al. 2016).

2.11.2 Learning and Memory Learning occurs throughout life. Virtually all stimuli and responses have the potential for being memorised and hence becoming factors influencing subsequent behaviour and physiological functioning. Developing and memorising a successful strategy for coping with an environmental disturbance should not only make ensuing exposures easier to deal with but, just as important, lead to the animal having less anxiety at the prospect of encountering such a disturbance. The consequences of having a memory are not all advantageous. If an animal fails to cope adequately with an imposition, its sensitivity and anxiety may be heightened by recalling this when next that problem looms (Brambell Report 1965). If the unpleasant imposition was caused by a human, handling may become more difficult for the human and more disturbing for the animal when later handled. Just as feedforward control can enable an animal to cope with a previously-experienced stimulus, so anticipation of a noxious stimulus not successfully countered on a previous occasion may be doubly distressing. Some of the displeasure may be negated if a reward is given simultaneously, and this can be a worthwhile practice when the unpleasant stimulation is beneficial, for example vaccination. Subsequent exposure may then be associated with pleasure rather than displeasure, and hence be accepted more willingly. If an animal has a poor memory so that it is fearless of an impending unpleasantness that it has experienced before, it will suffer the disadvantage of not being able to predict that the unpleasantness will eventually end (Rollin 1981). Many studies demonstrate, see review by Broom (2014), that various animal species can remember events for long periods. The food preferences of sheep can be influenced by what they, as young lambs, saw their mother eat during brief exposures 3 years previously (Keogh and Lynch 1982). Kendrick et al. (2001) found that sheep trained to discriminate individuals remembered this 2 years later. In practical terms the findings of Rushen (1990) are particularly relevant. Rushen assessed the willingness of sheep to proceed down a race after previously experiencing aversive experiences at the end of the same race. As is shown in Fig. 2.6, a sheep would run down the race in a few seconds if it had received no aversive treatment there, but took about 2 min to go down the race if it had been restrained at the far end or if the electrodes of an electro-immobiliser had been attached to it, though not switched on. When the electro-immobiliser was switched on, the sheep took 6 min to proceed down the race. The reluctance of the sheep to move along the race is a measure of how much aversion the sheep has to its previous treatment. The time interval between the experience and the exhibition of aversive behaviour was a day or two in Rushen’s

2.11

Development of Regulatory Systems

43

Fig. 2.6 Mean time taken by sheep to run through a race in which they were repeatedly electroimmobilised (E-l) or restrained physically (restraint). The sheep in the ‘wired-up’ group had the electrodes of the immobiliser attached, but the current was not turned on. Asterisks show the first trials at which the treatments differed significantly (P < 0.05) (after Rushen 1990)

studies, but cows may avoid a crush even months after an uncomfortable treatment there, and dogs can long be reluctant to enter a veterinary surgery long after they have had an unpleasant experience there.

2.11.3 Lifetime and Evolutionary Changes By adulthood, animals have built on their abilities and preferences at birth through a range of subsequent experiences, and have developed various skills. With each new experience, the bank of memories is modified and some slightly different regulatory response may be developed. Thus, during its life, an animal may change its regulatory responses to a given stimulus, because of accumulating experiences, biological and seasonal cycling, and ageing. Some of the regulatory responses to the environment that an animal could develop would improve its reproductive capabilities or fitness; others would reduce them. Thus, on the basis of the natural variations associated with age, experience, season and so on, one would expect some genetic selection to take place over many generations for improved adaptation to the environment through refinement of biological and social regulatory systems. If this theoretical prediction were borne out, animals would become progressively better adapted genetically to all the conditions we are exposing them to: sheep to farms, monkeys to zoos, horses to

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racing, and cats to fast-moving traffic. The slow rate of genetic change, however, makes it unrealistic to expect welfare problems to be solved by such selection. The probable time-scale for changes of this sort can be estimated. The animals that we now keep lived for several million years independently of humans, presumably meeting them occasionally when not alert and astute enough to escape human hunting. We have controlled animals through domestication for only a few thousand years, and kept them in close confinement for only a few decades. The influence of the many millennia before domestication will heavily outweigh changes imposed during the last few decades. Some changes have occurred and others will continue to occur, but most characteristics are very resistant to change. Genetic adaptation of hens to battery cages is unlikely to occur at all, even with genetic engineering to accelerate the rate of change. Evidence that adaptation to the wild is retained despite a veneer of domestication can be seen in the full range of ancestral wild boar behaviour shown by pigs when kept in semi-natural conditions (Wood-Gush 1988), and the ease with which this species, which seems to require careful management on farms, can revert to feral status and survive in the wild, for example in Australia, New Zealand, Hawaii, etc. A final but crucial point about the evolution of adaptation to the vicissitudes of the physical and social environment is that a very important part of that evolution has been the development of the complex appreciation of the interactions of an individual with the world in which it lives, which we call feelings. Complex brains, like those of vertebrates, have complex systems for regulating these interactions. If an individual has a system of feelings which involves changes in its mental, and perhaps in its hormonal, functioning because a certain kind of body regulation is difficult or because an anticipated event has not occurred, such an individual will have increased fitness in comparison with a genetically different individual which has no such system. It would be surprising if animals such as our domestic animals, all of which have an elaborate social organisation, did not have feelings similar to many of those of humans. A significant consequence of this is that if the various regulatory system components that are manifested as feelings are present in a species, there is a potential for suffering, and that is clearly of great importance both biologically and when considering moral questions.

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Sander D (2013) Models of emotion: the affective neuroscience approach. In: Armony J, Vuilleumier P (eds) The Cambridge handbook of affective neuroscience. Cambridge University Press, Cambridge, pp 5–53 Serova LI, Gueorguiev V, Cheng SY, Sabban EL (2008) Adrenocorticotropic hormone elevates gene expression for catecholamine biosynthesis in rat superior cervical ganglia and locus coeruleus by an adrenal independent mechanism. Neuroscience 153:1380–1389 Shah JY, Gardner WL (eds) (2008) Handbook of motivation science. The Guildford Press, New York Sibly R, McFarland D (1974) A state–space approach to motivation. In: McFarland DJ (ed) Motivational control systems analysis. Academic, London Sneddon LU, Elwood RW, Adamo SA, Leach MC (2014) Defining and assessing animal pain. Anim Behav 97:201–212 Sokolov EM (1960) Neuronal models and the orienting reflex. In: Brazier MA (ed) The central nervous system and behavior. Macy Foundation, New York Swaney W, Kendal J, Capon H, Brown C, Laland KN (2001) Familiarity facilitates social learning of foraging behaviour in the guppy. Anim Behav 62:591–598 Thorpe WH (1965) The assessment of pain and distress in animals. Appendix III in Report of the technical committee to enquire into the welfare of animals kept under intensive husbandry conditions, F.W.R. Brambell (chairman). H.M.S.O, London Tilbrook AJ (2007) Neuropeptides, stress-related. In: Fink G (ed) Encyclopedia of stress. Academic, Oxford, pp 903–908 Toates F (2002) Physiology, motivation and the organization of behaviour. In: Jensen P (ed) Ethology of domestic animals – an introduction. CAB International, Wallingford Tolkamp BJ, Howie JA, Bley TA, Kyriazakis I (2012) Prandial correlations and the structure of feeding behaviour. Appl Anim Behav Sci 137:53–65 Turner AI, Keating C, Tilbrook AJ (2012) Sex differences and the role of sex steroids in sympathoadrenal medullary system the hyporthalamo-pituitary adrenal axis responses to stress. In: Kahn SM (ed) Sex steroids. Tech. Publishing, Rijeka, pp 115–136 van Stegeren AH, Wolf OT, Everaerd W, Rombouts SART (2007) Interaction of endogenous cortisol and noradrenaline in the human amygdala. Prog Brain Res 167:263–268. https://doi. org/10.1016/S0079-6123(07)67020-4 Vince MA (1966) Artificial acceleration of hatching in quail embryos. Anim Behav 14:389–394 Wall PD (1992) Defining “pain in animals.”. In: Short CE, van Poznak A (eds) Animal pain. Churchill Livingstone, New York, pp 63–79 Weiss JM (1971) Effects of coping behaviour in different warning signal conditions on stress pathology in rats. J Comp Physiol Psychol 77:1–13 Wiepkema PR (1985) Abnormal behaviour in farm animals: ethological implications. Neth J Zool 35:279–289 Wiepkema PR (1987) Behavioural aspects of stress. In: Wiepkema PR, van Adrichem PWM (eds) Biology of stress in farm animals: an integrative approach. Current topics in veterinary medicine and animal science, vol 42. Martinus Nijhoff, The Hague, pp 113–183 Wood-Gush DGM (1988) The relevance of the knowledge of free ranging domesticated animals for animal husbandry. In: van Putten G, Unshelm J, Zeeb K (eds) Proceedings of the international congress of applied ethology in farm animals, Skara, Sweden. KTBL, Darmstadt

Chapter 3

Limits to Adaptation

Abstract The mechanisms of adaptation and coping are considered in detail in this chapter. Firstly, how can stimuli vary in time, intensity and modality? The links between the nature of stimuli and the responses that can result are illustrated diagrammatically. Habituation and sensitisation are defined and variation in patterns of adaptation discussed. Some of the disorders that result from difficulties in regulation and their relationships with welfare are considered. When can adaptation problems be tolerated, when do they cause poor welfare and when do coping mechanisms fail so that the impact becomes lethal? Keywords Adaptation limit · Coping · Welfare · Habituation · Sensitisation

3.1

Limitations of Timing and Temporal Aspects of Stimulus Modality

The interrelations of time, intensity and modality of stimulation are very complex and are depicted in this chapter in simple diagrams to highlight how they affect adaptation, developing ideas by Frese and Zapf (1988).

3.1.1

Changes in Frequency

A stimulus such as the sound of a car horn is a relatively innocuous and effective warning signal if heard once a day or once an hour (Fig. 3.1a). At higher frequencies (Fig. 3.1b), habituation may occur and diminish its effectiveness as a warning as alarms become ineffective if sounded too frequently. However, repeated stimulation may become irritating, such as when car-theft horn alarms sound frequently (see discussion of sensitisation in Chap. 2). At these frequencies, there will be an increasing level of response, perhaps reaching a point where the capacity to adapt to the stimuli is exceeded (Fig. 3.1c). For humans, the experience of car horns © Springer Nature Switzerland AG 2019 D. M. Broom, K. G. Johnson, Stress and Animal Welfare, Animal Welfare 19, https://doi.org/10.1007/978-3-030-32153-6_3

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Fig. 3.1 (a) Successive responses to stimuli without habituation (b) Successive responses to stimuli with habituation (c) Successive responses to stimuli with sensitisation (d) The first response adapts to the baseline before the second stimulus occurrence but the second response has adapted only partially when the second stimulus occurs so the total response is greater

50 Limits to Adaptation

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constantly sounding in dense traffic can be disorienting. A dog crossing a busy road may also become disoriented because multiple inputs result in a sensory overload that its control systems are not able to accommodate. Another factor determining the impact of pleasant or unpleasant stimuli is the rapidity of adaptation of the response to a stimulus (Fig. 3.1d). This can vary widely depending on the nature of the stimulus and its biological significance. Consider two examples of visual stimulation. The physiological reaction to the sight of a detailed geometric pattern may disappear within milliseconds or seconds. On the other hand, the effects of seeing a predator may last for hours. Although the complexity of the visual stimuli may differ little, the consequences are very different. If the exposure to the geometric pattern were repeated, the result would be an inconsequential reaction whereas sighting the predator again may cause alarm. A key factor here is whether or not the stimuli are directly threatening. Responses to even horrifying stimuli may habituate in time; witness the passivity that people can develop to wartime horror. A difference in response thus arises not solely from the nature of the stimulus but also, in part, from the interpretation of the signals in the light of past experience. Habituation is the waning of an individual’s response, which could still be shown, to a constant or repeated stimulus. It is very seldom a result of simple adaptation of receptors or of fatigue in effectors such as muscle. Nor is it the result solely of fatigue in other parts of the nervous pathway between receptor and effector; habituation must involve complex processing of multiple inputs. Sokolov (1960) described the habituation of the startle response of dogs on repeated presentation of a tone, and the reappearance of the response when the tone was varied in pitch or quality. Broom (1968) found that young domestic chicks exhibited a startle response when a small light in their pen was switched on for 10s, then left off for 20s. With repeated presentation the response habituated but it reappeared if the duration of illumination was changed. Furthermore, if the light went off after 5 s there was a reaction at that time. If the light stayed on to 15 s there was a response just after 10 s when the light should have gone off (Fig. 3.2). These results show that the habituation in both sets of experiments was for specific timing of illumination and that the animals must have had precise expectations about the stimulus input, which they matched with the actual input. In this case, the waning of a response to a stimulus involved cognitive processes just as complex as those that occur during conditioning. The specificity of habituation was also emphasised by Kant et al. (1985) who found that rats habituated to low level footshock, restraint, or forced running in an activity wheel showed the substantial response typical of naive animals when exposed to one of the other two treatments. Habituation to one negative treatment did not mean reduced responsiveness overall. A quite separate reason for different rates of adaptation can be dissimilarities in the nature of the stimuli. Most stimuli have very brief effects on the sensors. However, some that are transiently noxious, such as cuts, scratches and bruises, may have long-term residual effects related to the extent of tissue damage. This could be interpreted either as slow adaptation or as a stimulus of long duration. The effects of prolonged stimulation will be considered separately below.

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Fig. 3.2 Young domestic chicks responded (#) when a small light was switched on for 10 s in their home pen. This response habituated well before the 50th presentation but returned if the light went off too early or stayed on too long (data from Broom 1968)

3.1.2

Changes in Duration

A sustained painful stimulus is clearly a greater imposition on an individual than a brief painful stimulus. However, the effect is not simply related to stimulus duration. The effects of a brief stimulus (Fig. 3.3a) usually fade away at a rate depending on the characteristics of the stimulus and the animal, as described in the preceding section. For some sustained stimuli, a similar adaptation may also occur (Type 1), for example, after a saddle is put on a horse. The influence of the stimulus abates by adaptation despite its continued application. Other long-lasting stimuli can have an increasing impact with time (Fig. 3.3a, Type 2). The stimulus in this case may be tolerated if it lasts only briefly but, with the passage of time, the response of the animal increases. The animal becomes more and

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Fig. 3.3 Schematic relations between (a) a brief stimulus and a rapidly adapting response (b) a sustained stimulus and a response which adapts (Type 1) or is sensitised (Type 2)

more sensitive despite the constancy of the stimulus. Such an increase in response to continuing or repeated stimulation is called sensitisation (Sect. 2.4). By such progression, a stimulus that is initially tolerable may eventually reach an intolerable level. Biting insects or the sound of a pneumatic drill are repetitive stimuli to which people may become increasingly sensitive. What begins as a mild irritant can eventually become intolerable. Another example of this is the ‘dripping water torture’, where a stimulus that is quite innocuous when applied in isolation (namely, a drop of water on the forehead) is said to become sufficiently noxious to send a person crazy when applied repeatedly over hours and days. Interestingly, Lazarus and Folkman (1984) suggest that humans are less tolerant of sustained petty disruptions than of major tragic events in their life.

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If a stimulus exceeds the threshold of tolerance (Fig. 3.3b, Type 2) and an animal’s homeostasis is progressively disrupted, the effect on the animal depends directly on the duration of stimulus. Only brief exposures can be endured; prolonged exposures will lead to collapse and death.

3.1.3

The Impact of Novelty

The previous experience of a stimulus, that an individual has had, usually alters response to that stimulus. However, novel stimuli elicit increased alertness as well as reactions related to the nature of the stimulus. If the stimulus appears to be of little significance, the individual may show some curiosity but this will wane if the stimulus is repeated. If the stimulus is of great significance, the response will be one of continuing strong interest, or even alarm. The reaction to subsequent stimuli will then depend on the characteristics mentioned previously: intensity, duration and modality. A novel noise may generate little reaction from an animal that is familiar with it, but provoke alarm in an animal that has not heard it previously; that is, the threshold for response will be lower. Animals living in barren environments may seek some degree of novelty so the effects of novel but not disturbing stimulation can be positive. Lack of exposure to a varied environment can result in the animal showing alarm responses to quite mild stimuli. As a result, stimulation that seems to be within everyday experience may push inexperienced animals beyond their capacity to cope.

3.1.4

The Value of Forewarning

Forewarning that a stimulus is coming can help an animal prepare for pleasant or unpleasant consequences. Feedforward mechanisms (Chap. 2) use such information and earlier experiences to prepare animals for either environmental or social change. A situation in which preparation for unpleasant effects may be necessary occurs when regulatory systems come into conflict (Chap. 2) and an animal has to remain in conditions that are difficult in some respect. When animals have to tolerate adverse conditions, such as low air temperature or high predation risk to obtain food, they benefit greatly from previous knowledge and presumably prepare for the adversity, since deciding to forage necessarily involves prior assessment of the environment. In humans, forewarning can result in acceptance of a painful treatment with the expectation of relief from pain or other suffering. A human may accept an injection of an anaesthetic drug before dental treatment, injection of a vaccine, or potentially painful surgery as the cost of being cured of a disease. A domestic animal may be helped to tolerate such ‘costs’ by its owner’s reassuring voice encouraging it to accept stimuli that would normally elicit an avoidance or stronger reaction.

3.2 Limitations of Intensity as an Information Basis for Adaptation

3.2 3.2.1

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Limitations of Intensity as an Information Basis for Adaptation Changes in Intensity

Varying the intensity of a stimulus may appear to influence an animal, because the greater or lesser intensity results in more or fewer impulses being transmitted along nerves to the central nervous system, but the coding in nerves is more complex than that. Consider the difference between the effect on the visual system of a low luminance and a bright beam of light. How would this be different from stimulation by a bright, narrow beam and by a floodlight? In both situations there are differences in the impact of the stimuli, but the difference in the first case is in the intensity of the applied stimulus and, in the second, in the area over which the stimulus is applied. The light from the dull and bright beams may impinge on exactly the same cells of the retina, though the bright light activates those particular cells more than the dull one. The floodlight may affect individual retinal cells to the same extent as a bright beam, but its greater effect comes from the larger number of cells affected and hence the increased number of activated channels to the brain. Other differences of importance in animal welfare are those related to spatial and temporal summations of temperature, pressure, pain and other stimuli. In some situations, the same stimulating effect can be brought about by stimuli in various combinations of intensity and area, as shown schematically in Fig. 3.4. The greater is the total stimulation received by the animal, the greater will be the response. In practical terms, the contributions of density and area to total stimulation are especially important in assessing the effect of local, compared with generalised, trauma in an animal. Parts of an animal can be grossly disturbed locally, for example by infection or trauma, yet constitute only a moderate handicap to the animal. At the affected site, measures of damage, such as the frequency of pain-sensor discharge or the amount of degraded tissue, may indicate a serious state. Yet if the site affected is small, the overall effect on the animal may be inconsequential. Conversely, a stimulus of much milder intensity acting over a large area may constitute a handicap that leads to debilitation and death. The practical implications of this are important in cases of chronic infestation with parasites, or the simultaneous imposition of numbers of minor stimuli any one of which might be imperceptible, but which collectively cause drastic disturbances to animal function.

3.2.2

Hazard Avoidance and Lethal Limits

A stimulus may be so intense as to constitute an immediate threat to life. When an animal encounters such a threat, its response may be dominated by one of the physiological mechanisms that have apparently evolved to cope with such

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Fig. 3.4 (a) Different patterns of nerve stimulation resulting in equal inputs to homeostatic control mechanisms (b) Different combinations of stimulus intensity and area which result in responses which are associated with: (I) easy coping, (II) coping with difficulty, or (III) failure to cope

emergencies. These include the withdrawal reflex, the orientation reaction, the alarm response, and the tendency to flee or ‘freeze’, i.e. stay still. High intensity heat, light, noise, or pain activate powerful neurally-based reflexes to withdraw the affected part

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of the body from the noxious stimulus. In emergency situations all of these responses minimise damage and promote survival, but the inflexibility of the response can constitute a handicap. For example, hasty flight from a competitor without planning may exacerbate the problem. Freezing can be an appropriate and efficient response to threat but it has also been reported to disorganise other escape behaviour (Stephens 1988): animals stopping while crossing a busy road are sad examples. In extreme cases, stimuli can cause irreversible damage very quickly to an animal. Burns and traumatic wounds may be so severe that, once inflicted, an early death is the only possible outcome. Alarm and emergency responses may help animals avoid or minimise the effects of some hazards. For instance, toxic substances in the diet are hazards encountered by many individuals during their lifetime. The factors which minimise the likelihood of these substances having harmful effects include detoxification, especially by the liver, and behaviour patterns such as avoidance, or taking only small quantities, of novel foods. Individuals also learn to associate adverse effects with a particular food. The adaptation of an animal to an environment containing poisons will be limited by its capacity for detoxification, and by any failure to limit input or learn quickly that an ingested substance is harmful (Broom 1981).

3.3

Variation in Adaptation Has Consequences for Responses to Stimulation

The colonisation by animals of virtually every part of the world—deserts, swamps, city centres and Arctic tundra—indicates their wide tolerance of environmental conditions. There are, however, obvious species differences in sensitivity to various factors such as dehydration, noise, temperature, and so on. Some animals are acutely sensitive to cold, others are much more tolerant of it; some need food frequently, others easily cope with periods of reduced food availability. Adverse circumstances are not the same for all species, and this must be borne in mind when considering how to minimise stress and improve welfare. Ultimately a unique assessment is required for each situation, according to the needs of the animals concerned, as described in Chap. 9. However, some generalisations can be made. Two potentially noxious stimuli imposed together will generally evoke a greater response than either alone. However, an additive effect, a simple summation of the responses, cannot be assumed, for the combined response may be greater than the sum of the components. An occasional rustle in the undergrowth or a distant wolf howl might not result in any response from a deer, whereas both together might precipitate flight. On the other hand, the combined effect of two factors might be smaller than the addition of the two effects. Cattle living in tropical climates eat less and have a resultant fall in metabolic heat production and this allows them to tolerate the hot climate better. Hence providing less food for animals in environmental temperatures above normal can lead to less of a problem for the animal than

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would imposition of either food deprivation or heat load alone. Over many generations, animals that have adapted to such conditions need less feed intake and have improved heat tolerance.

3.4

Integrating Time, Intensity and Mode of Stimulation

The stimuli impinging on an animal vary in time (i.e. frequency and duration), intensity (i.e. density and area), mode (i.e. visual, gustatory, emotional, etc.), and degree of novelty. Before discussing how the process of integration might be achieved, we can outline the relatively simpler processes that presumably operate to integrate stimuli with different temporal and intensity characteristics. Figure 3.5 illustrates schematically how a sequence of stimuli of similar modality but varying duration and intensity could combine to constitute a lethal imposition, even though each one by itself is only moderate in its effects. Different kinds of negative stimuli can also combine to have effects that are much more than additive. When a wild animal is brought into captivity, possible impacts on it include: fear of human proximity, inability to show normal escape and other activity, absence of normal food, difficulty in controlling body temperature, exposure to new pathogens, and suppression of immune system function. Multiple stressors often result in death when each alone would not and adding expected effect would not. For example, wild birds and reptiles captured and sold for the pet trade have a high mortality rate

Fig. 3.5 Responses to a series of stimuli. Individually, these stimuli have moderate effects but, in combination, they are lethal

3.4 Integrating Time, Intensity and Mode of Stimulation

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between point of capture and point of sale, that of small birds being about 90% (Warwick et al. 2001; EFSA 2006). Few owners of wild-caught captive reptiles and birds realise the extreme mortality needed to provide for their desire for such a pet. Figure 3.5 illustrates possible changes in a single animal in a group of pigs, in which a social order has been established, in response to a particular sequence of events. At points 1 and 2, because of mixing of individuals unfamiliar with one another, aggressive challenges are made by other animals in the group, and the visual signals evoke transient responses which decline rapidly. Stimulus 3 arises because the pig is removed, somewhat roughly, from the group and put alone in a crate; the novelty of the surroundings and absence of companions elicits an increased response. Although the animal begins to habituate to this new situation, before the response has appreciably subsided, the animal is driven by an unfamiliar and unsympathetic stockman to a set of weighing scales, at point 4. Domestic pigs, especially those of some breeds, are severely affected by handling and may suffer cardiac problems as a consequence. When the same handler returns and begins loading the animal onto a truck, at point 5, the experience adds to the animal’s previous unpleasant experience and induces a cumulative effect such that the animal collapses and dies. In this example, we can easily appreciate the nature of the stimuli because they are visual or physical experiences, or recollections of such factors. In reality, stimulations are likely to be of various modalities. An animal may see a predator, hear a call from its offspring, experience a parasite biting its skin, have a sensation from its empty stomach, or be frustrated as a consequence of some restrictive aspect of its environment. All of these, and other stimuli as well, may converge on the animal’s sensorium simultaneously. Will the various stimuli be additive or multiplicative? The combined effect of a number of stimuli is likely to be more than that of any single stimulus. It is also possible that a combined stimulation could overwhelm an animal, even if each component stimulus could easily be accommodated. Additivity cannot be assumed and submitting animals to multiple problems can constitute cruelty. Is it possible to predict the integrated effect? The practical answer is often no, for several reasons. Stimuli vary in their sensory impact on an animal, in the responses they evoke, and in the extent to which they are remembered, and thus in their influence on subsequent exposures. Some stimuli elicit a reflex nervous response; others a hormonal response of slow onset. Some species have acute sensitivity to particular stimuli and relative insensitivity to others. Beyond appreciating that environmental and endogenous stimuli are collectively and cumulatively affecting each animal, the task of attempting to predict the integrated effect is very complex. In every situation, a reasoned risk assessment of the magnitude of the problem for the animal, taking account of the possibility of multiplicative effects, should be carried out. It was suggested by Selye (1950) that the combined impact of noxious stimulation is indicated by the output of glucocorticoid hormones from the adrenal cortex but this is now known to be incorrect, see Chap. 4.

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3.5

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Limits to Adaptation

The Concepts of Tolerance and Coping

Figures 3.4b and 3.5 depict the range of stimulation and response that an animal can tolerate, and this is divided into three. Responses in the first range (i.e. those below the first level marked on the diagrams) are to a stimulus which elicits a measurable response but which is tolerable indefinitely. For instance, people cope with such impositions as moderate heat or cold exposure, partial loss of sight or loss of some teeth; humans or other animals can bear easily minor scratches or bruises, a low level of parasitism, or low-level social abrasion. Such impositions may have a measurable effect on the individual concerned but it can be tolerated with no detectable detrimental effect in the long term. Indeed, some such stimulation early in life may be essential for effective later adaptation. Appreciably greater impositions on an animal may also be tolerable indefinitely, but induce temporary penalties of displaced homeostatic control and disturbed physiological, immunological and behavioural functioning. These responses are in the second range and some examples arise from a stimulus that causes pain but not permanent damage. This is the most widespread category of situations that adversely affect welfare. In human terms, such a situation might occur when a man has difficulties at work over several months, during which he develops stomach ulcers, finds social interactions troublesome, develops neurotic behaviour and succumbs more readily than usual to viral infections. He survives, and there may be no longterm detrimental effects, but coping has clearly been difficult for him during this time. Most people would consider that these are circumstances in which the welfare of the individual is considerably worse than normal, and would try hard to avoid them. The most serious impositions on an animal’s homeostasis are stimuli that elicit a response in the top range: they can be tolerated only for a strictly limited time, and if they continue, permanent damage and then death ensue. Within this range, the duration that can be tolerated may be a minute or a month before the animal succumbs. Figure 3.6 depicts the range of responses to stimuli in relation to coping and tolerance. The upper limit of the top range is the maximum response possible by the animal. Should the stimulus strength exceed that which elicits the maximum response, some of the disturbance will, by definition, be uncompensated. Incompletely compensated disturbance of a homeostatic system will cause progressive displacement of physiological variables outside the range necessary for survival. The animal will succumb unless corrective measures are taken. By proposing that there are varying levels of tolerance we are also introducing the notion that there is an inverse relation between strength of stimulus and tolerance time. That is to say, stimulations that are severe will be tolerated only briefly. A painful but localised injury such as a deep knife cut, or a traumatic event such as the death of an acquaintance are disturbing events that would be even more distressing if their effects were not relatively transient. More moderate stimulation, such as from a viral infection or social antagonism, is tolerable for longer periods, but if it continues indefinitely, the person or animal will be handicapped by the excessive stimulation

3.5 The Concepts of Tolerance and Coping

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Fig. 3.6 Levels of responses to stimuli in relation to coping ability and the extent to which these stimuli and responses can be tolerated

and may die prematurely. The mildest effects of endogenous or exogenous disturbance can be coped with without a biological penalty, and may perhaps even confer a biological advantage in terms of lifestyle, production or reproduction; for example, when experience of minor social altercations prevents the subsequent occurrence of more severe social problems. An important concept used in Fig. 3.6 is coping. In the scientific literature the ability to tolerate different degrees of stimulation, particularly noxious stimulation, is embodied in the concept of coping. In an account of human adaptation to various stimuli, Lazarus and Folkman (1984) suggested that it is the extent of the ability to cope that ultimately determines whether the individual survives in unfavourable conditions. To cope is to have control of mental and bodily stability (Fraser and Broom 1990) see Chap. 1. This control may be short-lived or prolonged but failure to be in control of mental and bodily stability leads to reduced fitness. Coping implies using the brain so is limited to animals. Other individual organisms may adapt to adverse conditions but do not cope as they have no nervous system. The interrelation between tolerance and coping requires further explanation. When an animal is under a moderate degree of continuous stimulation, but nonetheless coping, as in Fig. 3.5 after the third stimulus, its capacity to cope with subsequent stimuli could be reduced. In Fig. 3.5, the capacity for coping with future difficulties after the third stimulus is only about half that existing in the unstimulated animal. This is only one possible scenario as it could be that by switching to an alternative coping method, e.g. from active flight to freezing, the individual could enhance its efficiency of coping.

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Limits to Adaptation

Variations in Patterns of Adaptation Differing Rates and Methods of Adaptation

Disturbances of an animal’s homeostatic regulation induced, for example, by changing its feeding site, thermal regime or social grouping, take varying periods to be accommodated. If the feeding site on a farm or in a zoo were changed, the visual stimulus would be instantly recognized by the animal. The animal’s adjustments to the change would be rapid as long as there were no other social readjustments to be made, say, by being forced into the proximity of a rival. If, on the other hand, the feeding place of an animal was altered because it was being transported by truck, the modified visual stimulus would soon be accommodated, but the animal would need to develop new skills of balance and of coping with noise, vibration, and other physiological and chemical problems. Adaptation of physiological systems to this more complex environment would be slower. In humans and other species there are individual differences in coping methods (Leitenberg et al. 2004; Koolhaas et al. 2010). Individuals have established structures in their lives, including their place in social systems and patterns of where and when to feed, so disruption may disturb some individuals more than others. Individuals may also differ in adaptability to disruption because of their biological rhythms, for example the ovarian cycle. Females may accept environmental change more readily at one stage of their ovarian cycle than another. Sexual activity can also be strongly seasonal and hierarchical in males, such as deer. The effect of disturbance on stags will therefore depend greatly on the time of year and the social position of the animal. Each animal has a unique set of lifetime experiences upon which the process of accommodating change depends. There are inevitably differences among species in the readiness with which individuals adapt to environmental disruptions. Certain species are generally unable to adapt to zoo conditions and show abnormalities of behaviour, physiology, reproductive ability or disease susceptibility. In contrast, other species appear to adapt quickly and quite adequately to good zoo conditions. The difference is a result of their adaptation to the normal ecosystem in which the species lives. Clubb and Mason (2003) reported that animals that range over large areas in the wild are less well able to adapt to zoo environments and concluded that many of such species should not be kept in zoos as their welfare could never be good. For example, while brown bears, American mink and snow leopards adapted quite well to zoo conditions, clouded leopards and polar bears were likely to show stereotypies and other abnormal behaviour and physiology. The needs of some small animals and some domesticated animals can be met and their welfare can be good in zoos. However, the needs of many animals are not met in most zoo conditions so they should not be kept in zoos. When animals are obviously adversely affected by the conditions in zoos, members of the public may refuse to visit the establishments, exhibits or performances (Margodt 2000). While this is the case, there are still plenty of people willing to visit zoos, as evidenced by the continuing popularity of these tourism

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attractions. Suggestions about moral practices for zoos, in relation to the ethics of keeping animals that have different capabilities to adapt to the conditions, are detailed by Broom (2002, 2018).

3.6.2

Hypersensitivity

The levels at which stimulation becomes intolerable can alter with physiological and seasonal rhythms, and also depends on personal experience. They are set uniquely for each individual. Hypersensitivity is a further factor affecting the responses of individuals to environmental change. In terms of the operation of an input–output model of physiological regulation (Fig. 2.3b), the cause of hypersensitivity could be considered as a lowering of the set-point of the control system, or as an increase in the gain of the system. The result is that a given stimulus elicits a greater response than expected in such an animal. In circumstances of increasing stimulation, intolerable levels of response are reached more rapidly in a hypersensitive animal, and if these continue the animal will succumb and die sooner.

3.6.3

Hyposensitivity and Stress-Induced Analgesia

Reduced sensitivity to stimulation, or hyposensitivity, has been the subject of special study because of its relation to pain relief, or analgesia. Testing whether some animals tolerate noxious stimulation better than others, and whether it is because they have lower sensitivity, is fraught with methodological difficulties. Nonetheless, considerable evidence is available that exposure of animals to noxious stimulation can be associated with some suppression of the pain response because substances that have an analgesic effect are released within the central nervous system (CNS) and maybe elsewhere in the body. These substances, the enkephalins, endorphins and dynorphin, are chemically related to opioid drugs used as analgesics (Clarke et al. 2014). They occur in various CNS pathways, and their action in the brain can be blocked by various substances including naloxone. Agents other than endogenous opioids may also be involved, for example endocannabinoids (Hohmann et al. 2005). Opioids commonly act over long time-spans, but some analgesia is produced quickly. Furthermore, stimulation of sites in some parts of the brain, such as the locus coeruleus, can inhibit pain rapidly. The non-opioid systems for stress-induced analgesia are short-term. The combined short- and long-term systems appear to act as specific adaptive mechanisms to generalised excesses of stimulation. Examples of such analgesia are the reports, by those in battle, of limb loss or other very severe injury, without any sensation that this has happened and suppression of responses to mechanical pressure on the uterine cervix, tail pinch, localised heat, foot shock or cold water in rats.

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Free-living animals repeatedly face situations in which noxious stimulation is unavoidable, for example, when defending territory or offspring, or foraging in hostile climates. When caught and injured by a predator, it may be best for an animal’s chances of survival not to show an obvious pain response but this must be considered an extreme form of trying to cope.

3.7

Other Factors Affecting Adaptation and Coping

Animals have substantial welfare problems when they lack control of their interactions with their environment. Adaptation is clearly more difficult, or indeed impossible, if the control mechanisms cannot operate properly.

3.7.1

Lack of Stimulation

In natural conditions, animals are frequently stimulated by changes in their physical and social environments. Where animals are brought under closer environmental control, on farms, in zoos, or in people’s homes as pets, the levels of some of many components of stimulation are reduced, while others are increased. The reduced environmental stimulation is usually planned by people, partly to make animal management easier, but also to minimise the adverse effects on the animals of variability in temperature, food supply, etc. Paradoxically, although some adverse effects may be reduced, others can increase considerably. The net effect of attempting to reduce stimulation is usually greater difficulty for the animal to control its life and hence poorer welfare. The lack of control in the barren environments normally provided for farm, working, laboratory, zoo and some pet animals is, in part, because the animals have expectations of the consequences of different types of activity such as foraging, social interaction, and so on. Where these do not materialise, the animals are not able to utilise fully their own array of controlling procedures. Some animals respond to lack of stimulation with apathy, a response apparently associated with the lowest level of stimulation. Other animals, instead of becoming apathetic, may contrive to replace programmed requirements with stimuli of their own making, so that these appear as repetitious activities, or stereotypies. Not being responses to specific stimuli, such stereotypies can be manifest not only as purposeless routines, but as behaviour that damages the animal itself or others in its vicinity. There are close parallels in humans who are imprisoned or who experience at work a lack of stimulation, sometimes because of repetitive tasks. Such people can develop psychological disturbances due to failure to adapt. The relation between level of stimulation and level of response (Fig. 3.4) can be modified to show that with sustained low levels of stimulation, i.e. sensory deprivation, the response is appreciably elevated (Fig. 3.7), with adverse effects. The response that is elevated may be

3.7 Other Factors Affecting Adaptation and Coping

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Fig. 3.7 Responses to different levels of stimulation. If the level of stimulation is too low, responses can be high. Sensory deprivation or barren environments, as well as overload, can lead to poor welfare

the extreme response of inactivity and unresponsiveness. i.e. depression. For example, the whiskers, or vibrissae, of rats are important sources of sensory information and removal of these whiskers leads to changes in intracortical excitatory synapses in the somatosensory cortex, associated with long-term depression, and some of the neural mechanisms are now known (Allen et al. 2003; Margolis et al. 2012). A second consequence of lack of environmental stimulation, that is equally serious and also related to depression, is a loss of the capacity to cope with new environments. The mechanisms of coping appear to require repeated use and reinforcement, otherwise the ability to cope is reduced.

3.7.2

Unpredictable Stimulation

Response to stimulation is always likely to be more effective if there is some accurate anticipation of what is likely to happen. Mechanisms to achieve this exist

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as feedforward controls (Chap. 2). When there has been no prior experience of a situation, there can be no anticipation of what might be encountered so novelty is often disturbing. A variation of this problem arises when a pattern of stimulus and response has been established, for example in relation to feeding times or social groupings, but is then unpredictably disrupted. Animals encountering such unpredictable stimulation can become aggressive. Carlstead (1986) presented food to pigs kept in groups and, at the same time, a bell was sounded. If the bell and food presentation were suddenly changed so that they were no longer associated in time, the pigs showed much more aggression than they did during the period when the stimuli were associated, and more than did pigs which had been presented with the bell and food randomly throughout the study. When such situations continue, animals begin to show signs of maladaptation. Unpredictable and novel stimulation, or the absence of expected inputs, means that the animal has less control and is not able to regulate effectively. The extent to which an individual is disturbed by novel stimuli is reduced if that individual has had more complex early experience, for example in domestic chicks and in calves (Broom 1969; De Paula Vieira et al. 2012).

3.7.3

Frustration of Behavioural Output

Adaptation can also be disrupted if most of the factors required to effect a response are present, but critical ones are missing. In some circumstances, a genetically established reflex or learned response, such as to feed, mate, or escape, is appropriate, but one, or a few, of the essential factors are absent and the animal is thwarted in its efforts to carry out the activity. If the levels of most of the causal factors that promote a behaviour are high enough for the occurrence of the behaviour to be very likely but, because of the absence of a key stimulus or the presence of some physical or social barrier, the behaviour cannot occur, the animal is said to be frustrated (Broom 1985). If, under these circumstances, a response cannot be completed, the animal may direct its energies into another activity, not uncommonly into aggression against nearby animals. Duncan and Wood-Gush (1971, 1972) (see Duncan 2019) accustomed pairs of hens to being fed from a dish in a cage. If the dish was covered with a transparent cover, so that the hens were frustrated in their attempts to obtain the food, the hens showed a substantial increase in stereotyped pacing (Table 3.1) and an increase in aggressive pecking by one of the pair (Table 3.2). The response is similar in some of its physiological and behavioural characteristics to that of animals attempting to adapt to noxious stimulation. Like unpredictability of stimulation, frustration disrupts established patterns of adaptation to environmental change. When animals attempt to respond to stimuli that are associated with very aversive events, but are repeatedly unable to prevent the event, they may stop responding entirely to events in the world around them. This condition occurs in rats following

3.8 Effects of Human Selection of Animals on Their Ability to Adapt

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Table 3.1 Effects of frustrating hens on stereotyped pacing (data from Duncan and Wood-Gush 1972)

Hen deprived of food then fed Hen not deprived Hen deprived of food then food provided under transparent cover

Mean number of stereotyped pacing routines in SO minutes 13.3 18.7 161.0

Table 3.2 Effects of frustrating hen by food deprivation on attacks on subordinate hen (from Duncan and Wood-Gush 1971) Hours of food deprivation 2.5 5 7.5

Median number of attacks on subordinate hen in 20 min 3 11 18

repeated inescapable shock, and was called ‘learned helplessness’ by Maier and Seligman (1976). It was suggested that the rats learned that there was no way in which they could prevent themselves from being shocked, and so underwent various emotional and motivational changes which made it difficult for them to learn any new associations.

3.8

Effects of Human Selection of Animals on Their Ability to Adapt

In the wild, where a wide range of environmental factors act, genetic selection leads to an animal genotype that is well adapted to the environment. However, selective breeding by humans is aimed at increasing certain characteristics that are advantageous to those who attempt to manage the selection. This selection alters the distribution of resources that contribute to the animal’s body form and physiology. One consequence may be characters that are, in some or all environments, biologically maladaptive, whilst another consequence is that the quantity of resources available for other characteristics can be reduced. The idea that there are limits to the extent to which individual domestic animals can adapt to difficult environments, and that human selection has caused many of the problems, was presented by Beilharz (1985) and is discussed further by Rauw (2008). Conventional breeding methods need not affect welfare but can change animals in such a way that they have more difficulty in coping or are more likely to fail to cope (Broom 1995). One example of such an effect is the sensory, neurological or orthopaedic defects found commonly in certain breeds of dog (Rooney and Sargan 2010), for example the widespread brachycephalic obstructive airway syndrome in French Bulldogs (Liu et al. 2015). Other examples are the effects of the genes

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promoting obesity in mice, double muscling linked to parturition problems in cattle and many examples of selection promoting fast growth and large muscles in farm animals. Modern strains of pigs have relatively larger muscle blocks, more anaerobic fibres and smaller hearts than have the ancestral strains (Dämmrich 1987). They are more likely to die or to become distressed during any vigorous activity, for example during transport. Modern broiler strains grow to a weight of 2–2.5 kg in 35 days as compared with 12 weeks 40 years ago. Their muscles and guts grow very fast but the skeleton and cardiovascular system do not. Hence many of the birds have leg problems, such as tibial dyschondroplasia or femoral head necrosis, or cardiovascular malfunction often giving rise to ascites (Bradshaw et al. 2002; Knowles et al. 2008). Genetic selection of dairy cows for high milk production has led to increased leg disorders, mastitis and reproductive disorders, all of which are major welfare problems (Oltenacu and Broom 2010). Modern biotechnology, such as the use of genetically modified animals and cloning by nuclear transfer, can greatly accelerate genetic change in domestic animals, thus increasing the risk that the breeding procedures result in animals that cannot adapt to important aspects of the world in which they have to live (Broom 2014, 2018).

