Colobus Research Articles

Status of Zanzibar Red Colobus and Sykes's Monkeys in Two Coastal Forests in 2005

We censused two discrete subpopulations of the endangered Zanzibar red colobus (Procolobus kirkii) and sympatric Sykes's monkeys (Cercopithecus mitis albogularis) between February 2004 and September 2005 in two coastal forests in Zan- zibar, including the northernmost (Kiwengwa-Pongwe Forest) and some of the southernmost (Uzi and Vundwe Islands) extents of P. kirkii's range. Surveys totalled 365 hours and 307.8 km along >16 km of line transects; 472 sightings were made (Red colobus n = 252; Sykes's monkey n = 220). The southern forests (coral rag with adjacent mangrove) of Uzi and Vundwe Islands were found to support P. kirkii at a higher estimated density (29.6 groups/km²) relative to the northern coral rag forest (lacking mangrove) in Kiwengwa-Pongwe (7.5 groups/km²). However, for red colobus in coral rag, up to c.40% of these groups could EH�≥VXEJURXSV¥�EDVHGRQRXUREVHUYDWLRQVRIFRQVLVWHQW�oVVLRQ�

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.

Discovery and full genome characterization of two highly divergent simian immunodeficiency viruses infecting black-and-white colobus monkeys (Colobus guereza) in Kibale National Park, Uganda

BackgroundAfrican non-human primates (NHPs) are natural hosts for simian immunodeficiency viruses (SIV), the zoonotic transmission of which led to the emergence of HIV-1 and HIV-2. However, our understanding of SIV diversity and evolution is limited by incomplete taxonomic and geographic sampling of NHPs, particularly in East Africa. In this study, we screened blood specimens from nine black-and-white colobus monkeys (Colobus guereza occidentalis) from Kibale National Park, Uganda, for novel SIVs using a combination of serology and “unbiased” deep-sequencing, a method that does not rely on genetic similarity to previously characterized viruses.ResultsWe identified two novel and divergent SIVs, tentatively named SIVkcol-1 and SIVkcol-2, and assembled genomes covering the entire coding region for each virus. SIVkcol-1 and SIVkcol-2 were detected in three and four animals, respectively, but with no animals co-infected. Phylogenetic analyses showed that SIVkcol-1 and SIVkcol-2 form a lineage with SIVcol, previously discovered in black-and-white colobus from Cameroon. Although SIVkcol-1 and SIVkcol-2 were isolated from the same host population in Uganda, SIVkcol-1 is more closely related to SIVcol than to SIVkcol-2. Analysis of functional motifs in the extracellular envelope glycoprotein (gp120) revealed that SIVkcol-2 is unique among primate lentiviruses in containing only 16 conserved cysteine residues instead of the usual 18 or more.ConclusionsOur results demonstrate that the genetic diversity of SIVs infecting black-and-white colobus across equatorial Africa is greater than previously appreciated and that divergent SIVs can co-circulate in the same colobine population. We also show that the use of “unbiased” deep sequencing for the detection of SIV has great advantages over traditional serological approaches, especially for studies of unknown or poorly characterized viruses. Finally, the detection of the first SIV containing only 16 conserved cysteines in the extracellular envelope protein gp120 further expands the range of functional motifs observed among SIVs and highlights the complex evolutionary history of simian retroviruses.

Emergent group level navigation: an agent-based evaluation of movement patterns in a folivorous primate.

The foraging activity of many organisms reveal strategic movement patterns, showing efficient use of spatially distributed resources. The underlying mechanisms behind these movement patterns, such as the use of spatial memory, are topics of considerable debate. To augment existing evidence of spatial memory use in primates, we generated movement patterns from simulated primate agents with simple sensory and behavioral capabilities. We developed agents representing various hypotheses of memory use, and compared the movement patterns of simulated groups to those of an observed group of red colobus monkeys (Procolobus rufomitratus), testing for: the effects of memory type (Euclidian or landmark based), amount of memory retention, and the effects of social rules in making foraging choices at the scale of the group (independent or leader led). Our results indicate that red colobus movement patterns fit best with simulated groups that have landmark based memory and a follow the leader foraging strategy. Comparisons between simulated agents revealed that social rules had the greatest impact on a group’s step length, whereas the type of memory had the highest impact on a group’s path tortuosity and cohesion. Using simulation studies as experimental trials to test theories of spatial memory use allows the development of insight into the behavioral mechanisms behind animal movement, developing case-specific results, as well as general results informing how changes to perception and behavior influence movement patterns.

