Amy Lu

A Bruce Effect in Wild Geladas

Avoiding Infanticide In male dominated hierarchies, newly dominant males will sometimes kill resident infants. In lab studies in mice conducted in the 1950s, Hilda Bruce showed that females introduced to an unfamiliar male will terminate their pregnancies, a process subsequently referred to as a Bruce Effect. Roberts et al. (p. 1222, published online 23 February) followed multiple dominance transitions within wild gelada baboons and showed that live birthrate among females previously identified as pregnant within unstable groups was much lower than within stable groups. Furthermore, females that terminated their pregnancies following transitions had a much shorter interbirth interval than those that did not, suggesting a higher overall reproductive success and fitness. Long-term field studies show female monkeys improve their fitness by terminating their pregnancies when a new male becomes dominant. Female rodents are known to terminate pregnancies after exposure to unfamiliar males (“Bruce effect”). Although laboratory support abounds, direct evidence for a Bruce effect under natural conditions is lacking. Here, we report a strong Bruce effect in a wild primate, the gelada (Theropithecus gelada). Female geladas terminate 80% of pregnancies in the weeks after a dominant male is replaced. Further, data on interbirth intervals suggest that pregnancy termination offers fitness benefits for females whose offspring would otherwise be susceptible to infanticide. Taken together, data support the hypothesis that the Bruce effect can be an adaptive strategy for females.

Primate life histories and dietary adaptations: a comparison of Asian colobines and macaques.

Primate life histories are strongly influenced by both body and brain mass and are mediated by food availability and perhaps dietary adaptations. It has been suggested that folivorous primates mature and reproduce more slowly than frugivores due to lower basal metabolic rates as well as to greater degrees of arboreality, which can lower mortality and thus fecundity. However, the opposite has also been proposed: faster life histories in folivores due to a diet of abundant, protein-rich leaves. We compared two primate taxa often found in sympatry: Asian colobines (folivores, 11 species) and Asian macaques (frugivores, 12 species). We first described new data for a little-known colobine (Phayres leaf monkeys, Trachypithecus phayrei crepusculus) from Phu Khieo Wildlife Sanctuary, Thailand. We then compared gestation periods, ages at first birth, and interbirth intervals in colobines and macaques. We predicted that heavier species would have slower life histories, provisioned populations would have faster life histories, and folivores would have slower life histories than frugivores. We calculated general regression models using log body mass, nutritional regime, and taxon as predictor variables. Body mass and nutritional regime had the predicted effects for all three traits. We found taxonomic differences only for gestation, which was significantly longer in colobines, supporting the idea of slower fetal growth (lower maternal energy) compared to macaques and/or advanced dental or gut development. Ages at first birth and interbirth intervals were similar between taxa, perhaps due to additional factors (e.g., allomothering, dispersal). Our results emphasize the need for additional data from wild populations and for establishing whether growth data for provisioned animals (folivores in particular) are representative of wild ones.

Reproductive suppression in female primates: A review

Reproductive performance is the currency of evolution. All things being equal, an organism should reproduce as often as possible. The puzzling questions in evolutionary biology, therefore, are not how and why an organism does reproduce, but rather how and why an organism does not reproduce. It is difficult to understand why any individual, particularly a female, might forestall reproduction when one of the biggest limitations for female mammalian reproduction is time (that is, reproductive lifespan). The answer, now widely cited throughout behavioral ecology is quite simple: Reproductive suppression can be an adaptive strategy.

Reproductive characteristics of wild female Phayre's leaf monkeys.

