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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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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.

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Correspondence to An Martel.

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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.

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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  1. Majid Ali

    Fungal Pathogens and oxyphile - oxyphobe conflicts

    Stegen et. al. show a collapse without recovery of a Belgian population of fire salamander (Salamandra salamandra) with arrival of fungus Batrachochytrium salamandrivorans. (ref. 1) In the combined characteristics of the fungal disease ecology, they see the potential of a 'perfect storm' in which it is likely to rapidly extirpate susceptible salamander populations across Europe. Without an available option, they recognize ex-situ conservation as the only viable alternative. For the United States and other regions currently considered to be free of the fungus, prevention of introduction must be based on a clear understanding of the host-pathogen dynamics as well as availability of resistant or less susceptible reservoir host species for the pathogen.

    This writer recognizes the relevance and importance of the Stegen paper to the work of physicians. Fungal epidemics usually do not hold public interest for long. This has been so as well with medical practitioners who are clinically involved with fungal pathogens. This seems odd since physicians, by and large, do recognize important clinical differences between fungal and non-fungal infections. Historically, much was learned from non-fungal epidemics and some inferences could have been drawn concerning human disease from the past fungal epidemics involving bees, bats, and butterflies. Specifically, the examples of well-publicized large scale destructions of species include mass destruction of bats (with the white-nose syndrome caused by the fungus Pseudogymnoascus destructans, ref. 2), honey bees (collapsing colony disease caused by Nosema ceranae, ref. 3), and large scale disappearance of Monarch butterflies (by mycorrhizal fungi, ref. 4). Now Stegen and colleagues reveal a much deeper dimension of fungal pathogens. They also point out that the same fate of American salamander species may be expected when the fungus is introduced to the country. For these and other reasons, in this writer's view the Stegen paper raises important questions not only about damage inflicted by fungal pathogens in the wild but also for humans.

    Chytridiomycota are aquatic fungi that also thrive in the capillary network around soil particles. They are notable for their: (1) pathogenicity for amphibians; and (2) inhibition by amphibian cutaneous flora. However, this defense, as shown by Stegen et. al., does not protect fire salamander from Batrachochytrium salamandrivorans. The matter of such protection by the cutaneous flora of some amphibian species should be of interest to clinicians in considerations of host resistance.

    In Altered States of Bowel Ecology (1980), (ref. 5), this writer addressed the matter of systemic symptom-complexes which clinically respond to measures that reduce the total load of fungal species in the gut flora. That led to his interest in gut immunopathology and studies of IgE antibodies in tissues and IgG antibodies in the blood with specificity for fungal antigen. (ref.6,7) This work and his parallel interest in the molecular biology of oxygen, (ref.8-9) led him to questions concerning host-pathogen dynamics among oxygen-consuming human cells (?oxyphiles) and oxygen-shunning fungal organisms in human ecosystems (oxyphobes?).(ref.10,11) These 'oxyphile-oxyphobe conflicts' - it seemed to him - represent a different dimension of clinical mycology that is ecologically oriented, bioenergetically directed, and therapeutically mindful of the influence of prevailing oxygen and oxygen-related conditions in the body ecosystems, especially those of the gut, blood, and liver. (ref. 9-11)

    The recent report of incremental loss of oxygen from oceans (ref.12) is noteworthy in this context and so are the incremental oxidizing capacity of the planet Earth and the cumulative chemical load on its the ecosyetems. (ref.13) Might these factors be of importance in considerations of immunosuppression in our species? If so, might the matters of oxyphil-oxyphobe conflicts be clinically significant in the prevention and treatment of fungal overload and infections? Should physicians not think ecologically? Should they not be mindful of the state of oxygen homeostasis in their patients for health preservation and disease prevention?

    The work of Stegen et al. is clearly of relevance to physicians' work.

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