Physiological and Behavioral Effects of Capture Darting on Red Colobus Monkeys (Procolobus rufomitratus) with a Comparison to Chimpanzee (Pan troglodytes) Predation

Understanding how human activities affect wild primates is critical to the design of effective conservation strategies. Despite this need, few studies have examined the physiological and behavioral effects of field research methods in the wild. Here, we examine how the stress response, i.e., fecal cortisol, and behavior of Ugandan red colobus monkeys (Procolobus rufomitratus) in Kibale National Park are affected by chemical immobilization and collaring, i.e., capture. We compare this anthropogenic stressor to a naturally occurring stressor: a chimpanzee (Pan troglodytes) predation attack. Two adult males had peak cortisol levels of 283 and 284 ng/g 2–3 d after capture, which were 190% and 182% above their baseline levels, i.e., the first sample taken immediately after capture, but these peak levels did not remain elevated. Using long-term data, i.e., 11 mo of data, we found no difference in fecal cortisol levels between 10 darted and collared individuals and 14 individuals living in the same social group that were not darted or collared. For the chimpanzee attack, peak fecal cortisol levels (147–211% above baseline) were recorded 1–4 d after the attack, but these levels also did not remain elevated for long. These data show that darting and collaring and a chimpanzee predation attempt caused an acute stress response, but neither leads to sustained elevated cortisol levels. Thus, in situations in which research contributes significantly to the conservation of primates and cannot be conducted noninvasively, capture darting appears to be a useful technique with minimal long-term effects as long as injury and mortality are avoided. However, we encourage researchers to make similar physiological and behavioral comparisons in other field studies using similar techniques to provide a better understanding of the effects of research practices on the stress physiology and social behavior of wild primates.

Effect of mating activity and dominance rank on male masturbation among free-ranging male rhesus macaques.

The adaptive function of male masturbation is still poorly understood, despite its high prevalence in humans and other animals. In non-human primates, male masturbation is most frequent among anthropoid monkeys and apes living in multimale-multifemale groups with a promiscuous mating system. In these species, male masturbation may be a non-functional by-product of high sexual arousal or be adaptive by providing advantages in terms of sperm competition or by decreasing the risk of sexually transmitted infections. We investigated the possible functional significance of male masturbation using behavioral data collected on 21 free-ranging male rhesus macaques (Macaca mulatta) at the peak of the mating season. We found some evidence that masturbation is linked to low mating opportunities: regardless of rank, males were most likely to be observed masturbating on days in which they were not observed mating, and lower-ranking males mated less and tended to masturbate more frequently than higher-ranking males. These results echo the findings obtained for two other species of macaques, but contrast those obtained in red colobus monkeys (Procolobus badius) and Cape ground squirrels (Xerus inauris). Interestingly, however, male masturbation events ended with ejaculation in only 15% of the observed masturbation time, suggesting that new hypotheses are needed to explain masturbation in this species. More studies are needed to establish whether male masturbation is adaptive and whether it serves similar or different functions in different sexually promiscuous species.

Is Markhamia lutea’s abundance determined by animal foraging?

Understanding the determinants of tropical forest tree richness and spatial distribution is a central goal of forest ecology; however, the role of herbivorous mammals has received little attention. Here we explore the potential for red colobus monkeys (Procolobus rufomitratus) to influence the abundance of Markhamia lutea trees in a tropical forest by feeding extensively on the tree’s flowers, such that this tree population is not able to regularly set fruit. Using 14years of data from Kibale National Park, Uganda, we quantify M. lutea flower and fruit production. Similarly, using 21years of data, we quantify temporal changes in the abundance of stems in size classes from 1m tall and above. Our analyses demonstrate that M. lutea is rarely able to produce fruit and that this corresponds to a general decline in its abundance across all size classes. Moreover, using 7years of feeding records, we demonstrate that red colobus feed on M. lutea, consuming large amounts of leaf and flower buds whenever they were available, suggesting that this behavior limits fruit production. Therefore, we suggest that red colobus are presently important for structuring the distribution and abundance of M. lutea in Kibale. This dynamic raises the intriguing question of how a large M. lutea population was able to originally establish. There is no evidence of a change in red colobus population size; however, if this old-growth forest is in a non-equilibrium state, M. lutea may have become established when red colobus ate a different diet.

