Fernando A. Campos

Between-group variation in female dispersal, kin composition of groups, and proximity patterns in a black-and-white colobus monkey (Colobus vellerosus).

A growing body of evidence shows within-population variation in natal dispersal, but the effects of such variation on social relationships and the kin composition of groups remain poorly understood. We investigate the link between dispersal, the kin composition of groups, and proximity patterns in a population of black-and-white colobus (Colobus vellerosus) that shows variation in female dispersal. From 2006 to 2011, we collected behavioral data, demographic data, and fecal samples of 77 males and 92 females residing in eight groups at Boabeng-Fiema, Ghana. A combination of demographic data and a genetic network analysis showed that although philopatry was female-biased, only about half of the females resided in their natal groups. Only one group contained female-female dyads with higher average relatedness than randomly drawn animals of both sexes from the same group. Despite between-group variation in female dispersal and kin composition, female-female dyads in most of the study groups had higher proximity scores than randomly drawn dyads from the same group. We conclude that groups fall along a continuum from female dispersed, not kin-based, and not bonded to female philopatric, kin-based, and bonded. We found only partial support for the predicted link between dispersal, kin composition, and social relationships. In contrast to most mammals where the kin composition of groups is a good predictor of the quality of female-female relationships, this study provides further support for the notion that kinship is not necessary for the development and maintenance of social bonds in some gregarious species.

Drivers of home range characteristics across spatiotemporal scales in a Neotropical primate, Cebus capucinus

The factors that drive within-species variation in animal space use remain poorly understood. A growing body of evidence suggests that both home range attributes and biological interpretations of the home range may depend fundamentally on the scale of analysis. We utilize a multiscale mixed effects modelling framework to examine how seasonal fluctuations in climate, food resource abundance and group mass affect variance in home range area and the maturity stage of forest used by a group-living Neotropical primate, the white-faced capuchin, Cebus capucinus. Using an 8-year data set representing over 20 000 contact hours, we estimated home ranges for seven social groups at four nested temporal scales and three nested spatial scales using a movement-based kernel method. Group mass was consistently the most important predictor of home range size in our models, and its effects were relatively insensitive to spatial or temporal scale. Mean daily maximum temperature was an influential factor in shaping monthly range area and composition, with hotter weather favouring smaller home range size and increased use of mature evergreen forest. Greater fruit availability was also associated with smaller monthly range area. The effects of temperature and fruit availability were both scale dependent: the impact of both variables was greatest on the core zone. The different study groups showed marked variation in the habitat composition of their home ranges, but in all groups, higher-use zones consisted of older, more evergreen forest. Our study illustrates the complex ecological processes that affect movement behaviour in a Neotropical primate across a range of spatial and temporal scales, highlighting the importance of group mass, climatic seasonality, landscape heterogeneity and dietary shifts in shaping the home range.

Distribution, abundance, and spatial ecology of the critically endangered Ecuadorian capuchin (Cebus albifrons aequatorialis)

Geographically isolated from other C. albifrons taxa found east of the Andes, the Ecuadorian capuchin (Cebus albifrons aequatorialis) is a Critically Endangered primate that survives in a small number of localities in western Ecuador and extreme northern Peru. We assessed 11 forested areas in western Ecuador to determine presence/absence using a combination of on-foot searching and interviews with local informants. C. a. aequatorialis were present at seven of the sites surveyed, four of which represent new presence localities. We carried out extensive censuses of five small, private reserves to obtain estimates of population density and demographic information. We also examined home range characteristics and habitat selection at one well-studied site. Population densities based on absolute counts at these sites ranged from 2-22 individuals/km2 (median = 2.4). Jauneche, a 138 ha isolated fragment reserve with 22 individuals/km2, was a clear outlier. Although we observed some solitary individuals, C. a. aequatorialis live predominantly in multi-male multi-female social groups, with a mean group size of 13.9 (range 5-20). The composition of social groups was typical for Cebus: adult females outnumbered adult males slightly, and groups exhibited relatively high immature to adult female ratios (mean = 1.5). Home ranges were unusually large for the genus (507–561 ha). The capuchins exhibited strongest selection for mature forest near streams, although they also used degraded forest frequently. C. a. aequatorialis faces critical threats in the form of habitat loss, hunting, and harassment by farmers, but we suggest that some remaining populations have the potential to grow if effective protection can be established.

