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Invasive North American bullfrogs transmit lethal fungus Batrachochytrium dendrobatidis infections to native amphibian host species

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Abstract

Invasive species can be a threat to native species in several ways, including transmitting lethal infections caused by the parasites they carry. However, invasive species may also be plagued by novel and lethal infections they acquire when invading, making inferences regarding the ability of an invasive host to vector disease difficult from field observations of infection and disease. This is the case for the pathogenic fungus Batrachochytrium dendrobatidis (Bd) in Europe and one invasive host species, the North American bullfrog Lithobates catesbeianus, hypothesized to be responsible for vectoring lethal infection to European native amphibians. We tested this hypothesis experimentally using the alpine newt Ichthyosaura alpestris as our model native host. Our results show that infected bullfrog tadpoles are effective vectors of Bd. Native adult newts co-housed with experimentally infected bullfrog tadpoles became Bd infected (molecular and histological tests). Moreover, the exposed adult newts suffered mortality while the majority of infected bullfrog tadpoles survived until metamorphosis. These results cannot resolve the historical role of alien species in establishing the distribution of Bd across Europe or other regions in the world where this species was introduced, but they show its potential role as a Bd reservoir capable of transmitting lethal infections to native amphibians. Finally, our results also suggest that the removal of infected bullfrogs from aquatic environments may serve to reduce the availability of Bd in European amphibian communities, offering another justification for bullfrog eradication programmes that are currently underway or may be considered.

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Acknowledgments

All experimental work done here was ethically reviewed at Université de Savoie-Mont-Blanc. Authorization to catch Alpine newts was provided by the regional authorities (DREAL Rhône-Alpes, permit No. 2009–2010). CM, TD, AM, NCGG and AV were supported by ANR through the EU BiodivERsA-funded project R.A.C.E. (Risk Assessment of Chytridiomycosis to European amphibian biodiversity, M. Fisher coordinator), TWJG was supported by a NERC (Grant NE/G002193/1) through the EU BiodivERsA-funded project R.A.C.E., but is currently supported for research on chytridiomycosis by NERC standard grant NE/K012509/1. KS was hosted in France thanks to the Office Franco-Québéquois pour la Jeunesse, programme Formation & Emploi.

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Authors and Affiliations

  1. UMR CNRS 5553, Laboratoire d’Écologie Alpine, Université Savoie-Mont-Blanc, 73376, Le-Bourget-Du-Lac, France

    Claude Miaud, Tony Dejean, Karine Savard, Annie Millery-Vigues, Alice Valentini & Nadine Curt Grand Gaudin

  2. PSL University, Ecole Pratique des Hautes Etudes, Biogéographie et Ecologie des Vertébrés, Centre d’Ecologie Fonctionnelle et Évolutive (UMR 5175), Campus CNRS, 34293, Montpellier, France

    Claude Miaud

  3. Parc naturel régional Périgord-Limousin, 24450, La Coquille, France

    Tony Dejean

  4. Agriculture and Agri-Food Canada, Ottawa, ON, K1A 0C6, Canada

    Karine Savard

  5. Institute of Zoology, Zoological Society of London, Regents Park, London, NW1 4RY, UK

    Trenton W. J. Garner

  6. Environmental Sciences and Development, Northwest University, Private Bag X6001, Potchefstroom, 2531, South Africa

    Trenton W. J. Garner

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  1. Claude Miaud
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Correspondence to Claude Miaud.

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Miaud, C., Dejean, T., Savard, K. et al. Invasive North American bullfrogs transmit lethal fungus Batrachochytrium dendrobatidis infections to native amphibian host species. Biol Invasions 18, 2299–2308 (2016). https://doi.org/10.1007/s10530-016-1161-y

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