Ecological drivers of helminth infection patterns in the Virunga Massif mountain gorilla population
Status PubMed-not-MEDLINE Jazyk angličtina Země Velká Británie, Anglie Médium electronic-ecollection
Typ dokumentu časopisecké články
PubMed
35145846
PubMed Central
PMC8802862
DOI
10.1016/j.ijppaw.2022.01.007
PII: S2213-2244(22)00007-4
Knihovny.cz E-zdroje
- Klíčová slova
- Environmental and host factors, Helminth infection, Mountain gorilla, Strongylid nematode, Tapeworm,
- Publikační typ
- časopisecké články MeSH
The Virunga Massif mountain gorilla population has been periodically monitored since the early 1970s, with gradually increasing effort. The population declined drastically in the 1970s, but the numbers stabilized in the 1980s. Since then, the population has been steadily increasing within their limited habitat fragment that is surrounded by a dense human population. We examined fecal samples collected during the Virunga 2015-2016 surveys in monitored and unmonitored gorilla groups and quantified strongylid and tapeworm infections using egg counts per gram to determine environmental and host factors that shape these helminth infections. We showed that higher strongylid infections were present in gorilla groups with smaller size of the 500-m buffered minimum-convex polygon (MCP) of detected nest sites per gorilla group, but in higher gorilla densities and inhabiting vegetation types occurring at higher elevations with higher precipitation and lower temperatures. On the contrary, the impact of monitoring (habituation) was minor, detected in tapeworms and only when in the interaction with environmental variables and MCP area. Our results suggest that the Virunga mountain gorilla population may be partially regulated by strongylid nematodes at higher gorilla densities. New health challenges are probably emerging among mountain gorillas because of the success of conservation efforts, as manifested by significant increases in gorilla numbers in recent decades, but few possibilities for the population expansion due to limited amounts of habitat.
Biology Centre Institute of Parasitology Czech Academy of Sciences České Budějovice Czech Republic
Department of Botany and Zoology Faculty of Science Masaryk University Brno Czech Republic
Department of Primatology Max Planck Institute for Evolutionary Anthropology Leipzig Germany
Dian Fossey Gorilla Fund Musanze Rwanda
Here There Mapping Solutions Berlin Germany
Institut Congolais pour la Conservation de la Nature Kinshasa Congo
Institut Congolais pour la Conservation de la Nature Parc National de Kahuzi Biega Bukavu Congo
Institute of Vertebrate Biology Czech Academy of Sciences Brno Czech Republic
International Gorilla Conservation Programme Kigali Rwanda
Liberec Zoo Liberec Czech Republic
Rwanda Development Board Kigali Rwanda
School of Veterinary Medicine University of California Davis CA USA
Zobrazit více v PubMed
Advani N.K. World Wildlife Fund; Washington, DC: 2014. WWF Wildlife and Climate Change Series: Mountain gorilla.
Anderson R.M., May R.M. Population biology of infectious diseases: Part I. Nature. 1979;280:361–367. PubMed
Arneberg P., Skorping A., Grenfell B., Read A.F. Host densities as determinants of abundance in parasite communities. Proc. R. Soc. Lond. B Biol. Sci. 1998;265:1283–1289.
Ashford R.W., Lawson H., Butynski T.M., Reid G.D.F. Patterns of intestinal parasitism in the mountain gorilla Gorilla gorilla in the Bwindi-Impenetrable Forest, Uganda. J. Zool. 1996;239:507–514.
Barton K. 2020. MuMIn: Multi-Model Inference. R Package.https://CRAN.R-project.org/package=MuMIn version 1.43.17.
Bordes F., Morand S., Kelt D.A., Van Vuren D.H. Home range and parasite diversity in mammals. Am. Nat. 2009;173:467–474. PubMed
Brooks M.E., Kristensen K., Van Benthem K.J., Magnusson A., Berg C.W., Nielsen A., Skaug H.J., Machler M., Bolker B.M. glmmTMB balances speed and flexibility among packages for zero-inflated generalized linear mixed modeling. R J. 2017;9:378–400.
