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Microbiome differences between wild and aquarium whitespotted eagle rays (Aetobatus narinari)

BACKGROUND: Animal-associated microbiomes can be influenced by both host and environmental factors. Comparing wild animals to those in zoos or aquariums can help disentangle the effects of host versus environmental factors, while also testing whether managed conditions foster a ‘natural’ host microb...

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Autores principales: Clavere-Graciette, Ana G., McWhirt, Mary E., Hoopes, Lisa A., Bassos-Hull, Kim, Wilkinson, Krystan A., Stewart, Frank J., Pratte, Zoe A.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9128078/
https://www.ncbi.nlm.nih.gov/pubmed/35606841
http://dx.doi.org/10.1186/s42523-022-00187-8
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author Clavere-Graciette, Ana G.
McWhirt, Mary E.
Hoopes, Lisa A.
Bassos-Hull, Kim
Wilkinson, Krystan A.
Stewart, Frank J.
Pratte, Zoe A.
author_facet Clavere-Graciette, Ana G.
McWhirt, Mary E.
Hoopes, Lisa A.
Bassos-Hull, Kim
Wilkinson, Krystan A.
Stewart, Frank J.
Pratte, Zoe A.
author_sort Clavere-Graciette, Ana G.
collection PubMed
description BACKGROUND: Animal-associated microbiomes can be influenced by both host and environmental factors. Comparing wild animals to those in zoos or aquariums can help disentangle the effects of host versus environmental factors, while also testing whether managed conditions foster a ‘natural’ host microbiome. Focusing on an endangered elasmobranch species—the whitespotted eagle ray Aetobatus narinari—we compared the skin, gill, and cloaca microbiomes of wild individuals to those at Georgia Aquarium. Whitespotted eagle ray microbiomes from Georgia Aquarium were also compared to those of cownose rays (Rhinoptera bonasus) in the same exhibit, allowing us to explore the effect of host identity on the ray microbiome. RESULTS: Long-term veterinary monitoring indicated that the rays in managed care did not have a history of disease and maintained health parameters consistent with those of wild individuals, with one exception. Aquarium whitespotted eagle rays were regularly treated to control parasite loads, but the effects on animal health were subclinical. Microbiome α- and β-diversity differed between wild versus aquarium whitespotted eagle rays at all body sites, with α-diversity significantly higher in wild individuals. β-diversity differences in wild versus aquarium whitespotted eagle rays were greater for skin and gill microbiomes compared to those of the cloaca. At each body site, we also detected microbial taxa shared between wild and aquarium eagle rays. Additionally, the cloaca, skin, and gill microbiomes of aquarium eagle rays differed from those of cownose rays in the same exhibit. Potentially pathogenic bacteria were at low abundance in all wild and aquarium rays. CONCLUSION: For whitespotted eagle rays, managed care was associated with a microbiome differing significantly from that of wild individuals. These differences were not absolute, as the microbiome of aquarium rays shared members with that of wild counterparts and was distinct from that of a cohabitating ray species. Eagle rays under managed care appear healthy, suggesting that their microbiomes are not associated with compromised host health. However, the ray microbiome is dynamic, differing with both environmental factors and host identity. Monitoring of aquarium ray microbiomes over time may identify taxonomic patterns that co-vary with host health. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s42523-022-00187-8.
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spelling pubmed-91280782022-05-25 Microbiome differences between wild and aquarium whitespotted eagle rays (Aetobatus narinari) Clavere-Graciette, Ana G. McWhirt, Mary E. Hoopes, Lisa A. Bassos-Hull, Kim Wilkinson, Krystan A. Stewart, Frank J. Pratte, Zoe A. Anim Microbiome Research Article BACKGROUND: Animal-associated microbiomes can be influenced by both host and environmental factors. Comparing wild animals to those in zoos or aquariums can help disentangle the effects of host versus environmental factors, while also testing whether managed conditions foster a ‘natural’ host microbiome. Focusing on an endangered elasmobranch species—the whitespotted eagle ray Aetobatus narinari—we compared the skin, gill, and cloaca microbiomes of wild individuals to those at Georgia Aquarium. Whitespotted eagle ray microbiomes from Georgia Aquarium were also compared to those of cownose rays (Rhinoptera bonasus) in the same exhibit, allowing us to explore the effect of host identity on the ray microbiome. RESULTS: Long-term veterinary monitoring indicated that the rays in managed care did not have a history of disease and maintained health parameters consistent with those of wild individuals, with one exception. Aquarium whitespotted eagle rays were regularly treated to control parasite loads, but the effects on animal health were subclinical. Microbiome α- and β-diversity differed between wild versus aquarium whitespotted eagle rays at all body sites, with α-diversity significantly higher in wild individuals. β-diversity differences in wild versus aquarium whitespotted eagle rays were greater for skin and gill microbiomes compared to those of the cloaca. At each body site, we also detected microbial taxa shared between wild and aquarium eagle rays. Additionally, the cloaca, skin, and gill microbiomes of aquarium eagle rays differed from those of cownose rays in the same exhibit. Potentially pathogenic bacteria were at low abundance in all wild and aquarium rays. CONCLUSION: For whitespotted eagle rays, managed care was associated with a microbiome differing significantly from that of wild individuals. These differences were not absolute, as the microbiome of aquarium rays shared members with that of wild counterparts and was distinct from that of a cohabitating ray species. Eagle rays under managed care appear healthy, suggesting that their microbiomes are not associated with compromised host health. However, the ray microbiome is dynamic, differing with both environmental factors and host identity. Monitoring of aquarium ray microbiomes over time may identify taxonomic patterns that co-vary with host health. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s42523-022-00187-8. BioMed Central 2022-05-23 /pmc/articles/PMC9128078/ /pubmed/35606841 http://dx.doi.org/10.1186/s42523-022-00187-8 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research Article
Clavere-Graciette, Ana G.
McWhirt, Mary E.
Hoopes, Lisa A.
Bassos-Hull, Kim
Wilkinson, Krystan A.
Stewart, Frank J.
Pratte, Zoe A.
Microbiome differences between wild and aquarium whitespotted eagle rays (Aetobatus narinari)
title Microbiome differences between wild and aquarium whitespotted eagle rays (Aetobatus narinari)
title_full Microbiome differences between wild and aquarium whitespotted eagle rays (Aetobatus narinari)
title_fullStr Microbiome differences between wild and aquarium whitespotted eagle rays (Aetobatus narinari)
title_full_unstemmed Microbiome differences between wild and aquarium whitespotted eagle rays (Aetobatus narinari)
title_short Microbiome differences between wild and aquarium whitespotted eagle rays (Aetobatus narinari)
title_sort microbiome differences between wild and aquarium whitespotted eagle rays (aetobatus narinari)
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9128078/
https://www.ncbi.nlm.nih.gov/pubmed/35606841
http://dx.doi.org/10.1186/s42523-022-00187-8
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