Skip to main content

Advertisement

SpringerLink
Log in

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

  • Original Article
  • Published:
Primates Aims and scope Submit manuscript

Abstract

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Acha PN, Szyfres B (2003) Zoonoses and communicable diseases common to man and animals: parasitoses. Pan American Health Organization, Washington, DC

    Google Scholar 

  • Altizer S, Dobson A, Hosseini P, Hudson P, Pascual M, Rohani P (2006) Seasonality and the dynamics of infectious diseases. Ecol Lett 9:467–484

    Article  PubMed  Google Scholar 

  • Anderson RC (2000) Nematode parasites of vertebrates: their development and transmission, 2nd edn. CABI Publishing, Wallington

    Book  Google Scholar 

  • Anderson RM, Gordon DM (1982) Processes influencing the distribution of parasite numbers within host populations with special emphasis on parasite-induced host mortalities. Parasitology 85:373–398

    Article  PubMed  Google Scholar 

  • Anderson RM, May RM (1985) Herd immunity to helminth infection and implications for parasite control. Nature 315:493–496

    Article  CAS  PubMed  Google Scholar 

  • 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 42:85–96

    Article  CAS  PubMed  Google Scholar 

  • Behnke JM (1987) Evasion of immunity by nematode parasites causing chronic infections. Adv Parasitol 26:1–71

    Article  CAS  PubMed  Google Scholar 

  • Boots M, Bowers RG (2004) The evolution of resistance through costly acquired immunity. Proc R Soc Lond B Biol Sci 271(1540):715–723

    Article  Google Scholar 

  • Bundy DAP (1988) Gender-dependent patterns of infection and disease. Parasitol Today 4:186–189

    Article  CAS  PubMed  Google Scholar 

  • 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 81:85–94

    Article  CAS  PubMed  Google Scholar 

  • 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 272:1163–1169

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Crawley MJ (2007) The R book. Wiley, West Sussex

    Book  Google Scholar 

  • Crofton HD (1971) A quantitative approach to parasitism. Parasitology 62:179–193

    Article  Google Scholar 

  • 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 32:391–395

    Article  Google Scholar 

  • 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 105:11482–11489

    Article  CAS  PubMed  Google Scholar 

  • 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 18:863–864

    Article  CAS  PubMed  Google Scholar 

  • Fooden J, Aimi M (2005) Systematic review of Japanese macaques, Macaca fuscata (Gray, 1870). Fieldiana Zool 104:1–200

    Google Scholar 

  • Gillespie TR (2006) Non-invasive assessment of gastrointestinal parasite infections in free-ranging primates. Int J Primatol 27:1129–1143

    Article  Google Scholar 

  • Gillespie TR, Greiner EC, Chapman CA (2005) Gastrointestinal parasites of the colobus monkeys of Uganda. J Parasitol 91:569–573

    Article  PubMed  Google Scholar 

  • 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 51:53–69

    Article  Google Scholar 

  • Gotoh S (2000) Regional differences in the infection of wild Japanese macaques by gastrointestinal helminth parasites. Primates 41:291–298

    Article  Google Scholar 

  • Grencis RK (1993) Cytokine-mediated regulation of intestinal helminth infections: the Trichuris muris model. Ann Trop Med Parasitol 87:643–647

    CAS  PubMed  Google Scholar 

  • Grossman C (1989) Possible underlying mechanisms of sexual dimorphism in the immune response, fact and hypothesis. J Steroid Biochem 34:241–251

    Article  CAS  PubMed  Google Scholar 

  • 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 46:33–45

    Article  PubMed  Google Scholar 

  • Hanya G (2003) Age differences in food intake and dietary selection of wild male Japanese macaques. Primates 44:333–339

    Article  PubMed  Google Scholar 

  • 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 165:4544–4551

    CAS  PubMed  Google Scholar 

  • 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 387–402

    Google Scholar 

  • 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 43:305–322

    Article  CAS  PubMed  Google Scholar 

  • 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 23:416–431

    Article  Google Scholar 

  • 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 144–176

    Chapter  Google Scholar 

  • Huffman MA (1987) Consort intrusion and female mate choice in Japanese macaques (Macaca fuscata). Ethology 75:221–234

    Article  Google Scholar 

  • 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 307–350

    Chapter  Google Scholar 

  • Klein SL (2000) Hormones and mating system affect sex and species differences in immune function among vertebrates. Behav Process 51:149–166

