Social and hormonal mechanisms underlying male reproductive strategies in black howler monkeys (Alouatta pigra).

We investigated the social and hormonal mechanisms underlying male reproductive strategies in two multimale-multifemale groups of black howler monkeys (Alouatta pigra) during a 14-month study in Palenque National Park, Mexico. Fecal glucocorticoid (fGC) and androgen (fA) levels were analyzed for 343 fecal samples collected from 14 males during their presence in the study groups. Neither immigrating males nor resident males that remained in the group had elevated fGC and fA levels during 11 observed male migration events, suggesting that competition over group membership was not associated with variation in the fecal hormonal levels of males. Instead, fGC and fA levels were significantly higher in males who maintained a central position in the group and had almost exclusive access to fertile females than in other resident males. These "central" males were responsible for maintaining close spatial associations and cultivating strong affiliative relationships with cycling, sexually active females but not with noncycling, sexually inactive females. "Noncentral" males did not form strong social relationships with either cycling or noncycling females and had no or very few mating opportunities. Our findings suggest that male black howler monkeys compete nonaggressively by fostering relationships with cycling females and that the elevated fGC levels of central males may be indicative of the social challenges involved in their indirect competition.

Male reproductive strategies in new world primates.

Patterns of three variables of reproductive strategies in male New World primates are examined: (i) how males obtain access to potential mates; (ii) how males obtain actual mating opportunities; and (iii) how males affect infant survival and female reproductive success. Male opportunities to associate with females, whether by remaining in their natal groups, dispersing and forming new groups, or dispersing and taking over or joining established groups, are strongly influenced by local population densities and correlate with female reproductive rates and the extent of female reproductive seasonality and synchrony. Differences in male mating success are affected by female accessibility, whether male-male and male-female relationships are hierarchical or egalitarian, and whether female reproduction is seasonally restricted. Patterns of male behavior toward infants, characterized as active assistance, overt interference, or benign tolerance, appear to co-vary with differences in the degree to which males can affect female reproductive rates.These qualitative analyses suggest that the reproductive strategies of male New World primates can be classified along a continuum ranging from conservative to daring depending on whether female reproductive rates are relatively slow or fast and whether reproduction is strongly or weakly linked to seasonal ecological variables. Males adopt the conservative strategy of staying in their natal groups, forfeiting exclusive mating opportunities, and treating infants with tolerance when female reproduction is constrained by ecological factors. Conversely, males adopt the more daring strategy of dispersing and competing when potential payoffs through their ability to affect female reproduction are high.

Predicting primate responses to "Stochastic" demographic events.

Comparative approaches in contemporary primate behavioral ecology have tended to emphasize the deterministic properties of stochastic ecological variables. Yet, primate responses to ecological fluctuations may be mediated by the interactions among demographic processes at the levels of individuals, groups, and populations. In this paper I examine long-term data collected from June 1982-July 1998 on one expanding group of muriquis (Brachyteles arachnoides) at the Estação Biologica de Caratinga, Minas Gerais, Brazil to explore the demographic and life history correlates of reproductive seasonality and skewed infant sex ratios. Variation in the size of annual birth cohorts (≥2 infants) was positively related to variation in the annual distribution of births (r (s)=0.96,n=10,p<0.01), indicating the importance of considering the effects that the number of reproductive females may have on interpretations of reproductive seasonality. The female-biased infants sex ratio documented from 59 births was attributed exclusively to multiparous mothers. Primiparous mothers produced comparable numbers of sons (n=6) and daughters (n=7), and were increasingly likely to produce daughters with each subsequent reproductive event. Seven of the 11 females that have produced≥3 infants to date exhibited biases in favor of daughters whereas only 1 was biased in favor of sons. Variation in female sensitivity to local resource competition at different stages of their life histories may account for the female-biased infant sex ration in this population.

Atelinae adaptations: behavioral strategies and ecological constraints.

