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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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A number of factors have previously been identified that can affect GC levels in primates. These include species variation, individual variation, age, season, reproductive status, social status, aggression, social support, reproductive condition, male immigration, risk of infanticide, rank instability, predation, seasonal changes and the availability of resources (Abbott, et al., 2003; Anestis, Bribiescas, & Hasselschwert, 2006; Lane, 2006; Setchell, et al., 2008). In addition, there are many potential sources of stress for primates housed in captive settings (Morgan & Tromborg, 2007) (see Chapter 1). These can include routine husbandry events, presence of care staff, anticipation of feeding, sound, threat of predation, resource scarcity, a non stimulating environment, being housed alone, changes in composition and social dominance rank (for review see Honess & Marin, 2006a). One of the main sources of stress in a captive environment is loss of the opportunity for speciesspecific behaviours for which any animal has a behavioural need (Chapter 1).

A zoo environment offers specific conditions which distinguish it from other forms of captivity (see Chapter 1, section 1.5; Honess, et al., 2005; Hosey, 2005).

Many aspects of an animal’s life history, such as feeding and reproduction, are managed and are therefore beyond the control of the animals. Being confined can also reduce the ability of an individual to respond to aversive situations with appropriate escape or avoidance responses, which for social primates in particular can be significant (Hosey, 2005). These stressors can be in the form of proximity to predators, competing conspecifics, unfamiliar sounds, keeper interactions and the presence of visitors (See Chapter 3; Carlstead & Shepherdson, 2000; Hosey, 2000).

Although the impact of husbandry practices and social relationships on the HPA axis has been assessed in a number of primate species (Honess & Marin, 2006a), there have been only a handful of studies looking specifically at stressors within a zoo environment (Shepherdson, et al., 2004), and none previously reported in zoo-housed spider monkeys. Previous research into social stress in primates has predominately examined it from the perspective of dominance hierarchy relationships, which is important in many species and considered to be a major source of psychological stress (Abbott, et al., 2003; Cavigelli, Dubovick, Levash, Jolly, & Pitts, 2003; Engh, et al., 2006b). Modifying group membership can also be a significant source of social stress with potential to activate the HPA axis (Honess & Marin, 2006b). I first examined the various factors that influence the stress response and how they can be influenced within a zoo environment.

5.2 Environmental factors influencing the stress response

A considerable body of research has been carried out in laboratories on the assessment of housing conditions and husbandry practices on physiological measures of stress in non human primates (Clarke, Harrison, & Didier, 1996; Crockett, et al., 2000; Mendoza, Capitanio, & Mason, 2000; Whitten, Stavisky, Aureli, & Russell, 1998). For example, enclosure size and its structural complexity (Honess, et al.,

2005) has been identified as a potential major source of stress in primates with links to the performance of abnormal behaviours, infant mortality, aggression and growth rates (Morgan & Tromborg, 2007), although studies have shown mixed results. For example, one study increasing enclosure size for great apes found little or no effect on behaviour (S. F. Wilson, 1982), while a study into orang-utans (Pongo pygmaeus) found increasing size and usable space did predict changes in behaviour (Perkins, 1992). A decrease in abnormal behaviours was found with increases in enclosure size in rhesus macaques (Macaca mulatta) (Paulk, Dienske, & Ribbens, 1977), although no decrease was found in a study into long tailed macaques (M. fascicularis) (Crockett, et al., 1995) or pig tailed macaques (M. nemestrina) (Crockett, et al., 2000). However, it is the quality of space that is just as important as the size.

The provision of a complex and stimulating environment is now widely accepted as important in the general health and wellbeing of animals kept in captivity (Honess & Marin, 2006b). This concept of environmental enrichment, in particular, recognises the importance of allowing animals the opportunity to perform speciesspecific behaviours. Such conditions allow for greater control over their environment, which is important since a lack of control over the environment has been identified as potentially the greatest source of stress for animals in captivity (Sambrook & Buchanan-Smith, 1997). Furthermore, increased behavioural options allow animals to respond to adverse environmental conditions by managing confinement related stress. This has been demonstrated by reductions in GC levels in capuchins (Cebus apella) following environmental enrichment (Boinski, et al., 1999). However, while moving animals to more complex environments may, in the long term, be beneficial, in the short term a novel environment may cause a significant stress response (Hennessys, Mendoza, Mason, & Moberg, 1995; T. E.

