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

. 2020 Jul 02 ; 10 (1) : 10917. [epub] 20200702

Jazyk angličtina Země Velká Británie, Anglie Médium electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid32616818
Odkazy

PubMed 32616818
PubMed Central PMC7331812
DOI 10.1038/s41598-020-67959-7
PII: 10.1038/s41598-020-67959-7
Knihovny.cz E-zdroje

In light of the current biodiversity crisis, investigating the human impact on non-human primate gut biology is important to understanding the ecological significance of gut community dynamics across changing habitats and its role in conservation. Using traditional coproscopic parasitological techniques, we compared the gastrointestinal protozoan and metazoan symbiont richness of two primates: the Udzungwa red colobus (Procolobus gordonorum) and the yellow baboon (Papio cynocephalus). These species live sympatrically in both protected and unprotected forests within the Udzungwa Mountains of Tanzania with distinct ecological adaptations and diets. Our results showed that terrestrial and omnivorous yellow baboons had 2 (95% CI 1.47-2.73) and 3.78 (2.62-5.46) times higher gut symbiont richness (both including and excluding rare protozoans) compared to the arboreal and leaf-eating Udzungwa red colobus in unprotected and protected forest, respectively. We also found a consistent depletion of symbiont richness in red colobus living in the unprotected forest fragment compared to the continuous protected forests [the latter having 1.97 times (95% CI 1.33-2.92) higher richness], but not in yellow baboons. Richness reduction was particularly evident in the Udzungwa red colobus monkeys, confirming the pattern we reported previously for gut bacterial communities. This study demonstrates the impact of human activities even on the microbiodiversity of the intestinal tract of this species. Against the background of rapid global change and habitat degradation, and given the health benefits of intact gut communities, the decrease in natural gut symbionts reported here is worrying. Further study of these communities should form an essential part of the conservation framework.

Zobrazit více v PubMed

Cardinale BJ, et al. Biodiversity loss and its impact on humanity. Nature. 2012;486:59–67. PubMed

Ripple WJ, et al. Saving the world’s terrestrial megafauna. Bioscience. 2016;66:807–812. PubMed PMC

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. 2018;227:40–47.

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

Amato KR, et al. Habitat degradation impacts black howler monkey (Alouatta pigra) gastrointestinal microbiomes. ISME J. 2013;7:1344–1353. PubMed PMC

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

Pascoe EL, Hauffe HC, Marchesi JR, Perkins SE. Network analysis of gut microbiota literature: An overview of the research landscape in non-human animal studies. ISME J. 2017;11:2644–2651. PubMed PMC

Hauffe HC, Barelli C. Conserve the germs: The gut microbiota and adaptive potential. Conserv. Genet. 2019;20:19–27.

Trevelline BK, Fontaine SS, Hartup BK, Kohl KD. Conservation biology needs a microbial renaissance: A call for the consideration of host-associated microbiota in wildlife management practices. Proc. R. Soc. B. 2019;286:20182448. PubMed PMC

Huffman MA, Chapman CA. Primate Parasite Ecology: The Dynamics and Study of Host-Parasite Relationships. Cambridge: Cambridge University Press; 2009.

Sá RM, et al. Gastrointestinal symbionts of chimpanzees in Cantanhez National Park, Guinea-Bissau with respect to habitat fragmentation. Am. J. Primatol. 2013;75:1032–1041. PubMed

Hotez PJ, et al. Helminth infections: The great neglected tropical diseases. J. Clin. Invest. 2008;118:1311–1321. PubMed PMC

Nunn CL, et al. Parasites and the evolutionary diversification of primate clades. Am. Nat. 2004;164:S90–S103. PubMed

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

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

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

Broadhurst MJ, et al. Therapeutic helminth infection of macaques with idiopathic chronic diarrhea alters the inflammatory signature and mucosal microbiota of the colon. PLoS Pathog. 2012;8:e1003000. PubMed PMC

Fenton A, Brockhurst MA. The role of specialist parasites in structuring host communities. Ecol. Res. 2008;23:795–804.

Marcogliese DJ. Parasites: Small players with crucial roles in the ecological theater. EcoHealth. 2004;1:151–164.

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

Mann AE, et al. Biodiversity of protists and nematodes in the wild nonhuman primate gut. ISME J. 2019;14:609–622. doi: 10.1038/s41396-019-0551-4. PubMed DOI PMC

Colwell RK, Dunn RR, Harris NC. Coextinction and persistence of dependent species in a changing world. Ann. Rev. Ecol. Evol. Syst. 2012;43:183–203.

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

Wood CL, et al. Human impacts decouple a fundamental ecological relationship—the positive association between host diversity and parasite diversity. Glob. Change Biol. 2018;24:3666–3679. PubMed

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. 2015;84:1253–1263. PubMed

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

Jones KE, et al. Global trends in emerging infectious diseases. Nature. 2008;451:990–993. PubMed PMC

Mittermeier RA, Turner WR, Larsen FW, Brooks TM, Gascon C. Global biodiversity conservation: The critical role of hotspots. Biodivers. Hotspots. 2011 doi: 10.1007/978-3-642-20992-5_1. DOI

Laurance WF, et al. Averting biodiversity collapse in tropical forest protected areas. Nature. 2012;489:290–294. PubMed

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

Rovero F, Mtui AS, Kitegile AS, Nielsen MR. Hunting or habitat degradation? Decline of primate populations in Udzungwa Mountains, Tanzania: An analysis of threats. Biol. Conserv. 2012;146:89–96.

