Mammalian Biology

, Volume 94, Issue 1, pp 48–53 | Cite as

The effect of oil palm agricultural expansion on group size of long-tailed macaques (Macacafascicularis) in Peninsular Malaysia

  • Sze Ling Tee
  • Ahmad Solihhin
  • Shahidin A. Juffiry
  • Tengku Rinalfi Putra
  • Alex M. Lechner
  • Badrul AzharEmail author
Original investigation


Large-scale expansion of oil palm (Elaeis guineensis) monocultures across Southeast Asia are creating ecosystems with homogenous habitats with low species diversity. However, heterogeneity varies between oil palm smallholdings and large-scale plantations, with greater habitat heterogeneity found on smallholdings. To date, there has been a paucity of field research on primate species, particularly macaques in oil palm plantations. In this study, we investigate the group size of long-tailed macaques (Macacafascicularis) in four habitat types: unlogged forest, logged forest, large-scale oil palm plantations, and smallholdings. Field censuses were conducted in 2015 and 2016 to determine the group size of M. fascicularis in large-scale oil palm plantations and oil palm smallholdings. These data from oil palm plantations were compared to surveys conducted on a logged lowland forest reserve and a previous study in an unlogged lowland forest. We found that group size of M. fascicularis in large-scale plantations was lower compared to smallholdings, logged forest and unlogged forest. The chi-square test showed that the age class (juvenile or adult) of M. fascicularis was associated with farming systems. The paper concludes that the expansion of large-scale oil palm monocultures should be limited because of its adverse impacts on biodiversity including common species such as M. fascicularis.


