D.G.M. Wood-Gush Memorial lecture: Why has there not been more progress in animal welfare research?

APPLIED ANIMAL BEHAVIOUR SCIENCE

ELSEVIER

Applied Animal Behaviour

Science 53 (1997) 59-73

D.G.M. Wood-Gush Memorial lecture: Why has there not been more progress in animal welfare research? M.S. Dawkins Department Of.&dog)', University

qf Oxford,

South Parks Road, Oxford 0x1

3pS, IJK

Abstract Four possible answers to the question of why there has not been more progress in animal welfare research are discussed: (1) that the subject matter might be beyond the scope of scientific enquiry; (2) that the commonly employed approaches and methodologies might be faulty; (3) that the approaches are sound but that more time is needed to obtain valid results; (4) that valid results have been obtained but not disseminated to the public or politicians. Of these, (3) has the most credibility. Applied ethologists should not be ‘bullied’ into giving oversimplified answers to difficult questions. Some recent studies on social recognition in hens are described to illustrate the importance of a broad-based ethological approach. 0 1997 Elsevier Science B.V. Kewords:

Animal welfare; Consciousness;

Social recognition

1. Introduction Thank-you very much for inviting me to give the second Wood-Gush Memorial lecture. It is a great honour and I was very pleased and touched to be asked. I knew David Wood-Gush as a friend and I am also a great admirer of his work. Along with other people who knew him, I had hoped, and indeed assumed, that he would be around for a long time. He was part of the scene, part of the reason for wanting to go to conferences, one of the people one would want to meet and chew over ideas with. In fact, as he got older, he became more innovative, more adventurous in what he would take on. He was prepared to tackle questions about consciousness in animals, for example, long before it became fashionable. He was a pioneer in research in animal welfare and how to measure welfare long before these were considered respectable or even possible areas for a scientist to be to be working on. 016%1591/97/$17.00 0 1997 Elsevier Science B.V. All rights reserved. PII SOl68-1591~96~01151-3

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One of my most vivid personal memories of him was the occasion when we were both editing the proceedings of a workshop on self- awareness in domestic animals which was going to be published by UFAW. We had tape-recorded the entire proceedings, including all the informal discussions and had then looked for a secretary to transcribe the tapes. Unfortunately, the person we found was very willing but she was completely new to biology and so didn’t know any of the technical terms. She did her best to type what she heard but the result was some pretty spectacular errors, some of which were extremely funny. So David and I were confronted with a very rough-andready manuscript which was full of the most hysterical bloomers and which somehow had to be turned into a readable book. As David had come down from Edinburgh specially to do this, we spent the whole day on it and kept going without a break. By about five o’clock, we were both reduced to a giggly state in which the least little thing set us both off into helpless laughter. People passing outside my room kept putting their heads round the door and saying “What on earth are you two doing in there?” And we would reply, wiping the tears of laughter from our eyes: “Editing a book!“, as though that was the funniest thing anyone could be doing, which I suppose for that day, and in that context, it probably was. My other very vivid memory of David is of meeting him at conferences and having very detailed conversations with him about the design of experiments. He was always trying to think up ways of testing the apparently untestable such as whether pigs were aware of what they were doing or had a degree of self-awareness. But he never let theory run away with him. He was always trying to turn ideas into testable predictions, and his ideal bit of apparatus was one in which, if a pig had a concept of self, it would turn left and if it did not, it would turn right. (I exaggerate but only a little!). I think that was what made him so rewarding and so infuriating to talk to. He managed to combine being innovative and forward-thinking with keeping his feet firmly on the ground. If an idea were worth anything, it should be experimentally testable. He would try to push back the barriers of what was testable but he wouldn’t compromise on the ultimate test being a well-designed experiment. I should perhaps begin by explaining why I have chosen to give a lecture dedicated to the memory of David Wood-Gush with the title ‘Why hasn’t there been more progress in animal welfare research?’ The reason I felt stimulated to talk on this subject was that a few months ago I was lying in bed half asleep one morning listening to the farming programme when I heard some man-1 think he was a politician, but its probably just as well I didn’t catch his name-say that it was quite impossible to answer questions about animal welfare scientifically. He then went on to say that we could never know what an animal of another species was experiencing and there was no point even trying to find out. I sat up in bed and thought: How on earth can he get away with saying that? What does he think applied ethologists have been doing for the past 10, 15 and even 20 years? Is he not aware of how much scientific effort has gone into animal welfare research? I was even more disturbed when I picked up John Webster’s recent book Animal Welfare: A Cool Eye Towards Eden (Webster, 1995) and read: “The farm animal welfare movement has generated a great deal of anguish among a great number of consumers (and farmers!) but it has not, as yet, had any significant influence on he quality of life for the vast majority of animals reared for food” (p. 130). And on p. 240

