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The author explains why comfort in experimental animals is essential both for humane reasons and reasons of obtaining sound scientific data. He discusses how even "minor" distress can impact an animal's physiological and emotional well-being. Examples cited include studies of caged rats and dogs, preening and bathing birds, hunting and killing cats, feeding and grooming ducklings, scratching goats and zebras, and grooming baboons. The various levels of needs and comfort are also discussed.
In two ways, Chance (1956a) has extended and reinforced this general principle. First, he has pointed out and experimentally demonstrated another effect of behavioral disturbance. He has shown that such disturbance may greatly increase variation in physiological responses between individual animals. Now for most experimental purposes, but especially in the massive experiments of biological assay (the testing of biological substances, it is very necessary for the animals tested to be physiologically as uniform as possible. If there is great individual variation, many more animals must be used to obtain, with a given precision, an estimate of the effect of the drug. It follows that by eliminating sources of variance we can obtain equally good results from much fewer animals. It used to be supposed that, if all animals are treated uniformly (or uniformly badly), they will respond in a uniform way. Chance has shown that this is not so. On the contrary, in some behavioral conditions, even if uniformly applied to all the test animals, the individuals will vary much more than in other conditions. It is now possible to look for optimal conditions, in which variation will be greatly reduced. Although the principle has not yet been shown conclusively in this field, evidence from other sources makes it likely that these optimal conditions for reducing variance are precisely those in which the animals are most comfortable, happy, or at ease (Michie, 1955). This would mean animals would vary least just when they are most satisfactory as tools for physiological study. It may be that we shall sometimes have to balance the two claims--for reduction in numbers of animals used is of just as much importance, humanitarian and practical, as refinement of technique on those still employed (Russell, 1957). But in any event, the principle promises great gains for experimentation in both humaneness and efficiency, and it raises some very fundamental issues indeed.
The other thing Chance has shown is the extraordinarily slight and apparently trivial nature of the behavioral factors which are all-important here. Physiological variance in rats depends on such factors as whether the experimenter's hands smell of strange rats, whether the rats have been moved to an unfamiliar cage, and how many rats of the same sex are caged together, for a given amount of space per individual Chance (1957). There is no question here of severe distress. Nor is acute pain necessary to upset the physiology of an individual animal. Many other examples might be cited now (Lane-Petter, 1953). Dogs kept in cages slightly too small for them do not appear to be in serious pain. Rather, they appear, in the words of the experimenters who designed a better cage for this reason, "ill-at-ease" and "uncomfortable." Yet this is enough to disturb their excretion and metabolism to such an extent as to render them useless for biochemical study.
All this has an obvious implication for humane and efficient experimentation, and indeed in many other contexts, such as stockbreeding. It is not enough to avoid gross distress. We must also eliminate what appears to us as very mild malaise and discomfort. This is the logical ultimate goal of animal welfare. And so the thoughts of scientific animal-lovers must turn towards the problem of comfort in animals. We cannot hope to solve this problem overnight. To begin with, we must try to think about it as a general problem in its own right. This is what I shall try to do, in a very modest, rudimentary, and inconclusive way, in the present paper.
The starting-point lies in the physiological needs of the higher animal -- and in this paper I shall confine myself to vertebrates. By physiological need, I mean the need for keeping certain essential variables within a more or less narrow range, necessary for maintaining life (Ashby, 1952). For instance, the temperature, osmotic pressure, ion balance and ph of the blood must be kept within certain limits. The state and urgency of these needs must be signalled in the central nervous system, by mechanisms which we call instinctive controls, or primary drives. People sometimes speak of "peripheral tensions" as the source of such routine self-maintaining behavior. But the idea of tension at the periphery is meaningless without something in the brain to specify which of these states are tenser than others (Russell and Burch, 1959). This something we may call a routine primary drive, and to start with we may envisage a drive for each need, signalling, like a pointer reading, the state of the need concerned. The activities controlled by these drives ensure that urgent needs are satisfied, and these activities, through evolution in the species or conditioning in the individual, are so designed as to do this job as well as possible. Thus, if a signal comes through that the animal is drying up, the drive concerned will initiate drinking, or a move to a damper environment. Besides, the slow drift of the pointers towards the red, corrected by routine behavior, there are also two kinds of emergency. One is frustration, the appearance of something in the environment, such as a rival animal, which may prevent the routine satisfaction of all needs. The other is danger, the appearance of something, such as a predator, which threatens complete extinction. The corresponding two drives are those we call rage and fear, the drives of attack and escape. Finally, there are drives controlled in many lower animals by hormonal regulations, those whose activities lead to reproduction of the species--mating, parental behavior and so forth. This is, of course, the merest basic sketch. Complication soon arises, partly because some needs are physiologically intertwined, like water and heat balance, partly because some activities can serve several needs, and some needs can be satisfied by several drives lead to elaborate secondary organization of behavior.
