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Sample records for piliocolobus rufomitratus tephrosceles

  1. Genome Sequences of Polyomaviruses from the Wild-Living Red Colobus (Piliocolobus badius) and Western Chimpanzee (Pan troglodytes verus)

    PubMed Central

    Ben Salem, Nicole; Leendertz, Fabian H.

    2016-01-01

    We identified with PCR and sequencing the full genomes of the recently discovered Pan troglodytes verus polyomavirus 8 and Piliocolobus badius polyomavirus 2 in a western chimpanzee and a western red colobus free-ranging in Taï National Park of Côte d’Ivoire. PMID:27738028

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

    PubMed Central

    Wasserman, Michael D.; Chapman, Colin A.; Milton, Katharine; Gogarten, Jan F.; Wittwer, Dan J.; Ziegler, Toni E.

    2012-01-01

    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 = 45 weeks; 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. PMID:23010620

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

    PubMed

    Wasserman, Michael D; Chapman, Colin A; Milton, Katharine; Gogarten, Jan F; Wittwer, Daniel J; Ziegler, Toni E

    2012-11-01

    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=45 weeks; 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. PMID:23010620

  4. Killing of a pearl-spotted owlet (Glaucidium perlatum) by male red colobus monkeys (Procolobus tephrosceles) in a forest fragment near Kibale National Park, Uganda.

    PubMed

    Goldberg, Tony L; Gillespie, Thomas R; Rwego, Innocent B; Kaganzi, Clovis

    2006-10-01

    Adult male red colobus (Procolobus tephrosceles) were observed capturing and killing an owl (Glaucidium perlatum) in the Rurama forest fragment near Kibale National Park in western Uganda. The owl was not subsequently eaten by the colobus, their conspecifics, or the other primates present during the attack. Because the incident was preceded by an agonistic encounter with a raptor, the event is best interpreted as a misdirected antipredator behavior. Although antipredator behaviors are not unknown in red colobus, this is the first such incident directed against a raptor to be documented. PMID:16892411

  5. Gastrointestinal parasites of critically endangered primates endemic to Tana River, Kenya: Tana River red colobus (Procolobus rufomitratus) and crested mangabey (Cercocebus galeritus).

    PubMed

    Mbora, David N M; Munene, Elephas

    2006-10-01

    We conducted fecal egg counts of gastrointestinal parasites of 2 critically endangered primates endemic to the forest of Tana River, Kenya. We aimed to use the fecal egg counts as proxies to quantify the prevalence of gastrointestinal parasites between the 2 primates. The Tana River red colobus (Procolobus rufomitratus) and crested mangabey (Cercocebus galeritus) are of similar body size, but their behavioral ecology is very different. We predicted that mangabeys would have a higher prevalence of parasites because they are mostly terrestrial omnivores, live in larger social groups, and therefore range widely. We detected 10 nematodes and 3 protozoans in mangabeys and 7 nematodes and 2 protozoans in colobus. We detected a higher number of different parasite species in individual mangabeys, and 4 of the 5 nematodes requiring intermediate hosts were found in mangabeys. The overall prevalence of parasites was higher for mangabeys, but this difference was not statistically significant. For colobus, we found a trend whereby the number of different parasite species in individual monkeys was higher in males and in lactating females. However, there was no difference in the prevalence of parasites between the sexes or between lactating and nonlactating females.

  6. Beyond bushmeat: animal contact, injury, and zoonotic disease risk in Western Uganda.

    PubMed

    Paige, Sarah B; Frost, Simon D W; Gibson, Mhairi A; Jones, James Holland; Shankar, Anupama; Switzer, William M; Ting, Nelson; Goldberg, Tony L

    2014-12-01

    Zoonotic pathogens cause an estimated 70% of emerging and re-emerging infectious diseases in humans. In sub-Saharan Africa, bushmeat hunting and butchering is considered the primary risk factor for human-wildlife contact and zoonotic disease transmission, particularly for the transmission of simian retroviruses. However, hunting is only one of many activities in sub-Saharan Africa that bring people and wildlife into contact. Here, we examine human-animal interaction in western Uganda, identifying patterns of injuries from animals and contact with nonhuman primates. Additionally, we identify individual-level risk factors associated with contact. Nearly 20% (246/1,240) of participants reported either being injured by an animal or having contact with a primate over their lifetimes. The majority (51.7%) of injuries were dog bites that healed with no long-term medical consequences. The majority (76.8%) of 125 total primate contacts involved touching a carcass; however, butchering (20%), hunting (10%), and touching a live primate (10%) were also reported. Red colobus (Piliocolobus rufomitratus tephrosceles) accounted for most primate contact events. Multivariate logistic regression indicated that men who live adjacent to forest fragments are at elevated risk of animal contact and specifically primate contact. Our results provide a useful comparison to West and Central Africa where "bushmeat hunting" is the predominant paradigm for human-wildlife contact and zoonotic disease transmission.