References Allen CB, Celikel T, Feldman DE (2003) Long-term depression induced by sensory deprivation during cortical map plasticity in vivo. Nat Neurosci 6:291–299 Beilharz RG (1985) Special phenomena. In: Fraser AF (ed) World Animal Science A5. Ethology of farm animals. Elsevier, Amsterdam, pp 363–370 Bradshaw RH, Kirkden RD, Broom DM (2002) A review of the aetiology and pathology of leg weakness in broilers in relation to welfare. Avian Poult Biol Rev 13:45–103. https://doi.org/10. 3184/147020602783698421 Broom DM (1968) Specific habituation by chicks. Nature 217:880–881 Broom DM (1969) Effects of visual complexity during rearing on chicks’ reactions to environmental change. Anim Behav 17:773–780 Broom DM (1981) Biology of behaviour. Cambridge University Press, Cambridge, p 320 Broom DM (1985) Stress, welfare and the state of equilibrium. In: Wegner RM (ed) Proceedings of second European symposium on poultry welfare. World Poultry Science Association, Celle, pp 72–81 Broom DM (1995) Measuring the effects of management methods, systems, high production efficiency and biotechnology on farm animal welfare. In: Mepham TB, Tucker GA, Wiseman J (eds) Issues in agricultural bioethics. Nottingham University Press, Nottingham, pp 319–334 Broom DM (2002) Welfare in wildlife management and zoos. Proceedings of the 4th international congress on the physiology and behaviour of wild and zoo animals. Adv Ethol 37:4–6 Broom DM (2014) Sentience and animal welfare. CABI, Wallingford, p 200 Broom DM (2018) Animal welfare and the brave new world of modifying animals. In: Grandin T, Whiting M (eds) Are we pushing animals to their biological limits? CABI, Wallingford, pp 172–180 Carlstead K (1986) Predictability of feeding: its effect on agonistic behaviour and growth in grower pigs. Appl Anim Behav Sci 16:25–38 Clarke KW, Trim CM, Hall LW (2014) Veterinary anaesthesia. Saunders Elsevier, Edinburgh, p 712

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Clubb R, Mason G (2003) Animal welfare: captivity effects on wide-ranging carnivores. Nature 425:473–474 Dämmrich K (1987) Organ change and damage during stress – morphological diagnosis. In: Wiepkema PR, van Adrichem PWM (eds) Biology of stress in farm animals: an integrated approach. Martinus Nijhoff, Dordrecht, pp 71–81 De Paula Vieira A, de Passillé A-M, Weary DM (2012) Effects of the early social environment on behavioral responses of dairy calves to novel events. J Dairy Sci 95:5149–5155 Duncan IJH (2019) Frustration in hens. In: Choe JC (ed) Encyclopedia of animal behavior, vol 3, 2nd edn. Elsevier, Academic Press, pp 79–82. https://doi.org/10.1016/B978-0-12-809633-8. 90069-4 Duncan IJH, Wood-Gush DGM (1971) Frustration and aggression in the domestic fowl. Anim Behav 19:500–504 Duncan IJH, Wood-Gush DGM (1972) Thwarting of feeding behaviour in the domestic fowl. Anim Behav 20:444–451 EFSA (2006) Animal health and welfare risks associated with the import of wild birds other than poultry into the European Union. EFSA J 410:1–55 Fraser AF, Broom DM (1990) Farm animal behaviour and welfare. CAB International, Wallingford, p 437 Frese M, Zapf D (1988) Methodological issues in the study of work stress: objective vs subjective measurement of work stress and the question of longitudinal studies. In: Cooper CL, Payne R (eds) Causes, coping and consequences of stress at work, vol 376. Wiley, Chichester Hohmann AG, Suplita RL, Bolton NM, Neely MH, Fegley D, Mangieri R, Krey JF, Walker JM, Holmes PV, Crystal JD, Duranti A, Tontini A, Mor M, Tarzia G, Piomelli D (2005) An endocannabinoid mechanism for stress-induced analgesia. Nature 435:1108–1112. https://doi. org/10.1038/nature03658 Kant GJ, Eggleston T, Landman-Roberts L, Kenion CC, Driver GC, Meyerhoff JL (1985) Habituation to repeated stress is stressor specific. Pharmacol Biochem Behav 22:631–634. https://doi. org/10.1016/0091-3057(85)90286-2 Knowles TG, Kestin SC, Haslam SM, Brown SN, Green LE, Butterworth A, Pope SJ, Pfeiffer D, Nicol CJ (2008) Leg disorders in broiler chickens: prevalence, risk factors and prevention. PLoS One 3(2):e1545. https://doi.org/10.1371/journal.pone.0001545 Koolhaas JM, de Boer SF, Buwalda B (2010) Neuroendocrinology of coping styles: towards understanding the biology of individual variation. Front Neuroendocrinol 31:307–321. https:// doi.org/10.1016/j.yfrne.2010.04.001 Lazarus RS, Folkman S (1984) Stress, appraisal and coping. Springer, New York, p 456 Leitenberg H, Gibson LE, Novy PL (2004) Individual differences among undergraduate women in methods of coping with stressful events: the impact of cumulative childhood stressors and abuse. Child Abuse Negl 28:181–192. https://doi.org/10.1016/j.chiabu.2003.08.005 Liu N-C, Sargan DR, Adams VJ, Ladlow JF (2015) Characterisation of brachycephalic obstructive airway syndrome in French bulldogs using whole-body barometric plethysmography. PLoS One 10(6):e0130741. https://doi.org/10.1371/journal.pone.0130741 Maier SF, Seligman MEP (1976) Learned helplessness: theory and evidence. J Exp Psychol Gen 105:3–46 Margodt K (2000) The welfare ark: suggestions for a renewed policy in zoos. VU University Press, Brussels Margolis DJ, Lütcke H, Schulz K, Haiss F, Weber B, Kügler S, Hasan MT, Helmchen F (2012) Reorganization of cortical population activity imaged throughout long-term sensory deprivation. Nat Neurosci 15:1539–1546 Oltenacu PA, Broom DM (2010) The impact of genetic selection for increased milk yield on the welfare of dairy cows. Anim Welf 19(S):39–49 Rauw WM (ed) (2008) Resource allocation theory applied to farm animal production. CABI, Wallingford

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Rooney NJ, Sargan DR (2010) Welfare concerns associated with pedigree dog breeding in the UK. Anim Welf 19S:133–140 Selye H (1950) Stress and the general adaptation syndrome. Br Med J 1:1383–1392 Sokolov EN (1960) Neuronal models and the orienting reflex. In: Brazier MA (ed) The central nervous system and behavior. Macy Foundation, New York Stephens DB (1988) A review of experimental approaches to the analysis of emotional behaviour and their relation to stress in farm animals. Cornell Vet 78:155–177 Warwick C, Frye FL, Murphy JB (eds) (2001) Health and welfare of captive reptiles. Springer, Berlin

Chapter 4

Stress and Welfare: History and Usage of Concepts

Abstract This chapter clarifies previous and current usage of the words in the title of this book. The ways in which the term stress has been used in physics, psychology, psychiatry and general biology are discussed in detail. Using diagrams, response changes over time and their consequences are considered. The terms stereotypy and quality of life are defined. The authors’ view of the optimal use of stress and welfare is presented. A key part of the discussion of welfare concerns how to promote good welfare. In order to do this, and to avoid poor welfare, general principles of methods for assessing welfare in a quantitative and objective way are explained. The relationships between welfare and: suffering, stress, naturalness, quality of life, a life worth living, and sentience are discussed. Equivalent words to welfare in different languages are considered. Keywords Stress · Welfare · Suffering · Quality of life · Stereotypy

4.1

Stress

In common usage the term ‘stress’ implies exposure to unpleasant conditions that lead to adverse effects. In its earliest reported usage in 1440 its meaning was hardship or adversity. Key questions about the meaning are what exactly qualifies as unpleasant, hardship, or adverse. A new meaning, that first became well known from studies of the elasticity of materials, was that of the physicist Robert Hooke (1635–1703). Hooke’s studies, originally reported in Latin, referred to stress as ‘the physical pressure exerted on an object’ and also discussed ‘the strain of a load or weight’ and stated that ‘strain is proportional to stress’ (Hooke 1678). In physicists’ terms, strain is the deformation produced when a body is subjected to a stress, and stress is the force producing that deformation. Stress is thought of as the causative agent, strain as the response. The physicists’ differentiation between strain and stress has had limited influence on common use. In current dictionaries the terms often have virtually identical definitions. Stress has thus been used, illogically, to refer to both the cause of a disturbance and its effect. © Springer Nature Switzerland AG 2019 D. M. Broom, K. G. Johnson, Stress and Animal Welfare, Animal Welfare 19, https://doi.org/10.1007/978-3-030-32153-6_4

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The usages of the terms stress and strain, originally proposed by physicists, have been used in a confusing way in various branches of science over many years. They have appeared in physiology, ethology, animal science, psychology and ecology with scientifically unfortunate consequences. An effort to standardise definitions of stress was the work on biological adaptation to adverse environments by Hans Selye. Although aware of the original usage of stress and strain in physics (Selye 1976), Selye proposed an alternative vocabulary in which he suggested that stress was the biological consequence of exposure to adverse environments (Selye 1973). Selye described the adverse conditions themselves as ‘stressors’, and also referred to ‘stress responses’. Unfortunately, he used the word stress in several different ways and it later became clear that the scientific basis for his usage was unsound. Selye (1993) said: “my definition of stress is the nonspecific (that is, common) result of any demand upon the body, be the effect mental or somatic”. He argued that secretion of adrenal glucocorticoids is a widespread, non-specific response, as are suppression of the immune system, and the formation of gastro-intestinal ulcers. Furthermore, he noted similar patterns of physiological response in a range of animal species. These he summarized as: first an ‘alarm’ reaction, then a stage of physiological resistance to the disturbance involving glucocorticoids, and, if this continues for long enough, a stage of exhaustion of the adaptive processes, leading to death. The apparent general applicability of these concepts encouraged other studies, many of which confirmed that similar physiological responses could indeed be produced by a variety of different environmental conditions. The impression of a consistency in physiological responses to adversity led to wide acceptance of Selye’s ideas. Unfortunately this reached a point where the significance of reports that did not conform to Selye’s hypothesis was ignored. In recent years it has become apparent that, whilst some of what Selye said is helpful, his theory is not sufficiently precise to form a basis for theoretical arguments. Four reservations have been noted about Selye’s theory. First, the biological response to adversity does not always involve glucocorticoids as proposed, so his theory should not be taken as an assumption in experimental studies. Second, similar patterns of physiological responses can occur following both stressful and manifestly non-stressful stimuli. Third, Selye’s inconsistent use of terms has increased rather than dispelled confusion. Fourth, most of Selye’s uses of stress are different from the historical and widespread public use. In relation to the first point, similar physiological responses can follow a variety of adverse stimuli, but they are far from universal. Detailed analysis of the hormonal response, using assays that were not available to Selye, reveals that the physiological response is much more variable than Selye contended when advocating the existence of a ‘general adaptation syndrome’. Work by Mason’s group (Mason 1968, 1971, 1975a, b; Mason et al. 1968a, b, c, d, e, f) showed that, whilst cold conditions increased the activity of the adrenal cortex of rhesus monkeys, other unpleasant and sometimes life-threatening situations, which the monkeys would avoid if they could, did not lead to this response. For example, adrenal cortex activity decreased rather than increased when there was a gradual increase in environmental temperature to a level that required considerable corrective action. Also, there was often no response

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to haemorrhage, close confinement which had lasted for some time, or to a diet that was entirely non-nutritive so the individual was effectively fasting. A further example of an adverse situation eliciting no adrenal cortex response is dehydration in sheep (Thornton et al. 1987). Humans exposed to relatively high temperature in a sauna did not show an increase in cortisol unless other stimuli or expectations were involved (Pilch et al. 2007, 2013). High environmental temperature, lack of food and lack of water are all situations in which it is not biologically adaptive to show an adrenal response that would tend to use up energy and increase body heat production. In dehydrated sheep an adrenal response either is not initiated or is suppressed by more pervasive responses. The major criticism of Selye’s theory is that the neuroendocrinological and other biological responses to adversity are varied and stimulus dependent. It is clear that not only the neuroendocrinological but also the behavioural and immunological responses to noxious stimuli extend across considerable ranges. Recent studies reveal a complex interactive network of relationships among various parts of the brain and body involved in responses to adverse environmental conditions. Peptides, such as corticotrophin releasing hormone, ß-endorphin and others, are released and have a variety of different effects within the brain and body which vary with the levels of other peptides present at the time. In addition, it has been found that the adrenal cortex and the immune system have feedback effects on the production of peptides that are active in the brain. Effective opioid peptides include ß-endorphin, enkephalins and dynorphin, receptor sites for which exist in the brain and various other parts of the body, including on lymphocytes. It is clear that there is no single stress response, but rather a wide range of physiological and other changes which, although overlapping in some components, are usually quite specific to circumstances. The biological response to stress is considerably less uniform than the response proposed as the central tenet of Selye’s theory. The second problem with Selye’s hypothesis has arisen following more accurate and extensive analyses of the adrenal hormone production. Glucocorticoids are released in response to situations that are not normally regarded as stressful, including courtship, copulation and hunting (Broom 2017, see Chap. 1). Species differences also exist, and certain stimuli that elicit an undoubted adrenal response in one species cause little or no effect in others. As a result, single adrenal indices must be considered questionable indicators of stress in many circumstances because of the poor correlation with adverse effects, the specific effect of different stresses, and the wide individual variation (Moberg 1987; Ralph and Tilbrook 2016). The third difficulty is Selye’s inconsistent use of the word stress. Sometimes even within the same publication, Selye and those writing in support of his theories have used stress to indicate an environmental factor, the process by which such a factor affects an animal, and the long-term consequences of these environmental effects. Different words are needed for these different meanings. Use of the word ‘stress’ to describe long-lasting responses to environmental exposure is particularly distant from the physicists’ use of the term. The fourth problem with the terminology introduced by Selye is that it often differs from common usage. Before stress came to be equated with adrenocortical

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activity, as a result of Selye’s writings, or stress was used to mean just a disturbance of homeostasis, definitions and usage of stress and strain always implied adversity. Yet Selye (1973) has argued that ‘stress is not something to be avoided . . . we can enjoy it by learning more about its mechanism’. Such use of the term can only lead to confusion. This can be circumvented by discriminating between ‘stress’, which certainly should be avoided, and ‘stimulation’, which is an integral part of life and cannot be avoided. In fact, a minimum level of stimulation is desirable, as indicated in common usage by the implied value of ‘a stimulating environment’. The uncertainty resulting from this confusion reached such a level that some authors concluded that we would be better off without the term ‘stress’, or argued that stress cannot be defined and have recommended that the term be avoided (Freeman 1987). However, as argued in the first edition of this book (Broom and Johnson 1993), the concept of stress is important and valuable scientifically and socially so what is required is a clear definition for scientific use that is not too different from the meaning ascribed to the term by the general public. This is the basis for the definition presented in Chap. 1. It has gradually become apparent since the experimental studies of stress that were encouraged by the early studies of Cannon and Selye that psychologically disturbing situations are important causes of emergency responses. Mason (1971) emphasized that expectations and fears were important causes of adrenal cortex responses for animals. Lazarus (1993) described some of the differences between the physiological and behavioural consequences of psychological threats and physical threats. He pointed out difficulties in explaining psychologically what was a load or stressor. and also emphasised differences between harms, threats and challenges. His discussion of the wide range of coping responses, emphasising the adaptive contributions of various emotions, was particularly helpful. In arguments about what stress means, McGrath (1970) said that it is an ‘imbalance between environmental demand and response capability’. Lazarus and Folkman (1984) emphasized the importance of the perception of such an imbalance, by describing stress as ‘a particular relationship between the person and the environment that is appraised by the person as taxing or exceeding his or her resources and endangering his or her well-being’. These descriptions are not easily usable as definitions but are scientifically much better than ‘anything which causes an adrenal cortex response’. The ability of the individual to cope with whatever challenge is received has often been included in discussions about stress in the human psychological literature. For other animal species, however, individual variation in coping has been mostly ignored when stress has been considered. Some psychologists tend to overemphasize the importance of perception and coping, and forget about physical threats to the individual as sources of stress. This no doubt arises partly from different methods of study used on human and non-human subjects. However, Hobfoll (1989) defined psychological stress as a reaction to the environment in which there is real or threatened loss of resources, or a lack of gain following an investment of resources. The definition apparently includes any reaction to the environment, even the smallest one, and there may be factors that are not valued by the individual but should be, because their lack will cause problems; painful

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treatment for a serious disease would be an example. More recently, Ralph and Tilbrook (2016) proposed that stress is “a complex physiological state that embodies a range of integrative and behavioral processes when there is a real or perceived threat to homeostasis”. As with some previous proposals, this would include extremely trivial environmental impacts so is an inadequate definition. We contend that problems with the concept and vocabulary of stress are best solved by simplification. Other words used to describe adverse effects on individuals, for example ‘eustress’, ‘overstress’ and ‘distress’ do not overcome the problem. Some indication of the extent of any disruption of homeostasis is required in the definition. However, to imply that stress refers only to a single physiological phenomenon such as adrenocortical activity is scientifically restrictive and unwarranted. A description of the sequence of events occurring when stressors affect a human or other animal (Fig. 4.1) was developed by Moberg (1985). Moberg described the extent of negative impact on the individual in terms of prepathological state and then pathology. Some adverse consequences of the

Fig. 4.1 Model for response of animals to stressful event (from Moberg 1985)

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environment may not be considered pathological and a pathogen that has only a small effect might not be hazardous to the individual so the wording is helpful as explanation but not optimal. Since it seems advisable to define stress by reference to its consequences, we are faced with the necessity of producing a precise criterion for what constitutes adverse or detrimental consequences. As we are dealing with a biological phenomenon, one possibility is to consider the fitness of the individual as the variable that is ultimately limited by exposure to stress. The idea that stress is something that reduces individual fitness was put forward in a gradually evolving form by Broom (1983, 1985, 1988b); Broom and Johnson (1993); Broom and Fraser (2015). The fitness of an individual is reduced if it is more likely to die and less likely to have offspring. Measures of this include: age at first breeding, interval between successive breedings, survivorship from birth to first breeding, survivorship of adults between successive breedings, and number of female offspring per female breeding attempt (Sibly and Calow 1983). In practice, a high likelihood of fitness reduction is obvious from a range of measures (Chaps. 5 and 6). As discussed in Chap. 1, it is best to define stress as an effect with negative consequences of an impact on a response system of some aspect of its environment. The effect of stress occurring is to cause some or all of the control systems within the individual to work too hard for effective functioning, that is, to overtax them. When considering the concept of stress, many people refer to loss of control, failure to cope and adverse effects on the individual. Figure 4.2 depicts the time courses of responses to various environmental effects and to their long-term consequences. It is the environment of the overall response system that is referred to here. Some effects are from outside the body whilst others are from within. An external threat, or a pathological condition within the body, or a change in the body partly caused internally and partly externally, can result in stress. Some responses have a simple regulatory effect, for example shivering or moving to a water source (Fig. 4.2a). Others, which are cross-hatched in the diagrams, are extra responses which are utilised only when the simple responses are not likely to be sufficient for the body state to be maintained within the tolerable range (Fig. 4.2b). Such responses can include adrenal activity and various behavioural changes. The distinction between simple regulatory responses and extra responses which do not occur if the environmental effect is easily overcome and which may occur in a wide range of situations is useful, but not always clear cut. There may be different, specific regulatory responses that are activated after different amounts of effect on the animal. Also, some behavioural responses, such as small birds mobbing a predator, may be secondary and restricted to a narrow range of situations. Extra responses need not be associated with long-term adverse effects. Responses may be required for only a short time (Fig. 4.2a, b, e), or the system may not adapt for a longer time (Fig. 4.2c, d), or not at all (Fig. 4.2f–i). However, even if the continuation of a response is necessary for a long period (Fig. 4.2c, d, f), there may be no long-term effects of the kind that would reduce the fitness of the individual. Even if some energy were used up compensating for cool conditions or predator presence over a long period, survival and reproduction need not be affected.

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In another circumstance (Fig. 4.2g), the response level appears similar but fitness is reduced. Adverse long-term consequences of the environmental effect and of the various responses to it may be nil or they may be so substantial that the fitness of the individual is reduced (Fig. 4.2e, g, h, i).

Fig. 4.2 (a) The schematic response to an environmental effect in a system which adapts fully; fitness is not reduced. (b) The schematic responses to an environmental effect which elicits extra responses in a system which adapts fully; fitness is not reduced. (c) The schematic response to an environmental effect in a system which does not adapt fully but fitness is not reduced. (d) The schematic responses to an environmental effect which elicits extra responses in a system which does not adapt fully but fitness is not reduced. (e) As Fig. 4.2b, but more extra responses are elicited and fitness is reduced. (f) The schematic responses to an environmental effect in a system which never fully adapts; fitness is not reduced. (g) As fig. 4.2f, but fitness is reduced. (h) As Fig. 4.2f, but more responses elicited and more reduction in fitness. (i) The schematic responses to an environmental effect which overwhelms the animal and drastically reduces its fitness

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Fig. 4.2 (continued)

4 Stress and Welfare: History and Usage of Concepts

4.1 Stress

Fig. 4.2 (continued)

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4 Stress and Welfare: History and Usage of Concepts

Fig. 4.2 (continued)

As discussed above with reference to adrenal cortex responses, the differentiation between ‘simple’ and ‘extra’ responses is not precise enough to be used in the definition of stress. The continuation of a response to an environmental stimulus has been considered as a criterion for stress but, as mentioned earlier, some of the responses are so minimal that there is no adverse effect on the individual and the term ‘stress’ is inappropriate when compared with common usage. However, if there is a reduction in the fitness of an individual, or if such a reduction seems likely to occur in the future, most people would consider the individual to be stressed, so this is the criterion for stress that is used here. Therefore, we reach the conclusion presented in Chap. 1, that: stress is an environmental effect on an individual which overtaxes its control systems and reduces its fitness or appears likely to do so. As explained above, environmental includes effects on the control systems from inside or outside the body. The response to stress and the immediate and short-term consequences of the stress may be called strain. Whether it lasts for a short period or for much of the animal’s life, the animal is unable to cope with it. As explained above, failure to cope implies reduced fitness. Some brief effects, such as being heated up a little by high environmental temperature, having an injection, or sustaining a minor injury, which are not likely to reduce the fitness of the individual would not be called stresses. Prolonged housing in boring conditions, a limited amount of immunosuppression, or long-term minor infection with a pathogen would be called stresses only if they reduced fitness or appeared likely to do so. This definition of stress requires that there be an effect on fitness as well as an overtaxing of control systems (Fig. 3.6, level Ill). The definition also includes reference to circumstances in which the environmental effect appears likely to reduce fitness, though there may be no immediate measure of fitness. In practice there will be many situations in which it is not possible to be certain that the fitness of the individual will be reduced, but in which it is possible to deduce, using

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knowledge of the biology of the species, that this is likely. Such circumstances include substantial immunosuppression when disease challenge is likely, injury, behaviour abnormality, and physiological overload that increases the chances that food acquisition or the ability to avoid dangerous aggression will be reduced. A distinction is therefore made between minor disturbances to an animal’s equilibrium, which may result in the use of energy to correct them but have no consequence for fitness, and those disturbances that do, or are likely to, reduce fitness. The differentiation between energy usage that does not reduce fitness and real fitness reduction which may, but need not, involve energy usage is important here and in other circumstances where biological efficiency and the way in which natural selection acts are being considered. The term ‘stress’ is also relevant to plants or micro-organisms. In contrast to ‘welfare’, which is restricted to animals, this definition of stress could be used for any living organism. The state of the animal when it is stressed has often been called distress, although stress and distress may well have been the same word originally. For the sake of clarity it is best to define distress less rigorously and to use it for a description of the state of individuals that are stressed or affected in similar ways by their environment. Reference is often made to pain and distress in order to include all aspects of the state of the individual.

4.2

Welfare

To “fare” means to go through life, for example in Julius Caesar, Shakespeare’s character says: “Farewell my dearest sister, fare thee well” (Shakespeare 1599). Originally welfare meant the state or condition of how well one was doing, of one’s happiness, good fortune or prosperity. In Shakespeare’s Henry VI, (Shakespeare 1591) Queen Margaret says: “Take heed, my lord; the welfare of us all hangs on the cutting short of that fraudful man”. Similarly, Locke (1690) says: “Thus the being and welfare of a man’s children or friends, producing constant delight in him, he is said constantly to love them”. However, in the twentieth century the term welfare was often applied to the problems of poor people and even to refer to payments to poor people. The modern scientific meaning has broadened and, in doing so it has returned to the original meaning. A significant broadening is to refer to the welfare of all people and to species other than humans. Welfare has in recent years been closely linked to suffering and to the idea that many non-human animals, as well as under-privileged people, can suffer. Bentham (1789) stated that the key question about animals was not can they reason but do they suffer? Those people who have lived with or looked closely at companion or farm animals have usually assumed that they could suffer and also that they could reason to some extent. As Duncan (2006) has said, up to the nineteenth century, this view was very widespread but later there was some reluctance to hold the view because of anthropocentrism (Chap. 1) and difficulty to measure the suffering. People who considered that animals were suffering were often looking at animals with which

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they were familiar, were making observations and deducing from these observations, i.e. they were using a scientific approach. In the nineteenth century and the first half of the twentieth, knowledge about biological functioning increased greatly. By the end of this time, scientific disciplines such as ethology and neuroscience started to become accepted within the scientific community. As a result, it became clear that there were methods for the evaluation of suffering, feelings such as pain, anxiety and pleasure, and other methods of coping with the world. The various physiological and psychological measures of stress were being developed. At the same time, the idea that in most circumstances it was unacceptable to cause pain and other suffering to people and to other animals became more widespread and enshrined in legislation in the majority of countries. In the 1960s, the emphasis of discussions was on animal protection, a human activity, rather than on animal welfare. Ruth Harrison’s book “Animal Machines” (1964) pointed out that those involved in the animal production industry were often treating animals like inanimate machines rather than living individuals. As a consequence of this book, in 1965 the British government set up the Brambell Committee, a committee chaired by Professor F. Rogers Brambell, to report on the matter. The book and the report referred extensively to animal welfare. One of its members was W. H. Thorpe, an ethologist in Cambridge University. Thorpe emphasised that an understanding of the biology of the animals is important and explained that animals have needs with a biological basis, including some needs to show particular behaviours, and that animals would have problems if the needs were frustrated (Thorpe 1965). In the 1970s and early 1980s, the term animal welfare was used but not defined and not considered scientific by most scientists. Animal welfare was often confused with animal rights and such confusion still occurs. Following some generally accepted views of the functioning of animals and also the writings of Lorca, Hughes (1982) proposed that the term animal welfare meant that the animal was in harmony with nature, or with its environment. This is a biologically relevant statement and a precursor of later views but it is not a usable definition. Being in harmony is a single state so it does not allow the use of scientific measures of welfare. The key question is how much the individual is in harmony. The term welfare was being used more and more in science, in laws and in discussion about the effects of the treatment of laboratory, farm and companion animals. Hence there was a clear need for a definition of animal welfare for scientific study, for legislation and for practical use. This definition would have to refer to a characteristic of an individual that is measurable. The measurement should be separate from any judgement about what is morally acceptable. Welfare, as a measurable characteristic of animals, should vary over a range rather than being something that exists or does not exist in order to indicate how well an individual ‘fares’ or travels through life. Broom (1986) used this definition of welfare: the welfare of an individual is its state as regards its attempts to cope with its environment. This was further explained in a series of publications (Broom 1988a, 1991a, b, Broom and Johnson 1993). Equivalent words in other languages include bien-être, bienestar, bem estar, benessere, Wohlergehen, welzijn, velfærd, and dobrostan. The ‘state as regards attempts to cope’ refers to both how much has to be done in order to cope with the

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environment and the extent to which coping attempts are succeeding. Attempts to cope include the functioning of body repair systems, immunological defences, emergency physiological responses and a variety of behavioural responses and other systems that are coordinated by the brain. Feelings, such as pain, fear and the various forms of pleasure, are often part of a coping strategy and feelings are a key part of welfare. The system may operate successfully so that coping is achieved or may be unsuccessful in that the individual is harmed. One or more coping strategies may be used to attempt to cope with a particular challenge so a wide range of measures of welfare may be needed to assess welfare. Coping with pathology is necessary if welfare is to be good so health is an important part of welfare (Broom 2006). A key point of agreement amongst animal welfare scientists has been that animal welfare is measurable and hence is a scientific concept (Fraser 2008). Another unanimous view of animal welfare scientists is that welfare involves mental aspects. Current research on welfare involves measurements of brain function and of its consequences for behaviour and physiology. Many animal welfare indicators give information about positive and negative feelings and a range of indicators evaluate other coping mechanisms, including those that affect health. The O.I.E. (World Organization for Animal Health, OIE 2011) followed the Broom definition when writing about what is meant by animal welfare although some of the explanatory wording in the 2011 document was not precise. Discussion amongst animal welfare scientists about the term welfare has centred on the extent to which feelings contribute to welfare. Duncan argued that welfare is wholly about feelings (Duncan and Petherick 1991; Duncan 1993). Some contrasted this with Broom’s definition which was referred to by some by some as a functional definition that did not include feelings. However, all of Broom’s papers and books discussing the welfare definition referred to feelings as a part of welfare. Broom (1998) explained how feelings are functional and have evolved. The position of Dawkins (1980, 1990) was that the feelings of the individual are the central issue in welfare but other aspects such as the health of that individual are also important. Since feelings are a part of the functioning of animals, welfare should not be represented by a diagram of overlapping circles in which feelings are in a circle that does not fully overlap with a circle labelled function (Appleby and Hughes 1997). Since legislation has generally been written in such a way as to prevent human cruelty, and to prevent suffering in animals that humans use, there has been much emphasis on poor welfare. When coping is successful and problems are absent or minor, welfare is good. Good welfare is generally associated with feelings of pleasure or contentment. In recent years, more efforts have been made to promote good welfare in animals. This is linked with improving health and is taking account of the One Health and One Welfare concepts discussed in Chap. 1. There are various consequences of this concept of animal welfare and there remain some areas of confusion amongst the public about what animal welfare is (Broom 2014) as shown in Table 4.1. Some of these points are further discussed in Sects. 4.4 to 4.10.

1. Welfare is a characteristic of an individual human or other animal. In some American usage, welfare can refer to a service or other resource given to an individual, but that is entirely different from this scientific usage. Human action may improve welfare, but an action or resource provided should not be referred to as welfare. Some people confuse the concepts of protection of animals and animal welfare. However, the first is a human action and the second is a characteristic of an animal 2. Welfare can vary between very poor and very good. In order to use the concept of welfare in a scientific way it is desirable to specify the level of welfare and not simply to reserve the word to indicate that the individual has, or does not have, problems. We should not speak of preserving or ensuring welfare, but of improving welfare or ensuring that welfare is good. We must be able to talk about an animal’s welfare being poor when there is evidence that it is having difficulty in coping or is unable to cope. The continuum of welfare is exemplified in Figs. 4.3, 4.4, 4.5, 4.6 and 4.7 3. An animal’s welfare is poor when it is having difficulty in coping or is failing to cope. Failure to cope implies fitness reduction and hence stress. However, there are many circumstances in which welfare is poor without there being any effect on biological fitness. This occurs if, for example, animals are in pain, they feel fear, or they have difficulty controlling their interactions with their environment because of (a) frustration, (b) absence of some important stimulus, (c) insufficient stimulation, (d) overstimulation or (e) too much unpredictability (Chap. 3). If two situations are compared, and individuals in one situation are in slight pain but those in the other situation are in severe pain, then welfare is poorer in the second situation even if the pain or its cause does not result in any long-term consequences, such as a reduction in fitness. Pain, or other effects listed above, may not affect growth, reproduction, pathology or life expectancy, but do mean poor welfare 4. Animals may use a variety of methods when trying to cope, and there are various consequences of failure to cope. Any one of a variety of measurements can therefore indicate that welfare is poor, and the fact that one measure, such as growth, is normal does not mean that welfare is good (see Chaps. 5 and 6) 5. Pain and suffering are important aspects of poor welfare. Although individuals may be able to tolerate some pain and suffering, perhaps in order that some important objective be attained, all pain and suffering involves increased difficulty in coping with the environment and hence poorer welfare 6. The concept of health as a key part of welfare, rather than a separate topic is misunderstood by many, including medical and veterinary specialists who may not be familiar with the meaning of welfare 7. Welfare is affected by what freedoms are given to individuals and by the needs of individuals (Chap. 2) but it is not necessary to refer to these concepts when specifying welfare 8. Welfare can be measured in a scientific way that is independent of moral considerations. Welfare measurements should be based on the biology of the species and, in particular, on what is known of the methods used by animals to try to cope with difficulties and of signs that coping attempts are failing. The measurement and its interpretation should be objective. Once the welfare has been described, moral decisions can be taken 9. The ethical issues about whether or not animals should be killed for human benefit and whether or not poor welfare of animals is acceptable are different 10. The evolution of animals in their natural environment has led to them having certain needs that must be met for welfare to be good, and good conditions for animals will allow them to function in a natural way, i.e. a normal biological way. However naturalness is not a component of the definition of welfare 11. The dignity of an individual is a human concept that may be applied to non-human animals but there is no evidence that other species have such a concept. It may be used as an argument for treating animals well but it is not a part of welfare 12. The integrity of an animal, in the sense of its wholeness, has some biological basis and is sometimes used to criticise removal of, or change in, any part of an animal’s body including its limbs, appendages, organs and genotype

Table 4.1 Consequences of the concept of animal welfare and some areas of confusion about it

84 4 Stress and Welfare: History and Usage of Concepts

4.2 Welfare Fig. 4.3 The significance for welfare of measurements of adrenal cortex activity

Fig. 4.4 The significance for welfare of measurements of stereotypies

85

86 Fig. 4.5 The significance for welfare of measurements of growth, reproduction and life expectancy

Fig. 4.6 The significance for welfare of measurements of injury in relation to the extent to which the individual might be suffering

4 Stress and Welfare: History and Usage of Concepts

4.3 Welfare Assessment

87

Fig. 4.7 The significance for welfare of measurements of immune system function, disease condition and, hence, possible suffering

Animal welfare can be affected by a wide range of factors. Whilst the effects of disease, injury and starvation are negative, there can be beneficial stimulation and success in actions will have positive consequences. Social interactions and housing conditions can have positive or negative effects. Fraser et al. (2013) list ten factors to consider in order to promote good welfare in animals in production systems. Implicit in their paper, and required in order to do as stated in the list, is the necessity to consider scientific information about the needs of animals of the species and background under consideration so it has been put at (1) in Table 4.2. Also, the word “natural” has been changed to “adaptive” in (4) and “euthanasia” has been changed to “humane killing” in (8).

4.3

Welfare Assessment

In order that the definition of welfare is more easily understood and can be related to other concepts it is useful to consider examples of situations in which welfare is measured. Table 4.3 lists some measures of welfare. These measures are described in detail in Chaps. 5, 6 and 7. An animal encountering a varied environment but with no real problems will show only occasional bouts of adrenal cortex activity, and its welfare can be considered to be good (Fig. 4.3). If that same individual was frequently frustrated or frightened, an appropriate indicator of this situation might be increased

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Table 4.2 Factors to consider in order to promote good welfare in animals in production systems (1) Scientific information about the needs of animals of the species and background under consideration; (2) How genetic selection affects animal health, behaviour and temperament; (3) How the environment influences injuries and the transmission of diseases and parasites; (4) How the environment affects resting, movement and the performance of adaptive behaviour; (5) The management of groups to minimise conflict and allow positive social contact; (6) The effects of air quality, temperature and humidity on animal health and comfort; (7) Ensuring access to feed and water suited to the animals’ needs and adaptations; (8) Prevention and control of disease and parasites, with humane killing if the welfare is very poor and control or recovery is unlikely; (9) Prevention and management of pain; (10) Creation of positive human-animal relationships; and (11) Ensuring adequate skill and knowledge among animal handlers Modified after Broom (2014) and Fraser et al. (2013)

Table 4.3 Measures of welfare include the following • • • • • • • • • • • • • • • •

Physiological indicators of pleasure Behavioural indicators of pleasure Extent to which strongly preferred behaviours can be shown Variety of normal behaviours shown or suppressed Extent to which normal physiological processes and anatomical development are possible Extent of behavioural aversion shown Physiological attempts to cope Immunosuppression Disease prevalence Behavioural attempts to cope Behaviour pathology Brain changes Body damage prevalence Reduced ability to grow or breed Cellular changes indicating system failure and aging Reduced life expectancy

After Broom and Fraser (2015)

glucocorticoid production and synthetic enzyme activity in the adrenal cortex. If high levels of adrenal cortex activity occurred very frequently or over a long period, a consequence may be widespread pathological changes. In this case the animal’s welfare is even poorer. Sometimes the adverse effects may be so severe that adrenal function itself is impaired. Other measures also allow the position of an individual on the welfare scale to be identified. One of the widely used measures of abnormal behaviour is stereotypy.

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The welfare of individuals that show stereotypies for varying amounts of time are indicated in Fig. 4.4. Stereotypies are repeated relatively invariant sequences of movements which have no obvious function. Stereotypies such as bar biting or sham chewing in sows, tongue rolling in calves, crib biting in horses, or route tracing in zoo animals are often exhibited in conditions where an animal is frustrated or otherwise lacking in control over the world that impinges on it. It is possible that a stereotypy that has been carried out for a long time relates more to an earlier state of an animal than to the present condition (Mason 1991a, b). Nonetheless, high levels of stereotypies, self-mutilation or other abnormal behaviour do show that an individual has difficulty coping with the conditions that exist at the time of observation, so the welfare of an animal that shows such behaviour is clearly poorer than that of an individual that does not. Even if the animal’s problems were greater in the past and the abnormal behaviour has become a habit, the behaviour will gradually, or rapidly, disappear if there is no current problem for the animal. A person who has been in solitary confinement in a prison camp may show some abnormalities of behaviour whilst recovering from that experience, and these indicate that the welfare of that person is poorer than that of a normal person. The more of life that is spent showing abnormal behaviour, the worse the welfare is. A further behavioural response to conditions that pose problems for animals is to become inactive and unresponsive (Broom 1987). Such unresponsiveness may be associated with increased influence of endogenous opioids, because it is linked with μ-receptor density in the cerebral cortex (Zanella et al. 1991, 1992). This raises the possibility of assessing welfare by measuring endogenous opioid levels. This has to be done carefully taking account of all the roles of opioids. Production measurements such as growth rate and reproductive output are also welfare indicators. For a given genotype, if growth or reproduction is impaired then welfare is poorer (Fig. 4.5) and again a scale of welfare based on measurements can be drawn up. Other measures of welfare are discussed in the next two Sections and all measures are discussed in greater detail in Chaps. 5–7. Pleasant and unpleasant feelings are a key part of welfare and are experienced by an individual as it attempts to cope with its environment. Dawkins (1990) stated that ‘suffering occurs when unpleasant subjective feelings are acute or continue for a long time because the animal is unable to carry out the actions that would normally reduce risks to life and reproduction in those circumstances’. Suffering is one or more bad feelings continuing for more than a few seconds or minutes. Dawkins’ description of suffering, stated above, refers to feelings which are a consequence of inability ‘to carry out actions that would normally reduce risks to life and reproduction’. Most people would include all but the milder, briefer kinds of pain and many of the consequences of disease within the term suffering. A definition of suffering should be somewhat broader than Dawkins’ description. Not all pain and relevant disease effects are associated with the inability described, and suffering resulting from pain and disease does not necessarily result in risks to life or reproduction. Dawkins emphasizes important situations in which suffering occurs, but a better way

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of phrasing her view might be: suffering is an unpleasant subjective feeling which is prolonged or severe. Suffering is one of the most important aspects of poor welfare. We should all be concerned to identify suffering and to try to prevent it. If there is suffering, then the welfare will always be poor. However, welfare should not be defined solely in terms of subjective experiences, because situations arise in which the welfare of an individual can be affected without suffering occurring (Broom 1991b). For example, if an individual is injured, say by a bone breakage, a cut in the skin or an ulcer in the stomach, the welfare of that individual is poorer than that of an individual with no injury, even if there was no pain or other suffering from the injury, perhaps because of a pain system malfunction (Fig. 4.6). If the individual with the injury is asleep or anaesthetized, and hence not suffering, there is still an effect on welfare. If there is suffering
as well as an injury, then the welfare is poorer still. Few people would consider that a severe injury has no effect on welfare during sleep and that the welfare suddenly becomes poor on awakening because of consequent perception. It is difficult to see how the term welfare is to be used if there is extreme adherence to the concept advanced by Duncan and Petherick (1991) that only feelings count when welfare is being assessed. For example, should we consider the welfare of a person who is close to dying to be wholly good if, for a brief period, they experience a temporary good feeling? Levels of immunosuppression also correlate with levels of welfare, as shown in Fig. 4.7, (Broom and Fraser 2015). Levels may be mediated via hyperactivity of the adrenal cortex, but need not be. Changes may be preceded or accompanied by behavioural indicators of poor welfare. When welfare is good the immune system works effectively to counteract challenge by pathogens. There are sophisticated interrelations between the immune system and the brain. If there is immunosuppression, however, the animal will have to do more to cope with environmental challenges and will also show more pre-pathological effects that have the potential to reduce fitness. For both of these reasons the welfare is poorer than in an unaffected individual. It may be that the immunosuppressed individual does not suffer because it is not challenged by pathogens, but there is still an effect on its welfare, in that it is more vulnerable. If successful pathological attack occurs, with consequent morbidity and suffering, then the welfare is poorer still. Suffering is an important concept when considering the effects of conditions and procedures on animals, but it is not necessary to try to equate it with poor welfare. Some behaviour which is shown in response to adversity is clearly involved with attempts to cope with, for example, low temperature or lack of water. Other behaviour indicates how aversive a particular situation or stimulus is, and the degree of aversion can sometimes be assessed. However, there is also behaviour that appears to be unadaptive and can be considered pathological, for example most forms of self-mutilation. This distinction between behaviour pathology and adaptive attempts to cope is often difficult to make. Another measurement of behaviour listed in Table 4.3 as an indicator of poor welfare is suppression of normal behaviour. This measure assumes a knowledge of

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normal behaviour in conditions in which the individual can allocate its time and energy as it chooses. If the subject is a wild animal, it may be difficult to obtain information about normal behaviour because of the disturbing effect of the observer. The information can sometimes be obtained from studies of captive animals. If conditions are such that normal actions such as grooming behaviour, exercise or social interaction are not possible, then this will immediately be apparent when comparing animals in the conditions investigated with those in good conditions. Failure to show normal anatomical development and physiological functioning may also be seen in such comparisons. Considerable knowledge of the species concerned is necessary in order to be sure that the absence of a particular behaviour or physiological processes is not just a consequence of, for example, lack of appropriate hormonal state. Such evidence of poor welfare is commonly reinforced by the presence of other indicators of poor welfare in the animals. Good welfare is generally associated with a wide range of normal behaviour, especially behaviour that can be demonstrated to be strongly preferred (see Chap. 7). If all preferred behaviours can be shown, then welfare will be better than if some are prevented. An ideal for animal welfare research is to recognize pleasure in individuals by means of physiological or behavioural measurements. One physiological measure is oxytocin and for most species, behaviours associated with pleasure are known. There can be misinterpretation of behaviour such as tail wagging by dogs, which is often thought to indicate pleasure but may indicate submission. Play behaviour usually indicates good welfare. The development of the scientific assessment of welfare has occurred rapidly in non-human animals and much of the methodology is also relevant to assessing human welfare (see Dahlem Conference papers, Broom 2001) but is not often used. Human welfare is often assessed by psychiatrists using scales based on human verbal or written response to questions. However, all such human reporting is subject to deliberate or unintended lying so, in some cases, more objective methods like those developed for non-human species, are better.

4.4

Welfare in Relation to Stress

When considering what animals do when they encounter problems that affect their normal functioning, it is important to distinguish those effects that reduce fitness or are likely to do so, and hence involve stress, from those that do not. There are many occasions when individuals find coping difficult, but succeed without long-term adverse consequences by, for example, using a brief adrenal response or a behavioural change of some kind. A minor injury or a period of illness might have no effect on the fitness of an individual. In each of these situations and on all occasions in which there is any kind of suffering, there is an effect on welfare even if there is no effect on individual fitness. Hence, stress invariably implies poor welfare, but welfare can be poor without stress, and welfare will often be positive.

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Table 4.4 Gradations of stimulus and response in relation to usage of the terms adaptation, welfare and stress. A small reduction in fitness may have less of an effect on welfare than very considerable and prolonged coping difficulties that do not affect fitness Level Environmental stimulus Response by individual IV Extreme Instant death III Noxious Coping attempts unsuccessful, fitness impaired II Aversive Coping with difficulty I

Innocuous, with or without sensation

Regulation carried out easily

Description Lethal Stressed

Welfare Very poor until death Poor or very poor

Adaptation, not stressed Adaptation, not stressed

Poor or very poor Unaffected

The ideas developed in Chap. 3 (Figs. 3.4–3.7) are therefore developed further to include the terms welfare, stress and adaptation in Table 4.4.

4.5

Welfare in Relation to Naturalness

Fraser (1999) pointed out that when members of the public talk about animal welfare, their ideas often include the functioning of the animals, the feelings of the animals and the naturalness of the environment. The feelings referred to by Fraser and others fit comfortably into Broom’s definition of welfare as they are important components of coping mechanisms and of biological functioning. Rollin (1989) advocated that “animals should be able to lead reasonably natural lives”. This view has been reiterated by Rollin (1995), Fraser et al. (1997) and Fraser (2008) and, in all four publications, the authors refer to the importance of understanding animal needs. These authors did not say that naturalness contributes to a definition of welfare or should be part of welfare assessment. However, some other authors have described naturalness as a component of welfare and Appleby and Hughes’ (1997) diagram of what welfare is has naturalness as a circle partly overlapping with function and feelings. This is incorrect as naturalness is not part of the meaning of welfare. The state of an individual trying to cope with its environment does necessarily depend upon its biological functioning, or put another way, upon its nature. Natural conditions have affected the needs of the animal and the evolution of coping mechanisms in the species. Gygax and Hillman (2019) agree with this approach saying “Natural behaviour in this sense involves reaching adequate goal states for all persistent or recurring wants that arise in a given environment.” The environment provided should fulfill the needs of the animal but it does not have to be the same as the environment in the wild. Indeed, conditions in the wild may result in starvation, disease and predation, with consequent very poor welfare (Yeates 2018). The concept and definition of welfare does not include naturalness.

4.8 Welfare and a Life Worth Living

4.6

93

Welfare and Well-Being

Animal welfare scientists use the term welfare to refer to the positive and the negative. Welfare can be very good or very poor. During much of the usage of the term well-being, it is exactly synonymous with welfare but a higher proportion of people think just of the positive when they use it. Since welfare has been defined for many years and is the term used by most scientists and legislators, it is now considered to be a more precise term than well-being. In the U.S.A. there was initial reluctance to use welfare as a scientific term because many people thought of welfare as indicating hand-outs to the poor. More and more American scientists now use welfare, rather than well-being, and its use by the American Veterinary Medical Association now indicates international uniformity in the use of welfare.

4.7

Welfare and Quality of Life

The term quality of life has often been used used to refer to people, or companion animals, who are ill or recovering from illness. In judging quality of life, the impact on the functioning of the individual, including physiological and behavioural responses and especially indicators of pain or other suffering, should be evaluated. The measures of welfare include all of the measures of quality of life (Chap. 8). Both quality of life and welfare can be positive or negative, good or poor. There is some difference in the use of the terms as it would not be normal to talk about impaired quality of life, for example because of a thorn in the finger, over a very short time scale such as a few hours or days. Welfare, on the other hand, can refer to short-term situations. Quality of life means welfare during a period of more than a few days (Broom 2007). Hence quality of life can be assessed using the wide range of indicators that are available for assessing welfare (Chap. 6).