We may suppose that an animal is at his or her most contented when this system works smoothly, all needs being satisfied before they become urgent, and frustration and danger either absent or rapidly and efficiently coped with. For our present purpose, we can neglect the emergency and reproductive drives, and consider only routine functions. Social behavior is largely composed of the former, and routine behavior much less well understood. Some routine activities are sufficiently clear-cut, on the sensory or motor sides or in terms of function, to be eliminated from further discussion. In this way we can separate out such functions as those of feeding. A large residue remains. The complication of behavior systems has created a number of secondary, or strictly behavioral needs, which vary between species. Sometimes an activity originally related to a particular drive becomes split off as a quite separate mechanism. Hunting in cats is a means to obtaining food. But the hunting drive has become partly independent of, or emancipated from, the feeding drive (Tinbergen, 1952). Indeed, the complex has become split into four drives, those of catching, killing, plucking and eating. Each of these is a sort of secondary need. Leyhausen (1956) studied cats; some of whom had been satiated with meat, which they had not killed themselves, and some who were hungry. As fast as the cats killed mice, he gave them new ones. A very hungry cat would finish eating its first mouse before catching and killing the second. A completely satiated cat would leave its first mouse uneaten and hasten to catch and kill the second. A moderately hungry cat would finish its first mouse, but while doing so it would follow with its eyes the movements of the second mouse, make little tentative movements towards it, and eat its meal in a hurry. In other words, cats cannot live by meat alone, or at least not happily. It is not enough to satisfy the original physiological need; they must also get their hunting activities off their chests. Similar considerations account for the need, in many species, for a considerable amount of general activity or exercise. Such active birds as parrots, when restrained in a small cage or on a perch, develop curious behavior symptoms, which must reflect uneasiness (Morris, 1957). Social species often have a definite secondary need for companionship, quite apart from reproduction. Mallards, for instance, whose physiological needs appear to be satisfied, show symptoms of uneasiness when separated from their comrades, and will seek companionship even by moving away from a source of food (Weidmann, 1956). Finally, some animals, notably ravens and monkeys, have a definite secondary need to explore, and investigate strange objects. Butler (1953) has shown that monkeys will solve problems for the sole reward of being able to look out of their cages and see what goes on outside. Frustration of secondary needs like this must be a real deprivation, and Hediger (1955) has argued forcibly for various kinds of "occupational therapy" in the zoo.
Breathing, though reduced to a relatively simple mechanism in mammals, often involves quite complex behavior in lower vertebrates (Spurway and Haldane, 1953). Sleep has some special aspects, which I cannot now discuss. Then there are the various forms of discomfort associated with the respiratory and alimentary tracts and the bladder, related to various forms of coughing and sneezing, to vomiting, to defecation and urination. In all these activities, autonomic responses may be as prominent as somatic behavioral ones, especially in birds and mammals. The feathers of birds can be finely adjusted for warming or cooling purposes. Perhaps we should include here the sunbathing activities of many birds.
In several North American thrush species, for instance, "sunbathing is done whenever the opportunity presents itself... The bird stiffly orients its body at right angles to the source of heat and light, fluffs out its feathers, usually spreads the uppermost wing or raises it, spreads the tail and then remains in this position for some minutes at a time. The eye nearest the light source remains wide open and the bill is typically held parted" (Dilger, 1956). Marler (1956) describes a very similar posture in the chaffinch, Andrew (1956a) in the yellow-hammer and corn bunting: he interprets the gaping of the beak as a cooling response. Dilger found that both light and heat are necessary to evoke the response. He reports that sunbathing often follows water bathing "if the proper stimuli are present at the time." But Andrew's birds showed an almost identical posture after bathing irrespective of the presence of a light and heat source, and he calls it a drying activity. We thus have little clue to the causation, and none to the function of sunbathing in birds. It remains an open question whether for them it is a comfort or for captive birds, the (much cheaper) analogue of a trip to the Riviera.
