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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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For severe aggression (Figure 5.2B) a significant difference was found over time for actors [F (1, 2) = 3.264, P.05, AIC = 778.694] and for targets [F (1, 2) =

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6.909, P.05, AIC = 500.228], with post hoc test showing a significant increase in cortisol levels from the week prior to the day of aggression before returning back to pre aggression levels in the week following for both roles. The adult male (Ric) was identified as the actor for 10 of the 23 incidences of severe aggression. Of the 16 aggressive events between adults, where the target was known, the youngest adult female (Fay) was the recipient on eight occasions.

For lethal aggression there was also a change in cortisol levels seen over time (Figure 5.2C). For the bystander role cortisol levels showed a significant difference over time [F (1, 2) = 6.928, P.01, AIC = 142.531], with post hoc tests showing a significant increase on the day after the event against the week before. For actors levels of cortisol showed an increase in the week following the incident although this was not significant. The targets of the lethal aggression were juvenile males and no data were available for them as their data points were not available for the day of the aggression or the week after. The adult male was the actor for both cases of lethal aggression.

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* Figure 5.2 Mean values of cortisol over time for the actor, target and bystanders for the three aggressive events of A) minor; B) severe and C) lethal aggressive events.

Vertical lines depict standard errors of the means. See text for explanation of significant effects.

5.7.2 Reproduction A total of 56 events and 1732 samples were used in the analyses of reproduction (see Table 5.5 for summary). When I examined the impact of different categories of reproduction on the cortisol values for the female, adult male, and other adult females the week prior to, the day of and the week following the reproductive events a three way interaction of type, role and time provided the best fitting model with the lowest AIC value. [F (1, 26) = 2.869, P.0001, AIC = 9632.391]. For the other adult females category values were calculated using the means of the individual animals (see Table 5.6).

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Each type of reproductive event was again analysed separately to determine the reasons for the differences. For ovulation (Figure 5.3A) there was again no effect of time with cortisol levels similar in the week prior, the day of and the week following the ovulation event, nor was there any difference in role. There were also no effects of time or role on levels of cortisol for mating events (Figure 5.3B).

Finally for the birth events (Figure 5.3C) cortisol levels changed significantly over time [F (1, 2) = 5.520, P.01, AIC = 861.126], with post hoc tests showing levels significantly higher in mothers than in the male or other adult females for the week prior to birth. There was also a trend for higher cortisol in mothers prior to the birth, which decreased following birth and returned to baseline levels in the week following. Cortisol levels for the other adult females also changed significantly over time [F (1, 2) = 6.108, P.005, AIC = 1238.698], with post hoc tests showing levels significantly higher on the day of the event, compared to the week prior or the week following the event. Cortisol levels for the male did not fluctuate significantly across the three time periods.

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Figure 5.3 Mean values of cortisol over time for the female, male and other adult females for the three reproduction events of A) ovulation; B) matings and C) birth.

Vertical lines depict standard errors of the means. See text for explanation of significant effects.

5.7.3 Separation A total of 15 events and 536 samples were used in the analyses of separation (see Table 5.7 for summary). When I examined the impact of the three different types of separation on the cortisol values for the separated/reintroduced individuals and the bystanders over time a two way interaction of type of event and time provided the best fitting model with the lowest AIC value. [F (1, 7) = 2.375, P.021, AIC = 2181.822]. This meant combining all the individual values and these were calculated using the means of the individual animals (see Table 5.8).

For temporary separation (Figure 5.4 A) there was a trend for a reduction in cortisol levels was seen in the group the week prior to and the week following temporary separation, although the levels were very low. There was also a trend for a reduction in cortisol levels for the group for longer than 24hrs from the week prior (Figure 5.4 B), to the day of and in the week following separation. Again these were at low levels when compared to other events. No pattern of change in cortisol levels were seen during reintroduction events (Figure 5.4 C).

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Figure 5.4 Mean values of cortisol over time for all individuals for the three separation events of A) temporary; B) separation and C) reintroduction.

Vertical lines depict standard errors of the means. See text for explanation of significant effects.

5.8 Discussion The results of the present study revealed, for this group of zoo-housed spider monkeys, that different levels of stress response occurred following the three different social contexts of aggression, reproduction and separation. In particular, aggression was more stressful as measured by urinary cortisol than either reproduction or separation.





When I examined aggression only, I found that the patterns of aggression reported in Chapter 4 also occurred in the Chester Zoo group of spider monkeys.

Firstly, the predicted pattern of aggression with adult males directing minor aggression towards adult females and severe and lethal aggression towards sub adult males was supported (Asensio, et al., 2008; Aureli & Schaffner, 2008; Campbell, 2003, 2006b; Fedigan & Baxter, 1984; Slater, et al., 2008; Vick, 2008). The majority of the incidents of aggression were by one adult male (Ric). He was responsible for the majority of minor aggressive events, the vast majority of which were directed toward adult females, which is similar to observations found in wild spider monkeys (Fedigan & Baxter, 1984; Slater, et al., 2009). In addition, severe cases of aggression were carried out predominantly by Ric to other adult females, which have not been previously reported. There were, however, incidents of female-female aggression, in particular to the youngest adult female, which also corresponds to patterns of older females targeting younger, newly immigrant females in the wild (Asensio, et al., 2008; Aureli & Schaffner, 2008). Finally, both cases of lethal aggression were by Ric towards juvenile males. Although this was unexpected as Ric was related either as half brother or father to both the males, the pattern of older males targeting and killing younger, potentially related males is also documented in wild populations (Campbell, 2006b; Valero, et al., 2006) and has been reported in other zoo populations of spider monkeys (Chapter 4).

