How individual, social, and ecological conditions influence dispersal decisions in male vervet monkeys.

Dispersal between social groups reduces the risk of inbreeding and can improve individuals' reproductive opportunities. However, this movement has costs, such as increased risk of predation and starvation, loss of allies and kin support, and increased aggression associated with entering the new group. Dispersal strategies, such as the timing of movement and decisions on whether to transfer alone or in parallel with a peer, involve different costs and benefits. We used demographic, behavioral, hormonal, and ecological data to examine the causes and consequences of 36 dispersal events from 29 male vervet monkeys (Chlorocebus pygerythrus) at Lake Nabugabo, Uganda. Adult males' secondary dispersal coincided with the conception season in females, and males improved their potential access to females by moving to groups with higher female-to-male sex ratios and/or by increasing their dominance rank. Males that dispersed with a peer had lower fecal glucocorticoid and androgen metabolite levels than lone dispersers. Subadult males were not more likely to engage in parallel dispersals compared to adult males. Dispersal was also used as a mechanism to avoid inbreeding, but changes in hormone levels did not seem to be a trigger of dispersal in our population. Our findings illustrate the complex individual strategies used during dispersal, how many factors can influence movement decisions, as well as the value of dominance and hormone analyses for understanding these strategies.

Major histocompatibility complex class II DR and DQ evolution and variation in wild capuchin monkey species (Cebinae).

The major histocompatibility complex (MHC) is an important gene complex contributing to adaptive immunity. Studies of platyrrhine MHC have focused on identifying experimental models of immune system function in the equivalent Human Leukocyte Antigen (HLA). These genes have thus been explored primarily in captive platyrrhine individuals from research colonies. However, investigations of standing MHC variation and evolution in wild populations are essential to understanding its role in immunity, sociality and ecology. Capuchins are a promising model group exhibiting the greatest habitat diversity, widest diet breadth and arguably the most social complexity among platyrrhines, together likely resulting in varied immunological challenges. We use high-throughput sequencing to characterize polymorphism in four Class II DR and DQ exons for the first time in seven capuchin species. We find evidence for at least three copies for DQ genes and at least five for DRB, with possible additional unrecovered diversity. Our data also reveal common genotypes that are inherited across our most widely sampled population, Cebus imitator in Sector Santa Rosa, Costa Rica. Notably, phylogenetic analyses reveal that platyrrhine DQA sequences form a monophyletic group to the exclusion of all Catarrhini sequences examined. This result is inconsistent with the trans-species hypothesis for MHC evolution across infraorders in Primates and provides further evidence for the independent origin of current MHC genetic diversity in Platyrrhini. Identical allele sharing across cebid species, and more rarely genera, however, does underscore the complexity of MHC gene evolution and the need for more comprehensive assessments of allelic diversity and genome structure.

Comparison of gastrointestinal parasite communities in vervet monkeys.

Globally, habitat degradation is accelerating, especially in the tropics. Changes to interface habitats can increase environmental overlap among nonhuman primates, people, and domestic animals and change stress levels in wildlife, leading to changes in their risk of parasite infections. However, the direction and consequences of these changes are unclear, since animals may benefit by exploiting human resources (e.g., improving nutritional health by eating nutritious crops) and decreasing susceptibility to infection, or interactions with humans may lead to chronic stress and increased susceptibility to infection. Vervet monkeys are an excellent model to understand parasitic disease transmission because of their tolerance to anthropogenic disturbance. Here we quantify the gastrointestinal parasites of a group of vervet monkeys (Chlorocebus aethiops) near Lake Nabugabo, Uganda, that frequently overlaps with people in their use of a highly modified environment. We compare the parasites found in this population to seven other sites where vervet monkey gastrointestinal parasites have been identified. The vervets of Lake Nabugabo have the greatest richness of parasites documented to date. We discuss how this may reflect differences in sampling intensity or differences in the types of habitat where vervet parasites have been sampled.

Social Behaviours and Networks of Vervet Monkeys Are Influenced by Gastrointestinal Parasites.

