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Social and Ecological Correlates of Parasitic Infections in Adult Male Gray-Cheeked Mangabeys (Lophocebus albigena)

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Abstract

Intestinal parasites may constitute an important evolutionary and ecological force. We aimed to identify social, physiological, and environmental factors that correlate with intestinal parasite infections in adult male gray-cheeked mangabeys (Lophocebus albigena). We analyzed 102 fecal samples collected from 18 adult males over 19 mo for the incidence (proportions of samples with parasites) and intensity (total number of parasites per gram of feces) of infection of nematodes relative to social status, fecal glucocorticoid and testosterone metabolites, group size, and rainfall, all of which are factors that earlier studies suggested can be important mediators of parasite load. Parasite incidence was greater in immigrant males compared to low- and high-ranking males whereas parasite intensity was greater in immigrant males and low-ranking males compared to high-ranking males. Fecal samples with more parasites had higher concentrations of fecal glucocorticoid and testosterone metabolites than those with fewer parasites. As immigrant males had a greater incidence of parasites and higher concentrations of both metabolites than resident males, this profile appears to fit immigrant males best. We also found higher nematode intensities in mid-sized groups and during periods with more rainfall. Our results suggest that it will be fruitful for future studies to explore the role of immigrant males as spreaders of intestinal parasites.

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References

  • Alberts, S. C., Sapolsky, R. M., & Altmann, J. (1992). Behavioral, endocrine, and immunological correlates of immigration by an aggressive male into a natural primate group. Hormones and Behavior, 26, 167–178.

    Article  CAS  PubMed  Google Scholar 

  • Altizer, S., Nunn, C. L., Thrall, P. H., Gittleman, J. L., Antonovics, J., Cunningham, A. A., Dobson, A. P., Ezenwa, V., Jones, K. E., Pedersen, A. B., Poss, M., & Pulliam, J. R. C. (2003). Social organization and parasite risk in mammals: Integrating theory and empirical studies. Annual Review of Ecology, Evolution, and Systematics, 34, 517–547.

    Article  Google Scholar 

  • Arlet, M. E., Carey, J. R., & Molleman, F. (2009a). Species and sex differences in type and frequencies of injuries and impairments among four arboreal primate species in Kibale National Park, Uganda. Primates, 50, 65–73.

    Article  PubMed  Google Scholar 

  • Arlet, M. E., Grote, M. N., Isbell, L. A., Molleman, F., & Carey, J. R. (2009b). Reproductive tactics influence cortisol levels in individual male mangabeys (Lophocebus albigena). Hormones and Behavior, 55, 210–216.

    Article  CAS  PubMed  Google Scholar 

  • Arlet, M. E., & Isbell, L. A. (2009). Variation in behavioral and hormonal responses of adult male mangabeys (Lophocebus albigena) to crowned eagles (Stephanoaetus coronatus) in Kibale National Park, Uganda. Behavioral Ecology and Sociobiology, 63, 491–499.

    Article  Google Scholar 

  • Arlet, M. E., Isbell, L. A., Kaasik, A., Molleman, F., Chancellor, R. L., Chapman, C. A., Mänd, R., & Carey, J. R. (2015). Determinants of reproductive performance among female gray-cheeked mangabeys (Lophocebus albigena) in Kibale National Park, Uganda. International Journal of Primatology, 36, 55–73.

    Article  Google Scholar 

  • Arlet, M. E., Kaasik, A., Molleman, F., Isbell, L. A., Carey, J. R., & Mänd, R. (2011). Social factors increase fecal testosterone levels in wild male gray-cheeked mangabeys (Lophocebus albigena). Hormones and Behavior, 59, 605–611.

    Article  CAS  PubMed  Google Scholar 

  • Arlet, M. E., Molleman, F., & Chapman, C. A. (2008). Mating tactics in male grey-cheeked mangabeys (Lophocebus albigena). Ethology, 114, 841–852.

