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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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I aimed to investigate social and external environmental factors influencing the welfare of captive Colombian black-faced spider monkeys (Ateles geoffroyi rufiventris). Data from two field sites in Colombia (Miller, Savage, & Giraldo, 2004) reveal that these animals face a real threat of extinction due to severe habitat destruction, and no current information exists to estimate numbers left in the wild (Savage, personal communication). Consequently, this species has been recently reclassified from vulnerable to critically endangered (Cuarón, Shedden, RodríguezLuna, & de Grammont, 2008). The successful management of the captive population is therefore crucial for potential future re-introduction programmes as well as for educational, research and captive breeding reasons (Kleiman, Allen, Thompson, & Lumpkin, 1996; WAZA, 2005). The following series of studies described in this thesis adopted, where possible, a multi-disciplinary approach with investigations involving physiological as well as behavioural measures that entailed measuring glucocorticoids in urine samples under a variety of social and external environmental conditions. The results of this study may have implications for management across different zoological parks for this critically endangered sub species (IUCN, 2008).

The first aim of my thesis was the validation of an enzyme immunoassay to quantify levels of cortisol excreted in the urine of spider monkeys. Previous studies demonstrate that urine is an effective non invasive measure of hormones in Neotropical primates (French, et al., 1996; T. E. Smith & French, 1997a) and for reproductive steroid hormones in spider monkeys (Campbell, Shideler, Todd, & Lasley, 2001). The initial study involved the development and validation of a urinary cortisol assay for spider monkeys, which is presented in Chapter 2. The protocol involved biological validation which was determined by sampling urine across the diurnal phase of the 24-hour circadian cycle. Biochemical validation followed Reimers and Lamb’s (1991) suggestions for appropriate immunoassay protocols and entailed demonstrating assay accuracy, assay specificity and precision. The validation allowed for the second aim of the thesis, which was to investigate the impact of a variety of stressors on urinary cortisol in the spider monkeys housed at Chester Zoo.

Recently, attention has been paid to assessing the impact of zoo visitors on the wellbeing of animals with mixed results, as some studies find no adverse effect of visitors on animals, whereas others report enriching or even negative effects (Chamove, Hosey, & Schaetzel, 1988; Davey, 2007; Hosey, 2000, 2005). Until the current research presented here, there had been no investigation of the physiological impact of visitors on a zoo primate species. The advent of foot-and-mouth disease provided a unique opportunity to assess the physiological impact of visitors on the spider monkeys. Chester Zoo was closed for a period of six weeks, during which time urine collection was ongoing thus allowing for the collection of physiological data during periods of no visitors, to contrast with periods of varying visitor levels.

In Chapter 3 I present the physiological impact of visitors on the spider monkey HPA axis by assaying samples collected during various zoo visitor numbers, from zero when the zoological park was closed due to the foot and mouth outbreak, to very high when numbers exceeded 15,000 visitors in one day.

The next aim was to develop a questionnaire to determine whether any relationship between social structure and aggression could be determined across institutions. This was a research approach, which had been used previously, to assess patterns of aggression in golden-lion tamarins (Inglett, et al., 1989). This was subsequently sent out to 55 zoological parks and facilities around the world that housed four or more spider monkeys. A database was set up to record the number of aggressive acts, age and sex of the individuals involved, group structure at the time of the incident and finally the severity and context of that aggression. The information from this questionnaire presented in Chapter 4 should identify when aggressive acts occur and with whom and whether this is linked with social management practices in captivity.

The final aim was to assess the impact of different social factors on HPA activity in the spider monkey group at Chester Zoo. Over the seven years of the study period there were a variety of social events that occurred and these were assessed in Chapter 5 by examining cortisol levels in the urine of the individuals of the group in the week prior to, during and the week following each event. This included the impact of aggressive behaviour, reproductive behaviour and the separation and reintroduction of members of the group over the study period.

A change in the social environment of an established group is potentially the most disruptive and traumatic event in captivity. In Chapter 6, a case study approach was used to investigate the significant social event of the replacement of the resident male at Chester Zoo with a new male from another zoological park. Physiological and behavioural data were collected from the whole group for a two week period prior to the arrival of the new male through to the successful integration of the new male six weeks later.