The Roles of Phytoestrogens in Primate Ecology and Evolution

Most primates depend heavily on plant foods; thus their chemical composition is key to understanding primate ecology and evolution. One class of plant compounds of strong current interest are phytoestrogens, which have the potential to alter fertility, fecundity, and survival. These plant compounds mimic the activity of vertebrate estrogens, resulting in altered physiology and behavior. Here, we review what is known about phytoestrogens from an ecological and evolutionary perspective. Much of what is known about the effects of phytoestrogens on the endocrine system comes from research on human foods, especially soybeans (Glycine max). Two opposing perspectives have resulted from this research: 1) phytoestrogens provide health benefits, such as cancer prevention, or 2) phytoestrogens act as endocrine disruptors and threaten reproductive health. Studies of wild primates have only recently begun examining the presence of estrogenic plants in the primate diet and the effects of their consumption. Evidence that a number of primate species eat plants containing phytoestrogens and research documenting behavioral and hormonal effects of estrogenic plant consumption for red colobus monkeys (Procolobus rufomitratus) augment captive and laboratory studies to suggest that these compounds promote differential survival and reproduction. Although much debate is currently taking place over the role of phytoestrogens and other endocrine disruptors in human health issues and in threatening biodiversity, we argue that an ecological and evolutionary approach is needed to reach appropriate conclusions.

Voice discrimination in four primates

One accepted function of vocalisations is to convey information about the signaller, such as its age–sex class, motivation, or relationship with the recipient. Yet, in natural habitats individuals not only interact with conspecifics but also with members of other species. This is well documented for African forest monkeys, which form semi-permanent mixed-species groups that can persist for decades. Although members of such groups interact with each other on a daily basis, both physically and vocally, it is currently unknown whether they can discriminate familiar and unfamiliar voices of heterospecific group members. We addressed this question with playbacks on monkey species known to form polyspecific associations in the wild: red-capped mangabeys, Campbell's monkeys and Guereza colobus monkeys. We tested subjects’ discrimination abilities of contact calls of familiar and unfamiliar female De Brazza monkeys. When pooling all species, subjects looked more often towards the speaker when hearing contact calls of unfamiliar than familiar callers. When testing De Brazza monkeys with their own calls, we found the same effect with the longest gaze durations after hearing unfamiliar voices. This suggests that primates can discriminate, not only between familiar and unfamiliar voices of conspecifics, but also between familiar and unfamiliar voices of heterospecifics living within a close proximity.

Chimpanzee‐red colobus encounter rates show a red colobus population decline associated with predation by chimpanzees at Ngogo

Chimpanzees (Pan troglodytes) hunt various primates, but concentrate on red colobus monkeys (Piliocolobus spp.) wherever the two species are sympatric. The extraordinarily large Ngogo chimpanzee community in Kibale National Park, Uganda, preys heavily on the local population of red colobus (P. tephrosceles). Census data showed a steep decline in this population in the center of the chimpanzees' home range between 1975 and 2007 [Lwanga et al., 2011; Teelen, 2007b]. Given no obvious change in food availability, predation by chimpanzees was the most likely cause [ibid.; Teelen, 2008]. However, census data from other parts of the home range raised the possibility that the decline was restricted to this central area [Teelen, 2007a] We present data from 1998 to 2012 on the rate of encounters between chimpanzees and red colobus that provide a chimpanzee-centered estimate of red colobus density, thus of predation opportunities, throughout the home range. These corroborate census data by showing a long-term decline in encounters near the center. They also show that encounters become relatively more common at increasing distances from the center, but encounter rates have decreased even in peripheral areas and, by implication, the red colobus population has declined throughout the study area. These data corroborate Teelen's [2008] conclusion that chimpanzee predation on red colobus during the 1990s and early 2000s was unsustainable. Hunting rates and prey offtake rates have also declined markedly; whether this will allow the red colobus population to recover is unknown. In contrast, rates at which chimpanzees encountered redtail monkeys (Cercopithecus ascanius) and grey-cheeked mangabeys (Lophocebus albigena) did not decrease. Neither did they increase, however, contrary to long-term census data from the center of the study area [Lwanga et al., 2011].

