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Dietary adaptations of temperate primates: comparisons of Japanese and Barbary macaques

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Abstract

Habitat, diet and leaf chemistry are compared between Japanese and Barbary macaques to reveal the similarities and differences in dietary adaptations of temperate primates living at the eastern and western extremes of the genus Macaca. Tree species diversity and proportion of fleshy-fruited species are much higher in Japan than in North Africa. Both species spend considerable annual feeding time on leaves. Japanese macaques prefer fruits and seeds over leaves, and Barbary macaques prefer seeds. These characteristics are adaptive in temperate regions where fruit availability varies considerably with season, since animals can survive during the lean period by relying on leaf and other vegetative foods. The two species are different with respect to the higher consumption of herbs by Barbary macaques, and the leaves consumed contain high condensed and hydrolysable tannin for Barbary but not for Japanese macaques. Barbary macaques supplement less diverse tree foods with herbs. Because of the low species diversity and high tannin content of the dominant tree species, Barbary macaques may have developed the capacity to cope with tannin. This supports the idea that digestion of leaves is indispensable to survive in temperate regions where fruit and seed foods are not available for a prolonged period during each year.

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References

  • Agetsuma N (1995) Dietary selection by Yakushima macaques (Macaca fuscata yakui): the influence of food availability and temperature. Int J Primatol 16:611–627

    Article  Google Scholar 

  • Agetsuma N, Nakagawa N (1998) Effects of habitat differences on feeding behaviors of Japanese monkeys: comparison between Yakushima and Kinkazan. Primates 39:275–289

    Article  Google Scholar 

  • Ajbilou R, Maranon T, Arroyo J (2006) Ecological and biogeographical analyses of Mediterranean forests of northern Morocco. Acta Oecol 29:104–113

    Article  Google Scholar 

  • Ali R (1986) Feeding ecology of the bonnet macaque at the Mundanthurai Sanctuary, Tamil Nadu. J Bombay Nat Hist Soc 83:98–110

    Google Scholar 

  • Bleisch W, Liu Z, Dierenfeld E, Xie J (1998) Selected nutrient analysis of plants in the diet of the Guizhou snub-nosed monkey (Rhinopithecus [Rhinopithecus] brelichi). In: Jablonski N (ed) The natural history of the doucs and snub-nosed monkeys. World Scientific, Singapore, pp 241–254

    Google Scholar 

  • Burnham KP, Anderson DR (2002) Model selection and multi-model inference, 2nd edn. Springer, New York

    Google Scholar 

  • Clutton-Brock TH (1977) Primate ecology: studies of feeding and ranging behaviour in lemurs, monkeys and apes. Academic Press, Brighton

    Google Scholar 

  • Colwell RK, Coddington JA (1994) Estimating terrestrial biodiversity through extrapolation. Philos Trans R Soc Lond B Biol Sci 345:101–118

    Article  PubMed  CAS  Google Scholar 

  • Curtin F, Schulz P (1998) Multiple correlations and Bonferroni’s correction. Biol Psychiatry 44:775–777

    Article  PubMed  CAS  Google Scholar 

  • Drucker GR (1984) The feeding ecology of Barbary macaque and cedar forest conservation in the Moroccan Moyen Atlas. In: Fa JE (ed) The Barbary Macaque: a case study in conservation. Plenum, New York, pp 135–164

    Google Scholar 

  • Fa JE (1984a) The Barbary Macaque: a case study in conservation. Plenum, New York

    Google Scholar 

  • Fa JE (1984b) Habitat distribution and habitat preference in Barbary macaques (Macaca sylvanus). Int J Primatol 5:273–286

    Article  Google Scholar 

  • Fa JE (1989) The Genus Macaca: a review of taxonomy and evolution. Mammal Rev 19:45–81