  7. Beyond bushmeat: Animal contact, injury, and zoonotic disease risk in western Uganda

    PubMed Central

    Paige, Sarah B.; Frost, Simon D.W.; Gibson, Mhairi A.; Holland, James; Shankar, Anupama; Switzer, William M.; Ting, Nelson

    2014-01-01

    Zoonotic pathogens cause an estimated 70% of emerging and re-emerging infectious diseases in humans. In sub-Saharan Africa, bushmeat hunting and butchering is considered the primary risk factor for human-wildlife contact and zoonotic disease transmission, particularly for the transmission of simian retroviruses. However, hunting is only one of many activities in sub-Saharan Africa that bring people and wildlife into contact. Here, we examine human-animal interaction in western Uganda, identifying patterns of injuries from animals and contact with nonhuman primates. Additionally, we identify individual-level risk factors associated with contact. Nearly 20% (246/ 1,240) of participants reported either being injured by an animal or having contact with a primate over their lifetimes. The majority (51.7%) of injuries were dog bites that healed with no long term medical consequences. The majority (76.8%) of 125 total primate contacts involved touching a carcass; however, butchering (20%), hunting (10%), and touching a live primate (10%) were also reported. Red colobus (Piliocolobus rufomitratus tephrosceles) accounted for most primate contact events. Multivariate logistic regression indicated that men who live adjacent to forest fragments are at elevated risk of animal contact and specifically primate contact. Our results provide a useful comparison to West and Central Africa where “bushmeat hunting” is the predominant paradigm for human-wildlife contact and zoonotic disease transmission. PMID:24845574

  8. The role of sugar in diet selection in redtail and red colobus monkeys

    Technology Transfer Automated Retrieval System (TEKTRAN)

    A study of diet selection by folivorous (red colobine monkeys; Piliocolobus tephrosceles) and frugivorous (redtail monkeys; Ceropithecus ascanius) was performed to provide comparable compositional descriptions of the diets of the two species, to contrast sugar content of plant foods consumed by each...

  9. Divergent Simian Arteriviruses Cause Simian Hemorrhagic Fever of Differing Severities in Macaques

    PubMed Central

    Moncla, Louise H.; Weiler, Andrea M.; Charlier, Olivia; Rojas, Oscar; Byrum, Russell; Ragland, Dan R.; Cohen, Melanie; Sanford, Hannah B.; Qin, Jing

    2016-01-01

    ABSTRACT Simian hemorrhagic fever (SHF) is a highly lethal disease in captive macaques. Three distinct arteriviruses are known etiological agents of past SHF epizootics, but only one, simian hemorrhagic fever virus (SHFV), has been isolated in cell culture. The natural reservoir(s) of the three viruses have yet to be identified, but African nonhuman primates are suspected. Eleven additional divergent simian arteriviruses have been detected recently in diverse and apparently healthy African cercopithecid monkeys. Here, we report the successful isolation in MARC-145 cell culture of one of these viruses, Kibale red colobus virus 1 (KRCV-1), from serum of a naturally infected red colobus (Procolobus [Piliocolobus] rufomitratus tephrosceles) sampled in Kibale National Park, Uganda. Intramuscular (i.m.) injection of KRCV-1 into four cynomolgus macaques (Macaca fascicularis) resulted in a self-limiting nonlethal disease characterized by depressive behavioral changes, disturbance in coagulation parameters, and liver enzyme elevations. In contrast, i.m. injection of SHFV resulted in typical lethal SHF characterized by mild fever, lethargy, lymphoid depletion, lymphoid and hepatocellular necrosis, low platelet counts, increased liver enzyme concentrations, coagulation abnormalities, and increasing viral loads. As hypothesized based on the genetic and presumed antigenic distance between KRCV-1 and SHFV, all four macaques that had survived KRCV-1 injection died of SHF after subsequent SHFV injection, indicating a lack of protective heterotypic immunity. Our data indicate that SHF is a disease of macaques that in all likelihood can be caused by a number of distinct simian arteriviruses, although with different severity depending on the specific arterivirus involved. Consequently, we recommend that current screening procedures for SHFV in primate-holding facilities be modified to detect all known simian arteriviruses. PMID:26908578

  10. Prevalence and genetic diversity of simian immunodeficiency virus infection in wild-living red colobus monkeys (Piliocolobus badius badius) from the Taï forest, Côte d'Ivoire SIVwrc in wild-living western red colobus monkeys.

    PubMed

    Locatelli, Sabrina; Liegeois, Florian; Lafay, Bénédicte; Roeder, Amy D; Bruford, Michael W; Formenty, Pierre; Noë, Ronald; Delaporte, Eric; Peeters, Martine

    2008-01-01

    Numerous African primates are infected with simian immunodeficiency viruses (SIVs). It is now well established that the clade of SIVs infecting west-central African chimpanzees (Pan troglodytes troglodytes) and western gorillas (Gorilla gorilla gorilla) represent the progenitors of human immunodeficiency virus type 1 (HIV-1), whereas HIV-2 results from different cross-species transmissions of SIVsmm from sooty mangabeys (Cercocebus atys atys). We present here the first molecular epidemiological survey of simian immunodeficiency virus (SIVwrc) in wild-living western red colobus monkeys (Piliocolobus badius badius) which are frequently hunted by the human population and represent a favourite prey of western chimpanzees (Pan troglodytes verus). We collected faecal samples (n=88) and we assessed individual discrimination by microsatellite analyses and visual observation. We tested the inferred 53 adult individuals belonging to two neighbouring habituated groups for presence of SIVwrc infection by viral RNA (vRNA) detection. We amplified viral polymerase (pol) (650 bp) and/or envelope (env) (570 bp) sequences in 14 individuals, resulting in a minimal prevalence of 26% among the individuals sampled, possibly reaching 50% when considering the relatively low sensitivity of viral RNA detection in faecal samples. With a few exceptions, phylogenetic analysis of pol and env sequences revealed a low degree of intragroup genetic diversity and a general viral clustering related to the social group of origin. However, we found a higher intergroup diversity. Behavioural and demographic data collected previously from these communities indicate that red colobus monkeys live in promiscuous multi-male societies, where females leave their natal group at the sub-adult stage of their lives and where extra-group copulations or male immigration have been rarely observed. The phylogenetic data we obtained seem to reflect these behavioural characteristics. Overall, our results indicate that

  11. Redtail and red colobus monkeys show intersite urinary cortisol concentration variation in Kibale National Park, Uganda

    PubMed Central

    Aronsen, Gary P.; Beuerlein, Melanie M.; Watts, David P.; Bribiescas, Richard G.