Smith, et al., 1998).

An environment that provides opportunities for animals to retreat from other conspecifics and reduces proximity to humans or potential predators is beneficial for certain species. In particular, providing places for retreat or to hide is important when unfamiliar animals are introduced into new groups, which is often unavoidable as part of captive husbandry and can often be a cause of aggression (Doyle, et al., 2008;





Morgan & Tromborg, 2007). In a zoo environment the presence of visitors can be a significant factor (Davey, 2007; Hosey, 2000; see Chapter 3), although the effect can differ across different taxa and species and is dependent on the animals flight distance to humans (Hosey, 2008). The provision of areas of retreat can be beneficial. For example, through the provision of a camouflage barrier in front of visitors, reduced aggression and stereotypic behaviour was observed in gorillas (Gorilla gorilla) (Blaney & Wells, 2004). Proximity to animal carers is also a potential source of stress, (Hosey, 2008) although if relationships are positive then close contact can produce friendly interactions and can be a source of enrichment.

The handling of animals however, can be a substantial source of stress, even for animals that have been trained (Bassett, et al., 2003; Honess & Marin, 2006a). Other potential sources of stress include inappropriate environmental variables such as temperature, light, substrate and odour (Morgan & Tromborg, 2007), husbandry routines (Bassett & Buchanan-Smith, 2007) and feeding and foraging opportunities (Morgan & Tromborg, 2007).

5.3 Social factors influencing the stress response

Primates are highly social and intelligent animals normally living in groups (Fuentes, 2007; Kappeler & van Schaik, 2002; Silk, 2007). Group living offers a variety of benefits including improved detection and protection from predators, an increased likelihood of finding a resource as well as defending it from others, an increased chance of finding a potential mate, the transfer of information such as the location of resources, and also the facilitation of alloparental care (Bernstein, 2007;

van Schaik, 1989). However, it also has the negative consequences of increased direct competition over resources potentially leading to conflicts and aggression (Bernstein, 2007; van Schaik, 1989). While there is a general interest within a group in keeping the costs of competition low, and maintaining a cohesive network of social bonds and mutual dependencies (de Waal, 1986b), the potential for social stress from this competition is a constant possibility (Kikusui, et al., 2006). To overcome this, many primate groupings are characterised by dominance hierarchies, which are generally established through aggressive conflicts and then maintained through reliable signals of submission and dominance (Bernstein, 2007; de Waal, 1986b; Preuschoft & van Schaik, 2000). These highly ritualised contexts are designed for maximum benefit but minimum risk with the general principle that an animal consistently and without resistance abandons their place when approached by a more dominant group member (Kummer, 1971a). Knowledge of previous fight outcomes can be used to predict the outcome of the next fight, although appropriate action will still depend on evaluation of the incentive and the assessment of the determination of the opponent to contest that incentive using aggression (Bernstein, 2007). Although such behavioural mechanisms have been adopted to prevent aggressive escalation, conflicts of interest may be unavoidable for group living animals (Aureli, et al., 2002).

Social factors both alleviate and exacerbate the physiological response to stressful stimuli, making primates a good model to investigate links between the social environment and the physiological stress response (T. E. Smith & French, 1997a). Living in social groups offers the benefit of companionship (Kikusui, et al., 2006), and this is demonstrated by a high stress response when individuals are separated (Noble, McKinney Jr, Mohr, & Moran, 1976). Social animals also show a better recovery from aversive experiences when they are together (Mendoza, Coe, Lowe, & Levine, 1978).

5.3.1 Social buffering Social stressors are known to be particularly effective in stimulating the HPA axis (Mendoza, et al., 2000). Complex social affiliations can, however, provide social support protecting the animals from the consequences of stress (Levine, 2000). For example, being accompanied by a familiar group member has benefits in reducing the effect of social separation stress (Kikusui, et al., 2006; T. E. Smith & French, 1997b). This is known as social buffering or social support (Cohen & Wills, 1985).

