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