Social Behavior, Community Composition, Pathogen Strain, and Host Symbionts Influence Fungal Disease Dynamics in Salamanders
The emerging fungal pathogen, Batrachochytrium dendrobatidis (Bd), which can cause a fatal disease called chytridiomycosis, is implicated in the collapse of hundreds of host amphibian species. We describe chytridiomycosis dynamics in two co-occurring terrestrial salamander species, the Santa Lucia M...
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Frontiers Media S.A.
2021-11-01
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| Series: | Frontiers in Veterinary Science |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fvets.2021.742288/full |
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| author | Mae Cowgill Andrew G. Zink Wesley Sparagon Tiffany A. Yap Hasan Sulaeman Michelle S. Koo Vance T. Vredenburg Vance T. Vredenburg |
| author_facet | Mae Cowgill Andrew G. Zink Wesley Sparagon Tiffany A. Yap Hasan Sulaeman Michelle S. Koo Vance T. Vredenburg Vance T. Vredenburg |
| author_sort | Mae Cowgill |
| collection | DOAJ |
| description | The emerging fungal pathogen, Batrachochytrium dendrobatidis (Bd), which can cause a fatal disease called chytridiomycosis, is implicated in the collapse of hundreds of host amphibian species. We describe chytridiomycosis dynamics in two co-occurring terrestrial salamander species, the Santa Lucia Mountains slender salamander, Batrachoseps luciae, and the arboreal salamander, Aneides lugubris. We (1) conduct a retrospective Bd-infection survey of specimens collected over the last century, (2) estimate present-day Bd infections in wild populations, (3) use generalized linear models (GLM) to identify biotic and abiotic correlates of infection risk, (4) investigate susceptibility of hosts exposed to Bd in laboratory trials, and (5) examine the ability of host skin bacteria to inhibit Bd in culture. Our historical survey of 2,866 specimens revealed that for most of the early 20th century (~1920–1969), Bd was not detected in either species. By the 1990s the proportion of infected specimens was 29 and 17% (B. luciae and A. lugubris, respectively), and in the 2010s it was 10 and 17%. This was similar to the number of infected samples from contemporary populations (2014–2015) at 10 and 18%. We found that both hosts experience signs of chytridiomycosis and suffered high Bd-caused mortality (88 and 71% for B. luciae and A. lugubris, respectively). Our GLM revealed that Bd-infection probability was positively correlated with intraspecific group size and proximity to heterospecifics but not to abiotic factors such as precipitation, minimum temperature, maximum temperature, mean temperature, and elevation, or to the size of the hosts. Finally, we found that both host species contain symbiotic skin-bacteria that inhibit growth of Bd in laboratory trials. Our results provide new evidence consistent with other studies showing a relatively recent Bd invasion of amphibian host populations in western North America and suggest that the spread of the pathogen may be enabled both through conspecific and heterospecific host interactions. Our results suggest that wildlife disease studies should assess host-pathogen dynamics that consider the interactions and effects of multiple hosts, as well as the historical context of pathogen invasion, establishment, and epizootic to enzootic transitions to better understand and predict disease dynamics. |
| first_indexed | 2024-12-17T21:15:02Z |
| format | Article |
| id | doaj.art-4de2fd8ab71e49ca85d85e0685efb55e |
| institution | Directory Open Access Journal |
| issn | 2297-1769 |
| language | English |
| last_indexed | 2024-12-17T21:15:02Z |
| publishDate | 2021-11-01 |
| publisher | Frontiers Media S.A. |
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| series | Frontiers in Veterinary Science |
| spelling | doaj.art-4de2fd8ab71e49ca85d85e0685efb55e2022-12-21T21:32:21ZengFrontiers Media S.A.Frontiers in Veterinary Science2297-17692021-11-01810.3389/fvets.2021.742288742288Social Behavior, Community Composition, Pathogen Strain, and Host Symbionts Influence Fungal Disease Dynamics in SalamandersMae Cowgill0Andrew G. Zink1Wesley Sparagon2Tiffany A. Yap3Hasan Sulaeman4Michelle S. Koo5Vance T. Vredenburg6Vance T. Vredenburg7Department of Biology, San Francisco State University, San Francisco, CA, United StatesDepartment of Biology, San Francisco State University, San Francisco, CA, United StatesDaniel K. Inouye Center for Microbial Oceanography: Research and Education, Department of