Substantial research has shown that while some parasite infections can be fatal to hosts, most infections are sub-clinical and non-lethal. Such sub-clinical infections can nonetheless have negative consequences for the long-term fitness of the host such as reducing juvenile growth and the host's ability to compete for food and mates. With such effects, infected individuals are expected to exhibit behavioural changes. Here we use a parasite removal experiment to quantify how gastrointestinal parasite infections affect the behaviour of vervet monkeys (Chlorocebus aethiops) at Lake Nabugabo, Uganda. Behavioural profiles and the structure of nearest neighbour relationships varied significantly. As predicted, after deworming the duration of the resting events decreased, which is consistent with the idea that parasite infections are energetically costly. In contrast to what was predicted, we could not reject the null hypothesis and we observed no change in either the frequency or duration of grooming, but we found that the duration of travel events increased. A network analysis revealed that after deworming, individuals tended to have more nearest neighbours and hence probably more frequent interactions, with this effect being particularly marked for juveniles. The heightened response by juveniles may indicate that they are avoiding infected individuals more than other age classes because it is too costly to move energy away from growth. We consider that populations with high parasite burden may have difficulties developing social networks and behaviours that could have cascading effects that impact the population in general.

Male endocrine response to seasonally varying environmental and social factors in a neotropical primate, Cebus capucinus.

OBJECTIVE: Circannual variation in reproduction is pervasive in birds and mammals. In primates, breeding seasonality is variable, with seasonal birth peaks occurring even in year-round breeders. Environmental seasonality is reportedly an important contributor to the observed variation in reproductive seasonality. Given that food availability is the primary factor constraining female reproduction, predictions concerning responsiveness to environmental seasonality focus on females, with studies of males focusing primarily on social factors. We examined the influence of both environmental and social factors on male fecal testosterone (fT) and glucocorticoids (fGC) in moderately seasonally breeding white-faced capuchin monkeys (Cebus capucinus) in Costa Rica. METHODS: Over 17 months, we collected 993 fecal samples from 14 males in three groups. We used LMM to simultaneously examine the relative effects of photoperiod, fruit biomass, rainfall, temperature, female reproductive status (i.e., number of periovulatory periods, POPs), and male age and dominance rank on monthly fT and fGC levels. RESULTS: Male age and rank had large effects on fT and fGC. Additionally, some hormone variation was explained by environmental factors: photoperiod in the previous month (i.e., lagged photoperiod) was the best environmental predictor of monthly fT levels, whereas fGC levels were best explained by lagged photoperiod, fruit biomass, and rainfall. POPs predicted monthly fT and fGC, but this effect was reduced when all variables were considered simultaneously, possibly because lagged photoperiod and POP were highly correlated. CONCLUSIONS: Males may use photoperiod as a cue predicting circannual trends in the temporal distribution of fertile females, while also fine-tuning short-term hormone increases to the actual presence of ovulatory females, which may occur at any time during the year.

Competing pressures on populations: long-term dynamics of food availability, food quality, disease, stress and animal abundance.

Despite strong links between sociality and fitness that ultimately affect the size of animal populations, the particular social and ecological factors that lead to endangerment are not well understood. Here, we synthesize approximately 25 years of data and present new analyses that highlight dynamics in forest composition, food availability, the nutritional quality of food, disease, physiological stress and population size of endangered folivorous red colobus monkeys (Procolobus rufomitratus). There is a decline in the quality of leaves 15 and 30 years following two previous studies in an undisturbed area of forest. The consumption of a low-quality diet in one month was associated with higher glucocorticoid levels in the subsequent month and stress levels in groups living in degraded forest fragments where diet was poor was more than twice those in forest groups. In contrast, forest composition has changed and when red colobus food availability was weighted by the protein-to-fibre ratio, which we have shown positively predicts folivore biomass, there was an increase in the availability of high-quality trees. Despite these changing social and ecological factors, the abundance of red colobus has remained stable, possibly through a combination of increasing group size and behavioural flexibility.