Comparisons between the four genera that make up the Atelinae reveal two distinct behavioral patterns, one in which energy expenditure is minimized (Alouatta) and one in which energy intake is maximized (Lagothrix, Ateles, and Brachyteles). Among the atelins, Lagothrix and Ateles devote over 75% of their annual feeding time to fruit, while Brachyteles devotes between 50% and 67% of their feeding time to leaves. Pronounced seasonality in the Atlantic coastal forest inhabited by Brachyteles may be responsible for its more folivorous diet. Alouatta falls in the body size range of Lagothrix and is much smaller than Ateles and Brachyteles. Nonetheless, Alouatta is more folivorous than sympatric atelins. The atelins also share a rapid, suspensory mode of locomotion that appears to enable them to minimize travel time between widely dispersed fruit sources. Alouatta, by contrast, employs a slower, but more energetically efficient, quadrupedal locomotion. Ranging patterns among the Atelinae are consistent with both diet and locomotor abilities: Atelins travel daily distances up to 5,000 m; Alouatta ranges are much shorter. Further distinctions are evident in Atelinae grouping patterns. Alouatta remains in small cohesive groups that occupy home ranges less than 60 ha in size. Both Lagothrix and Ateles have large groups that fission to reduce the costs of intragroup feeding competition when preferred fruits occur in small patches within much larger community ranges. While greater reliance on low-energy foods such as leaves may release Brachyteles from similar competitive constraints, their tendency toward fluid grouping associations is consistent with the pursuit of a frugivorous diet.

Effects of patch size on feeding associations in muriquis (Brachyteles arachnoides).

Data were collected on one group of muriquis, or woolly spider monkeys (Brachyteles arachnoides) during a 14-month study at Fazenda Montes Claros, Minas Gerais, Brazil to examine the effects of food patch size on muriqui feeding associations. Muriqui food patches were larger than expected from the availability of patch sizes in the forest; fruit patches were significantly larger than leaf patches. Feeding aggregate size, the maximum number of simultaneous occupants, and patch occupancy time were positively related to the size of fruit patches. However, a greater number of individuals fed at leaf sources than expected from the size of these patches. Adult females tended to feed alone in patches more often than males, whereas males tended to feed in single-sexed groups more often than females. Yet in neither case were these differences statistically significant.

Behavioral and endocrine characteristics of the reproductive cycle in wild muriqui monkeys, Brachyteles arachnoides.

The analysis of fecal ovarian steroids provides a powerful noninvasive method to obtain insights into ovulatory cycles, gestation length, and the timing of sexual interactions relative to the periovulatory period in wild primates. Techniques developed to collect and assay feces from free-ranging muriqui monkeys (Brachyteles arachnoides) for estradiol and progesterone yield the first explicit reproductive data on this species, and provide the first opportunity to evaluate the timing of observed copulations with muriqui ovarian cycles. Hormonal profiles from seven females indicate average cycle lengths of 21.0 +/- 5.4 days (n = 20). Females conceived after 3-6 ovulatory cycles. Gestation length averaged 216.4 +/- 1.5 days for the five females for which conception cycles were sampled. Discrete copulation periods spanned an average of 2.1 +/- 1.2 days (n = 29), with intervals between these concentrated periods of copulations averaging 15.6 +/- 6.7 days (n = 20). There were no significant differences among females in cycle lengths, copulation period lengths, or copulation interval lengths. Ejaculation was visible following 71.8 +/- 26.7% of copulations during the females preovulatory periods. All females copulated outside the periovulatory period. The proportion of copulation days outside the periovulatory period was slightly greater (p = 0.08) for primiparous females (64.8 +/- 28.3%) than for multiparous females (28.7 +/- 19.7%).

Timing of births in sympatric brown howler monkeys (Alouatta fusca clamitans) and northern muriquis (Brachyteles arachnoides hypoxanthus).