    Article  Google Scholar 

  • Bailey, M. T., & Coe, C. L. (1999). Maternal separation disrupts the integrity of the intestinal microflora in infant rhesus monkeys. Developmental Psychology, 35, 146–155.

    Article  CAS  Google Scholar 

  • Barrett, G. M., Shimizu, K., Bardi, M., Asaba, S., & Mori, A. (2002). Endocrine correlates of rank, reproduction, and female-directed aggression in male Japanese macaques (Macaca fuscata). Hormones and Behavior, 42, 85–96.

    Article  CAS  PubMed  Google Scholar 

  • Bates, D., Maechler, M., Bolker, B. (2011). lme4: linear mixed--effects models using S4 classes. R package version 0.999375-41/r1341. http://R-Forge.R-project.org/projects/lme4/.

  • Bercovitch, F. B. (1993). Dominance rank and reproductive maturation in rhesus macaques (Macaca mulatta). Journal of Reproduction and Fertility, 99, 113–120.

    Article  CAS  PubMed  Google Scholar 

  • Bradley, A. J., McDonald, I. R., & Lee, A. K. (1980). Stress and mortality in a small marsupial (Antechinus stuartii, Macleay). General and Comparative Endocrinology, 40, 188–200.

    Article  CAS  PubMed  Google Scholar 

  • Braude, S., Tang-Martinez, Z., & Taylor, G. T. (1999). Stress, testosterone and the immunoredistribution hypothesis. Behavioral Ecology, 10, 345–350.

    Article  Google Scholar 

  • Burrell, A. S., Jolly, C. J., Tosi, A. J., & Disotell, T. R. (2009). Mitochondrial evidence for the hybrid origin of the kipunji, Rungwecebus kipunji (Primates: Papionini). Molecular Phylogenetics and Evolution, 51, 340–348.

    Article  CAS  PubMed  Google Scholar 

  • Cavigelli, S. A., & Pereira, M. E. (2000). Mating season aggression and fecal testosterone levels in male ring-tailed lemurs (Lemur catta). Hormones and Behavior, 37, 246–278.

    Article  CAS  PubMed  Google Scholar 

  • Chapman, C. A., Bowman, D. D., Ghai, R. R., Goldberg, T. L., Gogarten, J. F., Rothman, J. M., Twinomugisha, D., & Walsh, C. (2012). Protozoan parasites in group-living primates: Testing the biological island hypothesis. American Journal of Primatology, 74, 510–517.

    Article  PubMed  Google Scholar 

  • Chapman, C. A., Chapman, L. J., & Gillespie, T. R. (2002). Scale issues in the study of primate foraging: Red colobus of Kibale National Park. American Journal of Physical Anthropology, 117, 349–363.

    Article  PubMed  Google Scholar 

  • Chapman, C. A., & Lambert, J. E. (2000). Habitat alteration and the conservation of African primates: A case study of Kibale National Park, Uganda. American Journal of Primatology, 50, 169–186.

    Article  CAS  PubMed  Google Scholar 

  • Chapman, C. A., Rothman, J. M., & Hodder, S. A. M. (2009). Can parasites be a selective force influencing primate group size? A test with red colobus. In M. A. Huffman & C. A. Chapman (Eds.), Primate parasite ecology: The dynamics and study of host–parasite relationships. Cambridge Studies in Biological and Evolutionary Anthropology (pp. 423–440). Cambridge, U.K.: Cambridge University Press.

  • Chapman, C. A., Wasserman, M. D., Gillespie, T. R., Speirs, M. L., Lawes, M. J., Saj, T. L., & Ziegler, T. E. (2006). Do food availability, parasitism, and stress have synergistic effects on red colobus populations living in forest fragments? American Journal of Physical Anthropology, 131, 525–534.

