Coinfection of Ugandan Red Colobus (Procolobus [Piliocolobus] rufomitratus tephrosceles) with Novel, Divergent Delta-, Lenti-, and Spumaretroviruses ▿

PubMed Central

Goldberg, Tony L.; Sintasath, David M.; Chapman, Colin A.; Cameron, Kenneth M.; Karesh, William B.; Tang, Shaohua; Wolfe, Nathan D.; Rwego, Innocent B.; Ting, Nelson; Switzer, William M.

2009-01-01

Nonhuman primates host a plethora of potentially zoonotic microbes, with simian retroviruses receiving heightened attention due to their roles in the origins of human immunodeficiency viruses type 1 (HIV-1) and HIV-2. However, incomplete taxonomic and geographic sampling of potential hosts, especially the African colobines, has left the full range of primate retrovirus diversity unexplored. Blood samples collected from 31 wild-living red colobus monkeys (Procolobus [Piliocolobus] rufomitratus tephrosceles) from Kibale National Park, Uganda, were tested for antibodies to simian immunodeficiency virus (SIV), simian T-cell lymphotrophic virus (STLV), and simian foamy virus (SFV) and for nucleic acids of these same viruses using genus-specific PCRs. Of 31 red colobus tested, 22.6% were seroreactive to SIV, 6.4% were seroreactive to STLV, and 97% were seroreactive to SFV. Phylogenetic analyses of SIV polymerase (pol), STLV tax and long terminal repeat (LTR), and SFV pol and LTR sequences revealed unique SIV and SFV strains and a novel STLV lineage, each divergent from corresponding retroviral lineages previously described in Western red colobus (Procolobus badius badius) or black-and-white colobus (Colobus guereza). Phylogenetic analyses of host mitochondrial DNA sequences revealed that red colobus populations in East and West Africa diverged from one another approximately 4.25 million years ago. These results indicate that geographic subdivisions within the red colobus taxonomic complex exert a strong influence on retroviral phylogeny and that studying retroviral diversity in closely related primate taxa should be particularly informative for understanding host-virus coevolution. PMID:19692478

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

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.

Gastrointestinal parasites of the colobus monkeys of Uganda.

PubMed

Gillespie, Thomas R; Greiner, Ellis C; Chapman, Colin A

2005-06-01

From August 1997 to July 2003, we collected 2,103 fecal samples from free-ranging individuals of the 3 colobus monkey species of Uganda-the endangered red colobus (Piliocolobus tephrosceles), the eastern black-and-white colobus (Colobus guereza), and the Angolan black-and-white colobus (C. angolensis)--to identify and determine the prevalence of gastrointestinal parasites. Helminth eggs, larvae, and protozoan cysts were isolated by sodium nitrate flotation and fecal sedimentation. Coprocultures facilitated identification of helminths. Seven nematodes (Strongyloides fulleborni, S. stercoralis, Oesophagostomum sp., an unidentified strongyle, Trichuris sp., Ascaris sp., and Colobenterobius sp.), 1 cestode (Bertiella sp.), 1 trematode (Dicrocoeliidae), and 3 protozoans (Entamoeba coli, E. histolytica, and Giardia lamblia) were detected. Seasonal patterns of infection were not apparent for any parasite species infecting colobus monkeys. Prevalence of S. fulleborni was higher in adult male compared to adult female red colobus, but prevalence did not differ for any other shared parasite species between age and sex classes.

