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Preliminary Assessment of Gastrointestinal Parasites in Two Wild Groups of Endangered Moor Macaques (Macaca maura) from Sulawesi

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Abstract

Information on parasite biodiversity and abundance can improve our understanding of parasitic infections on endangered wildlife, as parasites can affect host survival and reproduction and may play a crucial role in determining population dynamics. We conducted a noninvasive assessment of gastrointestinal parasites in wild Macaca maura, an Endangered primate endemic to the Indonesian island of Sulawesi and examined the influence of season and sex on parasite richness and prevalence. We collected fecal samples (N = 72) from 18 individuals from two groups. We collected data from September 2014 to February 2015 and from June to November 2016, sampling each individual at least twice. We detected two taxa of nematodes (Trichuris sp. and Strongylida fam. gen.) and eight of protozoa (Giardia duodenalis, Chilomastix mesnili, Entamoeba hartmanni, Entamoeba polecki-like, Entamoeba coli, Iodamoeba bütschlii, Balantoides coli, and Blastocystis sp.). The gastrointestinal parasite richness (2.5 ± 0.4 SD) was below the mean reported for nonthreatened primates, whereas the mean prevalence of infection across all parasites (56.3%) was above the mean. We did not find any statistically significant difference in parasite richness or prevalence between seasons or the sexes. This preliminary assessment addresses the paucity of studies on parasites of wild primates in Southeast Asia and can contribute to our understanding of the newly emerging human–macaque interface at this site.

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References

  • Alamgir, M., Campbell, M. J., Sloan, S., Goosem, M., Clements, G. R., et al (2017). Economic, socio-political and environmental risks of road development in the tropics. Current Biology, 27(20), 1130–1140.

    Article  CAS  Google Scholar 

  • Albani, A. (2017). Ecology and habitat use of karst-forest dwelling Macaca maura, endemic endangered primate of South Sulawesi, Indonesia. Doctoral dissertation, Roma Tre University.

  • Altizer, S., Harvell, D., & Friedle, E. (2003). Rapid evolutionary dynamics and disease threats to biodiversity. Trends in Ecology & Evolution, 18(11), 589–596.

    Article  Google Scholar 

  • Altizer, S., Nunn, C. L., & Lindenfors, P. (2007). Do threatened hosts have fewer parasites? A comparative study in primates. Journal of Animal Ecology, 76(2), 304–314.

    Article  Google Scholar 

  • Anderson, R. M., & May, R. M. (1979). Population biology of infectious-diseases, Vol. 1. Nature, 280, 361–367.

    Article  CAS  PubMed  Google Scholar 

  • Anderson, R. M., & May, R. M. (1991). Infectious diseases of humans: Dynamics and control. Oxford: Oxford University Press.

    Google Scholar 

  • Bates, D., Maechler, M., Bolker, B., & Walker, S. (2014). lme4: Linear mixed-effects models using Eigen and S4. R package version 1.1–7, http://CRAN.R-project.org/package=lme4. Accessed July 25, 2019

  • Benavides, J. A., Huchard, E., Pettorelli, N., King, A. J., Brown, M. E., et al (2012). From parasite encounter to infection: Multiple-scale drivers of parasite richness in a wild social primate population. American Journal of Physical Anthropology, 147(1), 52–63.

    Article  PubMed  Google Scholar 

  • Bowman, D. D. (2014). Georgis’ parasitology for veterinarians. e-book. Philadelphia: Elsevier Health Sciences.

    Google Scholar 

  • Brito, D., Moreira, D. O., Coutinho, B. R., & Oprea, S. M. (2012). Ill nature: Disease hotspots as threats to biodiversity. Journal for Nature Conservation, 20(2), 72–75.

    Article  Google Scholar 

  • Busaeri, S. R., Salman, D., & Yusran (2015). Household livelihood strategies in Bantimurung Bulusaraung National Park, Maros District, South Sulawesi Province, Indonesia. International Journal of Humanities and Social Science, 5(1), 278–283.