    Article  PubMed  Google Scholar 

  • Crockford, C., Wittig, R. M., Whitten, P. L., Seyfarth, R. M., & Cheney, D. L. (2008). Social stressors and coping mechanisms in wild female baboons (Papio hamadryas ursinus). Hormones and Behavior, 53, 254–265.

    Article  PubMed  Google Scholar 

  • Davies, C. R., Ayres, J. M., Dye, C., & Deane, L. M. (1991). Malaria infection rate of Amazonian primates increases with body weight and group size. Functional Ecology, 5, 655–662.

    Article  Google Scholar 

  • Eckert, K. A., Hahn, N. E., Genz, A., Kitchen, D. M., Stuart, M. D., Averbeck, G. A., Stromberg, B. E., & Markowitz, H. (2006). Coprological surveys of Alouatta pigra at two sites in Belize. International Journal of Primatology, 27, 227–238.

    Article  Google Scholar 

  • Ezenwa, V. O. (2003). Habitat overlap and gastrointestinal parasitism in sympatric African bovids. Parasitology, 126, 379–388.

    Article  CAS  PubMed  Google Scholar 

  • Ezenwa, V. O., Ekernas, L. S., & Creel, S. (2012). Unravelling complex associations between testosterone and parasite infection in the wild. Functional Ecology, 26, 123–133.

    Article  Google Scholar 

  • Freeland, W. J. (1979). Primate social groups as biological islands. Ecology, 60, 719–728.

    Article  Google Scholar 

  • Friedman, E. M., & Lawrence, D. A. (2002). Environmental stress mediates changes in neuroimmunological interactions. Toxicological Sciences, 67, 4–10.

    Article  CAS  PubMed  Google Scholar 

  • Gillespie, T. R., Greiner, E. C., & Chapman, C. A. (2004). Gastrointestinal parasites of the guenons of western Uganda. Journal of Parasitology, 90, 1356–1360.

    Article  PubMed  Google Scholar 

  • Griffin, R. H., & Nunn, C. L. (2012). Community structure and the spread of infectious disease in primate social networks. Evolutionary Ecology, 26, 779–800.

    Article  Google Scholar 

  • Gordon, T. P., Rose, R. M., & Bernstein, I. S. (1976). Seasonal rhythm in plasma testosterone levels in the rhesus monkey (Macaca mulatta): A three-year study. Hormones and Behavior, 98, 168–175.

    Google Scholar 

  • Gulland, F. M. D. (1992). The role of nematode parasites in Soay sheep (Ovis aries L.) mortality during a population crash. Parasitological Research, 105, 493–503.

    Google Scholar 

  • Habig, B., & Archie, E. A. (2015). Social status, immune response and parasitism in males: A meta-analysis. Philosophical Transactions of the Royal Society of London B: Biological Sciences, 370, 20140109.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Harcourt, A. H. (1987). Dominance and fertility among female primates. Journal of Zoology, London, 213, 471–487.

    Article  Google Scholar 

  • Harris, E. E., & Disotell, T. R. (1998). Nuclear gene trees and the phylogenetic relationships of the mangabeys (Primaes: Papionini). Molecular Biology and Evolution, 15, 892–900.

    Article  CAS  PubMed  Google Scholar 

  • Hausfater, G., & Meade, B. J. (1982). Alternation of sleeping groves by yellow baboons (Papio cynocephalus) as a strategy for parasite avoidance. Primates, 23, 287–297.

    Article  Google Scholar 

  • Hausfater, G., & Watson, D. F. (1976). Social and reproductive correlates of parasite ova emissions by baboons. Nature, 262, 688–689.

    Article  CAS  PubMed  Google Scholar 

  • Higham, J. P., Heistermann, M., & Maestripieri, D. (2013). The endocrinology of male rhesus macaque social and reproductive status: A test of the challenge and social stress hypotheses. Behavioral Ecology and Sociobiology, 67, 19–30.

