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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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Alternatively, as aggressive bouts are seldom associated with copulation it has been proposed that female-directed male aggression is nothing more than a mechanism for spacing and asserting dominance (Bercovitch, Sladky, Roy, & Goy, 1987). Another theory is that it is a means of sexual coercion, when force is used to increase the chances of a successful mating, or decrease the chances of a successful mating with another male (Clutton-Brock & Parker, 1995; Smuts & Smuts, 1993). Although this has been reported in relatively few species of primate, e.g. Japanese macaques (G.

M. Barrett, et al., 2002) and orang-utans (Pongo pygmaeus) (Manson, 2007) it does occur where social organisation is characterised by fission-fusion dynamics and female dispersion (Slater, et al., 2008) and is normally associated with a behavioural stress response in the targeted females (e.g. Campbell, 2003).

Although it is generally believed that male primates are more aggressive than females (Reinhardt, 1987), this is not always the case. For example, work on captive rhesus macaques revealed that aggression was more an individual character trait than dependent on sex or rank (Reinhardt, 1987). There is also limited evidence for age related affects on aggression, although increases are related more to reproductive maturation and rank (Honess & Marin, 2006a).

5.3.3 Reproductive behaviour The effect of reproductive behaviour on GC levels has not been well studied although they are likely to be related to dominance. In a multi-male group living primate dominant males normally have a higher reproductive success than subordinates, although female choice may not necessarily be correlated with dominance rank (Manson, 2007). In a study on wild Japanese macaques (M. fuscata), rates of aggression and copulatory behaviour were the same in dominant and subordinate males, although cortisol levels were significantly higher in dominant males indicating a cost (G. M. Barrett, et al., 2002). In addition, it is possible that females choosing to mate with lower ranking males incur a cost in the form of increased aggression from dominant males in the group (Smuts & Smuts, 1993) and the potential cost of inferior genes.

There are also a handful of studies in non human primates that suggest giving birth may be stressful for females. In zoo-housed gorillas (Gorilla gorilla) individual variation in postpartum stress responses occur and appear to be related to failure of maternal behaviour (Bahr, Pryce, Dobeli, & Martin, 1998). There is also evidence of an increased stress response in lactating females when compared to non lactating females in captive rhesus macaques, which may be related to a heightened perceived risk from the mothers for their infants (Maestripieri, Hoffman, Fulks, & Gerald, 2008). Overall the link between cortisol and reproduction is complex as reproductive hormones can modify cortisol levels in various ways (see Chapter 1, section 1.4.9).

5.3.4 Group formations and introductions Changes in group composition, such as recruitment of new individuals, and loss of individuals through emigration represent periods of potential instability for group living animals. In wild chacma baboons (Papio hamadryas ursinus), significant rises in mean GC concentrations were observed following the immigration of unfamiliar males compared to when no immigration occurred (Beehner, Bergman, Cheney, Seyfarth, & Whitten, 2005; Engh, et al., 2006).

However, such rises appeared not to be the result of male instability itself, but more specific to the alpha male and to females with dependent young. In a group of yellow baboons (P. cynocephalus) the immigration of an aggressive male led to an increase in GC levels in the resident group, particularly in the females, as well as the new male (Alberts, Sapolsky, & Altmann, 1992).

In captivity the introduction of new individuals into a group of rhesus macaques caused high levels of aggression and severe injuries (see Honess & Marin, 2006b). In Wied’s marmosets the reaction of the females in the group to the introduction of a stranger was dependent on the size of the group, with smaller groups showing less aggressive behaviour (Schaffner & French, 1997), although the extent to which either result corresponded to higher GC levels is not known.

Due to the social nature of primates, separation and solitary housing is a well established stressful event (Boccia, et al., 1995; Crockett, Bowers, Bowden, & Sackett, 1994). Involuntary social separations have a substantial impact on the HPA axis causing increases in cortisol levels (Mendoza, et al., 2000), although this is also dampened by the presence of a preferred partner (Gust, Gordon, & Hambright, 1993;

T. E. Smith, et al., 1998). However, separation of group members in captive settings is sometimes unavoidable for management reasons.

