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Niche separation of sympatric macaques, Macaca assamensis and M. mulatta, in limestone habitats of Nonggang, China

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Abstract

Comparative studies of sympatric species are essential in understanding those species’ behavioral and ecological adaptations as well as the mechanisms that can reduce resource competition enough to allow coexistence. We collected data on diet, activity budget and habitat use from two sympatric macaque species, the Assamese macaque (Macaca assamensis) and the rhesus macaque (M. mulatta), in a limestone seasonal rainforest of Nonggang Nature Reserve, southwestern Guangxi, China. Our results show that the two sympatric macaques differ in diet, activity budget, and habitat use: (1) out of the 131 plant species that were used by both macaque species as food over the year, only 15 plant species (11 %) were shared. Rhesus macaques used more plant species as major foods, and had higher dietary diversity and evenness indexes than Assamese macaques. (2) Assamese macaques fed predominantly on leaves, whereas rhesus macaques fed more selectively on fruits. The rhesus macaques’ diet varied according to season, and was significantly correlated to season fluctuation in fruit availability. (3) Assamese macaques devoted more time to resting, and less time to feeding than rhesus macaques (4) Assamese macaques were present mostly on the cliff, and tended to stay on the ground, whereas rhesus macaques were present mostly on the hillside, and showed preference to lower and middle canopy. The observed differences in diet and habitat use between the two macaque species represent behavioral patterns enabling their coexistence.

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References

  • Ahsan MF (1994) Feeding ecology of the primates of Bangladesh. In: Thierry B, Anderson RJ, Roeder JJ, Herrenschmidt N (eds) Current primatology. vol. Ecology and evolution. University of Louis Pasteur, Strasbourg, pp 79–86

  • Altmann J (1974) Observational study of behavior: sampling methods. Behaviour 49:227–262

    Article  CAS  PubMed  Google Scholar 

  • Bennett EL, Davies AG (1994) The ecology of Asian colobines. In: Davies AG, Oates JF (eds) Colobine monkeys: their ecology, behavior and evolution. Cambridge University Press, Cambridge, pp 129–171

    Google Scholar 

  • Britt A, Randriamandratonirina NJ, Glasscock KD, Iambana BR (2002) Diet and feeding behaviour of Indri indri in a low-altitude rain forest. Folia Primatol 73:225–239

    Article  PubMed  Google Scholar 

  • Chalise MK (2003) Assamese macaques (Macaca assamensis) in Nepal. Primate Conserv 19:99–107

    Google Scholar 

  • Chapman CA, Pavelka MSM (2005) Group size in folivorous primates: ecological constraints and possible influence of social factors. Primates 46:1–9

    Article  PubMed  Google Scholar 

  • Chivers DJ, Hladik CM (1980) Morphology of the gastrointestinal tract in primates: comparisons with other mammals in relation to diet. J Morphol 166:337–386

    Article  CAS  PubMed  Google Scholar 

  • Cords M (1986) Interspecific and intraspecific variation in diet of two forest guenons, Cercopithecus ascanius and C. mitis. J Anim Ecol 55:811–827

    Article  Google Scholar 

  • Feeroz MM (2012) Niche separation between sympatric pig-tailed macaque (Macaca leonina) and rhesus macaque (M. mulatta) in Bangladesh. J Primatol 1:106

    Google Scholar 

  • Fooden J (1980) Classification and distribution of living macaques. In: Lindburg DG (ed) The macaques: studies in ecology, behavior and evolution. Van Nostrand Reinhold, New York, pp 1–9

    Google Scholar 

  • Ganzhorn JU (1989) Niche separation of seven lemur species in the eastern rainforest of Madagascar. Oecologia 79:279–286

    Article  Google Scholar 

  • Gause G (1934) The struggle for existence. Williams and Witkins, Baltimore

    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 

  • Guangxi Forest Department (1993) Nature reserve in Guangxi. China Forestry Publishing House, Beijing (in Chinese)

    Google Scholar 

  • Hadi S, Ziegler T, Waltert M, Syamsuri F, Mühlenberg M, Hodges JK (2012) Habitat use and trophic niche overlap of two sympatric colobines, Presbytis potenziani and Simias concolor, on Siberut Island, Indonesia. Int J Primatol 33:218–232

    Article  Google Scholar 

  • Hanya G, Ménard N, Qarro M, Tattou MI, Fuse M, Vallet D, Yamada A, Go M, Takafumi H, Tsujino R, Agetsuma N, Wada K (2011) Dietary adaptations of temperate primates: comparisons of Japanese and Barbary macaques. Primates 52:187–198

    Article  PubMed  Google Scholar 

  • Kummar RS, Mishra C, Sinha A (2007) Foraging ecology and time activity budgets of the Arunachal macaque Macaca munzala, a preliminary study. Curr Sci 93:532–539

    Google Scholar 

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

    Article  Google Scholar 

  • Liang ZF, Liang JY, Liu LF, Mo XL (1988) A report on vegetation in Nonggang Nature Reserve. Guihaia (Supplement 1): 83–184 (in Chinese)

  • MacKinnon J, MacKinnon K (1980) Niche differentiation in a primate community. In: Chivers D (ed) Malayan forest primates. Plenum Press, New York, pp 167–190

    Chapter  Google Scholar 

  • Nadjafzadeh MN, Heymann EW (2008) Prey foraging of red titi monkeys, Callicebus cupreus, in comparison to sympatric tamarins, Saguinus mystax and Saguinus fuscicollis. Am J Phys Anthropol 135:56–63