    Google Scholar 

  • Chapman, C. A., Gillespie, T. R., & Goldberg, T. L. (2005). Primates and the ecology of their infectious diseases: How will anthropogenic change affect host-parasite interactions? Evolutionary Anthropology: Issues, News, and Reviews, 14(4), 134–144.

    Article  Google Scholar 

  • Chapman, C. A., Hodder, S. A. M., & Rothman, J. M. (2009a). Host-parasite dynamics: Connecting primate field data to theory. In M. A. Huffman & C. A. Chapman (Eds.), Primate parasite ecology: The dynamics and study of host-parasite relationships (pp. 463–483). Cambridge: Cambridge University Press.

    Google Scholar 

  • Chapman, C. A., Rothman, J. M., & Hodder, S. A. M. (2009b). Can parasite infections be a selective force influencing primate group size? A test with red colobus. In M. A. Huffman & C. A. Chapman (Eds.), Primate parasite ecology: The dynamics and study of host–parasite relationships (pp. 371–385). Cambridge: Cambridge University Press.

    Google Scholar 

  • Cleaveland, S., Hess, G. R., Dobson, A. P., Laurenson, M. K., & McCallum, H. I. (2002). The role of pathogens in biological conservation. In P. J. Hudson, A. Rizzoli, B. T. Grenfell, H. Heesterbeek, & A. P. Dobson (Eds.), The ecology of wildlife diseases (pp. 139–150). New York: Oxford University Press.

    Google Scholar 

  • Clough, D., Heistermann, M., & Kappeler, P. M. (2010). Host intrinsic determinants and potential consequences of parasite infection in free-ranging red-fronted lemurs (Eulemur fulvus rufus). American Journal of Physical Anthropology, 142(3), 441–452.

    Article  PubMed  Google Scholar 

  • Cross, P. C., Drewe, J., Patrek, V., Pearce, G., Samuel, M. D., & Delahay, R. J. (2009). Wildlife population structure and parasite transmission: Implications for disease management. In R. J. Delahay, G. C. Smith, & M. R. Hutchings (Eds.), Management of disease in wild mammals (Vol. 62, pp. 9–29). New York: Springer Science+Business Media.

    Chapter  Google Scholar 

  • Daszak, P., Cunningham, A. A., & Hyatt, A. D. (2000). Emerging infectious diseases of wildlife: Threats to biodiversity and human health. Science, 287(5452), 443–449.

    Article  CAS  PubMed  Google Scholar 

  • Debenham, J. J., Tysnes, K., Khunger, S., & Robertson, L. J. (2017). Occurrence of Giardia, Cryptosporidium, and Entamoeba in wild rhesus macaques (Macaca mulatta) living in urban and semi-rural North-West India. International Journal for Parasitology: Parasites and Wildlife, 6(1), 29–34.

    PubMed  PubMed Central  Google Scholar 

  • Ekanayake, D. K., Arulkanthan, A., Horadagoda, N. U., Sanjeevani, G. M., Kieft, R., et al (2006). Prevalence of Cryptosporidium and other enteric parasites among wild non-human primates in Polonnaruwa, Sri Lanka. American Journal of Tropical Medicine and Hygiene, 74(2), 322–329.

    Article  Google Scholar 

  • Fedorko, D. P., Williams, E. C., Nelson, N. A., Mazyck, T. D., Hanson, K. L., & Cartwright, C. P. (2000). Performance of Para-Pak™ Ultra ECOFIX™ compared with Para-Pak™ Ultra formalin/mercuric chloride-based polyvinyl alcohol for concentration and permanent stained smears of stool parasites. Diagnostic Microbiology and Infectious Disease, 37(1), 37–39.

    Article  CAS  PubMed  Google Scholar 

  • Feng, M., Yang, B., Yang, L., Fu, Y., Zhuang, Y., et al (2011). High prevalence of Entamoeba infections in captive long-tailed macaques in China. Parasitology Research, 109(4), 1093.

