Diet Analysis of Sympatric Colobine Monkeys from Bako National Park, Sarawak, Borneo
Abstract
Habitat quality and abundant of food resources are among the key factors influencing the continued existence of primates in the wild. Although much has been studied on primate habitats and their diets, little is known about the nutritional value of the colobines’ foods. This study aimed to assess the dietary nutrient compositions of two sympatric colobine monkeys, Trachypithecus cristatus and Nasalis larvatus, in Bako National Park using proximate analysis of faecal, leaf and fruit samples of eight dominant tree species in Bako NP. Five nutrient parameters, namely crude protein, crude fat, crude fibre, ash, phosphorus, and energy content, were choosen to assess the nutritional demands of the monkeys in the wild. The faecal samples showed significantly higher percentage of crude fibre (27.58%) in N. larvatus compared to T. cristatus. In contrast, crude fat (8.52%), ash content (1.79%) and phosphorus (5.76 mg/g) were found to be significantly higher in the faecal samples of T. cristatus than in N. larvatus. The nutrient composition of leaves samples from the tree species consumed by N. larvatus and T. cristatus showed a significantly higher percentage of crude protein (14.56%) in Barringtonia asiatica (sea poison tree) and higher ash (13.70%) in Morinda citrifolia (Indian mulberry). Meanwhile, nutrient composition in fruit samples showed highest percentage of crude fibre (32.58%) and crude fat (12.35%) in Calophyllum inophyllum (Alexandrian laurel), whereas higher phosphorus (5.76%) and energy (24.26 KJ) were recorded in Ceriops tagal (Yellow mangrove). The higher crude fiber detected in N. larvatus’ faecal samples compared to T. cristatus may indicates that N. larvatus experiences lower digestibility as they are incapable of completely digesting the tough leaves or fruits. This study provides useful information for the conservation and management of these primate species especially on their dietary requirements in captivity or in a new habitat.
References
Albayrak, S.A., Turk, M., Yuksel, O. & Yilmaz, M. (2011). Forage yield and the quality of perennial legume grass mixtures under rainfed conditions. Notulae Botanicae Horti Agrobotanici Cluj-Napoca, 39(1): 114-118.
https://doi.org/10.15835/nbha3915853
AOAC (1980). Official methods of analysis. 11th edition. Washington DC. Association of Analytical Chemists. USA.
Ashton, P.S. (1971). The plants and vegetation of Bako National Park. Malayan Nature Journal, 24: 151-162.
Boaz, M. & Smetana, S. (1996). Regression equation predicts dietary phosphorus intake from estimate of dietary protein intake. Journal of the American Dietetic Association, 96(12): 1268-1270.
https://doi.org/10.1016/S0002-8223(96)00331-8
Brown, A.C. (2012). Anticancer activity of Morinda citrifolia (Noni) fruit: A review. Phytotherapy Research, 26(10): 1427-1440.
https://doi.org/10.1002/ptr.4595
Bukhori, M.F., Daud, R., Gintoron, C.S., Tingga, R. C.T. & Ghazali, R.I. (2018). Introduction to documentation of Nepenthes species in Bako National Park, Sarawak. Journal of Science and Mathematics Letters, 6: 1-9.
https://doi.org/10.37134/jsml.vol6.1.2018
Budeng, B. (2014). Behavioural activities and foraging ecology of proboscis monkey in Sarawak, Malaysia (Borneo). Final Report. PSGB: London.
Caton, J.M. (1999). Digestive strategy of the Asian colobine genus Trachypithecus. Primates, 40(2): 311-325.
https://doi.org/10.1007/BF02557555
Cetingul, I.S. & Yardimci, M. (2008). The importance of fats in farm animal nutrition. Kecatepe Veterinary Journal, 1: 77-81.
Chapman, C.A., Bicca-Marques, J.C., Dunham, A.E., Fan, P., Fashing, P.J., Gogarten, J.F., Guo, S., Huffman, M.A., Kalbitzer, U., Li, B., Ma, C., Matsuda, I., Omeja, P.A., Sarkar, D., Sengupta, R., Serio-Silva, J.C., Tsuji, Y. & Stenseth, N.C. (2020). Primates can be a rallying symbol to promote tropical forest restoration. Folia Primatalogica, 91: 669-687.
https://doi.org/10.1159/000505951
Chivers, D.D. (2001). Functional anatomy of the gastrointestinal tract. In Davies, A.G. & Oates, J.F. (Eds.) Colobine monkeys: Their ecology, behaviour and evolution. Cambridge: Cambridge University Press. Pp. 205-24.
