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«Item type Thesis or dissertation Authors Davis, Nicolas Citation Davis, N., Schaffner, C. M., & Smith, T. E. (2005). Evidence that zoo visitors ...»

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The final prediction, that the birth of an infant would be associated with increased cortisol was supported, although the increased sensitivity to potential stressors on the mother, postpartum, resulting in heightened GC levels (Behringer, et al., 2009) was not demonstrated. Instead GC levels were at their highest in the week prior to the birth, before falling back on the day of birth and returning to baseline levels for the week following. Pregnancy could be seen as a potential stressor due to increased metabolic costs and this could be related more to the physiological effects of pregnancy (Weingrill, et al., 2004). In humans plasma cortisol increases during pregnancy and then declines following parturition. By late trimester total cortisol levels are approximately three times non pregnant levels, rising to five times in late gestation (Keller-Wood & Wood, 2001). There are also well established links between reproductive status and basal cortisol levels. For example, squirrel monkeys (Vogt, Coe, & Levine, 1981), callitrichids (Saltzman, et al., 1998; T. E. Smith & French, 1997b; Ziegler, et al., 1995) ring-tailed lemurs (Lemur catta: (Cavigelli, 1999), chacma and yellow baboons (Papio hamadryas ursinus, P. cynocephalus) (Weingrill, et al., 2004), (Beehner, et al., 2006), marmosets (C. kuhlii) (T. E. Smith & French, 1997b), (Callithrix jacchus) (Tardif, Ziegler, Power, & Layne, 2005) all showing elevated cortisol levels during late gestation. However, the same pattern has not been found in rhesus macaques (Challis, Davies, Benirschke, Hendrickx, & Ryan, 1975). This heightened cortisol at a time of increased metabolic demand might not be surprising considering its metabolic role (Setchell, et al., 2008). An increase in GC levels is also related to the initiation of labour in humans, a mechanism that may also be found in other primates (R. Smith, Chan, Bowman, Harewood, & Phippard, 1993).

The increase in cortisol levels in the other females at birth was not predicted and was surprising. The timing of the births was checked to ensure that they did not coincide with any other stressful events which may have confounded the results, and no other significant events were found within the sample periods. A possible explanation for the increase may be that the arrival of an additional group member may represent a greater competition for food resources in the future. This post weaning resource competition would apply in particular for male infants in spider monkeys where there is female dispersal (Chapman, et al., 1989). Other possible explanations may be that the increase is related to the effect of novelty which can elicit increases in GC levels (Hennessys, et al., 1995), or an increase in overall activity as proposed when similar results were observed in a group of captive bonobos (Behringer, et al., 2009). A positive correlation between locomotion and levels of cortisol has also been observed in some species (e.g. T. E. Smith, et al., 1998).

Finally, I predicted that separation events would lead to a stress response, following separation, for the target individual. However, this prediction was only partially supported. The best fitting model for the data revealed that there was a twoway interaction of time and the type of separation. However, this was due to a trend for a reduction in cortisol levels following separation, with levels reducing in particular for the separated individual over time. No changes were shown following reintroduction. The reason for the separation needs to be considered. Generally, individuals were separated following an aggressive incident or for veterinary reasons which may mean cortisol levels prior to separation were elevated. Although in previous studies separation has led to a significant stress response (Boccia, et al., 1995; Crockett, et al., 1995). The conditions of the separation in this study meant the individuals were still within visual and tactile contact of the other members of the group which is known to have a social buffering effect (T. E. Smith, et al., 1998).

Species differences are known to occur with the effects of social isolation and these may depend on the behavioural and ecological characteristics of the primate (Crockett, et al., 2000). In addition, it may be that because spider monkeys live in a social system characterised by high fission-fusion dynamics and therefore typical to have individuals travelling on their own for days or weeks at time (Schaffner and Aureli personal communication) such separations are not stressful for this species.