    Article  PubMed  Google Scholar 

  • Gelman, A., & Hill, J. (2007). Data analysis using regression and hierarchical/multilevel models. New York: Cambridge University Press.

    Google Scholar 

  • Gillespie, T. R. (2006). Noninvasive assessment of gastrointestinal parasite infections in free-ranging primates. International Journal of Primatology, 27(4), 1129–1143.

    Article  Google Scholar 

  • 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. American Journal of Primatology, 70(3), 222–230.

    Article  PubMed  Google Scholar 

  • Gillespie, T. R., Chapman, C. A., & Greiner, E. C. (2005). Effects of logging on gastrointestinal parasite infections and infection risk in African primates. Journal of Applied Ecology, 42(4), 699–707.

    Article  Google Scholar 

  • Gillespie, T. R., Greiner, E. C., & Chapman, C. A. (2004). Gastrointestinal parasites of the guenons of western Uganda. Journal of Parasitology, 90(6), 1356–1361.

    Article  Google Scholar 

  • Gillespie, T. R., Lonsdorf, E. V., Canfield, E. P., Meyer, D. J., Nadler, Y., et al (2010). Demographic and ecological effects on patterns of parasitism in eastern chimpanzees (Pan troglodytes schweinfurthii) in Gombe National Park, Tanzania. American Journal of Physical Anthropology, 143(4), 534–544. https://doi.org/10.1002/ajpa.21348.

    Article  PubMed  PubMed Central  Google Scholar 

  • Gotoh, S., Takenaka, O., Watanabe, K., Hamada, Y., Kawamoto, Y., et al (2001). Hematological values and parasite fauna in free-ranging Macaca hecki and the M. hecki/M. tonkeana hybrid group of Sulawesi Island, Indonesia. Primates, 42(1), 27–34.

    Article  Google Scholar 

  • Hasegawa, H., Chapman, C. A., & Huffman, M. A. (2009). Useful diagnostic references and images of protozoans, helminths, and nematodes commonly found in wild primates. In M. A. Huffman & C. A. Chapman (Eds.), Primate parasite ecology: The dynamics and study of host-parasite relationships (pp. 507–514). Cambridge: Cambridge University Press.

    Google Scholar 

  • Hasegawa, H., Miyagi, I., Toma, T., Kamimura, K., Nainggolan, I. J., et al (1992). Intestinal parasitic infections in Likupang, North Sulawesi, Indonesia. Southeast Asian Journal of Tropical Medicine and Public Health, 23(2), 219–227.

    CAS  Google Scholar 

  • Hilser, H., Smith, Y. C. E., & Smith, D. A. E. (2014). Apparent mortality as a result of an elevated parasite infection in Presbytis rubicunda. Folia Primatologica, 85(5), 265–276.

    Article  Google Scholar 

  • Hopkins, M. E., & Nunn, C. L. (2007). A global gap analysis of infectious agents in wild primates. Diversity and Distributions, 13(5), 561–572.

    Article  Google Scholar 

  • Hudson, P. (2005). Parasites, diversity, and the ecosystem. In F. Thomas, F. Renaud, & J. F. Guéan (Eds.), Parasitism and ecosystems (pp. 1–12). New York: Oxford University Press.

    Google Scholar 

  • Hudson, P. J., Dobson, A. P., & Lafferty, K. D. (2006). Is a healthy ecosystem one that is rich in parasites? Trends in Ecology & Evolution, 21, 381–385.

    Article  Google Scholar 

  • Hudson, P. J., Dobson, A. P., & Newborn, D. (1998). Prevention of population cycles by parasite removal. Science, 282(5397), 2256–2258.

    Article  CAS  PubMed  Google Scholar 

  • Huffman, M. A., Nahallage, C. A. D., Hasegawa, H., Ekanayake, S., De Silva, L. G. D. D., & Athauda, I. R. K. (2013). Preliminary survey of the distribution of four potentially zoonotic parasite species among primates in Sri Lanka. Journal of the National Science Foundation of Sri Lanka, 41(4), 319–326. https://doi.org/10.4038/jnsfsr.v41i4.6246.

