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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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Duncan & Fraser, 1997). This was mainly by a longitudinal physiological approach with the measure of GCs recorded over a seven year period, although behavioural measures were key in the interpretation of the results. The use of physiological measures on their own can be difficult to interpret, but particularly over the long term can be an indicator as to how well an animal is coping within its environment (Barnett & Hemsworth, 1990; Lane, 2006). Such an approach has been recommended as a means of improving understanding of how to care for zoo animals, and in particular for identifying specific characteristics of a zoo environment that may have a significant impact on their lives (Carlstead & Shepherdson, 2000; Shepherdson, et al., 2004; Wielebnowski, 2003). Behavioural measures were also used to aid in the interpretation of the changes in cortisol and to identify particular behaviours or behaviour patterns that have been associated with a stress response. This study has contributed to the understanding of how well spider monkeys adapt to a particular zoo environment and has highlighted potential factors which can result in a stress response, and therefore a potential negative impact on their welfare. It has also highlighted the usefulness of cortisol studies in their potential in contributing to the assessment of welfare of individual animals within a zoo environment.

Information on the natural behavioural repertoire of spider monkeys in the wild were also used as a means to identify their species-specific requirements and to help explain the unusual aggressive behaviour patterns recorded in zoological parks (Stolba & Wood-Gush, 1989; Veasey, et al., 1996b). An integrative approach using behaviours as well can help identify behaviour patterns that may be indicative of a stress response as was identified in the elevated scratching rates recorded in adult females during the introduction of the new male (Chapter 6).

Overall several stressors were identified and assessed using these procedures, and included zoo visitors, aggression, social separations, introductions and births.

Although some of these events resulted in dramatic elevations in urinary cortisol in some individuals, they were not sustained. This suggests that although such events resulted in an acute stress response there was no clear evidence of chronic stress indicating that the spider monkeys at Chester zoo appeared to be able to adapt to their particular social and physical environmental. However there may still be a degree of individual variation which can be based on age, sex and experience. During the course of the study one individual Mil died from natural causes. However, she was a hand reared individual that appeared to be poorly integrated with other group members and for the year prior to her death had baseline cortisol levels three-fold higher than the baseline of other members. This sustained elevated level of cortisol may have placed her in a prepathelogical state (Moberg, 2000), which would have made her more susceptible to the viral infection that killed her.

7.6 Implications for other zoo studies

My findings add to the growing body of literature which indicates that urinary cortisol is an effective means of assessing the impact of environmental and social stressors within a zoological park setting (Carlstead & Shepherdson, 2000;

Wielebnowski, 2003). Providing there is appropriate validation for each species (Buchanan & Goldsmith, 2004), it can be used as a non invasive method to assess any potentially aversive impact on zoo animals. For example, to maintain genetic diversity the movement of animals across populations is essential, but it can be disruptive and cause social instability (Kleiman, 1980). This method can be used for monitoring the stress response to assess introductions and identify the least disruptive techniques. The activity of the HPA axis could also be used to assess visitor effect and other potential stressors within a zoo environment in a variety of taxa with important implications for the design of exhibits. An enclosure which allows the animals the opportunities to perform their natural behaviours will have positive consequences for their welfare, as well as education and conservation activities by zoological parks (Carlstead, 1996; WAZA, 2005). Finally such studies can add scientific evidence to husbandry requirements which are produced for many species of zoological park animals (Shepherdson, et al., 2004).

7.7 Further studies

Following the visitor effect on cortisol levels in the group of spider monkeys at Chester Zoo it would be important to also assess cortisol levels in other spider monkeys at other zoological parks, in particular in enclosures where there are not the opportunities to escape from visitors. A further study that validates more concretely a discrete behavioural measure of stress, such as scratching, would also be beneficial to allow for a more accessible and more cost effective method of assessing potential stressful events, such as introductions. More investigation is required into the effect of introductions of males into established groups and to assess various techniques of introduction. The assessment of female introductions would also be of interest to demonstrate whether introductions that reflect the natural dispersal pattern of spider monkeys are less stressful for the group and the individual. The measurement of GC levels in spider monkey groups in other zoological parks would provide additional evidence to assess whether enclosure characteristics may influence GC levels and help identify potential aversive factors which can then be investigated in order to improve their welfare. The measure of the GC response in other spider monkey relocations would also help identify whether there are any differences in age, sex or specific techniques which may provide information on the suitability of individuals to introductions.





