The Gastrointestinal Parasites in Habituated Group of Sulawesi Black-crested Macaque (Macaca nigra) in Tangkoko, North Sulawesi

https://doi.org/10.22146/jtbb.73044

Sitti Aisyah May Wulandari(1), Dyah Perwitasari-Farajallah(2*), Erni Sulistiawati(3)

(1) Animal Biosciences Graduate Program, Department of Biology, Faculty of Mathematics and Natural Sciences, IPB University, Jl. Raya Dramaga, Bogor, West Java, 16680, Indonesia.
(2) Animal Biosciences Graduate Program, Department of Biology, Faculty of Mathematics and Natural Sciences, IPB University, Jl. Raya Dramaga, Bogor, West Java, 16680, Indonesia; Primate Research Center, IPB University, Jl. Lodaya II/5, Bogor, West Java, 16151, Indonesia.
(3) Vocational School Study Program, IPB University, Jl. Kumbang No 14, Bogor, West Java, 16153, Indonesia
(*) Corresponding Author

Abstract


The Sulawesi black-crested macaque (Macaca nigra) is an endemic primate of North Sulawesi that is categorized as critically endangered (IUCN 2015). Endoparasite contributes to the decline of M.nigra. Therefore, this study aims to determine the prevalence of endoparasites in the Sulawesi black-crested macaque (M. nigra). We collected 80 fresh fecal samples representing all sex from the two habituated groups. We analyzed them using the direct examination technique (0.9% NaCl, iodine, methylene blue) and flotation technique with the modified McMaster test. A total of 15 endoparasite taxa were recorded and 78 of 80 samples were infected with at least one or several endoparasite taxa. Around 93.75% (75/80) samples were positive for protozoa (Balantidium sp., Entamoeba sp., Giardia sp., and Isospora sp.) and 88.75% (71/80) samples were positive for helminths (Ancylostoma sp., Strongyloides sp., Haemonchus sp., Trichuris sp., Trichostrongylus sp., Ascarid sp., Diphyllobothrium sp., Echinococcus sp., Hymenolepis sp., Schistosoma japonicum and Schistosoma mekongi). The abundance of protozoa was higher than helminth, although the number of helminth taxon (11) was higher. The average temperature and monthly rainfall did not affect the number of endoparasites (EPG). The prevalence was higher in females than males due to different social styles; female crested macaques are more tolerant than males. The group with a larger number of individuals had a higher prevalence of endoparasites. These results confirm the presence and high diversity of gastrointestinal endoparasites in M. nigra, which can help to understand transmission dynamics and zoonotic potential, as well as to consider conservation policies.

 


Keywords


Endangered species; Endoparasite gastrointestinal; Macaca nigra; McMaster test; Sulawesi black-crested Macaque

Full Text:

PDF


References

Benavides, J.A. et al., 2012. From parasite encounter to infection: Multiple-scale drivers of parasite richness in a wild social primate population. Am J Phys, 147(1), pp.52–63. doi:10.1002/ajpa.21627.

Bicca-Marques, J.C., 2003. Sexual selection and the evolution of foraging behavior in male and female tamarins and marmosets: Sexual Selection and Reproductive Competition in Primates: New Perspectives and Directions. American Society of Primatologists, Norman. pp.455-475. doi: 10.1016/j.neubiorev.2014.10.001

Boundenga, L. et al., 2018. Diversity and prevalence of gastrointestinal parasites in two wild Galago species in Gabon. Infect Genet Evol, 63(4), pp.249–256. doi:10.1016/j.meegid.2018.04.035.

Chapman, C.A. et al., 2006. Do food availability, parasitism, and stress have synergistic effects on red colobus populations living in forest fragments. American journal of Physical Anthropology, 131, pp. 525-534. doi: 10.1002/ajpa.20477.

Chitwood, B.G., et al. 1950. An introduction to nematology. Baltimore, Md: Monumental Printing Company.

