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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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University of




Social and environmental influences on the welfare of zoohoused spider monkeys (Ateles geoffroyi rufiventris)

Item type Thesis or dissertation

Authors Davis, Nicolas

Citation Davis, N., Schaffner, C. M., & Smith, T. E. (2005).

Evidence that zoo visitors influence HPA activity in spider

monkeys (Ateles goeffroyii rufiventris). Applied Animal

Behaviour Science, 90(2), 1331-1341.; Davis, N.,

Schaffner, C. M., & Wehnelt, S. (2009). Patterns of injury in zoo-housed spider monkeys: A problem with males?

Applied Animal Behaviour Science, 116(2-4), 250-259.;

Davis, N., Schaffner, C. M., & Smith, T. E. (2002). The impact of zoo visitors on hormonal indices of stress in spider monkeys (Ateles goeffroyii rufiventris). Paper presented at 19th International Primatological Society Congress in Beijing, China.; Davis, N., Schaffner, C. M., & Wehnelt, S. (2004). The context, direction and intensity of aggression in captive spider monkeys. Paper presented at 20th International Primatological Society Congress in Torino, Italy.; Davis, N., & Schaffner, C. M. (2005).

Dynamics of aggression in zoo-housed spider monkeys.

Paper presented at spring meeting of Primate Society of Great Britain in Chester, UK.; Davis, N., Schaffner, C. M., & Smith, T. E. (2008). Evidence for aggressive conflicts leading to increased urinary cortisol in zoo-housed group of spider monkeys. Paper presented at 22nd International Primatological Society Congress in Edinburgh, UK.; Davis, N., Schaffner, C. M., & Smith, T. E. (2009). The impact of social events on urinary cortisol in zoo-housed spider monkeys. Paper presented at spring meeting of Primate Society of Great Britain in Bournemouth, UK.

Publisher University of Liverpool (University of Chester) Rights Not to be included in EThOS.

Downloaded 16-Jul-2016 18:17:20 Item License http://creativecommons.org/licenses/by-nc-nd/3.0/ Link to item http://hdl.handle.net/10034/118072 This work has been submitted to ChesterRep – the University of Chester’s online research repository http://chesterrep.openrepository.com Author(s): Nicolas Davis Title: Social and environmental influences on the welfare of zoo-housed spider monkeys (Ateles geoffroyi rufiventris) Date: May 2009 Originally published as: University of Liverpool PhD thesis Example citation: Davis, N. (2009). Social and environmental influences on the welfare of zoo-housed spider monkeys (Ateles geoffroyi rufiventris). (Unpublished doctoral dissertation University of Liverpool, United Kingdom.

Version of item: Submitted version Available at: http://hdl.handle.net/10034/118072 Social and environmental influences on the welfare of zoo-housed spider monkeys (Ateles geoffroyi rufiventris) Thesis submitted in accordance with the requirements of the University of Liverpool for the degree of Doctor in Philosophy

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I hereby declare that this thesis is of my own composition and that all assistance has been acknowledged. The results presented in this thesis have not previously been submitted towards any other degree or for another qualification.

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Table 1.1 Farm animal welfare council’s Five Freedoms (FAWC 1992) 3 Table 2.

1 Recognised species and sub species of Ateles including their 39 latest conservation status Table 2.2 Individual spider monkeys that served as subjects throughout the 41 study period

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Table 4.1 Composition of groups by species/subspecies for group size, 75 number of adults and non-adults, modal number of males and females and total number of aggressive incidents Table 4.

2 Summary of response to the questionnaire showing number of 76 responses for each question and proportion of answers

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Table 5.4 Mean values and number of samples for every individual in the 108 bystander role for each aggression and time category.

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Table 5.7 Number of events and number of samples used for each type of 113 separation category Table 5.

8 Mean values and number of samples for every individual in each 114 type of separation and time category

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Figure 1.1 A model of biological response of animals to stress illustrating 14 the three stages an individual experiences as a result of stress

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Figure 2.9 The binding ratio (%B/Bo) of two serial dilutions of the spider 53 monkey urine pool A and the cortisol standards to demonstrate parallelism Figure 2.

10 Mean ± SEM levels of urinary cortisol across the time of day 55 Figure 3.1 Mean values ± SEM levels of cortisol for the visitor categories 65 of no visitors; low visitors; medium visitors and high visitors Figure 3.2 Urinary cortisol positively correlated with the number of visitors 66 Figure 5.1 % B/Bo of serial dilutions of the non defrosted and defrosted 105 pools and cortisol standards to demonstrate parallelism

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I would firstly like to thank my supervisor Professor Colleen Schaffner for providing the opportunity for me to carry out this research and also for her continued and fantastic support over the many years of the duration of this thesis. I would also like to thank Dr. Tessa Smith for her assistance and guidance in the assays and comments, and Dr. Stephanie Wehnelt for her assistance in the questionnaire. I am also grateful to Chester Zoo for allowing me the time and support so I was able to carry out this work, and the Primate team, particularly Andy Lenihan, who started his workday early on a regular basis to allow access to the spider monkeys. Jason Boyer, Claire Lightfoot, Helen Wright and Dr. Lindsay Skyner also made similar early morning sacrifices for the benefit of my research and Rob Coleman and Dr. Norber Asensio for their assistance in the laboratory. I am also grateful to Professor Robin Dunbar and Dr Lottie Hosie for their advice and support as accredited supervisors, and to Dr. Filippo Aureli, Claire Santorelli, Dr. Sonya Hill and Dr. Vicky Melfi for their advice and comments. I thank Pierre Gay, the European Studbook Keeper for assistance and support in distributing the questionnaire and the many zoo keepers, curators and research personnel at the following zoos that assisted: Aalborg Zoo, Apenheul Primate Park, Artis Zoo, Auckland Zoological Park, The Baltimore Zoo, Banham Zoo, Barcelona Zoo, Zoologischer Garten Berlin, Bristol Zoo Gardens, Cleveland Metroparks Zoo, Colchester Zoo, Copenhagen Zoo, Noorder Dierenpark Zoo Emmen, Frankfurt Zoo, John Ball Zoo, Zoo Köln, Zoo Landau in der Pfalz, Zoological Society of London, Zoo de Mullhouse, Zoo Osnabrück, Omaha’s Henry Doorly Zoo, Peaugres Zoo, Rotterdam Zoo, Santa Ana Zoo, Sequoia Park Zoo, Zoological Society of San Diego, Staten Island Zoo, Suffolk Wildlife Park, Twycross Zoo, Wilhelma Zoologisch–Botanischer Garten, Zoo Wuppertal and in particular Chester Zoological Gardens and ISIS. Finally, I would like to thank my friends and family for their continued support and understanding over these years, especially Lizzie, Tim and Jon. The research protocol was approved by the North of England Zoological Society who adheres to all laws pertaining to the care and treatment of captive animals.


