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Prevalence of gastrointestinal parasites in lion-tailed macaque Macaca silenus in central Western Ghats, India

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Abstract

This study examines gastrointestinal parasites in the endangered lion-tailed macaque, which is sympatric with the bonnet macaque that has relocated from nearby towns or agriculture landscapes dominated by humans and livestock. One hundred and ninety-four fresh fecal samples from lion-tailed macaques were collected from a group located at Chiksuli in the central Western Ghats. Of these, 48.5% had at least one endoparasite taxon. The prevalence of endoparasites varied from 0 to 75.0%, and observed endoparasite taxa varied between 0 and 10 across different months. The prevalence of endoparasites decreased with increasing rainfall and with increasing average maximum temperature across months. Of the 17 endoparasite taxa, 11 were nematodes, two were cestodes, and four were protozoans. The prevalence of Ascaris sp. and Entamoeba coli was higher than the other taxa. The overall load, helminth load, and protozoan load did not differ between months. The overall endoparasite load was greater in immature macaques in all seasons. Helminth load was higher in adult males, especially in the summer. Comparing our findings with those from sympatric relocated bonnet macaques of Chiksuli (Kumar et al. in PLoS ONE 13(11):e0207495, 2018) and lion-tailed macaques of Anamalai Hills (Hussain et al. in PLoS ONE 8(5):e63685, 2013) revealed: (a) a much higher prevalence of endoparasites in lion-tailed macaques from fragments of Anamalai Hills than in lion-tailed and bonnet macaques of Chiksuli; (b) higher richness of endoparasites in both macaque species of Chiksuli than in Anamalai lion-tailed macaques; and (c) more similar composition of endoparasite taxa between the Chiksuli lion-tailed and bonnet macaques than with the Anamalai Hills lion-tailed macaques. We suggest a complete cessation of relocation of commensal animals to the wild habitat. If relocation is necessary, then individuals to be relocated should be thoroughly screened and treated to prevent transferring endoparasite infections to wild populations.

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References

  • Altizer S, Nunn CL, Thrall PH, Gittleman JL, Antonovics J, Cunningham AA, Dobson AP, Ezenwa V, Jones KE, Pedersen AB, Poss M (2003) Social organization and parasite risk in mammals: integrating theory and empirical studies. Ann Rev Ecol Evol Syst 34:517–547

    Google Scholar 

  • Anderson RM, May RM (1978) Regulation and stability of host-parasite population interactions: I Regulatory processes. J Anim Ecol 41:219–247

    Google Scholar 

  • Arcari M, Baxendine A, Bennett CE (2000) Diagnosing medical parasites through coprological techniques. Online book: http://www.soton.ac.uk/~ceb/diagnosis/vol1.htm

  • Bapureddy G, Santhosh K, Jayakumar S, Kumara HN (2015) Estimate of primate density using distance sampling in the evergreen forests of the central Western Ghats, India. Curr Sci 108:118–123

    CAS  Google Scholar 

  • Baselga A, Orme D, Villeger S, De Bortoli J, Leprieur F, Baselga MA (2018) Package ‘betapart’

  • Benavides J, Huchard E, Pettorelli N, King AJ, Brown ME, Archer CE et al (2012) From parasite encounter to infection: multiple-scale drivers of parasite richness in a wild social primate. Am J Phys Anthropol 147:52–63

    PubMed  Google Scholar 

  • Bowman DD, Lynn RC, Georgi JR (1999) Georgis Parasitology for veterinarians. W.B. Saunders Company, Philadelphia

    Google Scholar 

  • Champion SH, Seth SK (1968) A revised survey of the forest types of India. A revised survey of the forest types of India

  • Chapman CA, Peres CA (2001) Primate conservation in the new millennium: the role of scientists. Evol Anthropol 10:16–33

    Google Scholar 

  • Chiodini PL, Moody AH, Mansar DW (2003) Atlas of medical helminthology and protozoology 4th Edition (DNP). Harcourt Publishers Limited, San Diego

    Google Scholar 

  • Collet J, Galdikas BMF, Sugarijito J, Jojosudharmo S (1986) A coprological study of parasitism in Orangutans (Pongo pygmaeus) Indonesia. J Med Primatol 15:121–129

