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Loss of protozoan and metazoan intestinal symbiont biodiversity in wild primates living in unprotected forests

  • 1.

    Cardinale, B. J. et al. Biodiversity loss and its impact on humanity. Nature 486, 59–67 (2012).

    ADS  CAS  PubMed  Google Scholar 

  • 2.

    Ripple, W. J. et al. Saving the world’s terrestrial megafauna. Bioscience 66, 807–812 (2016).

    PubMed  PubMed Central  Google Scholar 

  • 3.

    Jamhuri, J. et al. Selective logging causes the decline of large-sized mammals including those in unlogged patches surrounded by logged and agricultural areas. Biol. Conserv. 227, 40–47 (2018).

    Google Scholar 

  • 4.

    Barelli, C. et al. Habitat fragmentation is associated to gut microbiota diversity of an endangered primate: Implications for conservation. Sci. Rep. 5, 14862 (2015).

    ADS  CAS  PubMed  PubMed Central  Google Scholar 

  • 5.

    Amato, K. R. et al. Habitat degradation impacts black howler monkey (Alouatta pigra) gastrointestinal microbiomes. ISME J. 7, 1344–1353 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  • 6.

    Borbón-García, A., Reyes, A., Vives-Flórez, M. & Caballero, S. Captivity shapes the gut microbiota of Andean bears: Insights into health surveillance. Front. Microbiol. 8, 1316 (2017).

    PubMed  PubMed Central  Google Scholar 

  • 7.

    Pascoe, E. L., Hauffe, H. C., Marchesi, J. R. & Perkins, S. E. Network analysis of gut microbiota literature: An overview of the research landscape in non-human animal studies. ISME J. 11, 2644–2651 (2017).

    PubMed  PubMed Central  Google Scholar 

  • 8.

    Hauffe, H. C. & Barelli, C. Conserve the germs: The gut microbiota and adaptive potential. Conserv. Genet. 20, 19–27 (2019).

    Google Scholar 

  • 9.

    Trevelline, B. K., Fontaine, S. S., Hartup, B. K. & Kohl, K. D. Conservation biology needs a microbial renaissance: A call for the consideration of host-associated microbiota in wildlife management practices. Proc. R. Soc. B. 286, 20182448 (2019).

    PubMed  Google Scholar 

  • 10.

    Huffman, M. A. & Chapman, C. A. Primate Parasite Ecology: The Dynamics and Study of Host-Parasite Relationships (Cambridge University Press, Cambridge, 2009).

    Google Scholar 

  • 11.

    Sá, R. M. et al. Gastrointestinal symbionts of chimpanzees in Cantanhez National Park, Guinea-Bissau with respect to habitat fragmentation. Am. J. Primatol. 75, 1032–1041 (2013).

    PubMed  Google Scholar 

  • 12.

    Hotez, P. J. et al. Helminth infections: The great neglected tropical diseases. J. Clin. Invest. 118, 1311–1321 (2008).

    CAS  PubMed  PubMed Central  Google Scholar 

  • 13.

    Nunn, C. L. et al. Parasites and the evolutionary diversification of primate clades. Am. Nat. 164, S90–S103 (2004).

    PubMed  Google Scholar 

  • 14.

    Summers, K. et al. Parasitic exploitation as an engine of diversity. Biol. Rev. 78, 639–675 (2003).

    PubMed  Google Scholar 

  • 15.

    Barber, I. The role of parasites in fish-bird interactions: A behavioural ecological perspective. In Interactions Between Fish and Birds: Implications for Management (ed. Cowx, I. G.) 221–243 (Blackwell Science Ltd., Oxford, 2007).

    Google Scholar 

  • 16.

    Lefèvre, T. et al. The ecological significance of manipulative parasites. Trends Ecol. Evol. 24, 41–48 (2009).

    PubMed  Google Scholar 

  • 17.

    Broadhurst, M. J. et al. Therapeutic helminth infection of macaques with idiopathic chronic diarrhea alters the inflammatory signature and mucosal microbiota of the colon. PLoS Pathog. 8, e1003000 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  • 18.

    Fenton, A. & Brockhurst, M. A. The role of specialist parasites in structuring host communities. Ecol. Res. 23, 795–804 (2008).

    Google Scholar 

  • 19.

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

    Google Scholar 

  • 20.

    Gómez, A. & Nichols, E. Neglected wild life: Parasitic biodiversity as a conservation target. Int. J. Parasitol. Parasites Wildl. 2, 222–227 (2013).

    PubMed  PubMed Central  Google Scholar 

  • 21.

    Mann, A. E. et al. Biodiversity of protists and nematodes in the wild nonhuman primate gut. ISME J. 14, 609–622. https://doi.org/10.1038/s41396-019-0551-4 (2019).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • 22.

