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Drivers of salamander extirpation mediated by Batrachochytrium salamandrivorans

Nature volume 544, pages 353–356 (2017)Cite this article

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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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Figure 1: B. salamandrivorans leads to fire salamander population extirpation.
Figure 2: Effect of different variables on infection dynamics of B. salamandrivorans in fire salamanders.
Figure 3: B. salamandrivorans encysted spores avoid predation and infect fire salamanders.
Figure 4: Anuran and urodelan reservoirs promote B. salamandrivorans sustenance.

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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).

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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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The authors declare no competing financial interests.

Additional information

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.

Extended Data Table 1 Infection loads (expressed in GE/PCR reaction) for midwife toads (green) and fire salamanders (orange)
Full size table
Extended Data Table 2 Infectivity of experimentally infected B. salamandrivorans soil at 4 °C and 15 °C
Full size table
Extended Data Table 3 Infectivity of B. salamandrivorans in soil
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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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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