    CAS  PubMed  Google Scholar 

  • Coop RL, Holmes PH (1996) Nutrition and parasite interaction. Int J Parasitol 26:951–962

    CAS  PubMed  Google Scholar 

  • Corbin I, Blackburn BJ, Wolowiec T, Novak M (1996) Metabolic profile of the liver of mice infected with cysticerci of Taenia crassiceps. Parasitol Res 82:273–275

    CAS  PubMed  Google Scholar 

  • Crawley MJ (1992) The population biology of predators, parasites and diseases. Blackwell, Hoboken

    Google Scholar 

  • Crompton DWT, Arnold SE, Walters DE, Whitfield PJ (1985) Food intake and body weight changes in mice infected with metacestodes of Taenia crassiceps. Parasitol 90:449–456

    Google Scholar 

  • Daszak P, Cunningham AA, Hyatt AD (2001) Anthropogenic environmental change and the emergence of infectious diseases in wildlife. Acta Trop 78:103–116

    CAS  PubMed  Google Scholar 

  • Despommier DD, Gwadz RW, Hotez PJ (1995) Aberrant nematode infections. In: Parasitic diseases. Springer, New York, pp. 61–70

    Google Scholar 

  • Dobson A, Foufopoulos J (2001) Emerging infectious pathogens of wildlife. Phil Trans R Soc Lond B Biol Sci 356:1001–1012

    CAS  Google Scholar 

  • Dobson AP, Hudson PJ (1992) Regulation and stability of a free-living host-parasite system: Trichostrongylus tenuis in red grouse. II. Population models. J Anim Ecol 61:487–498

    Google Scholar 

  • Ezenwa VO (2002) Behavioral and nutritional ecology of gastrointestinal parasitism in African bovids. Doctoral Dissertation. Princeton University, Princeton

    Google Scholar 

  • Gulland FMD (1992) The role of nematode parasites in Soay sheep (Ovis aries. L) mortality during a population crash. Parasitol 105:493–503

    Google Scholar 

  • Gulland FMD (1995) The impact of infectious diseases on wild animal populations: a review. In: Dobson AP, Grenfell BT (eds) Ecology of infectious diseases in natural populations. Cambridge University Press, UK, pp 20–51

    Google Scholar 

  • Hammer Ø, Harper DAT, Ryan PD (2001) PAST-Palaeontological statistics. www.uv.es/~ pardomv/pe/2001_1/past/pastprog/past.pdf. acessadoem, 25(07)- 2009

  • Holmes JC (1982) Impact of infectious disease agents on the population growth and geographical distribution of animals. In: Anderson RM, May RM (eds) Population biology of infectious diseases. Report of the Dahlem Workshop on Population Biology of Infectious Agents, March 14–19, 1982. Springer, Berlin, pp 37–52

    Google Scholar 

  • Holmes JC, Bethel WM (1972) Modification of intermediate host behavior by parasites. Zool. J. Linn. Soc. 51(Suppl. 1):123–149

    Google Scholar 

  • Horii Y, Imada I, Yanagida T, Usui M, Mori A (1982) Parasite changes and their influence on the body weight of Japanese monkeys (Macaca fuscata fuscata) of the Koshima troop. Primates 23:416–431

    Google Scholar 

  • Huerta L, Terrazas LI, Sciutto E, Larralde C (1992) Immunological mediation of gonadal effects on experimental murine cysticercosis caused by Taenia crassiceps Metacestodes. J Parasitol 78:471–476

    CAS  PubMed  Google Scholar 

  • Hussain S, Ram MS, Kumar A, Shivaji S, Umapathy G (2013) Human presence increasesparasitic load in endangered lion-tailed macaques (Macaca silenus) in its fragmented rainforest habitats in southern India. PLoS ONE 8(5):e63685

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jessee MT, Schilling PW, Stunkard JA (1970) Identification of intestinal helminth eggs in old world primates. Lab Anim Care 20:83–87

    CAS  PubMed  Google Scholar 

  • Kavaliers M, Colwell DD, Choleris E (1999) Parasites and behavior: an ethopharmacological analysis and biomedical implications. Neurosci Biobehav Rev 23:1037–1045

