Environmental and individual determinants of parasite richness across seasons in a free-ranging population of Mandrills (Mandrillus sphinx)

American Journal of Physical Anthropology

Volumn 159, Issue 3, 2016, Pages 442-456

  Poirotte, Clémence ^a   Basset, Didier ^b   Willaume, Eric ^c   Makaba, Fred ^c   Kappeler, Peter M ^d   Charpentier, Marie J E ^a  

^a CENTRE D ECOLOGIE FONCTIONNELLE ET EVOLUTIVE   (France)

^b MONTPELLIER UNIVERSITY HOSPITAL   (France)

^c SODEPAL   (Gabon)

^d GERMAN PRIMATE CENTER   (Germany)

Author keywords

nematode; parasite richness; primate; protozoa

Indexed keywords

RAIN;

ADULT; AGE; ARTICLE; ENVIRONMENTAL TEMPERATURE; ESTRUS CYCLE; FEMALE; HUMIDITY; MALE; MANDRILLUS; MANDRILLUS SPHINX; NEMATODE; NONHUMAN; PARASITE DEVELOPMENT; PARASITISM; PROTOZOON; SEASONAL VARIATION; SEX DIFFERENCE; SOCIAL DOMINANCE; SPECIES RICHNESS; WILD ANIMAL; ANIMAL; ANIMAL PARASITOSIS; CLIMATE; ENTAMOEBA; FECES; GABON; PARASITOLOGY; PHYSICAL ANTHROPOLOGY;

ANIMALS; ANTHROPOLOGY, PHYSICAL; CLIMATE; ENTAMOEBA; FECES; FEMALE; GABON; MALE; MANDRILLUS; NEMATODA; PARASITIC DISEASES, ANIMAL;

EID: 84958941357     PISSN: 00029483     EISSN: 10968644     Source Type: Journal    
DOI: 10.1002/ajpa.22888     Document Type: Article

References (82)