    2015-01-01

    Non-invasive measurement of urinary cortisol is a proven method of evaluating the impact of environmental stressors on wild primates. Variation in cortisol concentrations can reflect physiological stress, and prolonged elevation of circulating cortisol can significantly affect individual and population-level health. In a previous study, we found that urinary cortisol concentrations in grey-cheeked mangabeys (Lophocebus albigena) were higher at a highly disturbed site (Mainaro) in Kibale National Park, Uganda compared with a minimally disturbed site (Ngogo) in the same habitat. Here, we expand on this research, reporting on cortisol concentrations in two other cercopithecid monkeys (Cercopithecus ascanius and Piliocolobus rufomitratus) at the same two sites. We hypothesized that C. ascanius would show no difference between sites, given its preference for secondary forests, while P. rufomitratus would have higher cortisol concentrations at the disturbed site. Contrary to expectations, both species exhibited significantly higher cortisol concentrations at Ngogo (minimally disturbed) compared with Mainaro (disturbed). We suggest that these results may be caused by inter- or intragroup social dynamics, intersite differences in predation rate, fruit/food availability and chemistry, or a combination of these factors. These initial evaluations of urinary cortisol concentrations provide testable hypotheses on habitat disturbance and Kibale primate ecophysiology. PMID:27293691

  12. High Genetic Diversity and Adaptive Potential of Two Simian Hemorrhagic Fever Viruses in a Wild Primate Population

    PubMed Central

    Weiler, Andrea; Sibley, Samuel D.; Dinis, Jorge M.; Bergman, Zachary; Nelson, Chase W.; Correll, Michael; Gleicher, Michael; Hyeroba, David; Tumukunde, Alex; Weny, Geoffrey; Chapman, Colin; Kuhn, Jens H.; Hughes, Austin L.; Friedrich, Thomas C.; Goldberg, Tony L.; O'Connor, David H.

    2014-01-01

    Key biological properties such as high genetic diversity and high evolutionary rate enhance the potential of certain RNA viruses to adapt and emerge. Identifying viruses with these properties in their natural hosts could dramatically improve disease forecasting and surveillance. Recently, we discovered two novel members of the viral family Arteriviridae: simian hemorrhagic fever virus (SHFV)-krc1 and SHFV-krc2, infecting a single wild red colobus (Procolobus rufomitratus tephrosceles) in Kibale National Park, Uganda. Nearly nothing is known about the biological properties of SHFVs in nature, although the SHFV type strain, SHFV-LVR, has caused devastating outbreaks of viral hemorrhagic fever in captive macaques. Here we detected SHFV-krc1 and SHFV-krc2 in 40% and 47% of 60 wild red colobus tested, respectively. We found viral loads in excess of 106–107 RNA copies per milliliter of blood plasma for each of these viruses. SHFV-krc1 and SHFV-krc2 also showed high genetic diversity at both the inter- and intra-host levels. Analyses of synonymous and non-synonymous nucleotide diversity across viral genomes revealed patterns suggestive of positive selection in SHFV open reading frames (ORF) 5 (SHFV-krc2 only) and 7 (SHFV-krc1 and SHFV-krc2). Thus, these viruses share several important properties with some of the most rapidly evolving, emergent RNA viruses. PMID:24651479

  13. High genetic diversity and adaptive potential of two simian hemorrhagic fever viruses in a wild primate population.

    PubMed

    Bailey, Adam L; Lauck, Michael; Weiler, Andrea; Sibley, Samuel D; Dinis, Jorge M; Bergman, Zachary; Nelson, Chase W; Correll, Michael; Gleicher, Michael; Hyeroba, David; Tumukunde, Alex; Weny, Geoffrey; Chapman, Colin; Kuhn, Jens H; Hughes, Austin L; Friedrich, Thomas C; Goldberg, Tony L; O'Connor, David H

    2014-01-01

    Key biological properties such as high genetic diversity and high evolutionary rate enhance the potential of certain RNA viruses to adapt and emerge. Identifying viruses with these properties in their natural hosts could dramatically improve disease forecasting and surveillance. Recently, we discovered two novel members of the viral family Arteriviridae: simian hemorrhagic fever virus (SHFV)-krc1 and SHFV-krc2, infecting a single wild red colobus (Procolobus rufomitratus tephrosceles) in Kibale National Park, Uganda. Nearly nothing is known about the biological properties of SHFVs in nature, although the SHFV type strain, SHFV-LVR, has caused devastating outbreaks of viral hemorrhagic fever in captive macaques. Here we detected SHFV-krc1 and SHFV-krc2 in 40% and 47% of 60 wild red colobus tested, respectively. We found viral loads in excess of 10(6)-10(7) RNA copies per milliliter of blood plasma for each of these viruses. SHFV-krc1 and SHFV-krc2 also showed high genetic diversity at both the inter- and intra-host levels. Analyses of synonymous and non-synonymous nucleotide diversity across viral genomes revealed patterns suggestive of positive selection in SHFV open reading frames (ORF) 5 (SHFV-krc2 only) and 7 (SHFV-krc1 and SHFV-krc2). Thus, these viruses share several important properties with some of the most rapidly evolving, emergent RNA viruses.