    Article  PubMed  PubMed Central  Google Scholar 

  • Howells, M. E., Pruetz, J., & Gillespie, T. R. (2010). Patterns of gastro-intestinal parasites and commensals as an index of population and ecosystem health: The case of sympatric western chimpanzees (Pan troglodytes verus) and guinea baboons (Papio hamadryas papio) at Fongoli, Senegal. American Journal of Primatology, 71, 1–7.

    Google Scholar 

  • Huffman, M. A., Gotoh, S., Turner. L. A., Hamai, M., & Yoshida, K. (1997). Seasonal trends in intestinal nematode infection and medicinal plant use among chimpanzees in the Mahale Mountains, Tanzania. Primates, 38, 111–125.

  • Huffman, M. A., & Chapman, C. A. (2009). Primate parasite ecology: The dynamics and study of host-parasite relationships. Cambridge, U.K.: Cambridge University Press.

    Google Scholar 

  • Jackson, L. A., & Farmer, J. N. (1970). Effect of host fighting behavior on the course of infection of Trypanosoma duttoni in mice. Ecology, 51, 672–679.

    Article  Google Scholar 

  • Janmaat, K. R., Olupot, W., Chancellor, R. L., Arlet, M. E., & Waser, P. M. (2009). Long-term site fidelity and individual home range shifts in grey-cheeked mangabeys. International Journal of Primatology, 30, 443–466.

    Article  PubMed  PubMed Central  Google Scholar 

  • Jessee, M. T., Schilling, P. W., & Stunkard, J. A. (1970). Identification of intestinal helminth eggs in Old World primates. Laboratory Animal Care, 20, 83–87.

    CAS  PubMed  Google Scholar 

  • Kraus, C., Heistermann, M., & Kappeler, P. M. (1999). Physiological suppression of sexual function of subordinate males: A subtle form of intrasexual competition among male sifakas (Propithecus verreauxi)? Physiology and Behavior, 66, 855–861.

    Article  CAS  PubMed  Google Scholar 

  • McEwen, B. S., & Stellar, E. (1993). Stress and the individual. Mechanisms leading to disease. Arch Intern Med 153, 2093–101.

  • McGrew, W. C., Tutin, C. E. G., Collins, D. A., & File, S. K. (1989). Intestinal parasites of sympatric Pan troglodytes and Papio spp. at two sites: Gombe (Tanzania) and Mt. Assirik (Senegal). American Journal of Primatology, 17, 147–155.

    Article  Google Scholar 

  • Møller, A., Dufva, R., & Allander, K. (1993). Parasites and the evolution of host social behavior. Advances in the Study of Behavior, 22, 65–102.

    Article  Google Scholar 

  • Mougeot, F., Redpath, S. M., & Piertney, S. (2006). Elevated spring testosterone increases parasite intensity in male red grouse. Behavioral Ecology, 17, 117–125.

    Article  Google Scholar 

  • Muehlenbein, M. P. (2006). Intestinal parasite infections and fecal steroid levels in wild chimpanzees. American Journal of Physical Anthropology, 130, 546–550.

    Article  PubMed  Google Scholar 

  • Muehlenbein, M. P. (2009). The application of endocrine measures in primate parasite ecology. In M. A. Huffman & C. A. Chapman (Eds.), Primate parasite ecology: The dynamics and study of host–parasite relationships. Cambridge, U.K.: Cambridge University Press.

    Google Scholar 

  • Muehlenbein, M. P., & Bribiescas, R. G. (2005). Testosterone-mediated immune functions and male life histories. American Journal of Human Biology, 17, 527–558.

    Article  PubMed  Google Scholar 

  • Muehlenbein, M. P., & Watts, D. P. (2010). The costs of dominance: Testosterone, cortisol and intestinal parasites in wild male chimpanzees. BioPsychoSocial Medicine, 4, 21.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Muehlenbein, M. P., Watts, D. P., & Whitten, P. L. (2004). Dominance rank and fecal testosterone in adult male chimpanzees (Pan troglodytes scheinfurthii) at Ngogo, Kibale National Park, Uganda. American Journal of Primatology, 64, 71–82.