Oil palm Large-scale plantation Logged forest Long-tailed macaque Smallholdings Unlogged forest 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Adila, N., Sasidhran, S., Kamarudin, N., Puan, C.I., Azhar, B., Lindenmayer, D.B., 2017. Effects of peat swamp logging and agricultural expansion on species richness of native mammals in Peninsular Malaysia. Basic Appl. Ecol. 22, 1–10.Google Scholar
  2. Aldrich-Blake, F.P.G., 1980. Long-tailed macaques. In: Chivers, D.J. (Ed.), Malayan Forest Primates: Ten Years’ Study in Tropical Rain Forest. Plenum Press, New York, pp. 147–165.Google Scholar
  3. Ancrenaz, M., Oram, F., Ambu, L., Lackman, I., Ahmad, E., Elahan, H., Kler, H., Abram, N.K., Meijaard, E., 2015. Of Pongo: palms and perceptions: a multidisciplinary assessment of Bornean orang-utans Pongo pygmaeus in oil palm context. Oryx 49, 465–472.Google Scholar
  4. Anderson, J., Rowcliffe, J.M., Cowlishaw, G., 2007. Does the matrix matter? A forest primate in a complex agricultural landscape. Biol. Conserv. 135, 212–222.Google Scholar
  5. Azhar, B., Lindenmayer, D.B., Wood, J., Fischer, J., Manning, A., McElhinny, C., Zakaria, M., 2011. The conservation value of oil palm plantation estates, smallholdings and logged peat swamp forest for birds. For. Ecol. Manage. 262, 2306–2315.Google Scholar
  6. Azhar, B., Lindenmayer, D., Wood, J., Fischer, J., Manning, A., McElhinny, C., Zakaria, M., 2013. Contribution of illegal hunting, culling of pest species, road accidents and feral dogs to biodiversity loss in established oil-palm landscapes. Wildl. Res. 40, 1–9.Google Scholar
  7. Azhar, B., Puan, C.L., Zakaria, M., Hassan, N., Arif, M., 2014. Effects of monoculture and polyculture practices in oil palm smallholdings on tropical farmland birds. Basic Appl. Ecol. 15, 336–346.Google Scholar
  8. Azhar, B., Saadun, N., Puan, C.L., Kamarudin, N., Aziz, N., Nurhidayu, S., Fischer, J., 2015. Promoting landscape heterogeneity to improve the biodiversity benefits of certified palm oil production: evidence from Peninsular Malaysia. Glob. Ecol. Conserv. 3, 553–561.Google Scholar
  9. Azhar, B., Saadun, N., Prideaux, M., Lindenmayer, D.B., 2017. The global palm oil sector must change to save biodiversity and improve food security in the tropics. J. Environ. Manage. 203, 457–466.PubMedGoogle Scholar
  10. Bernard, H., Fjeldsá, J., Mohamed, M., 2009. A case study on the effects of disturbance and conversion of tropical lowland rain forest on the non-valant small mammals in North Borneo: management implications. Mammal Study 34, 85–96.Google Scholar
  11. Bernstein, I.S., Balcaen, P., Dresdale, L., Gouzoules, H., Kavanagh, M., Patterson, T., Neymann-Warner, P., 1976. Differential effects of forest fragmentation on primate populations. Primates 17, 401–411.Google Scholar
  12. Bhagwat, S.A., Willis, K.J., 2008. Agroforestry as a solution to the oil-palm debate. Conserv. Biol. 22, 1368–1369.PubMedGoogle Scholar
  13. Brotcorne, F., Maslarov, C., Wandia, I.N., Fuentes, A., Beudels-Jamar, R.C., Huynen, M.C., 2014. The role of anthropic, ecological, and social factors in sleeping site choice by long-tailed Macaques (Macacafasaculans). Am. J. Primatol. 76, 1140–1150.PubMedGoogle Scholar
  14. Chung, G.F., Lee, C.T., Chee, K.H., 2016. Pictorial Guide to Oil Palm Cultivation and Mammalian Pests. Agricultural Crop Trust, Malaysia.Google Scholar
  15. Eudey, A.A., 2008. The crab-eating macaque (Macacafasaculans): widespread and rapidly declining. Primate Conserv. 23, 129–132.Google Scholar
  16. Fittinghoff, NA, 1978. Macaca fasciculans of Eastern Borneo: Ecology, Demography, Social Behavior, and Social Organization in Relation to a Refuging Habitus. University Microfilms International, London.Google Scholar
  17. Fitzherbert, E.B., Struebig, M.J., Morel, A., Danielson, F., Brühl, C.A., Donald, P.F., Phalan, B., 2008. How will oil palm expansion affect biodiversity? Trends Ecol. Evol. 23, 538–545.Google Scholar
  18. Fuentes, A., Gamerl, S., 2005. Disproportionate participation by age/sex classes in aggressive interactions between long-tailed macaques (Macaca fasciculans) and human tourists at Padangtegal monkey forest, Bali, Indonesia. Am. J. Primatol. 66, 197–204.PubMedGoogle Scholar
