When population growth intensifies intergroup competition, female colobus monkeys free-ride less.

Intergroup aggression often results in the production of public goods, such as a safe and stable social environment and a home range containing the resources required to survive and reproduce. We investigate temporal variation in intergroup aggression in a growing population of colobus monkeys (Colobus vellerosus) to ask a novel question: "Who stepped-up to produce these public goods when doing so became more difficult?". Both whole-group encounters and male incursions occurred more frequently as the population grew. Males and females were both more likely to participate in whole-group encounters when monopolizable food resources were available, indicating both sexes engaged in food defence. However, only females increasingly did so as the population grew, suggesting that it was females who increasingly produced the public good of home range defence as intergroup competition intensified. Females were also more active in male incursions at high population densities, suggesting they increasingly produced the public good of a safe and stable social environment. This is not to say that males were chronic free-riders when it came to maintaining public goods. Males consistently participated in the majority of intergroup interactions throughout the study period, indicating they may have lacked the capacity to invest more time and effort.

Social network dynamics, infant loss, and gut microbiota composition in female Colobus vellerosus during time periods with alpha male challenges.

The gut microbiota of group-living animals is strongly influenced by their social interactions, but it is unclear how it responds to social instability. We investigated whether social instability associated with the arrival of new males and challenges to the alpha male position could explain differences in the gut microbiota in adult female Colobus vellerosus at Boabeng-Fiema, Ghana. First, we used a data set collected during May-August 2007 and May 2008-2009 that consisted of (i) 50 fecal samples from adult females in eight social groups for V4 16S rRNA sequencing to determine gut microbiota composition, and (ii) demographic and behavioral data ad libitum to determine male immigration, challenges to the alpha male position, and infant births and deaths. Sørensen and Bray-Curtis beta diversity indices (i.e., between-sample microbiota variation) were predicted by year, alpha male stability, group identity, and age. Next, we used a more detailed behavioral data set collected during focal observations of adult females in one group with a prolonged alpha male takeover and three cases of infant loss, to create 12-month versus 3-month 1-m proximity networks that preceded and overlapped the gut microbiome sampling period in that group. The long versus short-term networks were not correlated, suggesting temporal variation in proximity networks. In this group, beta diversity among the five adult females was predicted by similarity in infant loss status and short-term (rather than yearly) 1-m proximity ties. Although the mechanism driving this association needs to be further investigated in future studies, our findings indicate that alpha male takeovers are associated with gut microbiota variation and highlight the importance of taking demographic and social network dynamics into account.

All together now: Assessing variation in maternal and nonmaternal handling of wild Colobus vellerosus infants.

Primatologists have a long-standing interest in the study of maternal care and nonmaternal handling (NH) of infants stemming from recognition that early social relationships can have enduring consequences. Though maternal care and NH often include expression of similar behaviors, they are regularly studied in isolation from each other with nonoverlapping terminology, thereby overlooking possible interplay between them and obfuscating potential developmental ramifications that ensue from trade-offs made between maternal (MH) and NH during infancy. To that end, identifying how MH and NH patterns interact and contribute to the total handling (TH) infants receive is a critical first step. We present durational handling data collected from 25 wild Colobus vellerosus infants from 2016 to 2017 and assess the relationships between TH, MH, and NH. Patterns of social affiliation are shaped in part by surrounding context, and therefore, we also assess whether NH and TH differ in their responsivity to various infant and social group characteristics. Ninety-four percent of observed handling was MH, while just 5.5% was NH. Young infants who received more MH (excluding nursing) also received more NH; there was no relationship between the two in older infants. Infants in larger groups participated in more handling of all types. Additionally, NH time was associated with infant sex and group stability. Non-nursing TH time was associated with group stability and infant cohort size. Though NH variation likely confers social-networking advantage, in this population NH is not a major contributor to TH and would not effectively replace reduced MH. The positive association between MH and NH during early infancy suggests that colobus mothers may play a mediating role in shaping infant socialization. This is a first step in elucidating how different forms of handling relate to one another in wild primates and in identifying the impact of handling on infant socialization.

Monkeys who experience more feeding competition utilize social information to learn foraging skills faster.

