Abstract

Anthrax is a globally important animal disease and zoonosis. Despite this, our current knowledge of anthrax ecology is largely limited to arid ecosystems, where outbreaks are most commonly reported1,2,3. Here we show that the dynamics of an anthrax-causing agent, Bacillus cereus biovar anthracis, in a tropical rainforest have severe consequences for local wildlife communities. Using data and samples collected over three decades, we show that rainforest anthrax is a persistent and widespread cause of death for a broad range of mammalian hosts. We predict that this pathogen will accelerate the decline and possibly result in the extirpation of local chimpanzee (Pan troglodytes verus) populations. We present the epidemiology of a cryptic pathogen and show that its presence has important implications for conservation.

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Acknowledgements

We thank the authorities in Côte d’Ivoire for long-term support, especially the Ministry of the Environment and Forests, the Ministry of Research, the directorship of the TNP and the CSRS in Abidjan; and national authorities from all other countries for providing permissions for our research (MINFoF, MINRESI, the Service de la Conservation de la Réserve du Dja, Cameroon, in Central African Republic; the Ministère des Eaux et Fôrets, Chasse et Peche and the Ministère de l’Education Nationale, de l’Alphabetisation, de l’Enseignement Superieur, et de la Recherche, the Agence Nationale des Parcs Nationaux, Gabon; Centre National de la Recherche Scientifique et Technologique, Gabon; Direction des Eaux, Forêts et Chasses, Senegal; Forestry Development Authority, Liberia; Institut Congolais pour la Conservation de la Nature, Democratic Republic of the Congo; Ministère de l’Agriculture de l’Elevage et des Eaux et Forêts, Guinea; Instituto da Biodiversidade e das Áreas Protegidas (IBAP), Guinea-Bissau; Ministère de la Recherche Scientifique, Democratic Republic of the Congo; Ministère de le Recherche Scientifique et Technologique, Democratic Republic of the Congo; Nigeria National Park Service, Nigeria, Uganda National Council for Science and Technology, Ugandan Wildlife Authority, Uganda). We thank the WWF Central African Republic, T. Börding, T. Hicks, Y. Moebius, V. Sommer, K. Zuberbühler and M. Peeters for their logistical support; the field assistants A. Henlin, K. Albrechtova and A. Lang for the collection of samples in TNP; and the field assistants from all other sites for their support; S. Becker, T. Franz, S. Howaldt, A. Lander, P. Lochau, H. Nattermann and A. Schneider for the laboratory work; J. Hinzmann, A. Nitsche and J. Tesch for sequencing; P. Wojciech Dabrowski and T. Semmler from RKI, as well as G. Hamilton at Glasgow Polyomics, for bioinformatic support; and M. Kovacev-Wegener for administrative support. We thank the German Research Council DFG KL 2521/1-1 and the Sonnenfeld-Stiftung for funding; and the Max-Planck-Society and Krekeler Foundation for funding of the Pan African Programme.

Author information

Author notes

    • Constanze Hoffmann
    •  & Fee Zimmermann

    These authors contributed equally to this work.

Affiliations

  1. Robert Koch Institute, P3: “Epidemiology of Highly Pathogenic Microorganisms”, Seestraße 10–11, 13353 Berlin, Germany

    • Constanze Hoffmann
    • , Fee Zimmermann
    • , Kathrin Nowak
    • , Anja Blankenburg
    • , Ariane Düx
    • , Jan F. Gogarten
    • , Siv Aina Leendertz
    • , Floraine Léguillon
    • , Therese Löhrich
    • , Kevin Merkel
    • , Sonja Metzger
    • , Svenja Niedorf
    • , Hélène De Nys
    • , Andreas Sachse
    • , Ulla Thiesen
    • , Doris Wu
    • , Sébastien Calvignac-Spencer
    •  & Fabian H. Leendertz
  2. Robert Koch Institute, ZBS 2: Centre for Biological Threats and Special Pathogens, Highly Pathogenic Microorganisms, Seestraße 10–11, 13353 Berlin, Germany

    • Fee Zimmermann
    • , Susann Dupke
    • , Roland Grunow
    •  & Silke R. Klee
  3. Institute of Biodiversity, Animal Health and Comparative Medicine, Boyd Orr Centre for Population and Ecosystem Health, College of Medical, Veterinary and Life Sciences, University of Glasgow, Glasgow G12 8QQ, UK