Burgunder J., Pafčo B., Petrželková K.J., Modrý D., Hashimoto C., MacIntosh A.J.J. Complexity in behavioural organization and strongylid infection among wild chimpanzees. Anim. Behav. 2017;129:257–268.
Caillaud D., Eckardt W., Vecellio V., Ndagijimana F., Mucyo J.-P., Hirwa J.-P., Stoinski T. Violent encounters between social units hinder the growth of a high-density mountain gorilla population. Sci. Adv. 2020;6 PubMed PMC
Caillaud D., Ndagijimana F., Giarrusso A.J., Vecellio V., Stoinski T.S. Mountain gorilla ranging patterns: influence of group size and group dynamics. Am. J. Primatol. 2014;76:730–746. PubMed
Callinan A.P.L., Westcott J.M. Vertical distribution of trichostrongylid larvae on herbage and in soil. Int. J. Parasitol. 1986;16:241–244. PubMed
Chylinski C., Lherminé E., Coquille M., Cabaret J. Desiccation tolerance of gastrointestinal nematode third-stage larvae: exploring the effects on survival and fitness. Parasitol. Res. 2014;113:2789–2796. PubMed
Condy J.B. Observations on internal parasites in Rhodesian elephant, Loxodonta africana Blumenbach 1797. Proc. Trans. Rhodesia Sci. Assoc. 1974;55:67–99.
Cousins D., Huffman M.A. Medicinal properties in the diet of gorillas: an ethno-pharmacological evaluation. Afr. Stud. Monogr. 2002;23:65–89.
Denegri G.M. Review of oribatid mites as intermediate hosts of tapeworms of the Anoplocephalidae. Exp. Appl. Acarol. 1993;17:567–580.
Dobson A.P. In: Parasite Communities: Patterns and Processes. Esch G.W., Bush A.O., Aho J.M., editors. Chapman and Hall; London: 1990. Models for multi-species parasite-host communities; pp. 261–288.
Doležalová J., Pafčo B., Modrý D., Jirků-Pomajbíková K. In: Parasites of Apes: an Atlas of Coproscopic Diagnostics. Modrý D., Pafčo B., Petrželková K.J., Hasegawa H., editors. Chimaira; Frankfurt am Main: 2018. Parasite quantification; pp. 34–38.
Doležalová J., Vallo P., Petrželková K.J., Foitová I., Nurcahyo W., Mudakikwa A., Hashimoto C., Jirků M., Lukeš J., Scholz T. Molecular phylogeny of anoplocephalid tapeworms (Cestoda: Anoplocephalidae) infecting humans and non-human primates. Parasitology. 2015;142:1278–1289. PubMed
Doran-Sheehy D.M., Derby A.M., Greer D., Mongo P. Habituation of western gorillas: the process and factors that influence it. Am. J. Primatol. 2007;69:1354–1369. PubMed
Eckardt W., Stoinski T.S., Rosenbaum S., Santymire R. Social and ecological factors alter stress physiology of Virunga mountain gorillas (Gorilla beringei beringei) Ecol. Evol. 2019;9:5248–5259. PubMed PMC
Eckardt W., Stoinski T.S., Rosenbaum S., Umuhoza M.R., Santymire R. Validating faecal glucocorticoid metabolite analysis in the Virunga mountain gorilla using a natural biological stressor. Conserv. Physiol. 2016;4:cow029. PubMed PMC
Freeland W.J. Pathogens and the evolution of primate sociality. Biotropica. 1976;8:12–24.
Ghai R.R., Fugere V., Chapman C.A., Goldberg T.L., Davies T.J. Sickness behaviour associated with non-lethal infections in wild primates. Proc. R. Soc. B Biol. Sci. 2015;282:20151436. PubMed PMC
Ghosh T.C. Ecologic study of soil oribatid mite, Scheloribates rectus (Acari) in high altitude Botanical Garden of Darjeeling Himalayas, India. Biologia. 2020;75:1289–1295.