Animals must learn foraging skills to successfully survive and reproduce but the sources of interindividual variation in learning are poorly understood. For example, there is little consensus on the role motivation plays, even though it is a key factor impacting learning outcomes in humans. Here, we conduct a field experiment on a wild primate to investigate whether an individual's vulnerability to feeding competition impacts their motivation to learn a beneficial foraging technique. We provided a group of monkeys with a food reward (i.e., a half banana) that needed to be retrieved from a box. The monkeys discovered an efficient technique that consistently allowed them to retrieve the banana quickly, decreasing the risk of food loss to competitors. We found that individuals who frequently experienced feeding competition learned this efficient technique significantly faster than individuals who rarely foraged in the presence of a dominant competitor. They appeared to use social learning to learn faster as they were more attentive to the handling techniques others used and improved their foraging skills after opportunities to observe a skilled demonstrator. These findings support that an individual's vulnerability to feeding competition impacts their motivation to learn foraging skills that reduce food loss to competitors.

Non-Reproductive Sexual Behavior in Wild White-Thighed Colobus Monkeys (Colobus vellerosus).

Rare behaviors are often missing from published papers, hampering phylogenetic analyses. Here, we report, for the first time, masturbation and same-sex sexual behavior (SSB) in both male and female black-and-white colobus monkeys. We recorded these behaviors during 32 months of observation (1573 h of focal animal sampling) on Colobus vellerosus collected at the Boabeng-Fiema Monkey Sanctuary in Ghana. Males were observed masturbating and involved in SSB more than females. Subadult males were the age-sex class that engaged in both of these behaviors most often and a third of all SSB observed in young males occurred when they were forming an all-male band (AMB), which are temporally transient social groups in this species. Our data support that masturbation in males may be a sexual outlet for individuals that do not have a current sexual partner, while in females it may function in mate attraction by advertising receptivity. SSB may occur as an evolutionary byproduct but given the temporal clustering of observed events in males prior to AMB formation, our data best support the hypothesis that these behaviors facilitate male-male bonding (i.e., act as social glue). Within AMB's, males engage in coalitionary behavior to take over social groups containing females and strong bonds are important for success and later access to females, which could have selected for SSB in C. vellerosus.

Assessing stress in wild black-and-white colobus monkeys non-invasively.

Analysis of glucocorticoid profiles serves as a valuable, multi-faceted tool for insight into the behavior and physiology of wild populations. Recently, the measurement of fecal glucocorticoid metabolites (FCMs) has exploded in popularity due to its compatibility with noninvasive techniques and remote environments A critical first step is to perform a biological validation to ensure that the assay accurately reflect changes in FCM levels. We use an enzyme immunoassay (EIA) to perform a biological validation on samples collected from two males and six females in a wild population of Colobus vellerosus in response to three naturally occurring potential stressors. We also describe the FCM response pattern in the week following parturition in three females and examine the influence of sex, reproductive state, and time of day on the concentrations of baseline samples collected daily from 13 adult individuals over a period of four months. We validated the assay: FCM levels increase in response to natural stressors with a two-day lag. In the two days surrounding parturition, FMC levels increased. Baseline concentrations were affected by collection time and female reproductive state, with lactating females having lower concentrations than pregnant or cycling females. Thus, we successfully carried out the first validation and characterization of FCMs in a wild African colobine. This will serve as an essential foundation for future studies of C. vellerosus and similar wild primates whose objective is to investigate the role glucocorticoids play in responses to social and ecological challenges.

Joint intergroup aggression in female colobus monkeys (Colobus vellerosus) is associated with grooming bonds, male participation, and group size.

Cooperative home range defense is common in primates, despite a collective action problem that arises when group members benefit from winning the intergroup encounter regardless of whether they participate. The costs associated with this collective action problem may be mitigated by residing in small groups, residing with kin, or by forming strong bonds with group members. The potential to decouple the effects of these variables provided an opportunity to investigate which of these three variables best explains coparticipation in intergroup encounters among adult and subadult female colobus at Boabeng-Fiema, Ghana. Because males are often the main participants, we also investigated the relationship between female-female coparticipation and adult and subadult male participation. We collected intergroup behaviors from 94 adult and subadult individuals in eight groups during 1 year. We quantified female grooming bond strength and approach rates using focal samples. We classified female dyads as close kin (i.e., halfsiblings or more closely related) or nonkin based on partial pedigrees and genotypes generated from 17 STR loci. Female-female coparticipation was higher in dyads with stronger grooming bonds but was not associated with dyadic kinship, approach rate, or age class. Female coparticipation decreased with increasing female group size as expected if there is a collective action problem. Females coparticipated less in groups with more males and male intergroup aggression, possibly because there is less need for female-female cooperation if males are participating in the intergroup encounter. Females in smaller groups may not only benefit from increased female-female cooperation during intergroup encounters, they are also likely to reside with a higher-quality alpha male, both of which may increase the likelihood of winning intergroup encounters. There may be strong selection for facultative female dispersal in populations like the Boabeng-Fiema colobus in which small groups are associated with multiple benefits and cooperation is not affected by kinship.

