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Freshwater Mussel Viromes Increase Rapidly in Diversity and Abundance when Hosts Are Released from Captivity into the Wild
by
, , , , , and
Jordan C. Richard
1,2,*,
Tim W. Lane
3,
Rose E. Agbalog
2,
Sarah L. Colletti
3,
Tiffany C. Leach
3,
Christopher D. Dunn
1,
Nathan Bollig
4,5,
Addison R. Plate
1,
Joseph T. Munoz
1,
Eric M. Leis
6,
Susan Knowles
4,
Isaac F. Standish
6,
Diane L. Waller
7 and
Tony L. Goldberg
1,* 1
Department of Pathobiological Sciences, University of Wisconsin-Madison, Madison, WI 53711, USA
2
Southwestern Virginia Field Office, U.S. Fish and Wildlife Service, Abingdon, VA 24210, USA
3
Aquatic Wildlife Conservation Center, Virginia Department of Wildlife Resources, Marion, VA 24354, USA
4
U.S. Geological Survey, National Wildlife Health Center, Madison, WI 53711, USA
5
Department of Biostatistics and Medical Informatics, University of Wisconsin-Madison, Madison, WI 53711, USA
6
La Crosse Fish Health Center, Midwest Fisheries Center, U.S. Fish and Wildlife Service, Onalaska, WI 54650, USA
7
U.S. Geological Survey, Upper Midwest Environmental Sciences Center, La Crosse, WI 54603, USA
*
Authors to whom correspondence should be addressed.
Animals 2024, 14(17), 2531; https://doi.org/10.3390/ani14172531 (registering DOI)
Submission received: 22 July 2024
/
Revised: 19 August 2024
/
Accepted: 27 August 2024
/
Published: 30 August 2024
(This article belongs to the Section Ecology and Conservation)
Simple Summary
Freshwater mussels create habitat, filter water, and enhance food webs, but they are also among the world’s most imperiled taxa. Conservation efforts largely rely on captive propagation in which mussels are grown in protected aquaculture environments (hatcheries) for later release. Recent evidence has highlighted the importance of pathogens in population losses of freshwater mussels. In response to ongoing mass mortality events of freshwater mussels in the Upper Tennessee River Basin in Virginia and Tennessee, USA, we conducted a multi-year study to document viruses across multiple restoration sites and compare them to viruses in mussels from the hatchery. Viral communities changed greatly after mussels were released. Of the 681 viruses of the 27 families we documented, only 20 viruses were found exclusively in hatchery mussels, compared to 451 viruses found only in mussels stocked to the wild. After release, mussels rapidly acquired new viruses, and the number of viruses increased steadily over time. These findings have implications for how mussel introduction programs might be managed for greater success, for example, by incorporating acclimatization periods prior to full release.
Abstract
Freshwater mussels (order: Unionida) are highly imperiled globally and are increasingly the focus of captive propagation efforts to protect and restore wild populations. The Upper Tennessee River Basin (UTRB) in Virginia is a freshwater biodiversity hotspot hosting at least 45 of North America’s ~300 species of freshwater mussels, including 21 threatened and endangered species listed under the U.S. Endangered Species Act. Recent studies have documented that viruses and other microbes have contributed to freshwater mussel population declines in the UTRB. We conducted a multi-year longitudinal study of captive-reared hatchery mussels released to restoration sites throughout the UTRB to evaluate their viromes and compare them to captive hatchery environments. We documented 681 viruses from 27 families. The hatchery mussels had significantly less viruses than those deployed to wild sites, with only 20 viruses unique to the hatchery mussels. After the hatchery mussels were released into the wild, their number of viruses initially spiked and then increased steadily over time, with 451 viruses in total unique to the mussels in the wild. We found Clinch densovirus 1 (CDNV-1), a virus previously associated with mass mortality events in the Clinch River, in all samples, but the wild site mussels consistently had significantly higher CDNV-1 levels than those held in the hatchery. Our data document substantial differences between the viruses in the mussels in the hatchery and wild environments and rapid virome shifts after the mussels are released to the wild sites. These findings indicate that mussel release programs might benefit from acclimatization periods or other measures to mitigate the potential negative effects of rapid exposure to infectious agents found in natural environments.
