Open Access Open Access  Restricted Access Subscription Access

Prevalence of gastrointestinal parasites in the Nicobar long-tailed macaque (Macaca fascicularis umbrosus) on the Nicobar Group of Islands, India


Affiliations
1 Department of Zoology, Bharathiar University, Coimbatore 641 046, India
2 Sálim Ali Centre for Ornithology and Natural History, Anaikatty Post, Coimbatore 641 108, India
3 Sálim Ali Centre for Ornithology and Natural History, Anaikatty Post, Coimbatore 641 108, India; Manipal Academy of Higher Education, Manipal 576 104, India
4 Department of Zoology, Bharathiar University, Coimbatore 641 046, India; Sálim Ali Centre for Ornithology and Natural History, Anaikatty Post, Coimbatore 641 108, India
5 Biopsychology Laboratory and Institution of Excellence, University of Mysore, Mysuru 570 006, India
6 Sálim Ali Centre for Ornithology and Natural History, Anaikatty Post, Coimbatore 641 108,, India
 Untitled  

Changes in the habitat can drive the species to adapt to the changing environment that may lead to a risk of infection and the emergence of diseases. The prevalence of gastrointestinal parasites (henceforth endoparasites) in a species is an indicator of changing habitat conditions, and the study of the same is important when the species is restricted to a few islands. Macaca fascicularis umbrosus, endemic to Great Nicobar, Little Nicobar and Katchal islands. The December 2004 tsunami destroyed much of its habitat and pushed them to agriculture fields, leading to a conflict. To study the endoparasites in these macaques, we collected 160 faecal samples from five groups of macaques on Great Nicobar, one group on Little Nicobar, and two groups on Katchal between 2014 and 2016. The endo­parasite eggs and cysts were isolated from the faecal samples using flotation concentration and sedi­mentation techniques in the laboratory. The number and percent prevalence of endoparasites recorded in Great Nicobar, Little Nicobar and Katchal was 13, 5 and 3, and 69.38%, 60.00% and 39.39% respectively. The Campbell Bay group on Great Nicobar had 12, whereas other groups had 2–7 endoparasite taxa. The protozoan load was higher than the helminth load but the overall, helminth, and protozoan load did not differ between the islands. Ascaris sp., Oesophagostomum sp., Strongyloide ssp., Bunostomum sp. and Balantidium coli were the predominant endoparasites. The persistence of macaque with people probably has increased the richness and prevalence of endoparasites on Great Nicobar than in the other two islands.

Keywords

Changing habitat, faecal samples, gastrointestinal parasites, islands, long-tailed macaque.
User
Notifications
Font Size