Ecology rather than psychology explains co-occurrence of predation and border patrols in male chimpanzees

The intense arousal and excitement shown by adult male chimpanzees, Pan troglodytes, during territorial attacks on other chimpanzees and predation upon monkeys suggest that similar psychological mechanisms may be involved. Specifically, it has been proposed that hunting behaviour in chimpanzees evolved from intraspecies aggression. Over 32 years, chimpanzees at Gombe National Park, Tanzania were significantly more likely to engage in a territorial border patrol on days when they hunted red colobus monkeys (Procolobus spp.), and vice versa, even after statistically controlling for male chimpanzee party size. We test the hypothesis that this correlation arises because hunting and patrolling are components of a specieslevel aggressive behavioural syndrome; specifically that predation arose as a by-product of territorial aggression in this species. However, hunting was equally likely to occur after a patrol and/or an intergroup interaction as it was before, and the occurrence of an intergroup interaction in which the chimpanzees approached strangers did not increase subsequent hunting probability. We also reject the hypothesis that hunting and patrolling reflect an individual-level behavioural syndrome. We identified two 'impact hunters' whose presence increased hunting probability. Similarly, there were also three 'impact patrollers', who increased the likelihood that a visit to the periphery of the community range resulted in a patrol. While this discovery has important implications for our understanding of the proximate causes of cooperation, it does not explain the temporal correlation between patrolling and hunting, since no males had such an impact in both contexts. Instead, the data suggest that the correlation arose because patrols typically involved males travelling long distances, which increased the probability of encountering prey. Additionally, parties that travelled to the periphery were more likely to encounter colobus in woodland, where hunts are more likely to occur and to succeed. Therefore, we conclude that ecological, rather than psychological, factors promote the co-occurrence of hunting and territorial aggression in this species.

A Novel Hepacivirus with an Unusually Long and Intrinsically Disordered NS5A Protein in a Wild Old World Primate

GB virus B (GBV-B; family Flaviviridae, genus Hepacivirus) has been studied in New World primates as a model for human hepatitis C virus infection, but the distribution of GBV-B and its relatives in nature has remained obscure. Here, we report the discovery of a novel and highly divergent GBV-B-like virus in an Old World monkey, the black-and-white colobus (Colobus guereza), in Uganda. The new virus, guereza hepacivirus (GHV), clusters phylogenetically with GBV-B and recently described hepaciviruses infecting African bats and North American rodents, and it shows evidence of ancient recombination with these other hepaciviruses. Direct sequencing of reverse-transcribed RNA from blood plasma from three of nine colobus monkeys yielded near-complete GHV genomes, comprising two distinct viral variants. The viruses contain an exceptionally long nonstructural 5A (NS5A) gene, approximately half of which codes for a protein with no discernible homology to known proteins. Computational structure-based analyses indicate that the amino terminus of the GHV NS5A protein may serve a zinc-binding function, similar to the NS5A of other viruses within the family Flaviviridae. However, the 521-amino-acid carboxy terminus is intrinsically disordered, reflecting an unusual degree of structural plasticity and polyfunctionality. These findings shed new light on the natural history and evolution of the hepaciviruses and on the extent of structural variation within the Flaviviridae.

Lentivirus restriction by diverse primate APOBEC3A proteins

Rhesus macaque APOBEC3A (rhA3A) is capable of restricting both simian–human immunodeficiency virus (SHIVΔvif) and human immunodeficiency virus (HIV-1Δvif) to a greater extent than hA3A. We constructed chimeric A3A proteins to define the domains required for differential lentivirus restriction. Substitution of amino acids 25–33 from rhA3A into hA3A was sufficient to restrict HIVΔvif to levels similar to rhA3A restriction of SHIVΔvif. We tested if differential lentivirus restriction is conserved between A3A from Old World monkey and hominid lineages. A3A from African green monkey restricted SHIVΔvif but not HIV-1Δvif and colobus monkey A3A restricted both wild type and SHIVΔvif and HIV-1Δvif. In contrast, the gibbon ape A3A restricted neither SHIVΔvif nor HIV-1Δvif. Restriction of SHIVΔvif and HIV-1Δvif by New World monkey A3A proteins was not conserved as the A3A from the squirrel monkey but not the northern owl monkey restricted SHIVΔvif. Finally, the colobus A3A protein appears to restrict by a novel post-entry mechanism.