4.8

Welfare and a Life Worth Living

Ethical judgements are required to judge whether or not a life is worth living and the judgement would have to be made by a human. Even though the decision might be based on scientific information, the concept of a life worth living is ethical rather than scientific. Worth depends here on a concept of the value of another individual. If the individual under consideration is non-human, it is a human evaluation rather than an evaluation by the subject. This is very different from the scientific concept of welfare and will vary from person to person. Investigation of welfare refers to a measureable quality of the animal and this is assessed in an objective way, trying to take account of what that animal needs and its current state in relation to those needs. As explained by Broom (2014), a decision about whether or not life is worth living

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would not be made in the same way by the person judging and by the animal itself. “A person might judge that a pet animal is in pain and that its life is not worth living. However, animals in pain still strive to survive and carry out assessments of risks to themselves. Would the animal choose to live or die? There are few reports of suicide in non-humans and most of these could have an alternative explanation. An injured prey animal, like a goat on a mountain ledge, when it is approached by a leopard will only jump off the ledge if the risk of so doing is less than that posed by the approaching predator. Suicide is a failure of risk and benefit assessment rather than a deliberate action, however great the pain caused by the injury.” The idea of a life worth living is of some use in order to emphasise that the whole life should be considered. It has been used to constructively criticise some housing systems or procedures on animals. However, when systems or procedures are evaluated there should be objective measurement of welfare taking account of the whole life of the animal, rather than subjective assessment of the worth of that life.

4.9

Welfare in Other Languages

The word welfare is used in English versions of modern European legislation. Most languages have a word to translate welfare, the equivalent to welfare in comparable legislation including: bien-être in French, bienestar in Spanish, bem-estar in Portuguese, Wohlbefinden or Wohlergehen in German, welzijn in Dutch, welfaerd in Danish and dobrostan in Polish. The common usages of some of these terms can make it difficult to use them to refer to poor, as well as good, welfare, though this is not a problem with Wohlbefinden or welzijn. However, it does seem surprising in colloquial usage to use a word meaning poor or bad to qualify bien-être, bienestar or welfaerd. It is generally desirable for a word in each language to be defined in a way that makes it equivalent to ‘welfare’ for scientific and legal use. Hence, as is necessary for all words used in a scientific or legal way, there should be international consistency of terminology, and the word for welfare in each language should be one which can be qualified with words for ‘good’ and ‘poor’. In some languages, the English word welfare is used for clarity.

4.10

Welfare and Sentience

The concept of sentience is introduced in Sect. 2.3 and discussed by Broom (2014). We can consider the welfare of every kind of living animal because each makes attempts to cope with its environment. Relatively simple animals, such as protozoans or flatworms, respond to adverse conditions such as too high or too low a temperature or contact with a detectable toxic or damaging substance. Behavioural avoidance and physiological change are the likely responses. Another way of coping with the environment is to approach or stay in areas where food or a potential mate are

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identified. These are positive responses to the environmental variable. When animals mount immunological responses to pathogens or healing responses when tissue is damaged, they are attempting to cope with their environments. All of these examples of coping attempts apply to humans and all other animals. If the animal is sentient it has the capability to use more elaborate and complex coping responses. An animal that can have one of the higher levels of awareness, and can have positive and negative feelings, can use these mechanisms in order to more closely control their daily lives. Not all scientists talk about the welfare of both sentient and non-sentient animals. Kirkwood (2006) argues that welfare depends upon having feelings and hence is a characteristic of only sentient beings. Whilst we can talk about and evaluate the welfare of any animal, people are usually more concerned about the more complex animals and may wish to protect sentient animals to a greater degree than they wish to protect animals that are not sentient.

References Appleby MC, Hughes BO (1997) Animal welfare. CAB Int, Wallingford Bentham J (1789) An introduction to the principles of morals and legislation. T. Payne, London Broom DM (1983) The stress concept and ways of assessing the effects of stress in farm animals. Appl Anim Ethol 11(1):79 Broom DM (1985) Stress, welfare and the state of equilibrium. In: Wegner RM (ed) Proceedings of the 2nd European symposium on poultry welfare. World Poultry Science Association, Celle, pp 72–81 Broom DM (1986) Indicators of poor welfare. Br Vet J 142:524–526 Broom DM (1987) Applications of neurobiological studies to farm animal welfare. In: Wiepkema PR, van Adrichem PWM (eds) Biology of stress in farm animals: an integrated approach. Current topics in veterinary medicine and animal science. Martinus Nijhoff, Dordrecht, pp 101–110 Broom DM (1988a) The scientific assessment of animal welfare. Appl Anim Behav Sci 20:5–19 Broom DM (1988b) Les concepts de stress et de bien-être. Receuils de Médecin Vétérinaire 164:715–722 Broom DM (1991a) Animal welfare: concepts and measurement. J Anim Sci 69:4167–4175 Broom DM (1991b) Assessing welfare and suffering. Behav Process 25:117–123 Broom DM (1998) Welfare, stress and the evolution of feelings. Adv Study Behav 27:371–403 Broom DM (ed) (2001) Coping with challenge: welfare in animals including humans. Dahlem University Press, Berlin, p 364 Broom DM (2006) Behaviour and welfare in relation to pathology. Appl Anim Behav Sci 97:71–83 Broom DM (2007) Quality of life means welfare: how is it related to other concepts and assessed? Anim Welf 16(Suppl):45–53 Broom DM (2014) Sentience and animal welfare. CABI, Wallingford, p 200 Broom DM (2017) Cortisol: often not the best indicator of stress and poor welfare. Physiol News 107:30–32 Broom DM, Fraser AF (2015) Domestic animal behaviour and welfare, 5th edn. CABI, Wallingford, p 472 Broom DM, Johnson KG (1993) Stress and animal welfare. Chapman and Hall, London, p 211 Dawkins MS (1980) Animal suffering: the science of animal welfare. Chapman & Hall, London

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Dawkins MS (1990) From an animals point of view: motivation, fitness, and animal welfare. Behav Brain Sci 13:1–61 Duncan IJH (1993) Welfare is to do with what animals feel. J Agric Environ Ethics 6(Suppl 2):8–14 Duncan IJH (2006) The changing concept of animal sentience. Appl Anim Behav Sci 100:11–19 Duncan IJH, Petherick JC (1991) The implications of cognitive processes for animal welfare. J Anim Sci 69:5017–5022 Fraser D (1999) Animal ethics and animal welfare science: bridging the two cultures. Appl Anim Behav Sci 65:171–189 Fraser D (2008) Understanding animal welfare: the science in its cultural context. Wiley Blackwell, Chichester Fraser D, Weary DM, Pajor EA, Milligan BN (1997) The scientific conception of animal welfare that reflects ethical concerns. Anim Welf 6:187–205 Fraser D, Duncan IJH, Edwards SA, Grandin T, Gregory NG, Guyonnet V, Hemsworth PH, Huertas SM, Huzzey JM, Mellor DJ, Mench JA, Spinka M, Whay HR (2013) General principles for the welfare of animals in production systems: the underlying science and its application. Vet J 198:19–27 Freeman BM (1987) The stress syndrome. World Poult Sci J 43:15–19 Gygax L, Hillman E (2019) “Naturalness” and its relation to animal welfare from an ethological perspective. Agriculture 8(9):136. https://doi.org/10.3390/agriculture8090136 Harrison R (1964) Animal machines. In: London: Vincent Stuart, reprinted with commentaries 2013. CABI, Wallingford Hobfoll SE (1989) Conservation of resources: a new attempt at conceptualizing stress. Am Psychol 44:513–524 Hooke R (1678) De Potentia Restitutiva. London Hughes BO (1982) The historical and ethical background of animal welfare. In: How well do our animals fare? Proc. 15th Annual Conference of the Reading University Agricultural Club, 1981, ed. J. Uglow, pp 1–9 Kirkwood JK (2006) The distribution of the capacity for sentience in the animal kingdom. In: Turner J, D’Silva J (eds) Animals, ethics and trade: the challenge of animal sentience. Compassion in World Farming Trust, Petersfield, pp 12–26 Lazarus RS (1993) From psycholoigical stress to the emotions: a history of changing outlooks. Annu Rev Psychol 44:1–22 Lazarus RS, Folkman S (1984) Stress, appraisal and coping. Springer, New York Locke J (1690) An essay concerning human understanding Mason JW (1968) A review of psychoendocrine research on the pituitary adrenal cortical system. Psychosom Med 30:576–607 Mason JW (1971) A re-evaluation of the concept of ‘non-specificity’ in stress theory. J Psychiatr Res 8:323–333 Mason JW (1975a) Psychoendocrine mechanisms in a general perspective of endocrine integration. In: Levi L (ed) Emotions – their parameters and measurement. Raven Press, New York, pp 143–182 Mason JW (1975b) Emotion as reflected in patterns of endocrine integration. In: Levi L (ed) Emotions – their parameters and measurement. Raven Press, New York, pp 183–191 Mason GJ (1991a) Stereotypies: a critical review. Anim Behav 41:1015–1037 Mason GJ (1991b) Stereotypies and suffering. Behav Process 25:103–115 Mason JW, Brady JV, Tolliver GA (1968a) Plasma and urinary 17-hydroxycorticosteroid responses to 72-hour avoidance sessions in the monkey. Psychosom Med 30:608–630 Mason JW, Jones JA, Ricketts PT (1968b) Urinary aldosterone and urine volume responses to 72-hour avoidance sessions in the monkey. Psychosom Med 30:733–745 Mason JW, Kenion CC, Collins DR (1968c) Urinary testosterone response to 72-hour avoidance sessions in the monkey. Psychosom Med 30:721–732 Mason JW, Taylor ED, Brady JV, Tolliver GA (1968d) Urinary estrone, estradiol, and estriol responses to 72-hour avoidance sessions in the monkey. Psychosom Med 30:696–709

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Mason JW, Tolson WW, Robinson JA et al (1968e) Urinary androsterone, etiocholanolone, and dehydroepiandrosterone responses to 72-hour avoidance sessions in the monkey. Psychosom Med 30:710–720 Mason JW, Wherry FE, Brady JV (1968f) Plasma insulin response to 72 hour avoidance sessions in the monkey. Psychosom Med 30:746–759 McGrath JE (1970) Social and psychological factors in stress. Holt, Rinehart and Winston, New York Moberg GP (1985) Biological response to stress: key to assessment of animal well-being? In: Moberg GP (ed) Animal stress. American Physiological Society, Bethesda, MD, pp 27–49 Moberg GP (1987) Problems in defining stress and distress in animals. J Am Vet Med Assoc 191:1207–1211 OIE (World Organization for Animal Health) (2011) Terrestrial animal health code. OIE, Paris Pilch W, Szyguła Z, Torii M (2007) Effect of the sauna-induced thermal stimuli of various intensity on the thermal and hormonal metabolism in women. Biol Sport 24:357–373 Pilch W, Pokora I, Szyguła Z, Pałka T, Pilch P, Cisoń T, Malik L, Wiecha S (2013) Effect of a single finnish sauna session on white blood cell profile and cortisol levels in athletes and non-athletes. J Hum Kinet 39:127–135. https://doi.org/10.2478/hukin-2013-0075 Ralph CR, Tilbrook AJ (2016) The usefulness of measuring glucocorticoids for assessing animal welfare. J Anim Sci 94:457–470. https://doi.org/10.2527/jas2015-9645 Rollin BE (1989) The unheeded cry: animal consciousness, animal pain and science. Oxford University Press, Oxford Rollin BE (1995) Farm animal welfare: social, bioethical and research issues. Iowa State University Press, Ames, IA Selye H (1973) The evolution of the stress concept. Am Sci 61:692–699 Selye H (1976) The stress of life, 2nd edn. McGraw-Hill Book Co, New York Selye H (1993) History of the stress concept. In: Goldberger L, Breznitz S (eds) Handbook of stress: theoretical and clinical aspects. Free Press, New York, pp 7–17 Shakespeare W (1591) Henry VI Shakespeare W (1599) Julius Caesar Sibly R, Calow P (1983) An integrated approach to life-cycle evolution using selective landscapes. J Theor Biol 102:527–547 Thornton SN, Parrott RF, Delaney CE (1987) Differential responses of plasma oxytocin and vasopressin to dehydration in non-stressed sheep. Acta Endocrinol 114:519–523 Thorpe WH (1965) The assessment of pain and distress in animals. Appendix III in Report of the technical committee to enquire into the welfare of animals kept under intensive husbandry conditions, F.W.R. Brambell (chairman). London: H.M.S.O. Yeates J (2018) Naturalness and animal welfare. Animals 8:53–70. https://doi.org/10.3390/ ani8040053 Zanella AJ, Broom DM, Hunter JC (1991) Changes in opioid receptors of sows in relation to housing, inactivity and stereotypies. In: Appleby MC, Horrell RI, Petherick JC, Rutter SM (eds) Applied animal behaviour: past, present and future. Universities Federation for Animal Welfare, Potters Bar, pp 140–141 Zanella AJ, Broom DM, Hunter JC (1992) Changes in opioid receptors in sows in relation to housing, inactivity and stereotypies. In: Animal welfare: proceedings of the XXIV world veterinary congress, Rio de Janeiro 1991. World Veterinary Association, London, pp 159–166

Chapter 5

Assessing Welfare: Short-Term Responses

Abstract This chapter provides an account of the responses of animals to shortterm disturbances. The measures of welfare that are used when an individual encounters problems over a timescale of minutes or hours are somewhat different from those used when problems last for days, weeks or years. People may experience and express delight or dismay at experiences lasting for only a few seconds or minutes and these may be important in life or relatively trivial. The situation is the same for other species. Animals respond to handling, transport or painful treatment and their responses can be measured. Some measures are of behaviour while many are of physiology. All are discussed in detail in this chapter. The concept of the magnitude of good or poor welfare, considering both intensity and duration of effect on the individual, is introduced. Keywords Short-term problems · Handling · Transport · Pain · Welfare · Stress

Since welfare refers to the state of an animal, measurements of that state are used in the assessment of welfare. The wide range of ways in which animals attempt to cope with their environment results in there being many indicators of good or poor welfare. Many coping attempts involve, or are associated with, positive or negative feelings (Broom 1991a, b, 1998) so the indicators are often indicators of feelings. It could be that, to combat some problem, one particular coping method is mainly employed, so measurements of that method would provide most of the necessary information. In most studies of welfare, however, it is desirable that a range of measures be obtained. Measures or techniques that are currently proving to be of value in assessing welfare are reviewed in this and the following two chapters. At present, measurements of poor welfare are more common than those of good welfare, since poor welfare is associated with more obvious behavioural, physiological and pathological signs. Some methods of trying to cope with problems are used for both transient and long-lasting problems, but most methods are concerned principally with one or the other. Indications that an individual is failing to cope may not be evident when a problem is brief because they occur only when the problem is long-lasting; these are © Springer Nature Switzerland AG 2019 D. M. Broom, K. G. Johnson, Stress and Animal Welfare, Animal Welfare 19, https://doi.org/10.1007/978-3-030-32153-6_5

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dealt with in Chap. 6. Responses to, and consequences of, short-term problems are considered in this chapter. Short-term is taken here to mean lasting a few hours, whereas long-term problems are those lasting for a day or more. Short-term problems include many in which pain is felt. Other problems, such as anxiety often last long enough to be excluded from this chapter. Any distinction on the basis of time is somewhat arbitrary, especially because biological scaling suggests that small animals are affected more quickly than large animals, so differences in the pace of living must be considered when carrying out practical studies. There are many occasions during life when new stimuli arise and the individual has to decide whether or not to respond to them and how to respond. In social situations, every response may communicate information to other social group members. If there is a potential interaction with a possible predator, that predator may be helped in its assessment of likely success if the particular prey individual were to be attacked by observing the individual’s response to other stimuli. Responses include physiological changes, like heart-rate or hormone level change, as well as behaviour changes. Every person responding to stimuli, in a situation where others may be observing, can alter most responses according to what information is more adaptive to that person when conveyed to the observer. The observer may, for example, represent possible: danger, or aid of some kind, or friendship, or need of help, or courtship opportunity, or information about a resource such as food. Behavioural and physiological responses to stimuli are often modified in order to have a useful effect on observers. In the same way, every dog, sheep, finch in a flock or minnow in a shoal can alter responses adaptively. Some of these responses are indicators of good welfare, happiness, effective coping and high level of functioning. If a person, sheep, finch or minnow clearly has difficulties when trying to make a simple response, they may be treated differently because of that ineffectual action. The detection of obvious difficulty might be very costly if the observer is a predator deciding whether or not to attack or a potential mate deciding whether or not to initiate courtship. Hence it is generally advantageous to indicate efficiency and good welfare, usually presenting an honest signal but sometimes concealing inadequacy if this can be done. As a result, there are many opportunities for assessing good welfare and some circumstances where poor welfare is concealed. In the course of assessing good or poor welfare it is useful to know what is normal in the species in each circumstance. Situations that can lead to short-term welfare problems for animals include potentially frightening human actions with close approach to the animal, handling, certain training methods, transport, some operations to help the animal, other operations carried out for convenience or vanity, deliberate cruelty, procedures preceding the slaughter of domestic animals, and some instances in which wild animals are trapped or killed. Other situations are not caused directly by human intervention; these include accidents, and attacks or threats by predators or animals of the same species (conspecifics). The consequences of these situations may be obviously adverse for the individual, for example severe injuries, or they may be masked and become evident only through specific tests. Attempts to cope with the situations may be adaptive and

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beneficial to an animal, or may be harmful, for example, when caged animals chew their limbs or pluck out their own feathers. In either case they are indicators of poor welfare.

5.1 5.1.1

Behavioural Measures of Welfare Orientation and Startle Responses

The most obvious indicator that an individual is experiencing difficulty in coping with a problem is often a behavioural response. The first behavioural responses to environmental change are orientation reactions. The individual turns so that bilaterally placed sense organs effectively locate and evaluate a directional sensory input. Alternatively the olfactory organ, i.e. the nose in mammals but an antenna or other organ in insects, is raised into the air or water stream so that efficient olfactory recognition can occur. The set of physiological changes which alerts the animal and prepares it for action is called an orientation reaction. This is not an indicator that the animal is encountering a problem. However it may be followed by startle responses and defensive or flight reactions. An orientation reaction may signal the onset of prolonged behavioural changes that are welfare indicators. Most orientation reactions in humans and other species are followed by responses that are neutral or positive because most animals organise their lives in such a way that events are seldom negative in impact. Control over likely changes in the environment is the norm and is advantageous for all species. Each animal seeks to control its interactions with its environment, using its motivational mechanisms, so happiness and pleasure are associated with control and lack of control is aversive. Of course there are negative possibilities so each individual has to be able to react effectively to these. It is the unusual nature of the negative that causes an individual to be startled when a stimulus that might be negative is detected. Startle responses, comprising postural changes, jumps and vocalisations, are more than orientation reactions and their intensity is related to the extent to which the individual has been disturbed. The disturbing effect of a particular sensory input, for example that resulting from a loud noise, the odour of a predator, or the sight of a branch moving, depends upon the characteristics of the input, the context in which it occurs and the previous experience of it. Hence, the same input might elicit a substantial, or a minimal, startle response. The response includes cessation of previous activity, such as resting, feeding or grooming, followed by initiation of immobility, a posture that allows flight, defence, a jump or other sudden movement, and often the production of characteristic sounds. These startle responses vary in detail from one species to another. Some species freeze when startled, others flee or prepare for defence, some vocalise whilst others are silent. The startle responses of young animals may elicit parental help, for example, mother hens react to chick distress calls (Edgar et al. 2011). When a domestic chick

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is startled by a local stimulus it stops its previous behaviour, orients to the stimulus and may give a brief call before freezing (Broom 1968). The duration of visual fixation of the stimulus and of freezing can be measured, as can later reactions, for example, the intensity and frequency of loud ‘cheep’ calls and duration of bouts of calling. The response often involves both freezing and vigorous activity and it varies with the age of the chick and its previous experience (Broom 1969a, b). Small rodents such as mice and rats also freeze when startled, usually after orienting with the ears and nose in a position to receive auditory and olfactory information. An alternative startle response is to make a sudden movement, such as withdrawal of the body by a hole-dwelling fish, jumping by a frog, or a quick movement to remove the animal from a perceived threat and perhaps to make it appear less suitable as prey. Amphibian tadpoles show a rapid locomotor response to an unexpected tactile stimulus (Eidietis 2010). Startle responses are far from automatic and vary according to the preceding combination of stimuli. For example, human startle responses to an acoustic stimulus are altered when it is combined with localised low temperature stimulation (Deuter et al. 2012). Startle responses are often followed by defensive or flight reactions. Indeed the dividing line between startle and active defence or flight is often unclear. However, the various components of the response may be quite distinct, as in the case of the squirrel that hears a sudden sound, orients, jumps, and then either runs away or prepares to fight according to whether the sound comes from a large predator or a rival. Flight from real or imaginary danger is usually easy to recognize. Defensive behaviour may be more difficult to identify, since it includes activities ranging from growling by dogs, to threatened or actual butting by cattle, and prolonged immobility that may make animals difficult to detect by, or appear dead to, a predator. The brain mechanisms involved in some aspects of defensive behaviour and the associated cardiovascular changes are discussed by Dampney et al. (2008). The intensity, duration and frequency of startle responses can be measured as an index of disturbance. Part of the behavioural response is the cessation of normal behaviour, so the delay before such activities are resumed can also be a useful measure. When young domestic chicks are startled, the duration of freezing, number of loud cheep calls, and delay before ground pecking and preening are resumed are greater in chicks reared with a familiar moving object than in those reared in a bare pen (Broom 1969b). Each of these measures showed that chicks reared with a preferred moving object were less disturbed by a novel stimulus than were chicks that had not had that experience. In social groups, social facilitatory effects can be of great importance in determining responses to disturbance. Chickens in a broiler house which are suddenly disturbed by a loud noise or a human action may show a flight response with alarm calls, which in turn promotes a similar response in other birds. The more the birds respond, the greater the stimulus to other birds. This positive feedback may result in mass hysteria, which can also occur in other social species, for example in crowds of people.

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Individual Differences in Behavioural Responses

There is considerable diversity in the responses, both behavioural and physiological, that animals show when disturbed. In addition to differences amongst species in such responses, there are differences amongst individuals within a species. When rats, mice, tree shrews (Tupaia) or pigs are threatened or attacked by another individual of their own species, some individuals actively fight whilst others are largely passive and avoid interactions as much as possible (von Holst 1986; Mendl et al. 1992). As mentioned above, fear responses may be active or passive or one then the other. The control of such responses involves the amygdala. When mice were showing behavioural conditioned fear responses, functional magnetic resonance imaging (fMRI) of the central nucleus of the amygdala identified a neural circuit that biased fear responses towards either active or passive strategies (Gozzi et al. 2010). Variation in behavioural responses is also evident in many other animals, such as pigs subjected to unfamiliar handling and to attempts to drive them and move them up a ramp on to a vehicle. Some pigs run away screaming, others freeze and are reluctant to move even when pushed, and a few pigs try to bite the person when approached closely. These are all responses to a situation that, for a pig that has not had much previous contact with people, is a disturbing experience. Likewise a dog, treated by a veterinary surgeon, may show escape attempts or piloerection, defensive snarling and biting. However, another dog may show withdrawal and reduced activity. Escape, active defence and withdrawal are all indicators of disturbance, the intensity and duration of which can be measured. In a study of the responses of cats confined in a cage in a veterinary hospital or animal shelter, McCune (1992, 2010) found that the most extreme responses were a retreat to the back of the cage, crouching and marked inactivity. Rochlitz (2014) listed low levels of activity and exploration in cats as an indicator of poor welfare.

5.1.3

Measures for Assessing Pain

As explained in Chap. 1, the term pain, like welfare, stress and health, has exactly the same meaning whether we are considering a person, a calf or a trout. This point has been emphasised by many animal welfare scientists and is one of the messages of “one welfare” (García Pinillos 2018). Pain is an aversive sensation and feeling associated with actual or potential tissue damage (Chap. 2 and Broom 2001). The major method used in human pain studies is self-reporting, for example on a scale from no pain to very severe pain. This method can be unreliable because people can lie or deceive themselves in relation to pain. It may be that measures of observed behaviour or physiological change, like those used in non-human studies, will in future be considered more accurate for people than human reporting. Indeed, Turk and Melzack (2011), reviewing pain assessment in humans, include several chapters on the use of direct observation to evaluate pain. The direct measures of pain are of

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behavioural responses, physiological measures of the blood and other organs and measures of brain changes. Most studies of pain as a short-term welfare problem include a combination of measures. Behavioural responses are of particular value when we attempt to assess the extent of pain. The simple observation that cattle react to individual mosquito bites demonstrates that the skin thickness does not prevent responses to painful stimuli. Thicker skin can reduce the likelihood or extent of abrasions following some contacts but the nociceptive cells under the skin function fully in animals like cattle. Short-term pain elicits a substantial behavioural response in some species but very little in others. Characteristic responses include changes in posture during abdominal pain, avoiding use of a painful limb, and licking the painful region. Other responses to localised pain are tightly closed eyelids in cases of eye pain, holding the head on one side or shaking the head in cases of ear pain, rubbing the mouth and unwillingness to eat in response to mouth pain, and vigorous responses when any painful area is touched. Grimace responses may be shown to pain in a wide range of parts of the body (Dalla Costa et al. 2014; McLennan et al. 2016). In addition to direct responses to pain, there can be centrally-mediated hypersensitivity responses when painful experiences occur in humans and other species (Latremoliere and Woolf 2009). Descriptions of responses to pain are to be found in Morton and Griffiths (1985), Turk and Melzack (2011), Broom (2014a) and Broom and Fraser (2015). Sophisticated behavioural measures are being used more and more in studies of pain. However, there are problems in pain recognition which make comparisons between species difficult. Severe pain can exist without any detectable sign. For example, a major response of rabbits that are in pain is inactivity (Leach et al. 2012). Individuals within a species vary in the thresholds for the elicitation of pain responses and species vary greatly in the kinds of behavioural responses that are elicited by pain (Rutherford 2002). Hence it is important to consider which behavioural pain responses are likely to be adaptive for any species that is being considered. Humans, like other large primates, dogs and pigs, live socially and can help one another when attacked by a predator. Parents may help offspring and other group members may help individuals who are attacked or otherwise in pain. Hence, distress signals such as loud vocalisations are adaptive when pain resulting from an injury is felt. Those species which can very seldom collaborate in defence, like the smaller ruminants, do not have obvious responses to pain as these are maladaptive. However, subtle changes in facial expression can be useful indicators of pain, for example in rabbits, rodents, sheep, goats and horses (Dalla Costa et al. 2014; McLennan et al. 2016). The sheep pain facial expression scale involves scoring five facial areas; orbital tightness, cheek tightness, ear position, lip and jaw profile, and nostril and philtrum position. Sheep with footrot, mastitis, or pregnancy toxaemia showed grimace responses and other indicators of pain. When farm ruminants are in pain because of farm operations, the increased cortisol production and an increased occurrence of a range of pain-related behaviours (Stafford and Mellor 2005; Gibson et al. 2007; Stilwell et al. 2008a, b, 2009, 2010) can be quantified. For example, pain-related behaviours in calves include: head-shaking, ear-flicking,

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head-rubbing, inert lying, alterations in gait, amount of walking, licking scrotum, lifting hind leg, abnormal lying, rapid transitions between behaviours and reluctance to go to the food trough. Measures of brain activity can also be used (Gibson et al. 2007) and pain can be prevented using anaesthetics and analgesics (Broom and Fraser 2015). The use of behavioural measures to assess the extent of pain is illustrated by the study of castration of piglets by Wemelsfelder and van Putten (1985). Piglets were castrated without anaesthetic during the fourth week of age, as occurs on many farms. Handling itself elicits struggling and loud squealing from piglets, so the movements and vocalisations of female piglets that were handled and male piglets that were both handled and castrated, were compared. The mean frequency of the scream during handling only was 3500 Hz but after the first cut during castration it was 4500 Hz and after the second cut it was 4857 Hz. Both the number of frequencies occurring in the sound and the number of changes in sound distribution over the frequency range were higher after castration. Similar results were obtained by Taylor and Weary (2000). Recently castrated piglets were less active and showed more trembling, leg shaking, sliding and tail jerking; some vomited, and all initially avoided lying, then later lay in a way that appeared to spare their hindquarters. The duration of the discomfort was indicated by the continuation of some of these changes in behaviour for 2–3 days. When there are behavioural responses which, it is suspected, indicate that the individual is in pain, a check is to administer an analgesic and observe any changes in response. For example, reduced levels of food and water intake and of activity following surgery in rodents were restored to near normal by analgesic (Flecknell and Liles 1991; Flecknell et al. 1991) while behavioural and physiological responses to painful disbudding in calves is prevented by anaesthesia and analgesia (Stilwell et al. 2009). It is important to consider that analgesics in one species may not be effective in another and the analgesic may itself affect behaviour. Further uses of behaviour in the assessment of pain are the tail pinch or tail warming experiments which give information about drug effects (Sect. 6.8) and the measurement of subsequent aversion after experience of a potentially painful treatment. The behavioural tail stimulation tests, combined with physiological measurements, shed light on the underlying mechanisms. For example, Goebel-Stengel et al. (2014) found that in rats, tail pinches activated hypothalamic paraventricular CRH neurons as well as affecting blood glucose and eating behaviour. Tail pinch could be sufficiently disturbing to rats that their associative learning was impaired (Misanin et al. 2006). The effects are more complex than was thought during some early experiments. In one aversion study, Cooper and Vierck (1986) trained monkeys to pull a bar in order to escape painful electrical stimulation. By titrating willingness to pull the bar against the electrical stimulus, pain tolerance levels were found to be similar to those of humans. Aversion after painful treatment was found by Fell and Shutt (1989) when they observed sheep subjected to the mulesing operation in Australia. This operation involves cutting away about 50 cm2 of skin from the tail and genital region in order to reduce the risk of attacks by flies which lay their eggs in damp wool causing wounds and death. It is carried out without anaesthetic. The

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mulesed sheep showed abnormal posture and locomotion and strong avoidance of the people who had restrained them during the operation. Many other studies use aversion after an experience as evidence of pain. For example, Braithwaite and Boulcott (2007) describe several studies in which fish avoided situations that had caused them pain. Other changes in behaviour that are a consequence of pain, and can therefore be indicators, are reduction in play (Mintline et al. 2013), grooming (Ellen et al. 2016) and eating (de Oliveira et al. 2014) and disruption of sleep (Ohayon 2005). Pain leads to physiological responses such as increased heart-rate, increased body temperature and changes in the concentration of glucocorticoids in blood and other body fluids (see below). However, these responses occur in response to impacts on the individual other than pain so they are best used as a pain indicator in situations where it is clear from other evidence that pain is the cause of the change. There are times when it is adaptive for an individual to block pain and this is often done by endogenous opioids. Opioids have many functions, one of which is natural analgesia. Metenkephalin and leuenkephalin are present in all vertebrates that have been tested. The endogenous opioid antagonist MIFI down-regulates sensitivity to opioids in both goldfish and rats. Opioids are one of several groups of analgesics and all of these are useful in pain assessment because they help in validation of measures. If behavioural or physiological measures disappear when an analgesic is administered, the measures were very likely to have been indicating pain. Pain assessment is further discussed by Rutherford (2002) and McLennan et al. (2019).

5.2

Physiological Measures of Welfare

When individuals are exposed to a relatively short-term problem a range of physiological measures can provide information about their welfare. An example of such a situation is a period of transport, when this is a novel experience for that individual, and Table 5.1 shows some of the measures that can be used. The measures are explained further below.

5.2.1

Heart Rate and Heart Rate Variability

Except in diving animals, increases in heart rate (tachycardia) occur when the level of physical activity of an animal and, hence, its metabolic rate, increases. But heart rate can increase before an action occurs, or it can decrease (bradycardia) as an emotional response to a situation, in humans even slowing to the point where the subject faints. In some species such a response may be adaptive in the presence of a dangerous predator or conspecific, which may refrain from attacking an individual that appears dead or at least is not showing behaviour eliciting pursuit. In general, the sympathetic nervous system causes the increase in heart rate and the

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Table 5.1 Physiological indicators of short-term problems, e.g. animal transport Stressor Food deprivation Dehydration Physical exertion, bruising Fear/arousal Motion sickness Inflammation, Hypothermia/hyperthermia

Physiological variable " FFA, " ß-OHB, # glucose, " urea " osmolality, " total protein, " albumin, " PCV " CK, " LDH5, " lactate " cortisol, " PCV " heart rate, # heart rate variability, " ventilation rate, " LDH5 " vasopressin " Acute phase proteins, e.g. haptoglobin, + large immunological responses C-reactive protein, serum amyloid-A Change in body and skin temperature, prolactin

FFA Free fatty acids, ß-OHB Beta hydroxy butyrate, PCV Packed cell volume, CK Creatine kinase, LDH5 Lactate dehydrogenase isoenzyme 5 Modified after Broom and Fraser (2015)

parasympathetic nervous system the decrease. The sophisticated system for controlling heart rate is important because it it maximises the chances that heart rate changes when it is adaptive to change and stops waste of energy and unwanted negative consequences if the heart rate is too high. If the resting heart rate is above 90–100 beats per minute for a long period in humans there is increased risk of cardiovascular malfunction (Fox et al. 2007). Measurement of heart rate can be a useful measure of the emotional response of an individual to short-term problems, provided that distinction is made between the metabolic and emotional effects, and that the measurement itself does not cause too much disturbance. The system used to monitor the heart rate must not itself have an effect on the animal. Mobile heart rate monitors for sports-oriented humans and for studies of other species are now widely available. Bradycardia often occurs during the orienting reaction just after a stimulus is detected, but the major part of the response of most species is tachycardia. Exceptions are those species which show freezing responses. Gabrielsen et al. (1977) recorded the heart rate of incubating willow grouse (Lagopus lagopus) and found that there was bradycardia when a predator approached the well-camouflaged bird, so the grouse was promoting immobility as it sat on its nest. Bradycardia has also been reported in rodents during the freezing response (Steenbergen et al. 1989). Humans may show bradycardia when they have neurological disorders or during neurosurgery thus prompting therapeutic action (Agrawal et al. 2008). When male tree shrews were defeated by other males in fights and remained passive thereafter, they exhibited bradycardia, in contrast to active fighters which showed tachycardia (von Holst 1986). Bradycardia is also well-known as an adaptive response during dives by air-breathing animals that are well adapted for diving. Care must be taken to consider the biology of the animal when using heart rate changes as an indicator of welfare. Studies of humans, sheep, calves, pigs, dogs and rats show that heart rate increases by 50–70% when there is close approach by an unknown person, climbing a ramp, handling, restraint or expectation of an electric shock. Telemetric studies by

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Table 5.2 Sheep heart rate responses (bpm) Treatment Spatial isolation Standing in stationary trailer Visual isolation Introduction to new flock (0–30 min) Introduction to new flock (30–120 min) Transport Approach of man Approach of man with dog

Change in heart rate (taking account of activity) 0 0 +20 +30 +14 +14 +45 +79

From Baldock and Sibly (1990)

Duncan and Filshie (1979) showed that hens in cages displayed tachycardia when a person approached their cage. The response lasted longer in birds of a strain which manifested little behavioural response and was regarded as docile, than in birds of a strain that showed a considerable behavioural response. A common problem in studies of heart rate is that changes as a result of metabolic activity cannot be distinguished from changes due to emotional responses. Baldock et al. (1988) and Baldock and Sibly (1990) overcame this problem by recording basal levels of heart rate of sheep engaged in normal levels of activity: lying, ruminating, standing, and walking (Table 5.2), and taking account of the level of activity. These sheep, which had frequent human contact, showed no heart rate change when they were spatially isolated or put into a stationary trailer, but other treatments caused varying degrees of tachycardia, which was maximal when the animal was approached by a strange person with a dog. Cardiac arrhythmias are sometimes a response to difficult situations. Liang et al. (1979) found that dogs anticipating an electric shock showed greater ventricular excitability. There is evidence in mammals that activity in the cerebral cortex, brain stem and autonomic nervous system play a part when mental disturbances initiate cardiac arrhythmias (Taggart et al. 2011). During normal function, heart rate varies from beat to beat. Heart rate variability results from the dynamic interplay between the multiple physiological mechanisms that regulate the heart rate. In particular, the autonomic nervous system interacts with the sino-atrial node of the heart (Acharya et al. 2007). The relationship between regional cerebral blood flow and heart rate variability is affected by activity in the amygdala and cerebral cortex and is linked to threatening and uncertain situations (Thayer et al. 2012). Heart rate variability gives information about stress and welfare (von Borell et al. 2007). Calming situations can lead to a drop in blood pressure so this measurement may sometimes give information about welfare. People who are interacting with familiar and trusted pets have been shown to show reduced blood pressure but animals, or indeed other people, who are not fully trusted are more likely to elicit blood pressure increases (Allen 2003). Increases in blood pressure can have many causes, for

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example anger in humans (Wagner et al. 2016), so the context of blood pressure measurements must be taken into account during interpretation.

5.2.2

Rate of Breathing, Breathlessness and Body Temperature

When an increase in activity, or a disturbing stimulus, causes tachycardia it usually also increases the rate of breathing and the body temperature. These can be easier to measure than heart rate without disturbing the animal. The rate of breathing should be called ventilation rate but is sometimes erroneously called respiration rate. The biological meaning of respiration is the process in living cells by which energy is released from glucose. Ventilation rate can be assessed by observation of a stationary animal from some distance, and is frequently monitored by veterinary surgeons treating animals. Changes in ventilation rate can occur during emotional disturbance without body activity (Mellor and Murray 1989). When Walker et al. (2011) studied the effect of hot-iron branding on sealions, amongst a variety of welfare indicators, breathing rate increased from a baseline level of 2.5 breaths per minute to 8.9 breaths per minute during branding, despite the fact that they were supposedly anaesthetised with isoflurane. Breathlessness has long been described as a negative consequence of inhalation of certain gases, for example it is one of the negative effects of inhaling the acidic gas carbon dioxide but is not shown if the inert gas argon is inhaled (Raj and Gregory 1996). Dwyer (2008) pointed out that breathlessness indicated severe problems in neonatal lambs and Beausoleil and Mellor (2015) have proposed that it can be used as a welfare indicator in a wide variety of negative situations. Body temperature measurement has long been used in humans as an indicator of certain pathologies, and hence of poor welfare. Core body temperature fluctuates diurnally but can increase following disturbing events. Bonnichsen et al. (2005) measured the core body temperature of rats and found that it increased from the basal temperature when the rat was forcibly given liquid, i.e. gavaged. Reite et al. (1981) found that infant macaque monkeys had elevated body temperature when they were protesting following separation from their mothers. However, the body temperature was reduced later when they reached an apparent ‘despair’ phase. Body temperature reduction is also an indicator of poor welfare in young mammals, such as lambs, exposed to a low environmental temperature (Dwyer 2008). For remote measurement of body temperature, infra-red eye thermography has been found to be valuable in human medicine (Lahiri et al. 2012). Again it is necessary to understand the biology of the animal and to identify the type of response that is being shown when trying to assess welfare by the use of this measure. Handling and transport which causes increased adrenal cortex activity can also elevate body temperature. Trunkfield et al. (1991) recorded rectal temperature of calves after removal from normal housing, loading onto a vehicle, a 1-hour journey

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and pre-slaughter handling. There was a significant increase in body temperature in crate-reared calves, which also showed the largest cortisol response to handling and transport. Although disturbing events can cause an increase in core temperature and inflammation, associated with injury and disease, can cause localised peripheral increases in temperature, peripheral temperature may drop in circumstances in which sympathetic nervous system activity causes vasoconstriction. These changes are often best measured using thermographic imaging. This can be done remotely so that the animal is not too disturbed during measurement. The use of thermographic imaging is reviewed by Lahiri et al. (2012) in connection with various aspects of human disease and by Nääs et al. (2014) in relation to disease, oedema and stress in farm animals.

5.2.3

The Adrenal Axes

Measurements of activity in the sympathetic-adrenal medullary system and especially in the hypothalamic-pituitary-adrenal cortex system are amongst the most useful in the assessment of how difficult it is for animals to cope with short-term problems. As emphasised at the end of this chapter, there is considerable individual variation in how these and other coping methods are used, but changes in the levels of hormones from these two systems are frequently seen as responses to problems arising from environmental conditions, especially those that are severe for short periods. Both systems cause changes in the body that alter the range of substrates available for emergency action: more glucose after adrenomedullary hormones, more amino acids and fatty acids after cortisol. These have the effect of making energy for emergency action more readily available. They differ in their time course in that adrenal medulla hormones circulate in the bloodstream for a shorter time than adrenal cortex hormones, about 2 min for noradrenaline but about 20 min for cortisol (Gregory 1998) and adrenal cortex hormones have more long-term effects. As explained in Chap. 2 and by Broom (2017), both systems can be activated in beneficial and detrimental circumstances so care must be taken to consider the context of their activation before deducing that any adverse effect on welfare has occurred. If it is clear that the behaviour being carried out is beneficial but involves increased physical activity or other energy usage, this possible effect must always be taken into account. The principal products of the adrenal medullary response to emergency situations are the catecholamines adrenaline (epinephrine) and noradrenaline (norepinephrine). In humans, emotional disturbances of the kind that elicit a more passive response cause a greater increase in adrenaline production, and those disturbances which are associated with physical activity, particularly aggression, cause a greater increase in noradrenaline production (Mason 1968). The release of these catecholamines from the adrenal medulla occurs within 1 or 2 s of the perception of the initiating stimulus, but their metabolism is very rapid, the half-life in rat blood being 70 s (McCarty 1983). When trout are subjected to hypoxia, e.g. the very low oxygen tension that

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occurs if they are taken out of water, they show a rapid increase in adrenaline in blood (Segner et al. 2012). The amount of adrenaline and noradrenaline released into the bloodstream when environmental conditions which cause problems are encountered is related to the extent of the problem, so sampling of blood must be very rapid if any useful information is to be obtained. Unless the impact on the animal of handling and sampling can be avoided, for example by using an intravascular cannula the measurements of adrenaline and noradrenaline are generally too difficult to interpret. Samples taken after killing cannot be used to evaluate the effects of procedures because there are large increases in plasma adrenaline and plasma noradrenaline following killing, e.g. after decapitation of rats, and these increases are higher than those caused by experimental manipulations. Levels of adrenaline and noradrenaline in urine can provide some information but they are very variable. An effect of high adrenaline concentration can be substantially increased pH in meat (Gregory 1998) so this measure can be used if the study involves slaughtered animals. The basal plasma levels of adrenaline and noradrenaline in a species vary and domestic guinea pigs had lower concentrations than wild guinea pigs, even after the “wild” strains had been kept in captivity for 30 generations (Künzl et al. 2003), so measurements should be compared with basal concentrations. When Kvetnansky et al. (1978) monitored plasma catecholamine levels in catheterized rats, they found that opening the cage door caused an increase, handling or transfer to a new cage caused a larger increase, and taping the animal to a board caused the greatest increase which was 40-fold for adrenaline and 6-fold for noradrenaline. Smulders et al. (2006) found that pigs with tail lesions and pigs kept at high stocking densities had higher noradrenaline concentrations in their urine than pigs with intact tails and pigs at lower stocking densities. Social interactions also result in increases in plasma catecholamine levels, for example in male guinea pigs defeated in fights (Sachser and Lick 1989). A variety of links between autonomic nervous system activity, including adrenaline and noradrenaline release, and emotion changes are reviewed by Sequeira et al. (2009). The use of plasma adrenaline and noradrenaline as a measure of welfare in conditions lasting for a short period is of value, but should be limited to studies where samples can be taken within 1 min of treatment. Similarly, measuring levels of a catecholamine metabolite such as 3-methoxy-4hydroxyphenylglycol (MHPG) in plasma or urine, is not normally of value as a welfare indicator but could be used in some circumstances provided that all of the sources of this substance have been investigated. For example, MHPG concentrations dropped after a “social stress test” in humans (Ohara et al. 2019). As explained in Chap. 2, the first action of the hypothalamic-pituitary-adrenal cortex system is production of corticotrophin releasing hormone (CRH). Measurements of CRH in the hypothalamus are possible but these can be made only in very restricted experimental conditions. After the release of adrenocorticotrophic hormone (ACTH) from the adenohypophysis (anterior pituitary) it is carried in the blood to the adrenal cortex where the glucocorticoids cortisol, corticosterone, or both are released. The production of ACTH and CRH is inhibited by glucocorticoids, and ACTH is removed quickly from the blood. Hence measurement of plasma ACTH

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levels must be made within a few minutes of the event whose effect on welfare is being assessed. The assay of ACTH is based on the use of one specific antibody for radioimmunoassay and two specific antibodies for radioimmunometric assay and has to be validated in each species (Mormède et al. 2007) so glucocorticoid assay is much more frequent when the extent of poor welfare is being measured. Meyerhoff et al. (1988) measured both ACTH and cortisol in soldiers undergoing an oral examination, and found that ACTH levels were elevated earlier than those of cortisol and that they returned more rapidly to basal values. Many studies of people with post-traumatic stress disorder record ACTH and cortisol increase when the people experience major or minor disturbance (de Kloet et al. 2006). In guinea pigs, rhesus monkeys and rats significantly increased plasma ACTH was measured after exposure to noise and vibration; confinement or immobilisation; exposure to a loud noise; electric shock; movement to a novel environment; or low temperature. Glucocorticoid levels rise in response to many short-term problems in life and their measurement, using radioimmunoassays (RIA) and enzyme-linked immunosorbent assays (ELISA) for glucocorticoids in blood plasma or saliva, gives valuable information about the welfare of animals. Cortisol can be measured in urine and compared with levels of creatinine which is excreted at a relatively constant rate (Stephen and Ledger 2006). Urine samples can sometimes be collected with minimal disturbance to the individual, but the collection must occur some considerable time after the event whose effects are being studied because of the time taken for the metabolism involved. A major problem with all attempts to measure adrenal cortex responses in plasma is that the action of taking a sample often evokes a considerable response. However, there is a much greater delay before glucocorticoids are released into the bloodstream than occurs before adrenaline or noradrenaline are released from the adrenal medulla. In most species the delay before glucocorticoids are released is at least 2 min, so the effects of a particular treatment can be measured if a blood sample is collected within 2 min of the beginning of the blood sampling procedure. A further problem is that there is a cycle in baseline adrenal cortex activity, and the magnitude of the response when an animal is stimulated can vary according to the stage of this cycle. For example Seggie and Brown (1975) found that the corticosterone response to handling was two and a half times greater in rats at the peak of the baseline cycle than in those at the trough. In some situations a saliva sample can be taken and assayed using ELISA. The quantity of cortisol in saliva is less than that in plasma so a more sensitive assay is needed. Plasma glucocorticoids exist in free and protein-bound forms (see Chap. 2). Only the free form is present in saliva but this is probably the most relevant when assessing responses to environmental difficulties. Salivary cortisol levels increase in response to ACTH injection, are not affected by salivary flow rate and increase in circumstances almost identical to those in which plasma cortisol increases in humans and many other vertebrate species. However, several factors result in some variability between changes in salivary and plasma cortisol concentrations (Hellhammer et al. 2009).

