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...
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PeerJ Inc.
2022-01-01
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| Online Access: | https://peerj.com/articles/12712.pdf |
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| author | Roland A. Knapp Maxwell B. Joseph Thomas C. Smith Ericka E. Hegeman Vance T. Vredenburg James E. Erdman Jr Daniel M. Boiano Andrea J. Jani Cheryl J. Briggs |
| author_facet | Roland A. Knapp Maxwell B. Joseph Thomas C. Smith Ericka E. Hegeman Vance T. Vredenburg James E. Erdman Jr Daniel M. Boiano Andrea J. Jani Cheryl J. Briggs |
| author_sort | Roland A. Knapp |
| collection | DOAJ |
| 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. |
| first_indexed | 2024-03-09T08:03:39Z |
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| language | English |
| last_indexed | 2024-03-09T08:03:39Z |
| publishDate | 2022-01-01 |
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| spelling | doaj.art-7b41aa444c494884959a688d537c0d482023-12-03T00:31:18ZengPeerJ Inc.PeerJ2167-83592022-01-0110e1271210.7717/peerj.12712Effectiveness of antifungal treatments during chytridiomycosis epizootics in populations of an endangered frogRoland A. Knapp0Maxwell B. Joseph1Thomas C. Smith2Ericka E. Hegeman3Vance T. Vredenburg4James E. Erdman Jr5Daniel M. Boiano6Andrea J. Jani7Cheryl J. Briggs8Sierra Nevada Aquatic Research Laboratory, University of California, Mammoth Lakes, California, United StatesEarth Lab, University of Colorado, Boulder, Colorado, United StatesSierra Nevada Aquatic Research Laboratory, University of California, Mammoth Lakes, California, United StatesSierra Nevada Aquatic Research Laboratory, University of California, Mammoth Lakes, California, United StatesDepartment of Biology, San Francisco State University, San Francisco, California, United StatesCalifornia Department of Fish and Wildlife, Bishop, California, United StatesSequoia and Kings Canyon National Parks, National Park Service, Three Rivers, California, United StatesPacific Biosciences Research Center, University of Hawai’i at Mànoa, Honolulu, Hawai’i, United StatesDepartment of Ecology, Evolution, and Marine Biology, University of California, Santa Barbara, California, United StatesThe 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.https://peerj.com/articles/12712.pdfAmphibian chytrid fungusBatrachochytrium dendrobatidisWildlife diseaseEpizooticHost population declineAntifungal treatment |
| spellingShingle | Roland A. Knapp Maxwell B. Joseph Thomas C. Smith Ericka E. Hegeman Vance T. Vredenburg James E. Erdman Jr Daniel M. Boiano Andrea J. Jani Cheryl J. Briggs Effectiveness of antifungal treatments during chytridiomycosis epizootics in populations of an endangered frog PeerJ Amphibian chytrid fungus Batrachochytrium dendrobatidis Wildlife disease Epizootic Host population decline Antifungal treatment |
| 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 | Amphibian chytrid fungus Batrachochytrium dendrobatidis Wildlife disease Epizootic Host population decline Antifungal treatment |
| url | https://peerj.com/articles/12712.pdf |
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