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

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

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

PubMed

Wahl-Jensen, Victoria; Johnson, Joshua C; Lauck, Michael; Weinfurter, Jason T; Moncla, Louise H; Weiler, Andrea M; Charlier, Olivia; Rojas, Oscar; Byrum, Russell; Ragland, Dan R; Huzella, Louis; Zommer, Erika; Cohen, Melanie; Bernbaum, John G; Caì, Yíngyún; Sanford, Hannah B; Mazur, Steven; Johnson, Reed F; Qin, Jing; Palacios, Gustavo F; Bailey, Adam L; Jahrling, Peter B; Goldberg, Tony L; O'Connor, David H; Friedrich, Thomas C; Kuhn, Jens H

2016-02-23

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. Outbreaks of simian hemorrhagic fever (SHF) have devastated captive

Partial Molecular Characterization of Two Simian Immunodeficiency Viruses (SIV) from African Colobids: SIVwrc from Western Red Colobus (Piliocolobus badius) and SIVolc from Olive Colobus (Procolobus verus)

PubMed Central

Courgnaud, Valerie; Formenty, Pierre; Akoua-Koffi, Chantal; Noe, Ronald; Boesch, Christophe; Delaporte, Eric; Peeters, Martine

2003-01-01

In order to study primate lentivirus evolution in the Colobinae subfamily, in which only one simian immunodeficiency virus (SIV) has been described to date, we screened additional species from the three different genera of African colobus monkeys for SIV infection. Blood was obtained from 13 West African colobids, and HIV cross-reactive antibodies were observed in 5 of 10 Piliocolobus badius, 1 of 2 Procolobus verus, and 0 of 1 Colobus polykomos specimens. Phylogenetic analyses of partial pol sequences revealed that the new SIVs were more closely related to each other than to the other SIVs and especially did not cluster with the previously described SIVcol from Colobus guereza. This study presents evidence that the three genera of African colobus monkeys are naturally infected with an SIV and indicates also that there was no coevolution between virus and hosts at the level of the Colobinae subfamily. PMID:12477880

Do food availability, parasitism, and stress have synergistic effects on red colobus populations living in forest fragments?

PubMed

Chapman, Colin A; Wasserman, Michael D; Gillespie, Thomas R; Speirs, Michaela L; Lawes, Michael J; Saj, Tania L; Ziegler, Toni E

2006-12-01

Identifying factors that influence animal density is a fundamental goal in ecology that has taken on new importance with the need to develop informed management plans. This is particularly the case for primates as the tropical forest that supports many species is being rapidly converted. We use a system of forest fragments adjacent to Kibale National Park, Uganda, to examine if food availability and parasite infections have synergistic affects on red colobus (Piliocolobus tephrosceles) abundance. Given that the size of primate populations can often respond slowly to environmental changes, we also examined how these factors influenced cortisol levels. To meet these objectives, we monitored gastrointestinal parasites, evaluated fecal cortisol levels, and determined changes in food availability by conducting complete tree inventories in eight fragments in 2000 and 2003. Red colobus populations declined by an average of 21% among the fragments; however, population change ranged from a 25% increase to a 57% decline. The cumulative basal area of food trees declined by an average of 29.5%; however, forest change was highly variable (a 2% gain to a 71% decline). We found that nematode prevalence averaged 58% among fragments (range 29-83%). The change in colobus population size was correlated both with food availability and a number of indices of parasite infections. A path analysis suggests that change in food availability has a strong direct effect on population size, but it also has an indirect effect via parasite infections. 2006 Wiley-Liss, Inc.

Primate vaginal microbiomes exhibit species specificity without universal Lactobacillus dominance.

PubMed

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

2014-12-01

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

No evidence for transmission of SIVwrc from western red colobus monkeys (piliocolobus badius badius) to wild west african chimpanzees (pan troglodytes verus) despite high exposure through hunting