  • Tiwari, S., Reddy, D. M., Pradheeps, M., Sreenivasamurthy, G. S. and Umapathy, G., Prevalence and co-occurrence of gastrointestinal parasites in Nilgiri langur (Trachypithecus johnii) of fragmented landscape in Anamalai Hills, Western Ghats, India. Curr. Sci., 2017, 113, 2194–2200.
  • Umapathy, G., Singh, M. and Mohnot, S. M., Status and distribution of Macaca fascicularis umbrosa in the Nicobar Islands, India. Int. J. Primatol., 2003, 24, 281–293.
  • Velankar, A. D., Kumara, H. N., Pal, A., Mishra, P. S. and Singh, M., Population recovery of Nicobar long-tailed macaque Macaca fascicularis umbrosus following a tsunami in the Nicobar Islands, India. PLoS ONE, 2016, 11, e0148205.
  • Fooden, J., Systematic review of Southeast Asian long-tailed macaques, Macaca fascicularis. Fieldiana Zool., New Ser., 1995, 81, 1– 206.
  • Carew-Reid, J., Conservation and protected areas in South Pacific islands. The importance of tradition. Environ. Conserv., 1990, 17, 29–38.
  • Nelleman, C., Miles, L., Kaltenborn, P., Virtue, M. and Alenius, H., The last stand of the orangutan – state of emergency: illegal logging, fire and palm oil in Indonesia’s National Parks. United Nations Environment Programme, Nairobi, with the Department for Environment, Food and Rural Affairs, the Great Ape Survival Project, and the United Nations Educational, Scientific and Cultural Organisation, 2007.
  • Molur, S. et al., The status of South Asian primates: Conservation Assessment and Management Plan (CAMP) Workshop Report, Zoo Outreach Organization, Coimbatore, 2003.
  • Eudey, A. A., The crab-eating macaque (Macaca fascicularis): widespread and rapidly declining. Primate Conserv., 2008, 23, 129–132.
  • Kumara, H. N., Kumar, A. and Singh, M., Macaca fascicularis ssp. umbrosa. The IUCN Red List of Threatened Species 2e.T39791A17985345, 2021; https://dx.doi.org/10.2305/IUCN. UK.2021-1.RLTS.T39791A17985345.en
  • Anon., Indian Wildlife Protection Act-1972, Ministry of Environment and Forests, Government of India, 1972.
  • Ramachandran, S. et al., Ecological impact of tsunami on Nicobar Islands (Camorta, Katchal, Nancowry and Trinkat). Curr. Sci., 2005, 89, 195–200.
  • Sivakumar, K., Impact of the tsunami (December 2004) on the long tailed macaque of Nicobar Islands, India. Hystrix – Ital. J. Mammal., 2010, 21, 35–42.
  • Mishra, P. S., Kumara, H. N., Thiyagesan, K., Singh, M., Velankar, A. D. and Pal, A., Chaos in coexistence: perceptions of farmers towards long-tailed macaques (Macaca fascicularis umbrosus) related to crop loss on Great Nicobar Island. Primate Conserv., 2020, 34, 175–183.
  • Pal. A., Kumara, H. N., Velankar, A. D., Mishra, P. S. and Singh, M., Extractive foraging and tool-aided behaviors in the wild Nicobar Long-tailed macaque (Macaca fascicularis umbrosus). Primates, 2018, 59, 173–183.
  • Pal, A., Kumara, H. N., Mishra, P. S., Velankar, A. D. and Singh, M., Between-group encounters in Nicobar long-tailed macaque (Macaca fascicularis umbrosus). Ethol. Ecol. Evol., 2018, 30, 582–599.
  • Pal, A., Kumara, H. N., Velankar, A. D., Mishra, P. S. and Singh, M., Demography and birth seasonality in the Nicobar long-tailed macaque (Macaca fascicularis umbrosus). Curr. Sci., 2018, 114, 1732–1737.
  • Foley, J. E., Swift, P., Fleer, K. A., Torres, S., Girard, Y. A. and Johnson, C. K., Risk factors for exposure to feline pathogens in California mountain lions (Puma concolor). J. Wildl. Dis., 2013, 49, 279–293.
  • Patz, J. A. et al., Unhealthy landscapes: policy recommendations on land use change and infectious disease emergence. Environ. Health Perspect., 2004, 112, 1092–1098.
  • Dobson, A. P. and May, R. M., Patterns of invasions by pathogens and parasites. In Ecology of Biological Invasions of North America and Hawaii, Springer, New York, USA, 1986, pp. 58–76.
  • Lyles, A. M. and Dobson, A. P., Infectious disease and intensive management: population dynamics, threatened hosts, and their parasites. J. Zoo Wildl. Med., 1993, 24, 315–326.