High levels of infant handling by adult males in Rwenzori Angolan colobus (Colobus angolensis ruwenzorii) compared to two closely related species, C. guereza and C. vellerosus.

Infant handling (holding or carrying) by adult males is rare in mammals; however, high levels have been reported in some primates. Though infant handling is a costly behaviour, there are many benefits that male handlers can accrue. Infant handling by males is most conspicuous in platyrrhines and tends to be uncommon in catarrhines. In the latter species, research on male-infant interactions has focused on low-cost behaviours, such as proximity and grooming. However, to better understand the evolution of infant handling by males, more data on its occurrence across the Primate order are essential, even in species where it is relatively uncommon. We compare the occurrence of infant handling by males in three closely related species of catarrhine: Colobus vellerosus, C. guereza, and C. angolensis ruwenzorii. We collected focal animal samples on infants to quantify infant handling rates and durations, and found that adult male C. a. ruwenzorii handled infants much more frequently and for much longer than males in the other two species. We discuss how C. a. ruwenzorii's unique social organization may explain high levels of infant handling by adult males in this species. More long-term and detailed comparisons of infant handling across species and populations will shed light on how sociality has shaped the evolution of this behaviour in the Primate order.

Premasticated food transfer by wild chimpanzee mothers with their infants: Effects of maternal parity, infant age and sex, and food properties.

Premasticated food transfer, when an individual partially breaks down food through chewing and feeds it to another individual, usually mouth-to-mouth, is described widely across human cultures. This behavior plays an important role in modern humans' strategy of complementary feeding, which involves supplementing maternal milk in infant diets with processed, easily digestible versions of adult foods. The extent to which other primates engage in premasticated food transfer with infants is unclear, as premasticated food transfers have been only occasionally reported in other ape species. We investigated premasticated food transfers in 62 mother-infant pairs of wild chimpanzees at Ngogo, Uganda, as well as unresisted food taking, when mothers passively allow infants to seize food. We evaluated the presence or absence and rates of premasticated food transfer and unresisted food taking relative to maternal parity and infant age and sex and assessed the food species and part used. We found that chimpanzee mothers regularly shared premasticated food with their infants aged between 6 months and 4 years, but they were more likely to share, and more frequently shared, with younger infants. The frequency with which females shared premasticated food may relate to maternal experience, as multiparous females shared premasticated food more often than did first-time mothers, which we did not find with unresisted food taking. Both easy-to-chew, commonly eaten foods and tougher, rarely eaten foods were shared. Premasticated food transfer and unresisted food taking may be infant-rearing strategies to facilitate the transition from a diet of exclusive maternal milk to solid food during early infancy. Premasticated food transfer in particular may provide energetic, immune, or growth benefits to infants through reduced chewing effort and maternal saliva. Given our findings in chimpanzees and earlier reports in other ape species, we suggest that the foundation of complementary feeding, a uniquely hominin strategy, might have been present in a common ancestor shared with the other great apes in the form of premasticated, mouth-to-mouth food transfer by mothers with their offspring.

Divergence in gut microbial communities mirrors a social group fission event in a black-and-white colobus monkey (Colobus vellerosus).

Host behavior and social factors have increasingly been implicated in structuring the composition of gut microbial communities. In social animals, distinct microbial communities characterize different social groups across a variety of taxa, although little longitudinal research has been conducted that demonstrates how this divergence occurs. Our study addresses this question by characterizing the gut microbial composition of an African Old World monkey, the black-and-white colobus (Colobus vellerosus), before and after a social group fission event. Gut microbial taxonomic composition of these monkeys was profiled using the V-4 hypervariable region of the bacterial 16S ribosomal RNA gene, and pairwise-relatedness values were calculated for all individuals using 17 short tandem repeat loci and partial pedigree information. The two social groups in this study were found to harbor distinct microbial signatures after the fission event from which they emerged, while these communities were not divergent in the same individuals before this event. Three genera were found to differ in abundance between the two new social groups: Parabacteroides, Coprococcus, and Porphyromonadaceae. Additionally, although this fission happened partially along lines of relatedness, relatedness did not structure the differences that we found. Taken together, this study suggests that distinct gut microbial profiles can emerge in social groups in <1 year and recommends further work into more finely mapping the timescales, causes, and potentially adaptive effects of this recurring trend toward distinct group microbial signatures.