  14. Sickness behaviour associated with non-lethal infections in wild primates

    PubMed Central

    Ghai, Ria R.; Fugère, Vincent; Chapman, Colin A.; Goldberg, Tony L.; Davies, T. Jonathan

    2015-01-01

    Non-lethal parasite infections are common in wildlife, but there is little information on their clinical consequences. Here, we pair infection data from a ubiquitous soil-transmitted helminth, the whipworm (genus Trichuris), with activity data from a habituated group of wild red colobus monkeys (Procolobus rufomitratus tephrosceles) in Kibale National Park, Uganda. We use mixed-effect models to examine the relationship between non-lethal parasitism and red colobus behaviour. Our results indicate that red colobus increased resting and decreased more energetically costly behaviours when shedding whipworm eggs in faeces. Temporal patterns of behaviour also changed, with individuals switching behaviour less frequently when whipworm-positive. Feeding frequency did not differ, but red colobus consumption of bark and two plant species from the genus Albizia, which are used locally in traditional medicines, significantly increased when animals were shedding whipworm eggs. These results suggest self-medicative plant use, although additional work is needed to verify this conclusion. Our results indicate sickness behaviours, which are considered an adaptive response by hosts during infection. Induction of sickness behaviour in turn suggests that these primates are clinically sensitive to non-lethal parasite infections. PMID:26311670

  15. Primate vaginal microbiomes exhibit species specificity without universal Lactobacillus dominance

    PubMed Central

    Yildirim, Suleyman; Yeoman, Carl J; Janga, Sarath Chandra; Thomas, Susan M; Ho, Mengfei; Leigh, Steven R; Consortium, Primate Microbiome; White, Bryan A; Wilson, Brenda A; Stumpf, Rebecca M

    2014-01-01

    Bacterial communities colonizing the reproductive tracts of primates (including humans) impact the health, survival and fitness of the host, and thereby the evolution of the host species. Despite their importance, we currently have a poor understanding of primate microbiomes. The composition and structure of microbial communities vary considerably depending on the host and environmental factors. We conducted comparative analyses of the primate vaginal microbiome using pyrosequencing of the 16S rRNA genes of a phylogenetically broad range of primates to test for factors affecting the diversity of primate vaginal ecosystems. The nine primate species included: humans (Homo sapiens), yellow baboons (Papio cynocephalus), olive baboons (Papio anubis), lemurs (Propithecus diadema), howler monkeys (Alouatta pigra), red colobus (Piliocolobus rufomitratus), vervets (Chlorocebus aethiops), mangabeys (Cercocebus atys) and chimpanzees (Pan troglodytes). Our results indicated that all primates exhibited host-specific vaginal microbiota and that humans were distinct from other primates in both microbiome composition and diversity. In contrast to the gut microbiome, the vaginal microbiome showed limited congruence with host phylogeny, and neither captivity nor diet elicited substantial effects on the vaginal microbiomes of primates. Permutational multivariate analysis of variance and Wilcoxon tests revealed correlations among vaginal microbiota and host species-specific socioecological factors, particularly related to sexuality, including: female promiscuity, baculum length, gestation time, mating group size and neonatal birth weight. The proportion of unclassified taxa observed in nonhuman primate samples increased with phylogenetic distance from humans, indicative of the existence of previously unrecognized microbial taxa. These findings contribute to our understanding of host–microbe variation and coevolution, microbial biogeography, and disease risk, and have important

  16. Exceptional Simian Hemorrhagic Fever Virus Diversity in a Wild African Primate Community

    PubMed Central

    Lauck, Michael; Sibley, Samuel D.; Hyeroba, David; Tumukunde, Alex; Weny, Geoffrey; Chapman, Colin A.; Ting, Nelson; Switzer, William M.; Kuhn, Jens H.; Friedrich, Thomas C.; O'Connor, David H.

    2013-01-01

    Simian hemorrhagic fever virus (SHFV) is an arterivirus that causes severe disease in captive macaques. We describe two new SHFV variants subclinically infecting wild African red-tailed guenons (Cercopithecus ascanius). Both variants are highly divergent from the prototype virus and variants infecting sympatric red colobus (Procolobus rufomitratus). All known SHFV variants are monophyletic and share three open reading frames not present in other arteriviruses. Our data suggest a need to modify the current arterivirus classification. PMID:23077302

  17. Discovery and Characterization of Distinct Simian Pegiviruses in Three Wild African Old World Monkey Species

    PubMed Central

    Sibley, Samuel D.; Lauck, Michael; Bailey, Adam L.; Hyeroba, David; Tumukunde, Alex; Weny, Geoffrey; Chapman, Colin A.; O’Connor, David H.; Goldberg, Tony L.; Friedrich, Thomas C.