    Colwell, R. K., Dunn, R. R. & Harris, N. C. Coextinction and persistence of dependent species in a changing world. Ann. Rev. Ecol. Evol. Syst. 43, 183–203 (2012).

    Google Scholar 

  • 23.

    Strona, G. Past, present and future of host-parasite co-extinctions. Int. J. Parasitol. Parasites Wildl. 4, 431–441 (2015).

    PubMed  PubMed Central  Google Scholar 

  • 24.

    Wood, C. L. et al. Human impacts decouple a fundamental ecological relationship—the positive association between host diversity and parasite diversity. Glob. Change Biol. 24, 3666–3679 (2018).

    ADS  Google Scholar 

  • 25.

    Bordes, F. et al. Habitat fragmentation alters the properties of a host-parasite network: Rodents and their helminths in South-East Asia. J. Anim. Ecol. 84, 1253–1263 (2015).

    PubMed  Google Scholar 

  • 26.

    Estrada, A. et al. Impending extinction crisis of the world’s primates: Why primates matter. Sci. Adv. 3, e1600946 (2017).

    ADS  PubMed  PubMed Central  Google Scholar 

  • 27.

    Jones, K. E. et al. Global trends in emerging infectious diseases. Nature 451, 990–993 (2008).

    ADS  CAS  PubMed  PubMed Central  Google Scholar 

  • 28.

    Mittermeier, R. A., Turner, W. R., Larsen, F. W., Brooks, T. M. & Gascon, C. Global biodiversity conservation: The critical role of hotspots. Biodivers. Hotspots https://doi.org/10.1007/978-3-642-20992-5_1 (2011).

    Article  Google Scholar 

  • 29.

    Laurance, W. F. et al. Averting biodiversity collapse in tropical forest protected areas. Nature 489, 290–294 (2012).

    ADS  CAS  PubMed  Google Scholar 

  • 30.

    Rovero, F. et al. Primates decline rapidly in unprotected forests: Evidence from a monitoring program with data constraints. PLoS One 10, e0118330 (2015).

    PubMed  PubMed Central  Google Scholar 

  • 31.

    Rovero, F., Mtui, A. S., Kitegile, A. S. & Nielsen, M. R. Hunting or habitat degradation? Decline of primate populations in Udzungwa Mountains, Tanzania: An analysis of threats. Biol. Conserv. 146, 89–96 (2012).

    Google Scholar 

  • 32.

    Barelli, C. et al. Altitude and human disturbance are associated with helminth diversity in an endangered primate, Procolobus gordonorum. PLoS One 14, e0225142 (2019).

    CAS  PubMed  PubMed Central  Google Scholar 

  • 33.

    Steel, R. I. The effects of habitat parameters on the behavior, ecology, and conservation of the Udzungwa red colobus monkey (Procolobus gordonorum). Ph.D. Thesis, Duke University, USA (2012).

  • 34.

    Warren, Y., Higham, J. P., Maclarnon, A. M. & Ross, C. Crop-raiding and commensalism in olive baboons: The costs and benefits of living with humans. Primates of Gashaka https://doi.org/10.1007/978-1-4419-7403-7_8 (2011).

    Article  Google Scholar 

  • 35.

    Raharivololona, B. M. & Ganzhorn, J. U. Seasonal variations in gastrointestinal parasites excreted by the gray mouse lemur Microcebus murinus in Madagascar. Endanger. Species Res. 11, 113–122 (2010).

    Google Scholar 

  • 36.

    Gillespie, T. R., Barelli, C. & Heistermann, M. Effects of social status and stress on patterns of gastrointestinal parasitism in wild white-handed gibbons (Hylobates lar). Am. J. Phys. Anthropol. 150, 602–608 (2013).

    PubMed  Google Scholar 

  • 37.

    Martínez-Mota, R., Garber, P. A., Palme, R. & Gillespie, T. R. The relative effects of reproductive condition, stress, and seasonality on patterns of parasitism in wild female black howler monkeys (Alouatta pigra). Am. J. Primatol. 79, e22669 (2017).

    Google Scholar 

  • 38.

    Barelli, C., Albanese, D., Stumpf, R. M., Asangba, A., Donati, C., Rovero, F. & Hauffe, H. C. The gut microbiota of wild arboreal and ground-feeding tropical primates are affected differently by habitat disturbance. mSystems 5(3), e00061–20 (2020).

    Google Scholar 

  • 39.

    Lukeš, J., Stensvold, C. R., Jirků-Pomajbíková, K. & Wegener Parfrey, L. Are human intestinal eukaryotes beneficial or commensals?. PLoS Pathog. 11, e1005039 (2015).

    PubMed  PubMed Central  Google Scholar 

  • 40.