  19. Gallmetzer, N., Schulze, C.H., 2015. Impact of oil palm agriculture on understory amphibians and reptiles: a Mesoamerican perspective. Glob. Ecol. Conserv. 4, 95–109.Google Scholar
  20. Gibson, L., 2011. Possible shift in macaque trophic level following a century of biodiversity loss in Singapore. Primates 52, 217–220.PubMedGoogle Scholar
  21. Gillespie, G.R., Ahmad, E., Elahan, B., Evans, A., Ancrenaz, M., Goossens, B., Scroggie, M.P., 2012. Conservation of amphibians in Borneo: relative value of secondary tropical forest and non-forest habitats. Biol. Conserv. 152, 136–144.Google Scholar
  22. Gumert, M.D., 2011. The Common Monkey of Southeast Asia: Longtailed Macaque Populations, Ethnophoresy, and Their Occurrence in Human Environments. Monkeys on the Edge: Ecology and Management of Long-tailed Macaques and Their Interface With Humans. Cambridge University Press, New York, pp. 3–44.Google Scholar
  23. Hadi, I., Suryobroto, B., Perwitasari-Farajallah, D., 2007. Food preference of semi provisioned macaques based on feeding duration and foraging party size. Hayati J. Biosci. 14, 13–17.Google Scholar
  24. Hamada, Y., Urasopon, N., Hadi, I., Malaivijitnond, S., 2006. Body size and proportions and pelage color of free-ranging Macaca mulatta from a zone of hybridization in northeastern Thailand. Int. J. Primatol. 27, 497–513.Google Scholar
  25. Hoffmann, A.A., Sgrö, C.M., 2011. Climate change and evolutionary adaptation. Nature 470, 479–485.PubMedGoogle Scholar
  26. Kamarul, H., Ahmad, I., Badrul-Munir, M.Z., Syaizwan, Z., Aainaa, A., 2014. Ranging behavior of long-tailed macaques (Macaca fasciculans) at the entrance of Kuala Selangor Nature Park. Malays. Appl. Biol. 43, 129–142.Google Scholar
  27. Karimullah, A.S., 2012. The dominant species of monkeys (Macaca fasciculans) in northern region of Peninsular Malaysia. Pak. J. Zool. 44, 1567–1574.Google Scholar
  28. Koh, L.P., Wilcove, D.S., 2008. Is oil palm agriculture really destroying tropical biodiversity? Conserv. Lett. 1, 60–64.Google Scholar
  29. Laurance, W.F., Lovejoy, T.E., Vasconcelos, H.L., Bruna, E.M., Didham, R.K., Stouffer, P.C., Gascon, C., Bierregaard, R.O., Laurance, S.G., Sampaio, E., 2002. Ecosystem decay of Amazonian forest fragments: a 22-year investigation. Conserv. Biol. 16, 605–618.Google Scholar
  30. Linder, J.M., 2013. African primate diversity threatened by New Waveöf industrial oil palm expansion. Afr. Primates 8, 25–38.Google Scholar
  31. Linder, J.M., Palkovitz, R.E., 2016. The threat of industrial oil palm expansion to primates and their habitats. Ethnoprimatology, 21–45.Google Scholar
  32. Malaivijitnond, S., Hamada, Y., 2008. Current situation and status of long-tailed macaques (Macaca fasciculans) in Thailand. Nat. Hist. 8, 185–204.Google Scholar
  33. Marshall, A.J., 2010. Effect of habitat quality on primate populations in Kalimantan: gibbons and leaf monkeys as case studies. In: Indonesian Primates. Springer, New York, NY, pp. 157–177.Google Scholar
  34. Mohd, A., Yaman, A.R., Jamaludin, M.A., 1999. Recreational opportunities for public use in Ayer Hitam forest: setting the stage and park management approach. Pertanika J. Trop. Agric. Sci. 22, 161–166.Google Scholar
  35. Narasimmarajan, K., Raghunathan, C., 2012. Status of long-tailed macaque (Macaca fasciculans) and conservation of the recovery population in Great Nicobar Island, India. Wildl. Biol. Pract. 8, 1–8.Google Scholar
  36. Plumptre, A.J., Sterling, EJ., Buckland, S.T., 2013. Primate census and survey techniques. In: Sterling, E.J., Bynum, N., Blair, M.E. (Eds.), Primate Ecology and Conservation: A Handbook of Techniques. Oxford University Press, Oxford, pp. 10–26.Google Scholar
  37. Poirier, F.E., Smith, E.O., 1974. The crab-eating macaques (Macaca fasciculans) of Angaur Island, Palau, Indonesia. Folia Primatol. 22, 258–306.PubMedGoogle Scholar
  38. Richard, A.F., Goldstein, S.J., Dewar, R.E., 1989. Weed macaques: the evolutionary implications of macaque feeding ecology. Int. J. Primatol. 10, 569.Google Scholar
  39. Riley, CM., 2007. The human-macaque interface: conservation implications of current and future overlap and conflict in Lore Lindu National Park, Sulawesi, Indonesia. Am. Anthropol. 9, 473–484.Google Scholar
