Introduction

The debate over the use of animals in research and exhibition involves issues of morality and ethics, as well as questions of scientific merit and appropriate husbandry. In recent years, public concern about the use of animals has been conveyed with increasing frequency to members of Congress. In 1985, Congress responded to the concern by amending the Animal Welfare Act of 1966 and 1978 to include a provision that was to have a substantial impact on all those who use primates, whether for research, for exhibition, or for other purposes. The new provision promulgated by the U.S. Department of Agriculture (USDA) as regulations in 1991 states that ''dealers, exhibitors, and research facilities must develop, document, and follow an appropriate plan for environmental enhancement adequate to promote the psychological well-being of nonhuman primates." Consequently, it is incumbent on all those who care for, use, or regulate the use of primates to grapple with the problem of how to evaluate the "psychological well-being" of these animals. Because of the great variety of needs of the many nonhuman primate species and the lack of understanding of their mental states, the sponsors of this report asked the National Research Council (NRC) to recommend ways in which to assess and promote psychological well-being. In response, NRC asked a committee of experts to develop such recommendations, which constitute this report. The purpose of this volume is to help scientists, veterinarians, curators, inspectors, duly appointed committees, and others concerned with the psychological well-being of nonhuman primates to deal more effectively with this complex issue.

Because verbal instruments are not suitable to assess psychological well-being in animals, some people have advocated the use of engineering standards,



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--> Introduction The debate over the use of animals in research and exhibition involves issues of morality and ethics, as well as questions of scientific merit and appropriate husbandry. In recent years, public concern about the use of animals has been conveyed with increasing frequency to members of Congress. In 1985, Congress responded to the concern by amending the Animal Welfare Act of 1966 and 1978 to include a provision that was to have a substantial impact on all those who use primates, whether for research, for exhibition, or for other purposes. The new provision promulgated by the U.S. Department of Agriculture (USDA) as regulations in 1991 states that ''dealers, exhibitors, and research facilities must develop, document, and follow an appropriate plan for environmental enhancement adequate to promote the psychological well-being of nonhuman primates." Consequently, it is incumbent on all those who care for, use, or regulate the use of primates to grapple with the problem of how to evaluate the "psychological well-being" of these animals. Because of the great variety of needs of the many nonhuman primate species and the lack of understanding of their mental states, the sponsors of this report asked the National Research Council (NRC) to recommend ways in which to assess and promote psychological well-being. In response, NRC asked a committee of experts to develop such recommendations, which constitute this report. The purpose of this volume is to help scientists, veterinarians, curators, inspectors, duly appointed committees, and others concerned with the psychological well-being of nonhuman primates to deal more effectively with this complex issue. Because verbal instruments are not suitable to assess psychological well-being in animals, some people have advocated the use of engineering standards,

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--> which focus on easily measured aspects of the physical environment. Others have argued that the performance of the animals should be used to assess psychological well-being. There has been considerable debate over the use of engineering versus performance standards (Novak and Drewson 1989; Sackett 1991). The USDA, the agency with primary authority for enforcing the Animal Welfare Act, initially preferred engineering standards, which had been the cornerstone of all previous regulations. In the absence of performance measures to validate the efficacy of physical manipulations, however, it proved very difficult to identify the environmental features that promoted psychological well-being. For example, USDA initially proposed to alter cage sizes, assuming that larger cages would promote psychological well-being. However, results of studies of the effects of cage expansion did not indicate that the change reduced abnormal behavior (Bayne and McCully 1989; Line and others 1990c); tension and aggression actually increased in some cases in which group-housed monkeys were given more floor space (Erwin 1979; Novak and Drewsen 1989). USDA also suggested that captive primates be given access to enrichment devices. However, it is often not clear what specific benefits enrichment devices provide or which devices actually provide enrichment, inasmuch as there are enormous individual and species differences in responses to such devices. As a consequence of the inadequacy of an engineering approach to psychological well-being, the committee believes that the focus should be on the primates themselves and on their reactions to various features of life in captivity. This emphasis on performance standards presupposes that explicit criteria are available for the evaluation of psychological well-being. Although psychological well-being implies a subjective mental state or private experience, the practical need for observable criteria as a basis for assessment is imperative. As a first step toward developing such criteria, assessments of psychological well-being should look for signs of chronic distress as manifested in maladaptive or pathological behavior. The essential next step is to decide on the signs of distress and on what constitutes maladaptive or pathological behavior (see also discussions of causes and signs of distress in NRC 1992). Meaningful judgments will involve some subjective component based on the observer's perceptions, experiences, and values, as well as reflect knowledge about the animal whose psychological state is being evaluated—ideally, knowledge based on experience with the species. Human perceptions and values, unless tempered by an understanding of the other species, can be a poor basis for judgments about psychological well-being. Many animals not only live their everyday lives under conditions that humans would find unendurable, but prosper in these circumstances. The natural lives of rats, lions, alligators, and giraffes differ from each other and from ours in myriad ways. So do the requirements of those species when they are maintained in captivity. Clearly, the criteria used to assess the psychological well-being of any species should be based on the best available information about that species.