    Sobotková, K. et al. Helminth therapy—From the parasite perspective. Trends Parasitol. 35, 501–515 (2019).

    PubMed  Google Scholar 

  • 41.

    Laforest-Lapointe, I. & Arrieta, M.-C. Microbial eukaryotes: A missing link in gut microbiome studies. mSystems 3, 20 (2018).

    Google Scholar 

  • 42.

    Kreisinger, J., Bastien, G., Hauffe, H. C., Marchesi, J. & Perkins, S. E. Interactions between multiple helminths and the gut microbiota in wild rodents. Philos. Trans. R. Soc. Lond. B Biol. Sci. 370, 20 (2015).

    Google Scholar 

  • 43.

    Leung, J. M., Graham, A. L. & Knowles, S. C. L. Parasite-microbiota interactions with the vertebrate gut: Synthesis through an ecological lens. Front. Microbiol. 9, 843 (2018).

    PubMed  PubMed Central  Google Scholar 

  • 44.

    Modrý, D., Pafčo, B., Petrželková, K. J. & Hasegawa, H. Parasites of Apes: An Atlas of Coproscopic Diagnostics (Edition Chimaira, Frankfurt am Main, 2018).

    Google Scholar 

  • 45.

    Chapman, C. A., Saj, T. L. & Snaith, T. V. Temporal dynamics of nutrition, parasitism, and stress in colobus monkeys: Implications for population regulation and conservation. Am. J. Phys. Anthropol. 134, 240–250 (2007).

    PubMed  Google Scholar 

  • 46.

    Chapman, C. A. et al. Do food availability, parasitism, and stress have synergistic effects on red colobus populations living in forest fragments?. Am. J. Phys. Anthropol. 131, 525–534 (2006).

    PubMed  Google Scholar 

  • 47.

    Gillespie, T. R., Greiner, E. C. & Chapman, C. A. Gastrointestinal parasites of the colobus monkeys of Uganda. J. Parasitol. 91, 569–573 (2005).

    PubMed  Google Scholar 

  • 48.

    Weyher, A. H., Ross, C. & Semple, S. Gastrointestinal parasites in crop raiding and wild foraging Papio anubis in Nigeria. Int. J. Primat. 27, 1519–1534 (2006).

    Google Scholar 

  • 49.

    Howells, M. E., Pruetz, J. & Gillespie, T. R. Patterns of gastro-intestinal parasites and commensals as an index of population and ecosystem health: The case of sympatric western chimpanzees (Pan troglodytes verus) and guinea baboons (Papio hamadryas papio) at Fongoli, Senegal. Am. J. Primatol. 73, 173–179 (2011).

    PubMed  Google Scholar 

  • 50.

    Akinyi, M. Y. et al. Costs and drivers of helminth parasite infection in wild female baboons. J. Anim. Ecol. 88, 1029–1043 (2019).

    PubMed  PubMed Central  Google Scholar 

  • 51.

    Rovero, F., Marshall, A. R., Jones, T. & Perkin, A. The primates of the Udzungwa Mountains: Diversity, ecology and conservation. J. Anthropol. Sci. 87, 93–126 (2009).

    PubMed  Google Scholar 

  • 52.

    Norton, G. W., Rhine, R. J., Wynn, G. W. & Wynn, R. D. Baboon diet: A five-year study of stability and variability in the plant feeding and habitat of the yellow baboons (Papio cynocephalus) of Mikumi National Park, Tanzania. Folia Primatol. 48, 78–120 (1987).

    CAS  PubMed  Google Scholar 

  • 53.

    Arneberg, P. Host population density and body mass as determinants of species richness in parasite communities: Comparative analyses of directly transmitted nematodes of mammals. Ecography 25, 88–94 (2002).

    Google Scholar 

  • 54.

    Mbora, D. N. M. & McPeek, M. A. Host density and human activities mediate increased parasite prevalence and richness in primates threatened by habitat loss and fragmentation. J. Anim. Ecol. 78, 210–218 (2009).

    PubMed  Google Scholar 

  • 55.

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

    Google Scholar 

  • 56.

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

    PubMed  Google Scholar 

  • 57.

    Zommers, Z., Macdonald, D. W., Johnson, P. J. & Gillespie, T. R. Impact of human activities on chimpanzee ground use and parasitism (Pan troglodytes). Conserv. Lett. 6, 264–273 (2013).

    Google Scholar 

  • 58.

    Ghai, R. R., Chapman, C. A., Omeja, P. A., Jonathan Davies, T. & Goldberg, T. L. Nodule worm infection in humans and wild primates in Uganda: Cryptic species in a newly identified region of human transmission. PLoS Neglect. Trop. D 8, e2641 (2014).