    Article  Google Scholar 

  • Kudo A, Oyamada T, Okutsu M, Kinoshita H (1996) Intermediate hosts of Gongylonema pulchrum Molin, 1857, in Aomori prefecture, Japan. Jpn J Parasitol 45:222–229

    Google Scholar 

  • 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 4:1–9

    Google Scholar 

  • Maruhashi T (1980) Feeding behavior and diet of the Japanese monkey (Macaca fuscata yakui) on Yakushima island, Japan. Primates 21:141–160

    Article  Google Scholar 

  • 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 112:489–497

    Article  PubMed  Google Scholar 

  • Muroyama Y, Shimizu K, Sugiura H (2007) Seasonal variation in fecal testosterone levels in free-ranging male Japanese macaques. Am J Primatol 69:603–610

    Article  CAS  PubMed  Google Scholar 

  • Nunn C, Altizer S (2006) Infectious diseases in primates. Oxford University Press, Oxford

    Book  Google Scholar 

  • Pacala SW, Dobson AP (1988) The relation between the number of parasites/host and host age: population dynamic causes and maximum likelihood estimation. Parasitology 96:197–210

    Article  PubMed  Google Scholar 

  • 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 61:951–955

    CAS  PubMed  Google Scholar 

  • 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 87:722–729

    Article  CAS  PubMed  Google Scholar 

  • Poulin R (1996a) Helminth growth in vertebrate hosts: does host sex matter? Int J Parasitol 26:1311–1315

    Article  CAS  PubMed  Google Scholar 

  • Poulin R (1996b) Sexual inequalities in helminth infections: a cost of being a male? Am Nat 147:287–295

    Article  Google Scholar 

  • Poulin R (2007) Are there general laws in parasite ecology? Parasitology 134:763–776

    Article  CAS  PubMed  Google Scholar 

  • Roberts JL, Swan RA (1981) Quantitative studies of bovine haemonchosis. I. Relationship between fecal egg counts and total worm counts. Vet Parasitol 8:165–171

    Article  Google Scholar 

  • Rolff J (2002) Bateman’s principle and immunity. Proc R Soc Lond B Biol Sci 269:867–872

    Article  Google Scholar 

  • 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):69–76

    Article  CAS  PubMed  Google Scholar 

  • Sprague DS (1992) Life-history and male intertroop mobility among Japanese macaques (Macaca fuscata). Int J Primatol 13:437–454

    Article  Google Scholar 

  • 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 39:339–349

    Article  Google Scholar 

  • Wakelin D (1996) Immunity to parasites: how parasitic infections are controlled. Cambridge University Press, Cambridge

    Google Scholar 

  • Watanabe K (2008) Macaca fuscata ssp. yakui. In: IUCN red list of threatened species, version 2009, 2. http://www.primate-sg.org/redlist08.htm

  • Weyher AH, Ross C, Semple S (2006) Gastrointestinal parasites in crop raiding and wild foraging Papio anubis in Nigeria. Int J Primatol 27:1519–1534

    Article  Google Scholar 

  • 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 6–44

    Google Scholar 

  • Woolhouse MEJ (1998) Patterns in parasite epidemiology: the peak shift. Parasitol Today 14:428–434

    Article  CAS  PubMed  Google Scholar 

  • 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 39:257–273

    Article  Google Scholar 

  • Zuk M (1990) Reproductive strategies and disease susceptibility: an evolutionary viewpoint. Parasitol Today 6:231–233

    Article  CAS  PubMed  Google Scholar 

  • Zuk M, McKean KA (1996) Sex differences in parasite infections: patterns and processes. Int J Parasitol 26:1009–1023

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

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.

Author information

Authors and Affiliations

  1. Section of Social Systems Evolution, Department of Ecology and Social Behavior, Kyoto University Primate Research Institute, 41-2 Kanrin, Inuyama, Aichi, 484-8506, Japan

    Andrew J. J. MacIntosh & Michael A. Huffman

  2. 508 Mueller Laboratories, Center for Infectious Disease Dynamics, The Pennsylvania State University, University Park, PA, 16803, USA

    Alexander D. Hernandez

Authors
  1. Andrew J. J. MacIntosh
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Alexander D. Hernandez
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Michael A. Huffman
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Andrew J. J. MacIntosh.

About this article

Cite this article

MacIntosh, A.J.J., Hernandez, A.D. & Huffman, M.A. Host age, sex, and reproductive seasonality affect nematode parasitism in wild Japanese macaques. Primates 51, 353–364 (2010). https://doi.org/10.1007/s10329-010-0211-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10329-010-0211-9

Keywords

Search

Navigation