1. Abernethy KA, White LJT, Wickings EJ., 2002. Hordes of mandrills Mandrillus sphinx: Extreme group size and seasonal male presence. J Zool 258: 131-137.
2. Altizer S, Dobson AP, Hosseini P, Hudson PJ, Pascual M, Rohani P., 2006. Seasonality and the dynamics of infectious diseases. Ecol Lett 9: 467-484.
3. Benavides JA, Huchard E, Pettorelli N, King AJ, Brown ME, Archer CE, Appleton CC, Raymond M, Cowlishaw G., 2012. From parasite encounter to infection: multiple-scale drivers of parasite richness in a wild social primate population. Am J Phys Anthropol 147: 52-63.
4. Bordes F, Morand S., 2009. Parasite diversity: An overlooked metric of parasite pressures? Oikos 118: 801-806.
5. Brockmeyer T, Kappeler PM, Willaume E, Benoit L, Mboumba S, Charpentier M., 2015. Social organization and space use of a wild mandrill (Mandrillus sphinx) group. Am J Primatol 77: 1036-1048.
6. Calvignac-Specer S, Leendertz SAJ, Gillespie TR, Leendertz FH., 2012. Wild great apes as sentinels and sources of infectious disease. Clin Microbiol Infect 18: 521-527.
7. Cattadori IM, Boag B, Bjørnstad ON, Cornell SJ, Hudson PJ., 2005. Peak shift and epidemiology in a seasonal host-nematode system. Proc Biol Sci 272: 1163-1169.
8. Chapman CA, Gillespie TR, Goldberg TL., 2005. Primates and the ecology of their infectious diseases: How will anthropogenic change affect host-parasite interactions? Evol Anthropol 14: 134-144.
9. Chapman CA, Saj TL, Snaith TV., 2007. Temporal dynamics of nutrition, parasitism, and stress in colobus monkeys: Implications for population regulation and conservation. Am J Phys Anthropol 134: 240-250.
10. Cleaveland S, Appel MGJ, Chalmers WSK, Chillingworth C, Kaare M, Dye C., 2000. Serological and demographic evidence for domestic dogs as a source of canine distemper virus infection for Serengeti wildlife. Vet Microbiol 72: 217-227.
11. Clemens LE, Siiteri PK, Stites DP., 1979. Mechanism of immunosuppression of progesterone on maternal lymphocyte activation during pregnancy. J Immunol 122: 1978-1985.
12. Clough D, Heistermann M, Kappeler PM., 2010. Host intrinsic determinants and potential consequences of parasite infection in free-ranging red-fronted lemurs (Eulemur fulvus rufus). Am J Phys Anthropol 142: 441-452.
13. Coop RL, Holmes PH., 1996. Nutrition and parasite interaction. Int J Parasitol 26: 951-962.
14. Cornell SJ, Bjornstad ON, Cattadori IM, Boag B, Hudson PJ., 2008. Seasonality, cohort-dependence and the development of immunity in a natural host-nematode system. Proc R Soc B Biol Sci 275: 511-518.
15. Cross PC, Drewe J, Patrek V, Pearce G, Samuel MD, Delahay RJ., 2009. Wildlife population structure and parasite transmission: Implications for disease management. In:, Delahay RJ, Smith GC, Hutchings MR, editors. Management of disease in wild mammals, Vol. 62. New-York: Springer. p 9-29.
16. Deluol A, Hellegouarc'h A, Lebras P, Ricq G., 1998. Colour atlas of parasitology, Vol. 1, Amoebae. St Maur: Varia.
17. Deluol A, Lebras P, Ricq G., 1999. Colour atlas of parasitology, Vol. 2, Flagellates-Ciliates-Coccidia-Microsporidia-Blastocystis hominis-Trichomonas vaginalis. St Maur: Varia.
18. Dixson AF., 1983. Observations on the evolution and behavioral significance of "sexual skin" in female primates. Adv Study Behav 13: 63-106.
19. Dobson A, Lafferty KD, Kuris AM, Hechinger RF, Jetz W., 2008. Colloquium paper: Homage to Linnaeus: How many parasites? How many hosts? Proc Natl Acad Sci USA 105: 11482-11489.
20. Dobson AP, Hudson PJ., 1992. Regulation and stability of a free living host-parasite system: Trichostrongylus tenuis in redgrouse. II. Population models. J Anim Ecol 61: 487-1989.
21. Dobson AP, Hudson PJ., 1995. The interaction between the parasites and predators of red grouse Lagopus lagopus scoticus. Ibis 137: 87-96.
22. Dunsmore JD., 1971. Influence of host hormones on nematode parsitism in rabbits, Oryctotagus cuniculus. Aust J Zool 19: 121-128.
23. Elliott GP, Wilson PR, Taylor RH, Beggs JR., 2010. Declines in common, widespread native birds in a mature temperate forest. Biol Conserv 143: 2119-2126.
24. Falzon LC, Menzies PI, Shakya KP, Jones-Bitton A, Vanleeuwen J, Avula J, Jansen JT, Peregrine AS., 2013. A longitudinal study on the effect of lambing season on the periparturient egg rise in Ontario sheep flocks. Prev Vet Med 110: 467-480.
25. Freeland WJ., 1980. Mangabey (Cerocebus albigena) movement patterns in relation to food availability and fecal contamination. Ecology 61: 1297-1303.
