Female mating strategies in tufted capuchin monkeys (Cebus apella nigritus)

Leakey Foundation Final Report

Female mating strategies in tufted capuchin monkeys (Cebus apella nigritus) Barbara Tiddi Postdoctoral Scientist, Cognitive Ethology Laboratory, German Primate Center (DPZ), Goettingen, Germany.

Brief Summary The present project investigated female mating strategies in tufted capuchin monkeys (Cebus apella nigritus, synonymous with Sapajus nigritus; Lynch-Alfaro et al., 2012). The specific focus was to determine the extent to which wild tufted capuchin females solve conflicts of reproductive interest with both sexes by exploring the following aspects of female mating strategies: 1) the extent to which female sexual and mating behaviour (i.e., proceptive behaviours and copulations) are hormonally driven; and 2) the adaptive function of female sexual behaviour within the context of intersexual conflict and intrasexual competition. As previously found in a captive group (Carosi et al., 1999), we demonstrated via hormone analysis that female sexual behaviour (hereafter proceptive behaviours) is highly associated with the female fertile phase, and thus our results corroborate the contention that proceptive behaviours among tufted capuchin females are a reliable indicator of ovarian function. Similarly, mating activity was highly concentrated during female fertile periods, resulting in a relatively short window for copulations occurring around the day of ovulation. Thus, we found an overall strong link between female sexual behaviour and progesteron levels. When considering the adaptive function of female proceptive behaviours, such behaviours varied according to the probability of ovulation. In contrast, female proceptivity did not vary with measures of female reproductive quality (e.g., fecundity, age and dominance rank). These findings are in accordance with the graded-signal hypothesis (Nunn 1999), suggesting that females tend to reduce male-imposed constraints (e.g., infanticide) by confusing and biasing paternity. Males responded to these signals by synchronizing their mating effort around the female fertile phase; alpha males in particular intensified their copulations during those days with a high probability of ovulation. Overall, as suggested by Janson (1984), copulations seem to be closely associated to the timing of ovulation more for alpha males than for subordinate males. Finally, although females often overlapped in

their proceptivity, we did not observe any direct aggression between females to gain access to alpha males. Females did not directly interfere with proceptive behaviour and copulations of other females regardless their reproductive status (fertile or non-fertile). Along with a lack of observed direct competition, hormonal analysis revealed that overlaps in proceptive behaviours were associated with peaks in progesterone levels, and thus females may synchronize their cycles rather than their mating activity (e.g., “you mate, I mate” synchrony; Fuertbauer et al., 2011).

Similarly, post-conceptive mating and sexual solicitations rarely occurred, and females in these cases targeted both alpha males and other males in their group. A more detailed test on the functional significance of overlap in female sexual behaviour and of post-conceptive mating is currently on-going.

Brief Summary of Publications We are currently finalizing manuscript preparation of the first part of our Leakey-funded project that focuses on the adaptive value of female sexual signaling and male mating response. We expect to submit this manuscript for publication by early Summer 2014. We will next prepare a manuscript in which we will test whether or not sexual synchrony represents an adaptive response to female-female intrasexual competition. The acquisition of additional funding for related projects allowed us to investigate additional aspects of female reproductive and male mating strategies, which we expect to result in at least two further, related publications.

Detailed description of results Female sexual behaviour and hormone profiles We observed a total of 72 proceptive periods over four mating seasons (2010-2013) in 16 females belonging to our three study groups. Proceptive periods lasted on average 3.7 ± 1.6 days (mean ± SD) ranging from 1 to 8 days. Fecal progesteron profiles allowed us to analyse the association between proceptive periods and female ovarian function in 42 of the 72 proceptive periods. The pattern of excretion of fecal progesterone metabolites is illustrated in Fig. 1, in which the daily mean values of metabolites from all females were used to describe a composite hormone profile. Measurements of the progesterone metabolites showed a clear cyclical pattern of secretion for all females with follicular and luteal phases of the cycle clearly distinguishable.

Although the number of cycles that could be measured from one progesterone surge to the next was low (n=13), the average length of a complete ovarian cycle was estimated around 21.5 Âą 4.1 days (ranging from 16 to 30 days). When considering the timing of ovulation, this seems to occur in the majority of the observed proceptive periods during the last day (Fig. 2). As expected, female sexual proceptivity was significantly associated with female fertile phase. Specifically, both proceptive behaviours and estrous calls were positively associated with female fertile phase (respectively for proceptive behaviours: N=378 observation days on 16 focal females, P<0.001; and for estrous calls: N=378, P<0.001).

Intersexual conflict Male constraints on female mating behaviour Overall, we did not observe any case of direct harassment by males towards proceptive females.

Females on rare occasions were seen injured during the days around their proceptive periods (5 observed cases of injures during 72 proceptive periods); however the context in which these injuries occurred was unclear, and it is yet to be determined if such injuries occur more often during proceptive periods than would be expected by chance. A focus on the relative role of both sexes during sexual interaction revealed that females commonly (if not uniquely) initiated the sexual interactions; similarly, females during their proceptive periods were actively responsible for maintaining proximity to the target male (0.82 of female-male dyads had a positive Hinde index value, indicating that females actively maintained proximity to males more often than vice versa). Dyadic Hinde index values did not change in relation to the intensity of female proceptivity (intensity measured as proportion of time spent soliciting alpha males), which varies with the timing of ovulation and thus potentially served to convey this information to males.

