, Volume 12, Issue 4, pp 621–633 | Cite as

Intestinal Helminths of Wild Bonobos in Forest-Savanna Mosaic: Risk Assessment of Cross-Species Transmission with Local People in the Democratic Republic of the Congo

  • Victor Narat
  • Jacques Guillot
  • Flora Pennec
  • Sophie Lafosse
  • Anne Charlotte Grüner
  • Bruno Simmen
  • Jean Christophe Bokika Ngawolo
  • Sabrina Krief
Original Contribution


Phylogenetic and geographic proximities between humans and apes pose a risk of zoonotic transmission of pathogens. Bonobos (Pan paniscus) of the Bolobo Territory, Democratic Republic of the Congo, live in a fragmented forest-savanna mosaic setting, a marginal habitat for this species used to living in dense forests. Human activities in the forest have increased the risk of contacts between humans and bonobos. Over 21 months (September 2010–October 2013), we monitored intestinal parasites in bonobo (n = 273) and in human (n = 79) fecal samples to acquire data on bonobo parasitology and to assess the risk of intestinal helminth transmission between these hosts. Coproscopy, DNA amplification, and sequencing of stored dried feces and larvae were performed to identify helminths. Little difference was observed in intestinal parasites of bonobos in this dryer habitat compared to those living in dense forests. Although Strongylids, Enterobius sp., and Capillaria sp. were found in both humans and bonobos, the species were different between the hosts according to egg size or molecular data. Thus, no evidence of helminth transmission between humans and bonobos was found. However, because humans and this threatened species share the same habitat, it is essential to continue to monitor this risk.


parasitology intestinal helminths zoonosis bonobos DRC 



We thank the Ministère de l’Environnement, Conservation de la Nature et Tourism for research permission, the Mbou-Mon-Tour NGO and traditional chiefs for authorization to conduct this work. Acknowledgements for fundings are due to the Action Transversale du Muséum “Relations Sociétés-Nature dans le long terme” and the UMR7206. This study would not have been possible without the field assistants Blanchard Bongwana, Osa Otsiu Epany, Mozungo Ngofuna and Debaba Munziu. We also thank all members of Mbou-Mon-Tour for their implication/contribution in the bonobo conservation. Special thanks to Adélaïde Nieguitshila, Emilie Lefoulon and Laure Ségurel for their advice on the genetic data, to Radia Guechi for his help with coproscopy analyses. Finally we thank the two anonymous reviewers for their useful comments to improve the manuscript.

Supplementary material

10393_2015_1058_MOESM1_ESM.docx (62 kb)
Supplementary material 1 (DOCX 62 kb)