5.2 Physiological Measures of Welfare Table 5.3 Effects of surgical procedures on lambs (from Shutt et al. 1987)

Control Tail dock Castration Mulesing and tail dock Mulesing, tail dock and castration

113 Cortisol (n mol l1) 87 136 171 187 232

In primates, dogs, cats, most ungulates and fish the predominant glucocorticoid produced is cortisol; in rodents and chickens, it is corticosterone. However, in some species, for example pigs, both are produced. The magnitude of the adrenocortical response is affected by a range of genetic and experiential factors. This fact and the evidence for wide individual variation in adrenal, as in other coping responses, have highlighted the need for careful control of genetic diversity in subjects and for the use of large sample sizes in studies of the effects of different treatments on adrenal cortex responses. Situations which would be expected to be painful are sometimes, but not always, associated with increased plasma glucocorticoid levels. Silver (1982) found such increases after surgical treatment for tendon damage in horses, and many studies have reported increases in cortisol levels associated with operations such as tail-docking, castration, and mulesing (Sect. 5.1.3) in sheep (Shutt et al. 1987), disbudding of calves (Stilwell et al. 2012) and castration in pigs (Prunier et al. 2005). In such studies, a greater severity of procedure leads to greater glucocorticoid concentration in plasma (Table 5.3). Cortisol levels were still high 24 h after mulesing, probably because of continuing pain. Further evidence for links between adrenal cortex response and pain comes from the findings that analgesia can substantially reduce the response, for example in new-born human infants undergoing surgery (Anand et al. 1987, 1988). Such results led to a general move to use analgesics after minor operations on new-born babies. Most people are amazed to learn that human babies up to 6 or 12 months were routinely operated upon without the use of analgesics until the 1970s–1990s, the date of change depending on country. In future there may be the same amazement that in 2019 many operations on sentient farm animals are conducted without analgesic use. Links between predictably painful situations, adrenal cortex response and suppression of this response by a proven analgesic are particularly useful in the assessment of pain (Stilwell et al. 2009). There can be adrenal cortex responses associated with tissue damage during farm operations even when an anaesthetic was used (Petrie et al. 1996). It may be that, although pain was prevented by the anaesthetic, the cortisol increase is a consequence of other poor welfare (Stilwell et al. 2012). Alternatively, the damage itself, even if not perceived, may cause an adrenal response. Cortisol is produced by epidermal cells when there is local tissue damage (Vukelic et al. 2011). Various forms of laboratory animal handling, for management or experimental purposes, elicit adrenal cortex responses. Kvetnansky et al. (1978) found that handling for 30 s doubled plasma glucocorticoid levels in rats and significant

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Fig. 5.1 Plasma corticosterone in mice in their home cage, and shortly after exposure to novel situations with different degrees of difference from the home cage (modified after Hennessy and Levine 1978)

increases also occurred in rats when their cages were moved from a rack to the floor or a table (Gärtner et al. 1980). Zebrafish Danio rerio, the commonest laboratory vertebrate, more than doubled their plasma cortisol concentration 3 min after being caught in a net (Ramsay et al. 2009). After 15 min the cortisol concentration was six times the basal level and, as is normal with cortisol, the concentration declined to basal level by 1 h after the handling. Mice and rats show elevated plasma corticosterone levels when put into a novel environment and the extent of corticosterone elevation is related to the degree of novelty, as shown in Fig. 5.1 (Hennessy and Levine 1978). Similarly, children with autism had increased plasma cortisol after exposure to novel stimuli (Spratt et al. 2012). Handling and other treatment causes increases in plasma cortisol levels in trout (Pickering and Pottinger 1985). Handling and transport of farm animals also results in an adrenal cortex response. Broom et al. (1986) reported that plasma corticosterone levels in hens from a battery house were 4.3 ng ml1 5 min after the normal, rough handling that occurs before transport to slaughter, but only 1.45 ng ml1 after gentle handling. Li et al. (2007) found that transported, catheterised piglets had rapidly increased plasma cortisol during the first 15 min of transport, continuing high concentration throughout a 2 h journey and decline to basal level by 15 min after the end of the journey.

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200

Cortisol (nmol/l)

150

100

50

L 0

1

3

5

7

9

11 13 15 17 19 21 23 25 27 29 31 Time (h)

Fig. 5.2 Mean plasma cortisol concentration in two groups of sheep, shorn and not shorn, sampled by catheter during a 14 h motorway journey, a 1 h rest period, a further 13 h on motorway and then 3 h on rural roads (modified after Parrott et al. 1998)

During the period of monitoring of sheep on a road journey shown in Fig. 5.2, the sheep showed a very marked increase in plasma cortisol when they were loaded on to the vehicle. This occurred despite the fact that the staff concerned were experienced animal handlers and did not treat the animals roughly. The sheep were clearly very disturbed by the loading, and the response lasted for 6 h. The cortisol concentration then dropped to close to the basal level as the sheep became accustomed to their new environment. During the last 3 h of the journey, cornering and acceleration caused problems for the sheep, so cortisol concentration increased (Parrott et al. 1998). It is clear from studies like this that measurement of cortisol concentration can provide information about the welfare of animals over relatively short periods. Laboratory experiments can lead to substantial adrenocortical responses. It has long been known that plasma glucocorticoid concentrations increase substantially in rats restrained in a plastic tube, monkeys restrained in a chair, rats receiving electric shocks, infant monkeys separated for 2-hour periods from their mothers, mice attacked after being put in a new colony, and rats or guinea pigs involved in fights (e.g. Sachser 1987). Even exposure to the odour of rats that had experienced shocks resulted in adrenal cortex responses (MacKay-Sim and Laing 1980). In general, it is clear that measures of glucocorticoid responses are of considerable value when assessing short-term negative effects on the welfare of humans and other animals. Although some effects of glucocorticoids are beneficial, high concentrations can damage the brain or impede its function, either directly or by increasing its susceptibility to other, coincident, damaging agents. Excess glucocorticoids can also impair both cognitive and affective function, and may contribute to the decline of cognitive ability with age (Herbert et al. 2006). The various problems and variables mentioned in this section must be taken into account during interpretation of data on changing concentrations of glucocorticoids.

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Other Hormones

In addition to glucocorticoids, several other hormones are affected by exposure to difficult conditions and some hormones increase in situations where there is good welfare. Prolactin, which can be measured in plasma using radioimmunoassay, was elevated in sheep after restraint but not affected by isolation (Parrott et al. 1987). Plasma prolactin concentrations are higher in overheated sheep but are not consistently related to other negative treatment (Parrott et al. 1998). Friendly interactions between dogs and dog owners led to increased plasma prolactin, oxytocin, β-endorphin, β-phenylalanine and dopamine (Odendaal and Meintjes 2003). Oxytocin concentration in the blood is higher during a range of pleasurable events. One of such events is nursing the young in a female mammal. Oxytocin is released with the let-down of milk but also leads to a feeling of pleasure. Oxytocin is synthesised in the paraventricular nucleus (PVN) of the hypothalamus and in the supraoptic nucleus. It binds to receptors that regulate HPA axis activity and in humans and other species of mammals its increase is associated with: ACTH and glucocorticoid decrease, lymphocyte proliferation, brain GABA increase, cardiac vagal tone increase and social stress reduction (Carter and Altemus 1997; Redwine et al. 2001; Smith and Wang 2012; Cardoso et al. 2014). In squirrel monkeys oxytocin reduces HPA response (Parker et al. 2005). In humans and other mammals, oxytocin modulates emotional responses controlled by the amygdala, anterior cingulate cortex, lateral septum, ventral tegmentum and nucleus accumbens (Tost et al. 2015). It is associated with parental care, emotional understanding of others, social support and inter-individual trust (Feldman et al. 2007; Ross and Young 2009; MeyerLindenberg et al. 2011). Oxytocin is associated with positive views of ambivalent stimuli, i.e. with positive cognitive bias, in both dogs and humans (Kis et al. 2015). Hence oxytocin is, at present, the most valuable physiological indicator of good welfare. Whilst there are sometimes changes in concentrations of luteinising hormone (LH), follicle stimulating hormone (FSH), thyroid stimulating hormone (TSH), growth hormone (GH) and testosterone in plasma after a variety of treatments, they are not of general use as welfare indicators. Glucagon is involved in the regulation of plasma glucose levels and showed transient increases followed tendon surgery in horses (Silver 1982) and surgical trauma in humans (Anand et al. 1987; Anand and Aynsley-Green 1988). Although glucagon is involved in interactions with catecholamines and glucocorticoids in stress-induced hyperglycaemia (Mormède et al. 2007), it seems to be of little use as a welfare indicator. Atrial natriuretic peptide (ANP) is produced by muscle cells in the cardiac atria when there is atrial stretching and, under certain conditions, in response to hormones from the adrenal cortex and adrenal medulla (Brenner et al. 1990). Levels of ANP in rat plasma following foot-shock and ANP measurement can be useful in treating cardiac and arterial disorders (Schoensiegl et al. 2007); it is not likely to be useful as a welfare indicator.

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The naturally occurring opioids, including ß-endorphin, are produced at the same time as ACTH in some circumstances. For this reason alone, measurements of their levels in plasma are of interest during welfare assessment. A further possibility is that these measures reflect their natural analgesic function (Hughes et al. 1975) or indicate the animal’s success in coping. Restraint and foot-shock leads to increases in plasma ß-endorphin in rats (Mueller 1981; Kant et al. 1983) and ß-endorphin, ACTH and cortisol increases when stallions are transported 100 km (Fazio et al. 2008). Horses involved in show-jumping have higher plasma cortisol and ß-endorphin when they have jumped 1.2 m or 1.3 m high fences than when the fences were only 1.1 m high (Ferlazzo et al. 2012). However, ß-endorphin concentrations do not change in the same way as changes in cortisol concentrations when animals are stunned. After stunning of horses there are increases in plasma cortisol and catecholamines but no increase in plasma ß-endorphin, hence ß-endorphin is not always released when ACTH is released (Micera et al. 2010).

5.2.5

Enzymes, Other Proteins and Metabolic Products

When individuals are subjected to difficult conditions, for example a novel experience of transport in suboptimal conditions, one response is an increase in the presence of proteins, referred to as acute phase proteins, in the blood plasma. In transported pigs, which are very much disturbed by transport, these include: major acute phase protein (Pig-MAP), haptoglobin, serum amyloid A and C-reactive protein (Piñeiro et al. 2007). Some of these proteins also play a role in defences against disease and have a role in inflammatory responses and anxiety (Lomborg et al. 2008). For example, haptoglobin has a role in removal of damaged haemoglobin and is immunomodulatory in action during diseases with inflammatory causes (Quaye 2008). Since welfare is worse when there is disease, acute phase proteins are often of use as welfare indicators but the earliest acute phase responses may indicate only a small change in welfare. Measurements of most plasma enzyme activity are more appropriate for longterm than for short-term welfare assessment because it takes time for additional enzyme to be produced following an environmental change. There can be transient increases in the plasma levels of the enzymes renin, alanine aminotransferase, aspartate aminotransferase and alkaline phosphatase but these enzymes may not change following exposure to a situation that causes a plasma cortisol increase (Gärtner et al. 1980). In the extreme negative situation for welfare where a wild animal is captured, there may be changes in a wide range of blood enzymes, e.g. in vicuña (Bonacic et al. 2006). Creatine kinase, is produced from heart and skeletal muscle after damage or vigorous exercise, as well as in a range of disturbing situations. It increased in rabbits following blood loss (Bacou and Bressot 1976), was positively correlated with injury score in pigs transported to slaughter (Brandt et al. 2013) and calves kept in outdoor yards where they could exercise had higher plasma creatine kinase levels than those kept in very small pens (Friend et al. 1985).

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The increase in creatine kinase in transported livestock appears to be a consequence of both muscular activity when trying to balance in a moving vehicle and the disturbing effects of the conditions (Sutherland et al. 2010). Lambs which were rounded up and loaded on to a vehicle and grouped together at lairage had increased plasma creatine kinase but after a 26 h, calm boat trip the creatine kinase concentration declined (Tadich et al. 2009). Gently handled cattle had lower plasma creatine kinase than roughly handled cattle (Sena Brunel et al. 2018). In a range of situations, especially those involving disturbing transport or injury, creatine kinase is a useful animal welfare indicator (Broom 2003, 2008, 2014b). The measurement of creatinine is useful when assessing measurements of cortisol metabolites in faeces as creatinine is produced at a relatively steady rate. Another enzyme which leaks from muscle into the bloodstream in certain situations is a form of lactate dehydrogenase (LDH). There are five isoenzymes of LDH; LDH5, which occurs mainly in striated muscle and liver, increases in plasma after muscle damage or exposure to disturbing conditions in pigs. A high incidence of pale, soft, exudative meat (PSE) in slaughter pigs is associated with high levels of LDH5. Increases in levels of plasma LDH5 in cattle after transport have been reported by Mormede et al. (1982). Plasma LDH5 also increased in red deer after transport (Goddard et al. 1997) and in park deer after capture, even in animals lying quietly with their heads covered (Jones and Price 1990). Hence it seems that the release of this isoenzyme into plasma cannot be just a consequence of exercise, but is a response of the animal to a disturbing situation. Plasma glucose levels are increased following the secretion of adrenal medullary and cortical hormones, but they can also be reduced by vigorous activity. Plasma glucose levels increased in rats following: electric shock, movement of their cage from the rack to the floor, exposure to ether and transfer into a new cage (de Boer et al. 1989). However, increases in plasma glucose levels are sometimes followed by a decrease below the baseline. Turnbull et al. (2005) included glucose in their salmon welfare score but it was not clear how it contributed. Overall it seems that measurements of plasma glucose are of little value as welfare indicators unless repeated samples of plasma are available, and the obtaining of these may cause further changes in adrenal activity and glucose production. Other metabolites such as free fatty acids and cholesterol have been measured following exposure to a variety of unpleasant situations, but the responses do not appear to be consistent or useful as indicators of welfare.

5.2.6

Blood, Muscle and Other Carcass Characteristics

When a blood sample is taken from an individual, if the sample volume is measured and then the sample is centrifuged in a standard way, the volume occupied by the cells can be measured and is called the packed cell volume (PCV). The ratio of the total volume of red blood cells to the total volume of blood is the haematocrit. When sheep were transported, an increase in plasma cortisol concentration was associated

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with a fall in PCV (Hall et al. 1998) whilst gently handled cattle had lower PCV than roughly handled cattle (Sena Brunel et al. 2018). The PCV changes may be related to dehydration. However, when considering the problems of overheated and dehydrated donkeys, these did not have PCV different from animals at normal temperature and degree of hydration (Pritchard et al. 2010). Packed cell volume declines if there has been blood loss (Petherick et al. 2014) but blood loss may be detected in easier ways. In certain circumstances PCV can be a useful measure but is not a general welfare measure. When farm animals are handled or transported, biochemical changes, especially those associated with glycogen metabolism, occur in muscle. When pigs are subjected to such disturbance before slaughter, there can be very rapid glycolysis, with consequent high production of lactic acid and fall in pH. As a result, the waterbinding capacity of muscle protein declines, water leaks out of the meat and the colour becomes paler and greyer. The incidence of the pale, soft, exudative (PSE) meat produced gives information about the welfare of the animals in the period shortly before slaughter, but the substantial genetic variation in the likelihood of PSE meat production must be taken into account (Faucitano 2010). Such meat is of considerably lower palatability and, hence, value. Dark, firm, dry (DFD) meat is produced if glycogen reserves are depleted before death so that little lactic acid can be produced in the muscles after death and the pH remains high. It is less attractive to shoppers choosing meat and, although it is usually more tender than normal meat, its value is lower. In cattle and pigs: fighting, disturbances caused by mixing animals from different groups, and adverse weather can lead to DFD meat after slaughter (Tarrant 1981; Faucitano 2010) and the same can be true in pigs. The presence of PSE and DFD meat provides evidence about the welfare of the animals prior to slaughter. In one study, when stunning of pigs was by gas instead of electrical, the incidence of PSE meat dropped from 35% to 6% (Velarde et al. 2001). Injuries to animals following handling or transport are important indicators of their welfare. Guise and Penny (1989a, b) reported that skin blemishes on carcasses of pigs after slaughter, including scratches and bruises, could be related to the conditions experienced by the animals during their last few hours. For example, the number of blemishes was increased if animals were mixed with strangers. Bone breakage can also occur, especially in poultry. Gregory and Wilkins (1989) dissected more than 3000 hens from battery cages in the UK and found that a mean of 29% had broken bones before they reached the water-bath stunner in the slaughter line. Stratmann et al. (2015) found that keel bone breakage in laying hens was reduced by providing soft perches so that the birds did not land heavily on them. Bone breakages and other injuries are important indicators of poor welfare, the effects ranging from very slight to extremely severe. There are scales of severity for bruises and cuts to use in comparative studies. These can be used in combination with indicators of pain and discomfort.

120

5.3

5 Assessing Welfare: Short-Term Responses

Using Indicators to Evaluate Welfare

When measures are made of the attempts of animals to cope with short-term problems, figures obtained for changed behavioural response, increased heart rate, or the extent of any increase in a hormone or enzyme, have to be interpreted. What do these figures tell us about how good or how poor the welfare is? How can the various measures be interrelated? Is a certain increase in heart rate equivalent to a certain degree of inhibition of normal behaviour? Some responses occur only in more extreme situations, whereas others appear when only a slight disturbance occurs. Nonetheless, levels of one measure may still be equated with levels of another. One kind of coping response may be an alternative to another. In recent years our ability to select and integrate welfare measures, and to balance positive and negative indicators, has developed rapidly so the questions posed above will now be considered in turn. Some behavioural responses to difficult situations either occur or do not occur but most are quantifiable. We can measure the number of distress calls, the frequency of kicking at a localized pain source, the strength of avoidance, or the duration of a response. In general it seems logical to assume that a more intense or prolonged response means a greater problem for the individual concerned. Hence in Baldock and Sibly’s (1990) study of heart rate in sheep (Sect. 5.2.1), animals were presumed to be more disturbed, as indicated by higher heart rates, when confronted by the strange man with a dog than by the man alone or by transport. There is a maximal level of heart rate, however, so it not always clear how different components of a set of stimuli contributes to the response. An additional measure that can be used is the delay before the high heart rate returns to resting levels (Duncan 1986). This measure is particularly useful because of the individual variation in heart rate response; with this technique, as in Baldock and Sibly’s study, animals can be used as their own controls. Measures of adrenal cortex response also show a graded increase above the basal level over a range of increasing difficulties and have a maximal response. For some physiological measures, however, the delay before return to resting levels may be either a function of the maximum level reached, in which case no extra information is obtained, or may be unrelated to the level reached or to the effects of conditions on the individual. In order to use any one of the measures discussed in this chapter as an indicator of welfare, the significance of different magnitudes of the effect and of different patterns of return to normal must be studied in the species concerned. A measure such as the occurrence of escape behaviour gives information about how poor the welfare of an individual is. However, a lower level of that response in another individual does not necessarily mean that the welfare of the second animal is better. The animal could be using a different coping method, or could be affected in a different way from the first. Duncan and Filshie’s (1979) finding that a supposedly docile strain of hens, which showed a small behavioural response to human approach, showed a much greater heart rate response than a supposedly ‘flighty’ strain (Sect. 5.2.1) is a good example of this. In welfare assessment, care must be

5.4 Short-Term Welfare Problems and Concepts of Stress

121

taken to consider that an extreme response in one individual may be immobility, whilst in others it may be flight or increased aggression (Broom 1986, 1988; Broom and Fraser 2015). A single measure can indicate that welfare is poor but a combination of measures is preferable if valid comparisons of conditions affecting the welfare of animals are to be made.

5.4

Short-Term Welfare Problems and Concepts of Stress

As explained in Chap. 4 the term stress is used when we can see that the environmental effect on an individual is reducing, or is likely to reduce, the fitness of the individual. Throughout this chapter, the assessment of welfare has been emphasised because, although it is often clear that the individual is having difficulty in coping, it is sometimes not clear that there will be an effect on fitness. A brief period of elevated heart rate, adrenal cortex activity, or emergency behaviour is an attempt to cope and measures of them indicate that welfare is poorer in the particular animal than in an individual that does not have such responses. However, the individual may cope effectively and the environmental impact and coping attempts may have no effect at all on life expectancy, the period before the next breeding or the number of young produced at next breeding. An extreme response or a series of relatively extreme responses is more likely to affect fitness. In an extreme situation, a substantial startle response could lead to a heart attack, or to some cardiac tissue damage that makes subsequent heart attacks more likely to be fatal. As discussed further in the next chapter, high levels of adrenal activity, even for short periods, can cause sufficient immunosuppression for a pathogen attack to be successful, whereas such an attack would otherwise be warded off by the immune system defences. Likewise a behavioural response to some short-term problem could make an individual more vulnerable to predator or parasite attack, and thereby reduce its fitness. Hence some responses to short-term problems will reduce fitness, even if the majority of such responses do not. The word stress can be used, somewhat loosely, in relation to many circumstances that result in poor welfare, but there are many circumstances in which welfare is affected but there is no stress. Sometimes a disturbing situation which is, in itself, very unlikely to reduce fitness can be very difficult for the individual to cope with, and so there is a considerable effect on welfare. Human phobias can be examples of this. The fear of spiders, in countries where there are no dangerous spiders, may mean that a brief encounter with a spider is disturbing to the person for a few seconds or minutes, so welfare is temporarily poorer, but no effect on fitness occurs unless the response itself increases risk of heart attack or otherwise adversely affects fitness. It is desirable that, for humans and other species, the relationships between shortterm problems and effects on fitness be more thoroughly understood. Firstly, there is the question raised above of the links between extreme, but brief, periods of poor welfare and ultimate effects on fitness. Secondly, we need to consider welfare in

122 Fig. 5.3 The measured intensity of good or poor welfare is plotted against time for two examples: (a) might be an animal being killed by a method involving prolonged pain and other poor welfare; (b) might be an animal being killed by a method that has a much more rapid effect. The magnitude of good or poor welfare is the area under the curve (modified after Broom 2001; 2014a, b)

5 Assessing Welfare: Short-Term Responses

High Intensity of effect Low High Intensity of effect Low

relation to time, and the relative importance of short- and long-term problems. For example, which is worse, severe pain for a few minutes or milder pain for many weeks? In the same way, which is better, substantial pleasure for a few minutes or less pronounced pleasure for many weeks? Over any timescale, measures of intensity of effect on welfare have to be related to the duration of the state. When welfare is evaluated, the relationship between its intensity (the word ‘severity’ is sometimes used where the effect is negative) and duration should be taken into account. Figure 5.3 was initially drawn to exemplify poor welfare during killing methods (Broom 2001) but the principle is the same for positive effects. Using an evaluation of good or poor welfare that takes account of time, the major welfare problems are seen to be those with a long duration. For humans, farm animal or any other animal, poor living conditions that lead to poor welfare are generally a much more important problem than short-term problems. Housing systems, for laboratory or farm animals, that do not meet the needs of the animals are much worse than short periods of transport, brief laboratory procedures or painful killing methods. This does not mean that the short-term problems do not matter but it does mean that inadequate housing, or other prolonged problems, are more cruel.

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Pickering AO, Pottinger JG (1985) Factors influencing blood cortisol levels of brown trout under intensive culture conditions. In: Lofts B, Holms WN (eds) Current trends in comparative endocrinology. Hong Kong University Press, Hong Kong, pp 1239–1242 Piñeiro M, Piñeiro C, Carpintero R, Morales J, Campbell FM, Eckersall D, Toussaint MJM, Lampreave F (2007) Characterisation of the pig acute phase protein response to road transport. Vet J 173:669–674. https://doi.org/10.1016/j.tvjl.2006.02.006 Pritchard JC, Barr ARS, Whay HR (2010) Validity of a behavioural measure of heat stress and a skin tent test for dehydration in working horses and donkeys. Equine Vet J 38:433–438. https:// doi.org/10.2746/042516406778400646 Prunier A, Mounier AM, Hay M (2005) Effects of castration, tooth resection, or tail docking on plasma metabolites and stress hormones in young pigs. J Anim Sci 83:216–222. https://doi.org/ 10.2527/2005.831216x Quaye IK (2008) Haptoglobin, inflammation and disease. Trans R Soc Trop Med Hyg 102:735–742. https://doi.org/10.1016/j.trstmh.2008.04.010 Raj ABM, Gregory NG (1996) Welfare implications of the gas stunning of pigs 2. Stress of induction of anaesthesia. Anim Welf 5:71–78 Ramsay JM, Feist GW, Varga ZM, Westerfield M, Kent ML, Schreck CB (2009) Whole-body cortisol response of zebrafish to acute net handling stress. Aquaculture 297:157–162. https://doi. org/10.1016/j.aquaculture.2009.08.035 Redwine LS, Altemus M, Leong Y-M, Carter CS (2001) Lymphocyte responses to stress in post partum women: relationship to vagal tone. Psychoneuroendocrinology 26:241–251 Reite M, Short R, Seiler C, Pauley JD (1981) Attachment, loss and depression. J Child Psychol Psychiatry 22:141–169 Rochlitz I (2014) Feline welfare issues. In: Turner DC, Bateson P (eds) The domestic cat: the biology of its behaviour, 3rd edn. Cambridge University Press, Cambridge, pp 131–153 Ross HE, Young LJ (2009) Oxytocin and the neural mechanisms regulating social cognition and affiliative behavior. Front Neuroendocrinol 30:534–547 Rutherford KMD (2002) Assessing pain in animals. Anim Welf 11:31–53 Sachser N (1987) Short–term responses of plasma norepinephrine, epinephrine, glucocorticoid and testosterone titers to social and non-social stressors in male guinea pigs of different social status. Physiol Behav 39:11–20 Sachser N, Lick C (1989) Social stress in guinea pigs. Physiol Behav 46:137–144 Schoensiegl F, Bekeredjian R, Schrewe A, Weichenhan D, Frey N, Katus HA, Ivandic BT (2007) Atrial natriuretic peptide and osteopontin are useful markers of cardiac disorders in mice. Comp Med 57:546–553 Segner H, Sundh H, Buchmann K, Douxfils J, Snuttan Sundell K, Mathieu C, Ruane N, Rutfeldt F, Toften H, Vaughan L (2012) Health of farmed fish: its relation to fish welfare and its utility as a welfare indicator. Fish Physiol Biochem 38:85–105. https://doi.org/10.1007/s10695-011-9517-9 Seggie JA, Brown GM (1975) Stress response patterns of plasma corticosterone, prolactin, and growth hormone in the rat, following handling or exposure to novel environment. Can J Physiol Pharmacol 53:629–637 Sena Brunel HS, Dallago BSL, Bezerra de Almeida AM, Zorzan de Assis A, Calzada RJB, Brasileiro de Alvarenga AB, Menezes AM, Barbosa JP, Lopes PR, González FHD, McManus C, Broom DM, Bernal FEM (2018) Hemato-biochemical profile of meat cattle submitted to different types of pre-loading handling and transport times. Int J Vet Sci Med 6:90–96. https://doi.org/10.1016/j.ijvsm.2018.04.002 Sequeira H, Hot P, Silvet L, Delplanque S (2009) Electrical autonomic correlates of emotion. Int J Psychophysiol 71:50–56. https://doi.org/10.1016/j.ijpsycho.2008.07.009 Shutt DA, Fell LR, Cornell R et al (1987) Stress induced changes in plasma concentrations of immunoreactive endorphin and cortisol in response to routine surgical procedures in lambs. Aust J Biol Sci 40:97–103 Silver IA (1982) The firing of horses. Final report to the Veterinary Advisory Committee of the Horserace Betting Levy Board, p 48

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Smith AS, Wang Z (2012) Salubrious effects of oxytocin on social stress-induced deficits. Horm Behav 61:320–330 Smulders D, Verbek G, Mormède P, Geers R (2006) Validation of a behavioral observation tool to assess pig welfare. Physiol Behav 89:438–447. https://doi.org/10.1016/j.physbeh.2006.07.002 Spratt EG, Nicholas JS, Brady KT, Carpenter LA, Hatcher CR, Meekins KA, Furlanetto RW, Charles JM (2012) Enhanced cortisol response to stress in children with autism. J Autism Dev Disord 42:75–81. https://doi.org/10.1007/s10803-011-1214-0 Stafford KJ, Mellor DJ (2005) Dehorning and disbudding distress and its alleviation in calves – a review. Vet J 169:337–349 Steenbergen JM, Koolhaas JM, Strubbe JH, Bohus B (1989) Behavioral and cardiac responses to a sudden change in environmental stimuli: effect of forced shift in food intake. Physiol Behav 45:729–733 Stephen J, Ledger RA (2006) A longitudinal evaluation of urinary cortisol in kennelled dogs, Canis familiaris. Physiol Behav 87:911–916. https://doi.org/10.1016/j.physbeh.2006.02.015 Stilwell G, Lima MS, Broom DM (2008a) Effects of nonsteroidal anti-inflammatory drugs on longterm pain in calves castrated by use of an external clamping technique following epidural anaesthesia. Am J Vet Res 69:744–750 Stilwell G, Lima MS, Broom DM (2008b) Comparing plasma cortisol and behaviour of calves dehorned with caustic paste after non-steroidal-anti-inflammatory analgesia. Livest Sci 119:63–69 Stilwell G, Carvalho RC, Lima MS, Broom DM (2009) Effect of caustic paste disbudding, using local anaesthesia with and without analgesia, on behaviour and cortisol of calves. Appl Anim Behav Sci 116:35–44 Stilwell G, Carvalho RC, Carolino N, Lima MS, Broom DM (2010) Effect of hot-iron disbudding on behaviour and plasma cortisol of calves sedated with xylazine. Res Vet Sci 88:188–193 Stilwell G, Lima MS, Carvalho RC, Broom DM (2012) Effects of hot-iron disbudding, using regional anaesthesia with and without carprofen, on cortisol and behaviour of calves. Res Vet Sci 92:338–341 Stratmann A, Fröhlich EKF, Harlander-Matauschek A, Schrader L, Toscano MJ, Würbel H, Gebhardt-Henrich SG (2015) Soft perches in an aviary system reduce incidence of keel bone damage in laying hens. PLoS One 10(3):e0122568. https://doi.org/10.1371/journal.pone. 0122568 Sutherland MA, Bryer PJ, Davis PL, McGlone JJ (2010) A multidisciplinary approach to assess the welfare of weaned pigs during transport at three space allowances. J Appl Anim Welf Sci 13:237–249. https://doi.org/10.1080/10888705.2010.483879 Tadich N, Gallo C, Brito ML, Broom DM (2009) Effects of weaning and 48h transport by road and ferry on some blood indicators of welfare in lambs. Livest Sci 121:132–136. https://doi.org/10. 1016/j.livsci.2008.06.001 Taggart P, Critchley H, Lambiase PD (2011) Heart–brain interactions in cardiac arrhythmia. Heart 97:698–708. https://doi.org/10.1136/hrt.2010.209304 Tarrant PV (1981) The occurrence, causes and economic consequences of darkcutting in beef – a survey of current information. In: Hood DE, Tarrant PV (eds) The problem of dark–cutting in beef. Martinus Nijhoff, The Hague Taylor AA, Weary DM (2000) Vocal responses of piglets to castration: identifying procedural sources of pain. Appl Anim Behav Sci 70:17–26 Thayer JF, Ahs F, Fredrikson M, Sollers JJ III, Wager TD (2012) A meta-analysis of heart rate variability and neuroimaging studies: implications for heart rate variability as a marker of stress and health. Neurosci Biobehav Rev 36:747–756. https://doi.org/10.1016/j.neubiorev. 2011.11.009 Tost H, Champagne FA, Meyer-Lindenberg A (2015) Environmental influence in the brain, human welfare and mental health. Nat Neurosci 18:4120–4131. https://doi.org/10.1038/nn.4108 Turk DC, Melzack R (2011) Handbook of pain assessment, 3rd edn. Guildford Press, New York

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Turnbull J, Bell A, Adams C, Bron J, Huntingford F (2005) Stocking density and welfare of cage farmed Atlantic salmon: application of a multivariate analysis. Aquaculture 243:121–132. https://doi.org/10.1016/j.aquaculture.2004.09.022 Trunkfield HR, Broom DM, Maatje K, Wieranga HK, Lambooy E, Kooijman J (1991) Effects of housing on responses of veal calves to handling and transport. In: Metz JHM, Groenestein CM (eds) New trends in veal calf production. Pudoc, Wageningen, pp 40–43 Velarde A, Gispert M, Faucitano L, Alonso P, Manteca X, Diestre A (2001) Effects of the stunning procedure and the halothane genotype on meat quality and incidence of haemorrhages in pigs. Meat Sci 58:313–319 von Borell E, Langbein J, Després G, Hansen S, Leterrier C, Marchant-Forde J, Marchant-Ford R, Minero M, Mohr E, Prunier A, Valance D, Veissier I (2007) Heart rate variability as a measure of autonomic regulation of cardiac activity for assessing stress and welfare in farm animals – a review. Physiol Behav 92:293–316. https://doi.org/10.1016/j.physbeh.2007.01.007 von Holst D (1986) Vegetative and somatic components of tree shrews’ behaviour. J Auton Nerv Syst (Suppl):657–670 Vukelic S, Stojadinovic O, Pastar I, Rabach M, Krzyzanowska A, Lebrun E, Davis SC, Resnik S, Brem H, Tomic-Canic M (2011) Cortisol synthesis in epidermis is induced by IL-1 and tissue injury. J Biol Chem 286:10265–10275. https://doi.org/10.1074/jbc.M110.188268 Wagner V, Klein J, Hanich J, Shah M, Menninghaus W, Jacobsen T (2016) Anger framed: a field study on emotion, pleasure, and art. Psychol Aesthet Creat Arts 10:134–146. https://doi.org/10. 1037/aca0000029 Walker KA, Mellish JE, Weary DM (2011) Effects of hot-iron branding on heart rate, breathing rate and behaviour of anaesthetised Steller Ssea lions. Vet Rec 169:363–368. https://doi.org/10. 1136/vr.d4911 Wemelsfelder F, van Putten G (1985) Behaviour as a possible indicator for pain in piglets, I.V.O. Report B–260. Institut voor Veeteelkundig Onderzoek, Zeist

Chapter 6

Assessing Welfare: Long-Term Responses

Abstract This chapter provides an account of the responses of animals to long-term disturbances and positive experiences. Measures of good welfare may be direct or may involve experimental investigation such as that of cognitive bias. Qualitative behavioural assessment can sometimes be useful but, as explained, should be used with caution. Methods for assessing welfare discussed include those of: reproduction, life expectancy, growth, heart and blood, immune system, body structure and injury, disease, brain, and behaviour. Measures of depression in humans and non-humans are described. Keywords Welfare assessment · Depression · Cognitive bias · Immunosuppression · Brain measures

Time is an important factor in welfare evaluation as weeks or months of severe problems are obviously worse than minutes or hours (see Chap. 5 and Fig. 5.3). In biological considerations of stress this difference is important because animals use different coping methods when problem situations are prolonged rather than brief. Persistent problems are also often the major causes for concern when we are judging the welfare of people or domestic animals. However, many decisions in life by humans and other species are taken in order to promote good welfare. When people are planning their lives, most opt, if possible, for an environment where they predict a high average level of positive aspects. They also aim for a low risk of major problems but many are willing to tolerate some short-term negative aspects. As explained in Chap. 2, many other sentient animals predict and plan for the future, hence aiming for the positive is not solely a human strategy. Using complex brain mechanisms to organise life so as to maximise good welfare in the long-term and to be able to react appropriately to problems when they arise, is a key part of biological function for sentient animals. If we are assessing the welfare of people or of other animals when problems or positive aspects are prolonged, it is necessary to measure a range of variables. Some of the measures of negative effects give information about actual or expected reduction in biological fitness and hence indicate stress. Others may or may not © Springer Nature Switzerland AG 2019 D. M. Broom, K. G. Johnson, Stress and Animal Welfare, Animal Welfare 19, https://doi.org/10.1007/978-3-030-32153-6_6

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indicate long-term adversity but are measures of the difficulty an individual has in coping with its environment. These measures overlap with some of those for shortterm problems described in Chap. 5, but because individuals adapt relatively rapidly to most short-term problems, different sets of measures are required for assessing short-term and long-term problems. The first sections in this chapter concern how to assess good welfare. Measurement of the responses of animals to long-term welfare problems where there is clear reduction in individual fitness, are then considered. These affect reproduction and survival, include some of the signs of poor welfare that are most obvious to the lay person and provide definitive evidence that the individual is stressed. The subsequent sections refer to measures that may or may not indicate stress but do indicate poor welfare.

6.1

Direct Measures of Good Welfare

When people are asked about their welfare, they may provide accurate information, or may say what they believe to be true, or may lie. It is difficult for the person asking the question, perhaps a psychiatrist or a researcher, to know how reliable the answer is. In some situations, more objective observations of the subject are possible. However, frequently no attempt is made by those studying humans to use objective measures of the quality of those used by animal welfare scientists. Whilst checks of methodology are sometimes made, the methodology in wide usage should be reconsidered. Most indicators of good welfare of human and non-human subjects are behaviours, but care should be taken in interpreting these. For example, smiling in humans, tail-wagging in dogs and purring in cats are all behaviours that can indicate more than one motivational state in the animals, and that may or may not mean that the welfare of the individual is good at that time (Broom and Fraser 2015). Observations of behaviour with some detail of its context are needed before good welfare can be identified and assessed. In an attempt to identify conditions that result in good welfare for hens, Edgar et al. (2013) asked animal welfare scientists to consider the evidence and specify what would lead to good welfare. These scientists would have been using information about the needs of hens, about whether or not these needs were being met, and about the whole spectrum of welfare measurements. Successful coping was suggested by Spruijt et al. (2001) to involve a balance between factors with a negative impact and reward systems. They proposed that good welfare would be indicated by showing anticipatory behaviour when a reward is imminent. Anticipatory behaviour occurred when rats knew from previous experience that they were about to be transferred from a barren cage to an enriched cage or to one where there would be sexual contact (van der Harst et al. 2003a). The amount of anticipatory behaviour was greater for rats from a very barren cage than for rats from an enriched cage (van der Harst et al. 2003b). The rats from the very barren cage were not apathetic and, at the time of anticipation, their welfare was

6.2 Cognitive Bias and Other Indirect Measures of Good Welfare

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better than when they did not anticipate the reward. The anticipatory behaviour did not allow evaluation of welfare in relation to housing condition but the reward was relatively greater after living in more barren conditions than when living in enriched conditions. It is clear that anticipatory behaviour is an indicator of good welfare over a certain time scale but must be interpreted carefully. Humans anticipating positive stimuli increased positive emotions and reduced impact of negative stimuli (Monfort et al. 2015). Good welfare is known to be associated with some physiological changes in the brain (Carter 2001; Broom and Zanella 2004). When people were shown happy pictures there was an increase in magnetic resonance imaging (MRI) activity on one side of the frontal area of the cerebral cortex, and amygdala activity dropped. A set of regions was found in which there was activity during sad, but not during neutral or cheerful, situations. As mentioned in Chap. 5 it is also known that oxytocin concentration in the blood is higher during some pleasurable events. One of such events is nursing the young in a female mammal. In this situation, oxytocin is not only associated with the let-down of milk but leads to a feeling of pleasure as well. It has the latter effect in other situations too. Oxytocin is synthesized in the paraventricular nucleus (PVN) of the hypothalamus and in the supraoptic nucleus. It binds to receptors that regulate HPA axis activity and increase in oxytocin is associated with: decrease in ACTH, glucocorticoids and social stress, and increases in lymphocyte proliferation, brain GABA concentration and cardiac vagal tone (Carter and Altemus 1997; Redwine et al. 2001; Smith and Wang 2012; Cardoso et al. 2014).

6.2

Cognitive Bias and Other Indirect Measures of Good Welfare

When an individual has a strong preference for a resource, it is likely that the availability of that resource will lead to good welfare. This area of research is considered in Chap. 7. When a situation is evaluated, there will often be some degree of ambiguity in the information available. In some circumstances the same sensory input could indicate that there is a likely consequence that could be either positive or negative. As Mendl et al. (2009) put it, should an individual interpret a rustle in the grass as danger or as food? It is possible that an animal’s interpretation of an ambiguous situation may be altered by its emotional state. Individuals whose welfare is good are presumed to be more likely to interpret ambiguous stimuli as positive whilst those in negative states would be more likely to respond as if the negative outcome will occur. The influence of affect on a range of cognitive processes including attention, memory and judgement has been called cognitive bias, or more accurately, cognitive affective bias (Paul et al. 2005; Mendl et al. 2009). After the individual has received training to approach a more positive or more negative reinforcer, the response to an

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intermediate position is assessed. Harding et al. (2004) presented higher or lower pitched tones to rats and then gave a tone of intermediate pitch. Rats from a richer environment were more likely to respond to this tone as positive than were rats from an impoverished environment. Studies of a range of species of animals have followed this work. Mendl et al. (2010) found that rescue shelter dogs with a higher separation score were more likely to react to an ambiguous position as negative. Doyle et al. (2011) trained sheep to respond to a positive and a negative bucket position. If they were shown a bucket in an ambiguous position between the positive and negative positions, they did not go to it after being stressed. Pigs from enriched environments showed more positive cognitive bias than those from barren environments (Douglas et al. 2012). Cognitive affective bias studies are reviewed by Mendl et al. (2009) and their significance and usefulness for evaluating welfare is also discussed by Broom (2010, 2014). Cognitive bias is a potentially valuable indicator of affect and of welfare. However, the choice made in such a test could be altered according to the strategies adopted by individuals in life as a whole, and in the test situation. What are the possible strategies, which of these are shown, and what will be the consequences of showing one or other strategy? Once this is ascertained, the probability that the supposed optimistic or pessimistic response will be shown can be calculated and compared with the data obtained. Since the affect, or the welfare, may not be reliably indicated by cognitive bias studies alone. A combination of studies is needed to increase the accuracy with which cognitive bias reveals feelings or allows assessment of welfare.

6.3

Qualitative Behavioural Assessment

Each of the direct measures of animal welfare gives information about an aspect of the attempts to cope with the environment but an understanding of one aspect does not necessarily allow an appreciation of welfare in general. If a range of coping attempts is assessed, using several measures, the welfare assessment is better. However, these measures may not provide adequate indications of the positive and negative feelings of the individual. In an attempt to address this problem, Wemelsfelder et al. (2000) advocated the use of human abilities to describe what they perceive about the animal’s welfare, referred to as qualitative behavioural assessment (QBA). Those who are very familiar with such animals sometimes have considerable ability to do this. This QBA methodology has parallels with the scoring of human or other temperament or personality; a substantial literature exists on this subject, most of which could be criticised on the basis of observer bias. In the course of QBA, observers are asked to consider all aspects of the animals, to observe animal behaviour and to try to evaluate the animals’ feelings. The ability of people to produce a whole animal assessment of welfare is exploited. As Wemelsfelder et al. (2000) and Fraser (2008) emphasise, it is important for observers to know enough about the behaviour of the species observed to avoid misinterpretation, e.g. of a chimpanzee’s grin as friendly when it actually indicates threat.