    Article  PubMed  Google Scholar 

  • Muller-Graf, C. D. M., Collins, D. A., & Woolhouse, M. E. J. (1996). Intestinal parasite burden in five troops of olive baboons (Papio cynocephalus anubis) in Gombe Stream National Park, Tanzania. Parasitology, 112, 489–497.

    Article  PubMed  Google Scholar 

  • Munck, A., Guyre, P., & Holbrook, N. (1984). Physiological functions of glucocorticoids during stress and their relation to pharmacological actions. Endocrine Reviews, 5, 25–47.

    Article  CAS  PubMed  Google Scholar 

  • Munro, C., & Stabenfeldt, G. (1984). Development of cortisol enzyme immunoassay in plasma. Clinical Chemistry, 31, 985.

    Google Scholar 

  • Negro, S. S., Caudron, A. K., Dubois, M., Delahaut, P., & Gemmell, N. J. (2010). Correlation between male social status, testosterone levels, and parasitism in a dimorphic polygynous mammal. PLoS ONE. doi:10.1371/journal.pone.0012507.

    Google Scholar 

  • Nunn, C. L. (2002a). A comparative study of leukocyte counts and disease risk in primates. Evolution, 56, 177–190.

    Article  PubMed  Google Scholar 

  • Nunn, C. L. (2002b). Spleen size, disease risk and sexual selection: A comparative study in primates. Evolutionary Ecology Research, 4, 91–107.

    Google Scholar 

  • Nunn, C. L., & Altizer, S. M. (2006). Infectious diseases in primates: Behavior, ecology and evolution. Oxford: Oxford University Press.

    Book  Google Scholar 

  • Nunn, C. L., Gittelman, J. L., & Antonovics, J. (2000). Promiscuity and the primate immune system. Science, 290, 1168–1170.

    Article  CAS  PubMed  Google Scholar 

  • Olupot, W. (1999). Mangabey dispersal and conservation in Kibale Forest National Park, Uganda. Doctoral Dissertation, Purdue University.

  • Olupot, W., & Waser, P. M. (2001a). Correlates of intergroup patterns in male grey-cheeked mangabeys. International Journal of Primatology, 22, 169–187.

    Article  Google Scholar 

  • Olupot, W., & Waser, P. M. (2001b). Activity patterns, habitat use and mortality risks of mangabey males living outside social groups. Animal Behaviour, 61, 1227–1235.

    Article  Google Scholar 

  • Olupot, W., & Waser, P. M. (2005). Patterns of male residency and inter-troop transfer in mangabeys (Lophocebus albigena). American Journal of Primatology, 66, 331–349.

    Article  PubMed  Google Scholar 

  • Peters, A. (2000). Testosterone treatment is immunosuppressive in superb fairy-wrens, yet free-living males with high testosterone are more immunocompetent. Proceedings of the Royal Society of London B: Biological Sciences, 267, 883–889.

    Article  CAS  Google Scholar 

  • Prall, S. P., & Muehlenbein, M. P. (2013). Testosterone and immune function in primates: A brief summary with methodological considerations. International Journal of Primatology, 35, 805–824.

    Article  Google Scholar 

  • Pusey, A., & Packer, C. (1997). The ecology of relationships. In J. R. Krebs & N. B. Davies (Eds.), Behavioural ecology: An evolutionary approach (4th ed., pp. 254–284). New York: Blackwell.

    Google Scholar 

  • R Development Core Team. (2011). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, austria. http://www.R-project.org/.

  • Rifkin, J. L., Nunn, C. L., & Garamszegi, L. Z. (2012). Do animals living in larger groups experience greater parasitism? A meta-analysis. American Naturalist, 180, 70–82.

