Conservation efforts have led to the recovery of the endangered mountain gorilla populations. Due to their limited potential for spatial expansion, population densities increased, which may alter the epidemiology of infectious diseases. Recently, clinical gastrointestinal illnesses linked to helminth infections have been recorded in both gorilla populations. To understand drivers and patterns of helminth infections we quantified strongylid and tapeworm infections across both Virunga Massif and Bwindi populations using fecal egg counts. We assessed the impact of age, sex, group size, season and spatial differences used as a proxy, which reflects observed variation in the occurrence of gastrointestinal problems, vegetation types, gorilla subpopulation growth and associated social structure on helminth infections. We revealed striking geographic differences in strongylid infections with higher egg counts mostly in areas with high occurrences of gastrointestinal disease. Increased helminth egg counts were also associated with decreasing group size in some areas. Observed spatial differences may reflect mutual effects of variations in subpopulation growth rates, gorilla social structure, and vegetation associated with altitude across mountain gorilla habitat. Helminth infection intensities in Virunga gorillas were lowest in the youngest and the oldest animals. Elucidating parasite infection patterns of endangered species with low genetic diversity is crucial for their conservation management.

Centre de Recherche en Sciences Naturelles de Lwiro Lwiro Democratic Republic of Congo

Department of Botany and Zoology Faculty of Science Masaryk University Brno Czech Republic

Department of Pathology and Parasitology Faculty of Veterinary Medicine University of Veterinary Sciences Brno Brno Czech Republic

Department of Physical Geography and Geoecology Faculty of Science Charles University Prague Czech Republic

Department of Veterinary Medicine Università degli Studi di Milano Milan Italy

Dian Fossey Gorilla Fund Musanze Rwanda

Gorilla Doctors Davis CA USA

Institut Congolais pour la Conservation de la Nature Kinshasa Democratic Republic of Congo

Institut Congolais pour la Conservation de la Nature Parc National de Kahuzi Biega Bukavu Democratic Republic of Congo

Institute of Parasitology Biology Centre The Czech Academy of Sciences Ceske Budejovice Czech Republic

Institute of Vertebrate Biology The Czech Academy of Sciences Brno Czech Republic

Liberec Zoo Liberec Czech Republic

Lwiro Primate Rehabilitation Center Democratic Republic of Congo and Ivan Carter Wildlife Conservation Alliance Orlando FL USA

Research Center Epidemiology and Molecular Surveillance of Infections ''EpiSoMI'' Università degli Studi di Milano Milan Italy

Rwanda Development Board Kigali Rwanda

School of Veterinary Medicine University of California Davis Davis CA USA

Sydney School of Veterinary Science Faculty of Science University of Sydney Sydney Australia

Uganda Wildlife Authority Kampala Uganda

Zobrazit více v PubMed

Weber AW, Vedder A. Population dynamics of the Virunga gorillas: 1959–1978. Biol. Conserv. 1983;26:341–366. doi: 10.1016/0006-3207(83)90096-4. DOI

Granjon A-C, et al. Estimating abundance and growth rates in a wild mountain gorilla population. Anim. Conserv. 2020;23:455–465. doi: 10.1111/acv.12559. DOI

Gray M, et al. Virunga Massif Mountain Gorilla Census—2010 Summary Report. IGCP & Partners; 2010.

Gray M, et al. Genetic census reveals increased but uneven growth of a critically endangered mountain gorilla population. Biol. Conserv. 2013;158:230–238. doi: 10.1016/j.biocon.2012.09.018. DOI

Robbins MM, et al. Extreme conservation leads to recovery of the Virunga mountain gorillas. PLoS One. 2011;6:e19788. doi: 10.1371/journal.pone.0019788. PubMed DOI PMC

Hickey JR, Granjon A-C, Vigilant L. Virunga 2015–2016 Surveys: Monitoring Mountain Gorillas, Other Select Mammals, and Illegal Activities. IGCP & Partners; 2019.

Kalpers J, et al. Gorillas in the crossfire: Population dynamics of the Virunga mountain gorillas over the past three decades. Oryx. 2003;37:326–337. doi: 10.1017/S0030605303000589. DOI

Robbins MM, Gray M, Kagoda E, Robbins AM. Population dynamics of the Bwindi mountain gorillas. Biol. Conserv. 2009;142:2886–2895. doi: 10.1016/j.biocon.2009.07.010. DOI

Hickey JR, Uzabaho E, Akantorana M. Bwindi-Sarambwe EM 2018 Surveys: Monitoring Mountain Gorillas, Other Select Mammals, and Human Activities. GVTC, IGCP & Partners; 2019. p. 40.