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--> That is also the case when the animals are primates. The need for information about particular species might be less widely recognized, however, when the animals are monkeys or apes. Resemblance of those animals to humans in appearance and behavior encourages the assumption that they have identical needs and abilities. But that cannot be accepted uncritically. Nonhuman primates are a highly diverse group. They not only differ from humans in many respects, but also differ widely from each other. Their normal behavior, needs, and abilities differ from one taxonomic group to another. Their diversity is easier to accept when one considers that there are more than 200 species of primates. In addition to humans, primates include apes, New World and Old World monkeys, and an assortment of other forms collectively referred to as prosimians, such as tarsiers, lemurs, aye ayes, and bushbabies. Nonhuman primates range in size from the diminutive mouse lemur, weighing only a few grams, to the gigantic mountain gorilla, weighing more than 180 kg. Species also differ in habitat, diet, activity patterns, use of space, reproductive physiology, growth rates, social relationships, and cognitive abilities. Few of the species are used extensively in research. Although more are maintained in zoos, some are rarely or never found in captivity. Information is lacking on the natural history, biology, and behavior of many species (Fleagle 1988; Smuts and others 1987). All primates are placed taxonomically in a single group called an order. The order Primates is subdivided into the traditional taxonomic categories, such as suborders, infraorders, superfamilies, families, subfamilies, genera, and species. The informal scheme that follows is consistent with the accepted system of classifying primate species (for example, see Fleagle 1988; Napier and Napier 1967, 1985) and will be adequate for our purposes. The prosimians include tarsiers, lemurs, sifakas, indris, aye ayes, lorises, pottos, and bushbabies or galagos (Fleagle 1988). Tree shrews, once considered in this group, have now been removed from the Primate order on the basis of structural considerations, most notably in the ear, and by early fossil differentiation. Most prosimians have pointed muzzles, a naked rhinarium (a moist patch of bare skin around the nose), and claws instead of nails on some fingers and toes. Many species of prosimians are nocturnal. Few institutions maintain them in captivity, but some lemurs, especially the ring-tailed lemur L. catta, and some species of Galago are found in exhibits. The anthropoids include all other species in the Primate order. These animals conform to the popular view of what a monkey or ape should look like. A popular distinction between monkeys and apes is that monkeys have tails. It is true that apes are tailless, but some monkeys are also virtually tailless. A more basic distinction within the anthropoids is between New World and Old World forms. New World anthropoids are distinguished from Old World anthropoids by having three rather than two premolars (bicuspids) and by having a broader septum between the nostrils.

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--> New World primates are found in Central and South America. They are known collectively as Platyrrhines and include marmosets, tamarins, howler monkeys, spider monkeys, capuchin monkeys, woolly monkeys, squirrel monkeys, night monkeys, titi monkeys, sakis, and uacaris. Some species of marmosets (genus Callithrix), tamarins (genus Saguinus) and squirrel monkeys (genus Saimiri) are often used in laboratory research (Bennett and others 1995; UFAW 1987) capuchins (genus Cebus ) and night (or owl) monkeys (genus Aotus) are used less often. Other species of New World monkeys are used little or not at all for research but can be found in zoos. Old World primates in their natural habitat are found mainly in Africa and Asia, although some species exist as introduced populations throughout the world. Old World primates include humans, apes (chimpanzees, gorillas, orangutans, and gibbons), and many monkey species. Because of their close phylogenetic relationship to humans, chimpanzees (genus Pan) are the subjects of choice for some kinds of biomedical research and for investigations of cognitive abilities, including the acquisition of language (NRC 1997b; Savage-Rumbaugh and others 1998). The monkeys most often encountered in laboratories are the macaques (genus Macaca ), especially rhesus monkeys (M. mulatta). Pigtail monkeys (M. nemestrina ), crab-eating monkeys (M. fascicularis), baboons (genus Papio), and vervets or green monkeys (Cercopithecus aethiops) are also relatively common in laboratory research, whereas other forms—such as mangabeys, talapoins, guenons, and patas—are seldom used and are generally found only in exhibits. The leaf-eating monkeys (Colobus, Presbytis, and related genera) are also less commonly seen, even in exhibits. There is no one correct taxonomic list of primates, and no comprehensive list is attempted in this report. Each of the taxonomic chapters (Chapter 5–9) includes an introduction to the major groupings in its taxon and the common and scientific names of species most likely to be found in captivity. In addition, lists of the generally accepted scientific names and typical common names that are used in referring to the primates mentioned in this report are provided in the front of Chapters 5–9. In spite of the many important variations among primate species, these animals share several features that, in combination, set them apart from most other biological groups. The primates are characterized by developmental periods that are long for mammals of their size (especially the periods of gestation and infant dependence), exceptional ability to modify behavior (intelligence, learning capacity, and behavioral flexibility), and prominent and consistent sociality associated with highly differentiated social relationships. Both the qualities common to all primates and the attributes peculiar to particular species must be considered in establishing standards for promoting and assessing psychological well-being. That requirement is reflected in the organization of this volume. The first four chapters deal with general issues. Chapter 1 is concerned with principles and criteria of psychological well-being that apply to

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--> all primates—and indeed to many nonprimates. Chapter 2 deals with the essential elements of an effective institutional program designed to ensure well-being. Chapter 3 reviews basic institutional procedures and routines from the standpoint of their impact on psychological well-being. Chapter 4 considers the challenges to well-being created by special conditions and procedures that might be required by research protocols. Each of the next five chapters deals with the particular attributes and requirements of a specific biological group in the Primate order. The recommendations presented in this volume are based on the collective experience of the committee and the information available to it. It should be emphasized, however, that many gaps exist in our knowledge of psychological well-being in nonhuman primates. The problems are multifaceted and cannot be wholly divorced from broader concerns regarding conservation, primatology, the effective and judicious use of primates in research, and other uniquely human enterprises. Even apart from those complex issues, research directly focused on psychological well-being is in its infancy. Chapter 10 suggests some of the pressing research needs. It is hoped that the contents of this volume will be reviewed within the next 5 years and that new information on psychological well-being will yield revisions and updates.