    Article  Google Scholar 

  • Huffman, M. A., Gotoh, S., Turner, L. A., Hamai, M., & Yoshida, K. (1997). Seasonal trends in intestinal nematode infection and medicinal plant use among chimpanzees in the Mahale Mountains, Tanzania. Primates, 38(2), 111–125. https://doi.org/10.1007/bf02382002.

    Article  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • IUCN. (2017) The IUCN Red List of Threatened Species. Version 2017-1. www.iucnredlist.org. Accessed December 24, 2017.

  • Jessee, M. T., Schilling, P. W., & Stunkard, J. A. (1970). Identification of intestinal helminth eggs in old world primates. Laboratory Animal Care, 20(1), 83–87.

  • Jones-Engel, L., Engel, G. A., Schillaci, M. A., Froehlich, J., Paputungan, U., & Kyes, R. C. (2004). Prevalence of enteric parasites in pet macaques in Sulawesi, Indonesia. American Journal of Primatology, 62(2), 71–82.

    Article  PubMed  Google Scholar 

  • Kamilar, J. M., & Pokempner, A. A. (2008). Does body mass dimorphism increase male-female dietary niche separation? A comparative study of primates. Behaviour, 1211–1234.

  • Key, C., & Ross, C. (1999). Sex differences in energy expenditure in non-human primates. Proceedings of the Royal Society of London B: Biological Sciences, 266(1437), 2479–2485.

    Article  CAS  Google Scholar 

  • Klaus, A., Zimmermann, E., Röper, K. M., Radespiel, U., Nathan, S., et al (2017). Co-infection patterns of intestinal parasites in arboreal primates (proboscis monkeys, Nasalis larvatus) in Borneo. International Journal for Parasitology: Parasites and Wildlife, 6(3), 320–329.

    PubMed  PubMed Central  Google Scholar 

  • Knezevich, M. (1998). Geophagy as a therapeutic mediator of endoparasitism in a free-ranging group of rhesus macaques (Macaca mulatta). American Journal of Primatology, 44(1), 71–82.

    Article  CAS  PubMed  Google Scholar 

  • Kouassi, R. Y. W., McGraw, S. W., Yao, P. K., Abou-Bacar, A., Brunet, J., et al (2015). Diversity and prevalence of gastrointestinal parasites in seven non-human primates of the Taï National Park, Côte d'Ivoire. Parasite, 22, 1.

    Article  PubMed  PubMed Central  Google Scholar 

  • Lane, K. E., Holley, C., Hollocher, H., & Fuentes, A. (2011). The anthropogenic environment lessens the intensity and prevalence of gastrointestinal parasites in Balinese long-tailed macaques (Macaca fascicularis). Primates, 52(2), 117–128.

    Article  PubMed  Google Scholar 

  • Lane, K. E., Lute, M., Rompis, A., Wandia, I. N., Putra, I. A., et al (2010). Pests, pestilence, and people: The long-tailed macaque and its role in the cultural complexities of Bali. In S. Gursky & J. Supriatna (Eds.), Indonesian primates, Developments in Primatology: Progress and Prospects (pp. 235–248). New York: Springer Science+Business Media.

    Chapter  Google Scholar 

  • Lazdane, K., Broll, A., Theisinger, O., Bearder, S. K., & Donati, G. (2014). A preliminary assessment of nematode infections in Eulemur collaris (Geoffroy, 1812) (Mammalia: Lemuridae) in remnant fragments of Malagasy littoral forest. Italian Journal of Zoology, 81(3), 374–380.

    Article  Google Scholar 

  • Lloyd-Smith, J. O., Schreiber, S. J., Kopp, P. E., & Getz, W. M. (2005). Superspreading and the effect of individual variation on disease emergence. Nature, 438(7066), 355.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lyles, A., & Dobson, A. (1993). Infectious disease and intensive management: Population dynamics, threatened hosts, and their parasites. Journal of Zoo and Wildlife Medicine, 24(3), 315–326.