Roy J, et al. Challenges in the use of genetic mark-recapture to estimate the population size of Bwindi mountain gorillas (Gorilla beringei beringei) Biol. Conserv. 2014;180:249–261. doi: 10.1016/j.biocon.2014.10.011. DOI

McNeilage AJ. Mountain Gorillas in the Virunga Volcanoes: Ecology and Carrying Capacity. University of Bristol; 1995.

Caillaud D, Ndagijimana F, Giarrusso AJ, Vecellio V, Stoinski TS. Mountain gorilla ranging patterns: Influence of group size and group dynamics. Am. J. Primatol. 2014;76:730–746. doi: 10.1002/ajp.22265. PubMed DOI

Caillaud D, et al. Violent encounters between social units hinder the growth of a high-density mountain gorilla population. Sci. Adv. 2020;6:eaba0724. doi: 10.1126/sciadv.aba0724. PubMed DOI PMC

Watts DP. Causes and consequences of variation in male mountain gorilla life histories and group membership. In: Kappeler PM, editor. Primate Males. Cambridge University Press; 2000. pp. 169–179.

Robbins MM, Robbins AM, Gerald-Steklis N, Steklis HD. Socioecological influences on the reproductive success of female mountain gorillas (Gorilla beringei beringei) Behav. Ecol. Sociobiol. 2007;61:919–931. doi: 10.1007/s00265-006-0321-y. DOI

Robbins AM, et al. Impact of male Infanticide on the social structure of mountain gorillas. PLoS One. 2013;8:e78256. doi: 10.1371/journal.pone.0078256. PubMed DOI PMC

Grueter CC, et al. Quadratic relationships between group size and foraging efficiency in a herbivorous primate. Sci. Rep. 2018;8:16718. doi: 10.1038/s41598-018-35255-0. PubMed DOI PMC

Eckardt W, Stoinski TS, Rosenbaum S, Santymire R. Social and ecological factors alter stress physiology of Virunga mountain gorillas (Gorilla beringei beringei) Ecol. Evol. 2019;9:5248–5259. doi: 10.1002/ece3.5115. PubMed DOI PMC

Harcourt AH, Parks SA, Woodroffe R. Human density as an influence on species/area relationships: Double jeopardy for small African reserves? Biodivers. Conserv. 2001;10:1011–1026. doi: 10.1023/A:1016680327755. DOI

Citterio CV, et al. Abomasal nematode community in an alpine chamois (Rupicapra r. rupicapra) population before and after a die-off. J. Parasitol. 2006;92:918–927. doi: 10.1645/GE-3551.1. PubMed DOI

Hudson PJ. Macroparasites: Observed patterns. Ecol. Infect. Dis. Nat. Popul. 1995;20:144–176.

Albon SD, et al. The role of parasites in the dynamics of a reindeer population. Proc. R. Soc. Lond. B Biol. Sci. 2002;269:1625–1632. doi: 10.1098/rspb.2002.2064. PubMed DOI PMC

Anderson RM, May RM. Age-related changes in the rate of disease transmission: Implications for the design of vaccination programmes. Epidemiol. Infect. 1985;94:365–436. PubMed PMC

Lloyd-Smith JO, Schreiber SJ, Kopp PE, Getz WM. Superspreading and the effect of individual variation on disease emergence. Nature. 2005;438:355–359. doi: 10.1038/nature04153. PubMed DOI PMC

Anderson RM, May RM. Regulation and stability of host-parasite population interactions: I. Regulatory processes. J. Anim. Ecol. 1978;47:219–247. doi: 10.2307/3933. DOI

Arneberg P, Skorping A, Grenfell B, Read AF. Host densities as determinants of abundance in parasite communities. Proc. R. Soc. Lond. B Biol. Sci. 1998;265:1283–1289. doi: 10.1098/rspb.1998.0431. DOI

Gillespie TR, Chapman CA. Forest fragmentation, the decline of an endangered primate, and changes in host–parasite interactions relative to an unfragmented forest. Am. J. Primatol. 2008;70:222–230. doi: 10.1002/ajp.20475. PubMed DOI

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. doi: 10.1111/j.1365-2656.2008.01481.x. PubMed DOI

dos Santos CN, et al. Seasonal dynamics of cyathostomin (Nematoda–Cyathostominae) infective larvae in Brachiaria humidicola grass in tropical southeast Brazil. Vet. Parasitol. 2011;180:274–278. doi: 10.1016/j.vetpar.2011.03.026. PubMed DOI