  1. Baker DG (2007) Flynn’s Parasites of Laboratory Animals, 2nd ed., Ames, IA: Blackwell Publishing. doi: 10.1002/9780470344552. [Online January 30, 2008]. Accessed Jan 8, 2014.
  2. Brooks DR, Glen DR (1982) Pinworms and primates: a case study in coevolution. Proceedings of the Helminthological Society of Washington 49(1):76–85. Accessed Dec 10, 2012.
  3. Bwangoy JRB, Hansen MC, Roy DP, Grandi GD, Justice CO (2010) Wetland mapping in the Congo Basin using optical and radar remotely sensed data and derived topographical indices. Remote Sensing of Environment 114(1):73–86. doi: 10.1016/j.rse.2009.08.004. Accessed July 29, 2015.
  4. Cameron TW (1929) The species of Enterobius Leach, in Primates. Journal of Helminthology 7(3):161–182. doi: 10.1017/S0022149X00018770. [Online June 5, 2009]. Accessed Jan 7, 2013.
  5. Chapman CA, Gillespie TR, Goldberg TL (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. doi: 10.1002/evan.20068. [Online August 25, 2005]. Accessed August 24, 2012.
  6. Dupain J, Garia P, Nell C, Van Elsacker L, Ponce F (2000) A survey of intestinal parasites of a sympatric population of bonobo (Pan paniscus) and humans (Homo sapiens) in the Democratic Republic of Congo. 6th Congress of the German Primate Society. Folia primatologica 71(4):222; doi: 10.1159/000021748. Accessed Nov 24, 2011.
  7. Dupain J, Nell C, Petrzelkova KJ, Garcia P, Modry D, Gordo FP (2009) Gastrointestinal parasites of bonobos in the Lomako Forest, Democratic Republic of Congo. In: Primate Parasite Ecology. The Dynamic and Study of Host-Parasite Relationship, Huffman MA, Chapman CA (editors), New York, NY: Cambridge University Press, pp 297–310. Accessed Nov 7, 2011.
  8. Ferber D (2000) Human diseases threaten great apes. Science 289(5483):1277–1278. doi: 10.1126/science.289.5483.1277. Accessed August 24, 2012.
  9. Fuehrer HP, Igel P, Auer H (2011) Capillaria hepatica in man—an overview of hepatic capillariosis and spurious infections. Parasitology Research 109(4):969–979. doi: 10.1007/s00436-011-2494-1. [Online June 30, 2011]. Accessed Dec 4, 2012.
  10. Gasser RB, Woods WG, Huffman MA, Blotkamp J, Polderman AM (1999) Molecular separation of Oesophagostomum stephanostomum and Oesophagostomum bifurcum (Nematoda: Strongyloidea) from non-human primates. International Journal for Parasitology 29(7):1087–1091. Accessed Jan 8, 2013.
  11. Ghai RR, Chapman CA, Omeja PA, Davies TJ, Goldberg TL (2014) Nodule worm infection in humans and wild primates in Uganda: cryptic species in a newly identified region of human transmission. PLoS Neglected Tropical Diseases 8(1):e2641. doi: 10.1371/journal.pntd.0002641. [Online January 9, 2014]. Accessed Feb 3, 2014.
  12. Goldberg TL (2008) Forest fragmentation as cause of bacterial transmission among nonhuman primates, humans, and livestock, Uganda. Emerging Infectious Diseases 14(9):1375–1382. doi: 10.3201/eid14.9.071196. Accessed Feb 17, 2014.
  13. Goldberg TL, Gillespie TR, Rwego IB, Wheeler E, Estoff EL, Chapman CA (2007) Patterns of gastrointestinal bacterial exchange between chimpanzees and humans involved in research and tourism in western Uganda. Biological Conservation 135(4):511–517. doi: 10.1016/j.biocon.2006.10.048. Accessed Feb 25, 2014.
  14. Greiner and McIntosh (2009) Collection methods and diagnostic procedures for primate parasitology. In: Primate Parasite Ecology. The Dynamic and Study of Host-Parasite Relationships, Huffman MA, Chapman CA (editors), New York, NY: Cambridge University Press, pp 29–46. Accessed Nov 7, 2011.
  15. Graczyk TK, Lowenstine LJ, Cranfield MR (1999) Capillaria hepatica (Nematoda) infections in human-habituated mountain gorillas (Gorilla gorilla beringei) of the Parc National des Volcans, Rwanda. The Journal of Parasitology 85(6):1168–1170. Accessed August 24, 2012.