Female sexual strategies as a response to male-imposed constraints Our results showed that tufted capuchin females tend to manipulate both the information available to males (to bias their paternity confidence), and the distribution of paternity among group males by mating promiscuously during their periovulatory periods (Fig. 3). In particular, we found that female proceptive behaviours, excluding the production of estrous vocalizations, varied significantly in relation to the day of ovulation, with the proportion of time spent

soliciting males being higher on the days immediately prior to ovulation relative to other days within the female fertile window (periovulatory period or POP; see Fig. 4). Interestingly, this pattern is in accordance with the idea that different signals may provide information on ovulation with different precision in both human and non-human primates (e.g., Fischer et al., 2011; Higham et al., 2008). In addition, when testing whether female proceptivity potentially provides information on female reproductive quality (Pagel, 1994), no significant relationship was found between female proceptivity (tested as either proportion of time spent soliciting the male target or the duration of proceptive periods) and measures of female reproductive quality (e.g., fecundity, age and dominance rank). The adaptive value of this sexual signal system may be explained in the light of two crucial characteristics of tufted capuchins. First, females face a high risk of infanticide that is linked to within-group male takeovers, with the replacement of the top ranking male as main cause of infant mortality during the first 8 months after birth (RamirezLlorens et al., 2007; Janson et al., 2012). In addition, alpha males in this species exercise a central role in both feeding and social contexts (Janson, 1985; Tiddi et al. 2011); therefore females, by signaling and mating with alpha males at the time of ovulation, may accrue from these males direct and/or indirect benefits.

Intrasexual competition Direct female-female aggression was rarely observed during the study period, and was not seen in the context of mating or sexual proceptivity by females. Thus females, despite targeting the same male, do not seem to compete directly by interfering with other femalesâ&#x20AC;&#x2122; solicitations or copulations, regardless of their reproductive status. Female proceptivity overlapped with that of other females to some extent (43 out of 167 observed days of proceptivity were characterized by more than one proceptive female), and in general, females tended to not simultaneously target the alpha male by soliciting other group males (N=8 days of proceptivity in which both females targeted the alpha males). Further analyses are currently focusing on whether overlap occurs more or less often than expected by chance, and on addressing the extent to which partner choice during periods of overlap is the result of several possible female mating strategies, including paternity confusion, or is instead a result of preferences by the alpha male for particular females.

Works cited: Carosi, M., Heistermann, M., & Visalberghi, E. (1999). Display of proceptive behaviors in relation to urinary and fecal progestin levels over the ovarian cycle in female tufted capuchin monkeys. Hormones and Behavior, 36, 252-265.

Fischer, J., Semple, S., Fickenscher, G., Juergens, R., Kruse, E., Heistermann, M., Ofer Amir, O. (2011) Do women’s voices provide cues of the likelihood of ovulation? The importance of sampling regime. Plos One, e24490.

Fuertbauer, I., Mundry, R., Heistermann, M., Schuelke, O., Ostner J. (2011) You mate, I mate: Macaque female synchronize sex not cycles. Plos One, e26144.

Higham, J.P., Semple, S., MacLarnon, A., Heistermann, M., Ross, C. (2009). Female reproductive signaling, and male mating behavior, in the olive baboon. Hormones and Behavior, 55, 60-67.

Janson, C.H. (1984) Female choice and mating system of the brown tufted capuchins Cebus apella. Zeit Tierpsychol 65:177-200.

Janson, C.H. (1985) Aggressive competition and individual food consumption in wild brown capuchin monkeys (Cebus apella). Behavioral Ecology and Sociobiology, 18, 125-138 Janson, C.H., Baldovino, M.C., Di Bitetti, M.S. (2012) The group life cycle and demography of brown capuchin monkeys (Cebus [apella] nigritus) in Iguazú National Park, Argentina.

In: Kappeler, P.M., Watts, D.P. (eds) Long-Term Field Studies of Primates. Springer, Heidelberg, pp 185-212.

Lynch-Alfaro, J.W., Boubli, J.P., Olson, L.E., Di Fiore, A., Wilson, B., Gutiérrez-Espeleta, G.A., Chiou, K.L., Schulte, M., Neitzel, S., Ross, V., Schwochow, D., Nguyen, M.T.T., Farias, I., Janson, C.H., Alfaro, M.E. (2012) Explosive Pleistocene range expansion leads to widespread Amazonian sympatry between robust and gracile capuchin monkeys. Journal of Biogeography 39, 272-288.

Nunn, C. L. (1999). The evolution of exaggerated sexual swellings in primates and the gradedsignal hypothesis. Animal Behaviour, 58(2), 229-246.

Pagel, M. (1994). The evolution of conspicuous oestrous advertisement in Old World monkeys.

Animal Behaviour, 47, 1333-1341.

Ramirez-Llorens, P., Di Bitetti, M., Baldovino, M., & Janson, C. (2008). Infanticide in black capuchin monkeys (Cebus apella nigritus) in Iguazu National Park, Argentina. American Journal of Primatology, 70, 473-484.

Tiddi, B., Aureli, F., Schino, G., Voelkl, B. (2011) Social relationships between adult females and the alpha male in wild tufted capuchin monkeys. American Journal of Primatology 73, 812-820.

Progesterone metabolites (µg/g)

Days of the ovarian cycle Figure 1. Mean (± SD) concentration of immunoreactive progesterone metabolites (PregDH) in feces representing 42 ovarian cycles in 16 tufted capuchin females. Individual profiles were centered on the day of fecal progesterone metabolite rise (day 0). The y-axis shows progesterone metabolite concentrations based on the weight of dry feces.

Figure 2. Duration of proceptive periods for 29 ovarian cycles from 14 study females. Only ovarian cycles with detailed sampling collection during proceptivity were considered (time lag between fecal samples < 2 days).

Figure 3. Proportion of group males females were observed to mate with during their proceptive periods. Each number on the x-axis represents a single individual female (N=9). The number of group males range from 3 to 6.

Figure 4. Proportion of time spent performing proceptive behaviors (dark grey) and estrous calls (light grey) in relation to the day of ovulation.