    2014-01-01

    Within the Flaviviridae, the recently designated genus Pegivirus has expanded greatly due to new discoveries in bats, horses, and rodents. Here we report the discovery and characterization of three simian pegiviruses (SPgV) that resemble human pegivirus (HPgV) and infect red colobus monkeys (Procolobus tephrosceles), red-tailed guenons (Cercopithecus ascanius) and an olive baboon (Papio anubis). We have designated these viruses SPgVkrc, SPgVkrtg and SPgVkbab, reflecting their host species’ common names, which include reference to their location of origin in Kibale National Park, Uganda. SPgVkrc and SPgVkrtg were detected in 47% (28/60) of red colobus and 42% (5/12) red-tailed guenons, respectively, while SPgVkbab infection was observed in 1 of 23 olive baboons tested. Infections were not associated with any apparent disease, despite the generally high viral loads observed for each variant. These viruses were monophyletic and equally divergent from HPgV and pegiviruses previously identified in chimpanzees (SPgVcpz). Overall, the high degree of conservation of genetic features among the novel SPgVs, HPgV and SPgVcpz suggests conservation of function among these closely related viruses. Our study describes the first primate pegiviruses detected in Old World monkeys, expanding the known genetic diversity and host range of pegiviruses and providing insight into the natural history of this genus. PMID:24918769

  18. Parasitology of five primates in Mahale Mountains National Park, Tanzania.

    PubMed

    Kooriyama, Takanori; Hasegawa, Hideo; Shimozuru, Michito; Tsubota, Toshio; Nishida, Toshisada; Iwaki, Takashi

    2012-10-01

    Parasitological surveillance in primates has been performed using coprological observation and identification of specimens from chimpanzees (Pan troglodytes schweinfurthii) in Mahale Mountains National Park, Tanzania (Mahale). In this study, we conducted coprological surveillance to identify the fauna of parasite infection in five primate species in Mahale: red colobus (Procolobus badius tephrosceles), red-tailed monkeys (Cercopithecus ascanius schmidti), vervet monkeys (Cercopithecus aethiops pygerythrus), yellow baboons (Papio cynocephalus), and chimpanzees. Fecal samples were examined microscopically, and parasite identification was based on the morphology of cysts, eggs, larvae, and adult worms. Three nematodes (Oesophagostomum spp., Strongyloides sp., and Trichuris sp.), Entamoeba coli, and Entamoeba spp. were found in all five primate species. The following infections were identified: Bertiella studeri was found in chimpanzees and yellow baboons; Balantidium coli was found in yellow baboons; three nematodes (Streptopharagus, Primasubulura, an undetermined genus of Spirurina) and Dicrocoeliidae gen. sp. were found in red-tailed monkeys, vervet monkeys, and yellow baboons; Chitwoodspirura sp. was newly identified in red colobus and red-tailed monkeys; Probstmayria gombensis and Troglocorys cava were newly identified in chimpanzees, together with Troglodytella abrassarti; and Enterobius sp. was newly identified in red colobus. The parasitological data reported for red colobus, vervet monkeys, and yellow baboons in Mahale are the first reports for these species. PMID:22661394

  19. Scapular Morphology and Forelimb Use during Foraging in Four Sympatric Cercopithecids.

    PubMed

    Dunham, Noah T; Kane, Erin E; McGraw, W Scott

    2015-01-01

    Most investigations of primate scapular morphology use differences in locomotion to explain variation; less is known about how scapular geometry covaries with nonlocomotor behavior. We examined forelimb use during foraging in 4 cercopithecids ranging throughout the Ivory Coast's Tai Forest. During 5-min feeding bouts, we recorded the frequency individuals of Piliocolobus badius, Colobus polykomos, Cercocebus atys and Cercopithecus diana performed 5 forelimb behaviors involved in the acquisition and introduction of food to the oral cavity. Scapulae from these populations were examined to determine whether differences in forelimb use were reflected in features known to correspond with varying degrees of arm flexion, abduction and elevation. Our results reveal that the species differ markedly in forelimb use and that these differences are interpretable via their scapular morphology. For example, P. badius engages in more frequent flexion, abduction and elevation of the arm above the head relative to C. polykomos, and red colobus scapulae are longer craniocaudally and have larger, more cranially directed supraspinous fossae than those of closely related black-and-white colobus. Our attempt to explore how nonlocomotor behavior covaries with skeletal morphology should provide for more informed interpretations of the primate fossil record. PMID:26745141

  20. Significance of color, calories, and climate to the visual ecology of catarrhines.

    PubMed

    Dominy, Nathaniel J; Lucas, Peter W

    2004-03-01

    Here we describe correlations among visual ecology and the physiochemical properties of fruits and leaves consumed by four species of catarrhine primate: Cercopithecus ascanius, Colobus guereza, Pan troglodytes, and Piliocolobus badius. Collectively, their diet was diverse, with each species relying on fruits and leaves to different extents. The mean chromaticity of both foods, as perceived by the green-red and yellow-blue signals that catarrhines decode, was distinct from background foliage. However, selection on the basis of color was evident only for leaves. Primates consumed leaves with higher green-red values than the leaves they avoided-sensory mechanism that correlated with key nutritional variables, such as increased protein and reduced toughness. Moreover, the monkeys ingested leaves near dusk, when reddish targets may be more salient. Similar patterns were never observed with respect to edible fruits, the chromaticities of which did not differ from unconsumed fruits or correlate with nutritional properties. We also found that primate biomass is higher in seasonal sites. We conclude that these findings are consistent with the notion that routine trichromatic vision evolved in a context where seasonal folivory was pivotal to survival. PMID:15027092

  1. Feeding and oral processing behaviors of two colobine monkeys in Tai Forest, Ivory Coast.

    PubMed

    McGraw, W Scott; van Casteren, Adam; Kane, Erin; Geissler, Elise; Burrows, Brittany; Daegling, David J