  16. Guillot J, Vermeulen B, Lafosse S, Chauffour S, Cibot M, Narat V, Masi S, Nieguitsila A, Snounou G, Bain O, Krief S (2012) Nematodes of the genus Oesophagostomum: an emerging risk for humans and apes in Africa? Bulletin de l’Académie nationale de médecine 195(8):1955–1963. Accessed Nov 13, 2012.
  17. Hasegawa H (2009) Methods of collection and identification of minute nematodes from the feces of primates, with special applications to coevolutionnary study of pinworms. In: Primate Parasite Ecology. The Dynamic and Study of Host-Parasite Relationships, Huffman MA, Chapman CA (editors), New York, NY: Cambridge University Press, pp 29–46. Accessed Nov 7, 2011.
  18. Hasegawa H, Ikeda Y, Fujisaki A, Moscovice LR, Petrzelkova KJ, Kaur T, Huffman MA (2005) Morphology of chimpanzee pinworms, Enterobius (enterobius) anthropopitheci (Gedoelst, 1916)(Nematoda: Oxyuridae), collected from chimpanzees, Pan troglodytes, on Rubondo island, Tanzania. Journal of Parasitology 91(6):1314–1317. doi: 10.1645/GE-569R.1. Accessed Dec 14, 2012.
  19. Hasegawa H, Kano T, Mulavwa M (1983) A parasitological survey on the feces of pygmy chimpanzees, Pan paniscus, at Wamba, Zaïre. Primates 24(3):419–423. doi: 10.1007/BF02381986. Accessed Dec 6, 2011.
  20. Hasegawa H, Modrý D, Kitagawa M, Shutt KA, Todd A, Kalousová B, Profousová I, Petrželková KJ (2014) Humans and great apes cohabiting the forest ecosystem in Central African Republic Harbour the Same Hookworms. PLoS Neglected Tropical Diseases 8(3):e2715. doi: 10.1371/journal.pntd.0002715. [Online March 20, 2014]. Accessed May 5, 2014.
  21. Hasegawa H, Udono T (2007) Chimpanzee pinworm, Enterobius anthropopitheci (Nematoda: Oxyuridae), maintained for more than twenty years in captive chimpanzees in Japan. Journal of Parasitology 9(4)3:850–853. Accessed Dec 14, 2012.
  22. Hasegawa H, Sato H, Fujita S, Nguema PPM, Nobusue K, Miyagi K, Kooriyama T, Takenoshita Y, Noda S, Sato A, Morimoto A, Ikeda Y, Nishida T (2010) Molecular identification of the causative agent of human strongyloidiasis acquired in Tanzania: dispersal and diversity of Strongyloides spp. and their hosts. Parasitology International 59(3):407–413. doi: 10.1016/j.parint.2010.05.007. Accessed August 22, 2014.
  23. Hercberg S, Chauliac M, Galan P, Devanlay M, Zohoun I, Agboton Y, Soustre Y, Bories C, Christides JP, Potier de CG (1986) Relationship between anaemia, iron and folacin deficiency, haemoglobinopathies and parasitic infection. Human Nutrition. Clinical Nutrition 40(5):371–379. Accessed May 25, 2010.
  24. Howells ME, Pruetz J, Gillespie TR (2011) 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. American Journal of Primatology 73(2):173–179. doi: 10.1002/ajp.20884. Accessed April 16, 2012.
  25. Hugot JP (1993) Redescription of Enterobius anthropopitheci (Gedoelst, 1916) (Nematoda, Oxyurida), a parasite of chimpanzees. Systematic Parasitology 26(3): 201–207. doi: 10.1007/BF00009727. Accessed Jan 7, 2013.
  26. Hugot JP (1999) Primates and their pinworm parasites: the Cameron hypothesis revisited. Systematic Biology 48(3):523–546. doi: 10.1080/106351599260120. Accessed Dec 14, 2012.
  27. Hugot JP, Reinhard KJ, Gardner SL, Morand S (1999) Human enterobiasis in evolution: origin, specificity and transmission. Parasite 6(3) 201–208. Accessed Feb 6, 2014.
  28. Inglis WG (1961) The oxyurid parasites (nematoda) of primates. Proceedings of the Zoological Society of London 136(1):103–122. doi: 10.1111/j.1469-7998.1961.tb06081.x. [Online August 20, 2009]. Accessed Feb 19, 2014.