    Article  Google Scholar 

  • Fleagle JG (1999) Primate adaptation and evolution, 2nd edn. Academic, London

    Google Scholar 

  • Fragaszy DM, Boinski S, Whipple J (1992) Behavioral sampling in the field: comparison of individual and group sampling methods. Am J Primatol 26:259–275

    Article  Google Scholar 

  • Furuichi T, Hashimoto C, Tashiro Y (2001) Fruit availability and habitat use by chimpanzees in the Kalinzu Forest, Uganda: examination of fallback foods. Int J Primatol 22:929–945

    Article  Google Scholar 

  • Goldstein SJ, Richard AF (1989) Ecology of rhesus macaques (Macaca mulatta) in northwest Pakistan. Int J Primatol 10:531–567

    Article  Google Scholar 

  • Grueter CC, Li DY, Ren BP, Wei FW, Xiang ZF, van Schaik CP (2009) Fallback foods of temperate-living primates: a case study on snub-nosed monkeys. Am J Phys Anthropol 140:700–715

    Article  PubMed  Google Scholar 

  • Hanya G (2004) Diet of a Japanese macaque troop in the coniferous forest of Yakushima. Int J Primatol 25:55–71

    Article  Google Scholar 

  • Hanya G, Aiba S (2010) Fruit fall in tropical and temperate forests: implications for frugivore diversity. Ecol Res 25:1081–1090

    Google Scholar 

  • Hanya G, Yamada H, Arakane T (2002) Expeditionary ranging by a Japanese macaque troop in Hieizan. Anthropol Sci 110:415–420

    Google Scholar 

  • Hanya G, Noma N, Agetsuma N (2003) Altitudinal and seasonal variations in the diet of Japanese macaques in Yakushima. Primates 44:51–59

    Article  PubMed  Google Scholar 

  • Hanya G, Yoshihiro S, Zamma K, Matsubara H, Ohtake M, Kubo R, Noma N, Agetsuma N, Takahata Y (2004) Environmental determinants of the altitudinal variations in relative group densities of Japanese macaques on Yakushima. Ecol Res 19:485–493

    Article  Google Scholar 

  • Hanya G, Kiyono M, Takafumi H, Tsujino R, Agetsuma N (2007) Mature leaf selection of Japanese macaques: effects of availability and chemical content. J Zool 273:140–147

    Article  Google Scholar 

  • Hasegawa K (1993) Nutritional analysis (in Japanese). Baifukan, Tokyo

    Google Scholar 

  • Hemingway C, Bynum N (2005) The influence of seasonality on primate diet and ranging. 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 57–104

    Chapter  Google Scholar 

  • Herrera CM (1984) A study of avian frugivores, bird-dispersed plants, and their interaction in Mediterranean scrublands. Ecol Monogr 54:1–23

    Article  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  PubMed  CAS  Google Scholar 

  • Iwamoto T (1982) Food and nutritional condition of free ranging Japanese monkeys on Koshima Islet during winter Primates 23:153–170

    Google Scholar 

  • Izumiyama S (2002) Above the forest limit (in Japanese). In: Oi T, Masui K (eds) Natural history of Japanese macaque: their ecological diversity and conservation. Tokai University Press, Tokyo, pp 67–77

    Google Scholar 

  • Janson C, Chapman C (1999) Resources and primate community structure. In: Fleagle J, Janson C, Reed K (eds) Primate communities. Cambridge Univ Press, Cambridge, pp 237–267

    Chapter  Google Scholar 

  • Kirkpatrick RC (1999) Colobine diet and social organization. In: Dolhinow P, Fuentes A (eds) The nonhuman primates. Mayfield, Mountain View, pp 93–105

    Google Scholar 

  • Kirkpatrick RC, Zou RJ, Dierenfeld ES, Zhou HW (2001) Digestion of selected foods by Yunnan snub-nosed monkey Rhinopithecus bieti (Colobinae). Am J Phys Anthropol 114:156–162

