Cargando…

Effectiveness of antifungal treatments during chytridiomycosis epizootics in populations of an endangered frog

The recently-emerged amphibian chytrid fungus Batrachochytrium dendrobatidis (Bd) has had an unprecedented impact on global amphibian populations, and highlights the urgent need to develop effective mitigation strategies. We conducted in-situ antifungal treatment experiments in wild populations of t...

Descripción completa

Detalles Bibliográficos
Autores principales: Knapp, Roland A., Joseph, Maxwell B., Smith, Thomas C., Hegeman, Ericka E., Vredenburg, Vance T., Erdman Jr, James E., Boiano, Daniel M., Jani, Andrea J., Briggs, Cheryl J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: PeerJ Inc. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8742549/
https://www.ncbi.nlm.nih.gov/pubmed/35036095
http://dx.doi.org/10.7717/peerj.12712
_version_ 1784629739004100608
author Knapp, Roland A.
Joseph, Maxwell B.
Smith, Thomas C.
Hegeman, Ericka E.
Vredenburg, Vance T.
Erdman Jr, James E.
Boiano, Daniel M.
Jani, Andrea J.
Briggs, Cheryl J.
author_facet Knapp, Roland A.
Joseph, Maxwell B.
Smith, Thomas C.
Hegeman, Ericka E.
Vredenburg, Vance T.
Erdman Jr, James E.
Boiano, Daniel M.
Jani, Andrea J.
Briggs, Cheryl J.
author_sort Knapp, Roland A.
collection PubMed
description The recently-emerged amphibian chytrid fungus Batrachochytrium dendrobatidis (Bd) has had an unprecedented impact on global amphibian populations, and highlights the urgent need to develop effective mitigation strategies. We conducted in-situ antifungal treatment experiments in wild populations of the endangered mountain yellow-legged frog during or immediately after Bd-caused mass die-off events. The objective of treatments was to reduce Bd infection intensity (“load”) and in doing so alter frog-Bd dynamics and increase the probability of frog population persistence despite ongoing Bd infection. Experiments included treatment of early life stages (tadpoles and subadults) with the antifungal drug itraconazole, treatment of adults with itraconazole, and augmentation of the skin microbiome of subadults with Janthinobacterium lividum, a commensal bacterium with antifungal properties. All itraconazole treatments caused immediate reductions in Bd load, and produced longer-term effects that differed between life stages. In experiments focused on early life stages, Bd load was reduced in the 2 months immediately following treatment and was associated with increased survival of subadults. However, Bd load and frog survival returned to pre-treatment levels in less than 1 year, and treatment had no effect on population persistence. In adults, treatment reduced Bd load and increased frog survival over the entire 3-year post-treatment period, consistent with frogs having developed an effective adaptive immune response against Bd. Despite this protracted period of reduced impacts of Bd on adults, recruitment into the adult population was limited and the population eventually declined to near-extirpation. In the microbiome augmentation experiment, exposure of subadults to a solution of J. lividum increased concentrations of this potentially protective bacterium on frogs. However, concentrations declined to baseline levels within 1 month and did not have a protective effect against Bd infection. Collectively, these results indicate that our mitigation efforts were ineffective in causing long-term changes in frog-Bd dynamics and increasing population persistence, due largely to the inability of early life stages to mount an effective immune response against Bd. This results in repeated recruitment failure and a low probability of population persistence in the face of ongoing Bd infection.
format Online
Article
Text
id pubmed-8742549
institution National Center for Biotechnology Information
language English
publishDate 2022
publisher PeerJ Inc.
record_format MEDLINE/PubMed
spelling pubmed-87425492022-01-14 Effectiveness of antifungal treatments during chytridiomycosis epizootics in populations of an endangered frog Knapp, Roland A. Joseph, Maxwell B. Smith, Thomas C. Hegeman, Ericka E. Vredenburg, Vance T. Erdman Jr, James E. Boiano, Daniel M. Jani, Andrea J. Briggs, Cheryl J. PeerJ Conservation Biology The recently-emerged amphibian chytrid fungus Batrachochytrium dendrobatidis (Bd) has had an unprecedented impact on global amphibian populations, and highlights the urgent need to develop effective mitigation strategies. We conducted in-situ antifungal treatment experiments in wild populations of the endangered mountain yellow-legged frog during or immediately after Bd-caused mass die-off events. The objective of treatments was