The second prediction that severe cases of aggression would lead to a higher stress response in the targets of aggression was also supported. The LMM was used to demonstrate the best fitting explanation of the data by testing the model that best explains the variance of the dependent variable while controlling for variation due to repeated measures of individuals (Tabachnik & Fidell, 2007). I found a three way interaction of severity, role and time as the best fitting model. For minor aggression no significant fluctuations in cortisol occurred across time or role. For severe aggression, however, a significant increase occurred in both actors and targets of the aggression on the day of the event. However, the cortisol levels returned to prior levels in the week following severe aggression. As cortisol responses were relatively short lived, providing that the events do not occur on a regular basis, such incidents should be of no concern for the welfare of the individual (Moberg, 2000). I also predicted that for severe aggression, no changes in cortisol would be detected in the bystander which was also supported. These results are similar to those found by Smith and French (1997b) who also looked at role in aggression in marmosets. They found elevated levels of cortisol in both the targets and actors immediately after aggression between siblings, which then returned to baseline within the week. No increases were reported in bystanders.

It was predicted that cases of severe or lethal aggression would be expected by adult males towards sub adult males (Campbell, 2006b; Valero, et al., 2006). It would also be expected that the largest increase in cortisol would be associated with the most severe cases of aggression (Ostner, et al., 2008), with severe and lethal aggression associated with the largest increased levels of cortisol. The largest stress response occurred in bystanders following lethal aggression on the day of the event compared to levels the week prior to the event and, with levels remaining high compared with levels prior to the aggressive event. Although no increase was seen in the actor on the day of the event, an increase was seen in the following week. Some caution may be needed in interpreting these results as this category had the lowest sample size (37 samples) and the high cortisol level for the role of bystander on the day following the event was driven by the high stress response from a mother of a killed infant. Her value on the day following aggression was 67.27 ug cort/mg creat, compared to the mean rate of 1.848 ug cort/ mg creat for other bystander females.

Such a response is not surprising as the highest stress responses in female primates are known to occur when they are separated from their infants or if infants die (Boccia, et al., 1995; Engh, et al., 2006; Maestripieri, et al., 2008).

Higher cortisol levels have been associated with levels of aggression in a number of primate studies in captivity (Eberhart, Keverne, & Meller, 1983; T. E.

Smith & French, 1997b) and in the wild (G. M. Barrett, et al., 2002; Beehner, et al., 2005; Cavigelli, et al., 2003; Muller & Wrangham, 2004; Ostner, et al., 2008;

Sapolsky, 1982). While a number of aggressive incidents were recorded in the spider monkey group over the six year study period, overall incidents of aggression were relatively low in comparison to other species of primate (Bernstein, et al., 1983; see Chapter 4).

Regarding reproductive events, the first prediction that ovulation or mating events would be associated with an increase in cortisol was not supported, as neither the male nor the females experienced increased cortisol during either of the events.

In the case of mating, the findings suggest that although the ability to mate in secrecy was compromised, which is a species-specific characteristic (Campbell & Gibson, 2008), this constraint on normal behaviour was not stressful. Given my own observations and those of others (Schaffner & Aureli, personal communication, March 2009) the Chester Zoo spider monkeys do mate in secrecy. On at least five occasions full copulations have been observed in which the male and female form a consortship away from other group members, remain vigilant during the entire event and manage to successfully copulate without visual knowledge of other group members. It may be the case, in other zoo populations, where secrecy is not possible that a higher stress response is more likely. In addition, the secrecy in mating is believed to be a strategy to avoid mating in the presence of other males (Campbell & Gibson, 2008). The population of spider monkeys housed at Chester Zoo has only one adult male, therefore, it may also be the case that in zoo populations with more than one male, the need to engage in secret copulations is more important and therefore a stress response may be more likely in these populations.

The fact that I did not find an increase in cortisol during ovulation was more surprising. Cortisol levels have been shown to change systematically in primates over a non-conceptive ovarian cycle (Saltzman, et al., 1998). Levels of cortisol increase steadily during the follicular phase, peak during the late follicular, periovulatory, and early luteal phases and decline in the mid- to late luteal phase (Saltzman, Schultz-Darken, Scheffler, Wegner, & Abbott, 1994; T. E. Smith & French, 1997b; Ziegler, et al., 1995). However similar findings were found in marmosets (C. kuhlii) by Smith and French (1997b) who found no increases during ovulation which suggests some species variation. The significance and mechanisms of such rises is unknown although it may be affected by the actions of changing levels of other steroid hormones such as progesterone and oestrogen (Beehner, Nguyen, Wango, Alberts, & Altmann, 2006; Saltzman, et al., 1998). That I did not find such increases may be because my measure of ovulation was mainly behavioural and was therefore not precise.

However, in spider monkeys it is difficult to determine where a female is ovulating because the various behaviours associated with ovulation are not necessarily associated with the peri-ovulatory period (Campbell & Gibson, 2008). It has even been suggested that the concept of oestrus does not apply to spider monkey sexual behaviour as matings have been observed when conception is not possible (Campbell, 2007). For a more accurate assessment of the affect of reproductive cycle on cortisol it would be necessary to focus on the sex hormone profile of females.

Further study is also required in this area focusing on using female hormone profiles to determine whether there are more subtle behavioural changes during their ovarian cycle (Campbell & Gibson, 2008).



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