In summary this long term investigation into the effects of various social stressors on a group of zoo-housed spider monkeys found aggressive events to elicit the greatest stress response and that these were affected by severity, time and role.

Only for the rare incidents of lethal aggression were there sustained increases in GCs, which may represent distress to the animals concerned. For reproductive events there was no evidence for any stress response associated with ovulation and mating events even though a zoo environment reduces the potential for consortships away from the rest of the group. High GC levels in the week prior to birth were found, but this represents physiological effects of a higher metabolism and has also been found in other primate species during late pregnancy (Setchell, et al., 2008). A high level of GC for other females during birth was unexpected but may be related to the effect of novelty which can elicit increases in GC levels (Hennessys, et al., 1995), or an increase in overall activity as proposed when similar results were observed in a group of captive bonobos (Pan paniscus) (Behringer, et al., 2009).





This was a retrospective study and there was no control over the various events studied, therefore, the likelihood of different events having confounding effects on cortisol should be considered. However, the statistical approach used, to examine the various factors take into account the magnitude of the response to the different variables individually in determining the best explanatory model for the data (Tabachnik & Fidell, 2007). However, to be extremely conservative and minimize such confounding factors any lower level events, which overlapped with any major events, were not analysed. However, it is possible that longer term effects of the higher level events may have influenced some of the results.

While enzyme immunoassays have been used previously to examine oestrogen (E1C) and progesterone (PdG) in captive spider monkeys (Campbell, et al., 2001), this is the first time levels of cortisol have been investigated with respect to aggression, reproduction or separation events in spider monkeys. Finally, separations did not evoke a considerable stress response unlike that observed in other species (Hennessys, et al., 1995). In fact it actually led to a significant reduction in GC levels, which may be explained both by the conditions of the separation and the natural fusion-fission characteristic of spider monkey social life. This could have implications for recommendations of management practices for separations or reintroductions for spider monkeys in zoological parks. Considerable differences have been found between species and sub species in the stress responses of various contexts, which could be caused by the different approaches in responding to stressors (Honess & Marin, 2006a).

–  –  –

6.1 Introduction For zoological parks to preserve populations of wild animal species over long periods of time it is necessary to maintain their genetic diversity and demographic security (Ballou & Foose, 1996). This means that populations need to be managed with carefully co-ordinated programmes requiring full co-operation across institutions (Hosey, et al., 2009a; Hutchins & Wiese, 1991). The consequences of trying to maintain genetic diversity in what is essentially a series of small and fragmented populations therefore requires the regular movement of individuals across a number of social groups.

Within wild populations dispersal occurs naturally, although there is variation across sex, age and life history stages (Pfeifer, 1996). The main evolutionary factors are to avoid inbreeding, reduce competition over local resources, reduce mate competition and co-operative behaviour among kin, with evolutionary stable patterns of dispersal assumed to result from a balance of these selected forces (Nagy, Heckel, Voigt, & Mayer, 2007). Typically among mammalian species, dispersal is sex-biased in favour of males (Greenwood, 1980), although there are exceptions such as wild dogs, Lycaon pictus (Frame & Frame, 1976), chimpanzees, Pan troglodytes (Pusey, 1987), traditional agrarian human societies, Homo sapiens (Boehm, 1992; Marlowe,

2005) and spider monkeys, Ateles spp (Di Fiore & Campbell, 2007; McFarland Symington, 1990). Although some adverse effect of relocating animals to new zoo settings is to be expected, it is essential that the dispersal patterns in natural populations are considered when planning such moves in order to minimise disruption and stress (Pfeifer, 1996).

The movement of animals across populations in captivity can be disruptive and can cause social instability in the existing group (Kleiman, 1980). The formation of new groups and the introduction of new animals into existing groups can be extremely stressful and potentially dangerous to the immigrant and members of the existing group, particularly in social primates (Brent, et al., 1997; A. S. Clarke, Czekala, & Lindburg, 1995; Reinhardt, Liss, & Stevens, 1995). The separation of individual monkeys which can happen for a period of months prior to and even following the translocation of individuals can also be extremely stressful (Noble, et al., 1976). The consequences of introductions and separations however show significant variation across different species of primates, which may be linked to their social organisation and mating patterns (A. S. Clarke, et al., 1995; Mendoza, et al., 2000) (see Chapter 5).