PubMed Central

2011-01-01

Background Simian Immunodeficiency Viruses (SIVs) are the precursors of Human Immunodeficiency Viruses (HIVs) which have lead to the worldwide HIV/AIDS pandemic. By studying SIVs in wild primates we can better understand the circulation of these viruses in their natural hosts and habitat, and perhaps identify factors that influence susceptibility and transmission within and between various host species. We investigated the SIV status of wild West African chimpanzees (Pan troglodytes verus) which frequently hunt and consume the western red colobus monkey (Piliocolobus badius badius), a species known to be infected to a high percentage with its specific SIV strain (SIVwrc). Results Blood and plasma samples from 32 wild chimpanzees were tested with INNO-LIA HIV I/II Score kit to detect cross-reactive antibodies to HIV antigens. Twenty-three of the samples were also tested for antibodies to 43 specific SIV and HIV lineages, including SIVwrc. Tissue samples from all but two chimpanzees were tested for SIV by PCRs using generic SIV primers that detect all known primate lentiviruses as well as primers designed to specifically detect SIVwrc. Seventeen of the chimpanzees showed varying degrees of cross-reactivity to the HIV specific antigens in the INNO-LIA test; however no sample had antibodies to SIV or HIV strain - and lineage specific antigens in the Luminex test. No SIV DNA was found in any of the samples. Conclusions We could not detect any conclusive trace of SIV infection from the red colobus monkeys in the chimpanzees, despite high exposure to this virus through frequent hunting. The results of our study raise interesting questions regarding the host-parasite relationship of SIVwrc and wild chimpanzees in their natural habitat. PMID:21284842

Characterization of the Fecal Microbiome from Non-Human Wild Primates Reveals Species Specific Microbial Communities

PubMed Central

Yildirim, Suleyman; Yeoman, Carl J.; Sipos, Maksim; Torralba, Manolito; Wilson, Brenda A.; Goldberg, Tony L.; Stumpf, Rebecca M.; Leigh, Steven R.; White, Bryan A.; Nelson, Karen E.

2010-01-01

Background Host-associated microbes comprise an integral part of animal digestive systems and these interactions have a long evolutionary history. It has been hypothesized that the gastrointestinal microbiome of humans and other non-human primates may have played significant roles in host evolution by facilitating a range of dietary adaptations. We have undertaken a comparative sequencing survey of the gastrointestinal microbiomes of several non-human primate species, with the goal of better understanding how these microbiomes relate to the evolution of non-human primate diversity. Here we present a comparative analysis of gastrointestinal microbial communities from three different species of Old World wild monkeys. Methodology/Principal Findings We analyzed fecal samples from three different wild non-human primate species (black-and-white colobus [Colubus guereza], red colobus [Piliocolobus tephrosceles], and red-tailed guenon [Cercopithecus ascanius]). Three samples from each species were subjected to small subunit rRNA tag pyrosequencing. Firmicutes comprised the vast majority of the phyla in each sample. Other phyla represented were Bacterioidetes, Proteobacteria, Spirochaetes, Actinobacteria, Verrucomicrobia, Lentisphaerae, Tenericutes, Planctomycetes, Fibrobacateres, and TM7. Bray-Curtis similarity analysis of these microbiomes indicated that microbial community composition within the same primate species are more similar to each other than to those of different primate species. Comparison of fecal microbiota from non-human primates with microbiota of human stool samples obtained in previous studies revealed that the gut microbiota of these primates are distinct and reflect host phylogeny. Conclusion/Significance Our analysis provides evidence that the fecal microbiomes of wild primates co-vary with their hosts, and that this is manifested in higher intraspecies similarity among wild primate species, perhaps reflecting species specificity of the microbiome in

Full-Length Genome Characterization of a Novel Simian Immunodeficiency Virus Lineage (SIVolc) from Olive Colobus (Procolobus verus) and New SIVwrcPbb Strains from Western Red Colobus (Piliocolobus badius badius) from the Taï Forest in Ivory Coast▿

PubMed Central

Liégeois, Florian; Lafay, Bénédicte; Formenty, Pierre; Locatelli, Sabrina; Courgnaud, Valérie; Delaporte, Eric; Peeters, Martine

