Abstract
One of the current threats to the bonobo (Pan paniscus), a highly endangered ape species only found in the Democratic Republic of the Congo, are anthropozoonoses caused by human respiratory viruses. To date, epidemiological information regarding respiratory viral infections in bonobos is limited. In this study, we examined fecal immunoglobulin A antibodies against human respiratory viruses in bonobos, which may help estimating the viral prevalence. A substantial proportion of bonobos were positive for the antiviral antibodies, including those against parainfluenza virus, respiratory syncytial virus, influenza virus, rhinovirus, and mumps virus. The prevalence of the antibodies was found to depend on the viral species and bonobo populations, suggesting that the bonobos had been exposed to these respiratory viruses. These results may indicate the need for an epidemiological evidence-based action plan for the protection of bonobos from anthropozoonoses.
Similar content being viewed by others
References
Boesch C (2008) Why do chimpanzees die in the forest? The challenges of understanding and controlling for wild ape health. Am J Primatol 70:722–726. https://doi.org/10.1002/ajp.20571
Dunay E, Apakupakul K, Leard S, Palmer JL, Deem S (2018) Pathogen transmission from humans to great apes is a growing threat to primate conservation. EcoHealth 15:148–162. https://doi.org/10.1007/s10393-017-1306-1
Gilardi KV, Gillespie TR, Leendertz FH, Macfie EJ, Travis DA, Whittier CA et al (2015) Best practice guidelines for health monitoring and disease control in great ape populations. Gland Switz IUCN SSC Primate Spec. https://doi.org/10.2305/IUCN.CH.2015.SSC-OP.56.en
Grützmacher KS, Keil V, Metzger S, Wittiger L, Herbinger I, Calvignac-Spencer S et al (2018) Human respiratory syncytial virus and Streptococcus pneumoniae infection in wild bonobos. EcoHealth 15:462–466. https://doi.org/10.1007/s10393-018-1319-4
Hashimoto C, Furuichi T (2006) Comparison of behavioral sequence of copulation between chimpanzees and bonobos. Primates 47:51–55. https://doi.org/10.1007/s10329-005-0144-x
Kaur T, Singh J, Tong S, Humphrey C, Clevenger D, Tan W et al (2008) Descriptive epidemiology of fatal respiratory outbreaks and detection of a human-related metapneumovirus in wild chimpanzees (Pan troglodytes) at Mahale Mountains National Park, Western Tanzania. Am J Primatol 70:755–765. https://doi.org/10.1002/ajp.20565
Kawamoto Y, Takemoto H, Higuchi S, Sakamaki T, Hart JA, Hart TB et al (2013) Genetic structure of wild bonobo populations: diversity of mitochondrial DNA and geographical distribution. PLoS ONE 8:e59660. https://doi.org/10.1371/journal.pone.0059660
Köndgen S, Kühl H, N’Goran PK, Walsh PD, Schenk S, Ernst N et al (2008) Pandemic human viruses cause decline of endangered great apes. Curr Biol 18:260–264. https://doi.org/10.1016/j.cub.2008.01.012
Kooriyama T, Okamoto M, Yoshida T, Nishida T, Tsubota T, Saito A et al (2013) Epidemiological study of zoonoses derived from humans in captive chimpanzees. Primates 54:89–98. https://doi.org/10.1007/s10329-012-0320-8
Krueger K, Marr I, Dobler A, Palme R (2019) Preservation of fecal glucocorticoid metabolites and immunoglobulin A through silica gel drying for field studies in horses. Concerv Physiol 7:coz065. https://doi.org/10.1093/conphys/coz065
Lantz EL, Lonsdorf EV, Heintz MR, Murray CM, Lipende I, Travis DA et al (2018) Non-invasive quantification of immunoglobulin A in chimpanzees (Pan troglodytes schweinfurthii) at Gombe National Park, Tanzania. Am J Primatol 80:e22558. https://doi.org/10.1002/ajp.22558
Leendertz FH, Pauli G, Maetz-Rensing K, Boardman W, Nunn C, Ellerbrok H et al (2006) Pathogens as drivers of population declines: the importance of systematic monitoring in great apes and other threatened mammals. Biol Conserv 131:325–337. https://doi.org/10.1016/j.biocon.2006.05.002