  • Laurenson, K., Sillero-Zubiri, C., Thompson, H., Shiferaw, F., Thirgood, S. and Malcolm, J., Disease as a threat to endangered species: Ethiopian wolves, domestic dogs and canine pathogens. In Animal Conservation Forum, Cambridge University Press, London, 1998, vol. 1(4), pp. 273–280.
  • Taraschewski, H., Hosts and parasites as aliens. J. Helminthol., 2006, 80, 99–128.
  • Kumar, S., Sundararaj, P., Kumara, H. N., Pal, A., Santhosh, K. and Vinoth, S., Prevalence of gastrointestinal parasites in bonnet macaque and possible consequences of their unmanaged relocations. PLoS ONE, 2018, 13(11), e0207495; https://doi.org/10.1371/journal.pone.0207495.
  • Hussain, S., Ram, M. S., Kumar, A., Shivaji, S. and Umapathy, G., Human presence increases parasitic load in endangered liontailed macaques (Macaca silenus) in its fragmented rainforest habitats in southern India. PLoS ONE, 2013, 8(5), e63685; doi:10.1371/journal.pone.0063685
  • Balakrishnan, N. P., Andaman Islands – vegetation and floristics. In Andaman, Nicobar and Lakshadweep. An Environmental Impact Assessment (ed. Saldanha, C. J.), Oxford and IBH, New Delhi, 1989, pp. 55–61.
  • Rao, N. V. S., Fauna of Andaman and Nicobar Islands: diversity, endemism, endangered species and conservation strategies. In Andaman, Nicobar and Lakshadweep. An Environmental Impact Assessment (ed. Saldanha, C. J.), Oxford and IBH, New Delhi, 1989, pp. 74–82.
  • Dryden, M. W., Payne, P. A., Ridley, R. and Smith, V., Comparison of common fecal flotation techniques for the recovery of parasite eggs and oocysts. Vet. Ther.: Res. Appl. Vet. Med., 2005, 6, 15–28.
  • Gillespie, T. R., Noninvasive assessment of gastrointestinal parasite infections in free-ranging primates. Int. J. Primatol., 2006, 27, 1129–1143.
  • Sloss, M. W., Kemp, R. L. and Zajac, A. M., Fecal examination: dogs and cats. In Veterinary Clinical Parasitology, Iowa State University Press, Ames, Iowa, USA, 1994, 6th edn.
  • Kumar, S., Kumara, H. N., Santhosh, K. and Sundararaj, P., Prevalence of gastrointestinal parasites in lion-tailed macaque Macaca silenus in central Western Ghats, India. Primates, 2019, 60, 537–546.
  • Jessee, M. T., Schilling, P. W. and Stunkard, J. A., Identification of intestinal helminth eggs in old world primates. Lab. Anim. Care, 1970, 20, 83–87.
  • Collet, J. Y., Galdikas, B. M., Sugarjito, J. and Jojosudharmo, S., A coprological study of parasitism in orangutans (Pongo pygmaeus) in Indonesia. J. Med. Primatol., 1986, 15, 121–129.
  • Bowman, D. D., Lynn, R. C. and Georgi, J. R., In Georgis’ Parasitology for Veterinarians, W.B. Saunders Company, Philadelphia, USA, 1999.
  • Arcari, M., Baxendine, A. and Bennett, C. E., Diagnosing Medical Parasites Through Coprological Techniques (online edn), 2000; http://www.soton.ac.uk/~ceb/diagnosis/vol1.htm
  • Chiodini, P. L., Moody, A. H. and Manser, D. W., Atlas of Medical Helminthology and Protozology, Churchill Livingstone Harcourt Publishers Limited, Edinburgh, UK, 2001, 4th edn (DNP).
  • Taira, N., Ando, Y. and Williams, J. C., A Color Atlas of Clinical Helminthology of Domestic Animals: Revised Version, Elsevier Science B.V., Amsterdam, The Netherlands, 2003.
  • SPSS Inc, IBM SPSS Statistics for Windows, Version 16.0. IBM Corp, New York, USA, 2007.
  • Wirawan, I. G. K. O., Kusumaningrum, D. and Oematan, A. B., Gastrointestinal endoparasites diversity of Macaca fascicularis in Goa Monyet Tenau Garden, Kupang. J. Sain Vet., 2015, 33, 94– 102.
  • Lane, K. E., Holley, C., Hollocher, H. and Fuentes, A., The anthropogenic environment lessens the intensity and prevalence of gastrointestinal parasites in Balinese long-tailed macaques (Macaca fascicularis). Primates, 2011, 52, 117–128.
  • Wenz-Muecke, A., Sithithaworn, P., Petney, T. N. and Taraschewski, H., Human contact influences the foraging behaviour and parasite community in long-tailed macaques. Parasitology, 2013, 140, 709–718.
  • Malaivijitnond, S., Chaiyabutr, N., Urasopon, N. and Hamada, Y., Intestinal nematode parasites of long-tailed macaques (Macaca fascicularis) inhabiting some tourist attraction sites in Thailand. In Proceedings of the 32nd Congress on Science and Technology of Thailand, Bangkok, Thailand, 2006, pp. 1–3.
