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.

Access optionsAccess options

Rent or Buy article

Get time limited or full article access on ReadCube.


All prices are NET prices.


Primary accessions


  1. 1.

    et al. Predictability of anthrax infection in the Serengeti, Tanzania. J. Appl. Ecol. 48, 1333–1344 (2011)

  2. 2.

    & Anthrax and wildlife. Rev. Sci. Tech. 21, 359–383 (2002)

  3. 3.

    & Ecology and epidemiology of anthrax in the Etosha National Park, Namibia. Onderstepoort J. Vet. Res. 61, 71–83 (1994)

  4. 4.

    & Anthrax in animals. Mol. Aspects Med. 30, 481–489 (2009)

  5. 5.

    WHO Guidelines Approved by the Guidelines Review Committee (World Health Organization, Department of Communicable Diseases Surveillance and Response, 2008)

  6. 6.

    , , & Naturally acquired anthrax antibodies in a cheetah (Acinonyx jubatus) in Botswana. J. Wildl. Dis. 44, 721–723 (2008)

  7. 7.

    , & Managing the 2004/05 anthrax outbreak in Queen Elizabeth and Lake Mburo National Parks, Uganda. Afr. J. Ecol. 46, 24–31 (2008)

  8. 8.

    , , & Massive outbreak of anthrax in wildlife in the Malilangwe Wildlife Reserve, Zimbabwe. Vet. Rec. 160, 113–118 (2007)

  9. 9.

    et al. Anthrax outbreak among Grevy’s zebra (Equus grevyi) in Samburu, Kenya. Afr. J. Ecol. 45, 483–489 (2007)

  10. 10.

    et al. Anthrax in wildlife in the Luangwa Valley, Zambia. Vet. Rec. 128, 399–403 (1991)

  11. 11.

    The ecology of anthrax in the Kruger National Park, South Africa. Salisbury Med. Bull. 68 (Suppl), 19–23 (1990)

  12. 12.

    et al. Serologic surveillance of anthrax in the Serengeti ecosystem, Tanzania, 1996–2009. Emerg. Infect. Dis. 17, 387–394 (2011)

  13. 13.

    et al. Distribution and molecular evolution of Bacillus anthracis genotypes in Namibia. PLoS Negl. Trop. Dis. 6, e1534 (2012)

  14. 14.

    et al. Anthrax kills wild chimpanzees in a tropical rainforest. Nature 430, 451–452 (2004)

  15. 15.

    et al. The genome of a Bacillus isolate causing anthrax in chimpanzees combines chromosomal properties of B. cereus with B. anthracis virulence plasmids. PLoS ONE 5, e10986 (2010)

  16. 16.

    et al. Capsules, toxins and AtxA as virulence factors of emerging Bacillus cereus biovar anthracis. PLoS Negl. Trop. Dis. 9, e0003455 (2015)

  17. 17.

    et al. Bacillus cereus biovar anthracis causing anthrax in sub-Saharan Africa—chromosomal monophyly and broad geographic distribution. PLoS Negl. Trop. Dis. 10, e0004923 (2016)

  18. 18.

    et al. Anthrax in western and central African great apes. Am. J. Primatol. 68, 928–933 (2006)

  19. 19.

    et al. Carrion fly-derived DNA as a tool for comprehensive and cost-effective assessment of mammalian biodiversity. Mol. Ecol. 22, 915–924 (2013)

  20. 20.

    Surveillance and control of anthrax and rabies in wild herbivores and carnivores in Namibia. Rev. Sci. Tech. 12, 137–146 (1993)

  21. 21.

    et al. Comparison of French and worldwide Bacillus anthracis strains favors a recent, post-Columbian origin of the predominant North-American clade. PLoS ONE 11, e0146216 (2016)

  22. 22.

    et al. Bacillus anthracis diversity in Kruger National Park. J. Clin. Microbiol. 38, 3780–3784 (2000)

  23. 23.