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of the same book we find: “It is difficult...to escape the conclusion that a lot of very well-intentioned welfare research is neither very good science nor very helpful to the animals.” Whereas it would have been possible to say that a politician was simply ignorant of what scientific research has been done, it is not possible to use this excuse in the face of criticisms from someone of John Webster’s standing and knowledge of what is going on. We have to face up to the unpleasant possibility that maybe we haven’t made as much progress as we should have done or indeed as much as we would like to think we have done. In other words, I feel it is an appropriate moment to examine the current state of animal welfare research and ask the question: Why aren’t we further ahead than we are? and possibly the subsidiary question: Why aren’t we seen to be more ahead than we are? I must stress that I am not saying that we have made no progress, nor am I necessarily agreeing with John Webster. As I shall argue, I believe that applied ethology is in many ways in a much healthier state than ‘pure’ ethology. Enormous progress has been made and is being made. What I want to ask is how can it be that despite this progress, we can still have politicians implying that the problems are as insoluble as ever, we can still have John Webster saying that we have achieved so little and we can still have people concerned with practical legislation saying that you lot are simply not telling us what we want to know? We are quite prepared to give you money for your research, we are prepared to change the laws to improve the lot of animals but you are simply not telling us what we need to know. However, because this is the David Wood-Gush Memorial Lecture and because David was, above everything, a pragmatist-someone who believed that if you didn’t know whether something was the case you should do an experiment to find out-1 am not going to spend my entire time talking in vague and general terms about where we are and are not going. In fact, if I thought David were in the audience, I would be extremely embarrassed if that was all I was going to deliver. So, I shall provide four different possible answers to the main question, some of which I should say, are more palatable to us than others, but I will then talk about some current research and describe some straightforward and down-to-earth experiments to illustrate some of the points I shall be making. To begin with, then, why hasn’t there been more progress in animal welfare research? And/or, why hasn’t more progress been seen to be done by the outside world? 1.1. Is it because the subject matter is beyond the scope of scientific enquiry? The first reason I want to consider is that what we are trying to do is something which is actually impossible. The subject matter of animal welfare research includes consciousness, self-awareness, well-being, welfare and so on. We’re concerned with the health of animals (which is fair enough) but also with their subjective experiences such as those of suffering and pain. We are able to identify the symptoms of health and disease in animals just as we able to identify the symptoms of health and disease in plants. Now, of course health and the absence of disease and suffering in animals are a major part of animal welfare, but the reason why we talk about animal welfare and we don’t talk about plant welfare is that most of us want at least to leave open the possibility that physical symptoms in animals can be accompanied by conscious states

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such as suffering or pain. Now, these conscious states are subjective. They are, strictly speaking, private, known only to the organism experiencing them. We cannot even know for certain that another human being has conscious experiences like ours. Our assumption that they do is just that-an assumption, not something that can be scientifically verified. How much more difficult-and even more unscientific-to try to study conscious experiences in other species. SO we have to face the possibility that at least part of what we are trying to do in animal welfare research is actually impossible. If we are trying to gain access to the private and subjective experiences of other species, maybe that early morning politician is right and we are on a fool’s errand. Perhaps the reason there has not been more progress in animal welfare research is the same reason that there has not been more progress in research into perpetual motion machines or squaring the circle: the end-point is impossible. There have been some very major changes in scientific attitudes to the study of conscious experiences in both humans and non-humans over, say, the last 20 yearscertainly over the time in which the Society for Veterinary Ethology and then the International Society for Applied Ethology have been in existence. In 1976 when Donald Griffin published his book The Question of Animal Awareness (Griffin, 1976), he definitely went out on a limb and risked his scientific reputation by saying that scientists should start trying to study the issue of animal consciousness. Even the study of human