The influence of male takeovers on female dispersal in Colobus vellerosus.

Male takeovers affect male tenure, female mate choice and ultimately, individual reproductive success in group-living primates. In social systems with female philopatry and high male reproductive skew, male takeovers largely determine female mate choice, whereas in species with female dispersal, females have the option of deserting a new male. We focused on a species with facultative female dispersal to investigate which factors promote female desertion of males after takeover, using 15 cases (12 for which we have complete data on the takeover process and the female dispersal outcome). These cases took place in nine groups of Colobus vellerosus between 2001 and 2013 at the Boabeng-Fiema Monkey Sanctuary, Ghana. Quick takeovers were usually achieved by single adult males and were never followed by female dispersal. Slow takeovers involved several males, and these takeovers were regularly accompanied by female emigration. Infant attacks and infanticide by males occurred during both kinds of takeovers, but females with dependent offspring never dispersed, regardless of whether their infant was attacked or killed by the new male(s). Subadult females, who were not constrained by the presence of infants, dispersed more often after slow takeovers than after quick takeovers. Whether female dispersal post-takeover is an expression of female mate choice, or occurs to avoid the social upheaval surrounding slow takeovers, remains to be investigated. Am. J. Primatol. 79:e22436, 2017. © 2015 Wiley Periodicals, Inc.

Female parity, maternal kinship, infant age and sex influence natal attraction and infant handling in a wild colobine (Colobus vellerosus).

Primate females often inspect, touch and groom others' infants (natal attraction) and they may hold and carry these infants in a manner resembling maternal care (infant handling). While natal attraction and infant handling occur in most wild colobines, little is known about the factors influencing the expression of these behaviors. We examined the effects of female parity, kinship, and dominance rank, as well as infant age and sex in wild Colobus vellerosus at Boabeng-Fiema Monkey Sanctuary, Ghana. We collected data via focal sampling of females in 2008 and 2009 (N = 61) and of infants in 2010 (N = 12). Accounting for the individuals who interacted with our focal subjects, this study includes 74 females and 66 infants in 8 groups. We recorded female agonistic interactions ad libitum to determine dominance ranks. We used partial pedigree information and genotypes at 17 short tandem repeat loci to determine kinship. We knew female parity, infant age and sex from demographic records. Nulliparous females showed more natal attraction and infant handling than parous females, which may suggest that interactions with infants are more adaptive for nulliparous females because they learn mothering skills through these behaviors. Compared to non-kin, maternal kin were more likely to handle infants. Maternal kin may be permitted greater access to infants because mothers are most familiar with them. Handlers may incur inclusive fitness benefits from infant handling. Dominance rank did not affect female interactions with infants. The youngest infants received the most natal attraction and infant handling, and male infants were handled more than female infants. The potential benefits of learning to mother and inclusive fitness, in combination with the relatively low costs of natal attraction and infant handling, may explain the high rates of these behaviors in many colobines.

Familiarity is more important than phenotypic similarity in shaping social relationships in a facultative female dispersed primate, Colobus vellerosus.

Animals often bias affiliative behaviors toward kin, but it is unclear what mechanism most species use to discriminate kin. We investigated if facultative dispersed female primates use phenotype matching and/or familiarity to discriminate female kin. We studied 38 adult female Colobus vellerosus at Boabeng-Fiema, Ghana. We determined dyadic co-residency status and age proximity using long-term demographic data, R-values from 17 short tandem repeat loci, and interaction rates using focal samples collected during one year. Approach rates were not strongly affected by how long females had resided together, which contrasts to the familiarity hypothesis. Females approached and groomed maternal kin more than other females, which supports the mother-mediated familiarity hypothesis. Females did not discriminate paternal half siblings from non-kin, and they did not prefer to interact with females of similar age. Short-term co-resident kin did not bias affiliation toward each other, indicating that female colobus cannot consistently recognize less familiar kin via phenotype matching or that biasing behaviors toward less familiar kin is not beneficial. Despite showing facultative dispersal that may reduce the accuracy of using familiarity as a kin recognition mechanism, female choice of social partners was based on familiarity, which conforms to the pattern observed in many female philopatric primates.