    • Roman Biek
  4. Max Planck Institute for Evolutionary Anthropology (MPI EVAN), Deutscher Platz 6, 04103 Leipzig, Germany

    • Hjalmar Kuehl
    • , Roger Mundry
    • , Anthony Agbor
    • , Samuel Angedakin
    • , Mimi Arandjelovic
    • , Gregory Brazolla
    • , Katherine Corogenes
    • , Tobias Deschner
    • , Paula Dieguez
    • , Karsten Dierks
    • , Henk Eshuis
    • , Yisa Ginath Yuh
    • , Jan F. Gogarten
    • , Anne-Céline Granjon
    • , Sorrel Jones
    • , Jessica Junker
    • , Juan Lapuente
    • , Kevin Lee
    • , Therese Löhrich
    • , Sergio Marrocoli
    • , Amelia Meier
    • , Mizuki Murai
    • , Hélène De Nys
    • , Joost van Schijndel
    • , Doris Wu
    • , Christophe Boesch
    •  & Roman M. Wittig
  5. LANADA/LCVB, Bingerville, 206, Côte d’Ivoire

    • Emmanuel Couacy-Hymann
  6. World Health Organization, 1211 Geneva 27, Switzerland

    • Pierre Formenty
  7. Chimbo Foundation, Amstel 49, 1011 PW Amsterdam, The Netherlands

    • Annemarie Goedmakers
    •  & Els Ton
  8. McGill University, Department of Biology, 855 Sherbrooke Street, West Montreal, Quebec H3A 2T7, Canada

    • Jan F. Gogarten
  9. The Ohio State University, Department of Anthropology, 4034 Smith Laboratory, 174 West 18th Avenue, Columbus, Ohio 43210, USA

    • Scott McGraw
  10. Lukuru Foundation, 1235 Avenue des Poids Lourds/Quartier de Kingabois, Kinshasa, Democratic Republic of the Congo

    • John Hart
  11. Limbe Wildlife Centre, Limbe, Cameroon

    • John Kiang
  12. Arizona State University, PO Box 872402, Tempe, Arizona 85287-2402, USA

    • Kevin Langergraber
  13. Wild Chimpanzee Foundation (WCF), Deutscher Platz 6, 04103 Leipzig, Germany

    • Vera Leinert
  14. German Primate Center, Kellnerweg 4, 37077 Göttingen, Germany

    • Kerstin Mätz-Rensing
  15. Robert Koch Institute, Seestraße 10–11, 13353 Berlin, Germany

    • Lothar H. Wieler

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Contributions

C.H., F.Z., A.A., S.A., M.A., G.B., K.C., T.D., P.D., K.D., H.E., P.F., Y.G.Y., A.G., A.-C.G., S.McG., J.H., S.J., J.J., J.K., K.La., J.L., K.Le., F.L., V.L., T.L., S.Ma., A.M., S.Me., M.M., J.v.S., E.T. and D.W. collected flies, bones and associated field data. Necropsies on wildlife that was found dead were performed by F.Z., K.N., A.B., E.C.-H., A.D., P.F., S.A.L., T.L., S.Me., S.N., H.D.N. and F.H.L. and laboratory analyses were performed by C.H., F.Z., K.N., S.D., R.G., K.M.-R., K.M., S.Me., H.D.N., A.S., U.T., S.R.K., L.H.W., S.C.-S. and F.H.L. The data were analysed by C.H., F.Z., R.B., H.K., R.M. and S.C.-S. and the manuscript was prepared by C.H., F.Z., R.B., H.K., R.M., J.F.G., S.C.-S. and F.H.L. The manuscript was revised and approved by all authors. The study was supervised by C.B., R.M.W., S.C.-S. and F.H.L.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Fabian H. Leendertz.

Publisher's note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Extended data

Supplementary information

PDF files

  1. 1.

    Supplementary Information

    This file contains a detailed method section as well as additional tables (Tables S1-10) and figures (Fig. S1-8).

Excel files

  1. 1.

    Supplementary Table 1

    This file contains results that were derived from the analyses of flies caught in TNP analyzed in this study. The file includes results from PCR and culture as well as flymeal analysis results for a selection of flies.

  2. 2.

    Supplementary Table 2

    This file contains results of fly meal analysis with taxonomic assignment at genus level. The file provides the number of sequences per amplicon assigned at genus level.

  3. 3.

    Supplementary Table 3

    This file contains results of fly meal analysis with taxonomic assignment at order level. The file provides the number of sequences per amplicon assigned at order level.

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