Longitudinal hormonal and behavioural monitoring, along with keeper and health records, can be also used to assess the effect of various environmental and social changes. Another possible area of further study would be to investigate how the zoo environment affects the welfare of other species of animals that also live in social systems that are normally characterised by high fission fusion dynamics such as chimpanzees (Pan troglodytes) (McFarland Symington, 1990), spotted hyena (Crocuta crocuta) (Holekamp, et al., 1997) and African elephants (Loxodonta africana) (Wittemyer, Douglas-Hamilton, & Getz, 2005).

7.8 Recommendations for management of zoo-housed spider monkeys

First, larger and more complex enclosures that allow opportunities for individuals to temporarily separate themselves from the larger social group, in order to simulate fission events in the wild, may reduce the frequency and severity of aggression and provide a means of retreating when zoo-visitor numbers are high (Caws, et al., 2008; Wehnelt, et al., 2006). This may be particularly important for spider monkeys as fissioning away from group members is an important strategy for coping with conflict in wild spider monkeys (Aureli and Schaffner, in prep;

Rebecchini, Schaffner & Aureli, in prep).

The relocation of males rather than females should be adopted in order to follow the normal immigration patterns of wild spider monkeys in which females emigrate and males are philopatric (Di Fiore & Campbell, 2007; Fedigan & Baxter, 1984; Vick, 2008). The social and physical environments in which spider monkeys tend to be kept in zoological parks do not reflect that found in nature and may exacerbate the propensity for male-male aggression in the wild. Therefore, those managing zoo populations of spider monkeys should consider relocating females rather than males. Due to well known problems of introducing male chimpanzees into new groups the relocation of females is already a protocol followed with a different primate species that has a social organisation characterised by high fissionfusion dynamics (Carlson, 2006; Fulk, 2000).

Third, the technique of a gradual introduction although still eliciting an increase in GC levels for the resident females along with some associated behavioural changes seemed to follow previous studies in captive primates (Brent, et al., 1997; Reinhardt, et al., 1995) and reduced the overall impact of the introduction.

By having the facility to separate individuals from a group, but to remain in full visual and tactile contact, helps facilitate what can be potentially stressful events such as introductions and should be recommended as a management technique for future introductions in spider monkey groups.

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Abbott, D. H., Keverne, E. B., Bercovitch, F. B., Shively, C. A., Mendoza, S. P., Saltzman, W., et al. (2003). Are subordinates always stressed? A comparative analysis of rank differences in cortisol levels among primates. Hormones and

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Achenbach, G. G., & Snowdon, C. T. (2002). Costs of caregiving: weight loss in captive adult male cotton-top tamarins (Saguinus oedipus) following the birth of infants. International Journal of Primatology, 23, 179-189.

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Anestis, S. F., & Bribiescas, R. G. (2004). Rapid changes in chimpanzee (Pan troglodytes) urinary cortisol excretion. Hormones and Behavior, 45(3), 209– 213.

Appleby, M. C. (1999). Human, animals and machines. In M. C. Appleby (Ed.), What should we do about animal welfare? (pp. 19-43). Oxford: Blackwell

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Asensio, N., Korstjens, A. H., Schaffner, C. M., & Aureli, F. (2008). Intragroup aggression, fission-fusion dynamics and feeding competition in spider monkeys. Behaviour, 145(7), 983-1001.

Aureli, F., Cords, M., & Van Schaik, C. P. (2002). Conflict resolution following aggression in gregarious animals: a predictive framework. Animal Behaviour, 64(3), 325-343.

Aureli, F., & de Waal, F. B. M. (1997). Inhibition of social behavior in chimpanzees under high-density conditions. American Journal of Primatology, 41(3), 213Aureli, F., Preston, S. D., & de Waal, F. B. M. (1999). Heart rate responses to social interactions in free-moving rhesus macaques (Macaca mulatta): A pilot study. Journal of Comparative Psychology, 113(1), 59-65.

Aureli, F., & Schaffner, C. M. (2007). Aggression and conflict management at fusion in spider monkeys. Biology Letters, 3(2), 147-149.

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Cambridge: Cambridge University Press.

Aureli, F., Schaffner, C. M., Boesch, C., Bearder, S. K., Call, J., Chapman, C. A., et al. (2008). Fission-fusion dynamics: New research frameworks. Current Anthropology, 49(4), 627-654.

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(2006). Raiding parties of male spider monkeys: insights into human warfare?

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