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The use of QBA is valuable is where quantitative welfare indicators are difficult to use. It is sometimes particularly difficult to assess welfare when the welfare of the animals is good. Human observers familiar with such animals may observe subtle changes in the animals and incorporate these in their assessment. (Wemelsfelder et al. 2012) asked farmers, veterinarians and those in animal protection groups to use QBA to assess the welfare of pigs from video clips. There was substantial agreement between these people from different backgrounds. Rutherford et al. (2012) found that pigs disturbed by being put in a novel situation were scored as more positive emotionally if treated with the neuroleptic, tranquilising drug azaperone. The 12 observers, blind to the treatment, scored the animals by making observations of behaviour, especially those involving emotional components. The responses of the pigs were indicated by the analysis to have two expressive dimensions. The observers were able to make a useful evaluation using QBA but it would also be of interest to ascertain exactly what the observers were observing and to develop these measures, rather than using a more vague evaluation. During QBA use, observers may not use the same observations, or the same weighting of observations, and hence that there could be poor inter-observer reliability. Whilst all scientific measurement is subject to some degree of lack of interobserver reliability, this risk can be higher when QBA is used than when objective welfare measures are used. However, there are several published studies in which carefully planned training led to good inter-observer reliability during QBA (e.g. Stockman et al. 2011). As discussed by Broom and Fraser (2015), an important possible problem when QBA is used, is that the observers could have a bias in their evaluation because of their expectations about animal welfare in the living conditions or after the treatment. Wemelsfelder et al. (2009) found that some components of QBA of pigs were modified by the perceptions of observers about the environment of the animals. This is not surprising because, in most studies, it is not possible for the observer to be entirely blind to the environment and treatment of the animals. Tuyttens et al. (2014) asked veterinary students to evaluate a set of videos of animals. They found that the QBA scoring was more positive when the students had been told that the conditions of the animals were good than when they had been told that the conditions were less good. The possibility of bias must always be a problem with QBA so the value of QBA must be questioned in studies where there is a potential for bias. All scientific measurements are subject to being altered by observer bias during the process and Tuyttens et al. (2014) also found some effect of the observers’ perceptions on other welfare measures. However, most measurements used as animal welfare indicators are likely to be altered only slightly by any bias. The fact that QBA could be altered greatly by bias but might not be altered at all makes it questionable to use. It is not clear that methods for QBA use can be developed to prevent the influence of any bias. A number of publications, e.g. Stockman et al. (2011b), have reported correlations between QBA and other widely-used measures. However, using observations of video clips of dairy cows by eight experienced and by ten inexperienced observers, Bokkers et al. (2012) found no correlation between QBA results and

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other welfare measures. Similarly, in a comparison of QBA and a range of measures of welfare recommended for dairy cattle by Welfare Quality (Keeling 2009), there was no meaningful pattern of relationship between these (Andreasen et al. 2013). The lack of correlation could be because the QBA evaluation gives information about the animals that is different from that obtained by other means. However, if a wide enough range of welfare measures is used, there should be correlations between some of these and the output of QBA. Wemelsfelder et al. (2009, 2012) advocate combining QBA with other welfare measures. The use of QBA as a stand-alone measure is inadvisable and QBA results are not valid if there is a potential for bias or if inter-observer reliability has not been checked. QBA is valuable in three circumstances: (i) in studies where non-scientists are asked to evaluate the welfare of animals: (ii) in preliminary studies of work where welfare assessment is proposed; and (iii) as a supplement to well-established welfare indicators where QBA produces information that they cannot produce and provided that bias by observers can be eliminated. The best procedure for scientific studies of welfare if preliminary QBA studies are carried out, is to identify the observations made during QBA to develop new quantitative welfare indicators and to combine the use of these with established indicators. It would be better for animal welfare scientists to limit the use of QBA to the three situations described above.

6.4

Reduced Reproductive Success

If an individual is so deprived of food or disturbed by its environment that it is unable to reproduce when given the opportunity, its welfare is poorer than that of another individual that can reproduce. In humans, in wild animals, and in domestic animals neglected by those responsible for them, starvation can delay or prevent reproduction. Even when the food supply is adequate, an animal may be so unsettled by its living conditions that it does not reproduce when given the opportunity. Many species of animals are not able to breed in the poor conditions in some zoos, and some species rarely breed in any zoo. This is a clear indication of poor welfare in those animals. Relative reproductive performance can be used to compare the welfare of animals in different conditions, although in practice conditions have to be very poor before reproduction is affected in most species, including humans. Body resources are often apportioned to reproductive effort even at the expense of basic body maintenance. Farm animals, having been selected for many generations for good reproductive performance, commonly maintain normal reproductive performance even under difficult conditions where other indicators show that their welfare is very poor. In farm animals, a failure to reproduce or a delay in reproduction can be a consequence of a pathogen, an inadequate diet or a behavioural abnormality resulting from housing and management inadequacy. Cows, mares, ewes and sows may be disturbed by the proximity of dominant individuals, or may be attacked by them, and so fail to show normal behavioural oestrus (Broom and Fraser 2015). This

6.5 Reduced Life Expectancy

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results in failure to breed and hence reduces fitness. Although most frequently seen in subordinate individuals or animals subjected to frequent changes in social group, lack of behavioural oestrus may also be caused by excessive noise, temperatures above 30  C and extreme weather conditions (Hurnik 1987). Male farm animals may fail to show appropriate sexual behaviour, and indeed may be unable to show it, in circumstances that create apprehension (Broom and Fraser 2015). Some males show an interest in a potential sexual partner, but are disoriented during copulation or fail to achieve intromission if they have been deprived of suitable social contact during their early lives (Beilharz 1985; Price 1985). Females can also have poor reproductive skills owing to disturbances or inadequacies in their early experience. Reproductive problems are one of the clearest indicators of poor welfare in dairy cows that have high milk yields (Oltenacu and Broom 2010). The genetic selection, feeding and management of these animals has such a negative effect on their metabolic function that they often fail to reproduce, or have high levels of mastitis or lameness. A cow that cannot reproduce is clearly failing to cope with her environment, therefore reduced reproductive performance of modern dairy breeds is a welfare concern. Many of the reproductive problems associated with highly productive dairy cows result from disease, such as uterine infections or other disorders (Sheldon et al. 2008) or from metabolic stress associated with milk production. In the United States, the calving interval increased from 14.5 months and number of inseminations per conception from 2.0 to >3.5 from 1980 to 2000 in 143 commercial herds (Lucy 2001). The pregnancy rate to first service declined by 0.5% per year between 1975 and 1997 (Beam and Butler 1999). In the UK the pregnancy rate to first service decreased over a similar period by 1% per year. Behaviour plays a critical role in the declining reproductive performance of genetically selected high-producing cows. Dransfield et al. (1998) showed that a higher proportion of cows with production above herd average exhibited only low intensity and short duration oestrus relative to lower-producing cows. Farm staff are more likely to fail to see oestrus signs that are brief and short. Lopez et al. (2004) reported an unfavourable association between milk production and oestrus behaviour with shorter oestrus periods in high relative to low producing cows. Emanuelson and Oltenacu (1998) found an extended interval to first breeding and to conception in herds with poorer oestrus detection. The decline in fertility also has economic consequences and several studies reported increasing reproductive costs for dairy cattle (Lucy 2001).

6.5

Reduced Life Expectancy

If the life expectancy of animals in one set of conditions is 2 years whilst that in another is 6 years, we could conclude that the welfare is poorer in the first case than in the second. This general idea has been presented by Hurnik and Lehman (1988) and Broom (1991). The majority of people regard those domestic animals living at a

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higher rate for a shorter time as being the more stressed, particularly when conditions are imposed rather than being chosen by the animals. Reduced life expectancy due to sub-optimal living conditions can occur in the wild, for example in trout (Pickering 1989). It is also known to occur when inappropriate animals are kept as pets or in zoos. For example, several small species of tortoise which can live for longer than 20 years in the wild have an average life expectancy of only 2 years in captivity (Warwick 1990). Wild-caught birds, whose mortality rate between catching and sale is 90% (EFSA 2006), often have short life expectancies in captivity, and primates kept as pets seldom live as long as those living in stable groups in the wild. Perhaps the best known examples of animals that do not live long in zoo conditions are cetaceans: whales and dolphins kept in pools no larger than human swimming pools live much shorter lives than those kept in larger marine enclosures or living in the wild (Brando et al. 2018). In relation to measurement of life expectancy, the welfare of farm animals is effectively measured by ‘potential’ rather than ‘real’ duration of life, since these animals are usually killed for human consumption before they die naturally. Dairy cows are usually kept by farmers until they cease to give a high milk yield, after which they are culled. Others are culled because they fail to become pregnant, or because they are lame or have some other disability. Some of these factors are similar to those that would result in premature death in the wild, whilst others, such as poor ability to conceive and rear young, impair biological fitness. Early culling or death for such reasons on a particular farm indicates conditions of poorer welfare than on another farm managed so that the animals live longer with less necessity for culling. Many farmers have reported that the average age to which their dairy cows live now is less than that of cows in earlier years. They link this with the high production rates of modern dairy cows. Cows fed a high protein diet and selected for high feedconversion efficiency over many generations have a high metabolic rate and, on average, their longevity is reduced. Evidence for such a change in dairy cows is indicated by the number of cows in Denmark being sent to rendering plants, which normally occurs after they have died on the farm. Using such data, Agger (1983) reported that the life expectancy of dairy cows was halved between 1960 and 1982. This trend has continued as milk production rates go on increasing. Wider use of bovine somatotrophin to increase milk production, in the few countries where its use is permitted, has accelerated the fall in life expectancy. Poor reproductive performance and severe lameness and mastitis has led to premature culling and decreased longevity of dairy cows. The association between the declines in fertility, reflected in increased calving interval, and decrease in longevity, measured by the proportion of cows still alive at 48 months of age in Holstein cows in the North-East US from 1957 to 2002 are shown in Fig. 6.1. Reduced longevity is also reflected in the mean number of calves produced during lifetime by Holstein dairy cows in Austria, which decreased by 10% over 10 years up to 2007 (Knaus 2009). In one analysis, the optimal profitability in dairy production was calculated to occur if the cows lived for six lactations (Essl 1998) but longer productive lives occur in other situations.

6.6 Weight, Growth and Body Condition

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85

16

15

75 70

14

65 60

13

55 50

Calving Interval (mo)

Alive at 48 mo (%)

80

12

45 1961 1966 1971 1976 1981 1986 1991 1996 2001 % alive at 48 mo

Calving interval

Fig. 6.1 Average calving interval and proportion of cows alive at 48 months of age over time for Holstein cows in the North-Eastern United States (from Oltenacu and Algers 2005)

6.6

Weight, Growth and Body Condition

An early sign that an individual might not reproduce, or is ill and likely to live for a shorter time, is an interruption to its growth or, in grown animals, a loss of weight. In both wild animals brought into captivity and in domestic animals, weight loss in adults or lack of weight gain in juveniles usually indicates severe conditions for the animal. Measures of weight change should take account of any change that results from gut emptying. Capture and handling led to weight loss in wild wood mice (McClaren et al. 2004) so there would be some long-term effects. The tree shrews studied by von Holst (1986) lost weight and died if they were confined with an individual that had beaten them in a fight and rats that consistently lost fights lost weight. In both cases the animals continued to feed, so presumably differences in metabolic rate associated with increased adrenal activity caused the weight loss. Daily exposure to cold, forced exercise, foot-shock and immobilisation have led to reduced body weight in rats. Rats subjected to various laboratory procedures, such as movement to a new room, change from a pelleted to a powdered diet, change from groups of three to single housing, oral dosing with water and daily cage change over a period of 44 days showed a net loss in weight, whilst undisturbed controls gained 9% in body weight over the same period (Steinberg and Watson 1960). Failure to have a steady weight gain is an indicator of poor welfare in caged animals such as guinea pigs (Sachser et al. 2007). Housing in a more complex environment resulted in a greater weight gain by mice and hamsters, even though these animals were more active than mice kept in bare cages (Chamove 1989). Instability of group, large size of group, frequent movement to a new social group and very crowded conditions all reduced weight gain in rats and quail (Mormède et al. 1990).

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Weight gain is monitored in many young farm animals. Efforts are made to minimise any reduction in growth rate, especially at weaning when there may be changes in location and social companions, as well as in diet. Piglets are commonly separated from their mothers at 3–5 weeks, well before natural weaning at 9–17 weeks. When piglets are put into a new pen and mixed with strangers there is an increase in fighting and a drop in food intake, so weight may drop or fail to increase at the previous rate, often for as long as a week. Lack of food, inappropriate food and some pathologies can lead to emaciation. If people who are responsible for animals fail to feed or manage them properly, the body condition is often good evidence for this. Body condition scores are available for humans and a range of other species and are welfare indicators. As explained by Broom and Fraser (2015), starvation starts when the individual starts to metabolise functional tissues. If muscle that is needed for effective body functioning is metabolised, the welfare is poor because there is less ability to cope with the environment. There will also be changes in body condition so that the individual becomes thin. If functional body tissues, other than specially adapted reserve tissues such as glycogen in the liver, or body fat, are being metabolised because energy levels from food are absent or are too low, the animal is starving. Hence starvation is the state of an individual with a shortage of nutrients or energy such that it starts to metabolise functional tissues rather than food reserves. Starvation refers to a metabolic change associated with overall energy availability deficit. There may also be metabolic changes associated with the lack of a specific nutrient such as a mineral, vitamin or essential amino acid. As Hogan and Phillips (2008) point out, food reserves such as adipose tissue also have other functions in the body so it is not always clear whether they are reserves or functional but the principle of this definition is helpful. If muscle is being used up because of lack of energy from ingested nutrients, for example in individuals provided with no food or in many milking cows, the animal is beginning to starve.

6.7

Cardiovascular and Blood Measures

Heart rate is a useful measure of welfare in the short term, but of little value when comparing long-term conditions, such as the quality of housing. However, long-term conditions can affect changes in heart rate or blood pressure which occur in test situations. Blood pressure measurements must be interpreted carefully, since taking the measurement can have a negative effect on the individual which alters the measurement required. After a study in which baboons were trained to hold out forelimbs for blood pressure measurement using an oscillometric monitor (Turkhan et al. 1989), many researchers use similar methods. Some implanted transducers are not major long-term impositions on the animal but do require surgery for implantation. Cuffs on the forearm of a primate, the ear of a rabbit or the tail of a rodent are non-invasive

6.8 Adrenal Axes

141

and seem to be practicable methods of blood pressure measurement, provided that the individual is not disturbed by the restriction of movement. Rats have a preference to rest on solid floors rather than perforated floors and for bedding rather than no bedding (Chap. 7). Their blood pressure was lower on solid floors with bedding than when they were on a perforated floor (Krohn et al. 2003). Prolonged increases in blood pressure occurred after frequent fights between mice over a period of months (Henry et al. 1975) and in rats or monkeys following daily exposure to noise, flashing lights, cage oscillation, daily electric shock or daily immobilisation. These experiments, which must have been particularly unpleasant for the animals, suggest that blood pressure changes could be useful in the assessment of welfare. However a complication is that blood pressure is different according to position in social structure of a group. The earlier methodologies were of limited use in welfare assessment because individuals were affected too much by the measurement of blood pressure. Implantable devices make it possible to monitor blood pressure telemetrically (Cong et al. 2009), as well as body temperature and heart rate.

6.8 6.8.1

Adrenal Axes Sympathetic Nervous System and Adrenal Medulla

Activation of the adrenal medulla is an effective response to short-term problems. Measurements of its activity are seldom of much use as indicators when the problem is long-term. The catecholamine breakdown product vanillylmandelic acid (VMA) is higher in the saliva of people suffering from hypertension (Zielinsky 1989), and is worth exploring further as a welfare indicator. In general, for long-term welfare problems resulting in adrenal medulla activity, it is difficult to get useful information about live animals, and the most useful measurements are those made on the organ itself after death.

6.8.2

Hypothalamic-Pituitary-Adrenal Cortex

The sequence of events in the production of glucocorticoids is described in Chap. 2 and the use of CRH, ACTH, cortisol and corticosterone as indicators of short-term welfare problems is described in Chap. 5. The rapid adaptation of the HPA axis glucocorticoid response has the result that cortisol and corticosterone are not generally suitable as indicators of long-term welfare problems (Broom 2017). Depressed people do not have higher plasma cortisol concentrations than non-depressed people and many depressed people have lower cortisol responses to potentially disturbing stimuli than non-depressed people (Burke et al. 2005). At one time, it appeared that the results of adrenal cortex function tests would give information about the longer

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term but it is now clear that these too change within a small number of hours. If there may have been a number of episodes that would have elicited glucocorticoid production during 1 or 2 days, HPA axis activity can be assessed by measuring glucocorticoid metabolites in faeces. The time for the excreted substances to get into the faeces must be taken into account, as must the sample location in the stool as cortisol enters from the gut wall so may be at higher concentration at the edges of the stool. Indeed, careful validation for each species is necessary in order to understand the information available from measurements of faecal cortisol (Touma and Palme 2005; Palme 2012). In the scientific literature, some publications assessing long-term housing conditions have stated that a particular condition does not adversely affect welfare because there is no increase in glucocorticoids in animals kept in this condition. Such statements are scientifically unsound as there are many examples of long-term conditions in which welfare is very poor but glucocorticoid concentrations are not increased at all, for example human depression. The other sections in this chapter include several measures of changes that are a consequence of repeated adrenal cortex activity, each of which led to brief increases in glucocorticoids, but with changes in immune system and other function which are measures of long-term problems. Some tests of adrenal activity involve looking at the size of the adrenal glands post mortem.

6.9

Measures of Immune System Function

Animals encountering difficult conditions often show some degree of immunosuppression (Kelley 1985). Ashley (2006) gives many exmples of stressful situations leading to immunosuppression in farmed fish. Research documenting this point has centred on humans, laboratory animals and farm animals but it is clear in all species that susceptibility to disease can be increased by a variety of biological disturbances. A wide range of examples of the effects of negative environmental conditions on bacterial diseases and viral diseases in farm animals is presented by Broom and Kirkden (2004). The differential effects of glucocorticoids upon different leucocyte populations explain the observation that stressors can increase the susceptibility of chickens to some pathogens (Gross 1976). Not only do glucocorticoids reduce the number of circulating lymphocytes, they also suppress the activity of B cells and cytotoxic T cells, for example by decreasing the synthesis of interleukins, by interacting with macrophages and T- helper cells. Glucocorticoids are not the only means by which stressors reduce immunocompetence (Yang and Glaser 2000). Catecholamines suppress the cell-mediated immune response. The majority of experimental studies to date have reported that poor welfare resulting from difficult conditions or treatment increase susceptibility to pathogens (Biondi and Zannino 1997). However, good welfare of animals generally leads to better immunocompetence. The production of β-endorphin in the anterior pituitary gland and the release of vasopressin and

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143

oxytocin from the neurohypophysis enhance T-cell proliferation and stimulate T-helper cells. The aim of this section is to consider the extent to which measures of immune system function can be used as indicators of poor welfare in the long term.

6.9.1

Measuring White Cell Numbers

One obvious way to discover effects of difficult conditions on an animal’s ability to combat disease is to count the white cells in samples of blood or other body fluids. Changes in total white cell numbers, however, occur in various circumstances, especially when there is a pathogen attack. White cell counts in milk, for example, change when groups of cows are mixed but such results are not obtained consistently and are not easy to interpret. Prenatal and postnatal exposure of human infants to polychlorinated biphenyls or DDE increased counts of lymphocytes and monocytes but decreased counts of eosinophils (Glynn et al. 2008). A refinement of total white cell counting is to calculate ratios between one kind of white cell and another. However, longer-term problems for the animals did not have consistent effects on such ratios. Some of the results of counting numbers of particular subsets of lymphocytes indicate that such values can be useful. Levels of T-helper and T-suppressor lymphocytes in human subjects were reduced when the subjects took examinations and in the most anxious individuals (Glaser et al. 1985). Some studies of immobilised rats showed that this extreme treatment led to lower levels of total T-lymphocytes, T-helper lymphocytes and T-suppressor lymphocytes (Steplewski and Vogel 1986) but other extreme treatments did not have such effects.

6.9.2

Antibody Production

Antibodies are immunoglobulins of four types known as IgA, IgE, IgG and IgM which are produced by B lymphocytes. Immunoglobulins can be measured in plasma, saliva or colostrum. Many of the earlier assays of humoral immune responsiveness measured the production of specific antibodies following an experimental challenge with an antigen injected either during exposure to the stressor, shortly before, or shortly afterwards. Sometimes, the primary antibody response is assessed, by estimating the amount of antibody present in blood samples obtained five or more days following the injection. One technique is agglutination, in which blood serum is added to a suspension of antigen particles and the level of clumping or agglutination which occurs reveals the concentration of the antibody. Alternatively, the secondary antibody response may be assessed, either by administering a second antigen challenge to the animal and estimating the number of antibodies in blood samples obtained subsequently, or by means of a plaque-forming cell assay. The plaqueforming cell assay employs foreign red blood cells (erythrocytes) as the antigen. Five

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or more days following injection of the erythrocytes, lymphocytes are taken from the spleen and incubated, with the erythrocyte antigen and complement, between two microscope slides. Complement is the name given to a series of enzymes that destroy cells presenting antigen bound to antibody. A plaque, clear of erythrocytes, forms around each B cell, its diameter being proportional to the level of antibody synthesis (Broom and Kirkden 2004). Total immunoglobulin levels have been found to be of little use in welfare assessment, although 8 days after injecting tethered and group-housed sows with Escherichia coli K99, Barnett et al. (1987) found lower IgG and IgM levels, positively correlated with previous higher plasma glucocorticoid levels, in the tethered sows than in the group-housed sows. Faecal IgA was measured in cats by Gourkow et al. (2014) after admission to an animal shelter. Emotionally disturbed cats, as assessed from behaviour measurements, had lower S-IgA concentrations than calmer cats. This methodology may well be useful to assess welfare in other situations. The production of specific antibodies following an experimental challenge with an antigen can give valuable information about welfare. Animals can be detrimentally affected by a housing system or treatment in such a way that they are less able to produce antibodies following antigen challenge. Metz and Oosterlee (1981) found that the antibody response to the injection of sheep’s red blood cells was less in recently tethered than in untethered sows. In a similar experiment, antibody production following injection of the bacteriophage X174 was considerably depressed in 6-month-old squirrel monkeys separated from their mothers compared with those not separated from their mothers (Coe et al. 1988). When sows were challenged with tetanus toxoid or atrophic rhinitis vaccine they produced antibodies to these in blood and colostrum a few days later. As shown in Fig. 6.2, sows which showed a greater response to ACTH challenge produced lower levels of antibodies following antigen challenge, suggesting that activation of the hypothalamic-pituitary system was suppressing antibody response (Zanella et al. 1991a, b). The plaque-forming cell assay (Esterling and Rabin 1987) is carried out with lymphocytes from the spleen of an animal previously sensitized to foreign red blood cells. Spleen samples would normally be taken from an animal after death and plaques allowed to form when the lymphocytes are incubated with the red blood cells in the presence of complement. Rabin et al. (1987) found that male mice housed five to a cage showed a lower plaque-forming response than those kept individually, and hence suggested that there was an association between the increased fighting which occurs in male mice crowded in a cage and reduced T-cell function. Females, which usually do not fight, did not show this difference.

6.9.3

T-Lymphocyte Function

Antibody production is affected by the lymphokines produced by one of the forms of T-lymphocyte, the T-helper cells, so measurement of reduction in antibody levels is

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145

Fig. 6.2 The amount of tetanus antibody in the colostrum of sows after a challenge with the tetanus toxoid is measured by the extent to which the sample can be diluted and still show detectable antibody. Sows which showed a smaller cortisol response to ACTH challenge had higher antibody levels (Zanella et al. 1991b)

an indirect way of ascertaining the difficulty an animal has in coping with its environment. T-lymphocytes can act directly on foreign antigens and their action is affected by an animal’s success in coping, so measurement of T-cell activity can be a useful indicator of how poor welfare is. However, interpretation of such measurements requires care, as T-cell proliferation and activity can be induced by various factors, especially pathogen presence. Assays of cell-mediated immune responsiveness measure the activity of cytotoxic T-cells. They can be classified into in vitro and in vivo techniques. In vitro techniques include measures of the proliferation of T cells, and of their production of cytokines, in response to antigen. For these tests, blood samples are obtained either during exposure to the stressor, shortly before, or shortly afterwards. In order to measure T-cell proliferation, the cells are mixed with antigen and incubated, sometimes in the presence of a mitogen, such as phytohaemagglutinin (PHA), concanavalin A (conA) or pokeweed mitogen (PWM), which stimulates proliferation. The rate of proliferation is estimated by measuring the uptake of radio-labelled thymidine, which dividing cells incorporate into new DNA. In order to measure the production of cytokines, blood samples are incubated with antigen and the resulting concentrations of cytokines are measured using a standard assay, such as the enzyme-linked immunosorbent assay (ELISA). A third in vitro technique estimates T cell cytotoxicity following exposure to antigen. In this case, the animal is injected with the antigen around the time of exposure to the stressor and blood samples are obtained later. T cells are then incubated with radio-labelled cells presenting the antigen.

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Cytotoxic action of the T cells releases the radio-label into solution, so the final concentration of the label yields an estimate of T cell activity. In vivo techniques are quite different. They measure a cell-mediated inflammatory response to antigen challenge on or below the skin surface, known as a delayed hypersensitivity reaction because it develops gradually over the course of several days. The inflammation is caused primarily by basophils, which are attracted to the site by T cells. An inflammatory response to most antigens only occurs when an animal has had previous exposure to them, in other words reactions of this kind are generally secondary cell-mediated immune responses. The antigen must therefore be injected intradermally on two occasions, the inflammatory response following the second injection being assessed by a measurement of skin thickness. However, certain chemical agents, including dinitrochlorobenzene (DNCB) and PHA, elicit a delayed hypersensitivity-like reaction on the first exposure, known as a contact sensitivity response. This allergic cell-mediated response is peculiar, in that it does not require previous sensitisation to an antigen. PHA is injected intradermally, while DNCB is painted onto the skin surface. The inflammatory response is assessed by measuring skin thickness. Other measure is natural killer (NK) cell activity and production of lymphokines such as interleukin-2. An example of a study measuring fluorescence following flow cytometry is the suppression of lymphocyte proliferation following conA or PWM stimulation in horses following transport (Padolino et al. 2017). Measures such as these have been found to be affected in rodents and monkeys by high noise levels, inescapable shock, high levels of crowding, social deprivation, infant separation from mother and in humans by depression and bereavement. Depression in humans is associated with an array of effects on the immune system including inflammatory activation of the peripheral immune systems and inactivation of the adaptive immune system (Leday et al. 2018). Indeed, environmental impacts that caused frequent systemic inflammation in women increased the likelihood that depression would develop (Bell et al. 2017) so these impacts are considered to be stressful. Information of this kind led Pariante (2016) to argue that distinctions among brain, mind and body are not useful (see also Broom 2003).

6.9.4

Other Body Defences

Foreign particles and cells which get into the body are removed by the phagocytic activity of neutrophils or monocytes. The effects of environmental conditions on animals have been assessed by measuring the ability of macrophages to kill leukaemia cells or ingest bacteria, yeasts or other particles. The functioning of the complement system, which facilitates the breakdown of foreign cells and the operation of the blood platelet system can also be impaired in an individual that is having difficulty in coping with its environment.

6.10

6.10

Bone Strength, Muscle Strength and Injury

147

Bone Strength, Muscle Strength and Injury

If the environmental impact on an individual is to prevent the development of normal anatomy, physiology and function, that individual is less good at coping with its current and future environment so welfare is poorer than that of a normally functioning individual. Effects on growth, on aspects of physiology and on the immune system have already been discussed. If bone or muscle strength are weak, coping ability is reduced and there is an increased risk of injury. A diet that is inadequate in quantity or in necessary nutrients could cause this. Housing conditions that do not meet the needs of each individual for exercise can also do so. Severely reduced exercise, because of lack of space or a lifestyle without exercise, can result in osteopenia and reduced bone strength. In studies of hens (Knowles and Broom 1990), birds that could not sufficiently exercise their wings and legs because they were housed in battery cages had considerably weaker bones than birds in percheries that could exercise. Similarly, Marchant and Broom (1996) found that sows in stalls had leg bones only 65% as strong as sows in group-housing systems. The actual weakness of bones means that the animals are coping less well with their environment, so welfare is poorer in the confined housing. If such an animal’s bones are broken there will be considerable pain and the welfare will be worse. Osteopenia can also be a consequence of too little exercise in humans. Astronauts in zero gravity have to undertake programmes of exercise in order to avoid bone loss. People who are vulnerable to osteopenia, sometimes because of hormonal conditions after menopause can lose bone and increase risk of bone breakage unless they take sufficient exercise. Bone weakness is always a welfare indicator and muscle weakness can be in some circumstances. Injuries cause poor welfare because of their impact on ability to carry out essential activities and because of any associated pain, fear or anxiety. When at risk of predator or conspecific attack, the fear of this attack and anxiety about such events over a longer timescale, may be more important causes of poor welfare than the pain caused by the injury. An injury can prevent adequate access to food and water or shelter from adverse temperature conditions. Injuries cause pain and many other negative effects on welfare. Research comparing welfare in different conditions often requires that an injury scale be developed. Such scales may measure the number and severity of bruises, skin lesions or bone breakages. There is often close overlap with disease measures because of pathology associated with the possible injuries. Pain assessment is described in detail in Chap. 5. Although some pain is of short duration, pain can also be chronic and some measures are appropriate for both. Mutilations, often have long-term negative consequences because of effects on essential behaviours and some involve long-term pain, perhaps because of neuroma formation. Examples in Chap. 5 mainly concern humans, farm and laboratory animals but there are also companion animal mutilations (Broom 2015). In many countries, some dog breeds routinely have parts of their anatomy surgically altered for cosmetic reasons and to comply with breed standards. In some countries, dogs

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may have most of their tail cut off, as in the Corgi, Boxer, Poodle and Rottweiler breeds. Dogs and cats may have their ears cut to make them pointed, their vocal apparatus removed or their teeth, claws and reproductive organs removed. The tail and ears are used in normal communication by dogs and cutting causes pain so there is poor welfare caused at the time of the operation and, additionally, tail-docking can lead to prolonged pain because of neuroma formation (Broom and Fraser 2015). Declawing of cats (onychectomy) has substantial effects on the ability of the cat to defend itself against other cats and to climb, both biologically important abilities, so poor welfare in declawed cats is not only a result of pain. The operation, involves removal of the third phalanx and associated soft tissues, and is painful to the cat even if anaesthetic and analgesic are used during the procedure. There is evidence of chronic pain developing after the procedure (Gaynor 2005).

6.11

Disease Incidence Measures

An enormous body of literature exists on the interrelations between environmental conditions and the consequences of infection by pathogens. As emphasised earlíer, the welfare of diseased individuals is poorer than that of non-diseased individuals, the extent of the effects on welfare depending on how much has to be done to combat the disease, how great is the body damage caused by the pathogen, and how much suffering occurs because of the disease. Responses to disease are important parts of coping systems and hence of welfare (Broom 2006; Hart 2011). When an individual has difficulty coping with its environment, and hence welfare is poor, the likelihood of disease is increased, a key aspect of the one welfare concept. Pasteur reported that chickens whose legs were immersed in cold water became more susceptible to anthrax (Nichol 1974). Damage to normal functioning in cells can occur because the individual is not able to cope with its environment, so is stressed. One example of a change that can occur faster in stressed animals is telomere shortening. This is associated with increased risk of cancer and premature aging and has been reported to occur in humans and other species, e.g. parrots kept in isolation (Aydinonat et al. 2014). Since the impact of disease on welfare is so great, factors that change disease incidence and the evaluation of the extent of the impact of disease on individuals are key aspects of welfare assessment. Changes in disease incidence with animal husbandry were reported by Sainsbury (1974) who pointed out that a gradual increase in chronic infections of poultry occurred when the incidence of intensive production practices was increased. Some disease increase is a consequence of the system whilst others are a result of poor management practices. Sainsbury commented that a poor system could be identified by the amount of antibiotic needed to allow it to function. An illustration of the relation between disease susceptibility and difficulty in coping with environmental conditions comes from studies on chickens. When birds which were strangers were put together they displayed, fought and had increased adrenal cortex activity. After such social mixing had occurred, challenge with

6.12

Brain Measures

149

Mycoplasma gallisepticum, Newcastle disease, Marek’s disease or haemorrhagic enteritis resulted in greater pathogen levels in the body, greater morbidity and greater mortality than in chickens that were not mixed with strangers (Gross and Siegel 1981). Similarly, the mixing of early-weaned pigs from different sources resulted in more Salmonella infections and the mixed pigs were more susceptible than unmixed pigs to tissue invasion by Salmonella, presumably because the experience of mixing was stressful (Callaway et al. 2006). Another example of a link between welfare and disease is shipping fever, also known as pneumonic pasteurellosis. This is a common cause of morbidity and death in calves following transportation and is sometimes responsible for 50% of mortalities in feedlots and 75% of cases of sickness (Edwards 1996). Shipping fever usually occurs within 14 days of transport and can involve fever, dyspnoea, fibrous pneumonia, gastroenteritis and internal haemorrhage (Tarrant and Grandin 2000). Shipping fever is caused primarily by the bacterium Pasteurella haemolytica, or occasionally Pasteurella multocida, but neither is normally pathogenic. Disease arises because its presence is combined with stressful experiences, such as transport, or with other pathogens. Several large-scale field studies have monitored the incidence of mortality from shipping fever in beef calves arriving at North American feedlots. Mixing of animals that are not familiar with one another is an important factor, partly because of stress associated with agonistic interactions, and partly because of increased risk of exposure to pathogens (Ribble et al. 1995). Adverse temperature leading to immunosuppression may play an important role in the development of shipping fever.

6.12

Brain Measures

Changes in the brain associated with good welfare and with stress and poor welfare are discussed in Chap. 2 and, as emphasised in Chaps. 3 and 4, most coping mechanisms are controlled from the brain. Hence, many welfare measures are an indication of brain action. In some circumstances, direct measurements of brain activity are possible. Endogenous opioids such as endorphins, enkephalins and dynorphin are involved in many different body control mechanisms in the brain including the release of prolactin, luteinizing hormone and growth hormone, and in pain perception and reward motivation. ß-endorphin is also secreted into the blood in parallel with ACTH from their mutual precursor pro-opiomelanocortin. Hence treatments which elevate ACTH and glucocorticoid production may also elevate plasma levels of ß-endorphin. Plasma ß-endorphin increases in circumstances such as: surgery in humans (Smith et al. 1985); mulesing, castration and tail-docking operations in sheep (Shutt et al. 1987) and many other actions damaging tissues or otherwise causing lon-term welfare problems. The analgesic action of endogenous opioid peptides has been known since the work of Hughes et al. (1975). Their action can explain that people who lose a limb in battle or who are badly injured in sporting

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competitions report that they were unaware of the injury until sometime after it occurred. The role of endogenous opioids in animals encountering difficult conditions has sometimes been studied by the use of endogenous opioid antagonists which block the receptors in the brain to particular opioids. The relevant brain receptors are mu (μ) receptors for endorphin, delta (δ) receptors for enkephalins and kappa (κ) receptors for dynorphin. Opioid receptors in the brain are not fixed in number: their frequency of occurrence can be altered by various factors, including social isolation, electric shock to the feet, restraint, or the use of agonists or antagonists. Long-term housing conditions and the behavioural responses they induce have been related to opioid receptor density by Zanella et al. (1991a, 1992, 1996). Sows which had been tethered for some months had a higher μ receptor maximum binding capacity in the frontal cortex than did group-housed sows. Tethered sows which were inactive for much of the time had high μ receptor densities, whereas those which showed high levels of stereotypies had lower k receptor densities. If lower receptor densities indicate down-regulation, i.e. a reduction in receptor density resulting from earlier high levels of the opioids binding to them, these results suggest that stereotypies may be related to high levels of dynorphin, and inactivity may be related to low levels of endorphin.

6.13

Behavioural Measures

The best indicators of long-term welfare problems are frequently measurements of behaviour. One approach for identifying conditions that result in poor welfare is to observe the individual’s behaviour when it is faced with them; such tests of preference and aversion are discussed in Chap. 7. Similar tests, of direct avoidance by animals of conditions in which they have recently been kept, may also be made, though these indicate short-term rather than long-term welfare problems. Various other analyses of behaviour also provide information about welfare. The simplest occurs when an individual has difficulty carrying out normal movements. A second is associated with the lack of a resource, or some specific frustration. A third group of behaviours arises as a consequence of frustration, inability to escape from perceived danger or unpleasant stimulation, an overall lack of stimulation, or confusion when too much is happening for the animal to make appropriate responses. A feature of all these difficult situations is the individual’s lack of control of its interactions with its environment. Fear and anxiety cause some very poor welfare in humans and other animal species and it is sometimes possible to identify the problem and assess its extent by the use of measures of behaviour. Mansell et al. (1999) reported that anxious people were less likely to look at emotionally disturbed human faces in a test situation. However, whilst anxiety research on non-human animals often includes the recording of behaviour, in studies of human anxiety, measures of the behaviour of the anxious subjects is rare. This is a failure to use potentially valuable information.

6.13

Behavioural Measures

151

Problems for dogs that lead to indicators of poor welfare include: lack of social contact, separation anxiety, fear of people, fear of other dogs, fear of environmental events such as thunder, and chronic disease conditions. Indicators of anxiety in dogs listed by Sonntag and Overall (2014) include: urination; defecation; panting; increased breathing rate and heart rate; trembling; lip-licking; nose-licking; hypersalivation; vocalisation; freezing; pacing; attempts to escape or hide; not meeting gaze; and changes in activity, grooming and social behaviour. Arhant et al. (2010) showed that small dogs are more likely to be punished for anxiety behaviour than are large dogs, and that training of small dogs is more inconsistent. Some of the ways by which fear and anxiety in dogs can be reduced are reviewed by Rooney et al. (2016). Fear is also reported by owners as a problem for dogs with fireworks, thunderstorms and gunshots eliciting fear responses. Much fear may also be shown when a dog perceives that there is a high risk of attack by a human or by another dog. On many occasions behaviours which indicate an animal’s welfare are part of its attempt to cope with an environmental difficulty. However, for some of these behaviours there is no evidence that the behaviour is helpful. It may in fact be making the situation worse for itself or for other animals; this is a behavioural pathology. In either case, measures of such behaviour indicate welfare problems, since welfare is poor both when an animal is having difficulty in its attempts to cope and when it is failing to cope.

6.13.1 Problems with Movement (a) Movement difficulties It is obvious that an individual which cannot walk has difficulties in coping with its environment. If the individual is capable of walking but, because the floor is slippery, it does not walk, or if it does not walk in a normal way, the same must be said. The normal movements of cattle standing or lying (Andreae and Smidt 1982). are shown in Fig. 6.3. When the animals were kept on slippery floors, they differed in the time, sequence and patterns of these movements. The first stage in lying down usually involved lowering the head and apparently sniffing the ground. After a few seconds, this was followed by the rest of the lying sequence on non-slippery floors, but only after prolonged pauses if the floor was slippery. Other interruptions in the sequence also occurred (Fig. 6.4), so the whole process of lying could take as long as 20 min. Sometimes the animal even changed the order of movements completely and lay down rump first (Fig. 6.5). Animals which have lived in conditions that preclude exercise may have movement difficulties. The calf which has lived for some months in a narrow crate, or an animal that has been kept on a short tether, may find walking and other locomotion difficult. A bird kept in a cage too small for wing movements is likely to be inefficient at flying. Direct effects of the confinement on the muscles, bones and perhaps nervous control mechanisms can account for these behavioural abnormalities.

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(b) Movement prevention While an animal is closely confined it will be unable to carry out certain movements, and modifications in behaviour will occur as a consequence. Other changes in behaviour may also become evident, owing perhaps to frustration. Sows which are kept in stalls and veal calves kept in crates may have difficulty in lying down because of the cramped conditions. Normal lying movements may even be completely prevented. Some individuals respond to this by ‘dog-sitting’ in which the hind quarters are on the ground but the front legs are extended, a posture that is rare in more spacious conditions. Confinement of circus animals, zoo animals, pets and some farm animals prevents them executing their normal range of locomotor, grooming, food-finding, sexual and other socially orientated movements. The consequence may be grossly modified attempts to show these movements. The results may be stereotypies, but need not be; in some cases, parts of normal behavioural sequences may be shown. Inability to complete normal grooming sequences frequently results in excessive grooming of the body parts which can be reached, for example, in veal calves which cannot turn around to groom their hindquarters. Inability to carry out sexual movements may result in bizarre sequences of substitute movements including elements which appear to be part of sexual display or attempts at sexual stimulation.

Fig. 6.3 The typical sequence of movements which occurs when a cow stands up (a) and lies down (b) (from Andreae and Smidt 1982)

6.13

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Fig. 6.4 Young cattle on slippery slatted floors show alterations in behaviour which inhibit, delay or prolong lying. (a) Repeated ground sniffing without lying down; (b) leg bent in without floor contact; (c) leg bent in with floor contact; (d) lying down interruptions. (from Andreae and Smidt 1982)

Fig. 6.5 In the same situation as that in Fig. 6.4, some young cattle lie down rump first, presumably to minimize painful events when trying to lie on the slippery floor (from Andreae and Smidt 1982)

6.13.2 Behaviour Associated with Lack of a Resource Animals which are deprived of part of their nutrient requirement, or a specific component of it, may show characteristic behaviour responses. Those responses often include movements associated with finding or obtaining the food. Carnivores

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might carry out prey-catching movements, and animals which find food items by sifting through earth or litter may carry out movements with a similar effect. Animals deprived of a component of their diet will often eat or chew a variety of materials which they would not otherwise eat. Phosphorus deficiency in farm animals can lead to ‘pica’, which is the chewing of wood, bones, soil, and so on; other abnormal feeding behaviour may also be the result of some dietary deficiency (Broom and Fraser 2015). The eating of such materials, or of hair or faeces, must be considered an indication of a welfare problem. In the examples given, the behaviour is related to the acquisition of the resource that is lacking. Other behaviour in such situations may be initiated by the deficiency, but some of the responses can seem unrelated to the problem. Sows confined in a stall often show bar-biting, drinker-pressing and shamchewing stereotypies (summaries by EU Scientific Veterinary Committee 1997; EFSA 2007). These stereotypies indicate great frustration and very poor welfare (see below).

6.13.3 Behaviour Associated with Lack of Social or Sexual Partners Searching for conspecifics is adaptive in humans and other social animals because the presence of companions may help in predator avoidance, food finding, food acquisition and environmental control (Broom 1981), in addition to providing potential sexual partners. The presence of conspecifics enriches an individual’s environment and opens up possibilities for a wide range of different experiences and behaviours. The animals normally kept on farms are social species, so if they are kept individually, especially if isolated from any contact, they show a variety of behavioural abnormalities as a consequence. There is certainly a great reduction in the occurrence of abnormal behaviours when social companions are present. Individually housed calves show much self-licking and repetitive tongue rolling. The incidence of these behaviours is usually less in socially reared calves, perhaps because of the possibilities for social interaction but probably also because of the opportunities provided by greater space for movement. Individually housed sows show very high levels of stereotypies and many individually-housed horses show stereotypies that indicate very poor welfare. Stereotypies are much rarer in grouphoused sows or horses than in individually housed animals. Prolonged isolation in sows and calves has been shown to lead to reduced reactivity to novel situations, reduced interaction with inanimate stimuli, poor social responsiveness, and failure in social competition. Tethered sows have also been reported to be particularly aggressive. High levels of aggression have been reported in rodents housed in isolation for long periods. The common practice of rearing domestic animals in isolation leads to a variety of abnormalities of sexual behaviour. Bulls and goats can show disorientation during

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copulation if they have had little social experience, but juvenile mounting experience reduced the incidence of this in beef bulls. Rams need contact with females during adolescence to show normal copulatory behaviour. Isolation-reared boars showed various inadequacies in mating behaviour, but contact with other boars through wire mesh reduced these (see references in Broom and Fraser 2015).

6.13.4 Consequences of Inability to Perform a Behaviour Although much of the behaviour of animals is clearly oriented towards acquiring resources, in certain circumstances individuals apparently try hard to carry out a behaviour that is normally the means of achieving an objective. The behaviour itself is apparently an objective since, in addition to making considerable efforts to show the behaviour, animals prevented from doing so show behavioural and physiological abnormalities. Examples of functional systems in which this occurs include keeping the body clean, having adequate knowledge of the environment, and preparing for reproduction or predator avoidance by establishing social relationships. The behaviours for achieving these include, respectively, grooming or preening, exploration or curiosity, and social interactions. Animals make considerable efforts to show these behaviours and exhibit clear signs of disturbance if they are unable to do so. As a consequence of the fact that some needs (Chap. 4) can be remedied only by being able to show certain behaviours, there are various behavioural and other consequences of living where such essential behaviours cannot be shown. One behaviour which seems to be important in itself is suckling by young mammals. This is defined as the obtaining of milk from the mother or another female by sucking a teat. There is an obvious nutritional objective, but the sucking behaviour itself also seems to be necessary. Young calves will drink as much milk from a bucket as they would take when suckling their mother, then spend long periods afterwards sucking the bucket handle, the bars of their pen or projecting parts of the anatomy of other calves. Human babies drink rapidly from a bottle but will also suck at fingers, appropriately shaped toys or pacifying dummies. Piglets will continue to suckle until 8–14 weeks if not separated from the mother. Hence it is not surprising that they show belly-nosing behaviour to other piglets if weaned at 3–5 weeks. Belly-nosing is a movement of the snout on the belly or soft tissue between the hind or forelegs of another piglet. It has some similarity to the massaging movements which piglets direct towards the udder of the sow. Bellynosing is often followed by sucking on the penis or navel. The frequency of bellynosing can be reduced by the provision of straw to chew. The manipulation of material such as straw is an activity which seems to be important for animals of several species, whilst rooting in soil or straw is a favoured activity of pigs. Rooting by domestic pigs presumably derives from the search for food in wild pigs, and the manipulation of the stems and leaves of vegetation is a part of natural feeding behaviour in cattle. When these activities are not possible, animals which are well fed still show abnormalities of behaviour. In such conditions, pigs,

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hens and calves may show stereotypies, and calves may show excessive licking. The incidence of such behaviour can be reduced in all these species by providing straw and, in pigs, by providing earth in which to root. Pigs living in groups without adequate environmental stimulation develop a behaviour in which the tails of other pigs are first manipulated and then bitten. This behaviour is less frequent if manipulable material is available for the pigs (Broom and Fraser 2015). The environments in which animals show stere otypies, such as excessive licking or tail biting are usually ones in which there is little for the individual to do. The behavioural abnormalities may be a consequence of living in a barren environment in which there is little stimulation and a lack of opportunity to show various behaviours, but it is clear that one of the forms of environmental enrichment which reduces the incidence of abnormal behaviour is the provision of manipulable material. The general appreciation that welfare problems arise in many species of animals when they live in barren conditions has led to increasing research on environmental enrichment (Chap. 7).