consciousness was avoided by psychologists as something not quite scientific. Now, there is approximately a book published each week about consciousness. It has in fact become an extremely trendy subject. New techniques such as brain imaging have opened up the study of consciousness and made it accessible to scientific investigation in ways no-one had dreamt of before. What this means is that many of the issues with which we have been grappling-such as what goes on in the minds of other organisms -while still considered to be very difficult to study, are now seen to be clearly within the realms of scientific enquiry. Consciousness is still one of the greatest mysteries in biology but it is yielding to scientific methods of study. In other words, I do not accept that we have not progressed all that far in animal welfare research because we have taken on a task that is impossible, but I do think that we may not have fully grasped how extraordinarily difficult that task is. The result is that we do not have a coherent theory of conscious experiences of animals-that is, of why the animals with which we are concerned have subjective feelings at all. I would like to suggest that there are three reasons why we have not made more progress in the study of animal consciousness, the understanding of which is such an important part of our assessment of its capacity to suffer. Firstly, we have confused the terms ‘cognitive’ and ‘conscious’. These are not the same. ‘Cognitive’ refers to the processes by which information is perceived, stored and processed. It is used when there is evidence of an internal representation of something in the outside world, which can be used flexibly. ‘Conscious’ refers to a wide range of states in which there is an immediate awareness of thought, image, memory or sensation. An organism, or a machine, can have a representation without necessarily being conscious. There are many complex tasks that we perform without necessarily being conscious. For example, driving a car demands a complex internal representation of the world but for much of

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the time, experienced drivers are not conscious of every single move that they make. My fingers automatically find the letters on a keyboard but I could not consciously say where each letter was positioned. Secondly, we have not adequately addressed some of the issues raised by other people working on consciousness. By this I mean that we may not always be sufficiently aware of the debates going on in other fields such as philosophy and psychology about the kinds of theories that now exist about what consciousness is. As these different theories have very different implications for animal welfare, we should at least be aware of what they are. There are for example, a number of people such as David Rosenthal (19931, who believe that consciousness is intimately associated with language, not so much with speech as with the complex and flexible ‘if-then’ pianning that language makes possible. Obviously such a view affects which animals are believed to be conscious because, taken to its logical conclusion, the linking of language with consciousness would imply that only humans and possibly some other apes are consciousness. Then there are those who believe that consciousness is associated with the capacity for self-awareness (for a discussions of this issue see Parker et al., 1994). This, too, leads to the view that only a very limited number of animal species are conscious-humans and chimpanzees certainly and some other species such as dolphins and goriilas possibly. By contrast, consciousness is a much wider range of species is implied by the view of animal consciousness put forward by Donald Griffin (1992). Griffin argues that the complexity of behaviour shown by many animals implies that they are consciously aware of what they are doing. While Griffin’s views have been very influential, they hdve also aroused a lot of criticism and we should be aware that many critics feel he has done nothing more than ‘tell stories’ and has wrongly assumed that complexity of behaviour implies consciousness. The third and most important reason why we may not have made as much progress as we could have done in the study of anitnal consciousness is that we have not adequately addressed the issue of animal emotions-or more specifically, of which emotional states are accompanied by the conscious states we call suffering. I feel this is a very major gap in our understanding of animals and of the brain. What most people do when they want to study animal consciousness or animal awareness is to try to find out how clever animals are. The implicit assumption is that the cleverer an animal is the rnore likely it is to suffer. But you don’t have to be very clever to feel pain. Nor do you have LObe a great intellectual to feel hunger or even fear. I think it is entirely possible that there are different kinds of consciousness and the kind that we associate wi;h beiq very clever-solving puzzles or performing ‘cognitive’ tasks-may in fact be a late deveiopment in evolution. On the other hand, the kind of conscious awareness associated with what we call suffering may not necessarily be confined to clever animals. It nldy be much older in evolution and consequently much more widespread in the animal kingdom. We should remember Jeremy Bentham’s (Bentham, 17S9) often quoted but very important point that “The question is not, Can they reason? uor, Can they talk? but, Can they suffer?” It is suffering that we need to concentrate on ill atknal welfare research and yet this aspect of conscious awareness has been relatively neglected.