Granjon A.-C., Robbins M.M., Arinaitwe J., Cranfield M.R., Eckardt W., Mburanumwe I., Musana A., Robbins A.M., Roy J., Sollmann R., Vigilant L., Hickey J.R. Estimating abundance and growth rates in a wild mountain gorilla population. Anim. Conserv. 2020;23:455–465.
Gray M., Fawcett K.A., Basabose A., Cranfield M., Vigilant L., Roy J., Uwingeli P., Mburanumwe I., Kagoda E., Robbins M. 2011. Virunga Massif Mountain Gorilla Census – 2010 Summary Report.
Gray M., McNeilage A., Fawcett K., Robbins M.M., Ssebide B., Mbula D., Uwingeli P. Censusing the mountain gorillas in the Virunga Volcanoes: complete sweep method versus monitoring. Afr. J. Ecol. 2010;48:588–599.
Gray M., McNeilage A., Fawcett K., Robbins M.M., Ssebide B., Mbula D., Uwingeli P. UWA, ORTPN, ICCN; 2005. Virunga Volcanoes Range and Census, 2003. Joint Organizers Report.
Gray M., Roy J., Vigilant L., Fawcett K., Basabose A., Cranfield M., Uwingeli P., Mburanumwe I., Kagoda E., Robbins M.M. Genetic census reveals increased but uneven growth of a critically endangered mountain gorilla population. Biol. Conserv. 2013;158:230–238.
Grueter C.C., Ndamiyabo F., Plumptre A.J., Abavandimwe D., Mundry R., Fawcett K.A., Robbins M.M. Long-term temporal and spatial dynamics of food availability for endangered mountain gorillas in Volcanoes National Park, Rwanda. Am. J. Primatol. 2013;75:267–280. PubMed
Grueter C.C., Robbins A.M., Abavandimwe D., Vecellio V., Ndagijimana F., Stoinski T.S., Robbins M.M. Quadratic relationships between group size and foraging efficiency in a herbivorous primate. Sci. Rep. 2018;8:16718. PubMed PMC
Harcourt A.H., Groom A.F.G. Gorilla census. Oryx. 1972;11:355–363.
Harcourt A.H., Parks S.A., Woodroffe R. Human density as an influence on species/area relationships: double jeopardy for small African reserves? Biodivers. Conserv. 2001;10:1011–1026.
Hartig F. 2020. DHARMa: Residual Diagnostics for Hierarchical (Multi-Level/Mixed) Regression Models (2017). R Package Version 01 5.
Hickey J.R., Granjon A.-C., Vigilant L. Virunga 2015–2016 surveys: monitoring mountain gorillas, other select mammals, and illegal activities. 2019. https://igcp.org/content/uploads/2020/09/Bwindi-Sarambwe-2018-Final-Report-2019_12_16.pdf
Higham J.E.S., Shelton E.J. Tourism and wildlife habituation: reduced population fitness or cessation of impact? Tourism Manag. 2011;32:1290–1298.
Hofer H., East M.L. In: Møller A.P., Milinski M., Slater P.J.B., editors. vol. 27. Academic Press; San Diego: 1998. Biological conservation and stress; pp. 405–525. (Advances in the Study of Behavior).
Hoste H., Torres-Acosta J.F., Paolini V., Aguilar-Caballero A., Etter E., Lefrileux Y., Chartier C., Broqua C. Interactions between nutrition and gastrointestinal infections with parasitic nematodes in goats. Small Rumin. Res. 2005;60:141–151.
Huffman M.A., Gotoh S., Turner L.A., Hamai M., Yoshida K. Seasonal trends in intestinal nematode infection and medicinal plant use among chimpanzees in the Mahale Mountains, Tanzania. Primates. 1997;38:111–125.