26. Galbany J, Romero A, Mayo-Alesõn M, Itsoma F, Gamarra B, Pérez-Pérez A, Willaume E, Kappeler PM, Charpentier MJE., 2014. Age-related tooth wear differs between forest and savanna primates. PLoS One 9: e94938.
27. Gillespie TR, Chapman CA., 2008. Forest fragmentation, the decline of an endangered primate, and changes in host-parasite interactions relative to an unfragmented forest. Am J Primatol 70: 222-230.
28. Gillespie TR, Lonsdorf EV, Canfield EP, Meyer DJ, Nadler Y, Raphael J, Pusey AE, Pond J, Pauley J, Mlengeya T, Travis DA., 2010. Demographic and ecological effects on patterns of parasitism in eastern chimpanzees (Pan troglodytes schweinfurthii) in Gombe National Park, Tanzania. Am J Phys Anthropol 143: 534-544.
29. Guernier V, Hochberg ME, Guégan JF., 2004. Ecology drives the worldwide distribution of human diseases. PLoS Biol 2: 740-746.
30. Hausfater G, Meade BJ., 1982. Alternation of sleeping groves by yellow baboons (Papio cynocephalus) as a strategy for parasite avoidance. Primates 23: 287-297.
31. Hausfater G, Watson DF., 1976. Social and reproductive correlates of parasite ova emissions by baboons. Nature 260: 619-621.
32. Hudson PJ, Dobson AP, Newborn D., 1992. Do parasites make prey vulnerable to predation? Red grouse and parasites. J Anim Ecol 61: 681-692.
33. Hudson PJ, Dobson AP., 1995. Macroparasites: Observed patterns in naturally fluctuating animal populations. In:, Grenfell BT, Dobson AP, editors. Ecology of infectious diseases in natural populations. Cambridge: Cambridge University Press. p 144-176.
34. Kappeler PM, Cremer S, Nunn CL., 2015. Sociality and health: Impacts of sociality on disease susceptibility and transmission in animal and human societies. Phylos Trans R Soc B 370: 20140116.
35. Kappeler PM, Van Schaik CP., 2001. Evolution of primate social systems. Int J Primatol 23: 707-740.
36. Kirchner JW, Roy BA., 1999. The Evolutionary advantages of dying young: Epidemiological implications of longevity in metapopulations. Am Nat 154: 140-159.
37. Klein SL., 2000. The effects of hormones on sex differences in infection: From genes to behavior. Neurosci Biobehav Rev 24: 627-638.
38. Klein SL., 2004. Hormonal and immunological mechanisms mediating sex differences in parasite infection. Parasite Immunol 26: 247-264.
39. Knezevich M., 1998. Geophagy as a therapeutic mediator of endoparasitism in a free-ranging group of rhesus macaques (Macaca mulatta). Am J Primatol 44: 71-82.
40. Kucik CJ, Martin GL, Sortor BV., 2004. Common intestinal parasites. Am Fam Phys 69: 1161-1168.
41. Lello J, Boag B, Hudson PJ., 2005. The effect of single and concomitant pathogen infections on condition and fecundity of the wild rabbit (Oryctolagus cuniculus). Int J Parasitol 35: 1509-1515.
42. MacIntosh AJJ, Hernandez AD, Huffman MA., 2010. Host age, sex, and reproductive seasonality affect nematode parasitism in wild Japanese macaques. Primates 51: 353-364.
43. MacIntosh AJJ, Jacobs A, Garcia C, Shimizu K, Mouri K, Huffman MA, Hernandez AD., 2012. Monkeys in the middle: Parasite transmission through the social network of a wild primate. PLoS One 7: e51144.
44. Mccallum H, Dobson A., 1995. Detecting disease and parasite threats to endangered species and ecosystems. Trends Ecol Evol 10: 190-194.
45. McGrew WC, Tutin CEG, Collins DA, File SK., 1989. Intestinal parasites of sympatric Pan troglodytes and Papio spp. at two sites: Gombe (Tanzania) and Mt. Assirik (Senegal). Am J Primatol 17: 147-155.
46. Miller TA., 1968. Pathogenesis and immunity in hookworm infection. Trans R Soc Trop Med Hyg 62: 473-489.
47. Milton K., 1996. Effects of bot fly (Alouattamyia baeri) parasitism on a free-ranging howler monkey (Alouatta palliata) population in Panama. J Zool 239: 39-63.
48. Minchella DJ., 1985. Host life-history variation in response to parasitism. Parasitology 90: 205-216.
49. Mor G, Cardenas I., 2010. The immune system in pregnancy: A unique complexity. Am J Reprod Immunol 63: 425-433.
50. Morand S, Harvey PH., 2000. Mammalian metabolism, longevity and parasite species richness. Proc Biol Sci 267: 1999-2003.
51. Muehlenbein MP, Watts DP., 2010. The costs of dominance: Testosterone, cortisol and intestinal parasites in wild male chimpanzees. Biopsychosoc Med 4: 1-21.
52. Muehlenbein MP., 2005. Parasitological analyses of the male chimpanzees (Pan troglodytes schweinfurthii) at Ngogo, Kibale National Park, Uganda. Am J Primatol 65: 167-179.