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Although I would clearly not conclude that progress in animal welfare research has been limited because we are trying to do something that is impossible, I do think that we may not have faced up to the extreme difficulties of what we are doing or gone about it in quite the right way. In attempting to understand what other animals experience, we are tackling one of the greatest of all mysteries and trying to solve problems that have baffled philosophers for thousands of years. We should not underestimate the difficulties, we should make ourselves aware of developments in the study of consciousness in other fields and, in particular,we should address the question that nobody has yet tackled satisfactorily-the relationship between emotions and consciousness. So, the first reason why we might not have made as much progress in animal welfare research as we could have done is that the subject matter is extraordinarily difficult. That is not our fault. Everybody finds it difficult. But it is not an impossible subject to study and, what is more, it is within the realms of science. 1.2. Is there something wrong with our approaches

or methods?

This is the most uncomfortable possibility and definitely what John Webster was getting at. How valid is the claim that a lot of animal welfare research isn’t very good? Are we to blame because we’ve been working in the wrong ways? Could more progress have been made if different projects had been undertaken or if better science had been done? I am going to stick my neck out and say that in general, I think we are on the right track. Where we have perhaps achieved less than we might have done is where we have either (a) departed from the broad-based approach that characterised early ethology and tried to carry out our research in isolation or (b) become too obsessed with the search for a single unified measure of ‘stress’. Last year, Ian Duncan in the first Wood-Gush Memorial Lecture stressed the importance of asking a broad range of questions-the so-called ‘four questions of ethology’-about mechanism, function, phylogeny and development. When Niko Tinbergen wrote his paper ‘On Aims and Methods in Ethology’ in 1963 (Tinbergen, 1963) the subject was broad based and encompassed both how animal bodies worked to produce behaviour as well as how natural selection affected behaviour. About this time, too, Ruth Harrison (1964) published her book Animal Machines which alerted the general public to the welfare problems of what came to be known as ‘factory farming’. As a direct result of her book, the UK Government set up the Brambell Committee to enquire into the welfare of farm animals. Now, just at the time when people were beginning to ask questions about animal welfare, ethologists began to turn away from broad-based questions about mechanism and development of behaviour and became much more interested in ‘sociobiology’. As a result, when they began to ask questions about what happened when you kept animals in small cages or whether animals that were unable to carry out their natural behaviour patterns in barren environments suffered as a result, very few pure ethologists bothered to answer. They were all off trying to answer questions about inclusive fitness. They were prepared to tell you all about the adaptiveness of an animal’s behaviour but were not interested in causal questions about behaviour, such as those about an animal’s

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motivation to do behaviour it was prevented from doing, which are the most relevant to animal welfare. In fact, the only motivational model around was the psychohydraulic model developed by Konrad Lorenz, which had been shown to be an inadequate explanation even for the behaviours it was designed for, such as feeding and stickleback courtship. Nevertheless, it continued to crop up in the applied ethological literature for at least 15-20 years because there was no coherent alternative. ‘Pure’ ethologists had simply not been sufficiently interested in motivational questions-they were all off asking adaptive questions and calling themselves behavioural ecologists. (It is now realised that behavioural ecology by itself is not enough. Even behavioural ecologists have realised that they have to take into account mechanism as well and adaptation and I’m glad to say are beginning to sound more like proper ethologists again. The study of animal behaviour today now looks more like the broad-based subject it was in the 1960s than it has for some time.) Meanwhile, applied ethologists, rightly becoming impatient with this narrow concentration on what was supposed to be just one of the four questions in ethology, went off on their own track, founded their own journal, had their own society and in many ways kept the light of a broad-based ethology burning much better than pure ethology. As Ian Duncan stressed in his lecture last year, the greatest progress in animal welfare research has come from taking an approach that involves asking different kinds of question. Conversely, there has been a lack of progress when people have taken too narrow a view and concentrated just on one approach. This is particularly well illustrated by the search for good physiological measures of stress. Rushen (1991), Mason and Mend1 (1993) and Broom and Johnson (1993) and many others have pointed out how difficult it is to obtain good physiological measures of stress because many of the results are contradictory. If corticosteroid levels are used as a measure of stress in hens, for example, we could conclude that battery caged hens are more stressed than those in pens, less stressed in cages than in pens, equally stressed in cages and pens or either equally or less stressed depending on how the birds are handled (Rushen, 1991). The fact that different answers are obtained in different studies could be taken as showing that the measures used are unreliable. But it may be that we are sometimes too obsessed with measuring one single variable such as corticosteroid levels and wanting it to conform to some nice neat pattern. Perhaps we should take a broader view and look at what other people have discovered about the way in which plasma corticosterone levels change in different species and at different times of the year. It may not be so much that plasma corticosterone levels are unreliable, but that we have failed to understand the enormous number of variables that affect corticosterone levels. For example, Wingfield et al. (1992) looked at the effect of capture stress on plasma corticosterone levels in two different species of birds, the inca dove and the black-throated sparrow. They showed that in the black-throated sparrow, there were major differences between winter and summer, with the rise in corticosterone levels being much smaller in summer. In the inca dove, by contrast there were no such seasonal effects. They were able to relate these differences to major differences in the breeding habits of the two species. So instead of giving up in despair and saying that changes in corticosteroid levels are so complicated and unreliable and we cannot measure stress properly, we should take a broader

