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The Development of Science-Based Guidelines for Laboratory Animal Care: Proceedings of the November 2003 International Workshop Dinner Speaker Kay E. Holekamp
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The Development of Science-Based Guidelines for Laboratory Animal Care: Proceedings of the November 2003 International Workshop A View from the Field: What the Lives of Wild Animals Can Teach Us About Care of Laboratory Animals Kay E. Holekamp My goal in this presentation is to review briefly a few seminal contributions from classical ethology and contemporary behavioral ecology that might help us develop better guidelines for use and care of laboratory animals. All of these contributions emphasize the importance of understanding the lives of animals in nature as we try to improve laboratory guidelines. I shall illustrate some of my points here with examples drawn from the lives of my own study animal, the spotted hyena (Crocuta crocuta), and other free-living mammals. In his charming treatise on animal behavior titled “A Stroll Through the Worlds of Animals and Men,” Jacob Von Uexkull (1934) observed that animals perceive only limited portions of their total environment. He asked the reader to consider a tick perched on a blade of grass, being bombarded at any given moment by thousands of wavelengths of both light and sound, hundreds of thousands of odorant molecules, myriad tactile stimuli, and information regarding gravity, humidity, and ambient temperature. Of all these countless stimuli hitting the tick, only a tiny few are important for its survival and reproduction, and it is only those few stimuli that the tick must sense and to which it must respond appropriately. All other stimuli are tuned out. Von Uexkull called the array of stimuli existing in the sensory-perceptual world of any animal its Umwelt. We now understand that the Umwelt of each species is unique, and it is important that we understand the Umwelt of each species in our care in the laboratory. This allows us to determine what is and is not salient to
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The Development of Science-Based Guidelines for Laboratory Animal Care: Proceedings of the November 2003 International Workshop the animal, which in turn allows us to make regulatory decisions that are truly in the best interests of our animal charges. A second important contribution from classical ethology is the ethogram. An ethogram is a complete descriptive inventory of an animal’s normal behavior, and as Niko Tinbergen (1951) pointed out, development of an ethogram is a critical first step in attempting to understand the behavior patterns of any species. All behaviors in the ethogram should ideally be described strictly in terms of the animal’s motor patterns and the contexts in which they occur, with minimal interpretation by the observer. Familiarity with an animal’s complete behavioral repertoire can be very useful to those of us working in the laboratory, because this information allows us to identify pathological behavior, distress, and contentment in our animal charges. New behaviors that arise, or normal behaviors that vanish from the ethogram, usually signal that something is wrong with the living conditions we have made available to the animal. The third contribution I shall briefly describe from classical ethology is a systematic comparison of the behavior of wild and captive savannah baboons performed by Thelma Rowell (1967). After intensive observations of wild baboons in Africa, she examined the behavior of a troop of conspecific baboons maintained in captivity. Although her captive troop was housed in a large seminatural enclosure, and although the inventory of behaviors emitted by Rowell’s baboons was the same in captivity and the wild, the rates at which certain behaviors occurred differed dramatically. Specifically, she found that rates of all social interactions were four times higher in captivity than in the wild, and that rates of aggression were eight times higher in captivity. These escalated rates of behavior presumably occurred because the captive animals had fewer opportunities to resolve their conflicts by moving away from each other. It is highly useful for us to understand conditions of life in nature for any species, and how these differ from conditions in the laboratory, because this understanding allows us to modify the captive environment in the best interests of the captive animals. Assuming we seek to maximize the external validity of the work we perform with captive animals, the more natural the animal’s behavior and physiology, the better our science. In recent decades, myriad studies in behavioral ecology have taught us that animals in nature confront multiple selection pressures every single day of their lives. To survive in the wild, animals must cope effectively with bad weather, hunger, thirst, intra- and interspecific competitors, predators, parasites, and pathogens. Furthermore, these selection pressures often act on animals in opposing directions, such that animals are forced to make trade-offs (e.g., Stearns 1992). For example, avoiding predation may be easier if one’s body size is larger, whereas ingesting enough calories to remain well fed may be easier if body size is smaller.