Hormonal correlates of male life history stages in wild white-faced capuchin monkeys (Cebus capucinus).

Much attention has been paid to hormonal variation in relation to male dominance status and reproductive seasonality, but we know relatively little about how hormones vary across life history stages. Here we examine fecal testosterone (fT), dihydrotestosterone (fDHT), and glucocorticoid (fGC) profiles across male life history stages in wild white-faced capuchins (Cebus capucinus). Study subjects included 37 males residing in three habituated social groups in the Área de Conservacíon Guanacaste, Costa Rica. Male life history stages included infant (0 to <12months; N=3), early juvenile (1 to <3years; N=10), late juvenile (3 to <6years; N=9), subadult (6 to <10years; N=8), subordinate adult (⩾10years; N=3), and alpha adult (⩾10years; N=4, including one recently deposed alpha). Life history stage was a significant predictor of fT; levels were low throughout the infant and juvenile phases, doubled in subadult and subordinate adults, and were highest for alpha males. Life history stage was not a significant predictor of fDHT, fDHT:fT, or fGC levels. Puberty in white-faced capuchins appears to begin in earnest during the subadult male phase, indicated by the first significant rise in fT. Given their high fT levels and exaggerated secondary sexual characteristics, we argue that alpha adult males represent a distinctive life history stage not experienced by all male capuchins. This study is the first to physiologically validate observable male life history stages using patterns of hormone excretion in wild Neotropical primates, with evidence for a strong association between fT levels and life history stage.

Comparing options for pair housing rhesus macaques using behavioral welfare measures.

In a biomedical research environment, research or management procedures may render continuous full contact pairing of rhesus macaques (Macaca mulatta) unfeasible. This study aimed to determine whether separation on a frequent basis or housing in adjacent cages with tactile contact interferes with the behavioral benefits of continuous full contact. Behavioral data (1260 hours) were collected from 32 adult females and 16 adult males housed at two National Primate Research Centers. Subjects were studied in four housing conditions: single housing, full contact pair housing, intermittent contact pair housing, and protected contact housing. After introduction, each pair was housed in each of the three social housing conditions in varying order. Among females, but not males, introducing animals into full and intermittent contact reduced levels of abnormal behavior. There was a trend toward this reduction in protected contact. In both females and males, full and intermittent contact was associated with lower levels of anxiety-related behavior, but protected contact was not. Females spent more time inactive in protected contact than either full or intermittent contact, and males showed a trend toward less inactivity following introduction into full contact. Both sexes showed less affiliation in protected contact compared to the other forms of social housing. Agonistic behavior among females was not affected by housing condition; among males, levels were equivalent in full and intermittent contact but were higher in intermittent than protected contact. Frequent separation of pairs does not appear to detract from the behavioral benefits of pair housing. Separation by a barrier permitting tactile contact is inferior to other forms of social housing but showed modest improvements over single housing nonetheless. This study can guide the provision of social contact to rhesus macaques under conditions restricting pairs from continuous full contact.

The association of intergroup encounters, dominance status, and fecal androgen and glucocorticoid profiles in wild male white-faced capuchins (Cebus capucinus).

Androgens play a role in male reproductive competition, frequently via aggression, while glucocorticoids are associated with the stress response. However, the relationships of these hormones with different sources of competition (intra- vs. intergroup) and dominance status are highly variable. Here, we consider the fecal androgen (fA) and glucocorticoid (fGC) profiles of alpha and subordinate male Cebus capucinus in the context of intergroup competition during a rare period of low intragroup competition (i.e. all females were either pregnant or lactating). Intergroup encounters (IGEs) are a long-term reproductive strategy in male white-faced capuchins, enabling them to assess the composition of neighboring groups. IGEs pose a threat to resident males as these can result in injury or death, loss of dominance rank, group eviction, and group takeovers that are frequently associated with infanticide. From February to July 2007, fecal samples were collected from eight males in three groups of white-faced capuchins in the Santa Rosa Sector of the Área de Conservación Guanacaste, Costa Rica. IGE rate was positively associated with both fA and fGC levels, indicating that IGEs are perceived as reproductive challenges by resident males, and may be associated with elevated metabolic costs. Alpha males sire the majority of group offspring and, accordingly, the threat of IGEs to both future (via rank loss or eviction) and current (via infanticide) reproductive success is greater than for subordinate males. Consistent with this observation, alpha males had higher fA and fGC levels than subordinate males. Given that all females were either pregnant or lactating and pronounced overt intragroup competition was absent, we interpret the difference in hormone profiles of alpha and subordinate males as being primarily associated with variation in the perceived threats of IGEs according to dominance status. Future studies should focus on the interaction of intra- and intergroup competition by examining hormone levels in the presence of periovulatory females.