6.13.5 Sickness Behaviour and Physiology The wide range of responses to pathology includes behavioural changes, physiological changes in the body such as the production of acute-phase proteins in body fluids and production of cytokines in the brain, as well as immunological changes. Shortterm responses to pathological effects include vomiting, which gets rid of some toxins and is promoted by certain interferons, and diarrhoea which also helps to get rid of toxins and is promoted by interleukin-2 (Gregory 2004). Longer-term responses include fever, the feeling of malaise and sickness behaviour which are linked to immunological changes (Hart 1988; Hart and Hart 2019). Fever is energetically costly but improves the success of several body defences. The body temperature is altered and body temperature is elevated through the action of inflammatory cytokines that are released from macrophages, blood monocytes, and lymphocytes upon exposure to bacteria and bacterial toxins such as lipopolysaccharide. The inflammatory cytokine interleukin-1 is involved in causing fever and in inducing other fever-related responses such as lowering blood concentrations of iron in order to reduce pathogen growth. Immune system responses may need much energy whilst pathogens may take energy directly from their host (Forkman et al. 2001). Hence, some sickness behaviour results in energy saving, some promotes body defence mechanisms, and all is adaptive (Broom 2006). Sickness behaviour is initiated when cytokines are released by infected cells, endothelial cells, phagocytes, fibroblasts and lymphocytes so there are many peripheral sources as well as brain-mediated sources (Gregory 1998, 2004). However, the importance of the brain in relation to responses to pathogens is clear from studies in which lesions to the hypothalamus and reticular formation reduce cellular immune responses whilst lesions to the locus coeruleus reduce antibody responses (McEwen 2001).

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Other Consequences of Frustration and Lack of Control

As explained in Chap. 4 and mentioned earlier in this chapter, many situations that result in poor welfare are those in which an individual lacks control over its interactions with the environment. For either humans or non-humans such situations often involve frustration or unpredictability. When a resource is lacking or a behaviour cannot be carried out, one part of the problem for the animal is the direct effect of the lack of a resource, such as water, and another is the feeling of frustration because the particular regulatory system cannot work properly. Similarly, an animal which might be subjected at any time to an attack by a conspecific will be disturbed both by the attack and by the uncertainty about when the unpleasant event will occur. Behavioural responses in such situations include increased aggression, stereotypies and apathetic or unresponsive behaviour.

6.14.1 Aggression Aggressive acts in frustrating situations are well known to us all. They can occur in people, domestic or laboratory animals subjected to frustration about access to an important resource such as food. In the experimental situation described in Chap. 3 (Duncan and Wood-Gush 1971, 1972) in which two hens were put into a cage in which they expected to be fed, but their feeding was thwarted by a perspex cover over the food container, one of the results was in increase in aggression. One hen pecked the other, even though she was not the cause of the frustrating situation, and the extent of pecking was altered by the duration of food deprivation (Table 3.2). An example of aggression arising due to unpredictability is the experimental study on pigs by Carlstead (1986). In these examples, the aggression is an indicator that the welfare of the aggressor is poor, though aggression does not necessarily indicate poor welfare of the aggressor in all situations. Most aggression does, of course, also adversely affect the welfare of the individual which is the target of the aggression.

6.14.2 Stereotypies Repetitive, stereotyped behaviours are amongst the most important indicators of long-term welfare problems. The best known examples are the route-tracing of human prisoners and of animals kept in cages, for example in zoos. Hediger (1934, 1941) and Meyer-Holzapfel (1968) describe route tracing and other stereotypies in zoo animals while Keiper (1970) studied the paths followed by canaries in

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cages. Scientific studies of human prisoners are not easy to find, but Charrière (1969) in his novel about convicts in prisons in the French West Indies gives vivid accounts of the repeated movements of those kept in solitary confinement for long periods. The rocking and weaving movements of children with autism or other psychiatric disorders are well known (Levy 1944; Hutt and Hutt 1970); Levy also describes various stereotypies in other species. Crib-biting and wind-sucking by horses are described by Brion (1964), bar biting by sows was reported by Fraser (1975). Detailed descriptions of stereotypies (Broom and Fraser 2015) have demonstrated that there is very little variation in the sequence of movements displayed. Movements with an obvious function, such as rumination, locomotion and some displays, are not referred to as stereotypies. Hence the definition of a stereotypy is: a repeated, relatively invariate sequence of movements with no obvious function. Some of the movements which are repeated are brief, as in sham chewing by sows or rocking by children; others, like route-tracing sequences by bears in zoos, are lengthy. Some movements are repeated regularly whilst others are not. People in situations where they lack control temporarily often show intermittent stereotypies, for example key jangling or pacing by an expectant father in a hospital waiting room. The question of how to decide whether an apparent stereotypy has a function is usually quite easily answered. Whilst a single movement may be part of a normal functional system, frequent repetitions of movements are necessary only for certain limited purposes. These purposes include locomotion to a particular place, and repeated feeding, respiratory, cleaning or display movements. A brief period of observation is usually sufficient to distinguish stereotypies from such movements. In the case of some stereotypies the movement is so bizarre that it is clearly unlikely to have a function, for example Mason (1991) describes a female mink in a 75  37.5  30 cm mink farm cage that would repeatedly rear up, cling to the cage ceiling with her front paws and then crash down on to her back. Some other stereotypies, however, are sufficiently similar to normal behaviour, or have sufficient possibilities for real function, to create doubt about whether or not they are stereotypies. Careful study usually clarifies the situation but there remain questions about whether behaviours such as thumb sucking and repetitive play by children, or wheel running in captive rodents should be classified as stereotypies. In the some cases, improvement in motor and cognitive development may result and in others the animal gets necessary exercise from the movement. Similarly, it might be argued that repeated tongue-rolling and sucking by early-weaned veal calves has a function, because calves need to suck something and the tongue sucking helps to satisfy that need. However, in these and other instances, the activity is not effective in helping the development of the young animal, or in providing exercise or satisfying a need. In addition, none of the possible beneficial effects of such movements require that the action has to be repeated in almost exactly the same way each time it occurs. Hence, in many cases, the repetition of the relatively invariate sequence of movements does not have a function and the behaviour is a stereotypy. The occurrence and causation of stereotypies is discussed by Mason (1993), Mason and Rushen (2008) and Broom and Fraser (2015). Stereotypies

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occur in situations where the individual lacks control of its environment. In some cases, the animal is obviously frustrated and in other cases the future events are rather unpredictable. Frustration about food inadequacy is one factor leading to increased likelihood of stereotypies (Vinke et al. 2002). Ideas about the causation of stereotypies and their possible function for the animal have been complicated by the fact that some situations where stereotypies are shown are barren environments, but others include disturbing or threatening factors. Hence, the stereotyped behaviour might increase the total sensory input in the barren environment but produce a more predictable and familiar input in the disturbing situation. McBride and Hemmings (2009) consider that horses are most at risk of showing stereotypies if they lack opportunities for sufficient social contact, or locomotion, or food intake. Housing in individual stables is a widespread cause of stereotypies and hence of poor welfare. The diversity of situations that lead to the occurrence of stereotypies suggests that they have multiple causes (Polanco et al. 2018). The behaviour sequence that becomes stereotyped is sometimes an incomplete form of a functional behaviour pattern. It might arise from direct attempts to remedy some problem, such as to remove a bar that is preventing escape or to obtain the last available particle of food. However, once the stereotypy is established, no simple function is served. The observation that animals showing stereotypies are often difficult to disturb is of interest, for they may have their brain state modified in a way that reduces responsiveness. There is no clear evidence that stereotypies alleviate the effects of adverse conditions. However, whether or not they are of any help to the animal, they are clearly an indicator of poor welfare. Every individual showing a stereotypy has poor welfare as a result of current or previous experiences. Indeed, some of the worst examples of long-term poor welfare are indicated by stereotypies. With most human stereotypies, even if they last for a short time the perpetrator is deduced to have a psychological problem. An occasional bout of stereotypy indicates that a person has a problem at that time; more frequent occurrence of stereotypies is interpreted as evidence of a more substantial problem. Most stereotypies, even those which involve little movement, such as sham-chewing in pigs, or those which are prolonged such as the elaborate movement routines of some caged mink, are easy to recognize if behaviour is observed carefully. These are sometimes ignored by those who keep animals, however, and may be taken to be normal behaviour by those people if they see only disturbed animals. For example, zoo keepers may see route tracing by cats or bears, laboratory staff see twirling around drinkers by rodents, and farmers may see bar biting by stall-housed sows without realizing that these indicate that the welfare of the animals is very poor. A greater awareness of the importance of stereotypies as indicators of poor welfare is resulting in changes in animal housing. More complex environments which give the individual more control and hence result in the occurrence of fewer stereotypies are now being provided in good animal accommodation. These environments reduce the incidence of stereotypies by providing animals with more chances of reaching consummation, so that their behaviour does not get stuck in its appetitive phase, as

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may be the case with some stereotypies. They also give opportunities for a larger proportion of the full behavioural repertoire to be expressed, and for the patterns of movements in the repertoire to be varied. The consequent reduction in frustration and increase in the proportion of an individual’s interactions with its environment that are under its control improve its welfare. Mason et al. (2007) explain how the poor welfare associated with the occurrence of some stereotypies can be alleviated or eradicated by appropriate environmental enrichment. There is variation amongst species of animals in the extent to which they show stereotypies when they are confined in a small area. Species of wild animals also vary in the proportion of time that they spend active. Clubb and Mason (2003) describe, for some wild animals, the extent of the time and distance spent in locomotion and report that locomotor stereotypies in confinement are greater when ranging is greater in wild conditions. When animals are motivated to range over great distances, they are more disturbed by confinement in a small space.

6.14.3 Depression, Apathy and Unresponsiveness People who are depressed because specific or general conditions of life make it difficult to cope may show reduced activity, apparent unawareness, and lack of interest in the surrounding world. Although it is modified function of the brain that is the direct cause of depression, the major measure of human depression, and of depression in other species, is behavioural. Whilst this section refers principally to reduced activity and responsiveness, other behavioural abnormalities, especially showing stereotypies, are clearly indicators of depression. The realisation that millions of animals, confined by people in very inadequate conditions, are suffering from depression is changing public views about what is acceptable in animal production. As mentioned earlier in this chapter, there are links between depression, immunosuppression and other function. The behaviour of mice treated so as to be a model of human depression for the testing of anti-depressants includes not showing much escape behaviour when startled, showing low levels of exploratory behaviour and not choosing actions that lead to acquisition of sucrose. These behaviours were associated with modification of function in mid-brain dopamine neurons (Tye et al. 2014). Apathetic behaviour has frequently been described in non-human species. The loss of an important companion, whether human or canine, can result in apathetic behaviour in dogs. Animals in inadequate conditions in zoos or farms are also often apathetic. Inactivity and apathy in sows confined for long periods in a small pen or tether stall was described by Wiepkema et al. (1983). The degree of apathy of sows in stalls was assessed using measures of responsiveness to three different stimuli by Broom (1987). Stalled sows were responsive to the arrival of food, but they showed little response to a person who stood in front of them unless that person approached to within 1 m. In a test in which 200 ml of water was tipped onto the back of sows

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that were lying but awake, those in stalls had a response lasting a median of 27 s whilst animals in the same building housed in groups had a response lasting a median of 344 s. A study by Zanella et al. (1992, 1996) showed that the density of μ receptors in the hypothalamus and striatum of sows was higher in unresponsive sows than in responsive animals. Regardless of whether the unresponsiveness is associated with endogenous opioid action, the behaviour of such animals is abnormal and they have substantial problems. Individuals who do not respond to events in their surroundings are clearly behaving in an abnormal and unadaptive way. Unwillingness to explore is often shown by people who are unresponsive to stimuli presented to them. Quantitative measures of responsiveness and explorative curiosity are useful measures when assessing the welfare of depressive, or potentially depressive, people as well as other animal species. The inactive behaviour of cats in cages, for example in a veterinary hospital, has long been remarked upon by veterinary nurses, veterinary surgeons and cat owners. The cat often lies down at the back of the cage, as far as possible from humans moving past and shows little reaction to stimuli, often keeping the eyes closed for long periods. It is now clear from the work of McCune (1992) and others that this is abnormal behaviour associated with poor welfare. A cat that is well adapted to its environment is active and alert for longer than those cats that are disturbed by the confinement conditions. Dogs also show abnormal inactivity in some circumstances. A dog deprived of social contact, perhaps when it has no canine companion and its human companions are away from it for many hours, may show great, sometimes destructive, activity or may be inactive and relatively unresponsive. Prolonged inactivity has been reported for sows confined in stalls and tethers; for example, Jensen (1979, 1980) recorded that tethered sows were lying for 68% of the daytime period, while the pigs in an area of woodland and field spent 50% of the daytime rooting and only a 6% lying (Stolba and Wood–Gush 1989). Various factors must affect the level of activity, but it is frequently found that confined animals are less active. Prolonged lying in sows can lead to urinary tract disorders (Tillon and Madec 1984). When calves are kept in small crates such that they are unable to turn around, lying down is sometimes difficult and it reduces sensory contact with events in the building. Calves often stand for long periods, lean against the side of the crate or adopt a semi-seated posture against the rear of the crate. During this chronic standing they may show some stereotypy or may remain completely immobile for very long periods (Broom and Fraser 2015). A posture indicating depression in horses is described by Fureix et al. (2012). This “withdrawn” posture involves standing with the neck at approximately the same height as the back. The nape-withers-back angle is approximately 180 degrees and the neck is stretched out. When horses are looking at their environment, the neck is higher and when a horse is resting, the neck is rounder. Chronic standing in horses and the withdrawn posture are more common in horses kept in separate stalls than in those in groups. Older horses with orthopaedic conditions of the hindquarters and hind legs may also stand for long periods and have difficulty in rising and lying.

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Lack of Stimulation and Overstimulation

6.15.1 Lack of Stimulation Studies of the effects of sensory deprivation on human and other species refer to the same continuum and the measurements used can give information about welfare. Experimental studies on humans are of short duration, but reports from people in such studies and from those who have endured solitary confinement in prison make it clear that it is most unpleasant to have inadequate levels of stimulation. Despite this, and our knowledge of the complexity of life of mammals and birds, many animals are kept in such barren environments that there is bound to be some sensory deprivation, a lack of novelty and few opportunities to explore. As mentioned earlier, various behavioural abnormalities occur when animals are kept in impoverished environments. The consequences of boredom are described by Wemelsfelder (1990) and, whatever the individual feels, we can certainly recognise abnormalities of behaviour in environments which we predict to be boring. Behavioural responses to boredom sometimes seem to be directed towards increasing the level of sensory input, but in the latter stages of stimulus deprivation the most frequent consequences are either stereotypies, inactivity or apathy. Meagher et al. (2013) found that mink in impoverished environments sometimes showed prolonged lying in the nest-box, interpreted as a measure of anxiety, and sometimes showed lying prone with eyes open, interpreted as an indicator of boredom. The level of environmental variation below which the effects of stimulus deprivation become evident must vary from one individual to another. Certain people will find levels of input to be too low when they would be quite adequate for other people; there must be similar variation in other species. The differences in responses to barren environments amongst caged animals may in part be differences in coping strategies or in pathological consequences, but some individuals could just be less affected than others. Environmental conditions during early development influence the severity of the effects of sensory deprivation during later life. However, neither early training nor genetic selection can push the individual beyond its biological potential and a profound lack of stimulation is something to which no vertebrate animal is likely to be able to adapt.

6.15.2 Overstimulation The problems associated with a lifestyle in which there is too much to decide are well known in modern human society. Physical consequences, such as stomach ulceration, have been described in rats and other animals as well as in people. Responses to overstimulation include withdrawal from the confusing part of the environment and concentration on activities with predictable consequences. Here again, stereotypies are a frequent response. This similarity of response to several different kinds of

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circumstances is further evidence for the concept that it is an individual’s lack of control of its environment that is the cause of the behavioural abnormality. There is a close parallel between humans and many other sentient species. Experimental data on the responses of animals subjected to too much decision making come from studies such as those of Weiss on rats (1971) and from work on ‘executive’ monkeys. Monkeys trained to follow exacting schedules of lever pressing to obtain resources which were important to them were apparently overloaded in ways similar to the experience of harassed business executives. The monkeys developed physical and behavioural symptoms indicating that their welfare was not good, particularly when the tasks became complex. Even these complex experimental tasks do not mimic the most difficult tasks in life, however, which are arguably those encountered during the establishment and maintenance of social relationships. Social animals must possess elaborate brain mechanisms to deal with these complexities of social life. When problems of social interaction in domestic animals combine with physical and nutritional difficulties, inability to master the situation will often lead to behavioural abnormalities. The pig which lives in a group but shows a stone-chewing stereotypy, and the cow which shows tongue-rolling in a cubicle house may be examples of animals trying to cope with overstimulation. People who are overloaded with decision making are often unwilling to explore or attempt to learn new skills. Reduced exploratory behaviour is also a possible response to overload in other species. Social behaviour in primates, dogs and some farm animals provides examples of having to contend with a disturbingly large array of variables in everyday life. In humans and non-humans we have much to learn about both causation and treatment of such problems. Animal handling is made difficult when animals show freezing responses or startle responses, but neither of these is necessarily abnormal behaviour. Shying, jibbing, or baulking by horses can sometimes be extreme in the extent to which they are shown and may necessitate the use of blinkers and the avoidance of potentially startling situations. Other domestic animals may also show extreme flight responses. However, this behaviour is within the normal range of responses to danger. Problems arise when individuals injure themselves because of their high reactivity or if they influence others to behave similarly. High-density housing of animals and the presence of dense flocks or herds at pasture can make such socially transmitted hyperactivity dangerous to the animals and to humans. Grazing animals suddenly disturbed, even by an innocuous object such as blown paper, may stampede. They are more likely to be injured due to collision or falling during a stampede. Primitive man exploited this behaviour in order to catch large herbivores; for example, Native American peoples in North America caused bison to stampede over cliffs. The behaviour is present in wild populations but it can be maladaptive. Stampedes of cattle, horses or sheep can be very damaging to the animals. Hysteria is just as dangerous in large groups of humans who may act in such a way as to cause unintentional mortality to others. Hyperactivity in general can also be a problem in humans and other species. For example, although young dogs might be regarded as being too active by relatively

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sedentary owners, pathological hyperactivity can also occur and sometimes necessitates drug treatment (Manteca 2002).

6.15.3 Problems Caused by Specific Localised Stimulation Localised stimulation usually causes short-term rather than long-term problems for individuals. In some circumstances, however, the stimulation is repeated at frequent intervals over a long period or persists at a low but detectable level. Mild stimulation, if sufficiently protracted, becomes disturbing and noxious. For example, some parasites cause irritation at frequent intervals. The threadworm Oxyuris is not painful, but it may cause repeated irritation in the anus which elicits behavioural responses such as rubbing the anus with the limbs or on other objects. Frequent rubbing behaviour indicates continual irritation and this may be associated with more substantial responses. Horses which show frequent rubbing of the anal region may be responding to Oxyuris, to fungal infection of the perineum, to louse infestation or, occasionally, to no obvious cause (Broom and Fraser 2015). Sometimes localised, persistent stimulation results from injury. The injury itself may elicit behavioural responses over a long period, even to the point of selfmutilation. In addition, tissue damage can result in the formation of neuromas. These may well cause an increase in behavioural responses ranging from reduced usage of that part of the body to increased aggressive behaviour or stereotypies.

6.16

Interrelationships Among Measures and Welfare Outcome Measures

As explained in Chap. 4, individuals vary in the methods that they use to try to cope with difficulties, and they may try several coping methods for a single problem. Hence they will also vary in the consequences they suffer due to failure to cope. Welfare should therefore be assessed by a range of measures. This leads to the problems of how to compare the results of different measurements and how to decide whether welfare is worse when, for example, a certain level of adrenal activity is recorded than when a certain frequency of stereotypy or degree of immunosuppression is recorded. An attempt to produce a welfare assessment system for horses is described by Young et al. (2012). Whilst research on animal welfare can use sophisticated equipment and prolonged investigations, an inspection of animal housing, transport etc. is necessarily brief and can use only those measures that can be evaluated in the time available for the inspection. The aspects of the animals that indicate previous welfare and can be recorded by an inspector are welfare outcomes. Welfare outcome indicators include behaviour, such as whether an animal can walk normally, injury

References

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scores, signs of disease and mortality rate (Broom 2014). This approach was a major aim of the Welfare Quality project (Keeling 2009; Blokhuis et al. 2010) and followed up by the Animal Welfare Indicators (AWIN) project (e.g. Dalla Costa et al. 2016). For example, it is possible to monitor the number of animals that are lame as a welfare outcome indicator. The welfare outcome scored is the animal’s ability to walk and this is done using a scientifically designed scale of walking ability. Animals on farm or arriving at a slaughterhouse can be checked and a threshold level of lameness can be used to decide whether or not their welfare complies with the law or code of practice. For dairy cows, the EFSA report and opinions on the welfare of dairy cows (EFSA 2009) proposed that the threshold for a group of dairy cows on farm or at the slaughterhouse might be 10%. In order to facilitate this approach, EFSA has produced a series of reports and opinions on animal-based welfare outcome indicators for several farm species (EFSA 2012a, b, c, d).

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Chapter 7

Preference Studies and Welfare

Abstract In this chapter the use of preference studies to provide information relevant to the assessment of welfare is discussed. How do humans and non-humans allocate their time, energy and other resources and to what extent does this inform us about what is important to them? The methodology of economics research can be applied to animal preference studies in order to assess the value of resources to individuals. The terms: resource, demand, price, income, price elasticity of demand and consumer surplus are defined. Methods for investigating what is important to animals are described. The question of what constitutes environmental enrichment is also discussed. Keywords Preference assessment · Welfare · Enrichment · Demand · Consumer surplus

If we want to find out what resources and living conditions people need for good welfare, we can study what they choose when given access to alternatives. Observing preferences is also a well-known guide to providing adequately for the animals we keep. Dog owners soon come to recognise the indications given by their dog that it wishes to have food or to go out for a walk. Similarly, studies in which farm animals are offered different foods have been of value in deciding which foods to provide and which to avoid. Once an option is chosen, we must then also take account of the actual effects of having that resource. The assessment of such effects was the subject of Chap. 6, while this chapter is about what is preferred and what is avoided. What people prefer is not always good for them, for example a person who chooses to take heroin or too much alcohol. In studies of rats given many different foods to choose from, most rats selected a balanced diet but a few chose only chocolate and would have died but for the intervention of the researchers (see Sect. 7.4). As explained in Chap. 2, since aspects of motivational systems have evolved and are adaptive, given appropriate interactions with their environment, most of the strong preferences of humans and other animals are for resources or actions that benefit them, i.e. that help them to survive and breed successfully. During development, individuals will have acquired much information that helps them to take © Springer Nature Switzerland AG 2019 D. M. Broom, K. G. Johnson, Stress and Animal Welfare, Animal Welfare 19, https://doi.org/10.1007/978-3-030-32153-6_7

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decisions that lead to benefits. Preferences may be for a resource that is only slightly different from another, such as one kind of cake rather than another, or may be the difference between life and death. As a consequence, the assessment of motivational strength is important in any attempt to ensure that poor welfare is avoided and good welfare is maximised (Duncan 1978, 1992; Dawkins 1990; Bak Jensen and Pedersen 2008; Fraser and Nicol 2011; Broom and Fraser 2015). One factor that influences a person to show a preference for some item or activity is their previous experience. Preferred foods, companions, resting places etc. differ according to early and recent experiences. Human experience of flavours in utero and post-natally can affect later flavour choices (Ventura and Worobey 2013). Styles, fashions and music popular during a consumer’s youth can influence lifelong preference (Schindler and Holbrook 2003) whilst natal experience can alter habitat choice in a wide range of taxa (Davis and Stamps 2004). The importance of previous experience in studies of preference that are relevant to animal welfare is emphasized by Mendl (1990). Dawkins (1977, 1981) reports that hens that had lived for some time in a battery cage preferred to go into a similar cage rather than to an outside run with grass during the first day such a choice was available to them. This preference was strongly reversed on following days, but the initial effect of the previous experience was clear. Mendl also suggests that animals that have prolonged experience of an environment over which they have little control may not show any meaningful preference if subsequently offered an alternative, because the first environment may have led to apathy and unresponsiveness (Broom 1987) or even learned helplessness (Overmier et al. 1980). Learned helplessness has associations with exaggerated fear, serotonin pathways in the dorsal raphe nucleus and amygdala and with corticotrophin releasing hormone action (Maier and Watkins 2005). There are clear links between learned helplessness, activity in the habenula and some forms of depression (Li et al. 2012) whilst an opportunity for periods of wheel-running in rats can correct some of the behavioural and brain abnormalities associated with learned helplessness (Greenwood et al. 2003).

7.1

Time and Energy Allocation in a Rich Environment

When people first encounter a novel, rich environment they usually spend some time exploring. Such behaviour will result in gaining information that will help them to satisfy present or future needs. The possibilities for defending themselves or otherwise responding to danger may have to be considered; water and food sources must be found; a suitable resting place must be decided upon; the potential for various forms of social interaction have to be assessed. As the environment becomes more familiar there is still an element of exploration, but the individual begins allocating time and energy according to a wider variety of needs. If there are many opportunities for activity, the way in which the person spends time will give an indication of their needs and what they find important. The necessary duration of the activity should be taken into account, for example the time spent actually drinking or

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defecating may be short but the activity is vital for good welfare. For a person in solitary confinement in a prison cell, on the other hand, many activities cannot occur. Information about what conditions are likely to result in good welfare for people is obtained from our knowledge of what people choose to do. The same approach is relevant to understanding the needs of other species of animals. Part of our knowledge of needs is gained from finding that adverse effects occur if a particular resource, condition, or possibility for action is lacking; part also follows from the observation that animals make efforts to obtain the resource. The idea that dogs need regular exercise stems largely from the observation of the preference of dogs to take exercise. Additionally, when a dog has been unable to exercise and is given the opportunity to do so, there is a rebound effect as the dog exercises more vigorously and for a longer time than after no deprivation of exercise possibilities. Similarly, most people would consider that birds of most species need to build a nest because they observe that, at times, individuals make considerable efforts to obtain certain materials, even at risk to themselves, and use these to construct a nest. The behaviour in the wild of some of the larger animals that we keep in zoos is quite well described, and such information should be used when designing accommodation for captive animals. That is not to say that all of the conditions in the wild, including the possibility of contracting severe disease or being chased and caught by predators, should be reproduced in captivity, but the needs of captive animals can certainly be deduced from studies of wild animals. Animals kept on farms, in laboratories and as pets should also be observed in rich environments. Species that have been domesticated for thousands of years are different from their ancestors in various ways, so the evidence should be taken from studies of the domesticated strain in varied or semi-natural conditions. It is of particular interest, however, that when detailed studies of feral animals of domestic strains were carried out, there were far more similarities to their wild equivalents than differences from them. McBride et al. (1969) found that the behaviour of domestic fowl, that had lived unrestrained for several generations, was very similar to that of red jungle fowl from which domestic fowl are descended. Similarly, modern pig breeds living in semi-natural conditions were very similar to wild boar. Stolba and Wood-Gush (1989) recorded how domestic sows allocated their time and energy to different behaviours when they were put in an area of grassland and woodland but were provided with the same concentrate food, in the same quantity, as that given to confined sows. The sows spent 31% of their time during daylight grazing, 21% rooting, 14% in locomotion and only 6% lying. Any preference action requires the animal to make a sacrifice of some sort when it gains access to some quantity of the resource or spends time consuming it. These sows paid a price for carrying out each activity in that they could have done something else instead. The careful observation of animals in complex environments also gives specific information about what they choose to do in particular circumstances. For example, Mills and McDonnell (2005) describe horse behaviour in natural conditions and Jensen (1989), in a study of pigs in fields and woodland, described the choice of farrowing locations and the nest-building behaviour of sows. Observation of 60 farrowings showed that the site chosen for farrowing was normally at some distance

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from the group resting area, and was in small wooded areas with fields around them more often than in open fields, fir plantations, or marshy areas. A substantial nest was usually built, with some time being spent selecting nesting materials. Some examples of the many types of preference tests (Fraser and Matthews 1997) are described below.

7.2

Experimental Studies of Animal Preferences

Very many investigations of the preferences of animals have been carried out, but those where results can be used to improve to animal welfare have mainly concerned farm animals. The simplest kind of experiment is that in which animals exhibit a preference by carrying out a simple motor activity. Hughes and Black (1973) wished to find out which kind of flooring would be chosen most by hens. They put hens in a cage with three types of flooring: hexagonal wire mesh, coarse but more rigid rectangular mesh and steel sheet perforated with large holes. The hens stood for longest on the hexagonal ‘chicken’ wire, probably because this gave the best support to their feet. The choice test is of some value to the animal welfare scientist when comparing resources that satisfy the same or a very similar need. It is important to consider the value of the resources compared. Resources can be of low value to the animal or of value but only as luxury items. Choice tests cannot usefully compare resources associated with different needs, whose motivational basis is quite different (Kirkden et al. 2003). The needs may vary, not only in motivational strength but also in the rate at which they can be satiated or the quantity of the resource required for satiation. Hence more sophisticated preference tests are generally better than simple choice tests.

7.2.1

Assessing the Importance of Preferences

As techniques of preference tests developed, it became apparent that good measures of strength of preference were needed. A sophisticated reversal of preference experiment, which involved balancing one preference against another, was used by van Rooijen (1980, 1981). He observed that pigs, in particular the gilts which he was studying, when offered several individual, freely accessible pens preferred to lie adjacent to a pen occupied by another gilt. He assessed the strengths of the gilts’ independent preferences for different types of flooring, and then balanced these against the social preference. An earth floor was preferred to a concrete floor sufficiently strongly to counteract the social preference (Fig. 7.1). However the preference for straw over wood shavings as a bedding material was not strong enough to overcome the preference for being near another gilt (Fig. 7.2). A further example of a study in which different preferences were balanced is that

7.2 Experimental Studies of Animal Preferences Fig. 7.1 Young female pigs (gilts), given the choice of lying on one of two different floors either nearer to the neighbouring gilt or further from her, spent longer (figures quoted for duration in hours) on earth, even at the expense of being further from the other gilt (from van Rooijen 1980)

Fig. 7.2 Gilts offered the choice of straw or wood shavings as bedding material did not have a strong enough preference for straw to overcome their preference for being near the other gilt (figures quoted for duration in hours) (from van Rooijen 1980)

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of Rioja-Lang et al. (2009) who found that while cows tested in a Y-maze normally chose to go to a larger quantity of food, they would select a lower quantity of food if the larger quantity involved standing next to a cow that might be aggressive to her.

7.2.2

Operant Techniques in the Assessment of Preferences

A more complex way of assessing the importance of resources to animals is to use an operant behaviour that is not directly related to the objective. An operant procedure is one used by many psychologists in which a subject animal is required to carry out an action, such as pressing a lever, in order to obtain a food reward. Rats would not normally associate a lever with food but, once the animal associates the action with the arrival of food, the strength of its motivation to obtain the food can be assessed. The first requirement is that the animal can learn to carry out the operant procedure in order to obtain the reinforcement. The second is to record how often the operant procedure is performed for a particular reward. The pioneer of such studies in relation to understanding the needs of farm animals was Baldwin (1972, 1979), see also Baldwin and Start (1985). Sheep and pigs learned to operate a switch by putting their nose in a slot and breaking a light beam monitored by a photocell. This action resulted in the subject obtaining food, light or heat (Fig. 7.3) so the animal’s evaluation of the optimum conditions could be discovered. Fig. 7.3 This pig is about to push the black panel and thus operate a switch. Pigs learned to press for food, for a period of heat, and to switch lights on or off (from Baldwin 1979, with the author’s permission)

7.2 Experimental Studies of Animal Preferences

179

Sheep learned that they could increase their ambient temperature by carrying out this operant procedure and hence it was possible to discover what temperature they preferred. As might be expected, the preferred temperature was higher in a recently shorn sheep than in one that was in full fleece. When young pigs in a group were able to switch heaters on or off in this way, they maintained an ambient temperature at night, when they huddled, that was 11  C lower than in the daytime when they moved about. The temperature chosen in the daytime was close to that found to lead to good growth rates but that chosen at night was substantially lower than that generally recommended for pig housing (Curtis 1983). Curtis also found that some pigs controlled the temperature by nudging other pigs until they switched the heater on or off. Once it is established that an animal will carry out an operant procedure, like pressing a lever or plate in order to obtain a reinforcement, it is possible to withhold the reinforcement until the operant procedure is performed several or many times. This can give a measure of how hard the animal will work for that reinforcer. Many studies with laboratory animals show that they will continue to work for food rewards by pressing a lever even if they have to press it 2, 10, 50, or several hundred times. In each experiment the number of times that the lever must be pressed for a constant reward is called the ‘fixed ratio’. If the rate of receiving food rewards is plotted against the rate of lever pressing (Fig. 7.4) the plot obtained is called a demand curve. If a flat or slowly changing rate of reward is seen (Reinforcer 1), the animal is said to have an inelastic demand for the resource. If the reinforcer is not sufficient to cause the animal to respond at a high rate, then the demand curve drops as the fixed ratio increases (Reinforcers 2 and 3).

Fig. 7.4 Results of experiments in which a subject receives one of three different positive reinforcers when it carries out an operant procedure, such as pressing a lever which it has learned to associate with rewards. When the number of lever presses for each reward is increased the subject increases the pressing rate and hence maintains the rate of receiving the reward for Reinforcer 1, but does not maintain it for Reinforcer 2, and compensates little for the increased pressing rate necessary for Reinforcer 3

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As Dawkins (1983, 1988, 1990) has pointed out, such studies give information about how important a resource is to an animal. This is valuable information in welfare assessment because the fact that an individual is working hard to obtain a resource tells us something about its attempts to cope with its environment and hence its welfare. The actual shape of a demand curve, however, will differ according to the size of the reward, the needs of the animal for the resource and the effort or time required to carry out the operant procedure in relation to other demands upon the animal. The demand curve for increasing fixed ratios of lever pressing for very small amounts of food might be flat if the animal has nothing else that it must do, but steeper if this activity is in competition with a possibility to attain other objectives at the same time. Another way of using the same kind of apparatus to measure the importance of a resource for an animal is to increase the number of lever presses needed for reinforcement continuously during each session. For example, Lawrence and Illius (1989), working with food-restricted pigs, found that the animals would press a panel for 6 g food pellets at a fixed ratio of 10 presses per reinforcement. When the pigs needed to press the panel once for the first pellet, twice for the second, three times for the third, and so on, they would continue up to 30 presses for a pellet if they had been fed to only 40% of appetite beforehand. We need to know how important space is to animals when we design housing conditions. As a consequence, preference experiments have been carried out on the space requirements of hens. Hughes (1975) and Dawkins (1976, 1977) found that, once hens were accustomed to having access to a large cage, animals previously kept in a battery cage preferred a large cage to a smaller one. The value put on earth for rooting and straw for nest building by pigs has been the subject of many studies. Wood-Gush and Beilharz (1983) found that piglets in small cages spent some time rooting in earth if it was provided and Hutson (1989) found that piglets would repeatedly lift a lever in order to gain access to earth. Studnitz et al. (2007) found that, in order to be strongly preferred and effectively reduce abnormal behaviour, material provided in pig pens must stimulate the exploratory behaviour of pigs for an extended length of time. Exploratory behaviour in pigs is best stimulated by materials that are complex, changeable, destructible, manipulable, and contain sparsely distributed edible parts. All pregnant sows build a nest of leaves, straw or similar material if they can, or as a depression in earth if they cannot (Hutson and Haskell 1990), usually during the 1 or 2 days before parturition. Arey (1992) found that sows readily pressed a panel on a fixed ratio of 10 for access to an adjacent straw pen in preference to an adjacent empty pen (Fig. 7.5a). Hutson (1992) showed that pre-parturient sows worked much harder for food than for access to straw, an unsurprising result given the high energy demand of piglet production. If straw and food were put in different pens adjacent to the starting pen (Fig. 7.5b) up to 2 days before farrowing, choices of straw and food were equal with a fixed ratio of one, but food was preferred with fixed ratios of 50–300, the ratio depending on the willingness of individual to press. On the day before farrowing, however, straw was as important to the animal as food (Table 7.1) so the motivation to build a nest is very high at this time.

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Fig. 7.5 By pressing the panel on the door, pre-parturient sows put into the central area could gain access to (a) the straw area or empty control area, or (b) the straw area or feed area (from Arey 1992)

Table 7.1 Pre-parturient sows: presses on panel to gain access to straw pen or food pen (from Arey 1992)

Presses per reinforcer (fixed ratio) 1 50–300 50–300

Day before farrowing 2 2 1

Presses For straw 17 2.6 16.4

For food 21 11.4 17

Other indicators of the effort that an individual is willing to make in order to obtain a resource are the distance that a cow will walk in order to be able to spend time at pasture rather than just being fed inside a building (Charlton et al. 2012) and the weight of a door that is lifted by a rat to get to a resource. The cows would walk in order to get to pasture more than the amount expected for food value only. In a study

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of the preferences of rats in relation to the floor that they had to stand on, Manser et al. (1996), studying floor preferences of laboratory rats, found that rats would lift a heavier door to reach a solid floor on which they could rest rather than a lighter one to reach a grid floor. This work started with an investigation of the choice of rats for a solid or a wire grid floor. Manser et al. (1995) found that rats in connected cages (see Fig. 7.6) would walk on either kind of floor but always rested on a solid floor if given the opportunity. The maximum weight of door that the rats would lift (see Fig. 7.7) in order to reach any resource was ascertained, and the weight lifted in order reach a

Fig. 7.6 Choice test for rats: a cage with a wire grid floor is connected to one with a solid floor. The rats preferred to rest on the solid floor. Photograph C.M. Manser (Manser et al. 1995)

Fig. 7.7 When this box was put between two rat cages, like those shown in Fig. 7.6, the rat had to lift the sliding door in order to get to the resource in the other cage. Photograph C.M. Manser (Manser et al. 1995)

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solid floor for resting was found to be very close to that maximum. Hence the solid floor was very important to the rat. In similar experiments, rats were found to choose bedding and a dark nest box and to be willing to lift 150 g in order to reach a novel empty cage, 290 g to reach a cage with bedding material in it, 330 g to reach a cage with a nest box and 430 g to reach a cage with both bedding and nest box (Manser et al. 1998a, b). The terminology used when motivational strength is being estimated is that of micro-economics (Kirkden et al. 2003). A resource is a commodity that the animal can use or an activity that it can carry out. The demand of the animal is the amount of action, for example, operant responses, which the animal shows in order to obtain a resource. The price that the animal pays is the amount of action required to obtain a unit of resource. The income of the animal is the amount of time, energy or other variable limiting the action that the animal has available to it. If an animal has learned to carry out an operant task such as pressing a plate, in order to obtain a resource, the individual’s demand can be assessed by varying the price of that resource. Ten presses on the plate are a higher price to pay for access than one press and a hundred presses is higher still. The pig in Arey’s study had to press the plate to gain a period of access to a pen with straw in it, while the rat in Manser et al.’s studies had to lift one of various weights to reach a cage with a particular floor or nest-site. If a range of prices are used, the animal’s behaviour can be described using an inverse demand curve in which price is plotted against demand (see Fig. 7.8). The demand value is how often the animal carried out the work required to obtain the resource.

Price elasticity of demand : slope at z

The area under this inverse demand curve is the consumer surplus of the quantity z. Fig. 7.8 This inverse demand curve shows how an individual’s demand for a resource is related to the price that has to be paid for the resource. Price elasticity of demand and the consumer surplus are indicated for a given demand (see Kirkden et al. 2003)

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The use of elasticity of demand as an index of motivational strength for hens and other animals was proposed by Dawkins (1983, 1988, 1990). If the demand for a resource does not decline much when the price increases, the demand is inelastic, whereas if demand drops as price increases it is elastic. For human consumers, if the price of coffee increases by 100% but most people still buy the same amount of coffee, those people’s demand for coffee is inelastic. On the other hand, if the price of beef increases by 100% and most people stop buying beef, or buy very much less of it, those people’s demand for beef is elastic. The price elasticity of demand is the proportional rate at which a subject’s consumption of the resource changes with the price of the resource, as indicated in Fig. 7.8 at a point on the curve. In a discussion applying microeconomics principles to studies of non-human animals and referring to the use of elasticity of demand, Kirkden et al. (2003) explained how researchers used the rate at which demand changes with price, the rate at which expenditure changes with price, the rate at which expenditure or expenditure share changes with income and the slope of a bilogarithmic plot of expenditure against income (e.g. Matthews and Ladewig 1994; Bubier 1996; Cooper and Mason 1997, 2000; Warburton and Nicol 2001). Four shortcomings of elasticity of demand indices are described in detail by Kirkden et al. (2003). First, since price elasticity of demand varies with price and successive units of a commodity are not worth the same as one another to an animal, it is not reasonable to assign a single value to the price elasticity of demand for a resource. Secondly, since individuals have a tendency to defend a preferred consumption level and to become satiated, the price elasticity of demand index will tend to overestimate the value of resources for which satiation occurs rapidly. Thirdly, the price elasticity of demand tends to underestimate the relative value of resources whose initial consumption levels are high. For example, bread is consumed by humans at higher levels than salt, so demand for salt would be more inelastic than demand for bread, not because salt is more important to people than bread but because it is consumed in smaller quantities when cheap. Fourthly, the income available to an animal will vary, but the price elasticity of demand does not take account of this. Since demand increases with income, the price elasticity of demand will underestimate the value of resources when a decrease in income causes an increase in demand, and overestimate it when an increase in income causes a reduction in demand. The consumer surplus is another index of strength of preference shown in Fig. 7.8. The consumer surplus is the area under the demand curve and can be readily measured whenever a demand curve can be generated. The consumer surplus is a measure of the difference between the largest price that a subject with a fixed income would be prepared to spend on a given quantity of a resource and the amount that actually has to be paid. The first three shortcomings of elasticity of demand indices described above do not apply to the consumer surplus index. The income of the animal will affect the consumer surplus index so, in studies of motivational strength, income should be set at the level that might occur in real life. If this can be done, the consumer surplus is the best indicator of motivational strength and should be used instead of elasticity of demand indices. In some cases,

7.3 Environmental Enrichment

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elasticity of demand indices provide a good indication of motivational strength, but the consumer surplus will always be more reliable. In the experiments of Duncan and Kite (1987), Manser et al. (1996), Mason et al. (2001), Olsson et al. (2002) and others, the reservation price, which is the maximum price paid for a resource, e.g. the maximum weight lifted by a rat, was measured. This value can be a useful shortcut to the consumer surplus in the circumstances where a demand curve cannot be generated. In a study of how important various resources are to rabbits, Seaman et al. (2008) used the consumer surplus to show that food and access to social companions were equally important, both were more important than access to a platform and this in turn was more important than access to an empty cage. All of the arguments presented here are explained in detail by Kirkden et al. (2003) and by Broom and Fraser (2015) and a useful example of comparisons of the different methods of assessing motivational strength is that of Fraser and Nicol (2011). The general conclusion of this review of measures of motivational strength is that preference tests, including those requiring the animal to use quantifiable operants, are of particular value in trying to find out what is important to animals. The consumer surplus is the best index of motivational strength when a demand curve can be produced, and the reservation price is a useful indicator when this is not possible. Once such information has been obtained, better housing and management conditions can be designed, and these can be compared with existing conditions using direct indicators of welfare. The conclusion reached here about measures of strength of preference has parallels with the current thinking of some economists. A widespread method used for human subjects is to measure of strength of preference in units of money. The idea that people can judge the amount of money that compensates for a difference in quality or subjective value between different options is fundamental to standard economic analysis. When this method was rigorously tested, a substantial bias was discovered (Butler et al. 2014). More direct methods such as those used in animal welfare research may be useful. Nicol et al. (2009) attempted to integrate preference measures and direct measures of welfare by comparing hens provided with what they chose and hens that were not. They found that measures of welfare associated with positive choice included lower body temperature, blood glucose, heterophil-lymphocyte ratio and response to novelty. Some other welfare indicators were not associated with positive preference, for example plasma corticosterone concentration. However, this is not surprising as elevation of corticosterone is a response to a short-term problem and not a response to prolonged positive or negative situations.