A number of studies have assessed the impact of group formation, using various indicators of stress including behavioural, physiological and immune responses (M. R. Clarke, et al., 1996; Doyle, et al., 2008; Gust, Gordon, & Hambright, 1993; Line, et al., 1996; Schaffner & Smith, 2005). Studies in the wild have shown significant increases in glucocorticoids (GCs) following the migration of unfamiliar males (Beehner, et al., 2005; Engh, et al., 2006). In captive studies GC levels have also been used alongside behavioural studies in order to assess the impact of group formation. Several studies have been conducted in macaques that examine the impact of changing group composition. Increased GC levels and significant aggressive behaviour occurred in rhesus macaques in response to group changes (Macaca mulatta) (M. R. Clarke, et al., 1996; Gust, Gordon, & Hambright, 1993;

Westergaard, Izard, Drake, Suomi, & Higley, 1999), and increased GC levels but no serious aggressive behaviour was observed in female pig tailed macaques (M.

nemestrina) when they were moved from individual cages to form a new group (Gust, et al., 1996). In a study comparing the group formation of two species of male macaques, GC levels decreased over time in cynomolgus macaques (M. fascicularis), while lion-tailed macaques (M. silenus), who showed more aggression, had GC levels that remained at high levels (A. S. Clarke, et al., 1995). In a study with marmosets (Callithrix kuhlii) the formation of multi-male polyandrous groups (using related males) found no changes in GCs (Schaffner & French, 2004).

In an evaluation of introduction procedures in chimpanzees, there was a great deal of variation from one facility to another (Alford, Bloomsmith, Keeling, & Beck, 1995; McDonald, 1994). Chimpanzees share a social organisation, like spider monkeys, which is characterised by a high degree of fission-fusion dynamics (McFarland Symington, 1990). They also demonstrate a fluid social structure with males showing the strongest bonds. In addition, males are not known to transfer between groups and instead remain in their natal group. In the wild, unfamiliar males are normally met with hostility and inter group aggression can be violent, leading to serious injury and even death (Watts, et al., 2006; M. L. Wilson, Wallauer, & Pusey, 2004; M. L. Wilson & Wrangham, 2003). With their size, strength and natural aggressive tendencies towards unfamiliar males, introductions in chimpanzee groups in captivity can often be difficult. The dangers are confounded by typical captive environments which are confined, providing fewer opportunities for individuals to avoid conflict or escape aggression. Atypical species groupings and the high frequency of movement between groups of chimpanzees are also probably related to an increased instability and aggression in the captive environment (Brent, et al., 1997).

6.2 Factors influencing introductions

Various strategies have been adopted for the introduction of primates into groups or the formation of new groups. For rhesus macaques simultaneous introductions resulted in high rates of serious aggression that resulted in high mortality rate (Bernstein, et al., 1983). Familiarisation of potential group members prior to introductions has been tried with four species of macaques with mixed results (Reinhardt, et al., 1995). The timing of familiarisation is also important so that the animals can establish rank relationships, but not too long as to exacerbate initial fear response if resolution is not achieved (Brent, et al., 1997; Reinhardt, et al., 1995). Repeated attempts to introduce rhesus macaques sometimes led to increasing tension between animals (Bernstein, 1991). However, if introductions were carried out gradually with a small number of animals at a time agonistic behaviours were greatly reduced in this species with higher rates of grooming and sexual interactions (Westergaard, et al., 1999). The size of the group can also be a factor, with the response from a group of black tufted-ear marmosets (Callithrix kuhli) to the introduction of a new female varying with group size, with a more aggressive response found in larger groups (T. E. Smith & French, 1997b).



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