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La parakinésie brachiale oscitante
Yawning: its cycle, its role
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Fetal yawning assessed by 3D and 4D sonography
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Applied Animal Behaviour Science
2010;124:68&endash;74
Correlates of self-directed and stereotypic behaviours in captive red-capped mangabeys (Cercocebus torquatus torquatus)
 
Lisa Reamer,Zena Tooze, Claire Coulson, Stuart Semple
 
Centre for Research in Evolutionary Anthropology, Roehampton University, Holybourne
 

Chat-logomini

 
The quantification of behaviours linked to anxiety or stress provides a powerful means to address applied questions related to the well-being of captive animals. This study explored correlates of two such behaviours &endash; self-directed (SDB) and stereotypic behaviour (STB) &endash; among captive red-capped mangabeys, Cercocebus torquatus torquatus. Study animals were held at two sites run by CERCOPAN, a primate sanctuary in Nigeria. At the first site (Calabar), animals were housed in traditional cage enclosures, while at the second (Rhoko), they lived in a semi-free ranging environment. Analyses revealed that while animals at the two sites did not differ in time spent in SDB (self-scratching, self-grooming, yawning and body shaking), animals at Calabar showed a higher prevalence of, and spent more time in STB (pacing and head rolling). There were no significant differences in time spent in SDB or STB between the sexes, or between captive-born and wild-born animals. A positive correlation was found between age and time spent in SDB, but not between age and time spent in STB. Finally, positive relationships were found between time spent in SDB and both time spent grooming and time spent being groomed; no relationships were found between grooming behaviour and STB. As stress and anxiety can have detrimental effects on psychological well-being, physical health and reproduction, these findings have important implications for the captive welfare and conservation of red-capped mangabeys, and also potentially of other endangered vertebrate species.
 
 
 
1. Introduction The study of anxiety and stress among animals in captivity has important implications for welfare and management (Moberg and Mench, 2000). The non-human primates represent particularly important animals for studies of this kind (Honess and Marin, 2006a). This is due primarily to ethical concerns about the well-being and potential for suffering of such animals (Wolfensohn and Honess, 2005). In addition, and closely related to this issue, is the potential impact of poor welfare on the health and reproduction of animals in captive breeding programmes for endangered species (Cockrem, 2005; Swaisgood, 2007). Understanding the factors linked to anxiety and stress levels in captivity, and investigating how animals might mediate these levels in such environments represent, therefore, important goals. Quantification of self-directed and stereotypic behaviours provides a powerful, noninvasive tool to address these issues.
 
Behavioural and pharmacological evidence from a range of primate species indicates that self-directed behaviours (SDB &endash; self-scratching, self-grooming, yawning and body shaking) provide an index of anxiety (Maestripieri et al., 1992a). While some SDBs, most notably selfgrooming or scratching, may normally have hygienic functions (Maestripieri et al., 1992a; Ventura et al., 2005), SDB rates have been observed to increase markedly in situations likely to elicit anxiety, such as when in close proximity to a dominant animal (olive baboons, Papio anubis: Castles et al., 1999), or after aggression (chimpanzees, Pan troglodytes: Fraser et al., 2008). Manipulations designed to reduce anxiety have also been seen to lower SDB levels; for example, in captive red-capped mangabeys, Cercocebus torquatus torquatus, environmental enrichment in the form of seeds and litter was found to be associated with a decline in rates of SDB's (Blois-Heulin and Jubin, 2004). Maestripieri et al. (1992b) found that administration of an anxiogenic drug increased the rate of selfscratching among infant rhesus macaques, while administration of an anxiolytic reduced the rate of body shaking. Two other measures of SDB &endash; self-grooming and yawning &endash; were unaffected by either treatment. Schino et al. (1996) found that combined rates of three SDBs (self-scratching, self-grooming and body shaking) in captive long-tailed macaques, M. fascicularis, increased after administration of anxiogenic drugs, and decreased when anxiolytic drugs were given.
 
Stress has been implicated as a key risk factor in the development and maintenance of a range of primate stereotypic behaviours (STB) (Honess and Marin, 2006a; Novak et al., 2005a). Both early social deprivation and later social isolation/separation are closely linked to the occurrence of STB in rhesus macaques (review by Novak et al., 2005b). In the same species, it has been found that exposure to stimuli associated with stressful experiences such as capture (Cross and Harlow, 1965) or electric shock (Gluck et al., 1985) can trigger or increase the frequency of stereotypies. Furthermore, pharmacological evidence supports the role of anxiety in maintaining stereotypic behaviour patterns. Hugo et al. (2003) found a reduction over time in STB among a group of vervet monkeys, Cercopithecus aethiops, given fluoxetine (Prozac1), with no such reduction seen in a control group. Similarly, Prosen and Bell (2001) reported that selective serotonin reuptake inhibitor treatment significantly reduced STB in a male bonobo, Pan paniscus, displaying marked behavioural problems linked to abnormal rearing conditions.
 
A number of environmental parameters may affect the anxiety or stress experienced by captive primates. Key factors in this regard are the nature and size of the captive environment. Semi-free ranging environments are more naturalistic than caged enclosures and typically have a lower density of individuals; both factors may be expected to be associated with improved welfare. Where animals are kept in traditional cage enclosures, larger and more enriched cages have been linked to reduced levels of aggression (Honess and Marin, 2006b), a major factor impacting on psychological well-being.
 
As well as this extrinsic factor, a range of intrinsic parameters may also be related to the anxiety and stress experienced by individuals in captivity, perhaps the most important of which are sex, age and rearing history. Lutz et al. (2003), for example, found that stereotypic (including self-injurious) behaviours were more common among male than female captive rhesus monkeys; Mallapur et al. (2005), by contrast, found that female captive lion-tailed macaques, M. silenus, showed higher rates of self-grooming than did males. Fittinghoff et al. (1974) proposed that stereotypic behaviour may change with age in male rhesus macaques, with the repertoire of such behaviours decreasing as individuals get older. Finally, Mallapur et al. (2005) provided evidence that rearing history can also affect the expression of abnormal behaviours in captive lion-tailed macaques; no STBs were seen in any wild-born animals, whereas captive-born animals did exhibit such repetitive behaviour.
 
Animals experiencing anxiety or stress in the captive environment may attempt to mediate these states behaviourally. In particular, it has been suggested that grooming may have an important tension-reduction function (Terry, 1970). In support of this hypothesis, Schino et al. (1988) found evidence in long-tailed macaques that the receipt of allogrooming from females reduced males' self-directed behaviour. In addition, an association between the receipt of grooming and lowered heart rates has been documented in rhesus macaques (Aureli et al., 1999) and pig-tailed macaques, M. nemestrina (Boccia et al., 1989). More recently, Shutt et al. (2007) provided evidence that the giving of grooming may also provide stress-reducing benefits: in this study of female Barbary macaques, M. sylvanus, the amount of grooming given was negatively associated with long term stress levels, as assessed from faecal concentrations of glucocorticoid metabolites.
 
The current study investigated factors linked to SDB and STB among captive red-capped mangabeys (C. torquatus torquatus). Time spent in SDB/STB was first compared between animals in different sized cages and between different enclosure types (cage enclosure or semi-free ranging). The relationships between SDB/STB and sex, age, and rearing history (captive-born or wild-born) were then examined. Finally, the relationship between SDB/STB and grooming behaviour was investigated.
 

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