    Google Scholar 

  • Mangali, A., Sasabone, P., Abadi, K., Hasegawa, H., Toma, T., et al (1993). Intestinal parasitic infections in Campalagian district, south Sulawesi, Indonesia. Southeast Asian Journal of Tropical Medicine and Public Health, 24(2), 313–320.

    CAS  Google Scholar 

  • Marcogliese, D. J. (2004). Parasites: Small players with crucial roles in the ecological theater. EcoHealth, 1, 151–164.

    Article  Google Scholar 

  • Marcogliese, D. J. (2005). Parasites of the superorganism: Are they indicators of ecosystem health? International Journal for Parasitology, 35, 705–716.

    Article  PubMed  Google Scholar 

  • McCallum, H. (2008). Landscape structure, disturbance and disease dynamics. In R. S. Ostfeld, F. Keesing, & V. Eviner (Eds.), Infectious disease ecology: Effects of ecosystems on disease and of disease on ecosystems (pp. 100–124). Princeton, NJ: Princeton University Press.

    Google Scholar 

  • McCallum, H., & Dobson, A. (2002). Disease, habitat fragmentation and conservation. Proceedings of the Royal Society of London B: Biological Sciences, 269(1504), 2041–2049.

    Article  Google Scholar 

  • McClure, H. M., Strobert, E. A., & Healy, G. R. (1980). Blastocystis hominis in a pig-tailed macaque: A potential enteric pathogen for nonhuman primates. Laboratory Animal Science, 30(5), 890–894.

    CAS  PubMed  Google Scholar 

  • Moore, S. L., & Wilson, K. (2002). Parasites as a viability cost of sexual selection in natural populations of mammals. Science, 297(5589), 2015–2018.

    Article  CAS  PubMed  Google Scholar 

  • Mul, I. F., Paembonan, W., Singleton, I., Wich, S. A., & van Bolhuis, H. G. (2007). Intestinal parasites of free-ranging, semicaptive, and captive Pongo abelii in Sumatra, Indonesia. International Journal of Primatology, 28(2), 407–420.

    Article  Google Scholar 

  • Müller-Graf, C. D. M., Collins, D. A., & Woolhouse, M. E. J. (1996). Intestinal parasite burden in five troops of olive baboons (Papio cynocephalus anubis) in Gombe Stream National Park, Tanzania. Parasitology, 112(5), 489–497.

    Article  PubMed  Google Scholar 

  • Murray, D. L., Keith, L. B., & Cary, J. R. (1998). Do parasitism and nutritional status interact to affect production in snowshoe hares? Ecology, 79, 1209–1222.

    Article  Google Scholar 

  • Nunn, C. L., & Altizer, S. (2006). Infectious diseases in primates: Behavior, ecology and evolution. Oxford: Oxford University Press.

    Book  Google Scholar 

  • Nunn, C. L., Altizer, S., Jones, K. E., & Sechrest, W. (2003). Comparative tests of parasite species richness in primates. American Naturalist, 162(5), 597–614.

    Article  Google Scholar 

  • Nunn, C. L., & Dokey, A. T. W. (2006). Ranging patterns and parasitism in primates. Biology Letters, 2, 351–354.

    Article  PubMed  PubMed Central  Google Scholar 

  • Patz, J. A., Graczyk, T. K., Geller, N., & Vittor, A. Y. (2000). Effects of environmental change on emerging parasitic diseases. International Journal of Parasitology, 30, 1395–1405.

    Article  CAS  PubMed  Google Scholar 

  • Poirotte, C., Basset, D., Willaume, E., Makaba, F., Kappeler, P. M., & Charpentier, M. J. (2016). Environmental and individual determinants of parasite richness across seasons in a free-ranging population of Mandrills (Mandrillus sphinx). American Journal of Physical Anthropology, 159(3), 442–456.