    Article  PubMed  Google Scholar 

  • Rose, R. M., Bernstein, I. S., & Gordon, T. P. (1975). Consequences of social conflict on plasma testosterone levels in rhesus monkeys. Psychosomatic Medicine, 37, 50–60.

    Article  CAS  PubMed  Google Scholar 

  • Salvador, A., Veiga, J. P., Martin, J., Lopez, P., Abelenda, M., & Puerta, M. (1996). The cost of producing a sexual signal: Testosterone increases the susceptibility of male lizards to ectoparasite infestation. Behavioral Ecology, 7, 145–150.

    Article  Google Scholar 

  • Sannen, A., van Elsacker, L., Heistermann, M., & Eens, M. (2004). Urinary testosterone-metabolite levels and dominance rank in male and female bonobos (Pan paniscus). Primates, 45, 89–96.

    Article  PubMed  Google Scholar 

  • Sapolsky, R. M. (1992). Cortisol concentrations and the social significance of rank instability among wild baboons. Psychoneuroendocrinology, 17, 701–709.

    Article  CAS  PubMed  Google Scholar 

  • Sapolsky, R. M. (1993). Neuroendocrinology of the stress-response. In J. B. Becker, S. M. Breedlove, & D. Crews (Eds.), Behavioral endocrinology (pp. 287–324). Cambridge: MIT Press.

    Google Scholar 

  • Sapolsky, R. M. (2004). Social status and health in humans and other animals. Annual Review of Anthropology, 33, 393–418.

    Article  Google Scholar 

  • Sapolsky, R. M. (2005). The influence of social hierarchy on primate health. Science, 5722, 648–652.

    Article  CAS  Google Scholar 

  • Sapolsky, R. M., Alberts, S. C., & Altmann, J. (1997). Hypercortisolism associated with social subordinance or social isolation among wild baboons. Archives of General Psychiatry, 54, 1137–1143.

    Article  CAS  PubMed  Google Scholar 

  • Sapolsky, R. M., & Spencer, E. M. (1997). Insulin-like growth factor I is suppressed in socially subordinate male baboons. American Journal of Physiology, 273, 1347–1351.

    Google Scholar 

  • Semple, S., Cowlishaw, G., & Bennett, P. M. (2002). Immune system evolution among anthropoid primates: Parasites, injuries and predators. Proceedings of the Royal Society of London B: Biological Sciences, 269, 1031–1037.

    Article  Google Scholar 

  • Seraphin, S. B. (2000). The reproductive ecology and stress physiology of free-ranging male chimpanzees in Budongo Forest, Uganda. Master’s thesis, Oxford University.

  • Setchell, J. M., Bedjabaga, I. B., Goossens, B., Reed, P., Wicking, E. J., & Knapp, L. A. (2007). Parasite prevalence, abundance, and diversity in a semi-free-ranging colony of Mandrillus sphinx. International Journal of Primatology, 28, 1345–1362.

    Article  Google Scholar 

  • Setchell, J. M., Charpentier, M., Abbott, K. A., Wickings, E. J., & Knapp, L. A. (2009). Is brightest best? Testing the Hamilton–Zuk hypothesis in mandrills. International Journal of Primatology, 30, 825–844.

    Article  Google Scholar 

  • Setchell, J. M., Smith, T., Wickings, E. J., & Knapp, L. A. (2010). Stress, social behaviour, and secondary sexual traits in a male primate. Hormones and Behavior, 58, 720–728.

    Article  CAS  PubMed  Google Scholar 

  • Sheldon, B. C., & Verhulst, S. (1996). Ecological immunology: Costly parasite defenses and trade-offs in evolutionary ecology. Trends in Ecology and Evolution, 11, 317–321.

    Article  CAS  PubMed  Google Scholar 

  • Sloss, M. W., Kemp, R. L., & Zajac, A. M. (1994). Veterinary clinical parasitology (6th ed.). Ames: Iowa State University Press.