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The Development of Science-Based Guidelines for Laboratory Animal Care: Proceedings of the November 2003 International Workshop Thus, over the course of evolutionary time, the animal may become a bit larger than optimal for feeding itself, but a bit smaller than optimal for purposes of evading predators. To accommodate opposing selection pressures, wild animals also routinely make shorter-term trade-offs. For instance, even though a rodent may be extremely hungry as it sets off to forage from its home burrow, the animal will nevertheless forego feeding altogether for a while longer if it detects a predator lurking outside the burrow entrance. When we bring animals into the laboratory, we expose them to a suite of artificial selection pressures that are quite different from the selection pressures they would encounter in nature. As their caretakers, we must make the same sorts of trade-off decisions for them that the animals would make on their own to accommodate opposing selection pressures in nature. Although we cannot ask animals directly about their preferences, these can often be inferred from the animals’ behavior or physiology. For example, in our free-living spotted hyena subjects in Kenya, we have gathered preliminary behavioral data indicating that although the hyenas are not terribly bothered by the intramuscular injection involved in being hit by a dart during routine immobilizations, they find the experience of anesthesia itself to be utterly terrifying. In addition, plasma glucocorticoid levels of hyenas that took only a few minutes longer than average to become unconscious were several times as high as in hyenas for which time to unconsciousness was in the normal range (8-13 minutes). Thus both the physiology and the behavior of the hyenas suggest that they find the experience of being out of control of their own bodies extremely stressful. Robert Sapolsky has observed the same phenomena in his free-living baboons in Kenya (Sapolosky 1982). Noninvasive methods are of course always preferable to invasive procedures; but where a choice must be made between use of anesthesia and causing our animals momentary pain or discomfort in our research, we must be careful to ensure that the trade-off decisions we make on behalf of our laboratory animals are truly based on the best interests of those animals. If common laboratory animals respond to being anesthetized in the same way as do our hyenas or Sapolsky’s baboons, then momentary pain or stress might often be vastly preferable, from the animal’s point of view, to being anesthetized for minor procedures. Finally, contemporary behavioral ecology has taught us that variation in nature is enormous and that free-living animals therefore inevitably confront a range of conditions rather than just one “average” condition. Everyone who works with laboratory animals recognizes that it would be inappropriate to apply identical husbandry practices to groups of zebra, zebra finch, and zebra fish. Yet, in addition to obvious interspecific differ-
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The Development of Science-Based Guidelines for Laboratory Animal Care: Proceedings of the November 2003 International Workshop ences, a great deal of variation often exists among free-living members of a single species. In the wild, conspecifics vary among populations occurring in different habitat types. For example, mice in the genus Peromyscus breed throughout the North American continent, across a huge latitudinal gradient ranging from 15° N to 60° N (Bronson 1989). It would therefore be very difficult to select one set of environmental conditions to which Peromyscus are exposed in their breeding range and declare that set to be the “typical” set of conditions encountered in nature by this species. Similarly, spotted hyenas occur in virtually all habitat types in sub-Saharan Africa, including the arid sands of the Kalahari Desert, the watery world of the Okavango Delta, the dense forests of central and western Africa, and the prey-rich short-grass plains of the Serengeti ecosystem. How then would one describe the environmental conditions confronted in nature by the “average” spotted hyena? Long-term field work on East African (Kruuk 1972) and Kalahari (Mills 1990) hyenas has shown that body size, diet, home range size, social group size, and circadian activity all differ significantly between these two habitats. Interestingly, however, two things remain constant between habitats: the basic structure of hyena society and the behaviors occurring in the species’ ethogram developed at each site. Conspecific animals vary not only among habitat types but also among populations occupying a single habitat. For example, reproduction and behavior vary quite dramatically between spotted hyena populations separated by only 60 kilometers within the Serengeti ecosystem in eastern Africa. Long-term study of hyenas in the southern part of this ecosystem by Hofer and East (1993a,b,c; 1995) has shown that prey numbers available to the resident hyenas in this area vary enormously with season of the year. During times of the year when prey are scarce, the resident hyenas must commute long distances to feed. They therefore have huge home ranges that encompass their commuting routes, and their attendance at dens to care for their cubs is sporadic. By contrast, in the northern portion of this same ecosystem, Dr. Smale, our colleagues, and I have found that prey are available year-round to resident hyenas, hyenas feed within relatively small home ranges rather than commute, and they attend their cubs at dens daily (Boydston and others 2003; Cooper and others 1999; Holekamp and others 1997b). Finally, even within a single population, variation in the conditions animals confront may be surprisingly large. Variation among individuals within a single wild population often has a number of different sources including age, sex, social rank, dispersal status, and reproductive condition (e.g., Boydston and others 2001; Holekamp and Smale 1998; Szykman and others 2001). For example, variables that vary dramatically with social rank among free-living spotted hyenas include age at first reproduction,
