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  1. Abstract

    The United States of America has a diverse collection of freshwater mussels comprising 301 species distributed among 59 genera and two families (Margaritiferidae and Unionidae), each having a unique suite of traits. Mussels are among the most imperilled animals and are critical components of their ecosystems, and successful management, conservation and research requires a cohesive and widely accessible data source. Although trait-based analysis for mussels has increased, only a small proportion of traits reflecting mussel diversity in this region has been collated. Decentralized and non-standardized trait information impedes large-scale analysis. Assembling trait data in a synthetic dataset enables comparison across species and lineages and identification of data gaps. We collated data from the primary literature, books, state and federal reports, theses and dissertations, and museum collections into a centralized dataset covering information on taxonomy, morphology, reproductive ecology and life history, fish hosts, habitats, thermal tolerance, geographic distribution, available genetic information, and conservation status. By collating these traits, we aid researchers in assessing variation in mussel traits and modelling ecosystem change.

     
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    Free, publicly-accessible full text available December 1, 2024
  2. Abstract

    Understanding patterns of diversity across macro (e.g. species‐level) and micro (e.g. molecular‐level) scales can shed light on community function and stability by elucidating the abiotic and biotic drivers of diversity within ecological communities. We examined the relationships among taxonomic and genetic metrics of diversity in freshwater mussels (Bivalvia: Unionidae), an ecologically important and species‐rich group in the southeastern United States. Using quantitative community surveys and reduced‐representation genome sequencing across 22 sites in seven rivers and two river basins, we surveyed 68 mussel species and sequenced 23 of these species to characterize intrapopulation genetic variation. We tested for the presence of species diversity–abundance correlations (i.e. the more‐individuals hypothesis, MIH), species‐genetic diversity correlations (SGDCs) and abundance‐genetic diversity correlations (AGDCs) across all sites to evaluate relationships between different metrics of diversity. Sites with greater cumulative multispecies density (a standardized metric of abundance) had a greater number of species, consistent with the MIH hypothesis. Intrapopulation genetic diversity was strongly associated with the density of most species, indicating the presence of AGDCs. However, there was no consistent evidence for SGDCs. Although sites with greater overall densities of mussels had greater species richness, sites with higher genetic diversity did not always exhibit positive correlations with species richness, suggesting that there are spatial and evolutionary scales at which the processes influencing community‐level diversity and intraspecific diversity differ. Our work reveals the importance of local abundance as indicator (and possibly a driver) of intrapopulation genetic diversity.

     
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  3. Abstract

    Invasive species introduction is one of the major ongoing ecological global crises. Identifying factors responsible for the success of invasive species is key for the implementation of effective management actions. The invasive filter-feeding bivalve,Corbicula, is of particular interest because it has become ubiquitous in many river basins across North America and elsewhere. Here we sampled bivalve assemblages, environmental indicators, and land cover parameters in the Ouachita highlands in southeastern Oklahoma and southwestern Arkansas, and in the Gulf Coastal Plain of Alabama to test three working models (using structural equation modeling, SEM) based on a priori scientific knowledge regardingCorbiculainvasions. Our models tested three competing hypotheses: (1) Native mussel declines are related to land use changes at the watershed level and subsequentCorbiculacolonization is a result of an empty niche; (2)Corbiculaabundance is one of the factors responsible for native mussel declines and has an interactive effect with land use change at the watershed level; (3) Native mussel declines andCorbiculasuccess are both related to land use changes at the watershed level. We found no evidence for the first two hypotheses. However, we found that environmental indicators and land cover parameters at the watershed scale were robust predictors ofCorbiculaabundance. In particular, agricultural land cover was positively related withCorbiculadensity. These results suggest that further improvement of conventional agricultural practices including the optimization of fertilizer delivery systems may represent an opportunity to manage this species by limiting nutrient inputs to stream ecosystems. Preservation of extensive floodplain habitats may help buffer these inputs by providing key ecosystem services including sediment and nutrient retention.

     
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  4. Abstract

    Freshwater mussels are important for nutrient cycling and ecosystem health as they filter feed on their surrounding water. This filter feeding makes these bivalves especially sensitive to conditions in their environment. Gut microbial communities (microbiomes) have been recognised as important to both host organism and ecosystem health; however, how freshwater mussel microbiomes are organised and influenced is unclear.

    In this study, the gut bacterial microbiome of Threeridge mussel,Amblema plicata, was compared across two river basins, five rivers, and nine local sites in the south‐eastern U.S.A. Mussel gut tissue was dissected, DNA extracted, and the microbiome characterised by high throughput sequencing of the V4 region of the 16S ribosomal RNA gene.

    Planctomycetes, Firmicutes, and Cyanobacteria were the most common bacterial phyla within the guts of all sampledA.plicata. However, the relative abundances of these major bacterial phyla differed between mussels sampled from different rivers and river basins, as did the relative abundance of specific bacterial operational taxonomic units (OTUs). Despite these differences, a core microbiome was identified across all mussels, with eight OTUs being consistent members of theA.plicatamicrobiome at all sites, the most abundant OTU identifying as a member of the family Planctomycetaceae. Geographic distance between sites was not correlated with similarity in the structure of the gut microbiome, which was more related to site physicochemistry.

