Advertisement

Primates

, Volume 55, Issue 2, pp 249–257 | Cite as

Mycophagy among Japanese macaques in Yakushima: fungal species diversity and behavioral patterns

  • Akiko Sawada
  • Hirotoshi Sato
  • Eiji Inoue
  • Yosuke Otani
  • Goro Hanya
Original Article

Abstract

Mycophagy (fungus-feeding) by Japanese macaques (Macaca fuscata yakui) in Yakushima has been observed by many researchers, but no detailed information is available on this behavior, including which fungal species are consumed. To provide a general description of mycophagy and to understand how and whether macaques avoid poisonous fungi, we conducted behavioral observation of wild Japanese macaques in Yakushima and used molecular techniques to identify fungal species. The results indicate that the diet of the macaques contains a large variety of fungal species (67 possible species in 31 genera), although they compose a very small portion of the total diet (2.2 % of annual feeding time). Fungi which were eaten by macaques immediately after they were picked up were less likely to be poisonous than those which were examined (sniffed, nibbled, carefully handled) by macaques. However, such examining behaviors did not appear to increase the macaques’ abilities to detect poisonous fungi. Fungi that were only partially consumed included more poisonous species than those fully consumed with/without examining behavior, yet this was not significant. Taste, therefore, might also play an important role in discriminating poisonous from non-poisonous.

Keywords

Japanese macaque Macaca fuscata yakui Mycophagy Poisonous fungi Fungal diversity 

Notes

Acknowledgments

The authors would like to express their gratitude to Drs. K. Watanabe, T. Furuichi, H. Imai and E. Sakaguchi for their great advice for this study. We are grateful to the members of the Department of Ecology and Social Behavior for their informative comments and advice. We are thankful to Mr. T. Saito for his great help in establishing phenology plots and to Yakushima Forest Environment Conservation Center and Kagoshima Prefectural Government for permission to carry out field research and sample collection on Yakushima. We also thank all our colleagues and friends who visited and stayed at Yakushima Field Station, Wildlife Research Center of Kyoto University, for sharing their valuable information and insights. This study was financially supported by JSPS/MEXT Grant-in-Aid for JSPS Fellows (No. 225374) to AS, JSPS-MEXT Grant-in-Aid for Challenging Exploratory Research (No. 23657018) and for Young Scientists (No. 20770195) to GH, and Global COE Program “Formation of a Strategic Base for Biodiversity and Evolutionary Research: from Genome to Ecosystem”. This research adhered to the guidelines established by KUPRI and the legal requirements in Japan.

Supplementary material

10329_2013_396_MOESM1_ESM.docx (54 kb)
Supplementary material 1 (DOCX 53 kb)