Chunhieng, T., Hay, L. & Montet, D. (2004). Detailed study of the juice composition of noni (Morinda citrifolia) fruits from Cambodia. Fruits, 60: 13-24.
https://doi.org/10.1051/fruits:2005008
Clayton, J.B., Gomez, A., Amato, K., Knights, D., Travis, D.A., Blekhman, R., Knight, R., Leigh, S., Stumpf, R., Wolf, T., Glander, K.E., Cabana, F. & Johnson, T.J. (2018). The gut microbiome of nonhuman primates: Lessons in ecology and evolution. American Journal of Primatology, 80(6): 1-27.
https://doi.org/10.1002/ajp.22867
Davies, A.G., Bennet, E.L. & Waterman, P.G. (1988). Food selection by two South-east Asian colobine monkeys (Presbytis rubicunda and Presbytis melalophos) in relation to plant chemistry. Biological Journal of the Linnean Society, 34: 33-56.
https://doi.org/10.1111/j.1095-8312.1988.tb01947.x
Dzulhelmi, M.N. & Abdullah, M.T. (2009). An ethogram construction for the Malayan flying lemur (Galeopterus variegatus) in Bako National Park, Sarawak, Malaysia, Journal of Tropical Biology and Conservation, 5: 31-42.
Felton, A.M., Felton, A., Lindenmayer, D.B. & Foley, W.J. (2009). Nutritional goals of wild primates. Functional Ecology, 23: 70-78.
https://doi.org/10.1111/j.1365-2435.2008.01526.x
Haurez, B., Dainou, K., Tagg, N., Petre, C.A. & Doucet, J.L. (2015). The role of great apes inseed dispersal of the tropical forest tree species Dacryodes normandii (Burseraceae) in Gabon. Journal of Tropical Ecology, 31: 395-402.
https://doi.org/10.1017/S0266467415000322
Hazebroek, H.P. & Abang-Kassim, A.M. (2000). National Park of Sarawak. Kota Kinabalu: Natural History Publication (Borneo).
Hock, L.B. & Sasekumar, A. (1979). A preliminary study on the feeding biology of mangrove forest primates, Kuala Selangor. Malayan Nature Journal, 33: 105-112.
Kassim, N., Hambali, K. & Amir, A. (2017). Nutritional composition of fruits selected by long-tailed macaque (Macaca fascicularis) in Kuala Selangor, Malaysia, Tropical Life Sciences Research, 28(1): 91-101.
https://doi.org/10.21315/tlsr2017.28.1.6
Katagiri, S., Yamakura, T. & Lee, S.H. (1991). Properties of soils in kerangas forest on sandstone at Bako National Park, Sarawak, East Malaysia, Southeast Asian Studies, 29(1): 35-48.
Khan, F.A.A., Sazali, S.N., Kumaran, J.V., Aban, S., Zaini, K., Ketol, B., Ryan, J.R., Julaihi, A., Hall, L.S. & Abdullah, M.T. (2007). Bats of Bako National Park, Sarawak, Malaysian Borneo. The Sarawak Musuem Journal, 63(84): 267-300.
Kombi, M. & Abdullah, M.T. (2013). Ethogram of the free ranging Nasalis larvatus in Bako National Park, Sarawak. Malayan Nature Journal, 65: 1-21.
Kombi, M. & Abdullah, M.T. (2016). A review of the proboscis monkey (Nasalis larvatus) in Borneo, with reference to the population in Bako National Park, Sarawak, Malaysian, Borneo. Tropical Natural History, 16(1): 42-56.
Koo, B.S., Hwang, E.H., Kim, G., Oh, H., Son, Y., Lee, D., Lim, K.S., Kang, P., Lee, S., Lee, H.Y., Jeong, K.J., Lee, Y., Baek, S.H., Jeon, C.Y., Park, S.J., Kim, Y.H., Huh, J.W., Jin, Y.B., Kim, S.U., Lee, S.R. & Hong, J.J. (2019). Evaluation of fecal microbiomes associated with obesity in captive cynomolgus monkeys (Macaca fascicularis), Journal of Veterinary Science, 20(3): 1-12.
https://doi.org/10.4142/jvs.2019.20.e19
Laman, C.J.M., Aziz, M.F.I.A. & Abdullah, M.T. (2007). Ethological pattern of Silvered Leaf Langur (Presbytis cristata) at Bako National Park. Research Bulletin Faculty of Resource Science and Technology, 4: 4.