Thus the four data chapters in this thesis cover physiological responses to zoo visitors, physiological responses to several different categories of social events, a case study examining both behavioural and physiological responses to replacement of a breeding male, and the behavioural patterning of aggression in zoo-housed spider monkeys.

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2.1 Subjects and housing 2.1.1 Classification The classification of Ateles has important implications regarding conservation priorities for both in situ and ex situ measures. Without a formal structure of names and an agreed system of usage, there can be no understanding of what exists to be conserved (Collar, 1997). New information regarding taxonomy from fields as diverse as physiology, genetics, behaviour and morphology are continually being published and to some degree the research is still in a state of flux (Collins, 2008;

Nieves, Ascunce, Rahn, & Mudry, 2005).

The original classification of Ateles proposed four species (Kellogg & Goldman, 1944), including A. geoffroyi with nine sub species from Central America;

A. fusciceps with two sub species in the Pacific coast region of north western South America; A. belzebuth with three separate sub species populations from Colombia through to the Amazon basin and A. paniscus with two distinct sub species from the Amazon basin. However, their classifications were based mainly on variations in pelage which differed considerably even within the proposed sub species. It has also been proposed that heterochromatism was responsible for the pelage variation and that all spider monkeys were in fact one polytypic species of A. paniscus (Hernandez-Camacho & Cooper, 1976; Hershkovitz, 1969, 1970). In a study based on morphological variation it was suggested that the genus instead should be separated into three distinct species of A. paniscus, A. belzebuth and A. geoffroyi (Froehlich, Supriantna, & Froehlich, 1991). However, Jacobs, Larson and Cheverud (1995) highlighted possible inaccuracies that arise from relying on pelage as a primary system for classification and demonstrated the importance of the genetic and developmental systems that underlie the phenotypic expression of pelage traits.

Using an analysis of the differences in karyotype in the populations of Ateles Medeiros, Barros and Pieczarka (1997) concluded that the genus should in fact be divided into four different species, but also indicated the necessity of a more coherent taxonomic arrangement for Ateles. An analysis of phylogenetic relationships based on mitochondrial DNA (Collins & Dubach, 2000b) and then on nuclear DNA (Collins & Dubach, 2001) also concluded that there were four separate species of Ateles raising A. hybridus to species status. These were A. paniscus, A.

belzebuth, A. hybridus and A. geoffroyi, including as subspecies the two former species A. geoffroyi and A. fusciceps from the Central American isthmus and the Choco region along the Pacific coast of Colombia and Ecuador, respectively (Kellogg & Goldman, 1944; Konstant, Mittermeier, & Nash, 1985). An assessment of the diversity of all Neotropical primates based on the diverse disciplines of taxonomy, biogeography, morphology and genetics (Rylands, et al., 2000) concluded that there were six separate species of Ateles making up a total of 16 taxa. These are A. geoffroyi, A. chamek, A. paniscus, A. marginatus, A. belzebuth and A. hybridus.

However, the latest review of spider monkey taxonomy using morphological analyses (Froehlich, et al., 1991), molecular studies (Collins & Dubach, 2000b,

2001) and chromosomal analysis (Nieves, et al., 2005) all concur on the three species, A. belzebuth, A. paniscus and A. geoffroyi, with the latter two also supporting the species status of A. hybridus. While further research is required to clarify the taxonomic classification of spider monkeys, and particularly the status of the various sub species, it has been suggested that the latter four species taxonomy, supported by recent studies should be adopted to provide a consensus in all fields of spider monkey research (Collins, 2008). The American Zoological Society has adopted this taxonomy for use in its management of captive spider monkey populations and was also adopted for this study.

2.1.2 Distribution Spider monkeys are found throughout Central and South America (Figure 2.1 and 2.2) with the northern, most distribution of A. geoffroyi vellerosus in Mexico ranging through to A. chamek in Bolivia and Peru in the south. Habitat preferences, behavioural characteristics, life history parameters and social structure are features of spider monkeys that were generally thought to be responsible for the present species distribution are reviewed in Collins and Dubach (2000a).