Female sociality and sexual conflict shape offspring survival in a Neotropical primate

Significance In group-living mammals, infants of females with strong social relationships sometimes exhibit higher survivorship than infants of less social females, a finding that holds true in our study population of wild white-faced capuchin monkeys. However, as in many mammals, new alpha male capuchins often kill young infants sired by other males. Our long-term research shows that infants of highly social females are at greater risk of dying or disappearing during periods of alpha male replacements than infants of less social females. These findings indicate that new alpha males are more likely to target the infants of more social, and therefore central, females. Our study provides evidence that female sociality can negatively affect offspring survival by increasing the likelihood of infanticide. Most mammals live in social groups in which members form differentiated social relationships. Individuals may vary in their degree of sociality, and this variation can be associated with differential fitness. In some species, for example, female sociality has a positive effect on infant survival. However, investigations of such cases are still rare, and no previous study has considered how male infanticide might constrain effects of female sociality on infant survival. Infanticide is part of the male reproductive strategy in many mammals, and it has the potential to override, or even reverse, effects of female reproductive strategies, including sociality. Therefore, we investigated the relationships between female sociality, offspring survival, and infanticide risk in wild white-faced capuchin monkeys using long-term data from Santa Rosa, Costa Rica. Female capuchins formed differentiated bonds, and bond strength was predicted by kin relationship, rank difference, and the presence of female infants. Most females formed stable bonds with their top social partners, although bond stability varied considerably. Offspring of highly social females, who were often high-ranking females, exhibited higher survivorship during stable periods compared with offspring of less social females. However, offspring of highly social females were more likely to die or disappear during periods of alpha male replacements, probably because new alpha males are central to the group, and therefore more likely to target the infants of highly social, central females. This study shows that female sociality in mammals can have negative fitness consequences that are imposed by male behavior.

Urine-washing in white-faced capuchins: a new look at an old puzzle

Some primates regularly wash their hands and feet with urine. This behaviour is outwardly similar to scent marking in other mammals, but it differs in that the urine is applied to the bare skin of the hands and feet rather than rubbed into the fur or applied directly onto an object in the environment. Empirical evidence for the functional significance of urine-washing remains inconsistent. We used rigorous statistical methods to examine environmental and social influences on urine-washing behaviour, using 4380 observation hours on five groups of wild white-faced capuchins (Cebus capucinus) in Costa Rica. Urine-washing frequencies were most strongly affected by environmental dryness, both within and between seasons, with markedly less urine-washing during humid conditions. Increased individual activity levels also promoted urine-washing. Among females, urine-washing was less frequent during lactation than during pregnancy and other reproductive states. Among males, urine-washing frequencies were greater in alpha males, who also exhibited a ‘vigorous’ form of urine-washing that may be functionally distinct. During the dry season, 3/5 groups exhibited more urine-washing than expected near fruit trees, but across groups there were no consistent spatial patterns for urine-washing with respect to water resources, home range overlap zones, core areas, inter-group encounter zones, and the home-range periphery. Urinewashing appears to differ fundamentally from common forms of mammalian scent marking. We suggest that its function is primarily mechanical, perhaps to apply a sticky residue to the hands and feet to improve grip on dry, arboreal substrates. Lesser signalling functions may include sexual signalling and resource labelling.

Inbreeding avoidance and female mate choice shape reproductive skew in capuchin monkeys (Cebus capucinus imitator)

