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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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Colombian black faced spider monkeys (Ateles geoffroyi rufiventris) face a real threat from extinction and their conservation status has been recently changed to critically endangered (Cuarón, Shedden, et al., 2008). The management of the captive population of this sub species is therefore crucial in order to maintain a longterm viable population as well as for their educational and research value (WAZA, 2005). In order to be able to provide an appropriate environment, which enhances the physical and emotional wellbeing of the individuals, it is essential that a better understanding of their needs is gained (Robinson, 1998). Despite their conservation value, little attention has been paid to this sub-species in captivity with only a handful of studies published (e.g. Campbell, et al., 2001; Eisenberg, 1976; Eisenberg & Kuehn, 1966; L. L. Klein & Klein, 1971; Konstant, et al., 1985; Schaffner & Aureli, 2005). Therefore, the aim of my thesis was to investigate the social and environmental factors influencing the wellbeing of spider monkeys kept in zoological parks. This series of studies adopted primarily a physiological approach that entailed measuring cortisol in urine samples collected over a seven year period to assess the impact of a variety of social and environmental conditions. These studies were supported by behavioural observations as well as a questionnaire study to collect information from other zoological parks around the world that maintain groups of spider monkeys. My findings are important for the long term welfare and have important implications for the management of this primate taxon in zoological parks.

7.2 The use of urinary cortisol to assess the stress response During the first stage of the study I developed a mechanism to use urinary cortisol as a means of measuring the activity of the hypothalamic-pituitary-adrenal (HPA) axis to assess physiological stress responses in spider monkeys. I achieved this through the validation of an enzyme immunoassay to quantify levels of cortisol excreted in the urine of spider monkeys (Chapter 2). Since I was able to show that levels of cortisol excreted in the urine accurately reflect levels of circulating cortisol, this then enabled me to assess a variety of potentially stressful events that occurred in the Chester Zoo group over the seven year study period.

7.3 Environmental stressors

The next stage of the study looked at one of the main environmental characteristics that defines a zoo environment, its visitors (Hosey, 2005). While the consensus from behavioural studies is that zoo visitors have a negative impact on primates, which may be detrimental to their welfare (Hosey, 2005), the interpretation of behavioural indices of stress is complex (Rushen, 2000). The impact of a chronic presence of large numbers of unfamiliar humans on the welfare of zoo primates through physiological measures was previously unknown. The effect of visitors on zoo primates, with their closer taxonomic links to humans may be more pronounced than that for other taxa (Hosey, et al., 2009b). Previously, only one study had examined the potential effect of visitors on the physiological aspect of stress regarding the levels of GCs and therefore the activity of the HPA axis (Kalthoff, et al., 2001). This study used salivary cortisol in a number of mammal species and no visitor effect was found. The results from my research revealed a significant effect of visitor numbers on urinary cortisol in spider monkeys, with cortisol levels rising with higher visitor numbers. However, whether this increase in cortisol represented a negative impact on their welfare is difficult to assess. In comparison to the known stressful events such as lethal aggression (values range from 0.453 – 67.27 ug cortisol / mg creatinine) the cortisol levels, which ranged from 1.73 -13.73 ug cortisol / mg creatinine, under high visitor conditions are comparatively low.

However, the effect of a prolonged exposure to high visitor numbers has the potential to have an impact on their welfare as it could leave the animal in a prepathological state, which leaves it more susceptible to other stressors (Moberg, 2000). That a stress response was found in the spider monkeys in an enclosure that is relatively large and complex, and which allows the individuals a degree of choice and control to move to areas away from zoo visitors, is indicative of just how potentially stressful large numbers of zoo visitors may be. It raises potential concerns about how spider monkeys housed in smaller traditional enclosures, which do not include such escape opportunities, may cope. This physiological effect highlights the need to consider the location of visitor viewing areas during the design of new zoo enclosures, and in the improvement of existing enclosures, which can have significant welfare implications.

7.4 Social stressors

Social stressors are particularly effective in producing chronic changes in the HPA axis in non human primates, although this is influenced by the species’ social organisation and an individual’s position within it (Engh, et al., 2006; T. E. Smith & French, 1997a; Ziegler, et al., 1995). Previous studies of primate aggression have primarily been carried out on group living species characterised with dominance hierarchies. Spider monkey social organisation is unusual in that they live in communities that have a high fission-fusion dynamic which has probably evolved as a means of dealing with competition for resources and social relationships (Aureli & Schaffner, 2008). This makes them an interesting test case for assessing various social factors that may have different impacts on their HPA responses. No previous studies carried out on Ateles have examined the relationship between aggression and their GC response. In a zoo environment where space is severely limited opportunities for fission can be extremely limited, and the impact of this restriction on the social relationships of spider monkeys was investigated. I carried out three different studies which examined the effect of various social dynamics on cortisol and behaviour in spider monkeys.





The first study followed incidents of aggression at Chester Zoo and assessed by means of a questionnaire (Chapter 4) the severity, context and direction of any aggression in groups of zoo-housed spider monkeys from 24 different zoological parks world wide. In the second study, I assessed how the activity of the HPA axis in individual spider monkeys fluctuated in response to aggression, reproductive events and social separation via urinary cortisol. Finally, I examined the impact of introducing a new male into the group of spider monkeys at Chester Zoo, and measured both behavioural and hormonal activity.