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ethological view, try to understand what these substances are doing in the lives of real animals and stop looking for a simple measure of stress. We must not over-simplify that which is complicated. We must acknowledge the complexity of what we are trying to do in animal welfare research and, although it would be nice to have simple measures, we may not be able to have them. After all, if we think about it from first principles, we would expect animals to respond differently depending on what was happening to them. The original finding of classical stress studies that there were similarities in the way in which animals responded to very different factors such as cold, overcrowding and so on is what is surprising. The whole point about behaviour is that it is flexible. Animal’s don’t just have one ‘danger response’ which they put into effect whether the danger comes from being too cold or from a predator. They have lots of different ways of responding. They will respond in one way if they are ‘stressed’ by aggression from members of their own species, but in another way if they are stressed by lack of food. So we really shouldn’t be surprised if we are unable to find a single measure of stress for all these different circumstances. I do feel that the search for this single measure of stress-as though it must be there if only we could catch it-may have been a serious obstacle to progress. There is no single answer, no magic litmus test for stress or its absence. Welfare is complex! One of the reasons we may have failed to make as much progress as we could have done is that we have not actually faced up to that. We have wanted simple answers and where we have looked for them and failed to find them, we’ve said “oh we can’t measure welfare: all the measures are inconsistent”. In order to understand the animals we work with, we have to understand that animal bodies are complex, so we must learn about mechanism from all sorts of points of view-physiological and behavioural, of how behaviour develops, of what triggers it to happen and how what we see in captive animals is related to behaviour that has evolved in the wild (there is a role for behavioural ecology too!). The task is a long and difficult one. This leads on nicely to the third possible reason why we could be accused of not having made much progress in animal welfare research. 1.3. Is it because our approaches answers?

and methods are sound but we need time to find the

This is basically the position that I think is the right one. Our subject matter is difficult, but not, as I’ve argued, impossible, especially if we keep a broad-based outlook. I would also say that where you are up against something complex, you are right to go carefully. It is an honourable thing to do to say “I don’t know” in the face of complexity. That is very much better than being tempted to give quick and easy but misleading answers to questions. I quote John Webster again: “One of the reasons why the animal welfare movement has achieved so little is that it has demanded too much. If we are to convert a proper concern for animal welfare into effective action, our approach must necessarily be pragmatic, utilitarian and circumspect.” (Webster, 1995, p. viii) If legislators complain that animal welfare researchers are not giving them the answers they want, we should listen carefully. We should ask ourselves whether we are

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doing as much as we can. In the end, however, we may have to say firmly that the answers are more difficult than can be settled by one simple experiment. We should not be intimidated, any more than people looking for a cure for cancer should be intimidated, by people saying well, you’ve had enough money, you should have found the answers by now. Some problems-like a cure for cancer or discovering the origin of the Universe or how genes control development-just are difficult and take much longer than politicians would like. Animal welfare-which, as I’ve argued, has to take into account many different aspects of animal health, physiology and behaviour-is one of those difficult subjects. How the brain works, how bodies work-these are not trivial questions and they won’t have trivial answers. So while I think we must always bear in mind that we perhaps could have achieved more, in the end we may have to say firmly that the task is too difficult-and too important-for quick and easy answers. This is perhaps an important point when politicians really start getting critical and saying that animal welfare research is falling a long way behind public opinion. They point out that the moral high ground-over the transport of animals, for example-is often taken by animal welfare activists, not scientists. Changes in the law are being driven by public opinion based on gut feelings not by overwhelming pressure from findings of the research community. Even in the face of such provocation, we should hold our ground. It is a wholly honourable and admirable thing to do. Anyone who wants simple answers to questions about animal welfare is going to get the wrong answers. This brings me to the final possible reason for why we have not made more obvious progress: 1.4. Is it because we have answers to critical problems the politicians?