Genetic evidence for spatio‐temporal changes in the dispersal patterns of two sympatric African colobine monkeys

Western black-and-white colobus and Temmink's red colobus are two forest-dependent African primates with similar ecological requirements, often found in sympatry. Their most striking difference lies in their social system: black-and-white colobus live in small groups with mainly male-mediated dispersal but where females can also disperse, whereas red colobus live in larger groups with males described as philopatric. To investigate whether genetic evidence supports the reported patterns of dispersal based on observational data, we examined eight black-and-white and six red colobus social groups from Cantanhez National Park, Guinea-Bissau. Microsatellite markers revealed a lack of sex-biased dispersal for black-and-white colobus. Gene flow, mainly mediated by females, better explained the genetic patterns found in red colobus, with some evidence for less extensive male dispersal. In contrast to the microsatellite data, low mitochondrial diversity for the black-and-white colobus suggests that historical and/or long-range male-mediated gene flow might have been favored. In red colobus, the co-existence of three divergent mitochondrial haplogroups suggests that the Cantanhez population contains a secondary contact zone between divergent lineages that evolved in allopatry. Female-biased dispersal in this species may be a major factor contributing to the colonization by such differentiated mitochondrial lineages in the region. Overall, we find evidence for a spatio-temporal change in the dispersal patterns of the colobus monkeys of Cantanhez, with mitochondrial DNA indicating dispersal by mainly a single sex and microsatellite data suggesting that recently both sexes appear to be dispersing within the population.

Microsatellite DNA suggests that group size affects sex-biased dispersal patterns in red colobus monkeys.

Dispersal is a major life history trait of social organisms influencing the behavioral and genetic structure of their groups. Unfortunately, primate dispersal is difficult to quantify, because of the rarity of these events and our inability to ascertain if individuals dispersed or died when they disappear. Socioecological models have been partially developed to understand the ecological causes of different dispersal systems and their social consequences. However, these models have yielded confusing results when applied to folivores. The folivorous red colobus monkey (Procolobus rufomitratus) in Kibale National Park, Uganda is thought to exhibit female-biased dispersal, although both sexes have been observed to disperse and there remains considerable debate over the selective pressures favoring the transfers of males and females and the causes of variation in the proportion of each sex to leave the natal group. We circumvent this problem by using microsatellite DNA data to investigate the prediction that female dispersal will be more frequent in larger groups as compared to smaller ones. The rationale for this prediction is that red colobus exhibit increased within-group competition in bigger groups, which should favor higher female dispersal rates and ultimately lower female relatedness. Genetic data from two unequally sized neighboring groups of red colobus demonstrate increased female relatedness within the smaller group, suggesting females are less likely to disperse when there is less within-group competition. We suggest that the dispersal system is mediated to some degree by scramble competition and group size. Since red colobus group sizes have increased throughout Kibale by over 50% in the last decade, these changes may have major implications for the genetic structure and ultimately the population viability of this endangered primate.

Analysing small-scale aggregation in animal visits in space and time: the ST-BBD method

Movement behaviour plays an important role in many ecological interactions. As animals move through the environment, they generate movement patterns, which are a combined result of landscape characteristics and species-specific behaviour. Measuring these ranging patterns is being facilitated by technological advances in collection methods, such as GPS collars, that are capturing movement on finer spatial and temporal scales. We propose the use of a novel spatiotemporal analytical framework (ST-BBD), based on the beta-binomial distribution (BBD) model, to measure small-scale aggregation in animal movement data sets, including two simulated and three collected primate data sets. We use this approach to distinguish different habitat uses of three primate species (red colobus, Procolobus rufomitratus, black howler, Alouatta pigra, and spider monkey, Ateles geoffroyi) and quantify their specific use of the landscape in space and in time, using a parameter of the BBD that measures the variation in sites visited on a landscape. We found that estimates of aggregation in habitat use were higher in the frugivorous spider monkey, compared to the more folivorous howler monkey, and that in the red colobus, aggregation in site visits was dependent on group size and food availability. Applications of this framework to animal movement data could be useful in understanding ecological systems where habitat use is an important factor, such as the relationships between hosts and parasites, or parent plants and seed dispersers.