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The Development of Science-Based Guidelines for Laboratory Animal Care: Proceedings of the November 2003 International Workshop reproductive success, family size, home range size, patterns of association with conspecifics, and even parasite load (Boydston and others 2003; Engh and others 2003; Holekamp and others 1996, 1997a). Most scientists work on animals in the laboratory rather than in the wild precisely to minimize the kind of variation I have described herein. Then why worry about it? My response is that naturally occurring variation is important to those regulating laboratory animal care because this variation suggests that even for a single species there is often likely to be an entire range of conditions under which the species will thrive in the laboratory. In summary, classical ethology and modern behavioral ecology have taught us that every animal comes into the laboratory with an evolutionary past and a set of traits shaped by natural selection. These include an Umwelt, a normal repertoire of behaviors, and an ability to survive and reproduce under a range of conditions. These traits should factor into our decision making about laboratory animal care guidelines. Given the diversity of conditions under which most species exist in nature, it seems reasonable to expect that a heterogeneous array of husbandry conditions can be utilized in the laboratory without compromising our ability to maintain a homogeneous set of ethical standards for the treatment of these animals. REFERENCES Boydston, E.E., Morelli, T.L., Holekamp, K.E. 2001. Sex differences in territorial behavior exhibited by the spotted hyena (Crocuta crocuta). Ethology 107:369-385. Boydston, E.E., Kapheim, K.M., Szykman, M., Holekamp, K.E. 2003. Individual variation in space utilization by female spotted hyenas (Crocuta crocuta). J Mamm 84:1006-1018. Bronson, F.H. 1989. Mammalian Reproductive Biology. Chicago: University of Chicago Press. Cooper, S.M., Holekamp, K.E., Smale, L. 1999. A seasonal feast: Long-term analysis of feeding behavior in the spotted hyaena Crocuta crocuta (Erxleben). Afr J Ecol 37:149-160. Engh, A.L., Nelson, K.G., Peebles, C.R., Hernandez, A.D., Hubbard, K.K., Holekamp. K.E. 2003. A coprological survey of the parasites of spotted hyaenas (Crocuta crocuta) in the Masai Mara National Reserve, Kenya. J Wildl Dis 39:224-227. Hofer, H., and East, M.L. 1993a. The commuting system of Serengeti spotted hyaenas: How a predator copes with migratory prey. I. Social organization. Anim Behav 46:547-557. Hofer, H., and East, M.L. 1993b. The commuting system of Serengeti spotted hyaenas: How a predator copes with migratory prey. II. intrusion pressure and intruders’ space use. Anim Behav 46:559-574. Hofer, H., and East, M.L. 1993c. The commuting system of Serengeti spotted hyaenas: How a predator copes with migratory prey. III. Attendance and maternal care. Anim Behav 46:575-589. Hofer, H., and East, M.L. 1995. Population dynamics, population size, and the commuting system of Serengeti spotted hyaenas. In: A.R.E. Sinclair and P. Arcese, eds. Serengeti II: Dynamics, Management, and Conservation of an Ecosystem. Chicago: University of Chicago Press. p. 332-363.
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The Development of Science-Based Guidelines for Laboratory Animal Care: Proceedings of the November 2003 International Workshop Holekamp, K.E., and L. Smale. 1998. Dispersal status influences hormones and behavior in the male spotted hyena. Hormones Behav 33:205-216. Holekamp, K.E., Smale, L., Szykman, M. 1996. Rank and reproduction in the female spotted hyaena. J Reprod Fertil 108:229-237. Holekamp, K.E., Cooper, S.M., Katona, C.I., Berry, N.A., Frank, L.G., Smale, L. 1997a. Patterns of association among female spotted hyenas (Crocuta crocuta). J Mamm 78:55-64. Holekamp, K.E., Smale, L., Berg, R., Cooper, S.M. 1997b. Hunting rates and hunting success in the spotted hyaena. J Zool Lond 242:1-15. Holekamp, K.E., Szykman, M., Boydston, E.E., Smale, L. 1999. Association of seasonal reproductive patterns with changing food availability in an equatorial carnivore. J Reprod Fertil 116:87-93. Kruuk, H. 1972. The Spotted Hyena. Chicago: University of Chicago Press. Mills, M.G.L. 1990. Kalahari Hyaenas. London: Unwin-Hyman Ltd. Rowell, T.E. 1967. A quantitative comparison of the behaviour of a wild and caged baboon group. Anim Behav 15:499-509. Sapolosky, R.M. 1982. The endocrine stress response and social status in the wild baboon. Hormones Behav 16:279-292. Stearns, S. 1992. The Evolution of Life Histories. Oxford, UK: Oxford University Press. Szykman, M., Engh, A.L., Van Horn, R.C., Funk, S., Scribner, K.T., Holekamp, K.E. 2001. Association patterns between male and female spotted hyenas reflect male mate choice. Behav Ecol Sociobiol 50:231-238. Tinbergen, N. 1951. The Study of Instinct. Oxford, UK: Oxford University Press. Uexkull, J. Von. 1934. A stroll through the worlds of animals and men. In: C.H. Schiller, ed. Instinctive Behavior. New York: International Universities Press. p. 5-80.
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