Principles of Psychological Well-Being of Nonhuman Primates
The use of the term psychological well-being in the development of legally mandated regulations has created concern and continuing controversy. Some have tried to equate psychological well-being with engineering standards that specify physical dimensions, such as square meters of floor space or types of cage furnishings. Others have argued that psychological well-being is a function of individual preferences and therefore cannot be defined broadly. Still others have suggested replacing well-being with such terms as environmental enrichment. Those views are problematic and in some cases inaccurate. Indeed, attempts to relate psychological well-being strictly to physical features, such as cage size, have been largely unsuccessful and unproductive (Crockett and others 1993a). In contrast, the view that psychological well-being is so variable among animals that it cannot be defined might be unnecessarily pessimistic.
Replacement terms, such as environmental enrichment, are also problematic because they refer to different processes. Environmental enrichment , although sometimes used interchangeably with psychological well-being , is an independent variable that refers to manipulations to improve the environments of captive primates to enhance psychological well-being. Enrichment is used in the sense of providing for species-appropriate activities in an otherwise restrictive and limited environment. In contrast, psychological well-being is an abstraction that is inferred by measuring behavioral and physiological variables in the affected primates to determine whether a manipulation had the desired effect.
The assessment of psychological well-being is based on the responses of animals to their environment. Multiple measures will be required in this assessment (Novak and Suomi 1988, 1991; Snowdon and Savage 1989). An emerging
consensus suggests that in addition to physical health the following criteria are important in assessing psychological well-being:
- The animal's ability to cope effectively with day-to-day changes in its social and physical environment (with reference to meeting its own needs).
- The animal's ability to engage in beneficial species-typical activities.
- The absence of maladaptive or pathological behavior that results in self-injury or other undesirable consequences (see Bayne 1996 for a discussion of the normal and abnormal behaviors).
- The presence of a balanced temperament (appropriate balance of aggression and passivity) and absence of chronic signs of distress as indexed by the presence of affiliative verses distress vocalizations, facial expressions, postures, and physiological responses (e.g., labored breathing, excessive cardiac response, and abnormal hormonal concentrations).
None of those criteria can stand alone as the defining measure of psychological well-being in captive primates. However, when used together, they might provide a detailed picture of a primate's psychological health.
In assessing general well-being, physical health is probably the easiest to assess on the basis of established veterinary procedures for captive nonhuman primates (Bennett and others 1995; Keeling and Wolf 1975). Routine health examinations given at specified intervals are usually supplemented with daily inspections of an animal to monitor for such variables as hair condition, alertness, gait, appetite, body weight, and injury. The inspections can be used to identify potential problems in both psychological and physical well-being. Good physical health, however, is not synonymous with good psychological health. Psychologically disturbed animals might appear to be in good physical condition, and evidence of poor physical condition does not preclude psychological well-being. For example, elderly monkeys can show signs of clinical disease, such as arthritis, but maintain social ties, breed successfully, and appear alert and responsive to environmental stimuli.
Two general principles are important in assessing behavioral indicators of psychological well-being. First, there should be behavioral diversity; animals should exhibit a broad range of species-typical patterns of behavior. That does not mean that every species-typical behavior described for a given species in nature need be exhibited by captive members of that species; this is neither possible in all cases (e.g., providing space equivalent to an animal's daily movements in nature) nor necessarily desirable (e.g., recreating intertroop conflicts, predator attacks, weather extremes, droughts, and environmental hardships). But captive primates should be provided with suitable opportunities to express a variety of species-typical behavior.
The second principle is that some kinds of species-typical behavior might be better indicators of psychological well-being than others. For example, repro-
ductive success (including reproductive behavior, fertility, prenatal adequacy, birth, and parental care) is often considered to be a good indicator of psychological well-being, but not all captive primates are of breeding age (they might be too young or too old), and some might be deliberately maintained in nonbreeding situations; furthermore, some types of reproductive failure (e.g., infertility) are not necessarily linked to poor psychological well-being. It could be argued that we should focus on searching for evidence of ill-being as represented by self-biting or bizarre, idiosyncratic activities, such as back-flips, eye-pokes, and hair-plucking. Although behavioral stereotypies might represent psychological disturbance brought about by environmental factors (Draper and Bernstein 1963), similar behavioral symptoms could result from atypical developmental processes and not be eliminated by manipulating housing. Nonhuman primates reared in deprived social environments during the first year of life often develop idiosyncratic behavior—such as rocking, self-clasping, and self-mouthing—as a replacement for maternal activities (Fritz 1986; Fritz and Howell, 1993a). Such patterns might persist for the life of the animal, and their appearance can reflect early rearing experience, rather than distress in the present environment (Mason and Berkson 1975). Some physical ailments can also be manifest in such symptoms as self-biting. Monkeys that develop reactive arthritis after shigella infections sometimes bite the affected limb, but in this case medical treatment will improve limb mobility and eliminate self-biting.