The intensity of the stress response due to separation and introductions can be mediated by age and sex (Gust, Gordon, & Hambright, 1993). For example, the separation of infants and juveniles is known to induce a severe behavioural stress response in the infants (Boccia, et al., 1995; Terao, Hamano, & Koyama, 1995). In contrast, the separation of adult male rhesus macaques from a group initially resulted in no response in the females remaining in the group or in the separated males, however, following reintroduction back into the group after a long-term separation a significant stress response occurred in both males (Gust, Gordon, Hambright, & Wilson, 1993). Below, I examined how these various influences on stress response may affect spider monkeys within a zoo environment.

5.4 Spider monkey social dynamics

5.4.1 Spider monkey social organisation: its relevance to stressors in captivity Spider monkeys live in multi-male/multi female communities, distinctive among monkey social organisation because this system is characterised by a high degree of fission-fusion dynamics in which members of the community frequently split and merge into fluid subgroups, so much so that members of a single community are rarely, if ever, altogether (Aureli & Schaffner, 2008; see Chapter 1).

Therefore, housing spider monkeys in confined settings, which precludes the opportunity for expressing any fission-fusion dynamics, could serve as a potential primary stressor in a zoo environment. Not only can captivity restrict the opportunities for natural behaviour but it can also reduce opportunities for animals to retreat from potential sources of stress, such as visitors or conspecifics (Hosey, 2005;

see Chapter 1).

5.4.2 The dynamics of aggression in spider monkeys Studies into aggression in monkeys have primarily been carried out on species that are not characterised by high fission-fusion dynamics. There are no previous studies carried out on Ateles that examine the relationship between aggression and their GC response. Spider monkeys also differ from most of their Old World counterparts because there is no evidence of clear cut dominance relationships in spider monkeys (Aureli & Schaffner, 2008), a hallmark of the social lives of many Old World primates (Kappeler & van Schaik, 2002).

Spider monkeys also show low levels of affiliative behaviours such as grooming (Ahumada, 1992; Fedigan & Baxter, 1984; Schaffner & Aureli, 2005;

Slater, et al., 2009). Such behaviours have been used in studies on primates in captivity as a means of a behavioural assessment of a stress response (Schaffner & Aureli, 2005), so this may make behavioural assessments more difficult in spider monkeys than other species. They do, however, have a suite of species-specific behaviours, which include embraces and pectoral sniffing, that may be used as a means of conflict management during potential periods of conflict immediately following an episode of separation (Aureli & Schaffner, 2007) and maybe useful as an alternative means of behavioural assessment. Scratching behaviour has also been used in previous studies in other primates as a non invasive means of measuring psychosocial stress (Maestripieri, et al., 1992) and may also be relevant in spider monkeys.

In wild spider monkeys the most commonly reported aggression is directed by males towards females, although physical attacks are rare (Campbell, 2003;

Campbell & Gibson, 2008; Fedigan & Baxter, 1984; McFarland Symington, 1987;

Slater, et al., 2008). Such aggression is believed to be a form of sexual coercion when females are ovulating (Slater, et al., 2008). Rates of aggression between males, however, are rarely reported. Males form the strongest bonds within a spider monkey community and spend most of their time together (Ahumada, 1992; Aureli & Schaffner, 2008; Slater, et al., 2008). However, there have been two recent reports of lethal aggression in the wild by adult males towards younger males (Aureli & Schaffner, 2008; Campbell, 2006b; Valero, et al., 2006). Also, there have been observations that relationships between young and older males are uncertain with young males keeping a safe distance (Aureli & Schaffner, 2008; Vick, 2008).

Indeed, as presented in Chapter 6, I found that in captive spider monkeys adult males were responsible for all cases of severe and lethal aggression.