Given the various types of social organisation displayed by primates, different responses to various social stressors occur in different species, depending on their relationship with their social buffering partner (Mendoza, et al., 2000). For example, this is illustrated by the differences in stress response during exposure to novelty and separation of monogamous titi monkeys (Callicebus moloch) and group living squirrel monkeys (Saimiri sciureus) (Hennessys, et al., 1995). During isolation the GC response to novelty was significantly more sensitive in titi monkeys than in squirrel monkeys indicating the high value of social partners for this species.

The cues responsible for social buffering will also depend on the species and on how they communicate social information to their conspecifics, but can be tactile, olfactory, vocal or visual (Kikusui, et al., 2006). In primates the importance of contact behaviour has been demonstrated in the rearing of rhesus monkeys (M.

mulatta) (Winslow, Noble, Lyons, Sterk, & Insel, 2003) and vocal buffering has been shown to reduce urine cortisol levels in isolated marmosets (C. kuhlii) (Rukstalis & French, 2005).

5.3.2 Aggression Conflict is inevitable among individuals in a social group and several studies have examined the environmental and social factors that regulate conflict and relationships in order to maintain group cohesion (Aureli, et al., 2002; Honess & Marin, 2006b). Aggression is a high risk strategy and primates often rely on noncontact ritualised aggression or dominance displays to reduce risks associated with less predictable more overt forms of aggression (Bernstein, 2007; Preuschoft & van Schaik, 2000).

5.3.2.1 Dominance Researchers have examined social factors that impact on the stress response in non-human primates with considerable focus on the context of dominance and social status (Abbott, et al., 2003; Creel, 2001). Studies indicate that the position in the hierarchy, whether dominant or subordinate, is generally maintained through a specific form of aggression: re-directed aggression (Sapolsky, 1990), and the unpredictable nature of this aggression is thought to contribute to the stress response (Sapolsky, 2004). Dominance interactions have physiological consequences on the HPA axis response, although there is no simple relationship and these interactions can vary across different species (Creel, 2001; Engh, et al., 2006; Ostner, Heistermann, & Schülke, 2008; Setchell, et al., 2008). As a consequence of these profound species differences in their social relationships, there is considerable variation in the ways in which social factors modulate the stress response (T. E.

Smith, et al., 1998), some of which are indicated below.

Callitrichids who live in family groups with a handful of breeding individuals, who are normally the parents of the other group members, showed a tendency for lower basal cortisol levels in subordinate females, e.g. Wied’s marmosets (C. kuhlii) (T. E. Smith & French, 1997b). Squirrel monkeys (Saimiri sciureus) who live in large multi-male/ multi-female groups show approximately equal basal cortisol levels in dominant and subordinate females (Saltzman, Mendoza, & Mason, 1991) and lower levels in dominant males (Manogue, 1975), whereas olive baboons (P. anubis), which also live in multi-male/ multi-female groups, have higher levels of GCs in subordinate males than dominant males (Sapolsky, 1982). Higher GC levels are found in high ranking dominant males than in subordinate males in Japanese macaques (M. fuscata) (L. Barrett, Gaynor, & Henzi, 2002) and ring-tailed lemurs (L. catta) (Cavigelli, 1999).

5.3.2.2 Aggression within and between the sexes Aggression between individuals of the same sex is related to dominance and can be explained through reproductive competition (Honess & Marin, 2006a). Due to the seasonal availability of resources many primate species are seasonal breeders (Dixson, 1998). An increase in aggression during the mating season is widely reported across a range of primates in the wild (Ostner, et al., 2008), although this has not always been replicated in captivity (Honess & Marin, 2006a). This rise in aggression has also been associated with an increase in levels of testosterone in males such as rhesus macaques (Herndon, Bein, Nordmeyer, & Turner, 1996), although this may be as a result of increased intrasexual aggression and not because of it (Cavigelli & Pereira, 2000).

Aggression between the sexes has been linked with a male reproductive strategy and intersexual selection, and may be associated with intensifying the social bonds that are required for reproductive success (Eaton, Modahl, & Johnson, 1981).



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