Lauper, M., Lechner, I., Barboza., P.S., Collins, W. B., Hummel, J., Codron, D. & Clauss, M. (2013). Rumination of different-sized particles in muskoxen (Ovibos moschatus) and moose (Alces alces) on grass and browse diets, and implications for rumination in different ruminant feeding types. Mammalian Biology, 78: 142-152.
https://doi.org/10.1016/j.mambio.2012.06.001
Legrand, J.J., Fisch, C., Guillaumat, P.O., Pavard, J.M., Attia, M., Jouffrey, S.D. & Claude, J.R. (2003). Use of biochemical markers to monitor changes in bone turnover in cynomolgus monkeys. Biomarkers, 8(1): 63-77.
https://doi.org/10.1080/1354750021000042448
Li, J., Karim, M.R., Li, D., Sumon, S.M.M.R., Siddiki, S.H.F. Rume, F.I., Sun, R., Jia, Y. & Zhang, L. (2019). Molecular characterization of Blastocystis sp. in captive wildlife in Bangladesh National Zoo: Non-human primates with high prevalence and zoonotic significance, International Journal for Parasitology: Parasites and Wildlife, 10: 314-320.
https://doi.org/10.1016/j.ijppaw.2019.11.003
Manjula, S.N., Ali, M. & Kenganora, M. (2016). Health benefits of Morinda citrifolia (noni): a review. Pharmacognosy Journal, 8(4): 321- 334.
https://doi.org/10.5530/pj.2016.4.4
Matsuda, I. (2008). Feeding and ranging behaviour of proboscis monkey Nasalis larvatus in Sabah, Malaysia. Retrieved from http://hdl.handle.net/2115/34633.
Matsuda, I., Murai, T., Clauss, M., Yamada, T., Tuuga, A., Bernard, H. & Higashi, S. (2011). Regurgitation and remastication in the foregut-fermenting proboscis monkey (Nasalis larvatus). Biology Letters, 7: 786-789.
https://doi.org/10.1098/rsbl.2011.0197
Matsuda, I., Tuuga, A., Bernard, H., Sugau, J. & Hanya, G. (2013). Leaf selection by two Bornean colobine monkeys in relation to plant chemistry and abundance. Scientific Reports, 3(1873): 1-6.
https://doi.org/10.1038/srep01873
Matsuda, I., Clauss, M., Tuuga, A., Sugau, A., Hanya, G., Yumoto, T., Bernard, H. & Hummel, J. (2017). Factors affecting leaf selection by foregut-fermenting proboscis monkey: new insight from in vitro digestibility and toughness of leaves. Scientific Report, 7(42774): 1-10.
https://doi.org/10.1038/srep42774
Matsuda, I., Bernard, H., Tuuga, A., Nathan, S.K.S. S., Sha, J.C.M., Osman, I., Sipangkui, R., Seino, S., Asano, S., Wong, A., Kreuzer, M., Saldivar, D. A. & Clauss, M. (2018). Fecal nutrients suggest diet of higher fiber levels in free-ranging than captive Proboscis Monkey (Nasalis larvatus). Frontiers in Veterinary Science, 4: 246.
https://doi.org/10.3389/fvets.2017.00246
Mazlan, N., Abd-Rahman, M.R., Tingga, R.C.T., Abdullah, M.T. & Khan, F.A.A. (2019). Population genetic analyses of endangerd proboscis monkey from Malaysian Borneo. Folia Primatologica, 90: 139-152.
https://doi.org/10.1159/000496022
McGrew, W.C., Marchant, L.F. & Philips, C.A. (2009). Standardised protocol for primate faecal analysis. Primates, 50: 363-366.
https://doi.org/10.1007/s10329-009-0148-z
Milton, K. (1993). Diet and primate evolution. Scientific American, 269: 86-93.
https://doi.org/10.1038/scientificamerican0893-86
Moges, E. & Balakrishnan, M. (2014). Nutritional composition of food plants of geladas (Theropithecus gelada) in Guassa community protected area, Ethiopia. Journal of Biology, Agriculture and Healthcare, 4(23): 38-44.
Mukhtar, Q.F., Alim, H. & Jadhav, B.L. (2017). In vitro evaluation of cytotoxic activity of fruit methanol extract of Ceriops tagal mangrove. International Research Journal of Pharmacy, 8(10): 157-159.
https://doi.org/10.7897/2230-8407.0810200
Naharuddin, N. M., Shazali, N., Libar, R., Karim, N. F., Mohd-Ridwan, A. R., Roslan, A., Azhar, M. I., Khalik, M. Z. & Khan, F. A. A. (2015). Bats of Bako National Park and additional notes on the rare partial albinism in fawn roundleaf bat (Hipposideridae: Hipposideros cervinus). Borneo Journal of Resource Science and Technology, 5(2): 44-52.
https://doi.org/10.33736/bjrst.221.2015
Nijboer, J. (2006). Fibre intake and faeces quality in leaf-eating primates. Retrieved from https://www.researchgate.net/profile/Joeke_Nijboer/publication/27692449_Fibre_inta-ke_and_faeces_quality_in_leafeating_primates/links/0deec537c7481e5e36000000/Fi-bre-intake-and-faeces-quality-in-leaf-eating-primates.pdf.