Aggression between adult females is relatively rare (Fedigan & Baxter, 1984;

Slater, et al., 2008) and relationships between unrelated females are reported to be of lower quality in spider monkeys (Aureli & Schaffner, 2008; Di Fiore & Campbell, 2007; Fedigan & Baxter, 1984; McFarland Symington, 1990). In fact, aggression in females is even low during periods of low food availability (Campbell & Gibson, 2008). Although there are no long term established dominance patterns between adult females, the older more established females have been reported to direct aggression towards newer immigrants who could be viewed as competing for resources (Asensio, et al., 2008; Chapman, et al., 1995; McFarland Symington, 1987). This could be explained by fission-fusion dynamics reducing scramble competition at the sub group level (Asensio, et al., 2008).

Competition for resources is believed to be the main antecedent of fissionfusion in spider monkeys – in particular for food (Aureli, et al., 2008; McFarland Symington, 1990). In a zoo environment where food is plentiful and therefore the proximate triggers for competition are reduced, aggression may be less frequent.

However, when one of the primary mechanisms for reducing competition in spider monkeys is removed (Aureli & Schaffner, 2008), i.e. the ability to fission from the group, it is possible that aggression could be exacerbated under captive conditions.

5.4.3 The social dynamics of reproductive behaviour As previously reported, the most frequent aggression in spider monkeys is female-directed male aggression (Aureli & Schaffner, 2008). It has been proposed that such aggression is linked to the reproductive state of the female (Campbell, 2003; McFarland Symington, 1987) and may be part of a ritualized intimidation display (Fedigan & Baxter, 1984). This has been supported in a recent study by Slater et al (2008). The authors found that aggressive male-female interactions could be split in to two categories of physical aggression involving contact, and a prolonged chase, the later taking place overwhelmingly during periods when the female was ovulating.

In addition, spider monkeys have unusual courtship patterns. In the wild the pair will deliberately and secretly move away from other member of their community as a “consortship” and stay away for what could be minutes or even full days (Campbell & Gibson, 2008). Behaviour during consortship suggests that they are avoiding other group members. Both the male and female are actively vigilant and avoid vocalising with other group members (Campbell, 2006a). This pattern of behaviour is also observed in captive settings with the male and female often leaving the rest of the group and finding a sheltered area away from other group members and maintaining a high degree of vigilance during copulation (personal observation).

A zoo environment may not allow opportunities for consortship because there is not enough space for the pair to move away from the rest of the group. This could potentially be stressful for the male during mating events and could be reflected in an increase in cortisol levels at this time. However, the reason for the secrecy in the wild situation may be due to male competition for females. As this is not present in most zoo settings (ISIS, 2008), their need for secrecy may not be as essential for successful mating to take place, but may still constitute a significant source of stress for both male and females if it is not enabled.

Unlike old world primates, spider monkeys do not exhibit visual demonstration of reproductive status, such as swellings, and instead researchers have to rely mainly on behavioural clues. Due largely to the often secretive nature of copulations, sexual behaviour in wild and even captive spider monkeys is rarely observed (Campbell & Gibson, 2008). Despite this, it has been suggested that ovulation is associated with a number of distinctive behaviours. They include copulation (Symington, 1987), place sniffing where the male sniffs the place where a female was sitting (L. L. Klein & Klein, 1971), clitoral stimulation by males and females (van Rooselmalen, 1985) and urine sniffing (Campbell, 2004). However, endocrinological data have shown that none of these behaviours are strictly associated with ovulation as they have been observed, albeit less frequently at other stages of the reproductive cycle (Campbell, 2004). It is likely that they are also used by the males as a means of gauging a female’s reproductive condition; therefore care should be taken when using behaviour alone as a means of assessing reproductive status (Campbell & Gibson, 2008). Cycle lengths of captive and free-ranging spider monkeys fall consistently between 20 and 24 days, with menstrual bleeding present over 2-4 days. However, this is not always externally visible and therefore cannot be relied on as a visual indicator of female reproductive status (Campbell, et al., 2001).

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