    Article  PubMed  Google Scholar 

  • Nakagawa N (1999) Differential habitat utilization by patas monkeys (Erythrocebus patas) and tantalus monkeys (Cercopithecus aethiops tantalus) living sympatrically in northern Cameroon. Am J Primatol 49:243–264

    Article  CAS  PubMed  Google Scholar 

  • Nakagawa N (2003) Difference in food selection between patas monkeys (Erythrocebus patas) and tantalus monkeys (Cercopithecus aethiops tantalus) in Kala Maloue National Park, Cameroon, in relation to nutrient content. Primates 44:3–11

    Article  PubMed  Google Scholar 

  • Pianka ER (1973) The structure of lizard communities. Ann Rev Ecol Syst 4:53–74

    Article  Google Scholar 

  • Pianka ER (1981) Competition and niche theory. In: May R (ed) Theoretical ecology: principles and applications. Blackwell Scientific Publications, Oxford, pp 167–196

    Google Scholar 

  • Porter LM (2001) Dietary differences among sympatric Callitrichinae in northern Bolivia: Callimico goeldii, Saguinus fuscicollis and S. labiatus. Int J Primatol 22:961–992

    Article  Google Scholar 

  • Powzyk JA, Mowry CB (2003) Dietary and feeding differences between sympatric Propithecus diadema diadema and Indri indri. Int J Primatol 24:1143–1162

    Article  Google Scholar 

  • Pyke GH, Pulliam HR, Charnov EL (1977) Optimal foraging: a selective review of theory and tests. Quart Rev Biol 52:137–157

    Article  Google Scholar 

  • Richard AF (1985) Primates in nature. W.H. Freeman, New York

    Google Scholar 

  • Richard AF, Goldstein SJ, Dewar RE (1989) Weed macaques: the evolutionary implications of macaque feeding ecology. Int J Primatol 10:569–594

    Article  Google Scholar 

  • Rodman PS (1991) Structural differentiation of microhabitats of sympatric macaca fascicularis and M. nemestrina in east Kalimantan, Indonsia. Int J Primaol 12:357–375

    Article  Google Scholar 

  • Schoener T (1974) Resource partitioning in ecological communities. Science 185:27–39

    Article  CAS  PubMed  Google Scholar 

  • Schreier BM, Harcourt AH, Coppeto SA, Somi MF (2009) Interspecific competition and niche separation in primates: a global analysis. Biotropica 41:283–291

    Article  Google Scholar 

  • Shu ZM, Zhao TL, Huang QC (1988) Vegetation survey in Nonggang Nature Reserve. Guihaia (Supplement 1): 185–214 (in Chinese)

  • Singh M, Roy K, Singh M (2011) Resource partitioning in sympatric langurs and macaques in tropical rainforests of the central western Ghats, south India. Am J Primatol 73:335–346

    Article  PubMed  Google Scholar 

  • Smith RJ, Jungers WL (1997) Body mass in comparative primatology. J Hum Evol 32:523–559

    Article  CAS  PubMed  Google Scholar 

  • Stevenson PR, Quinones MJ, Ahumada JA (2000) Influence of fruit availability on ecological overlap among four neotropical primates at Tinigua National Park, Colombia. Biotropica 32:533–544

    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 

  • Sushma HS, Singh M (2006) Resource partitioning and interspecific interactions among sympatric rainforest arboreal mammals of the Western Ghats, India. Behav Ecol 17:479–490

    Article  Google Scholar 

  • Tang HX, Zhou QH, Huang ZH, Meng YJ, Huang CM (2011) Activity patterns and time budgets of the rhesus macaque in karst habitat. Chin J Zool 46(2):32–38 (in Chinese)

    Google Scholar 

  • Tokeshi M (1999) Species coexistence: ecological and evolutionary perspectives. Blackwell Scientific Publications, Oxford

    Google Scholar 

  • Tomblin D, Cranford J (1994) Ecological niche differences between Alouatta palliate and Cebus capucinus comparing feeding modes, branch use and diet. Primates 33:265–274

    Article  Google Scholar 

  • Tutin CEG, Fernandez M (1993) Composition of the diet of chimpanzees and comparisons with that of sympatric lowland gorillas in the Lopé Reserve, Gabon. Am J Primatol 30:195–211

    Article  Google Scholar 

  • Zhang RZ, Cheng LW, Qu WY, Chris C (2002) The primates of China: biogeography and conservation status: past, present and future. China Forestry Publishing House, Beijing (in Chinese)

    Google Scholar 

  • Zhou QH, Wei H, Huang ZH, Li YB, Lu MX, Huang CM (2007) Activity patterns and time budgets of the Assamese macaque Macaca assamensis in the Longgang Nature Reserve, China. Acta Zool Sin 53(5):791–799 (in Chinese)

    Google Scholar 

Download references

Acknowledgments

This study was supported by National Nature Science Foundation of China (No. 31172122, 31360093, 31372145), Guangxi Nature Science Foundation (2012GXNSFAA053039, 2012GXNSFBA053045), Guangxi Key Laboratory of Rare and Endangered Animal Ecology, Guangxi Normal University (1301z003), and the Assessment, Monitoring and Conservation of Tibetan macaques Project of the National Forestry Administration of China. We thank the Guangxi Forestry Bureau, and Nonggang National Nature Reserve.

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Correspondence to Chengming Huang.

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Zhou, Q., Wei, H., Tang, H. et al. Niche separation of sympatric macaques, Macaca assamensis and M. mulatta, in limestone habitats of Nonggang, China. Primates 55, 125–137 (2014). https://doi.org/10.1007/s10329-013-0385-z

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