Kalema-Zikusoka G., Rothman J.M., Fox M.T. Intestinal parasites and bacteria of mountain gorillas (Gorilla beringei beringei) in Bwindi Impenetrable National Park, Uganda. Primates. 2005;46:59–63. PubMed
Kalpers J., Williamson E.A., Robbins M.M., McNeilage A., Nzamurambaho A., Lola N., Mugiri G. Gorillas in the crossfire: population dynamics of the Virunga mountain gorillas over the past three decades. Oryx. 2003;37:326–337.
Kayiranga A., Ndayisaba F., Nahayo L., Karamage F., Nsengiyumva J.B., Mupenzi C., Nyesheja E.M. Analysis of climate and topography impacts on the spatial distribution of vegetation in the Virunga Volcanoes Massif of East-Central Africa. Geosciences. 2017;7:17.
Knapp-Lawitzke F., von Samson-Himmelstjerna G., Demeler J. Elevated temperatures and long drought periods have a negative impact on survival and fitness of strongylid third stage larvae. Int. J. Parasitol. 2016;46:229–237. PubMed
Lindenfors P., Nunn C.L., Jones K.E., Cunningham A.A., Sechrest W., Gittleman J.L. Parasite species richness in carnivores: effects of host body mass, latitude, geographical range and population density. Global Ecol. Biogeogr. 2007;16:496–509.
MacIntosh A.J.J., Hernandez A.D., Huffman M.A. Host age, sex, and reproductive seasonality affect nematode parasitism in wild Japanese macaques. Primates. 2010;51:353–364. PubMed
Marian F., Sandmann D., Krashevska V., Maraun M., Scheu S. Altitude and decomposition stage rather than litter origin structure soil microarthropod communities in tropical montane rainforests. Soil Biol. Biochem. 2018;125:263–274.
Marley C.L., Cook R., Barrett J., Keatinge R., Lampkin N.H. The effects of birdsfoot trefoil (Lotus corniculatus) and chicory (Cichorium intybus) when compared with perennial ryegrass (Lolium perenne) on ovine gastrointestinal parasite development, survival and migration. Vet. Parasitol. 2006;138:280–290. PubMed
May R.M., Anderson R.M. Regulation and stability of host-parasite population interactions: II. Destabilizing Processes. J. Anim. Ecol. 1978;47:249–267.
McNeilage A. In: Mountain Gorillas: Three Decades of Research at Karisoke. Robbins M.M., Sicotte P., Stewart K.J., editors. Cambridge University Press; Cambridge: 2001. Diet and habitat use of two mountain gorilla groups in contrasting habitats in the Virunga; pp. 265–292.
McNeilage A.J. University of Bristol; 1995. Mountain Gorillas in the Virunga Volcanoes: Ecology and Carrying Capacity. PhD Thesis.
Muhangi D., Gardiner C.H., Ojok L., Cranfield M.R., Gilardi K.V., Mudakikwa A.B., Lowenstine L.J. Pathological lesions of the digestive tract in free-ranging mountain gorillas (Gorilla beringei beringei) Am. J. Primatol. 2021 PubMed
Nielsen M.K., Kaplan R.M., Thamsborg S.M., Monrad J., Olsen S.N. Climatic influences on development and survival of free-living stages of equine strongyles: implications for worm control strategies and managing anthelmintic resistance. Vet. J. 2007;174:23–32. PubMed
Nunn C.L., Altizer S., Jones K.E., Sechrest W. Comparative tests of parasite species richness in primates. Am. Nat. 2003;162:597–614. PubMed
O'Connor L.J., Walkden-Brown S.W., Kahn L.P. Ecology of the free-living stages of major trichostrongylid parasites of sheep. Vet. Parasitol. 2006;142:1–15. PubMed
Owiunji I., Nkuutu D., Kujirakwinja D., Liengola I., Plumptre A., Nsanzurwimo A., Fawcett K., Gray M., McNeilage A. Wildlife Conservation Society Report; 2005. The Biodiversity of the Virunga Volcanoes.