    , , , & Long-term research sites as refugia for threatened and over-harvested species. Biol. Lett. 7, 723–726 (2011)

  24. 24.

    , , , & The necrophagous fly anthrax transmission pathway: empirical and genetic evidence from wildlife epizootics. Vector Borne Zoonotic Dis. 14, 576–583 (2014)

  25. 25.

    et al. Mortality rates among wild chimpanzees. J. Hum. Evol. 40, 437–450 (2001)

  26. 26.

    et al. Pandemic human viruses cause decline of endangered great apes. Curr. Biol. 18, 260–264 (2008)

  27. 27.

    & The Chimpanzees of the Taï Forest: Behavioural Ecology and Evolution (Oxford Univ. Press, 2000)

  28. 28.

    Guidelines for the Surveillance and Control of Anthrax in Humans and Animals 3rd edn (World Health Organization, Department of Communicable Diseases Surveillance and Response, 1998)

  29. 29.

    et al. Rapid and sensitive identification of pathogenic and apathogenic Bacillus anthracis by real-time PCR. FEMS Microbiol. Lett. 214, 51–59 (2002)

  30. 30.

    et al. Characterization of Bacillus anthracis-like bacteria isolated from wild great apes from Cote d’Ivoire and Cameroon. J. Bacteriol. 188, 5333–5344 (2006)

  31. 31.

    et al. Diagnostic reverse-transcription polymerase chain reaction kit for filoviruses based on the strain collections of all European biosafety level 4 laboratories. J. Infect. Dis. 196 (Suppl 2), S199–S204 (2007)

  32. 32.

    et al. Animal DNA in PCR reagents plagues ancient DNA research. J. Archaeol. Sci. 34, 1361–1366 (2007)

  33. 33.

    et al. Comparing the performance of three ancient DNA extraction methods for high-throughput sequencing. Mol. Ecol. Resour. 16, 459–469 (2016)

  34. 34.

    & Ancient DNA extraction from bones and teeth. Nat. Protoc. 2, 1756–1762 (2007)

  35. 35.

    Scythe: a 3′-end adapter contaminant trimmer. (2014)

  36. 36.

    & Sickle: a sliding-window, adaptive, quality-based trimming tool for FastQ files. (2011)

  37. 37.

    Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM. Preprint at (2013)

  38. 38.

    et al. From FastQ data to high-confidence variant calls: the genome analysis toolkit best practices pipeline. Curr. Protoc. Bioinform. 43, 11.10.1–11.10. 33 (2013)

  39. 39.

    et al. A framework for variation discovery and genotyping using next-generation DNA sequencing data. Nat. Genet. 43, 491–498 (2011)

  40. 40.

    et al. The genome analysis toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res. 20, 1297–1303 (2010)

  41. 41.

    et al. Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28, 1647–1649 (2012)

  42. 42.

    , , & jModelTest 2: more models, new heuristics and parallel computing. Nat. Methods 9, 772 (2012)

  43. 43.

    Using MODELTEST and PAUP* to select a model of nucleotide substitution. Curr. Protoc. Bioinform. 00, 6.5.1–6.5.14 (2003)

  44. 44.

    et al. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst. Biol. 59, 307–321 (2010)

  45. 45.

    , , & Exploring the temporal structure of heterochronous sequences using TempEst (formerly Path-O-Gen). Virus Evol. 2, vew007 (2016)

  46. 46.

    , , & Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol. Biol. Evol. 29, 1969–1973 (2012)

  47. 47.

    , , & Relaxed phylogenetics and dating with confidence. PLoS Biol. 4, e88 (2006)

  48. 48.

    Estimation of evolutionary distances between homologous nucleotide sequences. Proc. Natl Acad. Sci. USA 78, 454–458 (1981)

  49. 49.

    Analyzing Linguistic Data: A Practical Introduction to Statistics using R (Cambridge Univ. Press, 2008)

  50. 50.