but have not conceyed them to

It is very important that we publicise what we do, although obviously not if it means distorting our findings. One of the problems with talking to journalists is that many (I can’t help suspecting most) are more interested in a good story than they are in the truth. They tend not to be interested in stories that involve taking a balanced view or in negative or incomplete findings. We do, however, have a duty to report to the public, to write up our work not just for scientific journals but also in more accessible forms. Popular science and farming journals are interested in animal welfare issues and we should take full advantage of this. I am also pleased to see that many of the mainstream behaviour journals are now publishing an increasing number of papers on animal welfare. In other words, I don’t think we are being seriously ignored but it may be that we should put more effort into publicising what we do so that politicians have no excuse for not knowing what we do. To conclude this section of the talk, I have argued that the subject matter of animal welfare research is difficult but not impossible. Even the central and most difficult problem-that of the subjective feelings of animals-is amenable to scientific investigation and indeed is being studied by scientists from many different disciplines. What we now lack is a coherent theory of pleasure and pain in animals. Although the study of the cognitive abilities is important, the study of animal emotions may be even more relevant to the study of animal welfare.

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I have also argued that, generally speaking, we are on the right track in what we are doing and are most likely to achieve useful results if we stick to a broad-based ethological view and take into account many different measures of welfare-health, physiology and behaviour. Finally, I believe that the main reason why we, as members of a discipline, may not have made more progress in animal welfare research is that our subject matter itself is difficult. We should not be bullied into over-simplifying what is complex, but we should make every effort to explain what we have achieved.

2. Social recognition in hens I said that I did not want to go through the whole of a David Wood-Gush Memorial lecture just talking in vague and general terms, so I’d like to end with a brief description of some experiments which illustrate one of the points I was making-namely, that you can go very wrong if you do not take a broad ethological approach. The experiments were carried out on an animal that David worked on for much of his life and form part of an investigation into how hens recognise each other and, in particular, how they recognise a member of their own group. As is well known, hens in small groups form dominance hierarchies or peck orders. Although it has been assumed that these peck orders are based on individual recognition, this is not a necessary prerequisite for their formation (Barnard and Burke, 1979) and direct evidence that hens recognise each other as individuals is surprisingly sparse. Consequently, a research student of mine, Harry Bradshaw, did what we thought was a simple and obvious experiment to see whether hens could be trained to discriminate between two familiar individuals. He trained hens in a Y-maze to go towards one individual rather than another for a food reward. Although the hens eventually learnt this discrimination, they only did so with enormous difficulty and took 150-200 trials to achieve criterion (Bradshaw, 1991). This result was surprising because we thought he was training hens to do something they did naturally all the time-indeed, he was using hens that were familiar to each other and so might be expected to have already learnt to discriminate each other. Yet, they were making extremely heavy weather of this supposedly simple task. In view of the time it had taken for them to learn, we decided to use slides rather than real birds and to automate the apparatus. However, we first had to be sure that they saw the slides as representing real hens. We therefore did an operant conditioning experiment in which hens were trained to peck a computer-controlled panel for food when they saw a photograph of hen A but not of hen B, but we ran the experiment under two conditions. Under the ‘familiar’ condition, the two hens appearing in the photographs were members of the subject bird’s own group, whereas under the ‘unfamiliar’ condition, neither hen was familiar. We argued that if the hens saw the photographs as representing real birds, there should be a difference between these two conditions, for example in speed of learning or ability to recognise novel views of the target hens. The fact that there was no difference at all led us to conclude that although the hens could learn the discrimination, they did not recognise the photographs as showing hens (Bradshaw and Dawkins, 1993).