Pafčo B., Benavides J.A., Pšenková-Profousová I., Modrý D., Červená B., Shutt K.A., Hasegawa H., Fuh T., Todd A.F., Petrželková K.J. Do habituation, host traits and seasonality have an impact on protist and helminth infections of wild western lowland gorillas? Parasitol. Res. 2017;116:3401–3410. PubMed
Pafčo B., Čížková D., Kreisinger J., Hasegawa H., Vallo P., Shutt K., Todd A., Petrželková K.J., Modrý D. Metabarcoding analysis of strongylid nematode diversity in two sympatric primate species. Sci. Rep. 2018;8:5933. PubMed PMC
Pafčo B., Kreisinger J., Čížková D., Pšenková-Profousová I., Shutt-Phillips K., Todd A., Fuh T., Petrželková K.J., Modrý D. Genetic diversity of primate strongylid nematodes: do sympatric nonhuman primates and humans share their strongylid worms? Mol. Ecol. 2019;28:4786–4797. PubMed
Pandey V.S. Effect of temperature on survival of the free-living stages of Ostertagia ostertagi. J. Parasitol. 1972;58:1042–1046. PubMed
Petrželková K.J., Uwamahoro C., Pafčo B., Červená B., Samaš P., Mudakikwa A., Muvunyi R., Uwingeli P., Gilardi K., Nziza J. Heterogeneity in patterns of helminth infections across populations of mountain gorillas (Gorilla beringei beringei) Sci. Rep. 2021;11:1–14. PubMed PMC
Plumptre A. University of Bristol; 1991. Plant-herbivore Dynamics in the Birungas. PhD Thesis.
Ripple W.J., Newsome T.M., Wolf C., Dirzo R., Everatt K.T., Galetti M., Hayward M.W., Kerley G.I., Levi T., Lindsey P.A. Collapse of the world's largest herbivores. Sci. Adv. 2015;1 PubMed PMC
Robbins M.M., Gray M., Fawcett K.A., Nutter F.B., Uwingeli P., Mburanumwe I., Kagoda E., Basabose A., Stoinski T.S., Cranfield M.R., Byamukama J., Spelman L.H., Robbins A.M. Extreme conservation leads to recovery of the Virunga mountain gorillas. PLoS One. 2011;6 PubMed PMC
Rossanigo C.E., Gruner L. The length of strongylid nematode infective larvae as a reflection of developmental conditions in faeces and consequences on their viability. Parasitol. Res. 1996;82:304–311. PubMed
Rothman J., Bowman D.D. In: Companion and Exotic Animal Parasitology. Bowman D.D., editor. International Veterinary Information Service; Ithaca, NY: 2003. A review of the endoparasites of mountain gorillas.
Rothman J.M., Pell A.N., Bowman D.D. Host-parasite ecology of the helminths in mountain gorillas. J. Parasitol. 2008;94:834–840. PubMed
Ryan S.J., Walsh P.D. Consequences of non-intervention for infectious disease in African great apes. PLoS One. 2011;6 PubMed PMC
Sánchez-Galindo L.M., Sandmann D., Marian F., Krashevska V., Maraun M., Scheu S. Leaf litter identity rather than diversity shapes microbial functions and microarthropod abundance in tropical montane rainforests. Ecol. Evol. 2021;11:2360–2374. PubMed PMC
Shutt K., Heistermann M., Kasim A., Todd A., Kalousová B., Profousouvá I., Petrželková K.J., Fuh T., Dicky J.-F., Bopalanzognako J.-B., Setchell J.M. Effects of habituation, research and ecotourism on faecal glucocorticoid metabolites in wild western lowland gorillas: implications for conservation management. Biol. Conserv. 2014;172:72–79.
