Drivers of salamander extirpation mediated by Batrachochytrium salamandrivorans (2024)

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Subjects Abstract Access options Additional access options: References Acknowledgements Author information Authors and Affiliations Contributions Corresponding author Ethics declarations Competing interests Additional information Extended data figures and tables Extended Data Figure 1 B. salamandrivorans GE loads in soil. Extended Data Figure 2 B. salamandrivorans GE loads detection in experimentally infected soil, incubated at 4 °C and 15 °C. Supplementary information In vitro culture of Batrachochytrium salamandrivorans cultured in TghL broth at 15°C PowerPoint slides PowerPoint slide for Fig. 1 PowerPoint slide for Fig. 2 PowerPoint slide for Fig. 3 PowerPoint slide for Fig. 4 Rights and permissions About this article Cite this article This article is cited by eDNA-based monitoring of Batrachochytrium dendrobatidis and Batrachochytrium salamandrivorans with ddPCR in Luxembourg ponds: takingsignals belowthe Limit of Detection (LOD)into account The two chytrid pathogens of amphibians in Eurasia—climatic niches and future expansion United States amphibian imports pose a disease risk to salamanders despite Lacey Act regulations Disease state associated with chronic toe lesions in hellbenders may alter anti-chytrid skin defenses Attitudes and Behavioral Intentions of Pet Amphibian Owners About Biosecurity Practices Comments
  • Letter
  • Published: 20 April 2017
  • Gwij Stegen1na1,
  • Frank Pasmans1na1,
  • Benedikt R. Schmidt2,3,
  • Lieze O. Rouffaer1,
  • Sarah Van Praet1,
  • Michael Schaub4,
  • Stefano Canessa1,
  • Arnaud Laudelout5,
  • Thierry Kinet5,
  • Connie Adriaensen1,
  • Freddy Haesebrouck1,
  • Wim Bert6,
  • Franky Bossuyt7 &
  • …
  • An Martel1

Nature volume544,pages 353–356 (2017)Cite this article

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Subjects

  • Conservation biology
  • Microbial ecology

Abstract

The recent arrival of Batrachochytrium salamandrivorans in Europe was followed by rapid expansion of its geographical distribution and host range, confirming the unprecedented threat that this chytrid fungus poses to western Palaearctic amphibians1,2. Mitigating this hazard requires a thorough understanding of the pathogen’s disease ecology that is driving the extinction process. Here, we monitored infection, disease and host population dynamics in a Belgian fire salamander (Salamandra salamandra) population for two years immediately after the first signs of infection. We show that arrival of this chytrid is associated with rapid population collapse without any sign of recovery, largely due to lack of increased resistance in the surviving salamanders and a demographic shift that prevents compensation for mortality. The pathogen adopts a dual transmission strategy, with environmentally resistant non-motile spores in addition to the motile spores identified in its sister species B. dendrobatidis. The fungus retains its virulence not only in water and soil, but also in anurans and less susceptible urodelan species that function as infection reservoirs. The combined characteristics of the disease ecology suggest that further expansion of this fungus will behave as a ‘perfect storm’ that is able to rapidly extirpate highly susceptible salamander populations across Europe.

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Drivers of salamander extirpation mediated by Batrachochytrium salamandrivorans (1)
Drivers of salamander extirpation mediated by Batrachochytrium salamandrivorans (2)
Drivers of salamander extirpation mediated by Batrachochytrium salamandrivorans (3)
Drivers of salamander extirpation mediated by Batrachochytrium salamandrivorans (4)

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Acknowledgements

The technical assistance of M. Claeys and M. Couvreur is appreciated. K. Roelants kindly provided the artwork. This research is supported by Ghent University Special research fund (GOA 01G02416 and BOF01J030313) and by the Research Foundation Flanders (FWO) (G007016N, FWO16/PDO/019, FWO12/ASP/210).

Author information

Author notes

  1. Gwij Stegen and Frank Pasmans: These authors contributed equally to this work.

Authors and Affiliations

  1. Department of Pathology, Bacteriology and Avian Diseases, Faculty of Veterinary Medicine, Ghent University, Salisburylaan 133, Merelbeke, 9820, Belgium

    Gwij Stegen,Frank Pasmans,Lieze O. Rouffaer,Sarah Van Praet,Stefano Canessa,Connie Adriaensen,Freddy Haesebrouck&An Martel

  2. Department of Evolutionary Biology and Environmental Studies, University of Zurich, Winterthurerstrasse 190, Zurich, 8057, Switzerland

    Benedikt R. Schmidt

  3. KARCH, Passage Maximilien-de-Meuron 6, Neuchâtel, 2000, Switzerland

    Benedikt R. Schmidt

  4. Swiss Ornithological Institute, Seerose 1, Sempach, 6204, Switzerland

    Michael Schaub

  5. Natagora c/o Mundo-Namur, Rue Nanon 98, Namur, 5000, Belgium

    Arnaud Laudelout&Thierry Kinet

  6. Department of Biology, Nematology Research Unit, Ghent University, K.L. Ledeganckstraat 35, Gent, 9000, Belgium

    Wim Bert

  7. Biology Department, Amphibian Evolution Lab, Vrije Universiteit Brussel, Pleinlaan 2, Brussels, 1050, Belgium

    Franky Bossuyt

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  1. Gwij Stegen

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Contributions

A.M., G.S. and F.P. designed the research. A.M., G.S., L.O.R., S.V.P., F.P., C.A., A.L., T.K. and W.B. carried out the research. A.M., F.P., G.S., S.C., B.R.S., M.S., L.O.R. and F.H. analysed the data. A.M., F.B., G.S., B.R.S. and F.P. wrote the paper with input from all other authors.

Corresponding author

Correspondence to An Martel.

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Competing interests

The authors declare no competing financial interests.

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Reviewer Information Nature thanks A. Dobson, M. Fisher and B. Han for their contribution to the peer review of this work.

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Extended data figures and tables

Extended Data Figure 1 B. salamandrivorans GE loads in soil.

To investigate whether B. salamandrivorans can be detected in terrestrial environments, soil samples were taken in the close vicinity of experimentally infected animals (experimental samples) and naturally infected salamanders in the Robertville outbreak area (outbreak samples). Error bars depict s.d.

Extended Data Figure 2 B. salamandrivorans GE loads detection in experimentally infected soil, incubated at 4 °C and 15 °C.

Error bars depict s.d.

Full size table
Full size table
Full size table

Supplementary information

In vitro culture of Batrachochytrium salamandrivorans cultured in TghL broth at 15°C

A sporulating zoosporangium, motile spores and floating encysted spores are shown at 400x magnification. This video was recorded through an Olympus IX50 inverted microscope using a videocapture plugin in ImageJ. (MP4 5759 kb)

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Drivers of salamander extirpation mediated by Batrachochytrium salamandrivorans (5)

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Stegen, G., Pasmans, F., Schmidt, B. et al. Drivers of salamander extirpation mediated by Batrachochytrium salamandrivorans. Nature 544, 353–356 (2017). https://doi.org/10.1038/nature22059

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Drivers of salamander extirpation mediated by Batrachochytrium salamandrivorans (2024)
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