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I ask you to remember these two negative results because I subsequently came to realise that they were the result of a faulty approach to the whole problem. All the next experiments were on real birds. The next question I asked was “What view of each other do hens have?” It seemed to be important to establish this since if hens always look at each other by looking at either the front or the side of each other, this could affect how they recognise each other. I did a simple experiment which involved removing a visual barrier between two birds and looking at the head angles the birds adopted with respect to each other. By confining both hens in small circular cages, I could control the distance between them. The hens were tested with the other bird at one of three distances: 0 m (cages touching), 0.7 m and 1.4 m, and with both birds that were familiar to each other and those that were unfamiliar. The whole experiment was filmed with an overhead video camera and the results were very interesting. No difference in head angle was found in whether the hens were looking at a familiar or unfamiliar bird but there was a major difference in how they looked with distance. At the medium (0.7 m) and long (1.4 m> distances the birds viewed each other at angles of between 54 and 72” from a straight line from one bird to the other, but at the closest distance they viewed each other with the head within 18” either side of straight ahead. This confirms results previously obtained on freely moving hens (Mankovitch and Banks, 1982; Keeling and Duncan, 1989) and are compatible with the view that hens are using the lateral field to view distant objects and the binocular field, which is about 27” wide to view close objects. Keeling and Duncan proposed that hens use the binocular field so that they can judge the distance of hens that are very close. However, I want to suggest that there may be another even more important reason why hens use the binocular field which I’ll explain in a moment. As a result of this experiment, I began to suspect that hens could only recognise each other when they were very close together indeed (Dawkins, 1995). To test this idea, I gave hens a choice between feeding near a familiar individual or feeding near an unfamiliar individual but I gave them this choice test at three different distances. This was done by placing a barrier between the two target hens, and making the barrier either 8 cm long (so that the hens could go right up close to both hens before making their choice), 66 cm long (so that they had to choose from much further away) or 124 cm long. The hens showed a preference for feeding near a familiar bird but only when they could approach closely (8 cm barrier). When forced to make their choice at either 66 or 124 cm they showed no such preference-their choices were essentially random. This result is compatible with the idea that hens can only recognise each other at a very short distance (although it is not the only possible explanation). But why should this be? When a chicken is looking forwards, the binocular overlap between the two eyes is not the only notable feature. Birds are also myopic in the lower frontal field, giving them the ability to see objects that are very close, for example food objects that they are about to peck. This lower frontal field has therefore been called the ‘pecking field’ but in fact it is more accurately described a gradient of myopia, and it allows them to keep

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different parts of the ground in focus at the same time (Hodos and Erichsen, 1990). Laying hens are between - 2D and - 3D, myopic in the lower frontal field. This means that hens would be unable to see the head of another bird in clear focus at distances greater than l/2- l/3 m if they are using the lower binocular field. While it is difficult or impossible to measure very accurately the angles and distances in 3D in freely moving birds, it is possible to see whether the hypothesis that the myopic lower frontal field is used in recognition is within the bounds of plausibility. For example, if hens never come near enough to use the myopic lower field, the hypothesis could be discarded. What is meant by close can be specified-somewhere between 0.3 m and 5 cm, which is the near point of accommodation for the chicken. I therefore placed two birds in a place that was unfamiliar to both of them, one on either side of a visual barrier. I then removed the visual barrier and videoed what the birds did. All the birds were familiar to each other, that is, they lived together in the same home cage and had in fact been together within the last 5 minutes. But none of them had been in the particular testing cage before. In all eight cases, the birds went up close to each other and either ‘scrutinised’ each other’s head region or even pecked them on the comb. The mean distance for such scrutinies was 13 cm. This suggests that the lower myopic field-the so-called pecking field of the retina-is also used for scrutinising other hens as part of the process of recognition, even when birds are familiar with each other. Further evidence for the importance of close-up scrutiny comes from observing the behaviour of hens before and after they have been allowed to scrutinise another hen close up. If it is true that hens are unable to recognise each other at a distance and can only do so when they are close (approximately 15 cm), then it should follow that at a distance, behaviour towards familiar and unfamiliar hens should be similar but it should differ once the close-up examination has taken place. I did yet another simple experiment, this time in which one bird was confined in a cage in one comer of a room and another (the experimental) bird was released into the room and was free either to interact with the caged bird or not. I measured how close the experimental bird went to the caged bird in the first three minutes they were together. Then I replaced the experimental bird in its start box, released it again and again measured its distance from the caged bird. I did this a total of four times. Each experimental bird received two such series of four tests, one in which the bird in the cage was familiar to it and one in which it was unfamiliar. If close-up scrutiny was an important part of recognition, then the behaviour of the birds in the first test (before they had examined the other bird) should be the same whether the other bird was familiar or unfamiliar, but should differ in the subsequent tests. The results were consistent with this. In the first test of a series, there was no difference in how close a bird went to a familiar or an unfamiliar bird-in all cases the caged bird was examined. But by the second test, when the birds had been through the recognition process, they continued to go close to familiar birds but kept their distance from unfamiliar ones (Dawkins, 1996) NOW we can begin to see why those earlier experiments did not work. Bradshaw’s experiment training birds to discriminate individual birds required the birds to make a discrimination between the two target birds at about 0.75 m-too far away for the