Rise to power: a case study of male fecal androgen and cortisol levels before and after a non-aggressive rank change in a group of wild white-faced capuchins (Cebus capucinus).

We examined fecal androgen and cortisol levels in three adult male white-faced capuchin monkeys (Cebus capucinus) before and after a non-aggressive rank increase in one habituated group residing in the Santa Rosa Sector of the Área de Conservación Guanacaste, Costa Rica. Fecal samples (n = 116) were collected opportunistically between July 2006 and July 2007. Alpha males had higher mean androgen levels than subordinates, and acquisition of the alpha position was linked to an immediate increase in mean androgens. Cortisol levels also increased in the alpha male after acquisition of his new rank, though this increase was delayed relative to the change in rank. These results indicate that, during a non-aggressive rank change, androgen and cortisol levels in male white-faced capuchins are physiological responses to dominance rank, rather than precursors that facilitate rank acquisition.

Positive reinforcement training moderates only high levels of abnormal behavior in singly housed rhesus macaques.

This study evaluated the application of positive reinforcement training (PRT) as an intervention for abnormal behaviors in singly housed laboratory rhesus macaques at 2 large primate facilities. Training involved basic control behaviors and body-part presentation. The study compared baseline behavioral data on 30 adult males and 33 adult females compared with 3 treatment phases presented in counterbalanced order: 6 min per week of PRT, 20 or 40 min per week of PRT, and 6 min per week of unstructured human interaction (HI). Within-subject parametric tests detected no main or interaction effects involving experimental phase. However, among a subset of subjects with levels of abnormal in the top quartile of the range (n = 15), abnormal behavior was reduced from 35% to 25% of samples with PRT but not with HI. These results suggest that short durations of PRT applied as enrichment for this species and in this context may not in itself be sufficient intervention for abnormal behavior because levels remained high. However, it may be appropriate as an adjunct to other interventions and may be best targeted to the most severely affected individuals.

The effects of observer presence on the behavior of Cebus capucinus in Costa Rica.

We report on the responses of Cebus capucinus in the Santa Rosa Sector of the Area de Conservación Guanacaste, Costa Rica, to the presence of observers over a 4-week period. Study groups were habituated to different degrees: (1) Cerco de Piedra (CP): continuous observations began in 1984; (2) Exclosure (EX): focus of an 18-month study on males from 1998 to 1999; and (3) NBH: never studied/followed but the group frequently encounters researchers. We collected three types of data: group scans (group state was coded as calm or agitated at observer presence), focal animal data (observer-directed behaviors were recorded), and fecal cortisol levels. The two less-habituated groups (NBH and EX) differed significantly from the habituated group (CP) in their behavioral and cortisol responses, and they showed an increase in habituation over the study period (agitation and cortisol levels both dropped). Individuals in NBH also decreased their responses to observers during focal follows; however, at the end of the study the responses of the two less-habituated groups (NBH and EX) remained elevated in comparison to the habituated group (CP), suggesting the need for further habituation. Unlike capuchin groups that rarely encounter humans, NBH and EX never fled from observers and they rarely emitted observer-directed alarm calls. We suggest that the permanence of habituation and the ability to habituate animals passively through a neutral human presence are both important considerations for researchers conducting studies in areas where animal safety from poachers, etc. cannot be guaranteed.