to reduce Bd infection intensity (“load”) and in doing so alter frog-Bd dynamics and increase the probability of frog population persistence despite ongoing Bd infection. Experiments included treatment of early life stages (tadpoles and subadults) with the antifungal drug itraconazole, treatment of adults with itraconazole, and augmentation of the skin microbiome of subadults with Janthinobacterium lividum, a commensal bacterium with antifungal properties. All itraconazole treatments caused immediate reductions in Bd load, and produced longer-term effects that differed between life stages. In experiments focused on early life stages, Bd load was reduced in the 2 months immediately following treatment and was associated with increased survival of subadults. However, Bd load and frog survival returned to pre-treatment levels in less than 1 year, and treatment had no effect on population persistence. In adults, treatment reduced Bd load and increased frog survival over the entire 3-year post-treatment period, consistent with frogs having developed an effective adaptive immune response against Bd. Despite this protracted period of reduced impacts of Bd on adults, recruitment into the adult population was limited and the population eventually declined to near-extirpation. In the microbiome augmentation experiment, exposure of subadults to a solution of J. lividum increased concentrations of this potentially protective bacterium on frogs. However, concentrations declined to baseline levels within 1 month and did not have a protective effect against Bd infection. Collectively, these results indicate that our mitigation efforts were ineffective in causing long-term changes in frog-Bd dynamics and increasing population persistence, due largely to the inability of early life stages to mount an effective immune response against Bd. This results in repeated recruitment failure and a low probability of population persistence in the face of ongoing Bd infection. PeerJ Inc. 2022-01-05 /pmc/articles/PMC8742549/ /pubmed/35036095 http://dx.doi.org/10.7717/peerj.12712 Text en © 2022 Knapp et al. https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, reproduction and adaptation in any medium and for any purpose provided that it is properly attributed. For attribution, the original author(s), title, publication source (PeerJ) and either DOI or URL of the article must be cited.
spellingShingle Conservation Biology
Knapp, Roland A.
Joseph, Maxwell B.
Smith, Thomas C.
Hegeman, Ericka E.
Vredenburg, Vance T.
Erdman Jr, James E.
Boiano, Daniel M.
Jani, Andrea J.
Briggs, Cheryl J.
Effectiveness of antifungal treatments during chytridiomycosis epizootics in populations of an endangered frog
title Effectiveness of antifungal treatments during chytridiomycosis epizootics in populations of an endangered frog
title_full Effectiveness of antifungal treatments during chytridiomycosis epizootics in populations of an endangered frog
title_fullStr Effectiveness of antifungal treatments during chytridiomycosis epizootics in populations of an endangered frog
title_full_unstemmed Effectiveness of antifungal treatments during chytridiomycosis epizootics in populations of an endangered frog
title_short Effectiveness of antifungal treatments during chytridiomycosis epizootics in populations of an endangered frog
title_sort effectiveness of antifungal treatments during chytridiomycosis epizootics in populations of an endangered frog
topic Conservation Biology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8742549/
https://www.ncbi.nlm.nih.gov/pubmed/35036095
http://dx.doi.org/10.7717/peerj.12712
work_keys_str_mv AT knapprolanda effectivenessofantifungaltreatmentsduringchytridiomycosisepizooticsinpopulationsofanendangeredfrog
AT josephmaxwellb effectivenessofantifungaltreatmentsduringchytridiomycosisepizooticsinpopulationsofanendangeredfrog
AT smiththomasc effectivenessofantifungaltreatmentsduringchytridiomycosisepizooticsinpopulationsofanendangeredfrog
AT hegemanerickae effectivenessofantifungaltreatmentsduringchytridiomycosisepizooticsinpopulationsofanendangeredfrog
AT vredenburgvancet effectivenessofantifungaltreatmentsduringchytridiomycosisepizooticsinpopulationsofanendangeredfrog
AT erdmanjrjamese effectivenessofantifungaltreatmentsduringchytridiomycosisepizooticsinpopulationsofanendangeredfrog
AT boianodanielm effectivenessofantifungaltreatmentsduringchytridiomycosisepizooticsinpopulationsofanendangeredfrog
AT janiandreaj effectivenessofantifungaltreatmentsduringchytridiomycosisepizooticsinpopulationsofanendangeredfrog
AT briggscherylj effectivenessofantifungaltreatmentsduringchytridiomycosisepizooticsinpopulationsofanendangeredfrog