  40. Riley, E.P., Fuentes, A., 2011. Conserving social-ecological systems in Indonesia: human-nonhuman primate interconnections in Bali and Sulawesi. Am. J. Primatol. 73, 62–74.PubMedGoogle Scholar
  41. Riley, CM., Jayasri, S.L., Gumert, M.D., 2015. Results of a nationwide census of the long-tailed macaque (Macaca fasciculans) population of Singapore. Raffles Bull. Zool. 63, 503–515.Google Scholar
  42. Sha, J.C.M., Gumert, M.D., Lee, B.P.Y.H., Fuentes, A., Rajathurai, S., Chan, S., Jones-Engel, L., 2009. Status of long-tailed macaque Macaca fasciculans in Singapore and implications for management. Biodivers. Conserv. 18, 2909–2926.Google Scholar
  43. Sha, J.C.M., Hanya, G., 2013a. Temporal food resource correlates to the behavior and ecology of food-enhanced long-tailed macaque (Macaca fasciculans). Mammal Study 38, 163–175.Google Scholar
  44. Sha, J.C.M., Hanya, G., 2013b. Diet, activity, habitat use, and ranging of two neighboring groups of food-enhanced long-tailed macaques (Macaca fasciculans). Am. J. Primatol. 75, 581–592.Google Scholar
  45. Smart, S.M., Thompson, K., Marrs, R.H., Duc, M.G.L, Maskell, L.C., Firbank, L.G., 2006. Biotic homogenization and changes in species diversity across human-modified ecosystems. Proc. R. Soc. Lond., B., Biol. Sci. 273, 2659–2665.Google Scholar
  46. Southwick, C.H., Cadigan, F.C., 1972. Population studies of Malaysian primates. Primates 13, 1–18.Google Scholar
  47. Sussman, R.W., Tattersall, L., 1986. Distribution, abundance, and putative ecological strategy of Macaca fasciculans on the Island of Mauritius, Southwestern Indian Ocean. Folia Primatol. 46, 28–43.Google Scholar
  48. Swartz, K.B., 1983. Species discrimination in infant pig-tailed macques with pictorial stimuli. Dev. Psychobiol. 16, 219–231.PubMedGoogle Scholar
  49. Tabarelli, M., Peres, C.A., Melo, F.P.L, 2012. The’ few winners and many losers’ paradigm revisited: emerging prospects for tropical forest biodiversity. Biol. Conserv. 155, 136–140.Google Scholar
  50. Takasaki, H., 1981. Troop size, habitat quality, and home range area in Japanese macaques. Behav. Ecol. Sociobiol. 9, 277–281.Google Scholar
  51. Tee, S.L., Samantha, LD., Kamarudin, N., Akbar, Z., Lechner, A.M., Ashton-Butt, A., Azhar, B., 2018. Urban forest fragmentation impoverishes native mammalian biodiversity in the tropics. Ecol. Evol.,, in press.Google Scholar
  52. Thierry, B., Singh, M., Kaumanns, W., 2004. Macaque Societies: a Model for the Study of Social Organization. Cambridge University Press, Cambridge.Google Scholar
  53. Thomson, L.A.J., Thaman, R.R., Retrieved from 2006. Pometia pínnata (tava), ver 2.1. Species profiles for Pacific Island Agroforestry. Permanent Agriculture Resources (PAR), Hōlualoa, Hawai’i, on 12 May 2016 Scholar
  54. van Noordwijk, M.A., van Schaik, C.P., 1985v. Male migration and rank acquisition in wild long-tailed macaques (Macaca fasciculans). Anim. Behav. 33, 849–861.Google Scholar
  55. Wheatley, B.P., 1978. The Behavior and Ecology of the Crab Eating Macaque (Macaca fasciculans) in the Kutai Nature Reserve. University Microfilms International., East Kalimantan, Indonesia. London.Google Scholar
  56. Wilcove, D.S., Koh, L.P., 2010. Addressing the threats to biodiversity from oil palm agriculture. Biodivers. Conserv. 19, 999–1007.Google Scholar
  57. Yaap, B., Struebig, M.J., Paoli, G., Koh, L.P., 2010. Mitigating the biodiversity impacts of oil palm development. CAB Int. 5, 1–11.Google Scholar
  58. Yeager, C.P., 1996. Feeding ecology of the long-tailed macaque (Macaca fasciculans) in Kalimantan Tengah, Indonesia. Int. J. Primatol. 17, 51–62.Google Scholar

Copyright information

© Deutsche Gesellschaft für Säugetierkunde 2019

Authors and Affiliations

  • Sze Ling Tee
    • 1
  • Ahmad Solihhin
    • 1
  • Shahidin A. Juffiry
    • 1
  • Tengku Rinalfi Putra
    • 2
  • Alex M. Lechner
    • 3
  • Badrul Azhar
    • 1
    • 4
    Email author
  1. 1.Faculty of ForestryUniversiti Putra MalaysiaSerdang, SelangorMalaysia
  2. 2.Faculty of VeterinaryUniversiti Putra MalaysiaSerdang, SelangorMalaysia
  3. 3.School of Environmental and Geographical SciencesUniversity of Nottingham Malaysia CampusSemenyih, SelangorMalaysia
  4. 4.Biodiversity Unit, institute of BioscienceUniversiti Putra MalaysiaSerdang, SelangorMalaysia

Personalised recommendations