Cuomo, M., Noel L.B. & White, D.B., 2009. Diagnosing Medical Parasites: A Public Health Officers Guide to Assisting Laboratory and Medical Officers. Defense technical information center.

Dancey, C., Reidy, J. & Using S., 2004. Statistics Without Maths for Psychology for Windows. 4th ed. England: Pearson Education Limited.

Duboscq, J. et al., 2013. Social Tolerance in Wild Female Crested Macaques (Macaca nigra) in Tangkoko-Batuangus Nature Reserve, Sulawesi, Indonesia. Am J Primatol, 75(4), pp.361–375. doi:10.1002/ajp.22114.

Escobedo, G., Leon-Nava, M.D. & Morales-Montor, J., 2010. Sex Differences in Parasitic Infections : Beyond the Dogma of Female-Biased Resistance. Sex Horm Immun to Infect. pp:187–204. doi:10.1007/978-3-642-02155-8.

Finlay, B.J., Mary, Q. & Esteban, G., 2013. Freshwater protozoa : Biodiversity and ecological function Freshwater protozoa: biodiversity and ecological function. Biodivers Conserv, 7(9), pp. 1163–1186. doi:10.1023/A.

Ghai, R.R. et al., 2015. Sickness behaviour associated with non-lethal infections in wild primates. Proc R Soc B Biol Sci, 282(1814) pp.1-8. doi:10.1098/rspb.2015.1436.

Gillespie, T.R., 2006. Noninvasive Assessment of Gastrointestinal Parasite Infections in Free-Ranging Primates. Int J Primatology, 27(4), pp. 1129-1141. doi: 10.1007/s10764-006-9064-x.

Gillespie, T.R & Chapman, C.A., 2008. Forest fragmentation, the decline of an endangered primate, and changes in host-parasite interactions relative to an unfragmented forest. Am J Primatol, 70(3), pp. 222–230. doi:10.1002/ajp.20475.

Hasegawa, H. et al., 1992. Intestinal parasitic infections in Likupang, North Sulawesi, Indonesia. Southeast Asian J Trop Med Public Health, 23(2), pp. 219–227.

Hilser, H. et al., 2013. Sulawesi Crested Black Macaque Macaca nigra Species Action Plan: Draft 1. Selamatkan Yaki. Pacific Institute, Manado, Indonesia.

Huffman, M.A., 2013. Preliminary survey of the distribution of four potentially zoonotic parasite species among primates in Sri Lanka. J Natl Sci Found Sri Lanka, 41(4), pp. 319–326. doi:10.4038/jnsfsr.v41i4.6246.

Hurtado, R.R. et al., 2017. Primates adjust movement strategies due to changing food availability. Behavioral ecology, 29(2), pp. 369-376. doi: 10.1093/beheco/arx176.

IUCN, 2015. IUCN Red List of Threatened Species. Version 2011, viewed 23 October 2020, from http://www.iucnredlist.org

Joesoef, J.A. et al., 2018. Keragaman Endoparasit pada Macaca fascicularis dan Potensi Zoonotiknya dengan Cuaca Berbeda di Kota Kupang. J Vet, 19(36), pp.451–459. doi:10.19087/jveteriner.2018.19.4.451.

Jones-Engel, L. et al., 2004. Prevalence of enteric parasites in pet macaques in Sulawesi, Indonesia. Am J Primatol. 62(2), pp.1–82. doi:10.1002/ajp.20008.

Klaus, A. et al., 2017. International Journal for Parasitology: Parasites and Wildlife Co-infection patterns of intestinal parasites in arboreal primates proboscis monkeys (Nasalis larvatus) in Borneo. International Journal for Parasitology: Parasites and Wildlife, 6(3), pp. 320-329. doi:10.1016/j.ijppaw.2017.09.005.