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experimental bird to ‘scrutinise’ and find out who it was. The fact that they eventually did learn to discriminate the two birds but only with great difficulty suggests that they were forced to use an entirely new cue. Secondly, it explains why the experiment using slides showed no evidence of transfer from real birds to photographs. The screen was put approximately 1.5 m in front of the pecking key and so was too far away for them to use their normal methods of recognition. I wasn’t being a proper ethologist. I was not thinking clearly about how birds normally approach each other. I reasoned that if this explanation were correct, then perhaps high quality photographs that hens can view close-up might work. However, I have now done two experiments in which hens were offered a choice between feeding near a photograph of a familiar bird and feeding near a photograph of an unfamiliar bird. In both cases, the hens showed an initial interest in the photographs, approached them cautiously, scrutinised them from a few centimetres and in some cases even pecked them on the combs. Then, as they were obviously not real chickens, they took no further notice of them and showed no preference (Dawkins, 1996). My research student, Richard D’Eath, has obtained very similar results with video images of familiar and unfamiliar hens (D’Eath and Dawkins, 1996). These results are compatible with the view that hens use close-up scrutiny as part of the process of social recognition. If they are not allowed to examine a photograph or even a live bird close up, they fail to recognise it. If they are allowed to examine a video image or a photograph closely, they quickly realise that it is not the real thing. You may be able to fool a monkey with a video or photographic image, but you can’t fool a chicken for very long! Now, two things may occur to you at this point. The first is: what a crazy idea to have recognition system that only works close-up. However, in wild junglefowl, or where domestic hens are kept in small groups, this would not be a particular disadvantage. Junglefowl live in groups of four to six birds and they remain close to particular individuals (Sullivan, 199 1). This means that they would not have to keep examining other birds to discover their identity. They could assume that they were familiar unless an unusual event (such as entering another group’s territory) occurred. On the other hand, in very large groups such as those in which hens are kept commercially in free-range or deep litter, it may be much more of a problem. Birds may actually not know the identity of the birds around them. The second thing that may occur to you is to wonder why hens might be unable to recognise except when very close, particularly as hens have good eyesight (e.g. Zeigler and Bischoff, 1993) and can be trained to make complex discriminations between stimuli seen from much larger distances. In other words, what is the cause of this constraint? There are a number of possible reasons. 1. They need to see the other hen from a viewpoint, perhaps the view from which they saw it when they fought in the original settlement of the peck order. Going close to another bird may be a way of forcing the other to turn and recreate the view that is familiar. 2. The cue used is only visible from a very short distance. If hens were using, say, the pattern of pits on the comb of another bird, they might have to go close in order to see it at all.

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3. They are unable to transfer something learnt in one part of the retina (e.g. the binocular frontal field used to view another bird during a fight to settle dominance) to the lateral field for more distant vision. I am at present investigating which, if any, of these explanations is likely to be correct. The conclusion that I would draw from this series of often unsuccessful experiments is that even if you are doing something as apparently straightforward as presenting photographic images, you have to take a broad view. You have to be an ethologist as Tinbergen conceived one-that is, to understand, amongst other things, what the animal’s natural behaviour is, what it is adapted to, how it acquires the relevant information as well as how it acquires and processes sensory information. To tie this in with the overall message of this lecture: if we stop being ethologists, we’re lost!

Acknowledgements

I am very grateful to the David Wood-Gush Memorial Fund for enabling me to attend the ISAE conference in Exeter and for their support in giving this lecture.

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