7.3

Environmental Enrichment

If the environment of an individual is enriched, the new environment should be better than the previous environment. The only realistic measure of what is better is the welfare of the individual concerned. An “enrichment” that just improves the

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comfort of an observer, such as a zoo visitor, may not enrich the environment of the subject animal. A knowledge of welfare assessment is therefore required in order to enrich an individual’s environment. As pointed out by Young (2003) two kinds of attempts to enrich the environment of captive animals, such as those in zoos, have either involved trying to replicate aspects of the conditions in the wild or, more recently, have used investigation of the needs of the animals (see Chap. 2). These approaches are not the same as the first is always a human view of the wild. It is inevitably principally visual, even if the captive species uses olfaction, hearing or other senses more than it uses vision. A widespread attempt at “enrichment” in zoos has been to paint a backdrop of how humans see the wild environment and put this behind the animals. Whilst this may educate the public, it is seldom of any benefit to the captive animals. Pictures of the natural environment generally do not improve the life of the captive animals. However, some recent enrichment attempts have been more biologically sensible and often do have the effect of reducing stereotypies and other abnormal behaviour (Swaisgood and Shepherdson 2005; Alligood and Leighty 2015). Other enrichment attempts are based more on guesswork than science and may or may not have any useful effect (Law and Kitchener 2017). Animals provided with children’s toys or music may improve welfare or may have zero benefit (Newberry 1995). Whilst some human toys are also attractive objects for non-humans, and some music can be calming to individuals of various species in noisy or otherwise disturbing environments, it is important to find out how members of a species respond to stimuli that might enrich their environment. Enrichment attempts may involve objects, tasks with food as a reward, gross structure of the exhibit, human contact, or contact with members of their own species (Shepherdson et al. 1998). Since the aim is to improve welfare, any change should not increase fear or disease risk. Tourists and other visitors will not always easily understand what is being done for the animals so explanation is needed. Other ways of improving the welfare of the animals are to give better food, deal with health problems better and shield animals from undesirable human contact, or sometimes all human contact (Carr and Broom 2018). Again, explanation for the viewing public is necessary. A zoo with the serious intention to rear animals for release into the wild would often have to explain to zoo visitors that they cannot see or approach the animals as human contact must be minimised. A great problem for the animals occurs when animal accommodation and management cannot be modified in such a way that the welfare is good. In that case, the animal should ideally be moved to a different zoo or aquarium where its needs can be met. If this cannot be done and return to the wild is impossible, it may be more ethical for it to be humanely killed than for it to be kept in conditions where its welfare is very poor. In any of these cases, no further animals of the species should be kept in the inadequate circumstances. Environmental enrichment is not just important for animals displayed to the public. Farm, companion, laboratory and working animals can all have welfare problems and for some, environmental enrichment is the best solution. The extent of poor welfare in widely-used animal keeping conditions is sometimes evident when environmental enrichment is used. Lazarov et al. (2005) found that enriched environments for transgenic mice reduced the deposition of Aβ peptides and amyloid

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187

deposits, both characteristic of Alzheimer’s patients, as compared with mice in normal laboratory conditions. Francis et al. (2002) improved the welfare of rats separated from their mothers by environmental enrichment and hence concluded that a richer environment could compensate for the effects of early life adversity whilst Douglas et al. (2012) increased emotionally optimistic responses during a cognitive bias test (see Chap. 6) in pigs by enriching their environment. The value of improving the welfare of laboratory animals by environmental enrichment for the quality of laboratory procedure results, as well as for the animals themselves, is emphasised by Baumans (2005).

7.4

Do Preference Studies Tell us What Is Important for Animals?

A fundamental question about the value of preference tests in animal welfare is whether or not animals make choices that benefit them. The actual choosing should result in some immediate improvement in welfare, but this cannot be assured, and it may even be offset by other adverse effects of the choice. Natural selection should result in animals showing behaviour that increases fitness, so some mechanisms promoting efficient selection of resources are likely to exist. This accounts for simple mechanisms like sodium appetite and more complex preferences like those for the sort of hiding places that will reduce predation risk. Strong preferences for opportunities to: display maternal characteristics, have social companions, be able to explore the immediate environment, and have particular conditions in which to lay eggs or give birth are also examples of animals’ basic biological characteristics that increase fitness. These preferences can be sufficiently strong to become established as needs that can be satisfied only by the animals being able to perform specific behaviours. This argument for animals showing preferences that will be beneficial is supported by a wide range of observations of preferred activities that apparently help the individual or promote the spread of genes carried by that individual within the population. Despite the general rule that animals prefer what is good for them, Duncan (1978) points out there are examples of preferred resources or activities causing harm. Grazing animals have to learn about a large number of plants but sometimes select poisonous plants and when rats were offered a wide range of different kinds of food, some chose solely chocolate bars that do not provide adequate nutrition (Rozin 1976; Broom 1981). Rats will even tolerate extreme cold to eat such food, despite a balanced diet being available in warm conditions available to them (Cabanac and Johnson 1983). Humans may eat so little that they die or so much that their health is damaged, and they may have strong preferences for drugs that eventually kill them. In some of these examples there is a short-term reward, so the showing of such a preference may be beneficial in certain situations, but have a long-term adverse effect. Early experience can have a strong effect on preferences and could result in a

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less than optimal resource or activity being preferred. As is evident from these possibilities, not every preference is beneficial. Dawkins (1988, 1990), Kirkden and Pajor (2006) and Broom (2014), in discussions of such problems, conclude that the solution is to take into account more than one measure of welfare. Preference studies should be combined with the use of indicators of good or poor welfare. Some difficulties in the interpretation of preference studies result from problems in experimental design, as mentioned elsewhere in this chapter, and other difficulties are discussed in detail by Dawkins. With care, most of these problems are soluble, and there is no doubt that preference tests are an important tool in the assessment of welfare. They have particular value in the planning of better housing facilities for animals, and in the selection of management procedures. Once designs for such facilities have been developed, the new system can be compared with alternative systems using both preference tests and other measures of welfare.

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Kirkden RD, Pajor EA (2006) Using preference, motivation and aversion tests to ask scientific questions about animals’ feelings. Appl Anim Behav Sci 100:29–47. https://doi.org/10.1016/j. applanim.2006.04.009 Kirkden RD, Edwards JSS, Broom DM (2003) A theoretical comparison of the consumer surplus and the elasticities of demand as measures of motivational strength. Anim Behav 65:157–178 Law G, Kitchener AC (2017) Environmental enrichment for killer whales Orcinus orca at zoological institutions: untried and untested. Int Zoo Yearb 51(1):232–247 Lawrence AB, Illius AW (1989) Methodology for measuring hunger and food needs using operant conditioning in pig. Appl Anim Behav Sci 24:273–285 Lazarov O, Robinson J, Tang Y-P, Hairston IS, Korade-Mirnics Z, Lee VM-Y, Hersh LB, Sapolsky RM, Mirnics K, Sisodia SS (2005) Environmental enrichment reduces Aβ levels and amyloid deposition in transgenic mice. Cell 120:701–713. https://doi.org/10.1016/j.cell.2005.01.015 Li B, Piriz J, Mirrione M, Chung C-H, Proulx CD, Schultz D, Henn F, Malinow R (2012) Synaptic potentiation onto habenula neurons in learned helplessness model of depression. Nature 470(7335):535–539. https://doi.org/10.1038/nature09742 Maier SF, Watkins LR (2005) Stressor controllability and learned helplessness: the roles of the dorsal raphe nucleus, serotonin, and corticotropin-releasing factor. Neurosci Biobehav Rev 29:829–841. https://doi.org/10.1016/j.neubiorev.2005.03.021 Manser CE, Morris TH, Broom DM (1995) An investigation into the effects of solid or grid cage flooring on the welfare of laboratory rats. Lab Anim 29:353–363 Manser CE, Elliott H, Morris TH, Broom DM (1996) The use of a novel operant test to determine the strength of preference for flooring in laboratory rats. Lab Anim 30:1–6 Manser CE, Broom DM, Overend R, Morris TH (1998a) Investigation into the preference of laboratory rats for nest-boxes and nesting materials. Lab Anim 32:23–35 Manser CE, Broom DM, Overend R, Morris TH (1998b) Operant studies to determine the strength of preference in laboratory rats for nest-boxes and nesting material. Lab Anim 32:36–41 Mason GJ, Cooper JJ, Clarebrough C (2001) Frustrations of fur-farmed mink. Nature 410:35–36 Matthews LR, Ladewig J (1994) Environmental requirements of pigs measured by behavioural demand functions. Anim Behav 47:713–719 McBride G, Parer IP, Foenandez F (1969) The social organisation and behaviour of the feral domestic fowl. Anim Behav Monogr 2:127–181 Mendl MT (1990) Developmental experience and the potential for suffering: does ‘out of experience’ mean ‘out of mind. Behav Brain Sci 13:28–29 Mills DS, McDonnell SM (2005) The domestic horse: the origins, development and management of its behaviour. Cambridge University Press, Cambridge Newberry RC (1995) Environmental enrichment: increasing the biological relevance of captive environments. Appl Anim Behav Sci 44:229–243 Nicol CJ, Caplen G, Edgar J, Browne WJ (2009) Associations between welfare indicators and environmental choice in laying hens. Anim Behav 78:413–424 Olsson IAS, Keeling LJ, McAdie TM (2002) The push-door for measuring motivation in hens: laying hens are motivated to perch at night. Anim Welf 11:11–19 Overmier JB, Patterson J, Wielkiewicz RM (1980) Environmental contingencies as sources of stress in animals. In: Levine S, Ursin H (eds) Coping and health. Plenum Press, New York, pp 1–38 Rioja-Lang FC, Roberts DJ, Healy SD, Lawrence AB, Haskell MJ (2009) Dairy cows trade-off feed quality with proximity to a dominant individual in Y-maze choice tests. Appl Anim Behav Sci 117:159–164. https://doi.org/10.1016/j.applanim.2008.12.003 Rozin P (1976) The selection of foods by rats, humans and other animals. Adv Study Behav 6:21–76 Schindler RM, Holbrook MB (2003) Nostalgia for early experience as a determinant of consumer preferences. Psychol Mark 20:275–302. https://doi.org/10.1002/mar.10074 Seaman SC, Waran NK, Mason G, D'Eath RB (2008) Animal economics: assessing the motivation of female laboratory rabbits to reach a platform, social contact and food. Anim Behav 75:31–42

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Shepherdson DJ, Mellen JD, Hutchins M (eds) (1998) Second nature: environmental enrichment for captive animals. Smithsonian Institution Press, Washington, DC Stolba A, Wood-Gush DGM (1989) The behaviour of pigs in a semi-natural environment. Anim Prod 48:419–425 Studnitz M, Bak Jensen M, Pedersen LJ (2007) Why do pigs root and in what will they root? A review on the exploratory behaviour of pigs in relation to environmental enrichment. Appl Anim Behav Sci 107:183–197. https://doi.org/10.1016/j.applanim.2006.11.013 Swaisgood RR, Shepherdson DJ (2005) Scientific approaches to enrichment and stereotypies in zoo animals: what’s been done and where should we go next? Zoo Biol 24:499–518 van Rooijen J (1980) Wahlversuche, eine ethologische Methode zum Sammeln von Messwerten, un Haltungseinflusse zu erfassen und zu beurteilen. Aktuelle Arbeiten zur artgemässen Tierhaltung, KTBL–Schrift 264:165–185 van Rooijen J (1981) Die Anpassungsfahigkeit von Schweinen an einstreulose Buchten. Aktuelle Arbeiten zur artgemässen Tierhaltimg, KTBL–Schrift 281:174–185 Ventura AK, Worobey J (2013) Early influences on the development of food preferences. Curr Biol 23:R401–R408. https://doi.org/10.1016/j.cub.2013.02.037 Warburton HJ, Nicol CJ (2001) The relationship between behavioural priorities and animal welfare: a test using the laboratory mouse (Mus musculus). Acta Agric Scand 30:124–130 Wood-Gush DGM, Beilharz RG (1983) The enrichment of a bare environment for animals in confined conditions. Appl Anim Ethol 10:209–217 Young RJ (2003) Environmental enrichment for captive animals. Blackwell, Oxford

Chapter 8

Ethics: Considering World Issues

Abstract In this chapter, the question considered is to how great a disturbance of homeostasis, or to what level of stimulation, should an individual be subjected? These impacts are partly a matter of biological judgement, since animals may manage better if exposed to a moderate level of stimulation, even if it is aversive, rather than being protected from stimulation entirely. However, ethical considerations dictate that there must be a limit. The ethical issues involved in this are surveyed and a guide to making ethical decisions about animal stress and welfare and putting it in a world context are presented. In order to put these questions into perspective, world problems such as anti-microbial resistance, climate change and reductions in sustainability are considered. Ethical aspects of interactions between humans and other species are discussed and possible solutions for the future are presented. Keywords Welfare · Ethics · Animal use · Sustainability · Climate change · Antimicrobial resistance

8.1

World Problems

Many people who are asked to consider world problems think only of current human problems. This is the major reason for the greatest world problems today. Firstly, because the “world” does not just contain humans and secondly, because human actions today have an effect on the world in the future as well as today. For much of human history, life was considered to involve a series of battles between people and a difficult and dangerous world. This view persists in the frontier spirit, where people still try to conquer nature, and in the extremely anthropocentric attitude where humans think that all world resources are there for them to exploit without questioning the consequences. In this chapter, value systems will be briefly discussed and then some of the major world issues considered. Whilst all of the issues mentioned are relevant to questions about stress and welfare systems and impacts, some specific links to such impacts will be considered in more detail. A key general point is that when decisions have to be taken about animal welfare, other © Springer Nature Switzerland AG 2019 D. M. Broom, K. G. Johnson, Stress and Animal Welfare, Animal Welfare 19, https://doi.org/10.1007/978-3-030-32153-6_8

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important issues of sustainability should also be considered. Similarly, when there are decisions about human welfare, these should also take account of what would be best for the wider world. What are the greatest problems in the world today? If we focus on humans, the view of the writer is that the greatest problem is anti-microbial resistance, followed by climate change and unsustainability of human activities including poor use of world resources. These are more important than terrorism, or crime, or human hunger. The first two issues are considered briefly below and sustainability of food production and the role of animal welfare in it is discussed at greater length. If we do not focus on humans, anti-microbial resistance is important to animals kept by humans but not to the majority of animals so climate change is the most important problem.

8.2

Value Systems

Humans and other sentient beings are referred to by many philosophers as moral agents so they can be the subject of moral actions and have moral value. The question of which human or non-human individuals have moral value is important in decisions about how to treat each one. Gert (1988) states that an act is morally relevant if it is done to: “existing or potential sentient beings”. Some writers, such as Rolston (1999) do not think of non-humans as moral agents. Rottschaefer (1998) refers to considering “ourselves” as moral agents but, in doing so, non-humans are not excluded from being “ourselves” and hence moral agents. Many non-human animals, especially those living socially, have been described as avoiding causing harm to others or acting in ways that directly benefit others (de Waal 1996; Broom 2003), i.e. acting in a moral way. Hence it seems illogical to say that the individuals concerned are not moral agents. Even for those who do not think of non-humans as being moral agents, they can be the subject of moral actions and so have moral value. Increased knowledge of the functioning of humans and of other animals has led to a change in who are included in “we” or “us” when we consider our moral obligations. Firstly increasing proportions of humans and secondly more kinds of non-human animals, are included as “us” when moral obligations are being considered (Broom 2003, 2014). When holy books say that “we” have been given dominion over, or responsibility for, the world, who are included in “we” or “us”? It now seems more logical to include all sentient beings as part of we or us. Two kinds of approach to how each individual decides how to act are the deontological, based on our duties, and the consequentialist, in which the cost and benefit consequences of actions are balanced. In practice, most people use both as there are some obligations that are paramount, some harms that are never done, and much evaluation of costs and benefit of actions. Each individual, especially those of a social species like humans, learns what are the consequences of actions and what

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are obligations to others. Of course, each individual has the genetic potential to do this (see Chap. 1). During development, there has always been learning about harms resulting from own actions, for example, if you push someone they may fall over and in some circumstances may fall down a cliff or under a bus. Hence we sentient beings are all very careful to assess risks and avoid harms throughout most or all of our lives. Our moral code includes the social component of condemning, and changing behaviour towards, those who do not behave in this way (Broom 2003, 2006, 2019b). Anti-social, immoral behaviour leads to punishment, ostracism or exclusion from the group. As the information available to each individual becomes more accurate, a wider view of the world is possible. Some of actions that were thought of as innocuous or desirable are now seen to have negative consequences to such a degree that they are viewed as morally questionable, or certainly immoral. If sewage or industrial effluent is put into a small river in order to safely remove it from a local community, this action can cause the deaths of many thousands of animals, the loss of a drinking water resource and the loss of human livelihoods for people downstream. If many people switch on their air-conditioning every day, a low-lying community in Bangladesh or Vanuatu may be permanently flooded. Both of the initial actions have to be viewed in a different way when the knowledge of the consequences is appreciated, as has the action of developing large weapons with possible wideranging effects. Sadly, the need to assess all risks and to consider all consequences of any development has not, so far fitted well with: the frontier spirit, maximise innovation for me now, the market will decide, attitude. If sentient life on earth is to survive, there must be rapid change towards a risk assessing society that preserves what is important in the world. Decisions about what might be considered justifiable impositions on non-human animals depend on our value systems. Each person has a private attitude, an aspect of their personal philosophy that is probably not clearly defined, or easy to enunciate but is based on reading, observation and discussion. This may or may not coincide with community value systems arising from family, religion, culture, or some other social belief. They will rarely be upheld unanimously in the population, but may be supported by a sizeable proportion of it and perhaps be reinforced by legislative control. For example, some societies demand a certain minimal level of treatment for animals, and have legal injunctions against cruelty. On the other hand, some societies accept and perhaps expect that people will impose on animals as part of rituals such as bull-fighting, game-hunting, or particular procedures of animal slaughter or sacrifice. Judgement as to whether acts causing distress to animals are justifiable or not is made by relating them to both one’s personal philosophy and to the current expectations of society. The objective scientific measures of stress and welfare described in earlier chapters can provide part of the answer to whether society should sanction a particular activity but the decision also depends on public and private attitudes as to what is ethically acceptable.

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Anti-Microbial Resistance

Most organisms have some capability to defend against bacterial infection. Humans have sophisticated systems to counter bacteria, viruses and other pathogens and parasites. However, the discovery and development of antibiotics has saved very many human lives and very many lives of animals used by man. Anti-parasitic and other anti-microbial chemicals have also extended the lives of treated humans and other animals. Human culture has many components that are associated with avoidance of, or defence against, disease but the major infectious diseases were terrifying to people only a few generations ago. Most families lost members to tuberculosis before the 1950s. Extensive misuse of antibiotics by human patients who did not understand the potential impact of their actions has been the major cause of accelerated development of bacterial strains resistant to some or all antibiotics. People demanded antibiotics when they had viral infections that are unaffected by antibiotics or when they had no infection at all. Other actions by patients whose consequence is that resistant bacterial strains are more likely to develop include: failure to complete courses of antibiotic treatment and the very damaging practice of disposal of antibiotics into the sewage system. Medical practitioners sometimes gave in to such patient pressure but are now being much more careful to minimise antimicrobial usage. People with viral infections are usually not now given antibiotics to reduce the risk of secondary bacterial infections unless this risk is high. On farms, antibiotics have been used as growth promoters or misused in the same way as by human patients (Ungemach et al. 2006). It is estimated that 65% of antimicrobial usage by weight is for farm animals (EU data from ECDC/EFSA/EMEA/SCENIHR 2009). However, the number of individuals treated is a more relevant figure when considering the risk of development of resistant strains of bacteria. The dose of antimicrobial given to an individual is related to body weight. Because farm animals are a mean of 2.4 times the weight of a human, calculations using the EU data are that the number of treatments with antimicrobials is 44% for farm animals and 56% for humans. For the antimicrobials assessed by WHO as the most important for humans, because they are the last resort against resistant bacteria, the figures for the use for farm animals are declining and, at the time of writing, are 36% of total use by weight and 19% by treatments. The use of antimicrobials as growth promoters is becoming illegal in more and more countries. The consequence of the development of resistant strains of pathogenic bacteria is that more people and more animals kept by people are dying of formerly treatable diseases. For example, Paterson et al. (2014) reported that methicillin resistant Staphylococcus aureus (MRSA) had been found and had caused mortalities in 14 different host species of farm, wild and companion animals. At the current rate of development of resistant strains it is likely that hundreds of millions of people will die of tuberculosis and other formerly treatable diseases 30 years from now. The World Health Organization in 2019 estimates that 25% of all people carry Mycobacterium tuberculosis, the bacterium that causes the disease. It is not likely that new anti-microbials can be developed fast enough to replace the strains of anti-microbials

8.5 Sustainability

197

that no longer function. This development of anti-microbial-resistant pathogens is the greatest threat to human welfare and to the welfare of animals kept by man. The risk of development of resistant strains is much greater in some countries than in others. The risk is greatest in those countries where the antimicrobial can be obtained by users without prescription by a medical doctor or veterinarian and where prescribers are easily persuaded to prescribe when they should not. Every human patient and every farmer in the world should respond to this dangerous situation. Further information is available from the World Health Organization WHO https://www. who.int/antimicrobial-resistance/en/ and the Food and Agriculture Organization of the United Nations FAO http://www.fao.org/antimicrobial-resistance/en/ and the World Organization for Animal Health OIE http://www.oie.int/en/for-the-media/ amr/.

8.4

Climate Change

Information about the production of greenhouse gases resulting directly from human activities has been available for many years (e.g. Preston and Leng 1989). Humans produce carbon dioxide by burning oil, gas, coal and wood. Until recently, almost all road motor vehicles, aeroplanes, trains and ships burned oil and produced greenhouse gases. The heating and air-conditioning of buildings by use of fossil fuels produces greenhouse gases. Disturbance of soil by tillage and ploughing for agriculture (Pagliai et al. 2004) and by excavation for mineral extraction produces greenhouse gases. Ruminants and, to a lesser extent, all other animals produce greenhouse gases in their gut. All of these must be reduced if climate change is to be avoided. Greenhouse gas production can be reduced by modified feeding and land management systems. Maintaining resources, such as soil with good structure, and retaining water that might be lost from the soil are important objectives, as are minimising usage of carbon-based energy and imported fertilisers. In some areas the change caused by greenhouse gases is increased temperature and desertification. In others it is increased occurrence of violent storms. The melting of the polar ice-caps and mountain glaciers is increasing water flow and sea-level so that areas are temporarily or permanently flooded. Information from the United Nations on climate change can be found at http://www.un.org/en/sections/issuesdepth/climate-change/index.html. No reputable scientist now doubts that the climate change that is occurring at present is caused mainly by human action.

8.5

Sustainability

For any production system, including those where it is human food that is being produced, a key question is whether or not it is sustainable. Sustainability now has a much wider meaning than it had in early writings on the subject. The ethics of the

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production method are now included and a system can be unsustainable because of negative impacts on human welfare, on animal welfare, or on the environment. A definition of sustainability is: a system or procedure is sustainable if it is acceptable now and if its expected future effects are acceptable, in particular in relation to resource availability, consequences of functioning and morality of action (Broom 2014, modified slightly after Broom 2001, 2010). What is taken into account when consumers are evaluating goods as high quality? The factors that people consider when they buy food or other goods has been changing. Whilst quality still includes immediately observable aspects and the consequences of consumption, for many people the ethics of the production method is now included. Modern consumers require transparency in commercial and government activities and take account of the ethics of production when they evaluate product quality (Broom 2010, 2017). What makes a food production system unsustainable and results in product quality being judged as poor? Each of the following seven negative impacts of production can lead to consumers not buying a product and can now be measured in an objective way.

8.5.1

Adverse Effects on Human Welfare, Including Human Health

Food products are not just evaluated in relation to taste and price. If they cause people to become sick, the quality is considered poor. Some foods are regarded as being better for the health of the consumers because of the nutrients present in them. A major effect on animal production in recent years, as a result of attempts to provide a healthy diet for people, has been the dramatic increase in the production of farmed fish, in part because they contain polyunsaturated fats (Wall et al. 2010). Another impact, as explained above, is that in all aspects of life, the use of antibiotics and other antimicrobials will have to decrease, in most countries via new legislation.

8.5.2

Poor Welfare of Animals

Many consumers will not buy animal products if there is close confinement of animals, individual rearing of social animals such as pigs and cattle, and other systems for housing and managing animals that do not meet the needs of the animals. A result of this is the increase in the number of people who decide to become vegetarian or vegan. Other people just decide not to buy particular animal products. Hence some widely-used animal housing systems are unsustainable (Broom 2017). Animal welfare is a key aspect of sustainability and product quality and for many consumers is the first consideration when deciding what they will purchase.

8.5 Sustainability

8.5.3

199

Unacceptable Genetic Modification

The use of genetically modified plants is not accepted by some consumers and few people accept the use of genetically modified or cloned animals. All cloning of farm animals is associated with poor welfare of animals and this is the reason why it is not permitted in the European Union (Broom 2014, 2018a). The public’s antipathy to genetic modification and cloning is partly dislike of modifying what is natural. Another aspect is that modified organisms may have allergenic proteins and many of the public do not believe that proper checks on such possibilities are in place (Lassen et al. 2002). Animals which are genetically modified may have welfare problems so there should be checks, using a wide range of welfare indicators, before modified animals are used in any way (Broom 2008, 2014).

8.5.4

Harmful Environmental Effects

Agricultural methods that result in low biodiversity are a consequence of widespread herbicide and pesticide use and are perceived to be the norm by many farmers and some of the general public. However, such a change is far from inevitable and agricultural systems that lead to much greater biodiversity on farmland could be used. Livestock production can also result in pollution, locally and on a world-wide scale, e.g. via greenhouse gas production. There has been over-exploitation of all open water fish and of whales. Widespread extinction of species is occurring very rapidly now. In some cases this occurs because of a specific use, e.g. feathers, ivory or rhino horn, but whole habitats are disappearing because of human activity. A livestock farming component that has led to a dramatic environmental effect is the widespread death of vultures in India caused by the use of the veterinary drug diclofenac (Green et al. 2004). The population declined to only 3% of its former level but is starting to recover following legislation. In temperate and tropical countries a dramatic example is that in the last 20 years we have seen the greatest decline in farmland birds, butterflies, bees and wild plants ever recorded. This is principally because of the use of herbicides but also because of pesticide use. These examples raise the question of what we want in our environment. Do we need vultures in India or farmland birds and butterflies in the UK or USA?

8.5.5

Inefficient Usage of World Food Resources

At present, there is often very inefficient usage of food and energy resources. Much human food used in homes, sold in restaurants and sold in shops is wasted. Some food for farmed animals is wasted. Almost all of this waste could be prevented. In

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addition, much food that humans could eat is fed to animals that are then eaten by people. This is a much less efficient process than for the humans to eat the food directly. What can be done in animal production to exploit existing resources better (Herrero et al. 2010)? The most important animals for food production are those that eat food that humans cannot eat. Hence animals eating forage plants, not cereals, are much more important than pigs or poultry that compete with humans for food (Broom et al. 2013). Similarly, herbivorous fish are more important than those fish that eat other fish. Land used for agriculture is sometimes degraded because of poor management, for example repeated tillage and use of the same crops, so is not exploited efficiently. Too much energy from fossil fuels is used in cultivation and transport of feed and products, as well as in production of fertilisers and other materials and equipment.

8.5.6

Not “Fair Trade”: Producers in Poor Countries Do Not Receive a Fair Reward

Consumers in many countries have now discovered that producers of food in poor countries are often not properly rewarded for their work. Most profits from the sale of some basic products bought by many people have been found to go to large companies. This is considered morally wrong by most consumers and, as a consequence of publicity about unfairness to poor producers, products like coffee, cocoa and fruit are among those that are independently checked and have a Fair Trade label (Nicholls and Opal 2005). Under these schemes, the producers receive a larger part of the money paid by shoppers.

8.5.7

Not Preserving Rural Communities

Small-scale rural farmers are often out-competed by large-scale production, with the result that local communities disappear. The general public often find this unacceptable so schemes are introduced by governments to safeguard such communities. Consumers may also buy locally-produced products, regarding this as a part of product quality. In the European Union, subsidies to preserve rural communities have prevented rural people migrating to towns and hence large cities becoming ever larger as has happened in most of the world, a major success of the EU Common Agricultural Policy (Gray 2000; Broom 2010).

8.6 How Humans Impose on Other Animals: And Vice Versa

8.6 8.6.1

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How Humans Impose on Other Animals: And Vice Versa The most Successful Animals

Which is the most successful animal in the world? In terms of numbers of multicellular animals, it is likely to be marine and a parasite. About 80% of the earth’s surface is sea and animals usually carry many parasites. The most numerous freeliving animal is probably a planktonic copepod crustacean and the commonest animal could be a parasite of those copepods. Amongst land animals, the most numerous animal may be a springtail, a small insect that lives in soil, or one of the smaller species of ants. There are several species of ants and of termites that are more numerous and have a greater biomass than humans. Humans modify many areas of the world but so do corals, ants and termites. Plants modify the world much more than animals do. All of such facts place the human impact in some perspective. However, humans do have some very wide-ranging effects and some extreme effects. The rate of extinction of living species, as a result of human actions, is greater now than it has ever been. Most people would say that it is morally wrong for people to cause the extinction of even a single plant or animal species but would not know what could be done to prevent it. Since humans modify large areas of the world, animals that can adapt to humanmodified conditions and can utilise human resources are likely to be numerous. Wolves exploited humans and encouraged collaboration with humans. In circumstances where wolves and humans sought the same prey, wolves were very good at finding the prey and chasing fast for short distances. Humans were good at chasing for long distances and killing prey that were large or hiding, for example in a tree. Hence both species benefitted from collaboration with the other and both would share food with fellow hunters. We can reasonably say that wolves domesticated humans and adapted themselves slightly to become dogs thus increasing the efficiency of exploitation. Of course most humans assume that they were the active party! The most successful animal in the exploitation of humans, that is to say in increasing its population as a result of interactions with humans, is the chicken. This tropical, Asian jungle bird is the commonest bird in the world because of its ability to live with humans. It is numerically successful but the welfare of most is not good. Other animals that successfully exploit humans include rats, mice, crows, starlings, house sparrows, house flies and many other insects. Many parasites and pathogens are common because they exploit humans.

8.6.2

Numbers of Animals Kept by Humans in Relation to Welfare Problems

The world populations of several species of animals kept by humans are greater than the world population of humans. The most numerous animals kept by people are

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farmed animals, the commonest being the broiler chicken. How do people view numerous animals? The concept of welfare applies to every individual animal but there is sometimes a tendency for the welfare of the individual to be considered less when the animals are numerous. In Europe there are more than 4000 million chickens kept for meat production (Broom 2017). The second commonest farmed animal in Europe is the trout, about 1000 million, and the third commonest is the Atlantic salmon, about 440 million. The remainder of the domestic fowl kept in Europe are about 400 million laying hens and tens of millions of parent birds kept for breeding broilers and laying hens. Other numerous farm animals include farmed rabbits, 340 million; ducks, 170 million; and turkeys, 150 million. The totals in the EU of the commoner large farm mammals are: pigs 148 million, bovines 88 million, sheep 83 million and goats 10 million (Eurostat). Companion animals are much less numerous than farm animals. There are about 99 million cats and 65 million dogs (www.statista.com) in Europe but many more aquarium fish. Animals used for experimental purposes total about 11 million. Whilst this last figure is far from trivial, the much greater importance of poor welfare in the commoner farm animals is clear. If most of the individuals of a numerous animal kept by people have a severe welfare problem, the total of poor welfare is high. At present, some of the worst animal welfare is that of broiler chickens during the latter part of the growing period when a high proportion of birds have leg and other disorders because of the fast growth caused by genetic selection and ad libitum food provision (EFSA 2010). The pathological condition causes much pain and other poor welfare. Since this a problem of thousands of millions of animals, it is the greatest animal welfare problem in the world. Close confinement of sows and calves, and the keeping of hens in small battery cages are rated by welfare scientists and consumers as extremely important causes of poor welfare. In parts of the world where there is no legislation preventing close confinement and hence the worst welfare in these animals; the problems of such sows, calves and hens are very great. There is a great magnitude of poor welfare in pigs reared for meat production in most parts of the world because the space and resources provided are insufficient and the needs of the animals are not met (EU SVC 1997; EFSA 2006, 2007a). Growing pigs need material to manipulate, or substratum in which to root. If this, and adequate food and water, are not provided there is a high risk that tail-biting and other abnormal behaviours associated with poor welfare will occur. Another important farm animal welfare problem is that of the high-producing dairy cow (EFSA 2009). Dairy cows producing large quantities of milk have high levels of leg disorders, mastitis and reproductive disorders. The proportion of cows affected by one or more of these disorders is high and the animals live with the poor welfare for a substantial part of their lives so the overall extent of the welfare problem is very great. There is rapid expansion in fish-farming and it is likely that the commonest farmed animal will soon be a species of fish. However, there is limited information about the welfare of the most widely farmed fish: Tilapia, carp and grass carp. There

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is more information about trout and salmon welfare. The welfare of farmed trout and salmon can be very good but stocking density is often too high and there can be major problems caused by insufficiently oxygenated water or by disease (EFSA 2007b, 2008). Many salmon and some trout are subject to fin-chewing by other fish, a behaviour that is principally the result of high stocking density. The fins are sensitive tissue so there will be pain if they are chewed. Also, the fins are of key importance in locomotion so substantial reduction in fin-size impairs normal function. Inspectors or consumers who know what intact fins look like can readily see that fins have been chewed when checking or buying fish, hence chewed fins are good welfare-outcome indicators (Santurtun et al. 2018). The poor welfare in salmon and trout is quite severe and often of long duration so the magnitude of the problem is high. The numbers of animals are hundreds of millions so the extent of the problem is great.

8.6.3

Ethics of Killing and Welfare

Slaughtering an animal, if done to alleviate human starvation is, in the minds of many people, justified. Slaughtering an animal to satisfy a person’s penchant solely for killing is, for many people, not justified. The acts may be identical, the objectively assessed welfare of the animals may be identical, but the justification for the acts is different. The law in most countries treats the two situations in very different ways. There are detailed regulations aimed at minimising suffering in the case of killing in a slaughterhouse but often no regulations limiting the suffering of animals that are hunted. Indeed the hunted animal can be killed inhumanely and can be subjected to extreme fear, pain and other suffering without any legal protection. The laws are based on quite different assumptions. If a decision on this issue seems straightforward, consider a dilemma any one of us may have to face. You, or someone in your family, has a painful and debilitating medical condition which you are told may be curable by a radical new therapy. You are also told, however, that it is possible that the treatment could be more distressing than the complaint, so medical advisors suggest it should first be tested on laboratory animals. Would you feel justified in imposing this test for your own benefit if it caused slight effects on an animal’s welfare, or quite severe effects, or very severe effects? Would it be reasonable to cause such effects in 1 mouse or 100 mice, 1 or 100 dogs, or 1 or 100 chimpanzees? Is it acceptable for pest insects to be exterminated because they are eating plants used as human food; or for experiments to be carried out on a few animals in order to improve the welfare of many more animals; or to kill pet animals because they are preying on other species? Returning to an issue raised in Chap. 1 and continued earlier in this chapter, how are humans different from other animal species? There are many similarities. Humans use certain animal species for transport; so do some insects and sucker fish. Some humans live on the flesh of animals; some animals live on the flesh of

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humans. Some humans live in highly structured societies with division of labour; so do some insects, birds and other mammals. Humans nurture and defend offspring until they are self-sufficient; so do many other species. Some humans hunt and slaughter more animals than is necessary to provide food; so, sometimes, do foxes and dogs. Humans farm plants and animals whilst many of the commonest ants and termites farm fungi and aphids. Animals of many species, including humans, have physiological mechanisms and behave in a way that indicates that they experience pain, anger, fear and love. Many non-human social animals plan for the future, behave in a way that indicates that they evaluate what concepts other individuals have, communicate in a manner that most would call language, and show moral behavior and some components of religion (Broom 2003, 2019b). So is there any important difference between man and other animals? The answer would seem to be a matter of degree. Humans are better than all other animals in relation to some abilities but other species are better than humans in some abilities.

8.7

Setting Ethical Limits to Assessed Welfare

It is clear that some human imposition on animals is unavoidable. The level of imposition should be minimized but with what limits? These limits could, theoretically, be absolute or relative. Some would be limits on what people are permitted to do but others would be defined by the consequences for the animals. A human action might be allowed unless the welfare outcome is too negative. Absolute values of coping ability are difficult, if not impossible, to prescribe, since the responses of different animal species to various impositions are highly variable. In practice, limits are therefore relative, and to some extent arbitrary, though ideally they will be logical and justifiable. Three comparisons for establishing standard limits for welfare are now considered.

8.7.1

Animals in a Natural Environment

Impositions on animals could be deemed acceptable if they impose no greater strain on the animals than that which they experience in their natural state. This is an attractive proposition in concept, but, for most species, unrealistic in practice for several reasons. Firstly, the strains on free-living animals are not adequately documented. Secondly, intervening in the life of an animal to estimate its level of strain could increase that strain to an extent that would be hard to determine. A third problem is that livestock and companion animals must have changed during the millennia of domestication. What animal should we compare with our present-day animals? Should a dairy cow be compared with an aurochs or a feral cow, and under what conditions? A free-living dog, with skills honed in the wild to hunt and escape, seems hardly the appropriate animal to indicate, by comparison,

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whether a house-dog is being provided with appropriate conditions. A final, particularly important problem arises from the fact that many animals die in the wild as a result of disease or predation. Most people consider that whenever we use animals we have obligations to care for them so that they do not die of disease and predation. The idea of relating animal welfare to experience in the wild is probably acceptable only in order to set a minimum standard. The practical difficulties of setting up welfare standards are formidable. However, valuable information does come from studying untamed animals or feral animals that have returned to the wild. For instance, the observations by Stolba and Wood-Gush (1989) and Jensen (1989) of domestic pigs roaming free outdoors provide valuable indicators of what aspects of an animal’s life are of importance to it.

8.7.2

Humans under the Same Strain

A feature of the general indices of stress, strain and welfare described in Chaps. 5, 6 and 7 is their applicability to many species, including humans. Levels of plasma cortisol, β-endorphin, adrenaline, or heart rate are likely to be altered in most animals subject to short-term stress. This parallel response could permit some comparison between humans and other animals. A human appreciation of what an animal might experience could perhaps be derived by noting which impositions elicit comparable strain. For example, suppose that the behavioural and hormonal disturbance of a calf during dehorning elicited the same response as that measured in a person having an intramuscular injection; in that case, it might be deemed tolerable. If, however, dehorning were comparable to a tooth extraction without anaesthetic, it might be considered unacceptable. However, once again complications intrude for, in a country where people do have tooth extractions without anaesthetic, the judgement as to what is an acceptable imposition on animals would be different. Does the level of acceptable animal welfare depend on the level of human tolerance of discomfort or pain? That would be the logical conclusion if we used this approach. Comparing species will also undoubtedly highlight disparities between indices, as there is interspecific variation in the coping methods used, so comparisons will not necessarily agree for all indices. That aside, the approach has the attraction that the impact of a stress on some non-human species can be interpreted in terms that are meaningful to a human.

8.7.3

The Informed and Compassionate Arbiter

Perhaps the most realistic procedure for determining limits of welfare is to use the judgement of one, or a panel of, human arbiters who take account of the biological characteristics of the animals, including their response to difficult conditions. Such

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people can weigh up the complexity of factors: the comparison of aggregate discomfort with perceived benefit. Given the biological inclination for animals, not least humans, to pursue their self-interest, the procedure is obviously sensitive to the influences of human inadequacies and biases. Systems to monitor this by giving agreed weighting to various aspects of a decision have been proposed in relation to pain by Bateson (1991). The earlier proposals to use the behaviour of undomesticated animals or human strain equivalents for comparison could also provide independent checks of, and complements to, ethical decisions. One implication of a scheme using arbiters is that standards of acceptable animal welfare are not absolute, but change with improvements in knowledge of welfare indicators and with society’s expectations. As already noted concerning comparisons of strains in humans and nonhumans, considerable differences in attitude are bound to exist. This will surprise no one in a world where commendable, agreed international declarations about human welfare are often swept aside by tides of political expediency. Despite dreams that it might be otherwise, acceptable impositions on animals will alter from peacetime to wartime, and in times of plague and famine. This does not imply that objective analyses of stress and welfare are worth nothing, quite the reverse. Measurements of welfare have been refined by increases in knowledge so we now have more precise information about whether or not an animal is suffering. Whether that suffering will or will not concern human society will depend on that society’s current preoccupations and priorities. Because of the need to reflect society’s views, making decisions about animal welfare must involve an opportunity for society to be represented and cannot rest solely with the scientists making the measurements. In some areas, this mechanism for public representation already exists in the form of membership of appropriate committees, e.g. Animal Experimentation Ethics Committees. In other circumstances, inspectors answerable to the government, and only more distantly to the electorate, judge what is currently acceptable to society, as is the case with the Home Office Inspectorate in the UK. In all such situations, decisions about animal welfare should be made by people who have a knowledge of, and an empathy with, non-human animals. Such people should understand animal welfare science and be aware of society’s expectations, both when these are embodied in laws and when they are otherwise advocated by the community.

8.8

Food Production Systems for the Future

What is the future for the production of food and other goods in the world? As explained by Broom (2018b), consumers in more and more countries have concerns about healthy food, biodiversity and animal welfare. There is an ever-increasing number of people with the view that we must provide for the needs of the animals that we keep and that we must use world resources more efficiently. In order to do

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this we should consume more plants and fewer animals. As mentioned above, if grain is produced, it is more efficient for people to consume the grain directly than for it to be fed to animals, with much loss of energy in the process, and then to consume the animals. Where meat is consumed, it should come mainly from animals eating food that humans cannot eat. Hence we should concentrate on producing mammals, birds, fish, etc. that can eat primary plant products like leaves. As a consequence, ruminants, that get their nutrients from leaves, are much more important than pigs or poultry that compete with humans for cereals and soya. A question which arises as a consequence of such arguments is “should we stop animal production and just produce plants?” If the basis upon which this will be decided is to do with the efficient utilisation of world food resources, the answer is no. We should reduce animal production. However, approximately 45% of land in the world is good for producing food for herbivores but not for producing plants as human food. If we stopped production of animals for human consumption, this land would produce almost no food for people. The remainder of the land would have to be farmed more intensively and there would probably be major food shortages. Of the food that is produced for human consumption, as much as 30% is wasted. In order to use that which would otherwise be wasted, some could be fed to other animals. For example, after it is treated to prevent the spread of disease, much could be fed to pigs (zu Ermgassen et al. 2016). A further factor is that most of the world surface is sea and there is potential for it to be better used for producing marine plants and animals for human food. A further question to consider is “is it morally right to consume animals?” The answer to this question depends upon which moral issues are considered the most important. For some people, the main view is that it is objectionable to consume animals or animal products. I see this as principally an aesthetic question but some others do not. People for whom this is the paramount issue, will not eat animals. A second moral argument is that “it is wrong to consume animals because we should not kill animals”. However, this argument does not logically lead to vegetarianism because large numbers of animals are killed in plant production. Some are small soil animals. Others are mammals, birds and insects that we call pests. Other animals die or are prevented from living at all in order that crop production methods can be used (Broom 2018b). Per unit of human food, some animal production methods allow far more animals to survive than some plant production methods. A third position is that we have an obligation to use animal production methods only where animal welfare is good. Where animal welfare is viewed as a part of sustainability, this position can be rewritten as all food production systems should be sustainable. Returning to the initial questions, it is clear that, if we stop or reduce animal production methods that misuse world resources, more food can be produced. We should concentrate on farming herbivorous mammals, birds, fish and perhaps insects or molluscs that can be fed grass, leaves and other plant products which humans cannot digest efficiently.

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Sustainable Animal and Forage Plant Systems

For many years we have been talking about grazing systems. The key plants have all been pasture plants. Trees and shrubs have been mainly considered as competitors for the pasture plants. Yet plant production from a mixture of herbs, shrubs and trees is much greater than from a single layer pasture system. Some shrubs and trees provide good food for ruminants and other animals, including herbivorous fish. Shrubs such as Leucaena have been used as forage for ruminants for many years. However, most animal production is still from pasture only. Work in Colombia, Mexico and Brazil on semi-intensive, three-level, rotational, silvopastoral systems has now reached a point where revolution is starting. This is because semi-intensive silvopastoral systems with grasses, leucaena Leucaena leucocephala or other protein-rich shrubs and trees, often with edible leaves, produce more forage and more animal product than monoculture pasture-only systems (Murgueitio et al. 2008). In addition, the welfare of the animals is better, including less disease; biodiversity is much greater; worker satisfaction is high; soil quality, including water-holding capacity, is much increased; there is less water run-off; conserved water use is six times less than feed-lot systems; there is 30% less greenhouse gas production per kg meat; there is better carbon sequestration; and the land area needed for beef production is 42% of that for feed-lots (Broom et al. 2013; Broom 2019a). Especially during dry periods when herbs and shrubs are less productive, the leaves of trees like ramón (Maya nut) Brosimum alicastrum can be cut and fed to livestock. Shrubs and trees that are too high for animals to reach can be cut and fed to ruminants or fish. This development can be taken up in many parts of the world now but, for the future, another step is to collect and eat the insects that feed on tree leaves. This means planting forests for farming.

8.9

Stress and Welfare in the General Ethical Framework

An understanding of stress and welfare and how to assess them is not isolated from major world issues but is relevant to several aspects of these. Concerns about one ethical issue should always be related to other ethical issues when decisions about action are being taken. Some of the topics discussed in this and earlier chapters are considered further in Chap. 9.

