, Volume 51, Issue 4, pp 353–364 | Cite as

Host age, sex, and reproductive seasonality affect nematode parasitism in wild Japanese macaques

  • Andrew J. J. MacIntosh
  • Alexander D. Hernandez
  • Michael A. Huffman
Original Article


Parasites are characteristically aggregated within hosts, but identifying the mechanisms underlying such aggregation can be difficult in wildlife populations. We examined the influence of host age and sex over an annual cycle on the eggs per gram of feces (EPG) of nematode parasites infecting wild Japanese macaques (Macaca fuscata yakui) on Yakushima Island. Five species of nematode were recorded from 434 fecal samples collected from an age-structured group of 50 individually recognizable macaques. All parasites exhibited aggregated EPG distributions. The age–infection profiles of all three directly transmitted species (Oesophagostomum aculeatum, Strongyloides fuelleborni, and Trichuris trichiura) exhibited convex curves, but concavity better characterized the age–infection curves of the two trophically transmitted species (Streptopharagus pigmentatus and Gongylonema pulchrum). There was a male bias in EPG and prevalence of infection with directly transmitted species, except in the prevalence of O. aculeatum, and no sex bias in the other parasites. Infection with O. aculeatum showed a female bias in prevalence among young adults, and additional interactions with sex and seasonality show higher EPG values in males during the mating season (fall) but in females during the birth season (spring). These patterns suggest that an immunosuppressive role by reproductive hormones may be regulating direct, but not indirect, life-cycle parasites. Exposure at an early age may trigger an immune response that affects all nematodes, but trophically transmitted species appear to accumulate thereafter. Although it is difficult to discern clear mechanistic explanations for parasite distributions in wildlife populations, it is critical to begin examining these patterns in host species that are increasingly endangered by anthropogenic threats.


Primate parasite ecology Macaca fuscata Parasite aggregation Host-sex bias Seasonal infection Coinfection Age–infection profile 



We thank the Kagoshima Prefectural Government and Yakushima World Heritage Office for permission to conduct research on Yakushima Island. We are grateful to Dr. Hideo Hasegawa for his support and guidance during this project. We are indebted to the Wildlife Research Center of Kyoto University for use of the Nagata Field station during field research, and to Dr. Goro Hanya and Dr. Hideki Sugiura for help with permits and logistics. We also thank Mr. Ryosuke Koda, Ms. Mariko Suzuki, and Ms. Mariko Nishikawa for help and support in the field, and Dr. Laurent Tarnaud for sharing information about the study group. This manuscript also benefited from the readings of Dr. David Hill and three anonymous reviewers. Finally, the Japan Ministry of Education, Culture, Sports, Science and Technology (MEXT) provided financial support to AJJM through a Monbukagakusho scholarship and to ADH through a Japan Society for the Promotion of Science (JSPS) postdoctoral fellowship. JSPS also awarded grant-in-aid funds to ADH and MAH, which helped finance this study.