    Article  PubMed  Google Scholar 

  • Pomajbíková, K., Oborník, M., Horák, A., Petrželková, K. J., Grim, J. N., et al (2013). Novel insights into the genetic diversity of Balantidium and Balantidium-like cyst-forming ciliates. PLoS Neglected Tropical Diseases, 7(3), e2140.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Core Team, R. (2019). R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing https://www.R-project.org/.

    Google Scholar 

  • Rivera, W. L., & Kanbara, H. (1999). Detection of Entamoeba dispar DNA in macaque feces by polymerase chain reaction. Parasitology Research, 85(6), 493–495.

    Article  CAS  PubMed  Google Scholar 

  • Rosida, A., Achmad, A., Malamassam, D., & Alam, S. (2014). Devolution model of forest management in conservation area. International Journal of Scientific & Technology Research, 3(8), 381–385.

    Google Scholar 

  • Ryan, U., & Cacciò, S. M. (2013). Zoonotic potential of Giardia. International Journal for Parasitology, 43(12), 943–956.

    Article  CAS  PubMed  Google Scholar 

  • Seguel, M., & Gottdenker, N. (2017). The diversity and impact of hookworm infections in wildlife. International Journal for Parasitology: Parasites and Wildlife, 6(3), 177–194.

    PubMed  PubMed Central  Google Scholar 

  • Smith, R. J., & Jungers, W. L. (1997). Body mass in comparative primatology. Journal of Human Evolution, 32(6), 523–559.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Stoner, K. E. (1996). Prevalence and intensity of intestinal parasites in mantled howling monkeys (Alouatta palliata) in northeastern Costa Rica: Implications for conservation biology. Conservation Biology, 10(2), 539–546.

    Article  Google Scholar 

  • Supriatna, J. (1991). Hybridization between Macaca maurus and M. tonkeana: A test of species status using behavioral and morphogenetic analyses. Doctoral dissertation, Department of Anthropology, University of New Mexico.

  • Supriatna, J., Froehlich, J. W., Erwin, J. M., & Southwik, C. H. (1992). Population, habitat and conservation status of Macaca maurus, Macaca tonkeana and their putative hybrids. Tropical Biodiversity, 1, 31–48.

    Google Scholar 

  • Supriatna, J., Shekelle, M., & Burton, J. (2008). Macaca maura. The IUCN Red List of Threatened Species 2008. Resource document. International Union for Conservation of Nature and Natural Resources https://doi.org/10.2305/IUCN.UK.2008.RLTS.T12553A3356200.en (Accessed January 10, 2018).

  • Thompson, R. C. A., Lymbery, A. J., & Smith, A. (2010). Parasites, emerging disease and wildlife conservation. International Journal for Parasitology, 40, 1163–1170.

    Article  CAS  PubMed  Google Scholar 

  • Tompkins, D. M., Dunn, A. M., Smith, M. J., & Telfer, S. (2011). Wildlife diseases: From individuals to ecosystems. Journal of Animal Ecology, 80(1), 19–38.

    Article  Google Scholar 

  • Tuda, J., Feng, M., Imada, M., Kobayashi, S., Cheng, X., & Tachibana, H. (2016). Identification of Entamoeba polecki with unique 18S rRNA gene sequences from celebes crested macaques and pigs in Tangkoko nature reserve, North Sulawesi, Indonesia. Journal of Eukaryotic Microbiology, 63(5), 572–577.

    Article  CAS  Google Scholar 

  • Verweij, J. J., Polderman, A. M., & Clark, C. G. (2001). Genetic variation among human isolates of uninucleated cyst-producing Entamoeba species. Journal of Clinical Microbiology, 39(4), 1644–1646.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vitone, N. D., Altizer, S., & Nunn, C. L. (2004). Body size, diet and sociality influence the species richness of parasitic worms in anthropoid primates. Evolutionary Ecology Research, 6(2), 183–199.