Silangwa SM, Todd AC. Vertical migration of trichostrongylid larvae on grasses. J. Parasitol. 1964;50:278–285. doi: 10.2307/3276286. PubMed DOI

Callinan APL, Westcott JM. Vertical distribution of trichostrongylid larvae on herbage and in soil. Int. J. Parasitol. 1986;16:241–244. doi: 10.1016/0020-7519(86)90050-0. PubMed DOI

Crofton HD. The ecology of immature phases of trichostrongyle nematodes: II. The effect of climatic factors on the availability of the infective larvae of Trichostrongylus retortaeformis to the host. Parasitology. 1948;39:26–38. doi: 10.1017/S0031182000083529. PubMed DOI

Zanet S, et al. Higher risk of gastrointestinal parasite infection at lower elevation suggests possible constraints in the distributional niche of Alpine marmots. PLoS One. 2017;12:e0182477. doi: 10.1371/journal.pone.0182477. PubMed DOI PMC

Derek Scasta J. Livestock parasite management on high-elevation rangelands: Ecological interactions of climate, habitat, and wildlife. J. Integr. Pest Manag. 2015;6:20. doi: 10.1093/jipm/pmv008. DOI

Huffman MA, Gotoh S, Turner LA, 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. doi: 10.1007/BF02382002. DOI

MacIntosh AJJ, Hernandez AD, Huffman MA. Host age, sex, and reproductive seasonality affect nematode parasitism in wild Japanese macaques. Primates. 2010;51:353–364. doi: 10.1007/s10329-010-0211-9. PubMed DOI

Pafčo B, et al. 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. doi: 10.1007/s00436-017-5667-8. PubMed DOI

Rothman JM, Pell AN, Bowman DD. Host-parasiteecology of the helminths in mountain gorillas. J. Parasitol. 2008;94:834–840. doi: 10.1645/GE-1454.1. PubMed DOI

Müller-Graf CDM, Collins DA, Woolhouse MEJ. Intestinal parasite burden in five troops of olive baboons (Papio cynocephalus anubis) in Gombe Stream National Park, Tanzania. Parasitology. 1996;112:489–497. doi: 10.1017/S0031182000076952. PubMed DOI

Alexander J, Stimson WH. Sex hormones and the course of parasitic infection. Parasitol. Today. 1988;4:189–193. doi: 10.1016/0169-4758(88)90077-4. DOI

Bundy DAP. Gender-dependent patterns of infections and disease. Parasitol. Today. 1988;4:186–189. doi: 10.1016/0169-4758(88)90076-2. PubMed DOI

Zuk M. Reproductive strategies and disease susceptibility: An evolutionary viewpoint. Parasitol. Today. 1990;6:231–233. doi: 10.1016/0169-4758(90)90202-F. PubMed DOI

Nunn C, Altizer S. Infectious Diseases in Primates: Behavior. Oxford: Ecology and Evolution. Oxford University Press; 2006.

Wilson, K. et al. Heterogeneities in macroparasite infections: Patterns and processes. In The Ecology of Wildlife Diseases 6–44 (2002).

Cattadori IM, Boag B, Bjørnstad ON, Cornell SJ, Hudson PJ. Peak shift and epidemiology in a seasonal host–nematode system. Proc. R. Soc. B Biol. Sci. 2005;272:1163–1169. doi: 10.1098/rspb.2004.3050. PubMed DOI PMC

Terio KA, et al. Oesophagostomiasis in non-human primates of Gombe National Park, Tanzania. Am. J. Primatol. 2018;80:e22572. doi: 10.1002/ajp.22572. PubMed DOI PMC

Gillespie TR, Nunn CL, Leendertz FH. Integrative approaches to the study of primate infectious disease: Implications for biodiversity conservation and global health. Am. J. Phys. Anthropol. 2008;137:53–69. doi: 10.1002/ajpa.20949. PubMed DOI

Collett MG, et al. Gastric Ollulanus tricuspis infection identified in captive cheetahs (Acinonyx jubatus) with chronic vomiting: Case report. J. S. Afr. Vet. Assoc. 2000;71:251–255. PubMed

Dennis MM, Bennett N, Ehrhart EJ. Gastric adenocarcinoma and chronic gastritis in two related Persian cats. Vet. Pathol. 2006;43:358–362. doi: 10.1354/vp.43-3-358. PubMed DOI

Smetana HF, Orihel TC. Gastric papillomata in Macaca speciosa induced by Nochtia nochti (Nematoda: Trichostrongyloidea) J. Parasitol. 1969;55:349–351. doi: 10.2307/3277407. PubMed DOI

Nybelin O. Anoplocephala gorillae n. sp. Ark Zool. 1924;19:1–3.