    Google Scholar 

  • Snaith, T. V., Chapman, C. A., Rothman, J. M., & Wasserman, M. D. (2008). Bigger groups have fewer parasites and similar cortisol levels: A multi-group analysis in red colobus monkeys. American Journal of Primatology, 70, 1072–1080.

    Article  PubMed  Google Scholar 

  • Stear, M. J., Bairden, K., Bishop, S. C., Duncan, J. L., Karimi, S. K., McKellar, Q., & Murray, M. (1995). Different patterns of faecal egg output following infection of Scottish blackface lambs with Ostertagia circumcincta. Veterinary Parasitology, 59, 29–38.

    Article  CAS  PubMed  Google Scholar 

  • Strier, K, B., & Ziegler, T, E. (1995). Advances in field-based studies of primate behavioural endocrinology. American Journal of Primatology 67, 1–4.

  • Strier, K. B., & Ziegler, T. E. (1997). Behavioral and endocrine characteristics of the reproductive cycle in wild muriqui monkeys, Brachyteles arachnoides. American Journal of Primatology, 67, 1–4.

    Article  Google Scholar 

  • Struhsaker, T. T. (1975). The red colobus monkey. Chicago: University of Chicago Press.

    Google Scholar 

  • Stuart, M. D., Greenspan, L. L., Glander, K. E., & Clarke, M. R. (1990). Coprological survey of parasites of wild mantled howling monkeys, Alouatta palliata palliata. Journal of Wildlife Diseases, 26, 547–549.

    Article  CAS  PubMed  Google Scholar 

  • Stuart, M. D., & Strier, K. B. (1995). Primates and parasites: A case for a multidisciplinary approach. International Journal of Primatology, 16, 577–593.

    Article  Google Scholar 

  • Stuart, M. D., Strier, K. B., & Pierberg, S. M. (1993). A coprological survey of parasites of wild muriquis Brachyteles arachnoides and brown howling monkeys Alouatta fusca. Journal of the Helminthological Society of Washington, 60, 111–115.

    Google Scholar 

  • Thompson, M. E., Zhou, A., & Knott, C. D. (2012). Low testosterone correlates with delayed development in male orang-utans. PLoS ONE, 7, e47282.

    Article  CAS  Google Scholar 

  • Tung, J., Barreiro, L. B., Burns, M. B., Grenier, J.-C., Lynch, J., Grieneisen, L. E., Altmann, J., Alberts, S. C., Blekhman, R., & Archie, E. A. (2015). Social networks predict gut microbiome composition in wild baboons. eLife. doi:10.7554/eLife.05224.

    Google Scholar 

  • Valtonen, A., Molleman, F., Chapman, C. A., Carey, J. R., Ayres, M. P., & Roininen, H. (2013). Tropical phenology: Bi-annual rhythms and interannual variation in an Afrotropical butterfly assemblage. Ecosphere, 4, 1–28.

    Article  Google Scholar 

  • VanderWaal, K. L., Atwill, E. R., Isbell, L. A., & McCowan, B. (2014a). Linking social and pathogen transmission networks using microbial genetics in giraffe (Giraffa camelopardalis). Journal of Animal Ecology, 83, 406–414.

    Article  PubMed  Google Scholar 

  • VanderWaal, K. L., Wang, H., McCowan, B., Fushing, H., & Isbell, L. A. (2014b). Multi-level social organization and space use in reticulated giraffe (Giraffa camelopardalis). Behavioral Ecology, 25, 17–26.

    Article  Google Scholar 

  • Vitone, N. D., Altizer, S. M., & Nunn, C. L. (2004). Body size, diet and sociality influence the species richness of parasitic worms in anthropoid primates. Evolutionary Ecology Research, 6, 1–17.

    Google Scholar 

  • Waser, P. M. (1977a). Individual recognition, intragroup cohesion and intergroup spacing: Evidence from sound playback to forest monkeys. Behaviour, 60, 27–74.