    Google Scholar 

  • Wenz-Mücke, A., Sithithaworn, P., Petney, T. N., & Taraschewski, H. (2013). Human contact influences the foraging behaviour and parasite community in long-tailed macaques. Parasitology, 140(6), 709–718.

    Article  PubMed  Google Scholar 

  • Whitmore, T. C. (1984). Tropical rain forest of the Far East. Oxford: Clarendon.

    Google Scholar 

  • Widjana, D. P., & Sutisna, P. (2000). Prevalence of soil-transmitted helminth infections in the rural population of Bali, Indonesia. Southeast Asian Journal of Tropical Medicine and Public Health, 31(3), 454–459.

    CAS  Google Scholar 

  • Woodroffe, R. (1999). Managing disease threats to wild mammals. Animal Conservation, 2, 185–193.

    Article  Google Scholar 

  • Ye, J., Xiao, L., Ma, J., Guo, M., Liu, L., & Feng, Y. (2012). Anthroponotic enteric parasites in monkeys in public park, China. Emerging Infectious Diseases, 18(10), 1640.

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

This work was supported by a Safari Ravenna Zoo’s grant for conservation to MC, and Roma Tre University doctoral funds granted to AA. We would like to mention Pak Dedy Asriady and Pak Abdul Azis Bakry (former and current Head of Administration Section at BBNP) for their assistance and logistical support, and Pak Haro, Pak Pado, Jack Syamsuddin, and Hendra (former and current rangers at BBNP) for their invaluable commitment in the field. We also thank all the students of the Laboratory of Parasitology and Cristina Sagnotti (Hasanuddin University, Indonesia), Lavinia Germani and Elena Amanti (Roma Tre University, Italy), K. T. Hanson (San Diego State University, USA), and Leonardo Sale (University of Turin, Italy) for their help and support in this project. We would also like to thank Amiruddin Bin Dahlan (Hasanuddin University, Indonesia) for his invaluable help in the field and for his friendship, and mama Aco and her family for taking great care of us. We kindly acknowledge Dr. Giuseppe Donati (Oxford Brookes University, UK) and Dr. Emiliano Mancini (Sapienza University of Rome, Italy) for their comments on earlier versions of this manuscript. Finally, we thank the editor-in-chief Dr. Joanna Setchell and two anonymous reviewers, whose comments greatly improved the manuscript.

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Authors and Affiliations

  1. Department of Sciences, Roma Tre University, Rome, Italy

    Alessandro Albani & Monica Carosi

  2. Istituto Zooprofilattico Sperimentale del Lazio e della Toscana “M. Aleandri”, Rome, Italy

    Claudio De Liberato & Giusy Cardeti

  3. Faculty of Medicine, Hasanuddin University, Makassar, Sulawesi, Indonesia

    Isra Wahid

  4. Department of Clinical Sciences and Translational Medicine, Tor Vergata University, Rome, Italy

    Federica Berrilli

  5. Department of Anthropology, San Diego State University, San Diego, CA, USA

    Erin Phelps Riley

  6. Faculty of Forestry, Hasanuddin University, Makassar, Sulawesi, Indonesia

    Putu Oka Ngakan

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  1. Alessandro Albani
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  4. Federica Berrilli
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  8. Monica Carosi
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Contributions

AA and MC originally formulated the idea. CDL, IW and FB developed methodology. AA conducted fieldwork. AA, CDL and IW performed morphological analyses. AA and MC wrote the manuscript. EPR, GC and PON provided substantial editorial advice.

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Correspondence to Alessandro Albani.

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Handling Editor: Joanna M. Setchell

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Albani, A., De Liberato, C., Wahid, I. et al. Preliminary Assessment of Gastrointestinal Parasites in Two Wild Groups of Endangered Moor Macaques (Macaca maura) from Sulawesi. Int J Primatol 40, 671–686 (2019). https://doi.org/10.1007/s10764-019-00114-w

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  • DOI: https://doi.org/10.1007/s10764-019-00114-w

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