    CAS  PubMed  Google Scholar 

  • Klein SL (2004) Hormonal and immunological mechanisms mediating sex differences in parasite infection. Parasite Immunol 26:247–264

    CAS  PubMed  Google Scholar 

  • Krishna BA, Singh M, Singh M (2006) Population dynamics of a group of lion-tailed macaques (Macaca silenus) inhabiting a rainforest fragment in the Western Ghats, India. Folia Primatol 77:377–386

    CAS  PubMed  Google Scholar 

  • Kumar A (1987) The ecology and population dynamics of the lion-tailed macaque (Macaca silenus) in South India. Doctoral dissertation, University of Cambridge

  • Kumar A (1995) The life history, ecology, distribution, and conservation problems in the wild. In: Kumar A, Molur S, Walker S (eds) The lion-tailed macaque: population and habitat viability assessment workshop. Zoo Outreach Organization, Coimbatore

    Google Scholar 

  • Kumar MA, Singh M, Kumara HN, Sharma AK, Bertsch C (2001) Male migration in lion-tailed macaques. Prim Rep 51:5–18

    Google Scholar 

  • Kumar MA, Singh M, Srivastava S, Udhayan A, Kumara HN, Sharma AK (2002) Distribution and management of wild mammals in Indira Gandhi Wildlife Sanctuary, Tamil Nadu, India. J Bombay Nat Hist Soc 99:184–210

    Google Scholar 

  • Kumar S, Sundararaj P, Kumara HN, Pal A, Santhosh K, Vinoth S (2018) Prevalence of gastrointestinal parasites in bonnet macaque and possible consequences of their unmanaged relocations. PLoS ONE 13(11):e0207495

    PubMed  PubMed Central  Google Scholar 

  • Kumara HN (2011) Declaration of “Aghanashini lion-tailed macaque conservation reserve”. Zoo’s Print 26(7):5

    Google Scholar 

  • Kumara HN, Santhosh K (2013) Development of conservation strategy for a newly discovered lion-tailed macaque Macaca silenus population in Sirsi-Honnavara, Western ghats: II. Understanding the impact of NTFP collection on lion-tailed macaque. Technical report submitted to CEPF-ATREE Small Grants. SACON, Coimbatore

  • Kumara HN, Santhosh K (2014) Evaluating the status of NTFP trees and development of a model for sustainable harvest of Garcinia gummi-gutta in Aghanashini Lion-tailed Macaque Conservation Reserve, Western Ghats, India. SACON Technical Report-130, submitted to Rufford Small Grants, SACON, Coimbatore

  • Kumara HN, Singh M (2004a) Distribution and abundance of primates in rainforests of the Western Ghats, Karnataka, India and the conservation of Macaca silenus. Int J Primatol 25:1001–1018

    Google Scholar 

  • Kumara HN, Singh M (2004b) The influence of differing hunting practices on the relative abundance of mammals in two rainforest areas of the Western Ghats, India. Oryx 38:321–327

    Google Scholar 

  • Kumara HN, Sinha A (2009) Decline of the endangered lion-tailed macaque Macaca silenus in the Western Ghats, India. Oryx 43:292–298

    Google Scholar 

  • Kumara HN, Raj VM, Santhosh K (2008) Assessment of Critical Wildlife Habitat in Sirsi-Honnavara Forest Division, Karnataka: with special emphasis on estimation of lion-tailed macaque (Macaca silenus) population. Technical Report 1, Karnataka Forest Department, Sirsi, India

  • Kumara HN, Pritham NS, Santhosh K, Raj VM, Sinha A (2011) Decline of suitable habitats and conservation of the endangered lion-tailed macaque: land-cover change at a proposed protected area in Sirsi-Honnavara, Western Ghats, India. Curr Sci 101:434–439

    Google Scholar 

  • Kumara HN, Singh M, Sharma AK, Santhosh K, Pal A (2014) Impact of forest fragment size on between-group encounters in lion-tailed macaques. Primates 55:543–548

    PubMed  Google Scholar 

  • MAFF (1979) Parasitological Laboratory Techniques, Technical Bulletin No. 18. Ministry of Agriculture, Fisheries and Food Manual of Veterinary, Her Majesty’s Stationery Office Office, London

