Olfaction in Animal Behaviour and Welfare Olfaction in Animal Behaviour and Welfare Edited by Birte Lindstrøm Nielsen INRA, France CABI is a trading name of CAB International CABI CABI Nosworthy Way 745 Atlantic Avenue Wallingford 8th Floor Oxfordshire OX10 8DE Boston, MA 02111 UK USA Tel: +44 (0)1491 832111 Tel: +1 (617) 682 9015 Fax: +44 (0)1491 833508 E-mail: [email protected] E-mail: [email protected] Website: www.cabi.org © CAB International 2017. All rights reserved. No part of this publication may be reproduced in any form or by any means, electronically, mechanically, by photocopying, recording or otherwise, without the prior permission of the copyright owners. A catalogue record for this book is available from the British Library, London, UK. Library of Congress Cataloging-in-Publication Data Names: Nielsen, Birte Lindstrøm, editor. Title: Olfaction in animal behaviour and welfare / edited by Birte Lindstrøm Nielsen, INRA, France. Description: Boston, MA : CABI, 2017. | Includes bibliographical references and index. Identifiers: LCCN 2017002054 (print) | LCCN 2017026487 (ebook) | ISBN 9781786391605 (epdf) | ISBN 9781786391612 (epub) | ISBN 9781786391599 (pbk. : alk. paper) Subjects: LCSH: Smell. | Animal behavior. Classification: LCC QP458 (ebook) | LCC QP458 .O4316 2017 (print) | DDC 591.5--dc23 LC record available at https://lccn.loc.gov/2017002054 ISBN-13: 978 1 78639 159 9 Commissioning editor: Caroline Makepeace Associate editor: Alexandra Lainsbury Production editor: Tim Kapp Typeset by SPi, Pondicherry, India Printed and bound in the UK by CPI Group (UK) Ltd, Croydon, CR0 4YY Contents List of Contributors vii Prologue ix Preface xi SECTION 1 – SETTING THE SCENE 1 The Nuts and Bolts of Olfaction 1 Nicolas Meunier and Olivier Rampin 2 Innateness and Learning in Olfactory Behaviour and Odour Perception 16 Birte L. Nielsen 3 Semiochemicals: Pheromones, Signature Mixtures and Behaviour 26 Tristram D. Wyatt 4 Behavioural Tests of Olfaction 39 Markus Fendt, Raimund Apfelbach and Burton Slotnick 5 Is There Such a Thing as a Bad Smell? 61 Roland Salesse and Laurent Dormont SECTION 2 – THE ROLE OF OLFACTION 6 The Role of Olfaction in Feeding and Foraging 73 Marije Oostindjer 7 The Role of Olfaction in Mate Selection and Reproductive Behaviour 85 Luisa Amo 8 The Role of Olfaction in Maternal Care and Offspring Survival 102 Frédéric Lévy and Raymond Nowak 9 The Role of Olfaction in Disease Detection and Prevention 123 Tadeusz Jezierski 10 The Role of Olfaction in Relation to Stress and Fear 136 Vincent Bombail 11 The Role of Olfaction in Animal Housing and as Enrichment 151 Deborah L. Wells and Peter G. Hepper SECTION 3 – OLFACTORY BEHAVIOUR 12 Olfactory Behaviour in Farm Animals 161 Caroline Clouard and J. Elizabeth Bolhuis v 13 Olfactory Behaviour in Zoo Animals 176 Róisín Campbell-Palmer and Frank Rosell 14 Olfactory Behaviour in Laboratory Animals 189 Olivia Le Moëne and Anders Ågmo 15 Olfactory Behaviour in Companion Animals 201 Peter G. Hepper and Deborah L. Wells Index 215 vi Contents List of Contributors Anders Ågmo, Institute of Psychology, University of Tromsø, N-9037 Tromsø, Norway. Luisa Amo, Department of Evolutionary Ecology, Museo Nacional de Ciencias Naturales (MNCN-CSIC), C/ José Gutiérrez Abascal, 2, E-28006 Madrid, Spain. Raimund Apfelbach, Neurobiology/Animal Physiology, University of Tübingen, Auf der Morgenstelle 28, D-72076 Tübingen, Germany. J. Elizabeth (Liesbeth) Bolhuis, Adaptation Physiology Group, Department of Animal Sciences, Wageningen University and Research, De Elst 1, NL-6708 WD Wageningen, The Netherlands. Vincent Bombail, NeuroBiologie de l’Olfaction, INRA, Université Paris-Saclay, Domaine de Vilvert, F-78350 Jouy en Josas, France. Roisin Campbell-Palmer, Faculty of Technology, Natural Sciences and Maritime Sciences, Department of Natural Sciences and Environmental Health, University College of Southeast Norway, N-3800 Bø i Telemark, Norway. Caroline Clouard, Adaptation Physiology Group, Department of Animal Sciences, Wageningen University and Research, De Elst 1, NL-6708 WD Wageningen, The Netherlands. Laurent Dormont, CNRS Centre d’Ecologie Fonctionnelle et Evolutive, UMR 5175, 1919 Route de Mende, F-34293 Montpellier Cedex 5, France. Markus Fendt, Medical Faculty, Institute for Pharmacology and Toxicology, Otto-von-Guericke-Universität Magdeburg, Leipziger Strasse 44, D-39120 Magdeburg, Germany. Peter G. Hepper, Animal Behaviour Centre, School of Psychology, Queen’s University Belfast, Belfast BT7 1NN, Northern Ireland, UK. Tadeusz Jezierski, Institute of Genetics and Animal Breeding, Polish Academy of Sciences, Department of Animal Behaviour, Jastrzebiec, Poland. Olivia Le Moëne, Institute of Psychology, University of Tromsø, 9037 Tromsø, Norway. Frédéric Lévy, Physiologie de la Reproduction et des Comportements, INRA UMR 85, CNRS UMR 7247, Université F. Rabelais, IFCE, F-37380 Nouzilly, France. Nicolas Meunier, NeuroBiologie de l’Olfaction, INRA, Université Paris-Saclay, Domaine de Vilvert, F-78350 Jouy en Josas, France. Birte L. Nielsen, NeuroBiologie de l’Olfaction, INRA, Université Paris-Saclay, Domaine de Vilvert, F-78350 Jouy en Josas, France. Raymond Nowak, Physiologie de la Reproduction et des Comportements, INRA