GASTROINTESTINAL PARASITES IN Macaca fascicularis LIVING IN TWO URBAN AREAS OF MALAYSIA
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Abstract
Macaca fascicularis or commonly known as long-tailed macaques, are nonhuman primates that are increasingly vulnerable in becoming natural reservoirs for many microorganisms including gastrointestinal (GI) parasites, largely due to anthropogenic activities. This study was conducted to detect and compare GI parasites in M. fascicularis found in densely urbanized settings. The fecal samples of the long-tailed macaques were collected at a public university campus (Universiti Kebangsaan Malaysia, Bangi) and a tourist site (Bukit Melawati, Kuala Selangor). A total of 80 fecal samples were collected: 50 at the university campus, and the remaining samples from the tourist site. The fecal samples were processed by flotation techniques to include the GI parasites and then were subjected to morphological analysis to identify important taxonomy keys under microscopic magnification. A total of 139 parasites were identified from both locations and classified into 5 phylums and 17 families. Among the 139 parasites, 33 parasites were grouped into 6 genus of GI parasites. Among the gastrointestinal parasites that were identified from both study sites, three parasites were zoonotic namely Strongyloids spp., Trichostrongylus spp. and Trichuris spp. Results showed that the diversity index of GI parasites was higher at the university campus compared to the tourist site with Simpson’s Index values of 0.953 and 0.880, respectively, while the Shannon’s Index values were 3.282 and 2.399, respectively. This research revealed that there are more parasite infections in the long-tailed macaques in the campus surroundings compared to those found in the tourist site. Therefore, it is highly suggested that authority intervention by translocating the long-tailed macaques elsewhere is necessary to avoid prolonged contact and possible parasite transmission to humans, and if any parasitic infections occur, appropriate medication such as anthelmintic drugs should be readily available at the university campus clinics.
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Licensee MJS, Universiti Malaya, Malaysia. This article is an open-access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
References
Amato, K.R., Yeoman, C.J., Kent, A., Righini, N., Carbonero, F., Estrada, A., Gaskins, H.R., Stumpf, R.M., Leigh, S.R. (2013). Habitat Degradation Impacts Black Howler Monkey (Alouatta pigra) Gastrointestinal Microbiomes, International Society for Microbial Ecology 7: 1344-1353. DOI: https://doi.org/10.1038/ismej.2013.16
Anderson, R.C., Chabaud, A., & Willmott, S. (1974). CIH keys to the nematode parasites of vertebrates (No. QL 391. N4. C54). Commonwealth Institute of Helminthology.
Beisner, B.A., Balasubramaniam, K.N., Fernandez, K., Heagerty, A., Seil, S.K., McCowan, B., Sinha, R.P. (2016). Prevalence of Enteric Bacterial Parasites with Respect to Anthropogenic Factors Among Commensal Rhesus Macaques in Dehradun, India, Primates 57 (4): 459-469. DOI: 10.1007/s10329-016-0534-2
Bowman, D.D. (2003). Georgis' Parasitology for Veterinarians 8 th edition. WB Saunders Company.
Chapman, C.A., Bonnell, T.R., Gogarten, J.F., Schoof, V.A.M., Calme, S. (2005). Competing Pressures on Populations: Long-term Dynamics of Food Availability, Food Quality, Disease, Stress, and Animal Abundance, Phil. Trans. R. Soc. B 26: 370-382. DOI: https://doi.org/10.1098/rstb.2014.0112
Chapman, C.A., Peres, C.A. (2001). Primate Conservation in the New Millennium: The Role of Scientists, Evolutionary Anthropology 10:16–33.
Ekanayake, D.K., Arulkanthan, A., Horadagoda, N.U. et al. (2006). Prevalence of Cryptosporidium and Other Enteric Parasites Among Wild Non-human Primates in Polonnaruwa, Sri Lanka, Journal of Tropical Medicine and Hygiene 74: 322-331.
Engel, G., Jones-Engel, L. (2011). The Role of Macaca fascicularis in Infectious Disease Transmission. In Gumert, M.D., Fuentes, A. & Jones-Engel, L. (eds.). Monkeys on the Edge: Ecology and Management of Long-tailed Macaques and Their Interface with Humans, pp. 183–203. United Kingdom: Cambridge University Press, Cambridge.
Gillespie, T.R. (2006). Noninvasive Assessment of Gastrointestinal Parasite Infections in Free-ranging Primates, International Journal of Primatology 27 (4): 1129-1172.
