Mass mortality in freshwater mussels (Actinonaias pectorosa) in the Clinch River, USA, linked to a novel densovirus

Jordan C Richard,Tony L Goldberg,Rose Agbalog,Joel Putnam,Christopher D Dunn,Eric Leis,Susan Knowles,Diane Waller

doi:10.1038/s41598-020-71459-z

Abstract

Freshwater mussels (order Unionida) are among the world’s most biodiverse but imperiled taxa. Recent unionid mass mortality events around the world threaten ecosystem services such as water filtration, nutrient cycling, habitat stabilization, and food web enhancement, but causes have remained elusive. To examine potential infectious causes of these declines, we studied mussels in Clinch River, Virginia and Tennessee, USA, where the endemic and once-predominant pheasantshell (Actinonaias pectorosa) has suffered precipitous declines since approximately 2016. Using metagenomics, we identified 17 novel viruses in Clinch River pheasantshells. However, only one virus, a novel densovirus (Parvoviridae; Densovirinae), was epidemiologically linked to morbidity. Clinch densovirus 1 was 11.2 times more likely to be found in cases (moribund mussels) than controls (apparently healthy mussels from the same or matched sites), and cases had 2.7 (log10) times higher viral loads than controls. Densoviruses cause lethal epidemic disease in invertebrates, including shrimp, cockroaches, crickets, moths, crayfish, and sea stars. Viral infection warrants consideration as a factor in unionid mass mortality events either as a direct cause, an indirect consequence of physiological compromise, or a factor interacting with other biological and ecological stressors to precipitate mortality.

Highlights

Freshwater mussels are important members of freshwater biomes, providing ecosystem services such as water filtration, nutrient cycling and deposition, physical habitat stabilization, and food web enhancement[1]
Unlike the aforementioned gradual declines, many mass mortality events in freshwater mussels have not been directly attributed to any specific environmental changes or events[12]
The Clinch River watershed in southwestern Virginia and northeastern Tennessee is one of the most ecologically important and biodiverse freshwater systems in North America[15]

Summary

Introduction

Freshwater mussels (order Unionida) are important members of freshwater biomes, providing ecosystem services such as water filtration, nutrient cycling and deposition, physical habitat stabilization, and food web enhancement[1]. Unlike the aforementioned gradual declines, many mass mortality events in freshwater mussels have not been directly attributed to any specific environmental changes or events[12]. Mass mortality events often affect only a single species of mussel within a broad ecological community. Collection of shells from freshly dead mussels, and comparisons to known species assemblage patterns demonstrated that the pheasantshell (Actinonaias pectorosa) comprised a disproportionate (to their relative abundance within the community) and overwhelming majority of affected individuals[17]. These mortality events resulted in population declines of approximately 50–90% of pheasantshells at monitoring sites throughout the lower river. There is great concern that this decline, if unchecked, could permanently alter the Clinch River’s ecology and irreversibly affect the ecosystem services that its mussels provide

Methods

Results

Conclusion