Figure 2.1 Distribution of Ateles across Central America based on Collins and Dubach (2000a).

Figure 2.2 Distribution of Ateles across South America based on Collins and Dubach (2000a).

2.1.3 Conservation status Spider monkeys are threatened by both habitat fragmentation and hunting pressure throughout much of their distribution (IUCN, 2006; Ramos-Fernandez & Wallace, 2008). They live primarily in the top canopy layers of low, humid, primary evergreen rainforest at elevations of less than 800m (Hernandez-Camacho & Cooper, 1976; Madden & Albuja, 1987). They are large-bodied and feed mainly on fruit necessitating large home ranges (Fedigan, Fedigan, Chapman, & Glander, 1988). In addition, spider monkeys have a long inter-birth interval of approximately three years and a slow development rate (Vick, 2008), which makes them particularly sensitive to hunting and deforestation.

Figure 2.3 IUCN Categories of threatened species.

The IUCN identifies species/subspecies as critically endangered (CR) if they are facing an extremely high risk of extinction in the wild with a criteria of 50% risk of extinction within ten years or three generations; endangered (EN) if they face a very high risk of extinction in the wild with at least a 20% chance of extinction within 20 years or five generations; vulnerable (VU) if they face a high risk of extinction in the wild with the criteria of at least a 10% probability within 100 years;

near threatened (NT) if close to qualifying for one of the above threatened categories or likely to qualify in the near future, and finally as least concern (LC) when a taxon is not evaluated in any threatened category and are widespread and abundant (see Figure 2.3) (IUCN, 2006). Refer to IUCN (2006) for a full explanation of the criteria for conservation status.

2.1.4 Spider monkeys at Chester Zoo The study group based at Chester Zoo was a breeding group of Colombian black faced spider monkeys. Formerly known as Ateles fusciceps robustus (Collins & Dubach, 2000a; Mittermeier, Rylands, & Coimbra-Filho, 1988) or as A. fusciceps rufiventris (Rylands, Groves, Mittermeier, Cortes-Ortiz, & Hines, 2005) following studies into variation of mitochondrial DNA they were recently reclassified as a subspecies of A. geoffroyi, and renamed as A. geoffroyii robustus (Collins & Dubach, 2000a, 2000b, 2001; Groves, 2001) or as A. geoffroyii rufiventris (Nieves, et al., 2005; Rylands, et al., 2005; Rylands, et al., 2000). Although the IUCN still classify them as A. fusciceps spp. rufiventris (Cuarón, Shedden, et al., 2008) in this study the sub species title of A. g. rufiventris has been adopted (see Table 2.1). Colombian black faced spider monkeys range from the western cordillera of the Andes from south western Colombia, northward on the west of the Rio Cauca to eastern Panama (Rylands, et al., 2005). Their conservation status has also recently been updated from vulnerable to critically endangered by the IUCN (Cuarón, Shedden, et al., 2008). For physical appearance see Figure 2.4.

The numbers of subjects varied over the study period from a minimum of eight to a maximum of eleven individuals (see Tables 2.2 and 2.3). Over the seven year study period the group changed as infants were born, sub adults were moved to other zoological parks or individuals died. Age classifications were categorised with adults over six years old (van Roosmalen & Klein, 1988), sub-adults from four to six years, juveniles from two to four years and infants under two years. This is s lightly different to some age classifications of spider monkeys in the wild (e.g. Shimooka, et al., 2008), as an individual was considered to be an adult if it had reached sexual maturity and zoo housed animals mature earlier than in the wild. During the study period two sub adult males were relocated to another zoological park in 2003, and the breeding male was relocated to another zoological park in 2008 with the

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1 Boubli, et al., (2008; 2000a, 2001; 1991; 2005; 1993); Collins & Dubach (2000a, 2000b, 2001); Froehlich, et al., (1991); Nieves, et al., (2005); Sampaio, et al., (1993) 2 Froehlich, et al., (1991); Medeiros et al., (1997); Collins & Dubach (2000a, 2000b, 2001); Rylands et al., (2000);

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