  • Müller-Graf CDM, Collins DA, Woolhouse MEJ (1996) Intestinal parasite burden in five troops of olive baboons (Papio cynocephalus anubis) in Gombe Stream National Park, Tanzania. Parasitology 112:489–497

    PubMed  Google Scholar 

  • Pascal JP (1988) Wet evergreen forests of the Western Ghats of India

  • Poulin R (1994) The evolution of parasite manipulation of host behaviour: a theoretical analysis. Parasitology 109:109–118

    Google Scholar 

  • Poulin R (2007a) Are there general laws in parasite ecology? Parasitology 134:763–776

    CAS  PubMed  Google Scholar 

  • Poulin R (2007b) The structure of parasite communities in fish hosts: ecology meets geography and climate. Parassitologia 49:169–172

    CAS  PubMed  Google Scholar 

  • Poulin R, Mouillot D (2004) The evolution of taxonomic diversity in helminth assemblages of mammalian hosts. Evol Ecol 18:31–247

    Google Scholar 

  • Poulin R, Krasnov BR, Mouillot D (2011) Host specificity in phylogenetic and geographic space. Trends Parasitol 27:355–361

    PubMed  Google Scholar 

  • Price PW (1990) Host populations as resources defining parasite community organization. Parasite communities: patterns and processes. Springer, Dordrecht, pp 21–40

    Google Scholar 

  • Ramachandran KK, Joseph GK (2000) Habitat utilization of Lion tailed macaque (Macaca silenus) in Silent Valley National park, Kerala, India. Prim Rep 58:17–26

    Google Scholar 

  • Rivera WL, Yason JAD, Adao DEV (2010) Entamoeba histolytica and Entamoebs dispar infections in captive macaques (Macaca fascicularis) in Philippines. Primates 51:69–74

    PubMed  Google Scholar 

  • Santhosh K, Raj VM, Kumara HN (2013) Conservation prospects for the lion-tailed macaque (Macaca silenus) in the forests of Sirsi-Honnavara, Western Ghats, India. Primate Conserv 27:125–131

    Google Scholar 

  • Santhosh K, Kumara HN, Velankar AD, Sinha A (2015) Ranging behavior and resource use by lion-tailed macaques (Macaca silenus) in selectively logged forests. Int J Primatol 36:288–310

    Google Scholar 

  • Schalk G, Forbes MR (1997) Male biases in parasitism of mammals: effects of study type, host age, and parasite taxon. Oikos 78:67–74

    Google Scholar 

  • Setchell JM, Bedjabaga IB, Goossens B, Reed P, Wickings EJ, Knapp LA (2007) Parasite prevalence, abundance, and diversity in a semi-free-ranging colony of Mandrillus sphinx. Int J Primatol 28:1345–1362

    Google Scholar 

  • Singh M, Singh M, Kumara HN, Kumar MA, D`Souza L (1997) Inter-and intra-specific associations of non-human primates in Anaimalai Hills, south India. Mammalia 61:17–28

    Google Scholar 

  • Singh M, Kumara HN, Kumar MA, Sharma AK (2001) Behavioral responses of lion-tailed macaque (Macaca silenus) to a changing habitat in a rain forest fragment in Western Ghats, India. Folia Primatol 72:278–291

    CAS  PubMed  Google Scholar 

  • Singh M, Singh M, Kumar MA, Kumara HN, Sharma AK, Kaumanns W (2002) Distribution, population structure, and conservation of lion-tailed macaques (Macaca silenus) in the Anaimalai Hills, Western Ghats, India. Am J Primatol 57:91–102

    PubMed  Google Scholar 

  • Singh M, Sharma AK, Krebs E, Kaumanns W (2006) Reproductive biology of lion-tailed macaque (Macaca silenus): an important key to the conservation of an endangered species. Curr Sci 90:804–811

    Google Scholar 

  • Singh M, Roy K, Singh M (2011) Resource partitioning in sympatric langurs and macaques in tropical rainforests of the central Western Ghats, South India. Am J Primatol 73:335–346

