Skip to main content
Top
Published in: EcoHealth 4/2015

01-12-2015 | Original Contribution

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

Authors: Victor Narat, Jacques Guillot, Flora Pennec, Sophie Lafosse, Anne Charlotte Grüner, Bruno Simmen, Jean Christophe Bokika Ngawolo, Sabrina Krief

Published in: EcoHealth | Issue 4/2015

Login to get access

Abstract

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.
Appendix
Available only for authorised users
Literature
go back to reference 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. 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.
go back to reference 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. 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.
go back to reference 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. http://www.ncbi.nlm.nih.gov/pubmed/10501618. Accessed Jan 8, 2013. 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. http://​www.​ncbi.​nlm.​nih.​gov/​pubmed/​10501618. Accessed Jan 8, 2013.
go back to reference 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. 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.
go back to reference 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. http://www.ncbi.nlm.nih.gov/pubmed/10647051. Accessed August 24, 2012. 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. http://​www.​ncbi.​nlm.​nih.​gov/​pubmed/​10647051. Accessed August 24, 2012.
go back to reference 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. http://www.ncbi.nlm.nih.gov/pubmed/22844754. Accessed Nov 13, 2012. 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. http://​www.​ncbi.​nlm.​nih.​gov/​pubmed/​22844754. Accessed Nov 13, 2012.
go back to reference 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. 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.
go back to reference 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. 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.
go back to reference 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. http://www.ncbi.nlm.nih.gov/pubmed/3533863. Accessed May 25, 2010. 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. http://​www.​ncbi.​nlm.​nih.​gov/​pubmed/​3533863. Accessed May 25, 2010.
go back to reference 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. http://www.ncbi.nlm.nih.gov/pubmed/20853397. Accessed April 16, 2012. 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. http://​www.​ncbi.​nlm.​nih.​gov/​pubmed/​20853397. Accessed April 16, 2012.
go back to reference 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. 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.
go back to reference 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. 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.
go back to reference 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. 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.
go back to reference 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. 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.
go back to reference 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. 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.
go back to reference 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. 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.
go back to reference 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. http://www.ncbi.nlm.nih.gov/pubmed/10205804. Accessed Jan 9, 2014. 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. http://​www.​ncbi.​nlm.​nih.​gov/​pubmed/​10205804. Accessed Jan 9, 2014.
go back to reference 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]. http://www.nature.com/nature/journal/v486/n7404/full/nature11128.html. Accessed August 24, 2014. 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]. http://​www.​nature.​com/​nature/​journal/​v486/​n7404/​full/​nature11128.​html. Accessed August 24, 2014.
go back to reference R Development Core Team (2012). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available: http://www.R-project.org/.Accessed May 5, 2012. R Development Core Team (2012). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available: http://​www.​R-project.​org/​.​Accessed May 5, 2012.
go back to reference 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. 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.
go back to reference 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. 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.
Metadata
Title
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
Authors
Victor Narat
Jacques Guillot
Flora Pennec
Sophie Lafosse
Anne Charlotte Grüner
Bruno Simmen
Jean Christophe Bokika Ngawolo
Sabrina Krief
Publication date
01-12-2015
Publisher
Springer US
Published in
EcoHealth / Issue 4/2015
Print ISSN: 1612-9202
Electronic ISSN: 1612-9210
DOI
https://doi.org/10.1007/s10393-015-1058-8

Other articles of this Issue 4/2015

EcoHealth 4/2015 Go to the issue