Novel simian foamy virus infections from multiple monkey species in women from the Democratic Republic of Congo

BackgroundZoonotic transmission of simian retroviruses in Central Africa is ongoing and can result in pandemic human infection. While simian foamy virus (SFV) infection was reported in primate hunters in Cameroon and Gabon, little is known about the distribution of SFV in Africa and whether human-to-human transmission and disease occur. We screened 3,334 plasmas from persons living in rural villages in central Democratic Republic of Congo (DRC) using SFV-specific EIA and Western blot (WB) tests. PCR amplification of SFV polymerase sequences from DNA extracted from buffy coats was used to measure proviral loads. Phylogenetic analysis was used to define the NHP species origin of SFV. Participants completed questionnaires to capture NHP exposure information.ResultsSixteen (0.5%) samples were WB-positive; 12 of 16 were from women (75%, 95% confidence limits 47.6%, 92.7%). Sequence analysis detected SFV in three women originating from Angolan colobus or red-tailed monkeys; both monkeys are hunted frequently in DRC. NHP exposure varied and infected women lived in distant villages suggesting a wide and potentially diverse distribution of SFV infections across DRC. Plasmas from 22 contacts of 8 WB-positive participants were all WB negative suggesting no secondary viral transmission. Proviral loads in the three women ranged from 14 – 1,755 copies/105 cells.ConclusionsOur study documents SFV infection in rural DRC for the first time and identifies infections with novel SFV variants from Colobus and red-tailed monkeys. Unlike previous studies, women were not at lower risk for SFV infection in our population, providing opportunities for spread of SFV both horizontally and vertically. However, limited testing of close contacts of WB-positive persons did not identify human-to-human transmission. Combined with the broad behavioral risk and distribution of NHPs across DRC, our results suggest that SFV infection may have a wider geographic distribution within DRC. These results also reinforce the potential for an increased SFV prevalence throughout the forested regions of Africa where humans and simians co-exist. Our finding of endemic foci of SFV infection in DRC will facilitate longitudinal studies to determine the potential for person-to-person transmissibility and pathogenicity of these zoonotic retroviral infections.

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.

Primate DNA suggests long-term stability of an African rainforest.

Red colobus monkeys, due to their sensitivity to environmental change, are indicator species of the overall health of their tropical rainforest habitats. As a result of habitat loss and overhunting, they are among the most endangered primates in the world, with very few viable populations remaining. Traditionally, extant indicator species have been used to signify the conditions of their current habitats, but they have also been employed to track past environmental conditions by detecting previous population fluctuations. Kibale National Park (KNP) in Uganda harbors the only remaining unthreatened large population of red colobus. We used microsatellite DNA to evaluate the historical demography of these red colobus and, therefore, the long-term stability of their habitat. We find that the red colobus population throughout KNP has been stable for at least ∼40,000 years. We interpret this result as evidence of long-term forest stability because a change in the available habitat or population movement would have elicited a corresponding change in population size. We conclude that the forest of what is now Kibale National Park may have served as a Late Pleistocene refuge for many East African species.

Estrogenic plant consumption predicts red colobus monkey (Procolobus rufomitratus) hormonal state and behavior

Numerous studies have examined the effects of anthropogenic endocrine disrupting compounds; however, very little is known about the effects of naturally occurring plant-produced estrogenic compounds (i.e., phytoestrogens) on vertebrates. To examine the seasonal pattern of phytoestrogen consumption and its relationship to hormone levels (407 fecal samples analyzed for estradiol and cortisol) and social behavior (aggression, mating, and grooming) in a primate, we conducted an 11-month field study of red colobus (Procolobus rufomitratus) in Kibale National Park, Uganda. The percent of diet from estrogenic plants averaged 10.7% (n=45weeks; range: 0.7–32.4%). Red colobus fed more heavily on estrogenic Millettia dura young leaves during weeks of higher rainfall, and the consumption of this estrogenic item was positively correlated to both their fecal estradiol and cortisol levels. Social behaviors were related to estradiol and cortisol levels, as well as the consumption of estrogenic plants and rainfall. The more the red colobus consumed estrogenic plants the higher their rates of aggression and copulation and the lower their time spent grooming. Our results suggest that the consumption of estrogenic plants has important implications for primate health and fitness through interactions with the endocrine system and changes in hormone levels and social behaviors.