Why It Is Important to Understand Animal Behavior

Joy Mench, Ph.D., is Professor in the Department of Animal Science, University of California, Davis, California. “Animals should be housed with a goal of maximizing species-specific behaviors and minimizing stress-induced behaviors” ( NRC 1996 , p 22)--a laudable goal, but can it be achieved? The answer is perhaps, but doing so will necessitate addressing some difficult questions. How do we maximize behaviors in an environment that is so different from the one in which the animal evolved its species-typical behaviors? Should the animal be allowed to perform all of its species-typical behaviors or only certain ones? If the latter, how do we choose which ones? How can we recognize and minimize stress-induced behaviors? Although people have long been fascinated by the behavior of animals, the formal discipline of animal behavior--ethology--is actually relatively new, dating to the work of Konrad Lorenz in Austria in the 1930s. Application of ethological principles and methods to the study of animal welfare is an even newer endeavor, of course, and one that has generated a great deal of stimulating discussion and controversy during its short history. In this paper, I provide an overview of the development of behavioral approaches to the study of animal welfare. I then discuss some reasons that behaviors are important to animals and describe how an understanding of behavior can be useful when designing housing environments for laboratory animals. The report on intensive farming practices authored by the Brambell committee (1965 ) was probably the first published document to emphasize the importance of behavior in assessing animal welfare. This committee was established by the British government after the public outcry following publication of Ruth Harrison's expos? of what she referred to as “factory farming” methods in Animal Machines (1964). After hearing testimony and reviewing farming practices in Europe, the members of the committee wrote ( Brambell 1965 , p 10): The scientific evidence bearing on the sensations and sufferings of animals is derived from anatomy and physiology on the one hand and from ethology, the science of human behavior, on the other … we have been impressed by the evidence to be derived from the study of the behavior of the animal. We consider that this is a field of scientific research in relation to animal husbandry which has not attracted the attention which it deserves and that opportunities should be sought to encourage its development. They further concluded that animals had behavioral needs that could not be satisfied in barren, restrictive environments, and that not providing for those needs was likely to cause suffering, ideas that have proven to be very influential in shaping ethological research on animal welfare. In an appendix to the Brambell report, the eminent zoologist W. H. Thorpe argued that welfare is promoted when animals are able to perform the activities that most closely resemble the behavioral repertoire of their free-ranging con-specifics. However, this idea soon fell into disfavor among many scientists studying animal welfare ( Dawkins 1980 ). Fraser (1989 ), for example, discussed the limitations of using the normal behavioral repertoire as the baseline for ensuring welfare with reference to 3 normal behaviors in swine: the distress calls given by piglets when they are separated from their mothers; nest building by sows before parturition; and wallowing, which is a thermoregulatory behavior shown only under hot conditions. Fraser pointed out that a pig's natural behavioral repertoire consists of things that the pig really does not want to do (such as give distress calls), wants to do (such as build a nest), and wants to do but only when conditions require it (such as wallow). The 3 behaviors described above obviously have different implications for welfare. Providing a pregnant sow kept in a temperature-controlled environment with a wallow would do little to improve her welfare, whereas giving her nest-building material might improve her welfare a great deal. Placing piglets in a situation in which they give distress calls, however, would actually reduce their welfare. Thus, to assess the welfare significance of particular behaviors, it is important to have an understanding of what causes the behavior to occur in the first place. Many factors can motivate the performance of behaviors, and a variety of models have been proposed in an attempt to explain how motivational systems work ( Jensen and Toates 1993 ; Toates 1986 ). One approach to studying motivation has been the attempt to determine the relative importance of internal and external factors in causing particular behaviors (for example, Hughes 1988 ). Some behaviors are classified as being motivated primarily by factors external to the animal, exemplified by thermoregulatory behaviors like wallowing in pigs and antipredator behaviors in prey species. Other behaviors, like food searching when hungry, appear to be largely internally motivated. Yet other behaviors are elicited by complex interplay between both internal and external factors. Mating behavior, for example, is motivated by hormonal state, which may in turn depend on seasonal and other environmental factors as well as the accessibility and readiness of appropriate sexual partners. Cues from one partner to the other during courtship can further influence the hormonal states and behavior of the courting pair. The study of motivation has been very important in applied ethology because of its link to the Brambell committee's ideas about behavioral needs. Behavioral needs are generally conceptualized as those behaviors that the animal must perform regardless of environmental circumstances, that is, primarily internally motivated behaviors that may occur even in the absence of appropriate external stimulation, although sometimes in an aberrant form. Hens kept in cages without litter material, for example, will still perform dustbathing behaviors, although the movements are somewhat abnormal and the dustbathing episode is short compared with a normal dustbathing episode ( Vestergaard 1980 ). Behaviors of this type are called vacuum activities (because they occur “in a vacuum,” so to speak). Another form these behaviors can take is to become stereotyped. Many oral stereotypies, for instance, have been shown to be associated with the lack of opportunity to perform particular components of feeding behavior, including foraging ( Bayne and others 1991 ; Redbo and Norblad 1997 ; Rushen and others 1993 ). A thorny question remains, however: Is the performance of an aberrant behavior, or not meeting a behavioral need, linked to “suffering” (hereafter referred to as distress) as the Brambell committee claimed? Duncan (1978a ) argued that independent verification was necessary to demonstrate that unusual or inappropriate behaviors indicated reduced welfare. One common approach to providing such verification has been to measure physiological (including immunological) parameters associated with stress and then to attempt to correlate those parameters with abnormal behaviors or responses to behavioral restriction. However, physiological measures also have many limitations, and it has generally proven difficult to interpret their significance as indicators of welfare ( Dawkins 1980 ; Mason and Mendl 1993 ; Rushen and de Passill? 