    Article  Google Scholar 

  • Waser, P. M. (1977b). Feeding, ranging and group size in the mangabey, Cercocebus albigena. In T. H. Clutton-Brock (Ed.), Primate ecology (pp. 183–222). London: Academic Press.

    Google Scholar 

  • Weatherhead, P. J., Metz, K. J., Bennett, G. F., & Irwin, R. E. (1993). Parasite faunas, testosterone and secondary sexual traits in male red-winged blackbirds. Behavioral Ecology and Sociobiology, 33, 13–23.

    Article  Google Scholar 

  • Whitten, P. L. (1983). Diet and dominance among female vervet monkeys (Cercopithecus aethiops). American Journal of Primatology, 5, 139–159.

    Article  Google Scholar 

  • Whitten, P. L., Brockman, D. K., & Stavisky, R. C. (1998). Recent advances in noninvasive techniques to monitor hormone-behavior interactions. Yearbook of Physical Anthropology, 41, 1–23.

    Article  Google Scholar 

  • Wingfield, J. C., & Sapolsky, R. M. (2003). Reproduction and resistance to stress: When and how. Journal of Neuroendocrinology, 15, 711–724.

    Article  CAS  PubMed  Google Scholar 

  • Ziegler, T. E., Scheffler, G., & Snowdon, C. T. (1995). The relationship of cortisol levels to social environment and reproductive functioning in female cotton-top tamarins Saguinus oedipus. Hormones and Behavior, 29, 407–424.

    Article  CAS  PubMed  Google Scholar 

  • Zuk, M. (1996). Disease, endocrine–immune interactions, and sexual selection. Ecology, 7, 1037–1042.

    Article  Google Scholar 

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Acknowledgments

We thank the Uganda Wildlife Authority, Uganda National Council for Science and Technology, and personnel at the Makerere University Biological Field Station for permission to work in Kibale National Park. We thank field assistants Akora Charles, Katusebe Swaibu, Kaseregenyu Richard, Koojo John, and Sabiti Richard for their invaluable assistance in the field. We thank Chesley Walsh and Johanna Bleecker for parasite analyses and Ants Kaasik and Veronique Biquand for advice on the statistical analyses. Finally, we appreciate the comments and suggestions by the editor and two anonymous reviewers that greatly improved the manuscript.

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Authors and Affiliations

  1. Animal and Human Ethology Research Unit, University of Rennes 1, 35042, Rennes, France

    Małgorzata E. Arlet

  2. Department of Anthropology and McGill School of Environment, McGill University, Montréal, Quebec, H3A 2T7, Canada

    Colin A. Chapman

  3. Wildlife Conservation, Bronx, New York, 10460, USA

    Colin A. Chapman

  4. Department of Anthropology and Animal Behavior Graduate Group, University of California, Davis, Davis, California, 95616, USA

    Lynne A. Isbell

  5. Ecosystems, Biodiversity and Evolution Research Unit, University of Rennes 1, 35042, Rennes, France

    Freerk Molleman

  6. Department of Zoology, Institute of Ecology and Earth Sciences, University of Tartu, Tartu, 50090, Estonia

    Freerk Molleman, Raivo Mänd & Peeter Hõrak

  7. Department of Entomology, University of California, Davis, Davis, California, 95616, USA

    James R. Carey

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  1. Małgorzata E. Arlet
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  2. Colin A. Chapman
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  3. Lynne A. Isbell
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Correspondence to Małgorzata E. Arlet.

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Arlet, M.E., Chapman, C.A., Isbell, L.A. et al. Social and Ecological Correlates of Parasitic Infections in Adult Male Gray-Cheeked Mangabeys (Lophocebus albigena). Int J Primatol 36, 967–986 (2015). https://doi.org/10.1007/s10764-015-9866-9

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  • DOI: https://doi.org/10.1007/s10764-015-9866-9

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