Perhaps this is true above all for birds, whose feathers are two-fold importance -- in flight and in temperature regulation. To some extent, different feathers are concerned in the two functions, and preening movements may be more or less sharply differentiated between the two (Van Iersel and Bol, 1958). Comfort activities seem specially conspicuous and persistent in birds. Tinbergen has described the pains taken by herring gulls to keep their feathers in order (1953). The bird appears to be keeping the barbs of the feathers joined, by bringing protruding feathers back into place, and "by nibbling individual feathers gently between the tips of the bill. This is done with the utmost care, and often the tiny white feathers of the neck alone take up fifteen minutes of a bird's time, many feathers being worked individually from the base to the tip." In many species, the feathers of birds can take up four different positions, sleeked, relaxed, fluffed or ruffled, control of the muscles being autonomic (Morris, 1956). Heat insulation is achieved by a layer of air trapped between feathers and skin. If the feathers are depressed (sleeked), this layer becomes thinner, and cooling results. If they are partly raised (fluffed), the feathers remain in contact with each other, and the layer of air still trapped under them becomes thicker, thus increasing insulation and conserving heat. But if they are fully raised (ruffled), the feathers lose contact and "the entrapped air spaces are lost and insulation with them" (Morris). Hence sleeking may be used for mild cooling, as during muscular exercise, fluffing for warming, and ruffling for intense cooling. The postures assume a new importance in water-birds, where fluffing probably maintains an air-barrier which water-proofs the bird, and so preserves him both from cold and water-logging.
Fabricius (1956) noticed that ducklings fed on raw, crushed fish could not keep their plumage dry in water. This water-proofing ability was restored by changing the diet to one of insects. Crushed fish proved to be harmless if given when the birds were in the water and had to dive for it. These birds have a complicated preening, which includes nibbling movements like those of the herring gull. So when fed on clean or dry food, they were able to keep their feathers in order, and thus to preserve the insulating layer of air. When fed on messy food, or crowded so that they became smeared with faeces, the barbules (small strands) of the feathers were disarranged and could not be preened, as was shown by direct observation of these. Fabricius concluded that water-birds should never be crowded or fed messy food on land. His study also shows the supreme importance of the preening activity itself. It takes little imagination to conceive the distress of a water-bird polluted by heavy oil.
The use of tools to reach inaccessible parts is virtually unheard of below the primates, but I have recently heard from Dr. D. Morris a remarkable account of a certain nanny-goat. This goat had an irritated udder, and was unable to reach it by normal means. She has spontaneously learned to select straws of suitable length and stiffness, and to use them in exactly the manner of an eighteenth-century back-scratcher. The inventor has already "taught" this technique to another goat. This must surely be a record in the annals of vertebrate comfort behavior.
Finally, we may mention the habit of many birds of bathing in water, dust, or sand (e.g. Poulsen, 1953; Baggerman et al., 1956; Marler, 1956; Andrew 1956a; Van Iersel and Bol, 1958). In dust, some birds throw up the dust with their feet, others with their beaks (Poulsen). Bathing of all these kinds is regularly followed by preening, usually exceptionally thorough and sustained.
Among comfort activities, the bathing drive seems to be a powerful one, which can dominate the behavior of the bird. "Once the tendency to bathe is aroused," writes Andrew (1957a), "a bird may repeatedly approach a water dish despite its fear of a superior perched near the dish." If the bathing drive is high, and the bathing dish occupied by another bird, some thrushes may go through the motions of bathing on dry land (Dilger, 1956)--an excellent example of vacuum activity, the process whereby a high drive is expressed in action in the absence of the normal external sensory inputs (Lorenz, 1937). In such cases, the bird not only does the bathing movements, but dries and preens itself as well, exactly as if it had a real bath. "It is ludicrous to see such a bird after `bathing' fly heavily, as if soaking wet, to a perch and commence the lengthy series of shakes and preens that normally follow a bath" (Dilger). Vacuum bathing activity has been observed in a number of other bird species, such as mallards (Weidmann, 1956; Dilger, l.c.). On the other hand, the preening performance is rather readily suppressed by other drives. "A bird with wet plumage will not give feather-settling movements for several minutes after being put into an unfamiliar cage" (Andrew). In general, comfort activities are rather readily suppressed by other drives; Van Iersel and Bol give abundant evidence in support of this. There is probably much truth in Tinbergen's comment, cited earlier, that preening fills "leisure hours when the bird has, so to say, nothing better to do." What the comfort drives lack in the capacity to compete with other drives, they probably make up by their persistent, almost permanent activity, which must enable them to seize any chance of controlling the motor system. Many workers have commented on the readiness of animals to preen or groom without any obvious external stimulus. But there are occasions when comfort proper does over-ride all other considerations. Hediger (1955) has spent much of his life observing animals in the wild with the object of making conditions in his zoo as natural and acceptable as possible. While in Africa, he noticed that termite hills were often rubbed smooth, and further investigation disclosed the fact that zebras chafe themselves against these natural scratching-posts. On his return, Hediger installed an imitation (cement) termite hill in the zebra paddock. Upon this the zebras positively went mad, and rushed in a body to the post. In order to give the cement time to set, the animals had to be beaten back to another enclosure by a posse of keepers. When the cement had set and they were again allowed access, it was like Paradise Regained.