1992 ). The answer to the question about suffering is therefore still elusive, as can be demonstrated by considering research on abnormal behaviors. In the laboratory setting, abnormal behaviors are often used as the benchmark of poor housing conditions and the need for environmental enrichment. Behaviors that cause injury to either the initiator (self-mutilation) or the recipient (cannibalism) clearly have a negative effect on the welfare of the individual sustaining the injury. However, no consistent relationship has been demonstrated between noninjurious abnormal behaviors, particularly stereotypies, and other measures of reduced welfare ( Lawrence and Rushen 1993 ; Mason 1991 ; Mench and Mason 1997 ). Stereotypies are sometimes, but not always, linked to physiological changes indicative of stress; and in fact, the performance of stereotypies sometimes appears to be rewarding or to reduce stress. Although abnormal behaviors often appear to arise from frustrated motivation, they may also be caused by factors that are not directly related to a poor environment, such as pathology or neurological predisposition. Most puzzling is that established stereotypies may also persist even when animals are placed in enriched environments. Has the enriched environment failed to improve the animal's welfare? Mason (1991 ) suggests instead that stereotypies may be as much “scars” of past experience as they are indicators of current frustration or environmental inadequacy. Since many stereotypies can be prevented from forming by altering the animal's environmental conditions, there is widespread agreement that appropriate steps should be taken to accomplish this ( Duncan and others 1993 ). Another way in which behavior has been used to provide information about welfare is in studies giving animals choices and opportunities to express preferences ( Dawkins 1980 ). In a pioneering study of animal preferences, Hughes and Black (1973 ) decided to test a recommendation made by the Brambell committee--that laying hens should be kept in cages with floors made of rectangular metal mesh, rather than fine-gauge “chicken wire,” because the latter sags and the hen's foot is not well adapted to grip it comfortably. Hughes and Black gave hens a choice of 4 different types of flooring including chicken wire, 2 types of rectangular mesh, and perforated metal. The hens obviously viewed the situation somewhat differently than did the Brambell Committee; they chose the chicken wire in preference to the other floors, and subsequent visual inspection showed that the chicken wire in fact provided the best support for their feet. Preference testing of this type has now been used widely in studies of animal welfare, including assessing preferences shown for cage height, light intensity, flooring, bedding material, and enrichment devices by rats ( Blom and others 1995 , 1996 ; Chmiel and Noonan 1996 ; Manser and others 1995 ; van de Weerd and others 1996 ), sleeping locations by mice ( Sherwin 1996 ), flooring and social companions by hamsters ( Arnold and Estep 1990 , 1994 ), and social companions by rabbits ( Held and others 1995 ). Cautions have been raised about the use and interpretation of preference testing ( Dawkins 1980 ; Duncan 1978b ). Preferences can be shaped by many factors, including genetics, previous experience, and the choices offered and testing methods used. Short-term choices may not correspond well to long-term welfare, since animals (like humans) may choose things that are immediately rewarding but are not necessarily best for them in the long term. An awareness of these problems has led to a rapid evolution of preference testing toward asking more precise questions and taking more comprehensive measures ( Fraser and others 1993 ); and preference testing is now widely considered to be a useful tool, particularly for evaluating specific aspects of the environment like flooring, temperature, and lighting. One enduring criticism leveled against preference testing, however, is that it fails to distinguish between important choices and not-so-important ones--between so-called “luxuries” and “necessities.” Dawkins (1990 ) developed a model that she suggested could address this concern by allowing the strength of the motivation underlying particular choices to be determined. Her “consumer demand” model is derived from economic theory and involves requiring animals to pay some kind of cost to acquire commodities. For instance, a hen might have to peck a key or push through a barrier to gain access to a nestbox or dustbath. The amount of key pecking or barrier pushing she is willing to do can be compared with the amount she is willing to do to obtain a commodity known to be important to her, such as food. Priority can then be given to providing opportunities for animals to perform those behaviors for which they show a strong demand (that is, needs). Dawkins argues that an animal will work the most for things that ensure its fitness or are perceived to be important in ensuring its fitness. This is an important concept because it emphasizes that domesticated and purpose-bred animals may continue to behave in ways shaped by their evolutionary history, even if those behaviors are not necessarily important for (or are sometimes even detrimental to) their survival or fitness in captivity. In fact, most behavioral changes accompanying domestication are qualitative rather than quantitative, that is, they result in changes in the frequency, rather than the elimination, of behaviors from the species-typical repertoire ( Price 1984 ). A number of problems have been reported (including by Dawkins herself) concerning application of the consumer demand model (see Dawkins 1990 and commentaries; Houston 1997 ), although these problems are largely methodological in nature. A broader issue, however, relates to the underlying assumptions of the model and, indeed, of the whole concept of behavioral needs. 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