53. Muehlenbein MP., 2006. Intestinal parasite infections and fecal steroid levels in wild chimpanzees. Am J Phys Anthropol 130: 546-550.
54. Müller-Graf CD, Collins DA, Woolhouse ME., 1996. Intestinal parasite burden in five troops of olive baboons (Papio cynocephalus anubis) in Gombe Stream National Park, Tanzania. Parasitology 112: 489-497.
55. Neveu-Lemaire. 1952. Précis de Parasitologie Vétérinaire. Paris: Vigot.
56. Nunn CL, Alitzer S., 2006. Infectious diseases in primates: Behavior, ecology and evolution. Oxford: Oxford University Press.
57. Nunn CL, Altizer S, Jones KE, Sechrest W., 2003. Comparative tests of parasite species richness in primates. Am Nat 162: 597-614.
58. Nunn CL, Altizer S, Sechrest W, Jones KE, Barton RA, Gittleman JL., 2004. Parasites and the evolutionary diversification of primate clades. Am Nat 164: S90-S103.
59. Nunn CL, Craft ME, Gillespie TR, Schaller M, Kappeler PM, Nunn CL., 2015. The sociality-health-fitness nexus: Synthesis, conclusions and future directions. Philos Trans R Soc B 370: 20140115.
60. Nunn CL, Dokey ATW., 2006. Ranging patterns and parasitism in primates. Biol Lett 2: 351-354.
61. O'Donnell S., 1997. How parasites can promote the expression of social behaviour in their hosts. Proc R Soc B Biol Sci 264: 689-694.
62. Parr NA, Fedigan LM, Kutz SJ., 2013. Predictors of parasitism in wild white-faced capuchins (Cebus capucinus). Int J Primatol 34: 1137-1152.
63. Pedersen AB, Davies TJ., 2010. Cross-species pathogen transmission and disease emergence in primates. Ecohealth 6: 496-508.
64. Peignot P, Charpentier MJE, Bout N, Bourry O, Massima U, Dosimont O, Terramorsi R, Wickings EJ., 2008. Learning from the first release project of captive-bred mandrills Mandrillus sphinx in Gabon. Oryx 42: 122-131.
65. Prociv P, Croese J., 1996. Human enteric infection with Ancylostoma caninum: Hookworms reappraised in the light of a 'new' zoonosis. Acta Trop 62: 23-44.
66. Rolland S, Fabricius H-A, Wolfgang H., 1978. Suppression of human T-cell colony formation during pregnancy. Nature 276: 831-832.
67. Sapolsky RM., 2005. The influence of social hierarchy on primate health. Science 308: 648-652.
68. Setchell JM, Bedjabaga IB, Goossens B, Reed P, Wickings EJ, Knapp LA., 2007. Parasite prevalence, abundance, and diversity in a semi-free-ranging colony of Mandrillus sphinx. Int J Primatol 28: 1345-1362.
69. Setchell JM, Lee PC, Wickings EJ, Dixson AF., 2002. Reproductive parameters and maternal investment in mandrills (Mandrillus sphinx). Int J Primatol 23: 51-68.
70. Setchell JM, Smith T, Wickings EJ, Knapp LA., 2008. Social correlates of testosterone and ornamentation in male mandrills. Horm Behav 54: 365-372.
71. Setchell JM, Wickings EJ., 2005. Dominance, status signals and coloration in male mandrills. Ethology 111: 25-50.
72. Simková A, Lafond T, Ondracková M, Jurajda P, Ottová E, Morand S., 2008. Parasitism, life history traits and immune defence in cyprinid fish from Central Europe. BMC Evol Biol 8: 29.
73. Stuart MD, Strier KB, Pierberg SM., 1993. A coprological survey of parasites of wild muriquies, Brachyteles arachnoides, and brown howling monkeys, Alouatta fusca. J Helminthol Soc Washingt 60: 111-115.
74. Szekeres-Bartho J., 1997. Progesterone-induced immunosuppression. Hum Reprod 12: 629-631.
75. Thompson RCA, Lymbery AJ, Smith A., 2010. Parasites, emerging disease and wildlife conservation. Int J Parasitol 40: 1163-1170.
76. Thorne ET, Williams ES., 2012. Disease and endangered species: The black-footed as a ferret recent example. Conserv Biol 2: 66-74.
77. Tompkins DM, Dunn AM, Smith MJ, Telfer S., 2011. Wildlife diseases: From individuals to ecosystems. J Anim Ecol 80: 19-38.
78. Valdespino C, Rico-Hernández G, Mandujano S., 2010. Gastrointestinal parasites of howler monkeys (Alouatta palliata) inhabiting the fragmented landscape of the Santa Marta mountain range, Veracruz, Mexico. Am J Primatol 72: 539-548.
79. Verthelyi D., 2001. Sex hormones as immunomodulators in health and disease. Int Immunopharmacol 1: 983-993.
80. Vitone ND, Altizer S, Nunn CL., 2004. Body size, diet and sociality influence the species richness of parasitic worms in anthropoid primates. Evol Ecol Res 6: 183-199.
81. Weinberg ED., 1987. Pregnancy-associated immune suppression: Risks and mechanisms. Microb Pathog 3: 393-397.
82. Zuk M, Mckean KA., 1996. Sex differences in parasite infections: Patterns and processes. Int J Parasitol 26: 1009-1024.