No less striking are the cases of more or less symbiotic relationship between animal species, where one grooms the other. For instance, many small fish of several species live in restricted territories on the sea-bottom. To these "barber-shops," as they have been called, come large fish at certain times of the day. Once arrived, the big fish give a special signal movement of invitation, whereupon the small ones swarm through their gills, disinfesting these of parasites by eating them.
The topic of interspecific interaction inevitably leads us to the relationship between man and other animals, and hence to the question of comfort in man. For if man tends to neglect discomfort in lower animals, it may be, in a quite fundamental way, the outcome of neglecting his own. Man can, of course, pursue comfort intelligently; but with his own peculiar pathology he can also repress discomfort. Freud himself, partly for lack of information about comfort activities in animals, was led to the strange and false conclusion that human infants like being dirty. In certain cultures (e.g., Europe in the Middle Ages) discomfort due to dirt has been repressed, and cleaning activities inhibited, to a quite remarkable extent A cartoon appeared recently in a London newspaper, which I cannot resist describing before I close this article. The picture shows an Oriental scene. In the foreground is a fakir, with an expression of surprise and delight, addressing a somewhat dubious friend. The fakir is lying on a plank studded with nails--but he has turned it upside down and is lying on the smooth side. "I've just made" he cries "the most wonderful discovery!"
From 1948 to 1954, he worked at Oxford on the endocrinology and behavior of clawed frogs, and developed with Dr. Richard Murray, a more humane method of killing this species. From 1954 to 1959, with Rex L. Burch, he worked for the Universities Federation for Animal Welfare (UFAW), and in 1959 they published The Principles of Humane Experimental Technique, in which they introduced "the three Rs of animal experimentation," which have been used as major guidelines for making life better for animals ever since. These are (in Dr. Russell's own words): 1) Replacement of animals by insentient material,
2) Reduction in numbers used to obtain given results,
3) Refinement of procedures to diminish distress imposed on animals, From 1959 to 1964, Professor Russell was in private practice as a psychoanalyst. From 1964 to 1966, he was a Scientific Information Officer at the Commonwealth Bureau of Pastures and Field Crops.
Since then he has been in the Department of Sociology, University of Reading as Lecturer (1966), Reader (1971), Professor (1986) and Emeritus Professor (1990). He has taught demography, elementary statistics, genetics, ecology, cultural evolution, and social aspects of ancient city-states.
From 1979 to 1982 he was President of the Folklore Society. In 1978
he co-edited, with Professor Canon J.R. Porter, the
Society's centenary
volume, Animals in
Folklore.
Retirement from other activities is now enabling him to renew his interest in laboratory animal welfare. In 1990, The Humane Society of the United States established the Russell and Burch Award for Contributions to Laboratory Animal Welfare. In 1994, professor Russell and Rex Burch were awarded the Smith Kline-Beecham prizes by the Research Defence Society, for their own contribution in developing the concept of "The 3 Rs" for animal welfare in research.
Professor Russell's ground-breaking book for animal welfare in research, The Principles of Humane Experimental Technique (1959) was the birth of the famous "3 Rs" of addressing animal welfare in research: REDUCTION, REPLACEMENT, REFINEMENT. He also published three others books, co-edited another book, and contributed to some thirty books and one hundred thirty scientific papers. He has made many radio and some television broadcasts, including eight years on BBC Radio 4's "Round Britain Quiz." Two of his books and many of his book contributions and papers were written jointly with his wife, Claire Russell, ethologist, psychoanalyst and poet. They have generally traveled too much to have animal companions, but in earlier times Claire Russell had notable cat friends, including an unusually intelligent Tom called Oedipus (Puss for short).
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| Copies of this journal are no longer available for sale, but our other two journals, Society & Animals and the Journal of Applied Animal Welfare Science, are available and subscriptions are quite affordable. They can be ordered online via our secure order page. |