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National Research Council (US) Institute for Laboratory Animal Research. The Development of Science-based Guidelines for Laboratory Animal Care: Proceedings of the November 2003 International Workshop. Washington (DC): National Academies Press (US); 2004.

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The Development of Science-based Guidelines for Laboratory Animal Care: Proceedings of the November 2003 International Workshop.

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Housing for Captive Nonhuman Primates: The Balancing Act

Melinda Novak*

Nonhuman primates are a crucial research resource because they serve as important models for understanding human health and well-being. However, their success as models depends on balancing two important needs: the research objectives and the well-being of the animals. The balance is not always easy to achieve because we do not fully understand how to maintain primate well-being in a laboratory setting. This discussion reviews information relevant to the housing of rhesus macaques, one of the most commonly used species for laboratory research.

SPECIES-TYPICAL BEHAVIOR

The key to developing effective strategies for housing rhesus monkeys in captivity is to understand their behavior in nature. From a social perspective, rhesus monkeys live in relatively large troops (~ 20-30 individuals on average) that consist of both sexes and all age classes (Lindburg 1971). These troops operate as “closed societies” and repel strangers with acts of aggression (Southwick and others 1965, 1974). Females spend their lives in their natal troop preferentially interacting with their female kin, whereas males usually leave their natal troop during adolescence. Emigrating males spend a period of time either alone or in the company of other adolescent males before attempting to gain entry to a new troop. It has been estimated that at least one-third of the males do not survive this change (Berard 1989; Dittus 1979).

Social interactions within the troop are based in part on dominance, wherein some animals have priority of access to incentives. Two features of the dominance hierarchy are redirection of aggression and recruitment of agonistic aid. Threats and aggression can cascade down the hierarchy, with low-ranking animals receiving more “bystander” aggression than higher-ranking animals. Animals threatened or attacked by others frequently attempt to “recruit” others to their defense by screaming at the attacker or by rapidly alternating their gaze between friends and foe (Gouzoules and others 1998).

From an ecological perspective, rhesus monkeys live in a wide variety of different habitats. They have been observed in remote forests, agricultural regions, and many urban areas (Teas and others 1980). Unlike some other primate species, rhesus monkeys appear to thrive in areas of deforestation, and they have been termed “weed” macaques because of this versatility (Richard and others 1989). Rhesus monkeys spend nearly 50% of their time moving to food sites and foraging for food (Goldstein and Richard 1989; Teas and others 1980). They subsist on the fruits and shoots of well over 100 species of plants, and they occasionally supplement their food with eggs, insects, and small animals. This widely varied diet may contribute to their ability to flourish in very different environments.

In addition to these general features, individual monkeys differ with respect to reactive and impulsive temperaments (Suomi 2000). Approximately 20% of the rhesus monkey population appears to be quite reactive to novel events. This reactivity is manifested by heightened and prolonged activation of the hypothalamic-pituitary-adrenal (HPA) axis and by behavioral responses including fear and withdrawal. In contrast, the remaining members of the population show only mild activation of the HPA axis and only brief responses of wariness or caution in response to novel stimuli (Suomi 1991). In nature, a high reactive temperament is associated with heightened emotional responses to maternal disruption (Berman and others 1994), and in males, with later emigration from the natal troop (Suomi and others 1992).

Individual rhesus monkeys also vary with respect to impulsivity. Some male monkeys (~5%) are highly aggressive and do not appear to moderate their aggressiveness with appeasement behavior. This trait is also associated with the presence of low levels of serotonin in the brain as measured by the metabolite 5-hydroxyindoleacetic acid (5-HIAA). In nature, low levels of CSF 5-HIAA in male rhesus monkeys are associated with extreme aggression, earlier emigration from their natal troop compared with other adolescent males (Mehlman and others 1995), and greatly increased risk of mortality (Higley and others 1996).

Knowledge of how monkeys behave in nature can inform how we house and enrich the environments of captive primates. From a social housing perspective, free-ranging monkeys live in complex social groups. Although it is not really possible to duplicate troop life in the laboratory, some form of social housing may be crucial for maintaining well-being. However, there are distinctions that must be considered along with potential costs and benefits. For example, males and females may be affected differently by the presence or absence of partners. Females live in large kin groups throughout their lives, whereas males emigrate and occasionally become solitary. Furthermore, some groupings or pairings will not necessarily be amicable. In nature, rhesus monkey troops are “closed societies,” and troop members react aggressively to strangers. Furthermore, social housing may not be optimal or even desirable for certain individuals. In nature, male monkeys with low central nervous system serotonin levels show extreme aggression and are ultimately forced out of their natal troop.