Reproductive skew in multimale groups may be determined by the need for alpha males to offer reproductive opportunities as staying incentives to subordinate males (concessions), by the relative fighting ability of the alpha male (tug‐of‐war) or by how easily females can be monopolized (priority‐of‐access). These models have rarely been investigated in species with exceptionally long male tenures, such as white‐faced capuchins, where female mate choice for novel unrelated males may be important in shaping reproductive skew. We investigated reproductive skew in white‐faced capuchins at Sector Santa Rosa, Costa Rica, using 20 years of demographic, behavioural and genetic data. Infant survival and alpha male reproductive success were highest in small multimale groups, which suggests that the presence of subordinate males can be beneficial to the alpha male, in line with the concession models assumptions. None of the skew models predicted the observed degree of reproductive sharing, and the probability of an alpha male producing offspring was not affected by his relatedness to subordinate males, whether he resided with older subordinate males, whether he was prime aged, the number of males or females in the group or the number of infants conceived within the same month. Instead, the alpha males probability of producing offspring decreased when he was the sire of the mother, was weak and lacked a well‐established position and had a longer tenure. Because our data best supported the inbreeding avoidance hypothesis and female choice for strong novel mates, these hypotheses should be taken into account in future skew models.

A Potential Distribution Model and Conservation Plan for the Critically Endangered Ecuadorian Capuchin, Cebus albifrons aequatorialis

Conservation actions that effectively and efficiently target single, highly threatened species require current data on the species’ geographic distribution and environmental associations. The Ecuadorian capuchin (Cebus albifrons aequatorialis) is a critically endangered primate found only in the fragmented forests of western Ecuador and northern Peru, which are among the world’s most severely threatened ecosystems. We use the MAXENT species distribution modeling method to model the potential distribution and environmental associations of Cebus albifrons aequatorialis, using all known presence localities recorded within the last 2 decades as well as 13 climate, topography, vegetation, and land-use data sets covering the entire geographic range of the subspecies. The environmental conditions that our model predicted to be ideal for supporting Cebus albifrons aequatorialis included ≥20% tree cover, mild temperature seasonality, annual precipitation <2000 mm, and low human population density. Our model identified 5028 km2 of suitable habitat remaining, although many of these forest fragments are unprotected and are unlikely to support extant populations. Using the median population density across all sites for which data are available, we estimate the total carrying capacity of the remaining habitat to be 12,500 total individuals. The true number of remaining individuals is likely to be considerably lower due to anthropogenic factors. We highlight four critical regions of high predicted suitability in western Ecuador and northern Peru on which immediate conservation actions should focus, and we lay out clear priorities to guide conservation actions for ensuring the long-term survival of this gravely threatened and little known primate.

Howler monkey foraging ecology suggests convergent evolution of routine trichromacy as an adaptation for folivory

Abstract Primates possess remarkably variable color vision, and the ecological and social factors shaping this variation remain heavily debated. Here, we test whether central tenants of the folivory hypothesis of routine trichromacy hold for the foraging ecology of howler monkeys. Howler monkeys (genus Alouatta) and paleotropical primates (Parvorder: Catarrhini) have independently acquired routine trichromacy through fixation of distinct mid‐ to long‐wavelength‐sensitive (M/LWS) opsin genes on the X‐chromosome. The presence of routine trichromacy in howlers, while other diurnal neotropical monkeys (Platyrrhini) possess polymorphic trichromacy, is poorly understood. A selective force proposed to explain the evolution of routine trichromacy in catarrhines—reliance on young, red leaves—has received scant attention in howlers, a gap we fill in this study. We recorded diet, sequenced M/LWS opsin genes in four social groups of Alouatta palliata, and conducted colorimetric analysis of leaves consumed in Sector Santa Rosa, Costa Rica. For a majority of food species, including Ficus trees, an important resource year‐round, young leaves were more chromatically conspicuous from mature leaves to trichromatic than to hypothetical dichromatic phenotypes. We found that 18% of opsin genes were MWS/LWS hybrids; when combined with previous research, the incidence of hybrid M/LWS opsins in this species is 13%. In visual models of food discrimination ability, the hybrid trichromatic phenotype performed slightly poorer than normal trichromacy, but substantially better than dichromacy. Our results provide support for the folivory hypothesis of routine trichromacy. Similar ecological pressures, that is, the search for young, reddish leaves, may have driven the independent evolution of routine trichromacy in primates on separate continents. We discuss our results in the context of balancing selection acting on New World monkey opsin genes and hypothesize that howlers experience stronger selection against dichromatic phenotypes than other sympatric species, which rely more heavily on cryptic foods.