References Bateson P (1991) Assessment of pain in animals. Anim Behav 42:827–839 Broom DM (2001) The use of the concept animal welfare in European conventions, regulations and directives. In: Food chain. SLU Services, Uppsala, pp 148–151

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Broom DM (2003) The evolution of morality and religion. Cambridge University Press, Cambridge Broom DM (2006) The evolution of morality. Appl Anim Behav Sci 100:20–28 Broom DM (2008) Consequences of biological engineering for resource allocation and welfare. In: Rauw WM (ed) Resource allocation theory applied to farm animal production. CABI, Wallingford, pp 261–275 Broom DM (2010) Animal welfare: an aspect of care, sustainability, and food quality required by the public. J Vet Med Educ 37:83–88 Broom DM (2014) Sentience and animal welfare. CABI, Wallingford Broom DM (2017) Animal welfare in the European Union. European parliament policy department, citizen’s rights and constitutional affairs, Brussels Broom DM (2018a) Animal welfare and the brave new world of modifying animals. In: Grandin T, Whiting M (eds) Are we pushing animals to their biological limits? CABI, Wallingford, pp 172–180 Broom DM (2018b) The scientific basis for action on animal welfare and other aspects of sustainability. In: D'Silva J, McKenna C (eds) Farming, food and nature: respecting animals, people and the environment. Earthscan, London Broom DM (2019a) Land and water usage in beef production systems. Animals 9:286. https://doi. org/10.3390/ani9060286 Broom DM (2019b) The biological basis for religion and religion’s evolutionary origins. In: Feierman J, Oviedo L (eds) The evolution of religion, religiosity and theology: a multi-level and multi-disciplinary approach, chapter 4. Routledge, London Broom DM, Galindo FA, Murgueitio E (2013) Sustainable, efficient livestock production with high biodiversity and good welfare for animals. Proc R Soc B 280:20132025. https://doi.org/10. 1098/rspb.2013.2025 de Waal F (1996) Good natured. Harvard University Press, Cambridge, MA EFSA (2006) The welfare of weaners and rearing pigs: effects of different space allowances and floor types. EFSA J 268:1–19 EFSA (2007a) The risks associated with tail biting in pigs and possible means to reduce the need for tail docking considering the different housing and husbandry systems. EFSA J 611:1–13 EFSA (2007b) Concerning animal welfare aspects of husbandry systems for farmed fish in relation to Atlantic salmon. EFSA J 736:1–31 EFSA (2008) Concerning animal welfare aspects of husbandry systems for farmed trout. EFSA J 796:1–22 EFSA (2009) Scientific report and opinions on the effects of farming systems on dairy cow welfare and disease. EFSA J 1143:1–38 EFSA (2010) Scientific opinion on the influence of genetic parameters on the welfare and the resistance to stress of commercial broilers. EFSA J 1666:1–82 EU Scientific Veterinary Committee (1997) The welfare of intensively kept pigs. EC Doc XXIV/ B3/ScVC/0005/1997, Brussels. http://europa.eu.int/comm/food/fs/sc/scah/out71_en.pdf Gert B (1988) Morality: a new justification of the moral rules. Oxford University Press, New York Gray J (2000) The common agricultural policy and the re-invention of the rural in the European Community. Sociol Rural 40:30–52 Green RE, Newton I, Schultz S, Cunningham AA, Gilbert M, Pain DJ, Prakash V (2004) Diclofenac poisoning as a cause of vulture population declines across the Indian subcontinent. J Appl Ecol 41:793–800 Herrero M, Thornton PK, Notenbaert AM, Wood S, Msangi S, Freeman HA, Bossio D, Dixon J, Peters M, van de Steeg J, Lynam J (2010) Smart investments in sustainable food production: revisiting mixed crop-livestock systems. Science 327:822–825 Jensen P (1989) Nest site choice and nest-building of free-ranging domestic pigs due to farrow. Appl Anim Behav Sci 22:13–21 Lassen J, Madsen KH, Sandøe P (2002) Ethics and genetic engineering – lessons to be learned from GM foods. Bioprocess Biosyst Eng 24:263–271 Murgueitio E, Cuartas CA, Naranjo JF (2008) Ganadería del Futuro. Fundación CIPAV, Cali

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Nicholls A, Opal C (2005) Fair trade. Sage, Thousand Oaks, CA Pagliai M, Vignozzi N, Pellegrini S (2004) Soil structure and the effect of management practices. Soil Tillage Res 79:131–143 Paterson GK, Harrison EM, Holmes MA (2014) The emergence of mecC methicillin-resistant Staphylococcus aureus. Trends Microbiol 22:42–47. https://doi.org/10.1016/j.tim.2013.11.003 Preston TR, Leng RA (1989) The greenhouse effect and its implications for world agriculture. The need for environmentally friendly development. Livest Res Rural Dev 1:1–5 Rolston H (1999) Genes, genesis and god: values and their origins in natural and human history. Cambridge University Press, Cambridge Rottschaefer WA (1998) The biology and psychology of moral agency. Cambridge University Press, Cambridge Santurtun E, Broom DM, Phillips CJC (2018) A review of factors affecting the welfare of Atlantic salmon (Salmo salar). Anim Welf 27:193–204. https://doi.org/10.7120/09627286.27.3.193 Stolba A, Wood-Gush DGM (1989) The behaviour of pigs in a seminatural environment. Anim Prod 48:419–425 Ungemach FR, Müller-Bahrdt D, Abraham G (2006) Guidelines for prudent use of antimicrobials and their implications on antibiotic usage in veterinary medicine. Int J Med Microbiol 296:33–38 Wall R, Ross RP, Fitzgerald GF, Stanton C (2010) Fatty acids from fish: the anti-inflammatory potential of long-chain omega-3 fatty acids. Nutr Rev 68:280–289. https://doi.org/10.1111/j. 1753-4887.2010.00287.x zu Ermgassen EKHJ, Phalan B, Green RE, Balmford A (2016) Reducing the land use of EU pork production: where there’s swill, there’s a way. Food Policy 58:35–48

Chapter 9

Stress and Welfare in the World

Abstract The major arguments presented in the book are summarised in this chapter. How can stress be evaluated and minimised and how can welfare be assessed in a scientific and objective way. When we have information about animal welfare, how can this information be used. What is the future for welfare in a moral world? Keywords Stress · Welfare · Stress evaluation · Welfare assessment · Ethics · Morality

9.1

Studying Stress and Welfare

In this chapter, information from other chapters in the book is drawn together without duplicating reference to the published sources of the information and ideas. Since the points are often based on the contents of more than one chapter, no specific reference to previous chapters is made. When a medical practitioner, veterinary surgeon, psychiatrist or animal welfare scientist talks about stress, welfare, health, pain, needs and related terms, the words mean the same in every case, whether the subject is human or non-human. There is some variation amongst species in the best measures to use but most measures can be used for a range of species. This is one of the messages of the one health and one welfare campaigns. Other messages are that treating and reducing disease is important for welfare, good welfare results in better immune system function and hence less disease and reducing some non-human diseases is essential for control of some human diseases and vice versa. The ways in which individuals cope with negative aspects of the world in which they live and react to positive aspects are a fundamental aspect of biology. The scientific evaluation of the welfare of humans and other animals is part of basic science and the methods have developed rapidly in recent years. These studies are a development of stress physiology; methods for studying adaptation and motivation; techniques for evaluating emotional, cognitive and behavioural responses, in

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particular the brain mechanisms; and the methods used by immunologists and pathologists for assessing disease and defences against it. One part of the revolution in stress and welfare research is a consequence of the understanding that all anatomical, physiological and behavioural mechanisms are a consequence of genetic information but that none is determined by genetic information as all can be affected by information from the environment of the system. A second part of the revolution in thinking is that all feelings are adaptive mechanisms that we need to understand if we are to fully appreciate how individuals cope with their world. There is now a wider range of methods for assessing pain, fear, pleasure and other feelings as well as the many other parts of coping systems. A third scientific realisation that has been important in animal welfare research is that we can directly investigate the needs of animals and that, once this has been done, it is best to consider these needs rather than the rather vague and misleading concept of freedoms. Whilst the concept of welfare refers to all animals, most people are more concerned about sentient beings, those that have the capacity to have feelings with the requisite cognitive ability and level of awareness, than about other animals. At present, sentient animals exclude those at too early a stage of development or with brain damage and, with these exceptions, include all vertebrates, cephalopod molluscs and decapod crustaceans. If an animal is sentient, it has a pain system so anaesthetics and analgesics should be used where necessary and there should be legal protection. The public attitude, in increasing numbers of countries in the world, is that humans have obligations to all animals with which they interact and greater obligations to sentient animals. The arguments are better phrased in terms of obligations than in terms of rights because rights arguments can be misused.

9.2

Using the Term Stress Scientifically

Stress is an important concept but has been used colloquially and scientifically in imprecise ways. The use of stress by scientists to refer to any disturbance of homeostasis or to any activation of the hypothalamic-pituitary-adrenal cortex (HPA) axis as stress led to the term being considered meaningless. If every disturbance of homeostasis is stress then it is trivial and if every HPA axis activation is stress then it is enormously wide in its biological meaning. The argument presented in this book is that stress is an environmental effect on an individual which overtaxes its control systems and reduces its fitness or appears likely to do so. This means that stress always has negative effects on an individual. This is the way in which most of the general public use the term stress. Welfare is always poorer when an individual is stressed. Since it is impossible to cease usage of the term stress, and it is scarcely useful as a concept unless it can be quantified, we should use the definition and

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measure the immediate and more prolonged consequences of stress as accurately as we can. An ability to monitor stress and welfare provides opportunities, both to avoid some stressful situations and to reduce unavoidable causes of poor welfare. Investigation should involve three aspects: an initial check of whether poor welfare can be prevented, attempts to reduce effects that cannot be avoided and, finally, some monitoring of the negative effects and coping responses induced by any remaining stress and other effects so that a practice that induces unacceptably poor welfare can be terminated. These three types of procedure will be discussed in turn.

9.2.1

Avoidance of Stress

In theory one could compile lists of relevant stresses for every genus of animal under human management. For each species, breed and individual there could be further extensions of those lists. But itemising stresses even for the commonly encountered animals would require a book far longer than the present one, and be quite impracticable. However, for some categories of animals, certain stressors have been identified. This is particularly so with farm livestock and laboratory animals, for which government offices or independent organisations have drawn up lists of requirements in the form of welfare codes. Some of the recommendations for the welfare of farm animals in various developed countries are based on those of the Standing Committee of the Council of Europe Convention on the Welfare of Animals Kept for Farming Purposes. In some guidelines, such as the welfare codes used in some countries, a general approach to specifying how to avoid stress is also used. Much more information about farm animal welfare is now available in the scientific literature and some areas are well summarised in reports of EFSA. People involved with animal management should also keep abreast of technical developments which can circumvent welfare problems. In the past, science and technology have rightly been accused of being part of the cause of welfare problems. However, they can also help to solve them. Welfare problems can disappear as a result of technical innovation. For example, close restraint of sows to control their food intake is not necessary commercially now that feeding can be adequately controlled in large pens by computer systems signalled from electronic collars and by the use of group housing with individual feeding. Computer-linked animal monitoring systems are now allowing much more efficient monitoring of disease and hence improvement in welfare. Modern communication systems permit sales of livestock to be carried out on the farm without the need to put animals in sale yards, thereby avoiding some of the undesirable impositions on farm animals during transport.

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Reduction of Stress and Improvement of Welfare

Some impositions on humans and other animals are unavoidable and some degree of stimulation, perhaps occasionally considerable, is not only normal but beneficial. Whilst it is desirable to avoid stress, environmental stimulation should be in the range that is less than the intensity that results in stress, yet above the critical lower level that constitutes sensory deprivation. Two procedures are involved in adjusting the level of stimulation in this way, in relation to both people managing their own lives and managing the lives of other people or captive animals. Some evaluation must be made of the success an individual is having in adapting to its environment; that is, how much it is having to do to cope, and the extent to which failure to cope is occurring or is likely. Where the species and the situation are well understood, such as with laboratory animals, and in some farm practices and zoo environments, the causative influences and the welfare outcome for the animal can be assessed. A second judgement required is how long a particular level of coping activity can be tolerated and whether it will lead to a reduction in biological fitness. Where a source of poor welfare can be identified, it should be removed if practicable.

9.2.3

Monitoring Welfare

Objective monitoring of individuals to identify stress and assess welfare is valuable whenever those individuals are at risk. For human patients, asking patients about their condition is always subject to the possibility of false answers so should be combined with measures of behaviour and physiology obtained by impartial observers. For animals kept by people, a range of indicators of poor welfare and a rather smaller number of indicators of good welfare are available to be used during monitoring. An aggregate of several measures is preferable to a single measure because of the diversity of coping methods. It may be possible to use an index incorporating several measures. If there is time for only a relatively brief inspection of the animals, welfare outcome indicators should be used. These animal-based measures can be combined with information about the resources available to the animals. Is it necessary to draw up a formal procedure for monitoring standards of animal care? Regrettably it is, because people’s desire to keep animals often outstrips their knowledge of the animal’s biology, and sometimes their appreciation of an animal’s suffering. Guidelines, whether they are laws or codes of practice, establish standards for the requirements for humane animal care. They codify what might otherwise be left to human judgement. In so doing they can draw attention to those instances where zoo operators, farmers, pet owners or other animal owners let standards slip. Humans have difficulties in setting benchmarks for their own animal husbandry. This is sometimes, but by no means always, because of economic pressures. Even

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pet owners may have animals that are neglected and debilitated. The recent efforts to standardise welfare outcome measures, discussed in earlier chapters, should be of value to inspectors, animal owners and, especially, to the animals themselves. A further benefit of formalising standards of welfare is that this gives us the ability to compare norms of management at different venues. Indices of welfare are important when monitoring or trying to improve the welfare of the animals that we keep. If goals have been identified and plans of development agreed, systematic studies of welfare can be carried out and new housing or management methods progressively introduced so that there is a steady improvement in animal welfare. In the establishment of animal welfare codes for various species there are opportunities for valuable cooperation between specialists and those people, such as members of canine associations, sheep farmers and so on, who have special affinities or involvement with a particular type of animal. These groups should seek to establish agreed codes of practice for these animals in order to improve the public image of their profession.

9.3

Welfare in the Moral World

Life on earth includes a wide variety of microorganisms, plants and animals. Each complex organism has within its body many microorganisms, most of which have positive or neutral effects on it. Humans have, inter-mingled among their organs and cells, a similar weight of bacteria to the weight of cells with human DNA. All animals are dependent on plants for their survival because the sources of new energy are the photosynthesising plants in water and on land. Many animals have gene compositions and phenotypic abilities extremely close to those of humans. Some animals have abilities that humans do not have. Humans have hardly any ability that some other animal does not have, at least to some degree. Given such information, the ideas that humans are special, or very different from all other animals, or more important than other animals, are scientifically naive. Humans evaluate what is moral but the moral world is not limited to humans as all social animals have to have moral behaviour if their social group is to remain stable. A moral approach to any issue by humans has to take account of other animals and other life in the world. A key aspect of moral behaviour is to consider the welfare of other individuals. Welfare is a scientific concept so is measurable. We can consider the welfare of any animal but not of non-living objects or of plants and other organisms that do not have a nervous system. The welfare of an individual is its state as regards its attempts to cope with its environment so it includes feelings, health and a range of other coping mechanisms. Welfare depends on biological function but is not limited to what happens in natural conditions. Welfare depends on brain mechanisms and is better when the individual has control over its environment. Hence welfare is better when needs are met. It is more scientific to consider the needs of individuals of a species, where such evidence exists, than to refer to the more vague concept of freedoms.

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9

Stress and Welfare in the World

In the 1970s and 1980s there were many scientific researchers studying health, an important aspect of welfare in humans and non-humans, but far fewer studying welfare. Animal welfare researchers numbered about 30, whereas now there are over 3000. The substantial increase in our knowledge about animal welfare science means that we can say much more about welfare as a result of genetic selection, housing, management, transport, stunning and slaughter. The extent of thinking and publication about the ethics of human interactions with other animals has also developed and has introduced many people to areas of philosophy who might not otherwise have read in such areas. There has been a great increase in legislation and provision of codes of practice about animal welfare and a valuable increase in mechanisms for evaluating human ethics topics that affect human welfare. Animal welfare and human welfare are now included in discussions about whether or not a human activity, such as a chemicals factory or production method for plants or animals, is sustainable. No system can be considered sustainable if its present and predicted future effects are not acceptable to the general public. We might soon consider in more detail whether or not it would be acceptable to, or in the interest of, other sentient animals. Human welfare and animal welfare are important parts of world problems but all possible impacts, positive and negative, associated with an activity should be considered when evaluating sustainability and product quality. No small group of people should be permitted to benefit greatly from an activity if that activity has significant negative consequences for other people, or other animals, or other organisms and environments. Whenever an activity is proposed, its effects on the rest of the world should be taken into account before it is continued. Everyday decisions for all people can take account of what is good or bad for the world so each individual has responsibilities. Individuals generally avoid causing easily identified harms but, because of the great increase in the availability of information each individual also has obligations in relation to world issues. Many people now consider it to be morally wrong to spread disease, promote antimicrobial resistance, cause other poor welfare to people or other animals, waste food, waste energy, pollute waterways, use non-recyclable materials, or use procedures that cause harmful production of greenhouse gases. The selection of food by individual consumers is now altered by knowledge that a general reduction in animal consumption is desirable and that if animals are eaten, it is better to eat animals and animal products where the animals eat food that humans cannot eat. The production of cultured meat, a culture of muscle cells to make products that do not require that animals be killed, is likely to become more important in future. Selection of plant food to minimise harms to animals and the environment is also starting to increase. Whilst some important changes should be brought into laws by governments, the public can bring pressure on governments. Consumers can exert pressure on commercial companies and governments by refusing to buy products if their production is regarded as unacceptable. Company policies are now readily changed by consumer pressure. The long-term effects of all of this should be increasing civilisation with more concern for other people, other animals and the world environment.

Glossary

Abnormal Behaviour, Aberrant Behaviour Behaviour which differs in pattern, frequency or context from that which is shown by most members of the species in conditions which allow a full range of behaviour. ACTH Adrenocorticotrophic hormone. This peptide hormone is released from the adenohypophysis, or anterior pituitary, and travels in the blood to the adrenal gland where it stimulates the outer part of this gland, the adrenal cortex, to produce glucocorticoids such as cortisol or corticosterone. Adaptation At the cell and organ level: (i) the waning of a physiological response to a particular condition, including the decline over time in the rate of firing of a nerve cell. At the individual level: (ii) the use of regulatory systems, with their behavioural and physiological components, in order to allow an individual to cope with its environmental conditions. In evolutionary biology: (iii) as a noun, any structure, physiological process or behavioural feature that makes an organism better able to survive and to reproduce in comparison with other members of the same species. Also: (iv) the evolutionary process that leads to the formation of such a trait. Affect Feelings, emotions and moods. Aggression An act or threat of action, directed by one individual towards another, with the intention of disadvantaging that individual by actually or potentially causing injury, pain or fear. Anomalous Behaviour Behaviour which is somewhat abnormal (see Abnormal behaviour), particularly with respect to deviations from the normal pattern or frequency. It may be a variant of a normal activity, such as chewing or licking. Aversive Causing avoidance or withdrawal. Awareness A state during which concepts of environment, of self and of self in relation to environment result from complex brain analysis of sensory stimuli or constructs based on memory. © Springer Nature Switzerland AG 2019 D. M. Broom, K. G. Johnson, Stress and Animal Welfare, Animal Welfare 19, https://doi.org/10.1007/978-3-030-32153-6

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218

Glossary

Causal Factors The inputs to a decision making centre, following interpretation in the light of experience, of a wide variety of external changes and internal states of the body. Cognition Having a representation in the brain of an object, event or process in relation to others, where the representation can exist whether or not the object, event or process is directly detectable or actually occurring at the time. Cognitive Bias The influence of affect on a range of processes, some of which are cognitive, e.g. judgement. However, the term has also been used for effects on attention, motivation and memory that may not be cognitive. Competition (i) Among individuals, the striving of an animal to obtain for itself a resource which is in limited supply. Success might result from such abilities as speed of action, strength in fighting or ingenuity in searching. (ii) Among genotypes, the ability to carry out any life function in a way which is better than that used by other genotypes so that the fitness (reproductive success) of the genotype is increased. Conscious Individual An individual that has the capability to perceive and respond to sensory stimuli. Cope Have control of mental and bodily stability; this control may be short-lived or prolonged. Prolonged failure to be in control of mental and bodily stability leads to reduced fitness (see Stress). Crowding The situation in which the movements or other activities of individuals in a group are restricted by the physical presence of others. Depression A condition of brain and behaviour associated with unresponsiveness, reduced cognitive function and sometimes with a characteristic, sagging posture. Displacement Activity An activity which is performed in a situation which appears not to be the context in which it would normally occur. Being so dependent for recognition on observer ability to determine relevance to context, the term is of limited use. Domestication The process, occurring over generations, by which a population of animals becomes adapted to man and to the captive environment by some combination of genetic changes and environmentally induced developmental events. Dominance An individual animal is said to be dominant over another when it acts so as to gain priority of access to a resource such as food or a mate. There are various ways to gain priority so a dominant individual need not be superior in fighting ability to a subordinate. Drive A collection of causal factors that promote related behaviours. The term often implies potential progression towards a goal. Although a definition is included here because the term drive is in widespread use, we consider it is easier to understand motivation if reference is normally made to causal factors rather than to drives.

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219

Emotion A physiologically describable component of a feeling characterised by electrical and neurochemical activity in particular regions of the brain, autonomic nervous system activity, hormone release and peripheral consequences including behaviour. Environment The source of external influences, for example on the development of behavioural or other biological traits. External means outside the system or unit under consideration, not necessarily outside the whole organism. Ethics The study of moral issues. Ethogram A detailed description of the behavioural features of a particular species. Ethology The observation and detailed description of behaviour in order to find out how biological mechanisms function. Sometimes such studies are carried out in a natural or semi-natural setting, but the study of animals on farms or in laboratories is also ethology. Experience A change in the brain resulting from information acquired from outside the brain. The information can originate in the environment of the individual or within the body, for example from sensory input, from low oxygen availability or from a new hormone level in the blood. Exploration An activity having the potential to allow an individual to acquire new information about its environment or itself. Fear A feeling that occurs when there is perceived to be actual danger or a high risk of danger. Feedback The effect of a system output, in response to a system input, which modifies that input by reducing it (negative feedback) or enhancing it (positive feedback). Feedforward The effect of a system output which, prior to any input, modifies the state of the system in such a way that the effect of an input is partly or wholly nullified. Feeling A brain construct, involving at least perceptual awareness, which is associated with a life-regulating system, is recognizable by the individual when it recurs and may change behaviour or act as a reinforcer in learning. Fitness Reduction This involves increased mortality, or failure to grow, or failure to reproduce. Flight Distance The space around an animal within which intrusion provokes a flight reaction. Flight Reaction A characteristic escape reaction which is specific to a particular enemy and surroundings, occurring as soon as the intruder approaches within a given distance.

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Glossary

Freedom A possibility for action conferred by one individual or group upon another. Frustration If the levels of most of the causal factors that promote a behaviour are high enough for the occurrence of the behaviour to be very likely, but because of the absence of a key stimulus or the presence of some physical or social barrier the behaviour cannot occur, the animal is said to be frustrated. Functional Systems The different sorts of biological activity in the living animal which together make up the life process, such as temperature regulation, feeding and predator avoidance. These functional systems have behavioural and physiological components. Genotype The genetic constitution of an individual organism designated with reference either to a single trait or to a set of traits (see Phenotype). Grooming The cleaning of the body surface or rearrangement of pelage by licking, nibbling, picking, rubbing, scratching, etc. When action is directed towards the animal’s own body, it is called self-grooming, when directed at another individual, it is referred to as allogrooming. Habituation The waning of an individual’s response, which could still be shown, to a constant or repeated stimulus. The process is distinct from fatigue. Health The state of an individual as regards its attempts to cope with pathology. Hierarchy A sequence of individuals or groups of individuals in a social group based upon some ability or characteristic. The term is most frequently used where the ability assessed is that of winning fights or displacing other individuals. Homeostasis The maintenance of a body variable in a steady state by means of physiological or behavoural regulatory action. Humane Treatment of animals in such a way that their welfare is good to a certain high degree. Humane Killing Use of a killing procedure that does not cause poor welfare and, if there is stunning, a stunning procedure that results in instantaneous insensibility or, if the agent causing insensibility or death is a gas or injectable substance, no poor welfare occurs before insensibility and then death. This may be achieved because the stunning or killing agent is not detectable by the animal. Individual Distance The minimum distance from an animal within which approach, normally by a conspecific, elicits attack or avoidance. Lameness Impaired locomotion or deviation from normal gait. Learning A change in the brain which results in behaviour being modified as a consequence of information acquired from outside the brain. The modification must last for longer than a few seconds otherwise the effect could simply be a reflex.

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221

Mood A brain state that often involves feelings, continues for more than a few minutes and influences decision-making and behaviour. Moral Pertaining to right rather than wrong. Motivation The process within the brain controlling which behaviours and physiological changes occur, and when. Motivational State The level of motivation resulting from the combined levels of all causal factors in the brain. Need A requirement, which is part of the basic biology of an animal, to obtain a particular resource or to respond to a particular environmental or bodily stimulus. To need is to have a deficiency that can be remedied by obtaining a particular resource or responding to a particular environmental or bodily stimulus. Obligation A duty to act, or to refrain from acting, in a way that potentially affects another individual. Overcrowding Crowding such that the fitness of individuals in the group is reduced. Pain An aversive sensation and feeling associated with actual or potential tissue damage. Pathology (i) The detrimental derangement of molecules, cells and functions that occurs in living organisms in response to injurious agents or deprivations; (ii) the study of such conditions. Periodicity The occurrence of a series of events separated by equal periods of time. Phenotype The observable properties of an organism as they have developed under the combined influences of the genetic constitution of the individual and the effects of environmental factors. Pheromone A substance which is produced by an animal and which conveys information to other individuals by olfactory means. Play Carrying out a movement or intellectual process, either in the absence of its usual objective, or by using an inefficient means of achieving a goal solely in order to engage in that movement or process. Preening Grooming activity in birds. Proprioceptor Sensory receptors within the body which transmit information about the relative positions of different parts of the body. Quality of Life Welfare during a period of more than a few days. Reaction Time The time between the occurrence of a stimulus and the beginning of the response of the animal.

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Glossary

Reinforcer An environmental change which increases the likelihood that an animal will make a particular response, i.e. a reward (positive reinforcer) or a cessation of punishment (negative reinforcer). Rhythm A series of events repeated in time at intervals whose distribution is approximately regular. Rights (i) A legal entitlement that can be defended using the laws of the country. In most countries animals do not have rights in this sense; (ii) a privilege justifiable on moral grounds. The moral grounds may be religious. Self-Awareness The cognitive process in an individual when it identifies and has a concept of its body or possessions as being its own so that it can discriminate these from non-self stimuli. Selfish The action of an individual in a way that increases its fitness at the expense of the fitness of one or more other individuals whilst being aware of the likely effects on itself and on the harmed individual or individuals. Sensitisation The increase in response to continuing or repeated stimulation. Sentient Having the awareness and cognitive ability necessary to have feelings. Sentient Being one that, in order to have feelings, has some ability: to evaluate the actions of others in relation to itself and third parties, to remember some of its own actions and their consequences, to assess risks and benefits and to have some degree of awareness. Social Facilitation Behaviour which is initiated or increased in rate or frequency by the presence of another animal carrying out the same behaviour. Starvation The state of an individual with a shortage of nutrients or energy such that it starts to metabolize functional tissues rather than food reserves. Stereotypy A repeated, relatively invariate sequence of movements which has no obvious purpose. Stimulation The effect of one or more stimuli on an individual animal or on part of it. Stimulus An environmental change which excites one or more receptors or other parts of the nervous system of an animal. Strain The short-term consequences of stress. Stress An environmental effect on an individual which overtaxes its control systems and results in adverse consequences and eventually reduced fitness. Fitness reduction involves increased mortality and failure to grow or reproduce. Suffering One or more bad feelings continuing for more than a short period.

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223

Sustainable A system or procedure is sustainable if it is acceptable now and if its expected future effects are acceptable, in particular in relation to resource availability, consequences of functioning and morality of action. Territory An area an animal defends by fighting, by signals or by demarcation that other individuals detect. Welfare The state of an individual as regards its attempts to cope with its environment.

Index

A ACTH, see Adrenocorticotrophic hormone (ACTH) Adaptation, 3, 15–44, 49–68, 72, 88, 92, 141, 211 limits to, 49 rates of, 51 and stress, 15, 72, 92 to zoos, 43, 62–64 Adrenaline, 24, 35, 110–112, 205 Adrenal responses, 73, 76, 110, 112–116, 120 cortex, 24, 25, 35, 59, 72–74, 80, 87, 112–116, 120 medulla, 24, 35, 110, 112, 116, 118, 141 and welfare, 87, 90, 91, 111, 113 Adrenocorticotrophic hormone (ACTH), 25, 111, 112, 116, 117, 133, 141, 144, 145, 149 Aggression, 26, 30, 33, 38, 41, 66, 81, 110, 121, 154, 157 Alarm reactions, 24, 35, 72 Anaesthesia, 105 Analgesia, 63, 64, 105, 106, 113 stress-induced, 63, 64 Animal production and welfare, 82, 198, 207 Animal usage, 7–9 ANP, see Atrial natriuretic peptide (ANP) Antibody indices, 143–145 Anti-microbial resistance, 194, 196–197 Anxiety, 10, 17, 24, 26, 34, 38, 41, 42, 82, 100, 117, 147, 150, 151, 162 Apathy, 64, 160–162, 174 Atrial natriuretic peptide (ANP), 116 Autism, 114, 158

Aversive stimuli, 66, 92 Avoidance as a welfare indicator, 94–95 awareness, 10, 212

B Bacteria withdrawal reponses, 1 Bar biting, 23, 89, 154, 158, 159 Bedarf, 5, 31, 32, 64, 153, 178, 180, 213, 214 Bedurfniss, 59, 214 Behaviour, 2, 16, 57, 81, 100, 132, 174, 195, 215 abnormal, 23, 62, 81, 88, 89, 105, 151, 154–156, 160–163, 174, 180, 186, 202 deprivation, 22, 30 movement problems, 151–152 pain indicators, 103–106 pathology, 10, 88, 90, 151, 156 (see also Abnormal) profile in wild, 44, 175 reproductive, 62 in rich environment, 174–176 suppression, 90 variety of, 83, 88 Bem estar, 82, 94 Bienestar, 82, 94 Bien–être, 82, 94 Blood parameters, 140–141 Bone breakages, 90, 119, 147 Boredom, 41, 162 See also Stereotypies; Stimulation, lack of; Unresponsiveness Bovine somatotrophin (BST), 138 Bradycardia, 106, 107

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226 Brain biochemistry and functioning, 17, 18, 83 BST, see Bovine somatotrophin (BST)

C Cardiovascular parameters, 140–141 Castration and welfare, 105, 113, 149 Catecholamines, 24, 26, 110, 111, 116, 117, 141, 142 See also Adrenaline; Noradrenaline Causal factors, 20–22, 29, 31, 34, 38, 66 Central nervous system (CNS), 2, 27, 55, 63 See also Brain biochemistry and functioning CK, see Creatine kinase (CK) Climate change, 194, 197 CNS, see Central nervous system (CNS) Codes of welfare, 165, 213, 215, 216 Cognitive bias, 116, 133–134, 187 Community standards of welfare, 204 Competitions, 149, 154, 180 Confinement individual, 73, 198 solitary, 89, 158, 162, 175 Control systems, 5, 16–18, 24, 26–35, 51, 63, 76, 80 and time, 27 Cope, coping, 2, 17, 54, 74, 99, 131, 180, 204, 211 active and passive, 103, 107 levels of, 60, 64, 110, 162 Corticosterone, see Glucocorticoids Corticotrophin releasing factor/hormone (CRF/CRH), 24, 25, 73, 105, 111, 141, 174 Cortisol, see Glucocorticoids Creatine kinase (CK), 107, 117, 118 CRF/CRH, see Corticotrophin releasing factor/ hormone (CRF/CRH) Crib biting, 89, 158 Crowding, 146 Cruelty, 2, 5, 59, 83, 100, 195

D Damage to body, see Injury Dark, firm, dry (DFD) meat, 119 Decision making, 20, 23, 31, 163 Defensive reaction, 101, 102 Depression and welfare, 10, 41, 65, 142, 146, 160–161, 174, 180 Development of regulation, 41–44 DFD meat, see Dark, firm, dry (DFD) meat Dilemmas, 33, 34, 203

Index Disease incidence, 148–149 Displacement activity, 31 Distress, 7, 33, 39, 42, 60, 68, 75, 81, 101, 104, 120, 195, 203 Dobrostan, 82, 94 Domesticated animals, 6, 62, 175, 201 Dominance, 59 Dopamine, 116, 160 Drinking, control of, 29 Drive, 30, 103 Duration of problem and welfare, 201–203 Dynorphin, 63, 73, 149, 150 See also Opioids

E Education, 8 EEG, see Electroencephalogram (EEG) EFSA, 59, 138, 154, 165, 196, 202, 203, 213 Electroencephalogram (EEG), 23 ELISA, see Enzyme-linked immunosorbent assay (ELISA) Endorphins, 25, 63, 150 See also Opioids Enkephalins, 25, 40, 63, 73, 149, 150 See also Opioids Environmental enrichment, 156, 160 Environment enrichment, 185–187 Enzyme-linked immunosorbent assay (ELISA), 112, 145 Enzymes as indicators, 117–118 Epigenetics, 9–10 Epinephrine, see Adrenaline Ethics and welfare, 8, 203–206, 208, 216 Ethology, 72, 82 Evolution of adaptability, 16, 44 Experience, 2, 17–20, 25–27, 29, 32, 34, 35, 38, 39, 41–43, 49, 51, 54, 59, 61–64, 66, 89, 90, 101–106, 112, 115, 117, 119, 132, 135, 137, 149, 154, 155, 159, 163, 174, 187, 204, 205 neonatal, 41 of pain, 39, 204 Exploration, 30, 103, 155, 174

F Fear, 10, 17, 18, 26, 33, 39, 41, 58, 74, 83, 84, 103, 107, 121, 147, 150, 151, 174, 186, 203, 204, 212 Feedback, 27, 35, 37, 73, 102 negative, 27, 35–37 positive, 35, 102

Index Feedforward, 35, 37, 54, 66 Feeding control of, 35, 37, 38, 42, 208, 213 development of, 62, 158, 208, 213 Feelings, 2, 8, 18, 39–41, 44, 82, 83, 89, 90, 92, 95, 99, 103, 116, 133, 134, 156, 157, 212, 215 Feral animals, 175, 205 Fighting, see Aggression Fight or flight reaction, 24 Fish, pain in, 106 Fitness, 4, 16, 38, 43, 44, 61, 76, 77, 80, 81, 84, 90–92, 121, 131, 132, 137, 138, 187, 212, 214 Flight reaction, 101, 102 Follicle stimulating hormone (FSH), 116 Food animals, 6 Forewarning, 54 Freedoms, 32, 33 the five, 32, 33 Freezing response, 107, 163 Frustration consequences of, 152, 157–161 FSH, see Follicle stimulating hormone (FSH) Functional system, 31, 155, 158

G Gain in control systems, 16, 27–29 Genetics, 6, 9–10, 30, 43, 44, 66–68, 88, 113, 119, 137, 162, 195, 199, 202, 212, 216 Genotype, 5, 67, 84, 89 Glucocorticoids in absence of stress, 73 during stress, 72 half-life in blood, 110 non-production during stress, 72 Glucose in plasma, 116, 118 Glycogen metabolism, 119 Grooming, 22, 31, 91, 101, 106, 151, 152, 155 Growth as welfare index, 89

H Habituation, 19, 20, 49–51 as a complex process, 19, 51 Handling, 42, 59, 100, 103, 105, 107, 109–114, 119, 139, 163 Hazard avoidance, 55, 57 Health and welfare, 1–11, 83, 84, 103, 198, 211, 215, 216 Heart rate, 19, 35, 100, 106–109, 120, 121, 140, 141, 151, 205

227 Hierarchy, 59 Homeostasis, 16, 17, 24, 26, 33, 54, 60, 74, 75, 212 Hormonal outputs, 24–26 Housing and welfare, 133, 159, 163, 164, 185, 198, 215, 216 Human stress, 5 See also Stress Hypersensitivity, 63, 64, 104, 146 Hyposensitivity, 63, 64 Hypothalamic-pituitary-adrenal cortex (HPA) axis, 24, 212 See also Adrenocorticotrophic hormone; Corticotrophin releasing factor; Glucocorticoids

I Immobility, see Freezing response Immune function, 58, 72, 73, 87, 142–146, 211 as index of welfare, 143, 211 Indicators of welfare, 83, 89–91, 93, 99–101, 103, 107, 109, 116–121 integration of, 120, 185 interrelations between, 90 Individual differences in responses, 103 Individual distance, 175, 181 Injury, 17, 33, 39, 40, 63, 64, 80, 81, 86–88, 90, 91, 94, 104, 110, 117, 118, 147–148, 150, 163, 164 Inputs to control systems, 18, 56 Isolation effects, 4, 33, 53, 108, 116, 148, 150, 154

L Lack of stimulation, 64, 150, 162–164 Lactate dehydrogenase (LDH), 118 LDH, see Lactate dehydrogenase (LDH) Learned helplessness, 38, 67, 174 Learning, 19, 20, 25, 31, 38, 40, 42, 43, 74, 105, 195 by neonates, 41 Legislation for needs, 32 Lethal hazard, 55, 57 LH, see Luteinizing hormone (LH) Life expectancy, 84, 86, 88, 121, 137–138 Light levels, 16 Luteinizing hormone (LH), 116, 149 Lymphocyte function measures, 143–146 numbers, 143

228 M Measurement problems, 99, 107, 132 Memory, 23, 25–27, 29, 42, 43, 133 Mitogens, 145 Moral decisions, 84 Moral obligations, 7, 194 Motivation, 23, 30, 31, 34, 149, 178, 180, 211 causal factors, 21, 22, 29, 31 dilemmas, 33, 34 and hormones, 149 and neuromuscular outputs, 23 Motivational state, 20–23, 29–32, 132 Movement problems, 151–152 Mulesing, 105, 113, 149 Muscle and carcass indicators of welfare, 118–119

N Naloxone, 63 Naturalness, 92 Needs, 2, 4, 5, 8–10, 15, 19, 23, 27–34, 36, 39, 57–59, 62, 67, 73, 76, 81, 82, 84, 87, 88, 90, 92, 93, 100, 112, 113, 121, 122, 132, 134, 140, 147, 148, 152, 155, 156, 158, 173–176, 178, 180, 186, 187, 195, 198, 199, 202, 206, 208, 211–213, 215 Neonatal behaviour, 41, 109 Nerve activity, 27 Neuromuscular outputs and motivation, 23 Nociceptive system, 104 Noradrenaline, 24, 25, 35, 110–112 Norepinephrine, see Noradrenaline Novelty, 54, 58, 59, 66, 114, 162, 185

O Obligations, moral, 7, 194 Operant techniques, 178–185 Operations, 16, 27, 30, 33, 34, 36, 63, 100, 104, 105, 113, 146, 148, 149 Opioids, 40, 63, 89, 106, 117, 149, 150, 161 receptors for, 73, 150 Orientation reaction, 19, 56, 101 Overstimulation, 84, 162–164 Oxytocin, 91, 116, 133, 142

P Pain, 8, 16, 54, 81, 100, 147, 202, 211 behavioural indicators of, 39, 40, 93, 103–105 toleration of, 84, 105 value of, 54 and welfare, 39, 55, 84, 147

Index Pale soft exudative (PSE) meat, 118, 119 Parasites, response to, 55, 121 Pathological effects of conditions, 76, 156, 202 Pets, socialization in, 41 Phenotype, 9, 10 Philosophies of welfare, 7, 8, 195, 216 Pituitary hormones, 24, 111, 142 Pleasure, 34, 41, 42, 82, 83, 88, 91, 101, 116, 122, 133, 212 Poisons, 57 Practical problems of welfare, 9, 24, 42, 44, 64, 68, 100, 104, 121–122, 132, 141, 149–151, 154, 156, 157, 186, 199, 201–203, 213 Predictability of stimuli, 37, 38 Preening, 102, 155 Preferences assessing the importance of, 176–185 causing harm, 187 operant techniques, 178–185 and welfare, 173–188 Pre-pathological state, 90 Prolactin, 35, 107, 116, 149 Proportional controllers, 27, 28 Proprioceptor, 17 Protozoa, sensory capabilities, 16, 17 PSE meat, see Pale soft exudative (PSE) meat

Q Qualitative behavioural assessment, 134–136

R Radioimmunoassay (RIA), 112, 116 Reaction time, 51 Reflexes, 22–24, 27, 35, 56 Reinforcement, 65, 178–180 Religious view, 8, 195, 204 Renin, 30, 117 Reproduction and welfare, 25, 86 Respiratory rate, 7, 26, 33, 158 Restraint, 43, 51, 107, 116, 117, 150, 213 Rewards for performance, 178 Rhythm, 29, 62, 63 RIA, see Radioimmunoassay (RIA) Rights, animal, 82 Route tracing, 89, 157–159

S Saliva hormone concentrations, 22, 26, 112, 141, 143 Selye’s concept of stress, 72, 73 Sensitive period, 41

Index Sensitivity hypersensitivity, 63, 104, 146 hyposensitivity, 63, 64 Sensitization, 19, 20, 49, 50, 53, 144, 146 Sensory inputs, 20, 31, 36, 101, 133, 159, 162 Sentience, 8, 15–44, 94–95 Separation anxiety, 109, 134, 146, 151 Set point in control systems, 27–30, 63 Sham chewing, 89, 158, 159 Silvopastoral, 208 Slaughter, 100, 114, 117–119, 195, 204, 216 Sleep, 34, 90, 106 Social disturbance, 62, 102 See also Aggression Social facilitation, 102 Socialization, 10, 41 Social preferences, 176 Startle responses, 19, 35, 51, 101–102, 121, 163 Stereotypies, 154, 156–164, 186 and opioids, 150 and welfare, 154, 159, 160 Stimulation, stimulus, 4, 16, 49, 74, 102, 146, 214 additivity, 59 hyper and hypo, 162–164 integration, 58, 59 intensity, 58, 59 lack of, 64, 150, 162 local, 55, 60, 102, 164 overload, 16, 51, 65 timing of, 34, 49–54 unavoidability, 64, 213, 214 unpredictable, 38, 65, 66 Strain, 68, 71, 72, 74, 80, 108, 111, 120, 175, 196, 197, 204–206 Stress, 2, 23, 57, 71, 103, 131, 193, 211 avoidance, 213 cannot be good, 213 definition, 5, 72, 74, 76, 80, 81, 212 definitions by others, 71–81 practical assessment, 10 reduction, 84, 116, 131, 214 relation to welfare, 91 use of terms, 72 Suffering, 5, 7, 17, 40, 41, 44, 54, 81, 82, 84, 89, 90, 141, 160, 203, 206, 214 and welfare, 81–84, 86, 87, 90, 91, 93, 148 Sustainable, 207, 208, 216 Sustainability, 194, 197, 198, 207, 216

T Tachycardia, 106–109 Tail wagging, 91

229 Temperature ambient, 179 body, 31, 36, 37, 58, 106, 109–110, 141, 156, 185 Territory, 64 Testosterone, 116 Thyroid hormones, 24, 27, 35, 116 Tolerance, 34, 54, 57, 58, 60, 61, 105, 205 Tongue rolling, 89, 154, 163 Trade-off concept, 33, 34 Training, 1, 4, 100, 133, 135, 151, 162 Transmitters, see Neurotransmitters Transport, 5, 25, 62, 68, 100, 106–109, 114, 117–120, 122, 146, 149, 164, 200, 203, 213, 216 Trapping, 100

U Ulceration, 162 Unpredictability, 38, 66, 84, 157 Unresponsiveness, 65, 89, 160, 161, 174 Usage of animals, 7–9, 29

V Value systems, 193–195 Vasopressin, 24, 30, 35, 107, 142

W Weight (body) changes, 139–140 Welfaerd, 94 Welfare and adrenal activity, 76, 85, 118, 142, 164 behavioural measures of, 91, 101–106, 150 as a characteristic, 1, 82, 84, 95 codes, 213, 215, 216 and coping, 3, 84, 92 definition, 3, 82–84, 87, 92 evaluation of measures of, 131, 133, 211 and fear, 150, 151 and freedom, 32, 33 and frustration, 37, 84, 150, 154 and health, 1–11 how poor and for how long?, 34, 120, 145, 214 interrelations of measures, 164–165 and lack of control, 38, 64, 101, 150, 157–161, 163 levels of, 90, 144 measuring long-term responses, 131–165 measuring short-term responses, 99–122, 156

230 Welfare (cont.) monitoring, 214–215 in other languages, 94 and pain, 39 physiological measures of, 23, 91, 104–120 and preferences, 173–188 public interest in, 5 and reproduction, 86, 89, 136, 137 standards and limits, 204–206, 215 and stress, 1–11, 15, 57, 71–95 and suffering, 81–84, 86, 87, 90, 91, 93, 148

Index Well being, 3, 74, 93 Welzijn, 82, 94 White blood cell indices, 118 Wohlbefinden, 94 World problems, 193–194, 216 World resources, 193, 194, 206, 207

Z Zoos, adaption to, 7, 43, 62–64