Sleeman JM, Meader LL, Mudakikwa AB, Foster JW, Patton S. Gastrointestinal parasites of mountain gorillas (Gorilla gorilla beringei) in the Parc National des Volcans, Rwanda. J. Zool. Wildl. Med. 2000;31:322–328. doi: 10.1638/1042-7260(2000)031[0322:GPOMGG]2.0.CO;2. PubMed DOI

Ashford RW, Lawson H, Butynski TM, Reid GDF. Patterns of intestinal parasitism in the mountain gorilla Gorilla gorilla in the Bwindi-Impenetrable Forest, Uganda. J. Zool. 1996;239:507–514. doi: 10.1111/j.1469-7998.1996.tb05939.x. DOI

Kalema-Zikusoka G, Rothman JM, Fox MT. Intestinal parasites and bacteria of mountain gorillas (Gorilla beringei beringei) in Bwindi Impenetrable National Park, Uganda. Primates. 2005;46:59–63. doi: 10.1007/s10329-004-0103-y. PubMed DOI

Owiunji, I, et al. The biodiversity of the Virunga Volcanoes. https://programs.wcs.org/portals/49/media/file/volcanoes_biodiv_survey.pdf (2005).

Langdale-Brown I, Osmaston H, Wilson JG. The Vegetation of Uganda and Its Bearing on Land-Use. Governmentt of Uganda; 1964.

Ashford RW, Reid GDF, Butynski TM. The intestinal faunas of man and mountain gorillas in a shared habitat. Ann. Trop. Med. Parasitol. 1990;84:337–340. doi: 10.1080/00034983.1990.11812477. PubMed DOI

Shutt K, et al. 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. doi: 10.1016/j.biocon.2014.02.014. DOI

Kayiranga A, et al. 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. doi: 10.3390/geosciences7010017. DOI

Cousins D, Huffman MA. Medicinal properties in the diet of gorillas: An ethno-phramacological evaluation. Afr. Stud. Monogr. 2002;23:65–89.

Woolhouse MEJ. Patterns in parasite epidemiology: The peak shift. Parasitol. Today. 1998;14:428–434. doi: 10.1016/S0169-4758(98)01318-0. PubMed DOI

Hayes KS, Bancroft AJ, Grencis RK. Immune-mediated regulation of chronic intestinal nematode infection. Immunol. Rev. 2004;201:75–88. doi: 10.1111/j.0105-2896.2004.00193.x. PubMed DOI

Maizels RM, et al. Helminth parasites—masters of regulation. Immunol. Rev. 2004;201:89–116. doi: 10.1111/j.0105-2896.2004.00191.x. PubMed DOI

Proudman CJ, Holmes MA, Sheoran AS, Edwards SER, Trees AJ. Immunoepidemiology of the equine tapeworm Anoplocephala perfoliata: Age-intensity profile and age-dependency of antibody subtype responses. Parasitology. 1997;114:89–94. doi: 10.1017/S0031182096008086. PubMed DOI

Gergócs V, Garamvölgyi Á, Homoródi R, Hufnagel L. Seasonal change of oribatid mite communities (Acari, Oribatida) in three different types of microhabitats in an oak forest. Appl. Ecol. Environ. Res. 2011;9:181–195. doi: 10.15666/aeer/0902_181195. DOI

Dobson A, Foufopoulos J. Emerging infectious pathogens of wildlife. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 2001;356:1001–1012. doi: 10.1098/rstb.2001.0900. PubMed DOI PMC

Xue Y, et al. Mountain gorilla genomes reveal the impact of long-term population decline and inbreeding. Science. 2015;348:242–245. doi: 10.1126/science.aaa3952. PubMed DOI PMC

Reed DH, Frankham R. Correlation between fitness and genetic diversity. Conserv. Biol. 2003;17:230–237. doi: 10.1046/j.1523-1739.2003.01236.x. DOI

Pafčo B, et al. Metabarcoding analysis of strongylid nematode diversity in two sympatric primate species. Sci. Rep. 2018;8:5933. doi: 10.1038/s41598-018-24126-3. PubMed DOI PMC

McNeilage A. Mountain Gorillas: Three Decades of Research at Karisoke. Cambridge University Press; 2001. Diet and habitat use of two mountain gorilla groups in contrasting habitats in the Virunga.