Thus it is extremely important to determine the etiology of atypical behavioral patterns before recommending any form of intervention. In some cases, medical treatment will be required; in others, environmental manipulations might be effective. Developmentally induced stereotypies are less amenable to treatment, but they can generally be avoided by rearing infant primates in a species-typical social environment. The severity of developmental abnormalities varies with the degree of early social deprivation. The most extensive data available come from rhesus monkeys (Macaca mulatta) and indicate that physical contact with social companions is essential for normal development (Mason 1991). If such contact is restricted to the mother alone or peers alone, some social deficits can persist for life (Mason 1991). Whereas limiting access to peers in a playroom situation seems to be less damaging than other forms of social restriction, the full range of species-typical behavior, including effective reproductive behavior, is more likely in animals given a sufficient amount of species-typical social experience. Only in a common enclosure can monkeys learn the consequences of their own actions on the behavior of social partners. It is that dimension of responsiveness that distinguishes social partners from inanimate objects.
When research protocols demand restrictions on early social experience, the institution should be prepared to deal with the long-term husbandry problems associated with such rearing practices. The atypical behavior exhibited by monkeys so restricted might reflect idiosyncratic devices to cope with early environmental deprivation, and in such cases direct intervention to disrupt the atypical
behavior could be harmful. In cases documented to result from early rearing conditions, the atypical behavior cannot be taken to mean that the animal is not being well cared for, given its early rearing experience.
Reducing stress is often considered the best way to promote the psychological well-being of captive primates, the assumption being that stress is the antithesis of well-being (Moberg 1985). However, stress occurs in many forms, both positive and negative, as noted by Selye (1974), who divided stressful stimuli into "eustress" and distress. It might be more useful to look for signs of distress in captive primates, such as chronic or excessive fear, grimacing, withdrawal, altered breathing, distress vocalizations, anorexia, or unusual postures (Morton and Griffiths 1985; NRC 1992).
The manner in which an animal adapts to environmental changes or brief environmental disruptions (e.g., cage-cleaning) can provide information about its psychological state (Mineka and Kihlstrom 1978; Mineka and others 1986). At issue are the appropriateness of the reaction, given the particular kind of disruption, and the time that it takes an animal to adjust to the temporary or new situation. One can examine adaptation in monkeys by evaluating their reactions to temporary but routine husbandry events, such as being removed from their home cage, or to more permanent events, such as a change in cage location.
The ability to adapt to change is a manifestation of a broader capability: to exhibit behavior appropriate to the environmental context. For example, it is expected that socially reared nonhuman primates will display a broad range of species-typical behavior and express the behavior patterns in relevant contexts. Such animals should interact in a socially competent, species-characteristic manner with cagemates (if present). They should not limit their movement through space to a small part of the environment or to a single repetitive pattern, such as pacing, but rather should display a variety of species-typical locomotor patterns.
Identification of species-typical patterns of behavior has depended heavily on studies of behavior in the natural environment. Some of the characteristics of wild populations that are thought to be relevant to captive primate well-being are the nature of social organization, mating system (e.g., monogamous), group size, group composition, spacing patterns, patterns of emigration and immigration, nature of habitat (e.g., open grassland or dense foliage), range of locomotor patterns (e.g., terrestrial or arboreal), food availability and dietary selection, sleeping places, nocturnality or diurnality, sedentary or mobile activity, feeding patterns, reproduction, age at sexual maturity, seasonality of breeding, parental care, communication, movement patterns, and normal postures of resting and sleeping. A plan for psychological well-being should take such characteristics into account. It should be noted, however, that there is a tremendous disparity in the amount of information available on the various species of primates held in captivity.
Even very closely related species (i.e., members of a genus) can differ substantially in behavior. For example, bonnet macaques (Macaca radiata) typically exhibit little intragroup aggression and show considerable group cohesion.
Female bonnet macaques display aunting behavior to the extent that infants develop close attachment bonds with adult females other than their own mothers; loss of a mother does not greatly alter the behavior and physiology of infant bonnets, because they are generally adopted by other females (Reite and others 1989). In contrast, pigtail macaques (M. nemestrina) typically exhibit greater intragroup aggression and less social cohesion than bonnet macaques (Kaufman and Rosenblum 1967). Mothers are highly protective of their infants, restricting their activity to the extent that the infants do not form social bonds with other unrelated adults in the social group; loss of a mother can result in profound behavioral and physiological changes in infants (Reite and others 1981) and can have adverse long-term behavioral consequences (Capitanio and Reite 1984) and immunological consequences (Laudenslager and others 1986, 1996).
Even within a species, substantial individual differences in behavior can influence our interpretation of psychological well-being. Nonhuman primates are known to exhibit marked individual differences in "personality" (Caine and others 1983; Stevenson-Hinde and Zunz 1978; Suomi and Novak 1991). Macaques, for example, display relatively stable differences in temperament that have behavioral and physiological analogues. Both genetic mechanisms (Boccia and others 1994) and experience (Capitanio and others 1986) are probably involved.
A sudden change in the appearance or behavior of an animal might indicate a problem. For example, a shift from normal to unusual behavior might indicate a deterioration of the animal's well-being and warrant attention. Conversely, alterations of behavior in response to environmental manipulations (e.g., enrichment attempts) can be used to validate an intervention if undesirable behavior (e.g., self-biting) declines and normal behavior increases.
In summary, we expect animals in a state of psychological well-being to engage in species-typical behavior if given the opportunity to do so, to be capable of coping with minor disruptions in routine, and to display a balanced affect (as opposed to behavior that is indicative of chronic distress) and a behavioral repertoire that does not include maladaptive or pathological behavior. The best ways to fulfill such expectations are discussed in the next three chapters: programs to promote psychological well-being, general considerations of animal care, and special conditions related to research requirements.