    Overall, these results suggest that while physicochemical conditions affect the composition of transient bacteria in the Threeridge mussel gut microbiome, the core microbiome is largely unaffected, and a portion of theA.plicatamicrobiome is retained regardless of the river system.

    How long transient bacteria remain in the gut, and to what extent these transient microbes aid in host function is still unknown. Core microbiota have been found to aid in multiple functions within animal hosts, and within freshwater mussels this core microbiome may aid in nutrient processing and cycling. Therefore, it is important to look at both transient and core microbes when studying the structure of freshwater invertebrate microbiomes.

     
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  5. Abstract

    This study aimed to identify the importance of ecological factors to distribution patterns of the invasive Clam (Corbicula fluminea) relative to native mussels (family: Unionidae) across seven rivers within the Mobile and Tennessee basins, Southeast United States. We quantitatively surveyed dense, diverse native mussel aggregations across 20 river reaches and estimated mussel density, biomass, and species richness along with density of invasiveC.fluminea(hereafterCorbicula). We measured substrate particle size, velocity, and depth in quadrats where animals were collected. Additionally, we characterized reach scale environmental parameters including seston quantity and quality (% Carbon, % Nitrogen, % Phosphorous), water chemistry (ammonium [], soluble reactive phosphorous [SRP]), and watershed area and land cover. Using model selection, logistic regression, and multivariate analysis, we characterized habitat features and their association to invasiveCorbiculawithin mussel beds. We found thatCorbiculawere more likely to occur and more abundant in quadrats with greater mussel biomass, larger substrate size, faster water velocity, and shallower water depth. At the reach scale,Corbiculadensities increased where particle sizes were larger. Mussel richness, density, and biomass increased with watershed area. Water column increased at reaches with more urban land cover. No land cover variables influencedCorbiculapopulations or mussel communities. The strong overlapping distribution ofCorbiculaand mussels support the hypothesis thatCorbiculaare not necessarily limited by habitat factors and may be passengers of change in rivers where mussels have declined due to habitat degradation. WhetherCorbiculais facilitated by mussels or negatively interacts with mussels in these systems remains to be seen. Focused experiments that manipulate patch scale variables would improve our understanding of the role of species interactions (e.g., competition, predation, facilitation) or physical habitat factors in influencing spatial overlap betweenCorbiculaand native mussels.

     
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  6. Abstract

    Obovaria olivariais a species of freshwater mussel native to the Mississippi River and Laurentian Great Lakes‐St. Lawrence River drainages of North America. This mussel has experienced population declines across large parts of its distribution and is imperiled in many jurisdictions.Obovaria olivariauses the similarly imperiledAcipenser fulvescens(Lake Sturgeon) as a host for its glochidia. We employed mitochondrial DNA sequencing and restriction site‐associated DNA sequencing (RAD‐seq) to assess patterns of genetic diversity and population structure ofOolivariafrom 19 collection locations including the St. Lawrence River drainage, the Great Lakes drainage, the Upper Mississippi River drainage, the Ohioan River drainage, and the Mississippi Embayment. Heterozygosity was highest in Upper Mississippi and Great Lakes populations, followed by a reduction in diversity and relative effective population size in the St. Lawrence populations. PairwiseFSTranged from 0.00 to 0.20, and analyses of genetic structure revealed two major ancestral populations, one including all St. Lawrence River/Ottawa River sites and the other including remaining sites; however, significant admixture and isolation by river distance across the range were evident. The genetic diversity and structure ofOolivariais consistent with the existing literature onAcipenser fulvescensand suggests that, although northern and southernOolivariapopulations are genetically distinct, genetic structure inOolivariais largely clinal rather than discrete across its range. Conservation and restoration efforts ofOolivariashould prioritize the maintenance and restoration of locations whereOolivariaremain, especially in northern rivers, and to ensure connectivity that will facilitate dispersal ofAcipenser fulvescensand movement of encysted glochidia.

     
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  7. Abstract

    Biogeochemical cycling has often been characterized by physical and microbial processes, yet animals can be essential mediators of energy and nutrients in ecosystems. Excretion by aggregated animals can be an important local source of inorganic nutrients in green food webs; however, whether animals are a source of dissolved energy that can support brown food webs is understudied.

    We tested whether animal aggregations are a substantial flux of bioavailable dissolved organic matter (DOM) by studying spatially stable, biogeochemical hotspots formed by filter‐feeding freshwater mussels. We used parallel‐factor analysis to quantify DOM fluorescent components composition of mussel excretion and expected digestive breakdown of particulate food sources would lead to excretion of labile DOM. Next, we combined measured excretion rates of DOM, ammonium (, N) and phosphorous (SRP; P) for 22 species with biomass estimates for 14 aggregations to quantify contributions of DOM, N and P to local availability. Because mussels occupy distinct stoichiometric niches, we anticipated that differences in species biomass and assemblage structure would elicit different flux and stoichiometries of aggregate excretion.