Shutt-Phillips K., Pafčo B., Heistermann M., Kasim A., Petrželková K.J., Profousová-Pšenková I., Modrý D., Todd A., Fuh T., Dicky J.-F. Fecal glucocorticoids and gastrointestinal parasite infections in wild western lowland gorillas (Gorilla gorilla gorilla) involved in ecotourism. Gen. Comp. Endocrinol. 2021;312:113859. PubMed
Sleeman J.M., Meader L.L., Mudakikwa A.B., Foster J.W., Patton S. Gastrointestinal parasites of mountain gorillas (Gorilla gorilla beringei) in the Parc National des Volcans, Rwanda. J. Zoo Wildl. Med. 2000;31:322–328. PubMed
Stewart K.J., Sicotte P., Robbins M.M. In: Mountain Gorillas: Three Decades of Research in Karisoke. Robbins M.M., Sicotte P., Stewart K.J., editors. Cambridge University Press; Cambridge: 2001. Mountain gorillas of the Virungas: a short history; pp. 2–26.
Stromberg B.E., Gasbarre L.C., Waite A., Bechtol D.T., Brown M.S., Robinson N.A., Olson E.J., Newcomb H. Cooperia punctata: effect on cattle productivity? Vet. Parasitol. 2012;183:284–291. PubMed
Thorne J.H., Seo C., Basabose A., Gray M., Belfiore N.M., Hijmans R.J. Alternative biological assumptions strongly influence models of climate change effects on mountain gorillas. Ecosphere. 2013;4:1–17.
Tompkins D.M., Dobson A.P., Arneberg P., Begon M.E., Cattadori I.M., Greenman J.V., Heesterbeek J.A.P., Hudson P.J., Newborn D., Pugliese A. In: The Ecology of Wildlife Diseases. Hudson P.J., Rizzoli A., Grenfell B.T., Heesterbeek H., Dobson A., editors. Oxford University Press; Oxford: 2001. Parasites and host population dynamics; pp. 45–62.
van Dijk J., de Louw M.D.E., Kalis L.P.A., Morgan E.R. Ultraviolet light increases mortality of nematode larvae and can explain patterns of larval availability at pasture. Int. J. Parasitol. 2009;39:1151–1156. PubMed
van Dijk J., Morgan E.R. The influence of temperature on the development, hatching and survival of Nematodirus battus larvae. Parasitology. 2008;135:269–283. PubMed
van Dijk J., Sargison N.D., Kenyon F., Skuce P.J. Climate change and infectious disease: helminthological challenges to farmed ruminants in temperate regions. Anim. Int. J. Anim. Biosci. 2010;4:377–392. PubMed
Villagomez F., Palacios-Vargas J.G., Castaño-Meneses G., Castellanos-Vargas I. Effect of tree identity, temporal variation and edaphic parameters on the structure of the edaphic community of oribatid mites in an evergreen tropical forest of Mexico. Appl. Ecol. Environ. Res. 2019;17:14621–14639.
Waterman P.G., Choo G.M., Vedder A.L., Watts D. Digestibility, digestion-inhibitors and nutrients of herbaceous foliage and green stems from an African montane flora and comparison with other tropical flora. Oecologia. 1983;60:244–249. PubMed
Watts D.P. University of Chicago; 1983. Foraging Strategy and Socioecology of Mountain gorillas (Pan gorilla Beringei) PhD Thesis.
Weber A.W., Vedder A. Population dynamics of the Virunga gorillas: 1959–1978. Biol. Conserv. 1983;26:341–366.
Woodford M.H., Butynski T.M., Karesh W.B. Habituating the great apes: the disease risks. Oryx. 2002;36:153–160.
Young R.R., Anderson N., Overend D., Tweedie R.L., Malafant K.W.J., Preston G.N. The effect of temperature on times to hatching of eggs of the nematode Ostertagia circumcincta. Parasitology. 1980;81:477–491. PubMed