    2016-09-01

    We collected frequency data on oral processing behaviors during feeding in habituated groups of Western red colobus, Piliocolobus badius, and Western black and white, Colobus polykomos, ranging in the Ivory Coast's Tai National Park. During the sampling period, the diet of red colobus consisted of approximately 75% leaves compared to approximately 47% leaves and buds in black and white colobus. Black and white colobus chewed more frequently per ingestive event than did red colobus. Black and white colobus also employed their anterior teeth much more frequently than did red colobus, a difference attributed to the frequent consumption by C. polykomos of Pentaclethra macrophylla seeds and pods. A material analysis of these food items reveals that both the seed coating and seed flesh are quite soft; however, the pod housing the seeds is very tough. We argue that the pod's toughness, geometry, and fiber orientation collectively result in a food that is very difficult to process, resulting in long handling times and frequent, aggressive use of the incisors. We compare these data with those collected on another Tai primate-the sooty mangabey, Cercocebus atys-and demonstrate that during feeding, both colobine species use their incisors less than the mangabey, but that the cercopithecine chews less than either colobine. Combining data on oral processing behaviors with those on the material properties of items being ingested should lead to more informed interpretations of dentognathic morphology.

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

    PubMed

    Bonnell, Tyler R; Campennì, Marco; Chapman, Colin A; Gogarten, Jan F; Reyna-Hurtado, Rafael A; Teichroeb, Julie A; Wasserman, Michael D; Sengupta, Raja

    2013-01-01

    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.

  3. Is Markhamia lutea’s abundance determined by animal foraging?

    PubMed Central

    Chapman, Colin A.; Bonnell, Tyler R.; Sengupta, Raja; Goldberg, Tony L.; Rothman, Jessica M.

    2013-01-01

    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 14 years of data from Kibale National Park, Uganda, we quantify M. lutea flower and fruit production. Similarly, using 21 years of data, we quantify temporal changes in the abundance of stems in size classes from 1 m 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 7 years 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. PMID:24288436

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

    PubMed

    Chapman, Colin A; Schoof, Valérie A M; Bonnell, Tyler R; Gogarten, Jan F; Calmé, Sophie

    2015-05-26

    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.

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

    PubMed

    Chapman, Colin A; Schoof, Valérie A M; Bonnell, Tyler R; Gogarten, Jan F; Calmé, Sophie

    2015-05-26

    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. PMID:25870398

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

    PubMed Central

    Chapman, Colin A.; Schoof, Valérie A. M.; Bonnell, Tyler R.; Gogarten, Jan F.; Calmé, Sophie

    2015-01-01

    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. PMID:25870398

  7. Phylogenetic Relationships among the Colobine Monkeys Revisited: New Insights from Analyses of Complete mt Genomes and 44 Nuclear Non-Coding Markers

    PubMed Central

    Roos, Christian; Ting, Nelson; Chen, Cui Ping; Wang, Jing; Zhang, Ya Ping

    2012-01-01

    Background Phylogenetic relationships among Asian and African colobine genera have been disputed and are not yet well established. In the present study, we revisit the contentious relationships within the Asian and African Colobinae by analyzing 44 nuclear non-coding genes (>23 kb) and mitochondrial (mt) genome sequences from 14 colobine and 4 non-colobine primates. Principal Findings The combined nuclear gene and the mt genome as well as the combined nuclear and mt gene analyses yielded different phylogenetic relationships among colobine genera with the exception of a monophyletic ‘odd-nosed’ group consisting of Rhinopithecus, Pygathrix and Nasalis, and a monophyletic African group consisting of Colobus and Piliocolobus. The combined nuclear data analyses supported a sister-grouping between Semnopithecus and Trachypithecus, and between Presbytis and the odd-nosed monkey group, as well as a sister-taxon association of Pygathrix and Rhinopithecus within the odd-nosed monkey group. In contrast, mt genome data analyses revealed that Semnopithecus diverged earliest among the Asian colobines and that the odd-nosed monkey group is sister to a Presbytis and Trachypithecus clade, as well as a close association of Pygathrix with Nasalis. The relationships among these genera inferred from the analyses of combined nuclear and mt genes, however, varied with the tree-building methods used. Another remarkable finding of the present study is that all of our analyses rejected the recently proposed African colobine paraphyly and hybridization hypothesis and supported reciprocal monophyly of the African and Asian groups. Significance The phylogenetic utility of large-scale new non-coding genes was assessed using the Colobinae as a model, We found that these markers were useful for distinguishing nodes resulting from rapid radiation episodes such as the Asian colobine radiation. None of these markers here have previously been used for colobine phylogenetic reconstruction

  8. Co-infection and cross-species transmission of divergent Hepatocystis lineages in a wild African primate community★

    PubMed Central

    Thurber, Mary I.; Ghai, Ria R.; Hyeroba, Hyeroba; Weny, Geoffrey; Tumukunde, Alex; Chapman, Colin A.; Wiseman, Roger W.; Dinis, Jorge; Steeil, James; Greiner, Ellis C.; Friedrich, Thomas C.; O’Connor, David H.; Goldberg, Tony L.