    & Generalized Linear Models Vol. 37 (CRC, 1989)

  51. 51.

    , , & Random effects structure for confirmatory hypothesis testing: keep it maximal. J. Mem. Lang. 68, 225–278 (2013)

  52. 52.

    & Conclusions beyond support: overconfident estimates in mixed models. Behav. Ecol. 20, 416–420 (2009)

  53. 53.

    & Cryptic multiple hypotheses testing in linear models: overestimated effect sizes and the winner’s curse. Behav. Ecol. Sociobiol. 65, 47–55 (2011)

  54. 54.

    & An Introduction to Generalized Linear Models (CRC, 2008)

  55. 55.

    R Core Team. R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, Vienna, Austria, 2013)

  56. 56.

    , , & Fitting linear mixed-effects models using lme4. J. Stat. Softw. 67, 1–48 (2015)

  57. 57.

    Geographic Distance Matrix Generator (version 1.2.3). (American Museum of Natural History, 2011)

  58. 58.

    , & APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20, 289–290 (2004)

  59. 59.

    & The ecodist package for dissimilarity-based analysis of ecological data. J. Stat. Softw. 22, 1–19 (2007)

  60. 60.

    , , , & The price of play: self-organized infant mortality cycles in chimpanzees. PLoS ONE 3, e2440 (2008)

Download references


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.


  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


  1. Search for Constanze Hoffmann in:

  2. Search for Fee Zimmermann in:

  3. Search for Roman Biek in:

  4. Search for Hjalmar Kuehl in:

  5. Search for Kathrin Nowak in:

  6. Search for Roger Mundry in:

  7. Search for Anthony Agbor in:

  8. Search for Samuel Angedakin in:

  9. Search for Mimi Arandjelovic in:

  10. Search for Anja Blankenburg in:

  11. Search for Gregory Brazolla in:

  12. Search for Katherine Corogenes in:

  13. Search for Emmanuel Couacy-Hymann in:

  14. Search for Tobias Deschner in:

  15. Search for Paula Dieguez in:

  16. Search for Karsten Dierks in:

  17. Search for Ariane Düx in:

  18. Search for Susann Dupke in:

  19. Search for Henk Eshuis in:

  20. Search for Pierre Formenty in:

  21. Search for Yisa Ginath Yuh in:

  22. Search for Annemarie Goedmakers in:

  23. Search for Jan F. Gogarten in:

  24. Search for Anne-Céline Granjon in:

  25. Search for Scott McGraw in:

  26. Search for Roland Grunow in:

  27. Search for John Hart in:

  28. Search for Sorrel Jones in:

  29. Search for Jessica Junker in:

  30. Search for John Kiang in:

  31. Search for Kevin Langergraber in:

  32. Search for Juan Lapuente in:

  33. Search for Kevin Lee in:

  34. Search for Siv Aina Leendertz in:

  35. Search for Floraine Léguillon in:

  36. Search for Vera Leinert in:

  37. Search for Therese Löhrich in:

  38. Search for Sergio Marrocoli in:

  39. Search for Kerstin Mätz-Rensing in:

  40. Search for Amelia Meier in:

  41. Search for Kevin Merkel in:

  42. Search for Sonja Metzger in:

  43. Search for Mizuki Murai in:

  44. Search for Svenja Niedorf in:

  45. Search for Hélène De Nys in:

  46. Search for Andreas Sachse in:

  47. Search for Joost van Schijndel in:

  48. Search for Ulla Thiesen in:

  49. Search for Els Ton in:

  50. Search for Doris Wu in:

  51. Search for Lothar H. Wieler in:

  52. Search for Christophe Boesch in:

  53. Search for Silke R. Klee in:

  54. Search for Roman M. Wittig in:

  55. Search for Sébastien Calvignac-Spencer in:

  56. Search for Fabian H. Leendertz in:


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.

About this article

Publication history






Further reading


By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.