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

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).

Warren Y, Higham JP, Maclarnon AM, Ross C. Crop-raiding and commensalism in olive baboons: The costs and benefits of living with humans. Primates of Gashaka. 2011 doi: 10.1007/978-1-4419-7403-7_8. DOI

Raharivololona BM, Ganzhorn JU. Seasonal variations in gastrointestinal parasites excreted by the gray mouse lemur Microcebus murinus in Madagascar. Endanger. Species Res. 2010;11:113–122.

Gillespie TR, 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. 2013;150:602–608. PubMed

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

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

Lukeš J, Stensvold CR, Jirků-Pomajbíková K, Wegener Parfrey L. Are human intestinal eukaryotes beneficial or commensals? PLoS Pathog. 2015;11:e1005039. PubMed PMC

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

Laforest-Lapointe I, Arrieta M-C. Microbial eukaryotes: A missing link in gut microbiome studies. mSystems. 2018;3:20. PubMed PMC

Kreisinger J, Bastien G, Hauffe HC, Marchesi J, Perkins SE. Interactions between multiple helminths and the gut microbiota in wild rodents. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2015;370:20. PubMed PMC

Leung JM, Graham AL, Knowles SCL. Parasite-microbiota interactions with the vertebrate gut: Synthesis through an ecological lens. Front. Microbiol. 2018;9:843. PubMed PMC

Modrý D, Pafčo B, Petrželková KJ, Hasegawa H. Parasites of Apes: An Atlas of Coproscopic Diagnostics. Frankfurt am Main: Edition Chimaira; 2018.

Chapman CA, Saj TL, Snaith TV. Temporal dynamics of nutrition, parasitism, and stress in colobus monkeys: Implications for population regulation and conservation. Am. J. Phys. Anthropol. 2007;134:240–250. PubMed

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

Gillespie TR, Greiner EC, Chapman CA. Gastrointestinal parasites of the colobus monkeys of Uganda. J. Parasitol. 2005;91:569–573. PubMed

Weyher AH, Ross C, Semple S. Gastrointestinal parasites in crop raiding and wild foraging Papio anubis in Nigeria. Int. J. Primat. 2006;27:1519–1534.

Howells ME, Pruetz J, Gillespie TR. 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. 2011;73:173–179. PubMed

Akinyi MY, et al. Costs and drivers of helminth parasite infection in wild female baboons. J. Anim. Ecol. 2019;88:1029–1043. PubMed PMC

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

Norton GW, Rhine RJ, Wynn GW, Wynn RD. 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. 1987;48:78–120. PubMed

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. 2002;25:88–94.

Mbora DNM, McPeek MA. Host density and human activities mediate increased parasite prevalence and richness in primates threatened by habitat loss and fragmentation. J. Anim. Ecol. 2009;78:210–218. PubMed

Vitone ND, Altizer S, Nunn CL. Body size, diet and sociality influence the species richness of parasitic worms in anthropoid primates. Evol. Ecol. Res. 2004;6:183–199.

Nunn CL, Altizer S, Jones KE, Sechrest W. Comparative tests of parasite species richness in primates. Am. Nat. 2003;162:597–614. PubMed

Zommers Z, Macdonald DW, Johnson PJ, Gillespie TR. Impact of human activities on chimpanzee ground use and parasitism (Pan troglodytes) Conserv. Lett. 2013;6:264–273.

Ghai RR, Chapman CA, Omeja PA, Jonathan Davies T, Goldberg TL. Nodule worm infection in humans and wild primates in Uganda: Cryptic species in a newly identified region of human transmission. PLoS Neglect. Trop. D. 2014;8:e2641. PubMed PMC

Bogitsh BJ, Carter CE, Oeltmann TN. Intestinal nematodes. In: Bogitsh BJ, Carter CE, Oeltmann TN, editors. Human Parasitology. London: Academic Press; 2018. pp. 277–312.

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

Hussain S, Ram MS, 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. 2013;8:e63685. PubMed PMC

Gillespie TR, Chapman CA, Greiner EC. Effects of logging on gastrointestinal parasite infections and infection risk in African primates. J. Appl. Ecol. 2005;42:699–707.

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

Resasco J, et al. Experimental habitat fragmentation disrupts nematode infections in Australian skinks. Ecology. 2019;100:e02547. PubMed

Cardoso TS, Simões RO, Luque JLF, Maldonado A, Gentile R. The influence of habitat fragmentation on helminth communities in rodent populations from a Brazilian Mountain Atlantic Forest. J. Helminthol. 2016;90:460–468. PubMed

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

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

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

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

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

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. 2015;50:23–30.

Gillespie TR. Noninvasive assessment of gastrointestinal parasite infections in free-ranging primates. Int. J. Primatol. 2006;27:1129–1143.

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

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

Stensvold CR, et al. Detecting Blastocystis using parasitologic and DNA-based methods: A comparative study. Diagn. Micr. Infect. Dis. 2007;59:303–307. PubMed

Poulin R. Quantifying parasite diversity. In: Morand S, Krasnov BR, Littlewood DT, editors. Parasite Diversity and Diversification: Evolutionary Ecology Meets Phylogenetics. Cambridge: Cambridge University Press; 2015. pp. 9–26.

Zuur AF, Ieno EN. A protocol for conducting and presenting results of regression-type analyses. Methods Ecol. Evol. 2016;7:636–645.

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...