UMR 85, CNRS UMR 7247, Université F. Rabelais, IFCE, F-37380 Nouzilly, France. Marije Oostindjer, Norwegian University of Life Sciences (NMBU), PO Box 5003, N-1432 Ås, Norway. Olivier Rampin, NeuroBiologie de l’Olfaction, INRA, Université Paris-Saclay, Domaine de Vilvert, F-78350 Jouy en Josas, France. Frank Rosell, Faculty of Technology, Natural Sciences and Maritime Sciences, Department of Natural Sciences and Environmental Health, University College of Southeast Norway, N-3800 Bø i Telemark, Norway. Roland Salesse, NeuroBiologie de l’Olfaction, INRA, Université Paris-Saclay, Domaine de Vilvert, F-78350 Jouy en Josas, France. Burton Slotnick, Department of Psychology, American University, 4400 Massachusetts Ave NW, Washington, DC 20016, USA. Deborah L. Wells, Animal Behaviour Centre, School of Psychology, Queen’s University Belfast, Belfast BT7 1NN, Northern Ireland, UK. Tristram D. Wyatt, Department of Zoology, University of Oxford, South Parks Rd, Oxford OX1 3PS, UK. vii Prologue As part of his famous collection of case histories The Man Who Mistook His Wife For A Hat, Dr Oliver Sacks wrote an article titled, ‘The Dog Beneath the Skin’ about a patient who had experimented with drugs. They ended up greatly enhancing his sense of smell. He described smelling in detail he had never experienced before. In a perfume store, he could distinguish all the different scents. Each slight difference in odour was now attached to an emotion. Each person he met now had a unique ‘smell-face’ and he could smell their emotional state. He described entering a whole new perceptual world. There are a few other humans that can distinguish a myriad of smells: the best wine stewards can identify hundreds of wines by smell alone, for example. This story fascinated me because I am a visualizer: my thoughts are in pictures instead of words. I had to learn that most people think in words. The first step to understanding is realizing that other people may perceive and think differently. This same principle needs to be applied to our understanding of animals. A dog’s social life revolves around smell. Time and time again I have seen dogs being walked and being jerked away from the things they are smelling. When a person walking a dog impatiently pulls his dog away from the bush where other dogs have left their mark, he is not allowing the dog to go into its smell universe. Dogs seem to like my luggage because it has been to many different smell places such as farms. At the airport, the security dog was in love with my well-worn handmade leather briefcase. These dogs are trained to sit when they smell contraband, but since it was obvious that there was nothing bad in my bag, the officer yanked his dog away. As I wrote this Prologue, pictures associated with smells came into my head. Since I am a visualizer, I see the pictures first, and then smell the odour associated with them. I see a cookie store that I went to when I was a graduate student. To entice customers, they had a fan that blew cookie smells into the street. Installation of the fan was a great business move. It increased sales. In my work with handling cattle, I have emphasized their reactions to what they see. Small distractions such as a reflection on a wet floor may make the animals balk and refuse to move through a race. Cattle will also react to smells. Handling in brand new facilities is often difficult due to the smell of fresh paint. The animals often refuse to enter the freshly painted area until I have dirtied it up. There is a smell of fear, and I have seen the reaction of cattle to it. At one place, a steer flipped over onto his back in a single file race. It took about 10 min to get the animal back on his feet. When he was stuck, he had slobbered on the floor. The next animal in line refused to walk over his ‘fear spit’. One animal balked and backed up several times before walking over the floor where the downed animal had slobbered. To get the other cattle to move easily, the race had to be washed down. It appears that for such fear odours to be secreted, the animal has to have a period of 5–20 min of severe stress. The presence of a fear pheromone has been documented by scientific studies discussed in this book. Since during my career I have worked on improving slaughter plants, I am often asked, ‘Are animals afraid of slaughter?’ In answer I would say that I have witnessed hundreds of cattle calmly walking into facilities that had blood on them – the most important factor seems to be that there has been no prolonged obvious aversive events with a duration of over 5–10 min. Cattle behaviour and cortisol levels are similar during movement through races both on the farm and at the abattoir. To end this Prologue, I will leave you with something to ponder. I once saw a group of intently curious heifers forming a circle around a groundhog that was on their pasture. Their behaviour was definitely moti- vated by curiosity, because the young heifers had never seen a groundhog before. On another occasion I witnessed a group of beef cows on a pasture congregated at a place where a herd-mate had died. The grass looked normal, but they all put their noses to this patch of ground and sniffed. They did not bellow or become ix