    2013-01-01

    Hemoparasites of the apicomplexan family Plasmodiidae include the etiological agents of malaria, as well as a suite of non-human primate parasites from which the human malaria agents evolved. Despite the significance of these parasites for global health, little information is available about their ecology in multi-host communities. Primates were investigated in Kibale National Park, Uganda, where ecological relationships among host species are well characterized. Blood samples were examined for parasites of the genera Plasmodium and Hepatocystis using microscopy and PCR targeting the parasite mitochondrial cytochrome b gene, followed by Sanger sequencing. To assess co-infection, “deep sequencing” of a variable region within cytochrome b was performed. Out of nine black-and-white colobus (Colobus guereza), one blue guenon (Cercopithecus mitis), five grey-cheeked mangabeys (Lophocebus albigena), 23 olive baboons (Papio anubis), 52 red colobus (Procolobus rufomitratus) and 12 red-tailed guenons (Cercopithecus ascanius), 79 infections (77.5%) were found, all of which were Hepatocystis spp. Sanger sequencing revealed 25 different parasite haplotypes that sorted phylogenetically into six species-specific but morphologically similar lineages. “Deep sequencing” revealed mixed-lineage co-infections in baboons and red colobus (41.7% and 64.7% of individuals, respectively) but not in other host species. One lineage infecting red colobus also infected baboons, but always as the minor variant, suggesting directional cross-species transmission. Hepatocystis parasites in this primate community are a diverse assemblage of cryptic lineages, some of which co-infect hosts and at least one of which can cross primate species barriers. PMID:23603520

  9. Co-infection and cross-species transmission of divergent Hepatocystis lineages in a wild African primate community.

    PubMed

    Thurber, Mary I; Ghai, Ria R; Hyeroba, David; Weny, Geoffrey; Tumukunde, Alex; Chapman, Colin A; Wiseman, Roger W; Dinis, Jorge; Steeil, James; Greiner, Ellis C; Friedrich, Thomas C; O'Connor, David H; Goldberg, Tony L

    2013-07-01

    Hemoparasites of the apicomplexan family Plasmodiidae include the etiological agents of malaria, as well as a suite of non-human primate parasites from which the human malaria agents evolved. Despite the significance of these parasites for global health, little information is available about their ecology in multi-host communities. Primates were investigated in Kibale National Park, Uganda, where ecological relationships among host species are well characterized. Blood samples were examined for parasites of the genera Plasmodium and Hepatocystis using microscopy and PCR targeting the parasite mitochondrial cytochrome b gene, followed by Sanger sequencing. To assess co-infection, "deep sequencing" of a variable region within cytochrome b was performed. Out of nine black-and-white colobus (Colobus guereza), one blue guenon (Cercopithecus mitis), five grey-cheeked mangabeys (Lophocebus albigena), 23 olive baboons (Papio anubis), 52 red colobus (Procolobus rufomitratus) and 12 red-tailed guenons (Cercopithecus ascanius), 79 infections (77.5%) were found, all of which were Hepatocystis spp. Sanger sequencing revealed 25 different parasite haplotypes that sorted phylogenetically into six species-specific but morphologically similar lineages. "Deep sequencing" revealed mixed-lineage co-infections in baboons and red colobus (41.7% and 64.7% of individuals, respectively) but not in other host species. One lineage infecting red colobus also infected baboons, but always as the minor variant, suggesting directional cross-species transmission. Hepatocystis parasites in this primate community are a diverse assemblage of cryptic lineages, some of which co-infect hosts and at least one of which can cross primate species barriers. PMID:23603520

  10. Nodule Worm Infection in Humans and Wild Primates in Uganda: Cryptic Species in a Newly Identified Region of Human Transmission

    PubMed Central

    Ghai, Ria R.; Chapman, Colin A.; Omeja, Patrick A.; Davies, T. Jonathan; Goldberg, Tony L.

    2014-01-01

    Introduction Soil-transmitted helminths (STHs) are a major health concern in tropical and sub-tropical countries. Oesophagostomum infection is considered endemic to West Africa but has also been identified in Uganda, East Africa, among primates (including humans). However, the taxonomy and ecology of Oesophagostomum in Uganda have not been studied, except for in chimpanzees (Pan troglodytes), which are infected by both O. bifurcum and O. stephanostomum. Methods and Findings We studied Oesophagostomum in Uganda in a community of non-human primates that live in close proximity to humans. Prevalence estimates based on microscopy were lower than those based on polymerase chain reaction (PCR), indicating greater sensitivity of PCR. Prevalence varied among host species, with humans and red colobus (Procolobus rufomitratus) infected at lowest prevalence (25% and 41% by PCR, respectively), and chimpanzees, olive baboons (Papio anubis), and l'hoest monkeys (Cercopithecus lhoesti) infected at highest prevalence (100% by PCR in all three species). Phylogenetic regression showed that primates travelling further and in smaller groups are at greatest risk of infection. Molecular phylogenetic analyses revealed three cryptic clades of Oesophagostomum that were not distinguishable based on morphological characteristics of their eggs. Of these, the clade with the greatest host range had not previously been described genetically. This novel clade infects humans, as well as five other species of primates. Conclusions Multiple cryptic forms of Oesophagostomum circulate in the people and primates of western Uganda, and parasite clades differ in host range and cross-species transmission potential. Our results expand knowledge about human Oesophagostomum infection beyond the West African countries of Togo and Ghana, where the parasite is a known public health concern. Oesophagostomum infection in humans may be common throughout Sub-Saharan Africa, and the transmission of this neglected

  11. Fecal Microbiomes of Non-Human Primates in Western Uganda Reveal Species-Specific Communities Largely Resistant to Habitat Perturbation

    PubMed Central

    McCORD, ALEIA I.; CHAPMAN, COLIN A.; WENY, GEOFFREY; TUMUKUNDE, ALEX; HYEROBA, DAVID; KLOTZ, KELLY; KOBLINGS, AVERY S.; MBORA, DAVID N.M.; CREGGER, MELISSA; WHITE, BRYAN A.; LEIGH, STEVEN R.; GOLDBERG, TONY L.