  • Sricharern, W., Inpankaew, T., Keawmongkol, S., Supanam, J., Stich, R. W. and Jittapalapong, S., Molecular detection and prevalence of Giardia duodenalis and Cryptosporidium spp. among long-tailed macaques (Macaca fascicularis) in Thailand. Infect. Genet. Evol., 2016, 40, 310–314.
  • Vaisusuk, K. et al., Blastocystis subtypes detected in long-tailed macaques in Thailand – Further evidence of cryptic host specificity. Acta Trop., 2018, 184, 78–82.
  • Wilcox, J. J., Lane-Degraaf, K. E., Fuentes, A. and Hollocher, H., Comparative community-level associations of helminth infections and microparasite shedding in wild long-tailed macaques in Bali, Indonesia. Parasitology, 2015, 142, 480–489.
  • Son, V. D., Intestinal parasites of Macaca fascicularis in a mangrove forest, Ho Chi Minh City, Vietnam. Lab. Primate Newsl., 2002, 41, 4–5.
  • Janagi, T. S., Report on gastro-intestinal helminth parasites found in Macaca fascicularis in Peninsular Malaysia. Malays. Appl. Biol., 1981, 10, 99–100.
  • Matsubayashi, K. et al., Clinical examinations on crab-eating macaques in Mauritius. Primates, 1992, 33, 281–288.
  • Kurniawati, D. A., Suwanti, L. T., Retno, N. D., Kusdarto, S., Suprihati, E., Mufasirin, M. and Pratiwi, A., Zoonotic potential of gastrointestinal parasite in long-tailed macaque Macaca fascicularis at Baluran National Park, Situbondo, East Java, Indonesia. Aceh J. Anim. Sci., 2020, 5, 47–55.
  • Feng, M., Cai, J., Min, X., Fu, Y., Xu, Q., Tachibana, H. and Cheng, X., Prevalence and genetic diversity of Entamoeba species infecting macaques in southwest China. Parasitol. Res., 2013, 112, 1529–1536.
  • Feng, M. et al., High prevalence of Entamoeba infections in captive long-tailed macaques in China. Parasitol. Res., 2011, 109, 1093–1097.
  • Rivera, W. L., Yason, J. A. D. and Adao, D. E. V., Entamoeba histolytica and Entamoeba dispar infections in captive macaques (Macaca fascicularis) in Philippines. Primates, 2010, 51, 69–74.
  • Zanzani, S. A., Gazzonis, A. L., Epis, S. and Manfredi, M. T., Study of the gastrointestinal parasitic fauna of captive non-human primates (Macaca fascicularis). Parasitol. Res., 2016, 115, 307–312.
  • Li, M. et al., Prevalence of gastrointestinal parasites in captive non-human primates of twenty-four zoological gardens in China. J. Med. Primatol., 2015, 44, 168–173.
  • Bolette, D. P., Cui, L. and Rogers, M. B., Enterobius (Enterobius) shriveri n. sp. (nematoda: oxyuridae: enterobiinae) from Macaca fascicularis Raffles, 1821 (Primates: Cercopithecidae: Cercopithecinae) and three other cercopitheciid primate species: with additional information on Enterobius (Enterobius) macaci yen, 1973. Comp. Parasitol., 2016, 83, 54–74.
  • da Silva Barbosa, A. et al., Balantidium coli and other gastrointestinal parasites in captive non-human primates of the Rio de Janeiro, Brazil. J. Med. Primatol., 2015, 44, 18–26.
  • Lim, Y. A. L., Ngui, R., Shukri, J., Rohela, M. and Naim, H. M., Intestinal parasites in various animals at a zoo in Malaysia. Vet. Parasitol., 2008, 157, 154–159.
  • Lee, J. I. et al., Investigation of helminths and protozoans infecting old world monkeys: captive vervet, cynomolgus, and rhesus monkeys. Korean J. Vet. Res., 2010, 50, 273–277.
  • Casim, L. F., Bandal, M. Z., Gonzales Jr, J. C. B., Valdez, E. M. M., Chavez Jr, G. C. S. and Paller, V. G. V., Enteroparasites of captive long-tailed macaques (Macaca fascicularis) from National Wildlife Research and Rescue Center, Diliman, Quezon City, Philippines. Asian J. Conserv. Biol., 2015, 4, 54–61.
  • Johnson-Delaney, C. A., Parasites of captive nonhuman primates. Vet. Clin.: Exotic Anim. Practice, 2009, 12, 563–581.
  • Tachibana, H., Cheng, X. J., Kobayashi, S., Matsubayashi, N., Gotoh, S. and Matsubayashi, K., High prevalence of infection with Entamoeba dispar, but not E. histolytica, in captive macaques. Parasitol. Res., 2001, 87, 14–17.
  • Chavez, G. C. S., Paller, V. G., Lorica, R. P. and Dimalibot, J., Zoonotic enteroparasites of Macaca fascicularis in Palawan, Philippines, Research Square-Preprint, 2021.