    Article  PubMed  CAS  Google Scholar 

  • Knott CD (1998) Changes in orangutan caloric intake, energy balance, and ketones in response to fluctuating fruit availability. Int J Primatol 19:1061–1079

    Article  Google Scholar 

  • Komiyama A, Kato S, Teranishi M (2001) Differential overstory leaf flushing contributes to the formation of a patchy understory. J For Res 6:163–171

    Article  Google Scholar 

  • Kurita H, Shiniomura T, Fujita T (2002) Temporal variation in Japanese macaque bodily mass. Int J Primatol 23:411–428

    Article  Google Scholar 

  • Lambert JE (1998) Primate digestion: interactions among anatomy, physiology, and feeding ecology. Evol Anthropol 7:8–20

    Article  Google Scholar 

  • Marshall AJ, Wrangham RW (2007) Evolutionary consequences of fallback foods. Int J Primatol 28:1218–1235

    Article  Google Scholar 

  • Mehlman PT (1988) Food resources of the wild barbary macaque (Macaca sylvanus) in high altitude fir forest, Ghomaran Rif, Morocco. J Zool 214:469–490

    Article  Google Scholar 

  • Ménard N (1985) Le régime alimentaire de Macaca sylvanus dans différents habitats d’Algérie: I. Régime en chênaie décidue. Revue d’Ecologie (La Terre Et La Vie) 40:351–466

    Google Scholar 

  • Ménard N (2002) Ecological plasticity of Barbary macaques (Macaca sylvanus). Evol Anthropol 11:95–100

    Article  Google Scholar 

  • Ménard N, Qarro M (1999) Bark stripping and water availability: a comparative study between Moroccan and Algerian Barbary Macaques (Macaca sylvanus). Revue d’Ecologie (La Terre Et La Vie) 54:123–132

    Google Scholar 

  • Ménard N, Vallet D (1986) Le régime alimentaire de Macaca sylvanus dans différents habitats d’Algérie: II. Régime en forêt sempervirente et sur les sommets roucheux. Revue d’Ecologie (La Terre Et La Vie) 41:173–192

    Google Scholar 

  • Ménard N, Vallet D (1988) Disponibilités et utilisation des ressources par le magot (Macaca sylvanus) dans différents milieux en Algérie. Revue d’Ecologie (La Terre Et La Vie) 43:201–250

    Google Scholar 

  • Muroyama Y, Kanamori H, Kitahara E (2006) Seasonal variation and sex differences in the nutritional status in two local populations of wild Japanese macaques. Primates 47:355–364

    Article  PubMed  Google Scholar 

  • O’Brien TG, Kinnaird MF (1997) Behavior, diet, and movements of the Sulawesi crested black macaque (Macaca nigra). Int J Primatol 18:321–351

    Article  Google Scholar 

  • Pond CM (1978) Morphological aspects and ecological and mechanical consequences of fat deposition in wild vertebrates. Annu Rev Ecol Syst 9:519–570

    Article  Google Scholar 

  • Porter LJ (1989) Tannins. In: Dey PM, Harborne JB (eds) Methods in plant biochemistry, vol 1. Plant phenolics. Academic, London, pp 389–419

    Google Scholar 

  • Rautio P, Bergvall UA, Karonen M, Salminen JP (2007) Bitter problems in ecological feeding experiments: commercial tannin preparations and common methods for tannin quantifications. Biochem Syst Ecol 35:257–262

    Article  CAS  Google Scholar 

  • Sakai S (2002) General flowering in lowland mixed dipterocarp forests of South-east Asia. Biol J Linn Soc 75:233–247

    Article  Google Scholar 

  • Skopec MM, Haley S, Torregrossa AM, Dearing MD (2008) An oak (Quercus agrifolia) specialist (Neotoma macrotis) and a sympatric generalist (Neotoma lepida) show similar intakes and digestibilities of oak. Physiol Biochem Zool 81:426–433