Grant, E., Kyes, R.C., Kyes, P., Trinh, P., Ramirez, V., Tanee, T., Dangtakot, R. Pinlaor, P., Rabinowitz, P.M. (2019). Fecal Microbiota Dysbiosis in Macaques and Human within Shared Environment, Public Library of Science ONE 14 (5): 134-156.
Gumert, M.D., Kluck, M., Malaivijitnond, S. (2011). The Physical Characteristics and Usage Patterns of Stone Axe and Pounding Hammers Used by Long-tailed Macaques in the Andaman Sea Region of Thailand, American Journal of Primatology 71 (7): 594–608.
Hahn, N.E., Proulx, D., Muruthi, P.M., Alberts, S., Altmann, J. (2003). Gastrointestinal Parasites in Free-ranging Kenyan Baboons (Papio cynocephalus and P. anubis), International Journal of Primatology 24: 271-280.
Hambali, K., Ismail, A., Md-Zain, B.M., Amir, A., Karim, F. A. (2014). Diet of Long-tailed Macaques (Macaca fascicularis) at the Entrance of Kuala Selangor Nature Park (Anthropogenic Habitat): Food selection That Leads to Human-macaque Conflict, Acta Biologica Malaysiana 3 (2): 58–68.
Hechenbleikner, E.M., McQuade, J.A. (2015). Parasitic Colitis, Clinics in Colon and Rectal Surgery 28: 79-86.
Karuppannan, K., Saaban, S., Mustapam A.R., Zainal Abidin, F.A., Azimat, N.A., Keliang, C. (2014). Population Status of Long-tailed Macaque (Macaca fascicularis) in Peninsular Malaysia, Journal of Primatology 3 (1): 34-37.
Klaus, A., Strube, C., Roper, K.M., Radespiel, U., Schaarschmidt, F., Nathan, S., Goossens, B., Zimmermann, E. (2018). Fecal Parasite Risk in the Endangered Proboscis Monkey is Higher in an Anthropogenically Managed Forest Environment Compared to a Riparian Rain Forest in Sabah, Borneo, Public Library of Science ONE 13 (4): 110-122.
Lane, K.E., Holley, C., Hollocher, H., Fuentes, A. (2010). The Anthropogenic Environment Lessens the Intensity and Prevalence of Gastrointestinal Parasites in Balinese Long-tailed Macaques (Macaca fascicularis), Primates 52: 117-128.
Lavikainen, A. (2010). Human Medical View on Zoonotic Parasites, Acta Vet Scand 52 (1), 1-2.
Mafuyai, H.B., Barshep, Y., Audu, B.S., Kumbak, D., Ojobe, T.O. (2013). Baboons as Potential Reservoirs of Zoonotic Gastrointestinal Parasite Infections at Yankari National Park, Nigeria, African Health Sciences 13 (2): 252-254.
Md-Zain, B. M., Sha’ari, N. A., Mohd-Zaki, M., Ruslin, F., Idris, N. I., Kadderi, M. D., Idris, W. M. R. (2010). A Comprehensive Population Survey and Daily Activity Budget on Long-tailed Macaques of Universiti Kebangsaan Malaysia, Journal of Biological Science 10 (7): 608–615.
Md-Zain, B.M., Tarmizi, M.R., Mohd-Zaki, M. (2011). Campus Monkeys of Universiti Kebangsaan Malaysia: Nuisance Problems & Students Perception. In Gumert, M.D., Fuentes, A. & Jones-Engel, L. (eds.). Monkeys on The Edge: Ecology and Management of Long-Tailed Macaques and Their Interface with Humans, pp. 110–117. United Kingdom: Cambridge University Press, Cambridge.
Md-Zain, B.M., Ruslin, F., Idris, W.M.R. (2014). Human-macaque Conflicts at the Main Campus of Universiti Kebangsaan Malaysia, Pertanika Journal of Tropical Agricultural Science 37 (1): 73-85.
Mifsut, C.L. (2015). Helminths: Handbook for Identification and Counting of Parasitic Helminth Eggs in Urban Wastewater. Iwa Publishing.
Norazila Kassim, Kamarul Hambali, Aainaa Amir. (2017). Nutritional Composition of Fruits Selected by Long-Tailed Macaques (Macaca fascicularis) in Kuala Selangor, Malaysia. Tropical Life Sciences Research 28 (1): 91–101.