The aim of this thesis was to provide a better understanding of the needs of spider monkeys (genus: Ateles) kept in zoological parks in order to provide an appropriate environment, which enhances the physical and emotional wellbeing of the individuals. 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. My studies also involved behavioural observations and a questionnaire study to collect information from other zoological parks that maintain groups of spider monkeys. In order to address the aims of my research I first validated an enzyme immunoassay for urinary cortisol which allowed for the activity of the HPA axis to be measured to assess the physiological stress responses in spider monkeys. The first study assessed the impact of visitors on spider monkeys by comparing levels of urinary cortisol collected with visitor numbers and I found an increase in visitor numbers was associated with an increase in cortisol. This was the first time the physiological impact of visitors was investigated and supports behavioural research that visitors adversely impact on primates in zoos. The second study I carried out involved a questionnaire to investigate frequency, direction and intensity of aggression in zoohoused spider monkeys in 55 other zoos around the world. The pattern of aggression reported indicated severe and lethal aggression was relatively frequent among captive spider monkeys. Adult males were the most frequent actors of aggression and sub adult males were the most frequent targets, contradicting reports from wild spider monkeys. This aggression could be a condition of the management of spider monkeys in the zoos whereby males are normally transferred between zoos contradicting reports from the wild spider monkeys in which females would emigrate on reaching maturity. Next I investigated aggressive, reproductive and separation stressors on the spider monkeys housed at Chester Zoo over a seven year period and measured their effects via changes in urinary cortisol prior to, at and following each event. Aggression had the largest effect, with targets and bystanders having the highest levels of cortisol on the day of aggression for severe and lethal aggression, respectively. When examining the reproductive events, cortisol levels were significantly elevated in the mother the week prior to and the day of birth, but were highest for bystander females on the day of birth. In the case of separations, cortisol was elevated when an individual was separated for longer than 24 hours for separations and less than 24 hour for reintroductions. Finally I investigated the replacement of the breeding male in the spider monkeys at Chester Zoo. Although a significant behavioural effect was identified in the adult females, there was little evidence of an increase in urinary cortisol among them. In addition, there were no instances of aggression between the adult male and juvenile male in the group.

Overall conclusions from this study indicate that the group of spider monkeys did demonstrate a varying stress response to a variety of social and environmental stressors associated with elevated cortisol levels and behavioural changes. However, there was no evidence of long term chronic stressors which are normally associated with poor welfare. This indicated that the environment provided for this particular group of zoo-housed spider monkeys generally allowed for the individuals within the group to cope and adapt. In light of these findings the study also makes a number of recommendations regarding the enclosure design, relocation of individuals and the gradual introduction of spider monkeys in zoos.

The findings of this study are important as it contributes to our understanding of the physiological responses to stressors in a zoo environment and therefore has implications for animal management. It also identifies potential species specific requirements for the spider monkey that should be considered.


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1.1 Introduction Eliciting naturalistic behaviours from captive species has important consequences for education, conservation and scientific research (Carlstead, 1996;

Mench & Kreger, 1996; WAZA, 2005). For the effective management of exotic animals in zoos the behavioural ecology of the species must be considered in order that an appropriate environment, which enhances the physical and emotional wellbeing of the individuals, can be provided (Carlstead, 1996; Robinson, 1998). Not only are zoological parks responsible for the provision of adequate food, shelter and health care, they must also provide the animals with the opportunity to express normal, natural behaviour within appropriate social settings.

To derive a full understanding of animal welfare researchers have investigated a variety of biological and social processes and their interplay. These include evolutionary history, behavioural ecology and proximate measures that cover behavioural and physiological events (Dawkins, 1980). Various factors have been documented that influence the physical and emotional wellbeing of animals (Dawkins, 1990). These include aspects of an individual’s social environment (Gust, Gordon, & Hambright, 1993) and to a lesser extent their physical environment (Crockett, et al., 1995; Crockett, Shimoji, & Bowden, 2000).

1.2 Definition of animal welfare

Due to the subjective nature of animal welfare there have been doubts about the scientific validity of its measurement and assessment. The term did not originate as a scientific concept, but arose in response to the need to express ethical concerns regarding treatment of animals by humankind (Duncan & Fraser, 1997). It refers to an animal’s quality of life (Broom, 2007) and involves making value judgements regarding elements such as physical health, ‘happiness’, and longevity for which people attach different levels of importance (Tannenbaun, 1991). However, due to the importance of animal welfare and to allow for the formation of effective legislation, scientific research has been used in an attempt to evaluate and measure it (D. Fraser & Duncan, 1998).

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