    Aggregate dissolved organic carbon (DOC) excretion was minor (1%–11%) compared to N (12%–2,860%) and P (1%–97%), yet generalities across assemblages emerged regarding organic matter transformation by mussels towards labile protein‐like compounds compared to abundant aromatic, humic compounds in ambient water.

    Aggregate excretion of labile DOM was a substantial pool of bioavailable energy, contributing 2%–114% of local labile DOM. Spatial differences in assemblage structure led to strong differences in aggregate flux and stoichiometry driven by biomass and stoichiometric trait expression of species with contrasting dominance patterns.

    Under the nutrient conditions of our study (high C:nutrient), biogeochemical hotspots associated with low‐trophic position animal biomass may indirectly control energy flow to the brown food web by shifting C:nutrient stoichiometry available to microbes or directly by increasing the flux of microbially available DOM. Collectively, our results highlight a potentially substantial flux of labile energy and nutrients to microbial communities through the transformation of ingested organic matter by aggregations of animals and emphasize that shared functional trait classification may not translate into shared ecological function.

    A freePlain Language Summarycan be found within the Supporting Information of this article.

     
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  8. Positive biodiversity–ecosystem functioning (BEF) relationships observed in experiments can be challenging to identify in natural communities. Freshwater animal communities are disproportionately harmed by global change that results in accelerated species loss. Understanding how animal-mediated ecosystems functions may change as a result of global change can help determine whether biodiversity or species-specific conservation will be effective at maintaining function. Unionid mussels represent half of imperiled species in freshwater ecosystems globally and perform important ecological functions such as water filtration and nutrient recycling. We explored BEF relationships for 22 naturally assembled mussel aggregations spanning three river basins. We used the Price equation to partition the contributions of species richness, composition, and context dependent interactions to two functions of interests: spatially-explicit standing-stock biomass (indirect proxy for function) and species-specific nitrogen (N) excretion rates (direct measure of N recycling). Random and non-random species loss each reduced biomass and N recycling. Many rare species with low contributions to biomass contributed to standing-stock biomass in all basins. Widespread species had variable function across sites, such that context dependent effects (CDEs) outweighed richness effects on standing-stock biomass in two basins, and were similar to richness effects in the third. Richness effects outweighed CDEs for N recycling. Thus, many species contributed a low proportion to overall N-recycling; a product we attribute to the high evenness and functional effect trait diversity associated with these communities. The loss of low-functioning species reduced the function of persisting species. This novel result using observational data adds evidence that positive species interactions, such as interspecific facilitation, may be a mechanism by which biodiversity enhances ecosystem functions. Our work stresses the importance of evaluating species-specific contributions to functions in diverse systems, such as nutrient cycling when maintaining specific animal-mediated functions is a management goal because indirect proxies may not completely characterize BEF relationships. 
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    Free, publicly-accessible full text available June 20, 2024
  9. The use of environmental DNA (eDNA) to assess aquatic biodiversity is a growing field with great potential for monitoring and managing threatened species, like freshwater mussel (Unionidae) populations. Freshwater mussels are globally imperiled and serve essential roles in aquatic systems as a food source and as a natural water filter making their management essential for ecosystem health. Unfortunately, mussel populations are often understudied, and challenges exist to accurately and efficiently describe the full suite of species present. Multispecies eDNA approaches may also be more challenging where freshwater mussel populations are most diverse due to ongoing and significant taxonomic restructuring that has been further complicated by molecular phylogenies using mitochondrial genes. For this study, we developed a microfluidic metabarcoding array that targets a wide range of species, from invertebrates to fishes, with an emphasis on detecting unionid mussels known to be present in the Sipsey River, Alabama. We compared mussel species diversity across six sites with well-studied mussel assemblages using eDNA surveys and traditional quadrat surveys in 2016. We examined how factors such as mussel population density, biomass and location in the river substrate impacted our ability to detect certain species; and investigated unexpected eDNA detections through phylogenetic analysis. Our eDNA results for fish and mussel species were broadly consistent with the data from traditional electrofishing and quadrat-based field surveys, although both community eDNA and conventional sampling detected species unique to that method. Our phylogenetic analysis agreed with other studies that treat Pleurobema decisum and P. chattanoogaense as synonymous species; however, they are still listed as unique species in molecular databases which complicates their identity in a metabarcoding assay. We also found that Fusconaia flava and F. cerina are indistinguishable from one another using a portion of the NADH dehydrogenase Subunit 1 (ND1) marker, which may warrant further investigation into whether or not they are synonymous. Our results show that many factors impacted our ability to detect and correctly identify Unionidae mussel species. Here we describe the obstacles we faced, including the murky phylogeny of Unionidae mussels and turbid river conditions, and our development of a potentially impactful freshwater mussel monitoring eDNA assay. 
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