References

  1. Agetsuma N, Noma N (1995) Rapid shifting of foraging pattern by Yakushima macaques (Macaca fuscata yakui) in response to heavy fruiting of Myrica rubra. Int J Primatol 16:247–260CrossRefGoogle Scholar
  2. Agrahar-Murugkar D, Subbulakshmi G (2005) Nutritional value of edible wild mushrooms collected from the Khasi hills of Meghalaya. Food Chem 89:599–603CrossRefGoogle Scholar
  3. Bermejo M, Illera G, Pí JS (1995) Animals and mushrooms consumed by bonobos (Pan paniscus): new records from Lilungu (Ikela), Zaire. Int J f Primatol 16:879–898CrossRefGoogle Scholar
  4. Camazine S, Resch J, Eisner T, Meinwald J (1983) Mushroom chemical defense. J Chem Ecol 9:1439–1447PubMedCrossRefGoogle Scholar
  5. Eren SH, Demirel Y, Ugurlu S, Korkmaz I, Aktas C, Güven FMK (2010) Mushroom poisoning: retrospective analysis of 294 cases. Clinics 65:491–496PubMedCentralPubMedCrossRefGoogle Scholar
  6. Hanson AM, Hodge KT, Porter LM (2003) Mycophagy among primates. Mycology 17:6–10CrossRefGoogle Scholar
  7. Hanson A, Hall M, Porter L, Lintzenich B (2006) Composition and nutritional characteristics of fungi consumed by Callimico goeldii in Pando, Bolivia. Int J Primatol 27:323–346CrossRefGoogle Scholar
  8. Hanya G (2004) Diet of a Japanese Macaque troop in the coniferous forest of Yakushima. Int J Primatol 25:55–71CrossRefGoogle Scholar
  9. Harrison M (1984) Optimal foraging strategies in the diet of the green monkey, Cercopithecus sabaeus, at Mt. Assirik, Senegal. Int J Primatol 5:435–471CrossRefGoogle Scholar
  10. Hilário RR, Ferrari SF (2010) Feeding ecology of a group of buffy-headed marmosets (Callithrix flaviceps): fungi as a preferred resource. Am J Primatol 72:515–521PubMedGoogle Scholar
  11. 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 43:305–320PubMedCrossRefGoogle Scholar
  12. Imazeki R, Otani Y, Hongo T (1988) Fungi of Japan. Yama-Kei Publishers (in Japanese), TokyoGoogle Scholar
  13. Ishihara Y, Yamaura Y (1992) Descriptive epidemiology of mushroom poisoning in Japan (in Japanese). Jpn J Hyg 46:1071–1078CrossRefGoogle Scholar
  14. Johnson CN (1996) Interactions between mammals and ectomycorrhizal fungi. Trends Ecol Evol 11:503–507PubMedCrossRefGoogle Scholar
  15. Lehmkuhl JF, Gould LE, Cázares E, Hosford DR (2004) Truffle abundance and mycophagy by northern flying squirrels in eastern Washington forests. For Ecol Manag 200:49–65CrossRefGoogle Scholar
  16. Murakami Y (1989) Spatial changes of species composition and seasonal fruiting of the Agaricales in Castanopsis cuspidate forest. Trans Mycol Soc Jpn 30:89–103Google Scholar
  17. Porter L (2001) Dietary differences among sympatric Callitrichinae in Northern Bolivia: Callimico goeldii, Saguinus fuscicollis and S. labiatus. Int J Primatol 22:961–992CrossRefGoogle Scholar
  18. Porter LM, Garber PA (2004) Goeldi’s monkeys: a primate paradox? Evol Anthropol 13:104–115CrossRefGoogle Scholar
  19. Rowe N, Mittermeier RA (1996) The pictorial guide to the living primates. Pogonias Press, East HamptonGoogle Scholar
  20. Sato H, Murakami N (2008) Reproductive isolation among cryptic species in the ectomycorrhizal genus Strobilomyces: population-level CAPS marker-based genetic analysis. Mol Phylog Evol 48:326–334CrossRefGoogle Scholar
  21. Sherratt TN, Wilkinson DM, Bain RS (2005) Explaining Dioscorides’ “double difference”: why are some mushrooms poisonous, and do they signal their unprofitability? Am Nat 166:767–775PubMedCrossRefGoogle Scholar
  22. Tsujino R, Sato H, Imamura A, Yumoto T (2009) Topography-specific emergence of fungal fruiting bodies in warm temperate evergreen broad-leaved forests on Yakushima Island, Japan. Mycoscience 50:388–399CrossRefGoogle Scholar
  23. Unluoglu I, Tayfur M (2003) Mushroom poisoning: an analysis of the data between 1996 and 2000. Eur J Emerg Med 10:23–26PubMedCrossRefGoogle Scholar
  24. Watts DP (1984) Composition and variability of mountain gorilla diets in the Central Virungas. Am J Primatol 7:323–356CrossRefGoogle Scholar
  25. White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols: a guide to methods and applications. Academic Press, San Diego, CA, pp 315–322Google Scholar
  26. Yamagiwa J (2008) History and present scope of field studies on Macaca fuscata yakui at Yakushima Island, Japan. Int J Primatol 29:49–64CrossRefGoogle Scholar

Copyright information

© Japan Monkey Centre and Springer Japan 2013

Authors and Affiliations

  • Akiko Sawada
    • 1
  • Hirotoshi Sato
    • 2
  • Eiji Inoue
    • 3
  • Yosuke Otani
    • 1
  • Goro Hanya
    • 1
  1. 1.Primate Research InstituteKyoto UniversityInuyamaJapan
  2. 2.Graduate School of Global Environmental StudiesKyoto UniversityKyotoJapan
  3. 3.Graduate School of ScienceKyoto UniversityKyotoJapan

Personalised recommendations