Understanding female reproductive characteristics is important for assessing fertility, interpreting female behavior, and designing appropriate conservation and captive management plans. In primate species lacking morphological signs of receptivity, such as most colobines, determination of reproductive parameters depends on the analysis of reproductive hormones. Here, we use fecal hormone analysis to characterize cycle patterns (N=6 females) and gestation length (N=7 females) in a group of wild Phayres leaf monkeys (Trachypithecus phayrei crepusculus) in Phu Khieo Wildlife Sanctuary, Thailand. We found that both fecal estrogen (fE) and progestin (fP) levels showed clear biological patterns indicative of ovulation and conception. However, because fP patterns were inadequate in determining the end of the luteal phase, we used fE rather than fP patterns to delineate menstrual cycle parameters. We found a mean cycle length of 28.4 days (N=10), with follicular and luteal phases of 15.4 (N=10) and 12.5 days (N=14), respectively. On average, females underwent 3.57 (N=7) cycles until conception. Average gestation length was 205.3 days (N=7), with fE levels increasing over the course of pregnancy. Overall, the reproductive characteristics found for Phayres leaf monkeys were consistent with results for other colobine species, suggesting that fecal hormone monitoring, particularly for fE metabolites, can provide useful reproductive information for this species. Am. J. Primatol. 72:1073–1081, 2010.

Juggling priorities: female mating tactics in Phayre's leaf monkeys.

Extended sexual receptivity in primates is thought to facilitate paternity confusion, thus decreasing the risk of infanticide. However, females might also provide some indication of ovulation to attract preferred males during fertile periods. We examined female mate preferences across defined receptive periods (N = 59) in a group of wild Phayres leaf monkeys (Trachypithecus phayrei crepusculus) at Phu Khieo Wildlife Sanctuary (February–September 2006; 2,603 contact hours). The group contained seven cycling adult females and three reproductively active males (one adult and two adolescents). We predicted that females would prefer the adult male during periovulatory (POP) receptive periods, but the adolescent males during nonperiovulatory (NPOP) and postconceptive (PC) periods. We collected focal and ad libitum data on sexual and agonistic behaviors to determine female preferences and male awareness of female fertility. We also determined the degree of mating overlap to assess if males were capable of monopolizing females. Our results indicate that females were more frequently proceptive and receptive toward the adult male during POP. By contrast, females were more proceptive and receptive toward one of the adolescent males during PC periods, but rarely interacted with the other adolescent. Patterns of attractivity and agonism across receptive periods suggested that the adult male could detect fertility, while the preferred adolescent could not. Finally, we found a high degree of overlap in total receptive period days, but a low degree of overlap in POP receptive days, suggesting that the adult male might have monopolized females, especially since he seemed to be aware of female fertility. Although these results suggest that females provide some information on ovulation, they also suggest that females attempt to confuse paternity, perhaps capitalizing on male differences in the ability to detect fertility. Am. J. Primatol. 74:471‐481, 2012.

Phytochemicals and reproductive function in wild female Phayre's leaf monkeys (Trachypithecus phayrei crepusculus).

Female reproduction is known to be influenced by food availability and its impact on energetic status. However, emerging evidence suggests that the phytochemical content of food may also be an important factor. Here, we investigated this hypothesis, presenting 20 months of data on fecal progestin (fP) patterns in wild female Phayres leaf monkeys (Trachypithecus phayrei crepusculus). We examined whether (a) the availability of Vitex (a plant known to contain phytochemicals) might be linked to seasonal fP levels, (b) fP levels were associated with female reproductive performance, and (c) reproductive performance might also be linked with energetic status (as measured by physical condition). We collected fecal samples (N=2077) from 10 adult females to analyze estrogen (fE) and progestin (fP) metabolites, behavioral data from 7 cycling females to determine receptivity, and monthly data on Vitex availability and female physical condition. Seasonally elevated fP levels were found in all females, with higher levels when Vitex leaves and fruits were abundant. During the period of high progestins, females had longer cycle lengths and follicular phases, while receptive periods did not change. Nevertheless, when ovulations occurred, females were more likely to conceive. On the other hand, conceptions were also more likely when physical condition was improving, suggesting that the effects of phytochemicals and energetic status on reproduction may be difficult to separate. Although our results support the predicted effects of Vitex on endocrine and reproductive function, future studies with detailed feeding data and chemical analyses of plants are needed to confirm this finding.