    2014-01-01

    Primate gastrointestinal microbial communities are becoming increasingly appreciated for their relevance to comparative medicine and conservation, but the factors that structure primate “microbiomes” remain controversial. This study examined a community of primates in Kibale National Park, Uganda, to assess the relative importance of host species and location in structuring gastrointestinal microbiomes. Fecal samples were collected from primates in intact forest and from primates in highly disturbed forest fragments. People and livestock living nearby were also included, as was a geographically distant population of related red colobus in Kenya. A culture-free microbial community fingerprinting technique was used to analyze fecal microbiomes from 124 individual red colobus (Procolobus rufomitratus), 100 individual black-and-white colobus (Colobus guereza), 111 individual red-tailed guenons (Cercopithecus ascanius), 578 human volunteers, and 364 domestic animals, including cattle (Bos indicus and B. indicus × B. taurus crosses), goats (Caprus hircus), sheep (Ovis aries), and pigs (Sus scrofa). Microbiomes sorted strongly by host species, and forest fragmentation did not alter this pattern. Microbiomes of Kenyan red colobus sorted distinctly from microbiomes of Ugandan red colobus, but microbiomes from these two red colobus populations clustered more closely with each other than with any other species. Microbiomes from red colobus and black-and-white colobus were more differentiated than would be predicted by the phylogenetic relatedness of these two species, perhaps reflecting heretofore underappreciated differences in digestive physiology between the species. Within Kibale, social group membership influenced intra-specific variation among microbiomes. However, intra-specific variation was higher among primates in forest fragments than among primates in intact forest, perhaps reflecting the physical separation of fragments. These results suggest that, in this

  12. Host density and human activities mediate increased parasite prevalence and richness in primates threatened by habitat loss and fragmentation.

    PubMed

    Mbora, David N M; McPeek, Mark A

    2009-01-01

    1. Habitat loss and fragmentation are the principal causes of the loss of biological diversity. In addition, parasitic diseases are an emerging threat to many animals. Nevertheless, relatively few studies have tested how habitat loss and fragmentation influence the prevalence and richness of parasites in animals. 2. Several studies of nonhuman primates have shown that measures of human activity and forest fragmentation correlate with parasitism in primates. However, these studies have not tested for the ecological mechanism(s) by which human activities or forest fragmentation influence the prevalence and richness of parasites. 3. We tested the hypothesis that increased host density due to forest fragmentation and loss mediates increases in the prevalence and richness of gastrointestinal parasites in two forest primates, the Tana River red colobus (Procolobus rufomitratus, Peters 1879) and mangabey (Cercocebus galeritus galeritus, Peters 1879). We focused on population density because epidemiological theory states that host density is a key determinant of the prevalence and richness of directly transmitted parasites in animals. 4. The Tana River red colobus and mangabey are endemic to a highly fragmented forest ecosystem in eastern Kenya where habitat changes are caused by a growing human population increasingly dependent on forest resources and on clearing forest for cultivation. 5. We found that the prevalence of parasites in the two monkeys was very high compared to primates elsewhere. Density of monkeys was positively associated with forest area and disturbance in forests. In turn, the prevalence and richness of parasites was significantly associated with monkey density, and attributes indicative of human disturbance in forests. 6. We also found significant differences in the patterns of parasitism between the colobus and the mangabey possibly attributable to differences in their behavioural ecology. Colobus are arboreal folivores while mangabeys are terrestrial

  13. Fecal microbiomes of non-human primates in Western Uganda reveal species-specific communities largely resistant to habitat perturbation.

    PubMed

    McCord, Aleia I; Chapman, Colin A; Weny, Geoffrey; Tumukunde, Alex; Hyeroba, David; Klotz, Kelly; Koblings, Avery S; Mbora, David N M; Cregger, Melissa; White, Bryan A; Leigh, Steven R; Goldberg, Tony L

    2014-04-01

    Primate gastrointestinal microbial communities are becoming increasingly appreciated for their relevance to comparative medicine and conservation, but the factors that structure primate "microbiomes" remain controversial. This study examined a community of primates in Kibale National Park, Uganda, to assess the relative importance of host species and location in structuring gastrointestinal microbiomes. Fecal samples were collected from primates in intact forest and from primates in highly disturbed forest fragments. People and livestock living nearby were also included, as was a geographically distant population of related red colobus in Kenya. A culture-free microbial community fingerprinting technique was used to analyze fecal microbiomes from 124 individual red colobus (Procolobus rufomitratus), 100 individual black-and-white colobus (Colobus guereza), 111 individual red-tailed guenons (Cercopithecus ascanius), 578 human volunteers, and 364 domestic animals, including cattle (Bos indicus and B. indicus × B. taurus crosses), goats (Caprus hircus), sheep (Ovis aries), and pigs (Sus scrofa). Microbiomes sorted strongly by host species, and forest fragmentation did not alter this pattern. Microbiomes of Kenyan red colobus sorted distinctly from microbiomes of Ugandan red colobus, but microbiomes from these two red colobus populations clustered more closely with each other than with any other species. Microbiomes from red colobus and black-and-white colobus were more differentiated than would be predicted by the phylogenetic relatedness of these two species, perhaps reflecting heretofore underappreciated differences in digestive physiology between the species. Within Kibale, social group membership influenced intra-specific variation among microbiomes. However, intra-specific variation was higher among primates in forest fragments than among primates in intact forest, perhaps reflecting the physical separation of fragments. These results suggest that, in this