2009-01-01

Simian immunodeficiency viruses (SIVs) are found in an extensive number of African primates and humans continue to be exposed to these viruses by hunting and handling of primate bushmeat. Full-length genome sequences were obtained from SIVs derived from two Colobinae species inhabiting the Taï forest, Ivory Coast, each belonging to a different genus: SIVwrc from western red colobus (Piliocolobus badius badius) (SIVwrcPbb-98CI04 and SIVwrcPbb-97CI14) and SIVolc (SIVolc-97CI12) from olive colobus (Procolobus verus). Phylogenetic analysis showed that western red colobus are the natural hosts of SIVwrc, and SIVolc is also a distinct species-specific lineage, although distantly related to the SIVwrc lineage across the entire length of its genome. Overall, both SIVwrc and SIVolc, are also distantly related to the SIVlho/sun lineage across the whole genome. Similar to the group of SIVs (SIVsyk, SIVdeb, SIVden, SIVgsn, SIVmus, and SIVmon) infecting members of the Cercopithecus genus, SIVs derived from western red and olive colobus, L'Hoest and suntailed monkeys, and SIVmnd-1 from mandrills form a second group of viruses that cluster consistently together in phylogenetic trees. Interestingly, the divergent SIVcol lineage, from mantled guerezas (Colobus guereza) in Cameroon, is also closely related to SIVwrc, SIVolc, and the SIVlho/sun lineage in the 5′ part of Pol. Overall, these results suggest an ancestral link between these different lentiviruses and highlight once more the complexity of the natural history and evolution of primate lentiviruses. PMID:18922864

Absence of Frequent Herpesvirus Transmission in a Nonhuman Primate Predator-Prey System in the Wild

PubMed Central

Murthy, Sripriya; Couacy-Hymann, Emmanuel; Metzger, Sonja; Nowak, Kathrin; De Nys, Helene; Boesch, Christophe; Wittig, Roman; Jarvis, Michael A.; Leendertz, Fabian H.

2013-01-01

Emergence of viruses into the human population by transmission from nonhuman primates (NHPs) represents a serious potential threat to human health that is primarily associated with the increased bushmeat trade. Transmission of RNA viruses across primate species appears to be relatively frequent. In contrast, DNA viruses appear to be largely host specific, suggesting low transmission potential. Herein, we use a primate predator-prey system to study the risk of herpesvirus transmission between different primate species in the wild. The system was comprised of western chimpanzees (Pan troglodytes verus) and their primary (western red colobus, Piliocolobus badius badius) and secondary (black-and-white colobus, Colobus polykomos) prey monkey species. NHP species were frequently observed to be coinfected with multiple beta- and gammaherpesviruses (including new cytomegalo- and rhadinoviruses). However, despite frequent exposure of chimpanzees to blood, organs, and bones of their herpesvirus-infected monkey prey, there was no evidence for cross-species herpesvirus transmission. These findings suggest that interspecies transmission of NHP beta- and gammaherpesviruses is, at most, a rare event in the wild. PMID:23885068

Absence of frequent herpesvirus transmission in a nonhuman primate predator-prey system in the wild.

PubMed

Murthy, Sripriya; Couacy-Hymann, Emmanuel; Metzger, Sonja; Nowak, Kathrin; De Nys, Helene; Boesch, Christophe; Wittig, Roman; Jarvis, Michael A; Leendertz, Fabian H; Ehlers, Bernhard

2013-10-01

Emergence of viruses into the human population by transmission from nonhuman primates (NHPs) represents a serious potential threat to human health that is primarily associated with the increased bushmeat trade. Transmission of RNA viruses across primate species appears to be relatively frequent. In contrast, DNA viruses appear to be largely host specific, suggesting low transmission potential. Herein, we use a primate predator-prey system to study the risk of herpesvirus transmission between different primate species in the wild. The system was comprised of western chimpanzees (Pan troglodytes verus) and their primary (western red colobus, Piliocolobus badius badius) and secondary (black-and-white colobus, Colobus polykomos) prey monkey species. NHP species were frequently observed to be coinfected with multiple beta- and gammaherpesviruses (including new cytomegalo- and rhadinoviruses). However, despite frequent exposure of chimpanzees to blood, organs, and bones of their herpesvirus-infected monkey prey, there was no evidence for cross-species herpesvirus transmission. These findings suggest that interspecies transmission of NHP beta- and gammaherpesviruses is, at most, a rare event in the wild.