  1. Acha PN, Szyfres B (2003) Zoonoses and communicable diseases common to man and animals: parasitoses. Pan American Health Organization, Washington, DCGoogle Scholar
  2. Altizer S, Dobson A, Hosseini P, Hudson P, Pascual M, Rohani P (2006) Seasonality and the dynamics of infectious diseases. Ecol Lett 9:467–484CrossRefPubMedGoogle Scholar
  3. Anderson RC (2000) Nematode parasites of vertebrates: their development and transmission, 2nd edn. CABI Publishing, WallingtonCrossRefGoogle Scholar
  4. Anderson RM, Gordon DM (1982) Processes influencing the distribution of parasite numbers within host populations with special emphasis on parasite-induced host mortalities. Parasitology 85:373–398CrossRefPubMedGoogle Scholar
  5. Anderson RM, May RM (1985) Herd immunity to helminth infection and implications for parasite control. Nature 315:493–496CrossRefPubMedGoogle Scholar
  6. Barrett GM, Shimizu K, Bardi M, Asaba S, Mori A (2002) Endocrine correlates of rank, reproduction, and female-directed aggression in male Japanese macaques (Macaca fuscata). Horm Behav 42:85–96CrossRefPubMedGoogle Scholar
  7. Behnke JM (1987) Evasion of immunity by nematode parasites causing chronic infections. Adv Parasitol 26:1–71CrossRefPubMedGoogle Scholar
  8. Boots M, Bowers RG (2004) The evolution of resistance through costly acquired immunity. Proc R Soc Lond B Biol Sci 271(1540):715–723CrossRefGoogle Scholar
  9. Bundy DAP (1988) Gender-dependent patterns of infection and disease. Parasitol Today 4:186–189CrossRefPubMedGoogle Scholar
  10. Bundy DAP, Cooper ES, Thompson DE, Anderson RM, Didier ES (1987) Age-related prevalence and intensity of Trichuris trichiura infection in a St Lucian community. Trans R Soc Trop Med Hyg 81:85–94CrossRefPubMedGoogle Scholar
  11. Cattadori IM, Boag B, Bjornstad ON, Cornell SJ, Hudson PJ (2005) Peak shift and epidemiology in a seasonal host-nematode system. Proc R Soc Lond B Biol Sci 272:1163–1169CrossRefGoogle Scholar
  12. 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 14:134–144CrossRefGoogle Scholar
  13. Crawley MJ (2007) The R book. Wiley, West SussexCrossRefGoogle Scholar
  14. Crofton HD (1971) A quantitative approach to parasitism. Parasitology 62:179–193CrossRefGoogle Scholar
  15. Dewit I, Dittus WPJ, Vercruysse J, Harris EA, Gibson DI (1991) Gastrointestinal helminths in a natural population of Macaca sinica and Presbytis spp. at Polonnaruwa, Sri Lanka. Primates 32:391–395CrossRefGoogle Scholar
  16. Dobson A, Lafferty KD, Kuris AM, Hechinger RF, Jetz W (2008) Homage to Linnaeus: how many parasites? How many hosts? Proc Natl Acad Sci USA 105:11482–11489CrossRefPubMedGoogle Scholar
  17. East IJ, Bourne AS (1988) A comparison of worm burden and fecal egg count for measuring the efficacy of vaccination against Oesophagostomum radiatum. Int J Parasitol 18:863–864CrossRefPubMedGoogle Scholar
  18. Fooden J, Aimi M (2005) Systematic review of Japanese macaques, Macaca fuscata (Gray, 1870). Fieldiana Zool 104:1–200Google Scholar
  19. Gillespie TR (2006) Non-invasive assessment of gastrointestinal parasite infections in free-ranging primates. Int J Primatol 27:1129–1143CrossRefGoogle Scholar
  20. Gillespie TR, Greiner EC, Chapman CA (2005) Gastrointestinal parasites of the colobus monkeys of Uganda. J Parasitol 91:569–573CrossRefPubMedGoogle Scholar
  21. Gillespie TR, Nunn CL, Leendertz FH (2008) Integrative approaches to the study of primate infectious disease: implications for biodiversity conservation and global health. Am J Phys Anthropol 51:53–69CrossRefGoogle Scholar
  22. Gotoh S (2000) Regional differences in the infection of wild Japanese macaques by gastrointestinal helminth parasites. Primates 41:291–298CrossRefGoogle Scholar