Nijman, V. & Meijaard, E. (2008). Trachypithecus cristatus. The IUCN Red List of Threatened Species. Retrieved from http://dx.doi.org/10.2305/IUCN.UK.2008.RLTS.T22035A9348474.en.
https://doi.org/10.2305/IUCN.UK.2008.RLTS.T22035A9348474.en
Nowak, R.M. (1999). Primates of the world. USA: Johns Hopkins University Press.
Parra, R. (1978). Comparison of foregut and hindgut fermentation in herbivores. In Montgomery, G.G. (Ed.) The ecology of arboreal folivores. Washington, DC: Smithsonian Institution Press. Pp. 205-230.
Phillipps, Q. & Phillipps, K. (2016). Phillipps' field guide to the mammals of Borneo and their ecology Sabah, Sarawak, Brunei and Kalimantan. Sabah, Malaysia: Natural History Publications (Borneo) Kota Kinabalu.
Power, M.L., Adams, J., Solonika, K., Colman, R.J., Ross, C. & Tardif, S.D. (2019). Diet, digestion and energy intake in captive common marmosets (Callithrix jacchus): research and management implications. Scientific Reports, 9(12134): 1-9.
https://doi.org/10.1038/s41598-019-48643-x
Qadri, N. & Jamil, K. (1993). Chemical constituents of the fruit and hypocotyl of mangrove, Ceriops tagal. Pakistan Journal of Marine Sciences, 2(2): 119-122.
Rose, C., Parker, A., Jefferson, B. & Cartmell, E. (2015). The characterisation of feces and urine: A review of the literature to inform advanced treatment technology. Enviromental Science and Technology, 45: 1827-1879.
https://doi.org/10.1080/10643389.2014.1000761
Strasser, E. & Delson, E. (1987). Cladistic analysis of cercopithecid relationship. Journal of Human Evolution, 16: 81-99.
https://doi.org/10.1016/0047-2484(87)90061-3
Wan-Azman, W.N.S., Mazlan, N., Wahab, M.F.A., Taib, A.A., Mali, S. & Khan, F.A.A. (2021). Silvered Langur (Trachypithecus cristatus) survey in Sibuti Wildlife Sanctuary, Miri, Sarawak. Journal of Tropical Biology and Conservation, 18: 243-250.
https://doi.org/10.51200/jtbc.v18i.3458
Waterman, P.G., Ross, J.A.M., Bennet, E.L. & Davies, A.G. (1988). A comparison of the floristics and leaf chemistry of the tree flora in two Malaysian rain forests and the influence of leaf chemistry on populations of colobine monkeys in the Old World. Biological Journal of the Linnean Society, 34: 1-32.
https://doi.org/10.1111/j.1095-8312.1988.tb01946.x
Wei-Hsien, L., Yen-Wenn, L., Zih-Fong, C., Wen-Fei, C., Ying-Chieh, T. & Chien- Chih, C. (2015). Calophyllolide content in Calophyllum inophyllum at different stages of maturity and its osteogenic activity. Molecules, 20: 12314-12327.
https://doi.org/10.3390/molecules200712314
Wiafe, E.D. (2015). Nutrient contents of three commonly consumed fruits of lowe's monkey (Cercopithecus campbelii lowei). SpringerPlus, 4(44): 1-5.
https://doi.org/10.1186/s40064-015-0814-0
World Health Organization. (2009). Medical plants in Papua New Guinea. Manila: Philippines.
Yeager, C.P., Silver, S.C. & Dierenfeld, E.S. (1997). Mineral and phytochemical influences on foliage selection by the proboscis monkey (Nasalis larvatus). American Journal of Primatology, 41(2): 117-128.
https://doi.org/10.1002/(SICI)1098-2345(1997)41:2<117::AID-AJP4>3.0.CO;2-#
Zahidin, M.A., Roslan, A., Marni, W., Kombi, M. & Abdullah, M.T. (2016). Biodiversity assessment and updated checklist of faunal diversity in Bako National Park, Sarawak, Malaysian Borneo. Journal of Sustainability Science and Management, 11(1): 53-72.
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