Kinship and similarity in residency status structure female social networks in black-and-white colobus monkeys (Colobus vellerosus).

Kinship shapes female social networks in many primate populations in which females remain in their natal group to breed. In contrast, it is unclear to which extent kinship affects the social networks in populations with female dispersal. Female Colobus vellerosus show routine facultative dispersal (i.e., some females remain philopatric and others disperse). This dispersal pattern allowed us to evaluate if facultative dispersed females form social networks shaped by an attraction to kin, to social partners with a high resource holding potential, or to similar social partners in terms of maturational stage, dominance rank, and residency status. During 2008 and 2009, we collected behavioral data via focal and ad libitum sampling of 61 females residing in eight groups at Boabeng-Fiema, Ghana. We determined kinship based on partial pedigrees and genotypes at 17 short tandem repeat loci. Kinship influenced coalition and affiliation networks in three groups consisting of long-term resident females with access to a relatively high number of female kin. In contrast, similar residency status was more important than kinship in structuring the affiliation network in one of two groups that contained recent female immigrants. In populations with female dispersal, the occurrence of kin structured social networks may not only depend on the kin composition of groups but also on how long the female kin have resided together. We found no consistent support for females biasing affiliation toward partners with high resource holding potential, possibly due to low levels of contest competition and small inter-individual differences in resource holding potential.

The effect of forest fragment characteristics on abundance of Colobus vellerosus in the forest-savanna transition zone of Ghana.

We explore the factors influencing the abundance of Colobus vellerosus in 11 forest fragments [Boabeng-Fiema Monkey Sanctuary and 9 surrounding forest fragments (range: 3.2-190 ha)] in the forest-savanna transition zone of Ghana. We used a 'complete' count for the colobus census in the fragments. We determined the fragment sizes using geographic information system methods and assessed forest fragment quality (tree species richness). Colobus individuals were absent from 4 forest fragments but present in 7 (densities of 0.13/ha-1.63/ha). We modelled colobus density using Poisson regression and selected models based on corrected Akaike information criterion model weights. Fragment size and tree species richness in the fragments were positively associated with colobus density, whereas isolation distance of the forest fragments (range: 20-5,632 m) was negatively associated with colobus density. Our analysis suggests that the isolation distance between the fragments and Boabeng does impede colobus movement. As the colobus populations in Boabeng and Fiema increase, some of the unoccupied fragments may become more attractive to dispersing monkeys. Management measures that aim at increasing tree species richness within fragments, while maintaining some large trees between fragments, might help to increase the occupancy of some of the fragments that currently have no permanent colobus groups.

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.

Use of sleeping trees by ursine colobus monkeys (Colobus vellerosus) demonstrates the importance of nearby food.

Examination of the characteristics and locations of sleeping sites helps to document the social and ecological pressures acting on animals. We investigated sleeping tree choice for four groups of Colobus vellerosus, an arboreal folivore, on 298 nights at the Boabeng-Fiema Monkey Sanctuary, Ghana using five non-mutually exclusive hypotheses: predation avoidance, access to food, range and resource defense, thermoregulation, and a null hypothesis of random selection. C. vellerosus utilized 31 tree species as sleeping sites and the species used differed per group depending on their availability. Groups used multiple sleeping sites and minimized their travel costs by selecting trees near feeding areas. The percentage that a food species was fed upon annually was correlated with the use of that species as a sleeping tree. Ninety percent of the sleeping trees were in a phenophase with colobus food items. Entire groups slept in non-food trees on only one night. These data strongly support the access to food hypothesis. Range and resource defense was also important to sleeping site choice. Groups slept in exclusively used areas of their home range more often than expected, but when other groups were spotted on the edge of the core area, focal groups approached the intruders, behaved aggressively, and slept close to them, seemingly to prevent an incursion into their core range. However, by sleeping high in the canopy, in large, emergent trees with dense foliage, positioning themselves away from the main trunk on medium-sized branches, and by showing low rates of site reuse, C. vellerosus also appeared to be avoiding predation in their sleeping site choices. Groups left their sleep sites later after cooler nights but did not show behavioral thermoregulation, such as huddling. This study suggests that access to food, range and resource defense, and predation avoidance were more important considerations in sleeping site selection than thermoregulation for ursine colobus.

Vigilance in ursine black and white colobus monkeys (Colobus vellerosus): an examination of the effects of conspecific threat and predation.