  23. Grencis RK (1993) Cytokine-mediated regulation of intestinal helminth infections: the Trichuris muris model. Ann Trop Med Parasitol 87:643–647PubMedGoogle Scholar
  24. Grossman C (1989) Possible underlying mechanisms of sexual dimorphism in the immune response, fact and hypothesis. J Steroid Biochem 34:241–251CrossRefPubMedGoogle Scholar
  25. Hamada Y, Suzuki J, Ohkura S, Hayakawa S (2005) Changes in testicular and nipple volume related to age and seasonality in Japanese macaques (Macaca fuscata), especially in the pre- and post-pubertal periods. Primates 46:33–45CrossRefPubMedGoogle Scholar
  26. Hanya G (2003) Age differences in food intake and dietary selection of wild male Japanese macaques. Primates 44:333–339CrossRefPubMedGoogle Scholar
  27. Herbert DR, Lee JJ, Lee NA, Nolan TJ, Schad GA, Abraham D (2000) Role of IL-5 in innate and adaptive immunity to larval Strongyloides stercoralis in mice. J Immunol 165:4544–4551PubMedGoogle Scholar
  28. Hernandez AD, MacIntosh AJ, Huffman MA (2009) Primate parasite ecology: patterns and predictions from an on-going study of Japanese macaques. In: Huffman MA, Chapman CA (eds) Primate parasite ecology: the dynamics and study of host-parasite relationships. Cambridge University Press, Cambridge, pp 387–402Google Scholar
  29. Hill DA (1997) Seasonal variation in the feeding behavior and diet of Japanese macaques (Macaca fuscata yakui) in lowland forest of Yakushima. Am J Primatol 43:305–322CrossRefPubMedGoogle Scholar
  30. Horii Y, Imada I, Yanagida T, Usui M, Mori A (1982) Parasite changes and their influence on the body weight of Japanese monkeys (Macaca fuscata fuscata) of the Koshima troop. Primates 23:416–431CrossRefGoogle Scholar
  31. Hudson P, Dobson AP (1995) Macroparasites: observed patterns. In: Grenfell BT, Dobson AP (eds) Ecology of infectious diseases in natural populations. Cambridge University Press, Cambridge, pp 144–176CrossRefGoogle Scholar
  32. Huffman MA (1987) Consort intrusion and female mate choice in Japanese macaques (Macaca fuscata). Ethology 75:221–234CrossRefGoogle Scholar
  33. Janson CH, Verdolin J (2005) Seasonality of primate births in relation to climate. In: Brockman DK, van Schaik CP (eds) Seasonality in primates: studies of living and extinct human and non-human primates. Cambridge University Press, Cambridge, pp 307–350CrossRefGoogle Scholar
  34. Klein SL (2000) Hormones and mating system affect sex and species differences in immune function among vertebrates. Behav Process 51:149–166CrossRefGoogle Scholar
  35. Kudo A, Oyamada T, Okutsu M, Kinoshita H (1996) Intermediate hosts of Gongylonema pulchrum Molin, 1857, in Aomori prefecture, Japan. Jpn J Parasitol 45:222–229Google Scholar
  36. Machida M, Araki J, Koyama T, Kumada M, Horii Y, Imada I, Takasaka M, Honjo S, Matsubayashi K, Tiba T (1978) The life cycle of Streptopharagus pigmentatus (Nematoda, Spiruroidea) from the Japanese monkey. Bull Natl Sci Mus Ser A Zool 4:1–9Google Scholar
  37. Maruhashi T (1980) Feeding behavior and diet of the Japanese monkey (Macaca fuscata yakui) on Yakushima island, Japan. Primates 21:141–160CrossRefGoogle Scholar
  38. Muller-Graf CDM, Collins DA, Woolhouse MEJ (1996) Intestinal parasite burden in five troops of olive baboons (Papio cynocephalus anubis) in Gombe Stream National Park, Tanzania. Parasitology 112:489–497CrossRefPubMedGoogle Scholar
  39. Muroyama Y, Shimizu K, Sugiura H (2007) Seasonal variation in fecal testosterone levels in free-ranging male Japanese macaques. Am J Primatol 69:603–610CrossRefPubMedGoogle Scholar
  40. Nunn C, Altizer S (2006) Infectious diseases in primates. Oxford University Press, OxfordCrossRefGoogle Scholar
  41. Pacala SW, Dobson AP (1988) The relation between the number of parasites/host and host age: population dynamic causes and maximum likelihood estimation. Parasitology 96:197–210CrossRefPubMedGoogle Scholar