  29. Inogwabini BI, Bewa M, Longwango M, Abokome M, Vuvu M (2008) The bonobos of the lake Tumba—lake Maindombe hinterland: threats and opportunities for population conservation. In: The Bonobos: Behaviour, Ecology and Conservation, Furuichi T and Thompson J (editors), New York, NY: Springer editions, pp 273–290. Accessed Dec 6, 2011.
  30. IUCN and ICCN (2012). Bonobo (Pan paniscus): Conservation Strategy 2012–2022. Gland, Switzerland: IUCN/SSC Primate Specialist Group & Institut Congolais pour la Conservation de la Nature. Accessed Dec 24, 2012.
  31. Justine JL (1988) Capillaria brochieri n. sp. (Nematoda: Capillariinae) intestinal parasite of the chimpanzee (Pan paniscus) in Zaire. Annales de parasitologie humaine et comparée 63(6):420–438. Accessed Dec 6, 2011.
  32. Kalousová B, Piel AK, Pomajbíková K, Modrý D, Stewart FA, Petrželková KJ (2014) Gastrointestinal Parasites of Savanna Chimpanzees (Pan troglodytes schweinfurthii) in Ugalla, Tanzania. International Journal of Primatology 35(2):463–475. doi: 10.1007/s10764-014-9753-9. [Online March 8, 2014]. Accessed March 17, 2014.
  33. Kawamoto Y, Takemoto H, Higuchi S, Sakamaki T, Hart JA, Hart TB, Tokuyama N, Reinartz GE, Guislain P, Dupain J, Cobden AK, Mulavwa MN, Yangozene K, Darroze S, Devos C, Furuichi T (2013) Genetic structure of wild Bonobo populations: diversity of mitochondrial DNA and geographical distribution. PLoS ONE 8(3):e59660. doi: 10.1371/journal.pone.0059660. [Online March 27, 2013]. Accessed Feb 6, 2014.
  34. Kaur T, Singh J (2009) Primate-parasitic zoonoses and anthopozoonoses: a literature review. In: Primate Parasite Ecology. The Dynamic and Study of Host-Parasite Relationships, Huffman MA, Chapman CA (editors), New York, NY: Cambridge University Press, pp 199–230. Accessed Nov 7, 2011.
  35. Köndgen S, Kühl H, N’Goran PK, Walsh PD, Schenk S, Ernst N, Biek R, Formenty P, Mätz-Rensing K, Schweiger B, Junglen S, Ellerbrok H, Nitsche A, Briese T, Lipkin WI, Pauli G, Boesch C, Leendertz FH (2008) Pandemic human viruses cause decline of endangered great apes. Current Biology 18(4):260–264. doi: 10.1016/j.cub.2008.01.012. [Online February 26, 2008]. Accessed Jan 7, 2014.
  36. Krief S, Jamart A, Mahé S, Leendertz FH, Mätz-Rensing K, Crespeau F, Bain O, Guillot J (2008) Clinical and pathologic manifestation of oesophagostomosis in African great apes: does self-medication in wild apes influence disease progression? Journal of Medical Primatology 37(4):188–195. doi: 10.1111/j.1600-0684.2008.00285.x. [Online March 10, 2008]. Accessed Nov 11, 2011.
  37. Krief S, Huffman MA, Sévenet T, Guillot J, Bories C, Hladik CM, Wrangham RW (2005) Noninvasive Monitoring of the Health of Pan troglodytes schweinfurthii in the Kibale National Park, Uganda. International Journal of Primatology 26(2):467–490. doi: 10.1007/s10764-005-2934-9. [Online April 1, 2005]. Accessed Jan 21, 2011.
  38. Krief S, Vermeulen B, Lafosse S, Kasenene JM, Nieguitsila A, Berthelemy M, L’Hostis M, Bain O, Guillot J (2010) Nodular worm infection in wild chimpanzees in western uganda: a risk for human health? PLoS Neglected Tropical Diseases 4(3):e630. doi: 10.1371/journal.pntd.0000630. [Online March 16, 2010]. Accessed Nov 4, 2011.
  39. Masi S, Chauffour S, Bain O, Todd A, Guillot J, Krief S (2012) Seasonal effects on great ape health: a case study of wild chimpanzees and western gorillas. PLoS ONE 7(12):e49805. doi: 10.1371/journal.pone.0049805. [Online December 5, 2012]. Accessed Dec 5, 2012.
  40. Mclennan MR, Huffman MA (2012) High Frequency of Leaf Swallowing and its Relationship to Intestinal Parasite Expulsion in “Village” Chimpanzees at Bulindi, Uganda. American Journal of Primatology 74(7):642–650. doi: 10.1002/ajp.22017. [Online May 29, 2012]. Accessed Nov 7, 2012.