Effects of age, reproductive state, and the number of competitors on the dominance dynamics of wild female Hanuman langurs

Female dominance hierarchies form as a result of individual differences in resource holding potential, social processes such as winner-loser effects or coalitions, and ecological conditions that favor contest competition. Contest competition is assumed to result in despotic, nepotistic, and stable hierarchies. However, female Hanuman langurs are exceptions to this pattern, with data from provisioned populations indicating despotic, yet individualistic (age-inversed) and unstable hierarchies despite strong within-group contest. We present data on hierarchical linearity, stability, and the determinants of female rank and rank change in a population of unprovisioned, wild Hanuman langurs (Ramnagar, Nepal). Based on 12 490 dyadic displacement interactions collected over 5 years from a medium-sized group (P group, mean = 6.9 adult females) and a large group (O group, mean = 13.6 adult females), stable periods (P group, N = 14 ; O group, N = 31 ) were identified and dominance hierarchies constructed with the program MatMan. In both groups, dominance hierarchies were linear ( p < 0 . 05 ), with high directional consistency within dyads. Rank was negatively related with age, while the presence of maternal kin had no effect. Reproductive state affected dominance rank in the larger group, with females ascending the hierarchy prior to conception, and dropping in rank after birth. Ranks were unstable, with group size and the number of juvenile females driving the effect (GLMM, p < 0 . 001 ). These results match earlier findings for provisioned populations. In female Hanuman langurs, competition seems most intense around conception and during gestation, creating rank instability, which is further exacerbated by the number of adult as well as maturing females.

Growth trajectories in wild geladas (Theropithecus gelada).

Life history and socioecological factors have been linked to species‐specific patterns of growth across female vertebrates. For example, greater maternal investment in offspring has been associated with more discrete periods of growth and reproduction. However, in primates it has been difficult to test such hypotheses because very few studies have obtained growth measurements from wild populations. Here we utilize a promising noninvasive photogrammetric method—parallel lasers—to examine shoulder‐rump (SR) growth in a wild primate, the gelada (Theropithecus gelada, Simien Mountains National Park, Ethiopia). In this species, a graminivorous diet coupled with high extrinsic infant mortality risk suggests that maternal investment in neonates is low. Therefore, in contrast with other closely related papionins, we expected female geladas to exhibit less discrete periods of growth and reproduction. For both sexes, we compared size‐for‐age patterns (N = 154 females; N = 110 males) and changes in growth velocity relative to major life history milestones. Female geladas finished 88.5% of SR growth by first sexual swelling, and 97.2% by first reproduction, reaching adult body size by 7.72 years of age. Compared to closely related papionins, gelada females finished more growth by first reproduction, despite producing relatively small, and presumably “cheap,” neonates. Male geladas finished 85.4% of growth at dispersal, and 96.0% at estimated first birth. Contrary to other polygynous primates, males are larger than females because they grow for a longer period of time (not because they grow faster), surpassing females around 6 years of age when female growth slows. Our results demonstrate that parallel lasers are an easy and promising new method that can be used to construct comprehensive life history perspectives that were once out of reach for wild populations. Am. J. Primatol. 78:707–719, 2016.

The Goldilocks Effect: Female geladas in mid-sized groups have higher fitness

The cost-to-benefit ratio of group-living is thought to vary with group size: individuals in “optimal” groups should have higher fitness than individuals in groups that are too large or small. However, the relationship between group size and individual fitness has been difficult to establish, a gap we address here in the gelada. We demonstrate group size effects on the production of surviving offspring and on female mortality rates, which are largely explained by group-size variation in infanticide risk and foraging competition. We also identify a mechanism by which females may alter group size: in large groups, females groomed with less than half of their group, increasing the likelihood of fissions. Our findings provide insight into how and why group size shapes fitness in long-lived species.