    PubMed  Google Scholar 

  • SPSS Inc. (2007) IBM SPSS statistics for Windows, version 16.0. IBM Corp, New York

    Google Scholar 

  • Sushma HS, Singh M (2006) Resource partitioning and interspecific interactions among sympatric rain forest arboreal mammals of the Western Ghats, India. Behav Ecol 17:479–490

    Google Scholar 

  • Taira N, Ando Y, Williams JC (2003) A color atlas of clinical helminthology of domestic animals: revised version. Elsevier, Amsterdam

    Google Scholar 

  • Thompson SN, Kavaliers M (1994) Physiological bases for parasite-induced alterations of host behaviour. Parasitology 109:119–138

    Google Scholar 

  • Tiwari S, Reddy DM, Pradheeps M, Sreenivasamurthy GS, Umapathy G (2017) Prevalence and co-occurrence of gastrointestinal parasites in Nilgiri Langur (Trachypithecus johnii) of fragmented landscape in Anamalai Hills, Western Ghats, India. Curr Sci 113:1194–2200

    Google Scholar 

  • Tompkins DM, Dobson AP, Arneber P, Begon M, Cattadori IM, Greenman JV, Heesterbeek JAP, Hudson PJ, Newborn D, Pugliese D, Rizzoli A, Rosa R, Rosso F, Wilson K (2001) Parasites and host population dynamics. In: Hudson PJ, Rizzoli A, Grenfell BT, Heesterbeek H, Dobson AP (eds) Wildlife diseases. Oxford University Press, London, pp 45–62

    Google Scholar 

  • Tompkins DM, Dunn AM, Smith MJ, Telfer S (2011) Wildlife diseases: from individuals to ecosystems. J Anim Ecol 80:19–38

    PubMed  Google Scholar 

  • Trejo-Macías G, Estrada A, Cabrera MÁM (2007) Survey of helminth parasites in populations of Alouatta palliata mexicana and A. pigra in continuous and in fragmented habitat in southern Mexico. Int J Primatol 28:31–945

    Google Scholar 

  • Umapathy G, Hussain S, Shivaji S (2011) Impact of habitat fragmentation on the demography of lion-tailed macaque (Macaca silenus) populations in the rainforests of Anamalai Hills, Western Ghats, India. Int J Primatol 32:889–900

    Google Scholar 

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Acknowledgments

We would like to thank B.K. Singh, PCCF(Wildlife), Karnataka state, for permissions and his constant support; Conservators of Forests, Vijay Mohan Raj, Manoj Kumar, Vasanth Reddy, and Yatish Kumar for their encouragement. This work was carried out with financial support from the Rufford Small Grants to Shanthala Kumar (Grant number: 16567-1, dated: 7 November 2014). We thank Dr. Michael Huffman, Kyoto University, and Prof. Hideo Hasegawa, Oita University, Japan, for their help in identification of endoparasites. We acknowledge the support of Gangadhar for help in the field; Mahender Reddy, J. Rubi, Giza Rachel George and A. Periyasamy for their support in the laboratory. We thank K. Gowri Dhatri and K. Samhitha for their help and cooperation during the entire study. We are also grateful to Dr. S. Babu for help in data analysis. The research complied with protocols approved by the appropriate Institutional Animal Care Committee. The study does not involve animal handling. The research adhered to the legal requirements of the country in which the research was conducted. All research protocols reported in this manuscript were reviewed and approved by an appropriate institutional and governmental agency that regulates research with animals. On behalf of all authors, the corresponding author states that there are no conflicts of interest to declare.

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  1. Nematology Unit, Department of Zoology, Bharathiar University, Coimbatore, Tamil Nadu, India

    Shanthala Kumar & Palanisamy Sundararaj

  2. Sálim Ali Centre for Ornithology and Natural History, Anikatty Post, Coimbatore, Tamil Nadu, India

    Honnavalli Nagaraj Kumara & Kumar Santhosh

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  1. Shanthala Kumar
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Kumar, S., Kumara, H.N., Santhosh, K. et al. Prevalence of gastrointestinal parasites in lion-tailed macaque Macaca silenus in central Western Ghats, India. Primates 60, 537–546 (2019). https://doi.org/10.1007/s10329-019-00751-y

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