  41. Murata K, Hasegawa H, Nakano T, Noda A, Yanai T (2002) Fatal infection with human pinworm, Enterobius vermicularis, in a captive chimpanzee. Journal of Medical Primatology 31(2):104–108. doi: 10.1034/j.1600-0684.2002.01017.x. [Online June 25, 2002]. Accessed Dec 14, 2012.
  42. Narat V, Cibot M, Bokika Ngawolo JC, Dumez R, Krief S (2012) Etude préliminaire de l’influence des disponibilités alimentaires et des activités humaines sur l’utilisation spatiale de l’habitat par les chimpanzés et les bonobos. Revue de primatologie 4. doi: 10.4000/primatologie.1121. Accessed Jan 25, 2013.
  43. Narat V, Pennec F, Krief S, Ngawolo JCB, Dumez R (2015b) Conservation communautaire et changement de statuts du bonobo dans le Territoire de Bolobo: Animal juridique, économique et écologique. Revue d’ethnoécologie (7) [Online]. doi: 10.4000/ethnoecologie.2206. Accessed July 13, 2015.
  44. Narat V, Pennec F, Simmen B, Ngawolo JCB, Krief S (2015a) Bonobo habituation in a forest–savanna mosaic habitat: influence of ape species, habitat type, and sociocultural context. Primates [Online first]. doi: 10.1007/s10329-015-0476-0. Accessed July 14, 2015.
  45. Neveu-Lemaire M (1917) Contribution à l’étude des organs reproducteurs et de la reproduction chez les strangles dépourvus de capsule buccale (Metastrongiliddae). Mémoires de la société zoologique de France 27. Accessed August 22, 2014.
  46. Nsubuga AM, Robbins MM, Roeder AD, Morin PA, Boesch C, Vigilant L (2004) Factors affecting the amount of genomic DNA extracted from ape faeces and the identification of an improved sample storage method: getting more DNA from faeces. Molecular Ecology 13(7):2089–2094. doi: 10.1111/j.1365-294X.2004.02207.x. [Online May 20, 2004]. Accessed Dec 12, 2011.
  47. Nunn C, Altizer S. (2006) Infectious Disease and Primate Sociecology. Oxford: Oxford University Press. Accessed August 24, 2014.
  48. Orihel TC (1971) Necator americanus Infection in Primates. The Journal of Parasitology 57(1):117–121. Accessed August 22, 2014.
  49. Pedersen AB, Davies TJ (2010) Cross-species pathogen transmission and disease emergence in primates. EcoHealth 6(4):496–508. doi: 10.1007/s10393-010-0284-3. [Online December 1, 2009]. Accessed Dec 2, 2013.
  50. Pit DSS, De Graaf W, Snoek H, De Vlas SJ, Baeta SM, Polderman AM (1999) Diagnosis of Oesophagostomum bifurcum and hookworm infection in humans: day-to-day and within-specimen variation in larval counts. Parasitology 118(3):283–288. Accessed Jan 9, 2014.
  51. Polderman AM, Blotkamp J (1995) Oesophagostomum infections in humans. Parasitology today 11(12):451–455. doi: 10.1016/0169-4758(95)80058-1. Accessed Jan 8, 2013.
  52. Pomajbíková K, Petrželková KJ, Profousová I, Petrášová J, Kišidayová S, Varádyová Z, Modrý D (2010) A survey of entodiniomorphid ciliates in chimpanzees and bonobos. American Journal of Physical Anthropology 142(1):42–48. doi: 10.1002/ajpa.21191. Accessed Jan 6, 2014.
  53. Prüfer K, Munch K, Hellmann I, Akagi K, Miller JR, Walenz B, Koren S, Sutton G, Kodira C, Winer R, Knight JR, Mullikin JC, Meader SJ, Ponting CP, Lunter G, Higashino S, Hobolth A, Dutheil J, Karakoç E, Alkan C, Sajjadian S, Catacchio CR, Ventura M, Marques-Bonet T, Eichler EE, André C, Atencia R, Mugisha L, Junhold J, Patterson N, Siebauer M, Good JM, Fischer A, Ptak SE, Lachmann M, Symer DE, Mailund T, Schierup MH, Andrés AM, Kelso J, Pääbo S (2012) The bonobo genome compared with the chimpanzee and human genomes. Nature 486:527–531. doi: 10.1038/nature11128. [Online June 13, 2012]. Accessed August 24, 2014.
  54. R Development Core Team (2012). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available: May 5, 2012.
  55. Roberts LS, Janovy J (2009) Gerald D. Schmidt and Larry S. Roberts’ Foundations of Parasitology, 8th ed., Boston, MA: McGraw-Hill Higher Education. Accessed Jan 10, 2013.