  42. Pit DSS, Rijcken FEM, Raspoort EC, Baeta SM, Polderman AM (1999) Geographic distribution and epidemiology of Oesophagostomum bifurcum and hookworm infections in humans in Togo. Am J Trop Med Hyg 61:951–955PubMedGoogle Scholar
  43. Pit DSS, Polderman AM, Baeta S, Schulz-Key H, Soboslay PT (2001) Parasite-specific antibody and cellular immune responses in humans infected with Necator americanus and Oesophagostomum bifurcum. Parasitol Res 87:722–729CrossRefPubMedGoogle Scholar
  44. Poulin R (1996a) Helminth growth in vertebrate hosts: does host sex matter? Int J Parasitol 26:1311–1315CrossRefPubMedGoogle Scholar
  45. Poulin R (1996b) Sexual inequalities in helminth infections: a cost of being a male? Am Nat 147:287–295CrossRefGoogle Scholar
  46. Poulin R (2007) Are there general laws in parasite ecology? Parasitology 134:763–776CrossRefPubMedGoogle Scholar
  47. Roberts JL, Swan RA (1981) Quantitative studies of bovine haemonchosis. I. Relationship between fecal egg counts and total worm counts. Vet Parasitol 8:165–171CrossRefGoogle Scholar
  48. Rolff J (2002) Bateman’s principle and immunity. Proc R Soc Lond B Biol Sci 269:867–872CrossRefGoogle Scholar
  49. Seivwright LJ, Redpath SM, Mougeot F, Watt L, Hudson PJ (2004) Faecal egg counts provide a reliable measure of Trichostrongylus tenuis intensities in free-living red grouse Lagopus lagopus scoticus. J Helminthol 78(1):69–76CrossRefPubMedGoogle Scholar
  50. Sprague DS (1992) Life-history and male intertroop mobility among Japanese macaques (Macaca fuscata). Int J Primatol 13:437–454CrossRefGoogle Scholar
  51. Takahata Y, Suzuki S, Agetsuma N, Okayasu N, Sugiura H, Takahashi H, Yamagiwa J, Izawa K, Furuichi T, Hill DA, Maruhashi T, Saito C, Sato S, Sprague DS (1998) Reproduction of wild Japanese macaque females of Yakushima and Kinkazan islands; a preliminary report. Primates 39:339–349CrossRefGoogle Scholar
  52. Wakelin D (1996) Immunity to parasites: how parasitic infections are controlled. Cambridge University Press, CambridgeGoogle Scholar
  53. Watanabe K (2008) Macaca fuscata ssp. yakui. In: IUCN red list of threatened species, version 2009, 2.
  54. Weyher AH, Ross C, Semple S (2006) Gastrointestinal parasites in crop raiding and wild foraging Papio anubis in Nigeria. Int J Primatol 27:1519–1534CrossRefGoogle Scholar
  55. Wilson K, Bjornstad ON, Dobson AP, Merler S, Poglayen G, Randolph SE, Read AF, Skorping A (2002) Heterogeneities in macroparasite infections: patterns and processes. In: Hudson P, Rizzoli A, Grenfell BT, Heesterbeek H, Dobson AP (eds) The ecology of wildlife diseases. Oxford University Press, New York, pp 6–44Google Scholar
  56. Woolhouse MEJ (1998) Patterns in parasite epidemiology: the peak shift. Parasitol Today 14:428–434CrossRefPubMedGoogle Scholar
  57. Yamagiwa J, Hill DA (1998) Intraspecific variation in the social organization of Japanese macaques: past and present scope of field studies in natural habitats. Primates 39:257–273CrossRefGoogle Scholar
  58. Zuk M (1990) Reproductive strategies and disease susceptibility: an evolutionary viewpoint. Parasitol Today 6:231–233CrossRefPubMedGoogle Scholar
  59. Zuk M, McKean KA (1996) Sex differences in parasite infections: patterns and processes. Int J Parasitol 26:1009–1023CrossRefPubMedGoogle Scholar

Copyright information

© Japan Monkey Centre and Springer 2010

Authors and Affiliations

  • Andrew J. J. MacIntosh
    • 1
  • Alexander D. Hernandez
    • 2
  • Michael A. Huffman
    • 1
  1. 1.Section of Social Systems Evolution, Department of Ecology and Social BehaviorKyoto University Primate Research InstituteInuyamaJapan
  2. 2.508 Mueller Laboratories, Center for Infectious Disease DynamicsThe Pennsylvania State UniversityUniversity ParkUSA

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