We monitored the birth patterns of sympatric brown howler monkeys (Alouatta fusca clamitans) and northern muriquis (Brachyteles arachnoides hypoxanthus) during a 4-yr period from October 1996 to August 2000 at the Estação Biológica de Caratinga, Minas Gerais, Brazil. Brown howler monkey births (n = 34) occurred throughout the year, and birth frequencies did not differ between rainy and dry season months. The aseasonal birth patterns of the howler monkeys differed significantly from the dry season concentration and dry month peak in muriqui births (n = 23). We found no effects of infant sex or the number of females on interbirth intervals (IBIs) in our 10 howler monkey study troops. IBIs of brown howler monkeys averaged 21.2 +/- 2.5 mo (n = 8, median = 21.0 mo), and were significantly shorter following dry season births than rainy season births. Their IBIs and yearling survivorship (74%) were similar to those reported for other species of howler monkeys, but yearling survivorship was much lower than that of muriquis (94%), whose IBIs were more than 12 mo longer than those of the howler monkeys. Our study extends comparative knowledge of birth patterns in Alouatta to a poorly known species, and provides insights into the different ways in which diet and life history may affect the timing of births in large-bodied platyrrhines under the same seasonal ecological conditions.

Seasonal and social correlates of fecal testosterone and cortisol levels in wild male muriquis (Brachyteles arachnoides).

Fecal testosterone and cortisol levels were analyzed from six wild male muriquis (Brachyteles arachnoides) over a 19-month period at the Estação Biológica de Caratinga in Minas Gerais, Brazil, to investigate the hormonal correlates of seasonal sexual behavior and environmental conditions. Group mean testosterone levels based on weekly samples from the six males did not differ between copulatory and noncopulatory periods or between rainy and dry seasons. Cortisol levels did change with copulatory periods, and were significantly higher during the second dry season, when mating continued following an exceptionally heavy rainy season, than during the first dry season, when mating ceased. Males exhibited individual variation in the timing of their hormone shifts relative to their sexual activity, but neither hormone levels nor sexual activity were related to male age. Despite individual differences in the timing of testosterone fluctuations around the onset and offset of the copulatory season, all males exhibited elevated cortisol concentrations following a slight increase in testosterone at the beginning of the copulatory season. Both the lack of significant changes in testosterone levels with the onset of the rainy and copulatory season and the lack of prebreeding increases in cortisol may be related to the low levels of overt aggression displayed by male muriquis over access to mates.

Habitat, density and group size of primates in a Brazilian tropical forest.

Habitats, population densities and group sizes of 5 primate species (Callithrix flaviceps, Callicebus personatus personatus, Cebus apella nigritus, Alouatta fusca clamitans, and Brachyteles arachnoides) were estimated, using the method of repeated transect sampling, in an area of montane pluvial forest in eastern Brazil (Atlantic forest). A. fusca and C. apella had the highest densities in terms of groups and individuals per square kilometer, respectively, while B. arachnoides was least abundant. The highest primate densities were observed in areas of secondary vegetation. Both group sizes and population densities for the 5 species were generally lower at the Reserva Biologica Augusto Ruschi than those reported in other areas of Atlantic forest. Hunting pressure and the different carrying capacity of the habitat are suggested as possible causes for the low number of sightings registered for these species.

Steroid excretion during the ovarian cycle in captive and wild muriquis, Brachyteles arachnoides.

Urine, feces, and copulation frequency were collected from two captive muriqui females, Brachyteles arachnoides, at the Centro de Primatologia do Rio de Janeiro following the resumption of postpartum ovarian cycles. Fecal steroid profiles from seven wild muriqui females at the Estação Biologica de Caratinga, Minas Gerais, Brazil, were compared to the captive females to determine the approximate patterns of steroid excretion relative to the urinary LH peak. Hormonal profiles from one of the captive female muriquis revealed a discrete urinary LH peak. For this female, fecal progesterone increased on the same day as the urinary LH peak, while fecal estradiol increased 6 days later and urinary steroids increased 5 days later. For both captive females, the onset of fecal progesterone increase was preceded by the onset of copulations, which occurred during at least a 5-day period. The complete fecal hormonal profiles of the one captive female for which continuos data were available were similar to those found in wild muriqui monkeys, with the onset of an increase in sustained progesterone levels occurring several days prior to the onset of sustained estradiol increase. These patterns suggest that fecal progesterone may be excreted rapidly in this species. The onset of sustained increase in fecal progesterone levels, together with the consistent delay in the onset of the sustained increase in estradiol, may provide the best indicators of the periovulatory period for muriqui females.