Sinayitutse E, et al. Daily defecation outputs of mountain gorillas (Gorilla beringei beringei) in the Volcanoes National Park, Rwanda. Primates. 2020 doi: 10.1007/s10329-020-00874-7. PubMed DOI

Burgunder J, et al. Complexity in behavioural organization and strongylid infection among wild chimpanzees. Anim. Behav. 2017;129:257–268. doi: 10.1016/j.anbehav.2017.06.002. DOI

Chapman CA, Speirs ML, Gillespie TR, Holland T, Austad KM. Life on the edge: Gastrointestinal parasites from the forest edge and interior primate groups. Am. J. Primatol. 2006;68:397–409. doi: 10.1002/ajp.20233. PubMed DOI

Anderson RM, Schad GA. Hookworm burdens and faecal egg counts: An analysis of the biological basis of variation. Trans. R. Soc. Trop. Med. Hyg. 1985;79:812–825. doi: 10.1016/0035-9203(85)90128-2. PubMed DOI

Warnick LD. Daily variability of equine fecal strongyle egg counts. Cornell Vet. 1992;82:453–463. PubMed

Tomczuk K, et al. Comparison of the sensitivity of coprological methods in detecting Anoplocephala perfoliata invasions. Parasitol. Res. 2014;113:2401–2406. doi: 10.1007/s00436-014-3919-4. PubMed DOI PMC

Williamson R, Beveridge I, Gasser R. Coprological methods for the diagnosis of Anoplocephala perfoliata infection of the horse. Aust. Vet. J. 1998;76:618–621. doi: 10.1111/j.1751-0813.1998.tb10242.x. PubMed DOI

Cringoli G, et al. The Mini-FLOTAC technique for the diagnosis of helminth and protozoan infections in humans and animals. Nat. Protoc. 2017;12:1723–1732. doi: 10.1038/nprot.2017.067. PubMed DOI

Guschanski K, et al. Counting elusive animals: Comparing field and genetic census of the entire mountain gorilla population of Bwindi Impenetrable National Park, Uganda. Biol. Conserv. 2009;142:290–300. doi: 10.1016/j.biocon.2008.10.024. DOI

Zuur A, Ieno EN, Walker N, Saveliev AA, Smith GM. Mixed Effects Models and Extensions in Ecology with R. Springer; 2009.

Bates D, Mächler M, Bolker B, Walker S. Fitting linear mixed-effects models using lme4. J. Stat. Softw. 2015;67:1–48. doi: 10.18637/jss.v067.i01. DOI

R Core Team. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/ (2020).

Forstmeier W, Schielzeth H. Cryptic multiple hypotheses testing in linear models: Overestimated effect sizes and the winner’s curse. Behav. Ecol. Sociobiol. 2011;65:47–55. doi: 10.1007/s00265-010-1038-5. PubMed DOI PMC

Engqvist L. The mistreatment of covariate interaction terms in linear model analyses of behavioural and evolutionary ecology studies. Anim. Behav. 2005;70:20. doi: 10.1016/j.anbehav.2005.01.016. DOI

Gelman A, Hill J. Data Analysis Using Regression and Multilevel/Hierarchical Models. Cambridge University Press; 2007.

Schielzeth H. Simple means to improve the interpretability of regression coefficients. Methods Ecol. Evol. 2010;1:103–113. doi: 10.1111/j.2041-210X.2010.00012.x. DOI

Johnson JB, Omland KS. Model selection in ecology and evolution. Trends Ecol. Evol. 2004;19:101–108. doi: 10.1016/j.tree.2003.10.013. PubMed DOI

Burnham KP, Anderson DR. Model Selection and Multimodel Inference: A Practical Information-Theoretic Approach. Springer; 2002.

Barton, K. MuMIn: Multi-Model Inference. R package version 1.43.17. https://CRAN.R-project.org/package=MuMIn (2020).

Anoplocephalid tapeworms in mountain gorillas (Gorilla beringei beringei) inhabiting the Volcanoes National Park, Rwanda

High diversity and sharing of strongylid nematodes in humans and great apes co-habiting an unprotected area in Cameroon

Ecological drivers of helminth infection patterns in the Virunga Massif mountain gorilla population

Association of human disturbance and gastrointestinal parasite infection of yellow baboons in western Tanzania