Several aspects of these studies are important for understanding how social dynamics impact on the welfare of spider monkeys. The most dramatic findings stem from aggression within the Chester Zoo group and in spider monkeys from different zoological parks. Spider monkeys differ from most of their Old World counterparts because there is no evidence of clear-cut dominance relationships (Aureli & Schaffner, 2008), a hallmark of the social lives of many Old World primates (Kappeler & van Schaik, 2002). Results from the questionnaire found proportionally high incidences of male-male aggression which was surprising considering the reported strong bonds between males in the wild (Aureli & Schaffner, 2008). While total numbers of incidents of aggression were low compared to other primates, the incidences of severe aggression which resulted in injuries and even death were comparatively high. These more serious incidents were almost exclusively reported as being between males and of the six lethal incidents reported both actors and targets were male. Serious incidents of aggression are known to trigger a high stress response in other primate species (Eberhart, et al., 1983; Ostner, et al., 2008;

Sapolsky, 1982; T. E. Smith & French, 1997b) and this was supported by my research which demonstrated that the highest levels of cortisol occurred in the aftermath of severe and lethal aggression. For severe aggression this led to short term high levels of urinary cortisol on the day following the conflict for the targets of aggression, whereas lethal aggression led to long-term elevations in cortisol for at least a week following the attacks. These levels of cortisol following aggression were four to seven times higher than the other stressful events I identified in my study.

That male-male aggression would be so prevalent and result in so many lethal events was not anticipated because the majority of the literature reports that male directed female aggression is the most frequent form of spider monkey aggression (Fedigan & Baxter, 1984; Slater, et al., 2009) and males have the strongest social bonds among the different age sex classes (Ahumada, 1992; Aureli & Schaffner, 2008). However, lethal male-male aggression has recently been reported in some of the long term field studies of spider monkeys (Campbell, 2006b; Valero, et al., 2006). This evidence seems to suggest a more complex relationship exists between the males and in particular the sub adult males who seem especially vulnerable to the lethal aspects of aggression. One interpretation of the male-male aggression observed in the wild is that it stems from competition for females and may be triggered by the operational sex-ratio in wild communities (Valero, et al., 2006).

Spider monkeys are unusual compared to most other monkey species in that the males remain in their natal group and are therefore likely to be closely related (Di Fiore & Campbell, 2007), while the females disperse. In the management of spider monkeys in zoological parks however it is common practice to move males between groups, despite the recognised importance of maintaining animals in zoological parks in natural social groupings and context (Carlstead, 1996; Robinson, 1998; WAZA, 2005). This practice may then exacerbate the natural tendency of males to target each other when reproductive competition is high. In fact, in the questionnaire study (Chapter 4), introducing males although infrequent was highlighted as being a significant catalyst for aggression and could be traced back to introducing unrelated males together in the same social group. This study therefore recommends that the transfer of young adult females should be considered instead of males as this replicates the natural dispersal patterns of spider monkeys in the wild. Identified problems with male-male aggression, even between related individuals, will however also need to be carefully monitored and managed.

Given the pattern of male-male aggression and the HPA response that spider monkeys experienced in the aftermath of severe and lethal aggression, I believed it was essential to capture the behavioural and physiological responses in the spider monkeys when Chester Zoo replaced their breeding male in 2008 (Chapter 6).

Although the case study found a significant behavioural effect in the resident adult females, there was little evidence of an increase in urinary cortisol among the females. In addition, there were no instances of aggression between the adult male and juvenile male in the group. This could be because the new male on his arrival was not deemed a threat, and this was supported by the male showing no aggressive behaviour towards any of the resident animals throughout the study. There were also no other adult or sub adult males present during this introduction which otherwise may have been a source of tension. Unfortunately, there were insufficient samples taken from the new male to determine whether the introduction did cause a significant stress response in him, although there was some behavioural evidence.

The method of introduction may also have been significant in reducing the overall stress response. A gradual approach was adopted with the male being kept initially in a separated section of the indoor enclosure that allowed full visual and partial tactile contact with the rest of the group. This has been shown in other species to reduce the impact of an introduction and appeared to have also been successful in reducing the overall stressful nature of the introduction (Alford, et al., 1995;

Reinhardt, et al., 1995; Schaffner & Smith, 2005). This provides evidence of the successful introduction of a new male into a group and points to recommendations for managing captive spider monkey populations (see below 7.6).

Another unanticipated result was the change in cortisol levels observed in other adult females during the births. There seemed to be a definite pattern of an increase in the other females immediately following a birth. The reasons for this are unclear, but evidence from the field suggests new spider monkey mothers often spend much of their time alone (McFarland Symington, 1987), which may be an evolutionary trait to keep away from others who may see the infant as a future potential competitor for resources (Chapman, et al., 1989). The forced proximity with the restriction of area within a zoo environment reduces the opportunities for females to fission from the social group at this critical time and this may have been a potential stressor.

7.5 Assessing the welfare in zoo-housed spider monkeys

Three main strategies have been proposed for the assessment of welfare (see Chapter 1, section 1, 3). The assessment of welfare in zoo-housed spider monkeys in this study adopted measures of biological functioning (Barnett & Hemsworth, 1990;



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