Female transference and mate choice among Tana River red colobus.

PubMed

Marsh, C W

1979-10-18

Red colobus are one of a small number of primate species in which females have been reported to transfer between breeding groups more commonly than males. Several authors have hypothesised that in such species transference may serve to reduce the risk to females of producing offspring of lower fitness through inbreeding. The hypothesis offers no explanation of why females rather than males are responsible for outbreeding in these species, but remains plausible so long as male membership of breeding groups is relatively stable; for once members of one sex have evolved dispersal mechanisms reducing the risk of inbreeding, pressures on the other sex to do likewise will be lowered. Hence, if both sexes commonly migrate, the hypothesis is weakened. I describe here the membership dynamics of a group of Tana River red colobus, Colobus badius rufomitratus, which provide the first evidence of high rates of membership turnover by both sexes in primates, and speculate that the function of female transference in this case may be related to mate choice and the avoidance of infanticide.

Feeding behaviour of red colobus and black and white colobus in East Africa.

PubMed

Clutton-Brock, T H

1975-01-01

The feeding behaviour of one troop of red colobus (Colobus badius tephrosceles) was observed between August 1969 and June 1970 in the Gombe National Park. Similar observations were made on two troops of red colobus and two of black and white colobus (C. guereza uellensis) in Kibale Forest Reserve, Uganda, between August and October 1970. The red colobus at Gombe were highly selective in their choice of food, feeding on the leaves, shoots, flowers and fruit of a wide variety of tree species. The animals appeared to choose a varied diet, eating different foods in different feeding bouts on the same day. The amount of time which they spent feeding on different foods varied seasonally, usually in association with changes in food availability. Different parts of the animals' range provided them with different kinds of food. The feeding behaviour of the red colobus troops at Kibale was similar to that of the Bombe troop. In contrast, black and white colobus at Kibale fed almost exclusively on mature leaves during at least one period of the year and fed largely on two tree species only. These differences in feeding behaviour may explain why red colobus live in large troops in large ranges whiel black and white colobus live in small troops in small ranges.

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.

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. © 2015 The Author(s) Published by the Royal Society. All rights reserved.

Craniofacial variation and dietary adaptations of African colobines.

PubMed

Koyabu, Daisuke B; Endo, Hideki

2009-06-01

African colobine monkeys show considerable craniofacial variation among species, although the evolutionary causes of this diversity are unclear. In light of growing evidence that diet varies considerably among colobine species, we investigated whether colobine craniofacial morphology varies as a function of their diet. We compared craniofacial morphology among five African species: Colobus angolensis, C. guereza, C. polykomos, Piliocolobus badius, and P. verus. Matrix correlation analysis indicated a significant correlation between species-specific morphological distance and dietary distance matrices. The mechanical advantage of the masseter muscle was higher in seed-eaters (C. angolensis and C. polykomos) and lower in those that eat mainly young leaves (C. guereza, P. badius, and P. verus). Canonical correspondence analysis revealed that the durophagous colobines possess relatively wider bigonial breadths, anteroposteriorly shorter faces, shorter postcanine tooth rows, more medially positioned dental batteries, wider bizygomatic arches, and anteroposteriorly longer zygomatic arches. Under the constrained lever model, these morphological features suggest that durophagous colobines have the capacity to generate relatively greater maximum bite forces. However, no consistent relationship was observed between diet and variation in the mandibular corpus and symphysis, implying that robust mandibles are not necessarily adaptations for stress resistance. Factors that may influence mandibular robusticity include allometry of symphyseal curvature and canine tooth support. Finally, linear measures of mandibular robusticity may suffer from error.