Lonsdorf EV, Murray CM, Lonsdorf EV, Travis DA, Gilby IC, Chosy J et al (2011) A retrospective analysis of factors correlated to chimpanzee (Pan troglodytes schweinfurthii) respiratory health at Gombe National Park, Tanzania. EcoHealth 8:26–35. https://doi.org/10.1007/s10393-011-0683-0
Nackoney J, Molinario G, Potapov P, Turubanova S, Hansen MC, Furuichi T (2014) Impacts of civil conflict on primary forest habitat in northern Democratic Republic of the Congo, 1990–2010. Biol Conserv 170:321–328. https://doi.org/10.1016/j.biocon.2013.12.033
Negrey JD, Reddy RB, Scully EJ, Phillips-Garcia S, Owens LA, Langergraber KE et al (2019) Simultaneous outbreaks of respiratory disease in wild chimpanzees caused by distinct viruses of human origin. Emerg Microbes Infect 8:139–149. https://doi.org/10.1080/22221751.2018.1563456
Oates JF (2006) Is the chimpanzee, Pan troglodytes, an endangered species? It depends on what “endangered” means. Primates 47:102–112. https://doi.org/10.1007/s10329-005-0149-5
Reed PE, Mulangu S, Cameron KN, Ondzie AU, Joly D, Bermejo M et al (2014) A new approach for monitoring ebolavirus in wild great apes. PLoS Negl Trop Dis 8:e3143. https://doi.org/10.1371/journal.pntd.0003143
Ryan SJ, Walsh PD (2011) Consequences of non-intervention for infectious disease in African great apes. PLoS ONE 6:e29030. https://doi.org/10.1371/journal.pone.0029030
Sakamaki T (2010) Coprophagy in wild bonobos (Pan paniscus) at Wamba in the Democratic Republic of the Congo: a possibly adaptive strategy? Primates 51:87–90. https://doi.org/10.1007/s10329-009-0167-9
Scully EJ, Basnet S, Wrangham RW, Muller MN, Otali E, Hyeroba D et al (2018) Lethal respiratory disease associated with human rhinovirus C in wild chimpanzees, Uganda, 2013. Emerg Infect Dis 24:267–274. https://doi.org/10.3201/eid2402.170778
Szentiks CA, Köndgen S, Silinski S, Speck S, Leendertz FH (2009) Lethal pneumonia in a captive juvenile chimpanzee (Pan troglodytes) due to human-transmitted human respiratory syncytial virus (HRSV) and infection with Streptococcus pneumoniae. J Med Primatol 38:236–240. https://doi.org/10.1111/j.1600-0684.2009.00346.x
Thompson ME, Machanda ZP, Scully EJ, Enigk DK, Otali E, Muller MN et al (2018) Risk factors for respiratory illness in a community of wild chimpanzees (Pan troglodytes schweinfurthii). R Soc Open Sci 5:180840. https://doi.org/10.1098/rsos.180840
Vogel G (2000) Conflict in Congo threatens bonobos and rare gorillas. Science 287:2386–2387. https://doi.org/10.1126/science.287.5462.2386
Yoshida T, Takemoto H, Sakamaki T, Tokuyama N, Hart J, Hart T et al (2016) Epidemiological surveillance of lymphocryptovirus infection in wild bonobos. Front Microbiol 7:1262. https://doi.org/10.3389/fmicb.2016.01262
Acknowledgments
We wish to thank Akino Watanabe, Shohei Watanabe, Tomoko Ikoma, and Ayaka Washizaki for their technical assistance. We also wish to thank the staff of the Wamba Committee for Bonobo Research, the Centre de Recherche en Ecologie et Foresterie, the African Wildlife Foundation, the Institut Congolais pour la Conservation de la Nature, and the Tshuapa-Lomami-Lualaba Project for field research assistance. This research was supported by the Environment Research and Technology Development Fund (D-1007 to T. Furuichi) from the Ministry of the Environment, Japan, Grants-in-Aid for Scientific Research (19405015 to C. Hashimoto, 20212194 to T. Furuichi, and 23510295 to T. Yoshida), the Asia-Africa Science Platform Program (2009–2011 and 2012–2014 to T. Furuichi) of the Japan Society for the Promotion of Science, and the Cooperation Research Program (2012 to T. Yoshida) of the Wildlife Research Center, Kyoto University.
Author information
Authors and Affiliations
Corresponding authors
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
About this article
Cite this article
Yoshida, T., Takemoto, H., Sakamaki, T. et al. Prevalence of antibodies against human respiratory viruses potentially involving anthropozoonoses in wild bonobos. Primates 62, 897–903 (2021). https://doi.org/10.1007/s10329-021-00935-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10329-021-00935-5