Maneasa, E., Simandjuntak, S. & Semuel M.Y., 2021. Density of the crested black macaque (Macaca nigra) and habitat quality in Tangkoko, Bitung, North Sulawesi. Jurnal Biologi Tropis. 21(2), pp. 587-592. doi: 10.29303/jbt.v21i2.2789

McKenna, S.L. & Dohoo, I.R., 2006. Using and interpreting diagnostic tests. Vet Clin North Am Food Anim Pract, 22(1), pp.195-205. doi.org/10.1016/j.cvfa.2005.12.006

Melfi, V., 2010. Selamatkan Yaki! Conservation of Sulawesi Crested Black Macaques Macaca nigra. In: Gursky S., Supriatna J. (eds) Indonesian Primates. Developments in Primatology: Progress and Prospects. Springer, New York, NY.

Mul, I.F. et al., 2007. Intestinal parasites of free-ranging, semi-captive, and captive Pongo abelii in Sumatra, Indonesia. Int J Primatol, 28(2), pp.407–420.doi:10.1007/s10764-007-9119-7.

O’Brien, T.G. & Kinnaird, M.F., 1997. Behavior, diet, and movements of the Sulawesi crested black macaque (Macaca nigra). Int J Primatol, 18(3), pp.321–351. doi:10.1023/A:1026330332061.

Palacios, J.F.G. et al., 2012. Status of, and conservation recommendations for, the critically endangered crested black macaque Macaca nigra in Tangkoko, Indonesia. Oryx. 46(2), pp. 46: 290–297.doi: 10.1017/S0030605311000160.

Patterson, J.E.H. & Ruckstuhl, K.E., 2013. Parasite infection and host group size: A meta-analytical review. Parasitology, 140(7), pp.803–813. doi:10.1017/S0031182012002259.

R Core Team, 2018. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/.

Rismayanti, 2020. Intergroup Competition For Sleeping Sites And Their Function In Home Range And Group Defense In Crested Black Macaques (Macaca nigra). Institut Pertanian Bogor.

Saroyo, K.R., 2010. Pemetaan Distribusi dan Densitas Monyet Hitam Sulawesi (Macaca nigra) di Sulawesi Utara. Biosfera, 27(3), pp. 133-139. doi:10.20884/1.mib.2010.27.3.203.

Schuster, F.L. & Ramirez-avila, L., 2008. Current World Status of Balantidium coli. Clin Microbiol Rev, 21(4), pp.626–638. doi:10.1128/CMR.00021-08.

Sueur, C. et al., 2011. A comparative network analysis of social style in macaques. Anim Behav, 82(4), pp.845–852. doi:10.1016/j.anbehav.2011.07.020.

Thienpont, D., Rochette, F. & Vanparijs, O.F.J., 2003. Diagnosing Helminthiasis by Coprological Examination. 3rd ed. Beerse, Belgium: Janssen Animal Health.

Wenz-Mücke, A. et al., 2013. Human contact influences the foraging behaviour and parasite community in long-tailed macaques. Parasitology, 140(6), pp.709–718. doi:10.1017/S003118201200203X.

WHO, 2019. Bench Aids For the Diagnosis of Intestinal. 2nd ed. Geneva: World Health Organization.

Wolfe, N.D., Dunavan, C.P. & Diamond, J., 2007. Origins of major human infectious diseases. Nature, 447(7142), pp.279–283. doi:10.1038/nature05775.

Zajac, A. & Conboy, G., 2012. Veterinary Clinical Parasitology. 8th ed. USA: Wiley-blackwell.



DOI: https://doi.org/10.22146/jtbb.73044

Article Metrics

Abstract views : 439 | views : 201

Refbacks

  • There are currently no refbacks.


Copyright (c) 2022 Journal of Tropical Biodiversity and Biotechnology

Creative Commons License
This work is licensed under a Creative Commons Attribution-ShareAlike 4.0 International License.

Editoral address:

Faculty of Biology, UGM

Jl. Teknika Selatan, Sekip Utara, Yogyakarta, 55281, Indonesia

ISSN: 2540-9581 (online)