Abstract Views: 197

PDF Views: 121 PDF Views: 83




  • Prevalence of gastrointestinal parasites in the Nicobar long-tailed macaque (Macaca fascicularis umbrosus) on the Nicobar Group of Islands, India

Abstract Views: 197  |  PDF Views: 121 PDF Views: 83

Authors

Shanthala Kumar
Department of Zoology, Bharathiar University, Coimbatore 641 046, India
Honnavalli N. Kumara
Sálim Ali Centre for Ornithology and Natural History, Anaikatty Post, Coimbatore 641 108, India
Avadhoot D. Velankar
Sálim Ali Centre for Ornithology and Natural History, Anaikatty Post, Coimbatore 641 108, India; Manipal Academy of Higher Education, Manipal 576 104, India
Partha Sarathi Mishra
Department of Zoology, Bharathiar University, Coimbatore 641 046, India; Sálim Ali Centre for Ornithology and Natural History, Anaikatty Post, Coimbatore 641 108, India
Arijit Pal
Sálim Ali Centre for Ornithology and Natural History, Anaikatty Post, Coimbatore 641 108, India; Manipal Academy of Higher Education, Manipal 576 104, India
P. Sundararaj
Department of Zoology, Bharathiar University, Coimbatore 641 046, India
Mewa Singh
Biopsychology Laboratory and Institution of Excellence, University of Mysore, Mysuru 570 006, India
S. Vinoth
Sálim Ali Centre for Ornithology and Natural History, Anaikatty Post, Coimbatore 641 108,, India

Abstract


Changes in the habitat can drive the species to adapt to the changing environment that may lead to a risk of infection and the emergence of diseases. The prevalence of gastrointestinal parasites (henceforth endoparasites) in a species is an indicator of changing habitat conditions, and the study of the same is important when the species is restricted to a few islands. Macaca fascicularis umbrosus, endemic to Great Nicobar, Little Nicobar and Katchal islands. The December 2004 tsunami destroyed much of its habitat and pushed them to agriculture fields, leading to a conflict. To study the endoparasites in these macaques, we collected 160 faecal samples from five groups of macaques on Great Nicobar, one group on Little Nicobar, and two groups on Katchal between 2014 and 2016. The endo­parasite eggs and cysts were isolated from the faecal samples using flotation concentration and sedi­mentation techniques in the laboratory. The number and percent prevalence of endoparasites recorded in Great Nicobar, Little Nicobar and Katchal was 13, 5 and 3, and 69.38%, 60.00% and 39.39% respectively. The Campbell Bay group on Great Nicobar had 12, whereas other groups had 2–7 endoparasite taxa. The protozoan load was higher than the helminth load but the overall, helminth, and protozoan load did not differ between the islands. Ascaris sp., Oesophagostomum sp., Strongyloide ssp., Bunostomum sp. and Balantidium coli were the predominant endoparasites. The persistence of macaque with people probably has increased the richness and prevalence of endoparasites on Great Nicobar than in the other two islands.

Keywords


Changing habitat, faecal samples, gastrointestinal parasites, islands, long-tailed macaque.

References





DOI: https://doi.org/10.18520/cs%2Fv122%2Fi10%2F1199-1208