In addition to their complex social environment, rhesus monkeys exist in habitats where they must forage for food and find suitable resting/ sleeping sites. Movement and exploration are therefore crucial for survival. Exposure to novel stimuli or foraging devices (i.e., environmental enrichment) would appear to be essential for housing monkeys in captivity; however, this view must be adjusted to account for differences in temperament. Reactive monkeys may show heightened stress responses to enrichment.

LABORATORY FINDINGS

Both social housing and environmental enrichment are considered important regulatory requirements for promoting psychological well-being in captive primates. The logic of this view for rhesus monkeys is derived in part from their life history. However, there are also laboratory studies in which the effectiveness of social housing and environmental enrichment have been examined, and the emerging picture from this work suggests that there are both benefits and costs, depending on the research objectives.

Social Housing

Scientific evidence suggests that there are a number of potential benefits to social housing, the most obvious of which is the ability to groom and affiliate with other monkeys. Companions may also serve as a buffer to stressful events (Winslow and others 2003). Other potential benefits of companionship include increased disease resistance (Shively and others 1989) and improved immune response (Lilly and others 1999; Schapiro and others 2000). However, these relationships are more complex than these descriptions imply. For example, in Shively and colleagues' (1989) study, socially housed female macaques showed less coronary artery disease than singly housed monkeys, but this difference was evident only for dominant socially housed females. Another important benefit of social housing is that there is greater correspondence to the human situation. In a recent study, intracerebroventricular infusions of corticotropin-releasing factor caused depressive-like symptoms, but only in socially housed monkeys (Strome and others 2002).

Social housing is not without cost, and one of the most significant costs is the development of aggression and competition. Rhesus monkeys do not always coexist amicably. Even in stable social groups, aggression can escalate and lead to violent outcomes (Hird and others 1975). From a research perspective, there may be circumstances in which social housing increases experimental variability. For example, moving monkeys from individual cage housing to social housing led to an increase in the availability of dopamine D2 receptors in dominant, but not subordinate, monkeys (Morgan and others 2002). Social housing may also minimize the effects of certain manipulations (e.g., coronary artery disease) or introduce other variables that may mask the effects of manipulations. For example, removal from companions for testing may induce stress reactions as a consequence of separation (see Lyons and others 1998 for squirrel monkeys).

Environmental Enrichment

There are many different methods to enrich the environment of captive primates, ranging from the provision of objects, foraging devices, or videotapes to the redesign of the cage environment (see various commercial cage vendors). As with social housing, the emerging picture suggests that there are both costs and benefits. The most obvious benefit is that environmental enrichment promotes species-typical behavior in the form of exploration. Thus, most monkeys spend some time using foraging devices (Lutz and Novak 1995) and manipulating objects (Novak and others 1993). Some monkeys also appear to watch videotapes (Platt and Novak 1997). The benefits of enrichment may extend beyond mere exploration to include a reduction in stress levels (Boinski and others 1999; Byrne and Suomi 1991) and a decrease in stereotypic behavior (Bayne and others 1991). However, enrichment has not been shown to reduce severe forms of abnormal behavior, such as self-injurious behavior (Novak and others 1998).

Enrichment efforts also incur costs to the animal and to the research enterprise. Rotation of enrichment devices through the colony can increase the risk of disease transmission (Bayne and others 1993). The provision of foraging devices can lead to increased body weight (Brent 1995). Plastic and rubber objects are typically gnawed and chewed, and in some cases can result in injury from foreign material in the intestine (Hahn and others 2000).

Developing optimal housing strategies for rhesus monkeys requires balancing two different but interconnected needs: promoting primate well-being and achieving research objectives. A strong case can be made that both social housing and environmental enrichment foster well-being. However, there are also risks to housing monkeys in social groups and to enriching the environment. Furthermore, the costs and benefits are often relative. What may be a benefit under some conditions can become a cost under other conditions. A thorough review of life history patterns and a careful cost-benefit analysis may provide guidance in designing housing strategies for particular research programs.

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Footnotes

*

This report was presented at the workshop by Dr. Kathryn Bayne, with thanks.

Copyright © 2004, National Academy of Sciences.
Bookshelf ID: NBK25428

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