  56. Sakamaki T (2010) Coprophagy in wild bonobos (Pan paniscus) at Wamba in the Democratic Republic of the Congo: a possibly adaptive strategy? Primates 51(1):87–90. doi: 10.1007/s10329-009-0167-9. [Online October 31, 2009]. Accessed Nov 18, 2011.
  57. Sandosham, AA (1950) On Enterobius vermicularis (Linnaeus, 1758) and some related species from primates and rodent. Journal of Helminthology 24(4):171–204. doi: 10.1017/S0022149X00019246. [Online June 5, 2009]. Accessed August 21, 2014.
  58. Sorci G, Morand S, Hugot JP (1997) Host-parasite coevolution: comparative evidence for covariation of life history traits in primates and oxyurid parasites. Proceedings of the Royal Society B: Biological Sciences 264(1379):285–289. doi: 10.1098/rspb.1997.0040. Accessed Dec 14, 2012.
  59. Stam AB (1960) Un cas mortel d’ascaridiose (Ascaris lumbricoides L.) chez le chimpanzé nain (Pan paniscus Schwartz). Annales De Parasitologie Humaine Et Comparée 35(4):675. Accessed Nov 20, 2012.
  60. Tutin CEG, Fernandez M (1991) Responses of wild chimpanzees and gorillas to the arrival of primatologists: behaviour observed during habituation. In: Primate Responses to Environmental Change, HO Box (editor), Netherlands: Springer editions, pp 187–197. Accessed Sep 10, 2012.
  61. Van Elsacker L, Vervaecke H, Verheyen RF (1995) A review of terminology on aggregation patterns in bonobos (Pan paniscus). International Journal of Primatology 16(1):37–52. doi: 10.1007/BF02700152. Accessed July 17, 2014.
  62. Wolfe ND, Escalante AA, Karesh WB, Kilbourn A, Spielman A, Lal AA (1998) Wild primate populations in emerging infectious disease research: the missing link? Emerging Infectious Diseases 4(2):149–158. Accessed Jan 7, 2014.
  63. Woodford MH, Butynski TM, Karesh WB (2002) Habituating the great apes: the disease risks. Oryx 36(2):153–160. doi: 10.1017/S0030605302000224. [Online May 7, 2002]. Accessed August 21, 2012.
  64. Zommers Z, Macdonald DW, Johnson PJ, Gillespie TR (2013) Impact of human activities on chimpanzee ground use and parasitism (Pan troglodytes): Researcher presence and infection dynamics. Conservation Letters 6(4):264–273. doi: 10.1111/j.1755-263X.2012.00288.x. [Online September 25, 2012]. Accessed Feb 7, 2014.
  65. Wallis J, Rick Lee D (1999) Primate conservation: the prevention of disease transmission. International Journal of Primatology 20(6):803–826. Accessed August 24, 2012.
  66. World Health Organization (2008) Chimioprévention des helminthiases chez l’homme utilisation coordonnée des médicaments anthelminthiques pour les interventions de lutte: manuel à l’intention des professionnels de la santé et des administrateurs de programmes. Geneva: Organisation mondiale de la Santé. Accessed July 29, 2015.

Copyright information

© International Association for Ecology and Health 2015

Authors and Affiliations

  • Victor Narat
    • 1
  • Jacques Guillot
    • 2
  • Flora Pennec
    • 1
  • Sophie Lafosse
    • 1
  • Anne Charlotte Grüner
    • 3
  • Bruno Simmen
    • 4
  • Jean Christophe Bokika Ngawolo
    • 5
  • Sabrina Krief
    • 1
  1. 1.Muséum national d’Histoire naturelle, UMR7206 (MNHN-CNRS-Paris7) Eco-anthropologie et ethnobiologieSite du Musée de l’HommeParisFrance
  2. 2.Ecole Nationale Vétérinaire d’Alfort, Parasitology department, Dynamyc research groupMaisons-AlfortFrance
  3. 3.Muséum national d’Histoire naturelle, UMR7206 (MNHN-CNRS-Paris7) Eco-anthropologie et ethnobiologieParis CedexFrance
  4. 4.Centre national de la recherche scientifique, UMR7206 (MNHN-CNRS-Paris7) Eco-anthropologie et ethnobiologieParis CedexFrance
  5. 5.NGO Mbou-Mon-Tour, NkalaTerritoire de BoloboDemocratic Republic of Congo

Personalised recommendations