    Article  PubMed  Google Scholar 

  • Su HH, Lee LL (2001) Food habits of Formosan rock macaques (Macaca cyclopis) in Jentse, northeastern Taiwan, assessed by fecal analysis and behavioral observation. Int J Primatol 22:359–377

    Article  Google Scholar 

  • Suzuki A (1965) An ecological study of wild Japanese monkeys in snowy areas: focused on their food habits. Primates 6:31–72

    Article  Google Scholar 

  • Terborgh J (1983) Five New World primates. Princeton University Press, Princeton

    Google Scholar 

  • Ting S, Hartley S, Burns KC (2008) Global patterns in fruiting seasons. Glob Ecol Biogeogr 17:648–657

    Article  Google Scholar 

  • Tsuji Y, Takatsuki S (2004) Food habits and home range use of Japanese macaques on an island inhabited by deer. Ecol Res 19:381–388

    Article  Google Scholar 

  • Tsuji Y, Fujita S, Sugiura H, Saito C, Takatsuki S (2006) Long-term variation in fruiting and the food habits of wild Japanese macaques on Kinkazan Island, northern Japan. Am J Primatol 68:1068–1080

    Article  PubMed  Google Scholar 

  • van Schaik CP, Pfannes K (2005) Tropical climates and phenology: a primate perspective. 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 23–54

    Chapter  Google Scholar 

  • van Schaik CP, Terborgh JW, Wright SJ (1993) The phenology of tropical forests: adaptive significance and consequences for primary consumers. Annu Rev Ecol Syst 24:353–377

    Article  Google Scholar 

  • van Soest PJ, Robertson JB, Lewis BA (1991) Methods for dietary fiber, neutral detergent fiber, and nonstarch polysaccharides in relation to animal nutrition. J Dairy Sci 74:3583–3597

    Article  PubMed  Google Scholar 

  • Wada K (1975) Ecology of wintering among Japanese monkeys in Shiga heights and its adaptive significance. Physiol Ecol Jpn 16:9–14

    Google Scholar 

  • Waterman P (1984) Food acquisition and processing as a function of plant chemistry. In: Chivers DJ, Wood BA, Bilsborough A (eds) Food acquisition and processing in primates. Plenum, New York, pp 177–211

    Google Scholar 

  • Willis RB, Allen PR (1998) Improved method for measuring hydrolyzable tannins using potassium iodide. Analyst 123:435–439

    Article  CAS  Google Scholar 

  • Willson MF, Irvine AK, Walsh NG (1989) Vertebrate dispersal syndromes in some Australian and New Zealand plant communities, with geographic comparisons. Biotropica 21:133–147

    Article  Google Scholar 

  • Yamagiwa J, Hill D (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 

  • Yeager CP (1996) Feeding ecology of the long-tailed macaque (Macaca fascicularis) in Kalimantan Tengah, Indonesia. Int J Primatol 17:51–62

    Article  Google Scholar 

Download references

Acknowledgments

We would like to thank our friends and colleagues who supported our fieldwork in Japan, Morocco and Algeria. The Ministry of Environment and Forestry Agency, Japan, and Haut Commissariat aux Eaux et Forêt et à la Lutte Contre la Désertification, Morocco gave us permission to study in the area. Dr. Y. Tsuji kindly provided his published data. This study was financed by the JSPS Core-to-core Program HOPE, Cooperation Research Program of KUPRI and the MEXT Grant-in-Aid for JSPS Fellows, Grant-in-Aid for Young Scientists (#20770195 and #22687002) to G.H., the 21st Century COE Program (A14) and Global COE Program “Formation of a Strategic Base for Biodiversity and Evolutionary Research: from Genome to Ecosystem”.

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Hanya, G., Ménard, N., Qarro, M. et al. Dietary adaptations of temperate primates: comparisons of Japanese and Barbary macaques. Primates 52, 187–198 (2011). https://doi.org/10.1007/s10329-011-0239-5

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