Oceanography and Sea Grant College Program, UUniversity of Hawai‘i at Mānoa, HI, United StatesCenter for Biological Diversity, Oakland, CA, United StatesDepartment of Biology, San Francisco State University, San Francisco, CA, United StatesMuseum of Vertebrate Zoology, University of California, Berkeley, Berkeley, CA, United StatesDepartment of Biology, San Francisco State University, San Francisco, CA, United StatesMuseum of Vertebrate Zoology, University of California, Berkeley, Berkeley, CA, United StatesThe emerging fungal pathogen, Batrachochytrium dendrobatidis (Bd), which can cause a fatal disease called chytridiomycosis, is implicated in the collapse of hundreds of host amphibian species. We describe chytridiomycosis dynamics in two co-occurring terrestrial salamander species, the Santa Lucia Mountains slender salamander, Batrachoseps luciae, and the arboreal salamander, Aneides lugubris. We (1) conduct a retrospective Bd-infection survey of specimens collected over the last century, (2) estimate present-day Bd infections in wild populations, (3) use generalized linear models (GLM) to identify biotic and abiotic correlates of infection risk, (4) investigate susceptibility of hosts exposed to Bd in laboratory trials, and (5) examine the ability of host skin bacteria to inhibit Bd in culture. Our historical survey of 2,866 specimens revealed that for most of the early 20th century (~1920–1969), Bd was not detected in either species. By the 1990s the proportion of infected specimens was 29 and 17% (B. luciae and A. lugubris, respectively), and in the 2010s it was 10 and 17%. This was similar to the number of infected samples from contemporary populations (2014–2015) at 10 and 18%. We found that both hosts experience signs of chytridiomycosis and suffered high Bd-caused mortality (88 and 71% for B. luciae and A. lugubris, respectively). Our GLM revealed that Bd-infection probability was positively correlated with intraspecific group size and proximity to heterospecifics but not to abiotic factors such as precipitation, minimum temperature, maximum temperature, mean temperature, and elevation, or to the size of the hosts. Finally, we found that both host species contain symbiotic skin-bacteria that inhibit growth of Bd in laboratory trials. Our results provide new evidence consistent with other studies showing a relatively recent Bd invasion of amphibian host populations in western North America and suggest that the spread of the pathogen may be enabled both through conspecific and heterospecific host interactions. Our results suggest that wildlife disease studies should assess host-pathogen dynamics that consider the interactions and effects of multiple hosts, as well as the historical context of pathogen invasion, establishment, and epizootic to enzootic transitions to better understand and predict disease dynamics.https://www.frontiersin.org/articles/10.3389/fvets.2021.742288/fullchytridiomycosissocialitysymbiotic bacteriahistorical prevalencemicrobiomeBatrachochytrium dendrobatidis |
| spellingShingle | Mae Cowgill Andrew G. Zink Wesley Sparagon Tiffany A. Yap Hasan Sulaeman Michelle S. Koo Vance T. Vredenburg Vance T. Vredenburg Social Behavior, Community Composition, Pathogen Strain, and Host Symbionts Influence Fungal Disease Dynamics in Salamanders Frontiers in Veterinary Science chytridiomycosis sociality symbiotic bacteria historical prevalence microbiome Batrachochytrium dendrobatidis |
| title | Social Behavior, Community Composition, Pathogen Strain, and Host Symbionts Influence Fungal Disease Dynamics in Salamanders |
| title_full | Social Behavior, Community Composition, Pathogen Strain, and Host Symbionts Influence Fungal Disease Dynamics in Salamanders |
| title_fullStr | Social Behavior, Community Composition, Pathogen Strain, and Host Symbionts Influence Fungal Disease Dynamics in Salamanders |
| title_full_unstemmed | Social Behavior, Community Composition, Pathogen Strain, and Host Symbionts Influence Fungal Disease Dynamics in Salamanders |
| title_short | Social Behavior, Community Composition, Pathogen Strain, and Host Symbionts Influence Fungal Disease Dynamics in Salamanders |
| title_sort | social behavior community composition pathogen strain and host symbionts influence fungal disease dynamics in salamanders |
| topic | chytridiomycosis sociality symbiotic bacteria historical prevalence microbiome Batrachochytrium dendrobatidis |
| url | https://www.frontiersin.org/articles/10.3389/fvets.2021.742288/full |
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