Rehabilitation of research chimpanzees: Stress and coping after long-term isolation

Abstract

We report on the permanent retirement of chimpanzees from biomedical research and on resocialization after long-term social isolation. Our aim was to investigate to what extent behavioral and endocrine measures of stress in deprived laboratory chimpanzees can be improved by a more species-typical social life style. Personality in terms of novelty responses, social dominance after resocialization and hormonal stress susceptibility were affected by the onset of maternal separation of infant chimpanzees and duration of deprivation. Chimpanzees, who were separated from their mothers at a younger age and kept in isolation for more years appeared to be more timid personalities, less socially active, less dominant and more susceptible to stress, as compared to chimpanzees with a less severe deprivation history. However, permanent retirement from biomedical research in combination with therapeutic resocialization maximizing chimpanzees' situation control resulted in reduced fecal cortisol metabolite levels. Our results indicate that chimpanzees can recover from severe social deprivation, and may experience resocialization as less stressful than solitary housing.

Introduction

This study reports on the rehabilitation of former biomedical research chimpanzees who were resocialized into one all-male group. Permanent retirement of research chimpanzees was recommended by the U.S. National Research Council in tribute to the profound psychological and social similarities between chimpanzees (Pan troglodytes) and humans (Gagneux et al., 2005, National Research Council, 1997). However, chimpanzees entering into retirement programs are often burdened with the consequences of inadequate rearing and housing conditions. Therefore, retirement of chimpanzees is to be combined with their rehabilitation including diagnosis and care of behavioral problems to enable them to lead more species-appropriate lives (Brent, 2001, Brüne et al., 2006).

Adverse early life experiences like maternal separation can seriously compromise the behavioral and psychological adjustment of primates and lead to stress-related behavioral deficiencies (Harlow et al., 1965, Rogers and Davenport, 1970). Infantile trauma and chronic stress such as long-term isolation may result in a lasting increase in sensitivity of the HPA axis (hypothalamo-pituitary–adrenocortical axis) as expressed by heightened levels of the stress hormones ACTH (adrenocorticotrophin) and glucocorticoids (i.e., cortisol; Anisman et al., 1998, Cavigelli and McClintock, 2003, Levine et al., 1957, Lyons et al., 2000, Matthews, 2002, Weiss et al., 2004). Stress responses are mediated by a primate's ability to control a stressor through prediction and active interference with onset, duration, or intensity of the stressor (Anisman et al., 1998, Levine and Mody, 2003, Weiss et al., 2004). Repeated exposure especially to unpredictable and inescapable stress can lead to learned helplessness in humans and nonhuman species, a state that is characterized by anxiety, inactivity and neophobia, as well as chronically increased cortisol values (Seligman, 1974, Weiss et al., 2004). On the other hand, repeated physical restraint in rhesus macaques has lead to physiological adaptation combined with a general decrease of the output of HPA hormones (Ruys et al., 2004), and adult humans with posttraumatic stress disorder show lower basal cortisol excretion compared to normal people (Yehuda et al., 2004).

The extent to which an individual can control stressors is influenced by personality factors such as boldness versus timidity, which in turn are influenced by learning and rearing history (Capitanio, 2004, Capitanio and Mason, 2000, Cavigelli and McClintock, 2003, Hall et al., 1997, Lyons et al., 2000, Weiss et al., 2004). Moreover, in gregarious species such as chimpanzees stress can be efficiently modulated by social support – affiliation and agonistic coalitions – and by dominance status (Aureli and Schino, 2004, Sapolsky, 2005). Personality has been identified in several primate and nonprimate species (Capitanio, 1999, Gosling and John, 1999, King and Figueredo, 1997, Lilienfeld et al., 1999, Stevenson-Hinde et al., 1980) and is operationalized through behavior which is related to four personality dimensions: sociability, confidence, excitability, and equability (Capitanio, 1999). One personality dimension indicates an individual's tendency to respond to strange situations with fear versus exploration (excitability). An objective method to assess this personality dimension is to confront subjects in a standard situation with a novel object or environmental challenge. An individual's reaction to those situations reflects the personality dimension “bold versus timid” (Boissy and Bouissou, 1995, Manteca and Deag, 1993).

The purpose of this study was to investigate how former laboratory chimpanzees cope with the stress of being relocated to a more species-appropriate environment and the challenges of resocialization and group living in one all-male group. We investigated personality in terms of boldness–timidity, social dominance after resocialization and how these traits were affected by the onset of maternal separation of infant chimpanzees and duration of deprivation. In addition to behavioral data, stress susceptibility was determined by measuring fecal glucocorticoid metabolites.