    Google Scholar 

  • 59.

    Bogitsh, B. J., Carter, C. E. & Oeltmann, T. N. Intestinal nematodes. In Human Parasitology (eds Bogitsh, B. J. et al.) 277–312 (Academic Press, London, 2018).

    Google Scholar 

  • 60.

    Cable, J. et al. Global change, parasite transmission and disease control: Lessons from ecology. Philos. Trans. R. Soc. Lond. B Biol. Sci. 372, 20160088 (2017).

    PubMed  PubMed Central  Google Scholar 

  • 61.

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

    ADS  CAS  PubMed  PubMed Central  Google Scholar 

  • 62.

    Gillespie, T. R., Chapman, C. A. & Greiner, E. C. Effects of logging on gastrointestinal parasite infections and infection risk in African primates. J. Appl. Ecol. 42, 699–707 (2005).

    Google Scholar 

  • 63.

    Martínez-Mota, R., Pozo-Montuy, G., Bonilla Sánchez, Y. M. & Gillespie, T. R. Effects of anthropogenic stress on the presence of parasites in a threatened population of black howler monkeys (Alouatta pigra). Therya 9, 161–169 (2018).

    Google Scholar 

  • 64.

    Resasco, J. et al. Experimental habitat fragmentation disrupts nematode infections in Australian skinks. Ecology 100, e02547 (2019).

    PubMed  Google Scholar 

  • 65.

    Cardoso, T. S., Simões, R. O., Luque, J. L. F., Maldonado, A. & Gentile, R. The influence of habitat fragmentation on helminth communities in rodent populations from a Brazilian Mountain Atlantic Forest. J. Helminthol. 90, 460–468 (2016).

    CAS  PubMed  Google Scholar 

  • 66.

    Marshall, A. R. Ecological Report on Magombera Forest. https://www.easternarc.or.tz/groups/webcontent/documents/pdf/MagomberaEcologicalReport2008.pdf (2008).

  • 67.

    Cavada, N., Tenan, S., Barelli, C. & Rovero, F. Effects of anthropogenic disturbance on primate density at the landscape scale. Conserv. Biol. 33, 873–882 (2019).

    PubMed  Google Scholar 

  • 68.

    Bahrndorff, S., Alemu, T., Alemneh, T. & Lund Nielsen, J. The microbiome of animals: Implications for conservation biology. Int. J. Genom. Proteom. 5304028, 20 (2016).

    Google Scholar 

  • 69.

    Barelli, C. et al. Modeling primate abundance in complex landscapes: A case study from the Udzungwa Mountains of Tanzania. Int. J. Primatol. 36, 209–226 (2015).

    Google Scholar 

  • 70.

    Ruiz-Lopez, M. J. et al. A novel landscape genetic approach demonstrates the effects of human disturbance on the Udzungwa red colobus monkey (Procolobus gordonorum). Heredity 116, 167–176 (2016).

    CAS  PubMed  Google Scholar 

  • 71.

    Barelli, C., Rovero, F., Hodges, K., Araldi, A. & Heistermann, M. Physiological stress levels in the endemic and endangered Udzungwa red colobus vary with elevation. Afr. Zool. 50, 23–30 (2015).

    Google Scholar 

  • 72.

    Gillespie, T. R. Noninvasive assessment of gastrointestinal parasite infections in free-ranging primates. Int. J. Primatol. 27, 1129–1143 (2006).

    Google Scholar 

  • 73.

    Hasegawa, H. Methods of collection and identification of minute nematodes from the feces of primates, with special application to coevolutionary study of pinworms. In Primate Parasite Ecology: The Dynamics of Host-parasite Relationships (ed. Huffman, M. A. C. C.) 29–46 (Cambridge University Press, Cambridge, 2009).

    Google Scholar 

  • 74.

    Jirků-Pomajbíková, K. et al. Molecular identification of Entamoeba species in savanna woodland chimpanzees (Pan troglodytes schweinfurthii). Parasitology 143, 741–748 (2016).

    PubMed  Google Scholar 

  • 75.

    Stensvold, C. R. et al. Detecting Blastocystis using parasitologic and DNA-based methods: A comparative study. Diagn. Micr. Infect. Dis. 59, 303–307 (2007).

    CAS  Google Scholar 

  • 76.

    Poulin, R. Quantifying parasite diversity. In Parasite Diversity and Diversification: Evolutionary Ecology Meets Phylogenetics (eds Morand, S. et al.) 9–26 (Cambridge University Press, Cambridge, 2015).

    Google Scholar 

  • 77.

    Zuur, A. F. & Ieno, E. N. A protocol for conducting and presenting results of regression-type analyses. Methods Ecol. Evol. 7, 636–645 (2016).

    Google Scholar 


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