Vigilance is thought to have evolved as an antipredator defense but, in primates, conspecific threat often better explains this behavior. We examined vigilance in one group of Colobus vellerosus inhabiting the Boabeng-Fiema Monkey Sanctuary in Ghana. We aimed to (1) describe factors affecting vigilance in this population, and (2) examine the importance of predation avoidance and conspecific threat in explaining vigilance patterns. Because of a male takeover preceding the study, our focal group (B2) consisted of six adult males and three adult females. We collected 490 10-min focal samples (82 hr) from all adults in the group (N=9) from July to November, 2001. To avoid predators, individuals should be more vigilant (i) with fewer neighbors, and (ii) in areas of the canopy with higher predation risks. Conspecific threats can be divided into extra- and intra-group threats. Extra-group threats should lead to higher vigilance levels (iii) during intergroup encounters, and (iv) in areas where the home range overlaps with other groups of colobus. Intra-group threats should lead to greater vigilance (v) in the presence of neighbors and (vi) while feeding or occupying food patches (if resources are limiting). Our results best support the hypothesis that vigilance functions primarily to detect extra-group, conspecific threats. Individuals were most vigilant during intergroup encounters and in areas of range overlap, and monthly vigilance rates were associated with monthly encounter rates. Individuals tended to scan less in proximity to familiar vs. unfamiliar group mates, suggesting that relationship quality may affect colobus vigilance. Finally, predation pressures or anthropogenic disturbances might have influenced vigilance, as individuals were more vigilant low in the canopy. However, this last result could also be due to the lower visibility because of dense foliage or to the fact that the monkeys have access to fewer escape routes when ranging lower in the canopy.

Ecology of the gastrointestinal parasites of Colobus vellerosus at Boabeng-Fiema, Ghana: possible anthropozoonotic transmission.

Parasite richness and prevalence in wild animals can be used as indicators of population and ecosystem health. In this study, the gastrointestinal parasites of ursine colobus monkeys (Colobus vellerosus) at the Boabeng-Fiema Monkey Sanctuary (BFMS), Ghana, were investigated. BFMS is a sacred grove where monkeys and humans have long lived in relatively peaceful proximity. Fecal samples (n = 109) were collected opportunistically from >27 adult and subadult males in six bisexual groups and one all-male band from July 2004 to August 2005. Using fecal floatation, we detected three protozoans (two Entamoeba sp., Isospora sp.), five nematodes (Ascaris sp., Enterobius sp., Trichuris sp., two strongyle sp.), and one digenean trematode. Using fluorescein labeled antibodies, we detected an additional protozoan (Giardia sp.), and with PCR techniques, we characterized this as G. duodenalis Assemblage B and also identified a protistan (Blastocystis sp., subtype 2). The most prevalent parasite species were G. duodenalis and Trichuris sp. Parasites were more prevalent in the long wet season than the long dry. Parasite prevalence did not vary by age, and average parasite richness did not differ by rank for males whose status remained unchanged. However, males that changed rank tended to show higher average parasite richness when they were lower ranked. Individuals that spent more time near human settlements had a higher prevalence of Isospora sp. that morphologically resembled the human species I. belli. The presence of this parasite and G. duodenalis Assemblage B indicates possible anthropozoonotic and/or zoonotic transmission between humans and colobus monkeys at this site.

Test of the ecological-constraints model on ursine colobus monkeys (Colobus vellerosus) in Ghana.

For group-living mammals, the ecological-constraints model predicts that within-group feeding competition will increase as group size increases, necessitating more daily travel to find food and thereby constraining group size. It provides a useful tool for detecting scramble competition any time it is difficult to determine whether or not food is limiting. We tested the ecological-constraints model on highly folivorous ursine colobus monkeys (Colobus vellerosus) at the Boabeng-Fiema Monkey Sanctuary in Ghana. Three differently sized groups were followed for 13 months and two others were followed for 6 months each in 2004-2005 using focal-animal sampling and ranging scans; ecological plots and phenology surveys were used to determine home-range quality and food availability. There was relatively little difference in home-range quality, monthly food availability, diet, adult female ingestion rates, and rate of travel within food patches between the groups. However, home-range size, day-range length, and percent of time spent feeding all increased with group size. We performed a single large test of the ecological-constraints model by combining several separate Spearman correlations, each testing different predictions under the model, using Fisher's log-likelihood method. It showed that the ecological-constraints model was supported in this study; scramble competition in this population is manifesting in increased ranging and time spent feeding. How costly this increased energy expenditure is for individuals in larger groups remains to be determined.