Nunn, C.L., Altizer, S.M. (2006). Infectious Diseases in Primates: Behavior, Ecology and Evolution. Oxford University Press, Oxford.
Pumipuntu, N. (2018). Detection for Potentially Zoonotic Gastrointestinal Parasites in Long-tailed Macaques, Dogs and Cattle at Kosamphi Forest Park, Maha Sarakham, Veterinary Integrative Sciences 16 (2): 69-77.
Raja, T.N., Hu, T.H., Zainudin, R., Lee, K.S., Perkins, S.L., Singh, B. (2018). Malaria Parasites of Long-tailed Macaques in Sarawak, Malaysian Borneo: A Novel Species and Demographic and Evolutionary Histories, BMC Evolutionary Biology 18 (1): 49.
Sha, J.C.M., Gumert, M.D., Benjamin, P.Y.H.L., Jones-Engel. L., Chan, S., Fuentes, A. (2009). Macaque-human Interactions and the Societal Perceptions of Macaques in Singapore, American Journal of. Primatology 71: 825–839.
Siregar, J.E., Faust, C.L., Murdiyarso, L.S., Rosmanah, L., Saepuloh, U., Dobson, A.P., Iskandriati, D. (2015). Non-invasive Surveillance for Plasmodium in Reservoir Macaque Species, Malaria Journal 14: 404-412.
Sricharern, W., Inpankaew, T., Keawmongkol, S., Supanam, J., Stich, R.W. & Jittapalapong, S. (2016). Molecular Detection and Prevalence of Giardia duodenalis and Cryptosporidium spp. Among Long-tailed Macaques (Macaca fascicularis) in Thailand, Infection, Genetics and Evolution 40: 310–314.
Trejo-Macias, G., Estrada, A. (2012). Risk Factors Connected to Gastrointestinal Parasites in Mantled Alouatta palliata mexicana and Black Howler Monkeys Alouatta pigra Living in Continuous and in Fragmented Rainforests in Mexico, Current Zoology 58 (3): 375-383.
Ukwubile, C.A., Bingari, M.S. (2018). Flatworms (Platyhelminthes) Associated with Slaughtered Cows in Abattoirs Found in Bali Town Taraba State Nigeria, International Journal of Research (6): 18-22.
Ungar, P.S. (1996). Feeding Height and Niche Separation in Sympatric Sumatran Monkeys and Apes, Folia Primatologica 6 (1): 163–168.
Valenta, K., Twinomugisha, D., Godfey, K., Liu, C., Schoof, V.A.M., Goldberg, T.L., Chapman, C.A. (2017). Comparison of Gastrointestinal Parasite Communities in Vervet Monkeys, Integrative Zoology 12 (6): 512-520.
Verweij, J.J., Vermeer, J., Brienen, E.A., Blotkamp, C., Laeijendecker, D., van Lieshout, L., Polderman, A.M. (2003). Entamoeba histolytica Infections in Captive Primates, Parasitology Research 90:100–103.
Viswanath, A., Williams, M. (2019). Trichuris trichiura (Whipworm, Roundworm). In: StatPearls [Internet]. Treasure Island (FL): StatPearls
Wallis, J. (2000). Prevention of Disease Transmission in Primate Conservation, Annals of the New York Academy of Sciences 916: 691-693.
Webber, A.D., Hill, C.M., Reynolds, V. (2007). Assessing the Failure of a Community-based Human-wildlife Conflict Mitigation Project in Budongo Forest Reserve, Uganda, Oryx 41: 117-125.
Wenz-Muecke, A., Sithithaworn, P., Petney, T.N., Taraschewski, H. (2013). Human Contact Influences the Foraging Behaviour and Parasite Community in lLong-tailed Macaques, Parasitology 140 (6): 709-719.
Wolfe, N.D., Tassey-Prosser, A., Carr, J.K., Tamoufe, U., Mpoudi-Ngole, E., Ndongo Torimiro, J., LeBreton, M., McCutchan, F.E., Birx, D.L., Burke, D.S. (2004). Exposure to Non-human Primates in Rural Cameroon, Emerging Infectious Diseases 10: 2094–2099.
Zanzani, S.A., Gazzonis, A.L., Epis, S., Manfredi, M.T. (2015). Study of the Gastrointestinal Parasitic Fauna of Captive Non-human Primates (Macaca fascicularis), Parasitology Research 6 (2):1.