Unionid Mussels Research Articles

Native and non-native unionids respond differently to the presence of fouling dreissenid mussels

Unionid mussels are globally threatened by several human disturbances, including the introduction of non-native species. Among these, biofouling zebra and quagga mussels of Ponto-Caspian origin are considered to be especially detrimental to unionid locomotion, filtration and physical condition. The aim of our study was to determine and compare the impact of dreissenid fouling and/or presence on locomotion and burrowing of the native Unio tumidus and invasive Sinanodonta woodiana, a novel invader expanding its range in Europe in recent decades. We tested unionids collected from Lake Balaton (central Europe) that were fouled by dreissenids (zebra and quagga mussels mixed), cleaned of fouling or non-fouled (collected without any signs of dreissenid fouling). Moreover, unionids were tested in the presence or absence of other fouled individuals and dreissenids isolated in mesh bags to determine the influence of direct fouling and presence of dreissenids in the environment on unionid behaviour. Movement initiation time, locomotion distance and burrowing level were retrieved from videos recorded for 24 hours. Direct fouling affected only the behaviour of U. tumidus, limiting their burrowing and delaying movements. After removal of fouling, movement timing returned back to normal, but mussels still burrowed less than the control non-fouled individuals, indicating persisting effects of fouling on physical condition. Moreover, U. tumidus reduced their locomotion in the presence of fouled unionids. Sinanodonta woodiana responded to the presence of dreissenids (especially quagga mussels) with increased burrowing. These different responses of the two unionid species to Dreissena spp. indicate that biofoulers may influence biotic interactions between the unionids by promoting the invasive species (less susceptible to negative effects of fouling). Moreover, S. woodiana may indirectly affect U. tumidus through apparent competition, constituting an environmental reservoir of biofoulers exerting a stronger impact on the native species.

Bacteriological analysis of unionid hemolymph collected from freshwater mussel populations in the Pacific northwestern United States

AbstractNative freshwater mussel (Unionidae) mortality events have been occurring with increased frequency in recent decades, with few investigations into potential etiological agents. In the western United States, no surveys have been published regarding the bacteria associated with unionid mussels. Herein, we examine locations of known mussel mortality events in the Chehalis River (Washington), in the Crooked River (Oregon), and Owyhee River (Oregon). Mussel populations considered healthy were sampled in the Skookumchuck River (Washington) for comparison. A variety of bacteria were isolated from these populations, and most notably, Acinetobacter spp. were identified from 82% of moribund individuals of Gonidea angulata in the Owyhee River. Future work evaluating whether Acinetobacter spp. are pathogenic to freshwater mussels could be valuable in unraveling the factors associated with these enigmatic mortality events.

Quantifying Effects and Ingestion of Several Pristine Microplastics in Two Early Life Stages of Freshwater Mussels.

Microplastics have been found in freshwater systems, and in turn have been detected in freshwater bivalves. However, there is limited research that defines the toxicity of bicroplastics to native freshwater bivalves that have long been imperiled in North America. Our objective was to determine whether a suite of pristine microplastics has an adverse effect on two early life stages of unionid freshwater mussels. Glochidia of Lampsilis fasciola (a Canadian species at risk) and Lampsilis siliquoidea (widespread across Canada) were individually exposed to spheres of polystyrene (6 and 90 μm), polyethylene (28, 90, and 1000 μm), and cellulose acetate (1000 μm), as well as fibers of polyethylene terephthalate (60 μm). After 24 h, there was no significant decrease in glochidia viability in either species. Juvenile L. siliquoidea mussels were also exposed to spheres of polystyrene (6 and 90 μm) and polyethylene (28 μm), and fibers of polyethylene terephthalate (60 μm) in individual 28-day subchronic tests followed by a 7-day depuration period. Burial was assessed weekly, and ingestion of each microplastic was compared in nondepurated and depurated mussels. There was no sustained effect on juvenile burial with any microplastic tested. Ingestion of microplastics was concentration dependent, and depuration occurred for all particles and size ranges tested. The results suggest that pristine microplastics were not acutely toxic to the early life stages of these freshwater mussels, but that the energetic costs associated with particle uptake and depuration, which were not measured in our study, may have an impact on fitness that warrants further investigation. In addition, testing with other shapes and polymers of microplastics typically detected in the environment is recommended. Environ Toxicol Chem 2024;00:1-12. © 2024 The Author(s). Environmental Toxicology and Chemistry published by Wiley Periodicals LLC on behalf of SETAC.

Evaluation of survivorship and annulus validation in calcein-stained freshwater unionid mussels

Unionid mussels deposit growth rings (annuli) within the shell, which can be used to estimate age and growth. Thin-sectioning is a common technique for counting annuli, wherein a cross-section of a shell valve is taken and evaluated by multiple readers. Correctly identifying annuli can be challenging because ambiguous annuli can bias growth estimates. Staining with calcein, a fluorescent chemical, is a technique that has been used with marine and freshwater species to improve accuracy of growth estimates. This method chelates calcium, causing a permanent mark that fluoresces under ultraviolet light. Calcein has seen limited testing on unionid mussels so it remains unclear if this method has adverse effects on survival and growth. We evaluated calcein against 2 concentrations (125 mg L−1 and 250 mg L−1) at 2 exposure times (12 and 24 h) on Cyclonaias pustulosa, a common North American unionid. Survivorship remained above 80% 6 months post-immersion. Mark quality and retention for 250 mg L−1 were high for both 12- and 24-h immersions, although historical annuli were not highlighted. These findings corroborate studies indicating calcein immersion is generally safe and effective in juveniles and adults and suggest it may be useful in validating new growth.

Assessment of haemolymph parameters of some freshwater snails and mussels collected from a lentic habitat of Bangladesh

ABSTRACT The present study was conducted to determine certain haemolymph parameters of natural populations of two freshwater snails Pila globosa and Filopaludina bengalensis, and four unionid mussels Lamellidens jenkinsianus, L. phenchooganjensis, L. marginalis, and L. corrianus collected from Darikanthal Beel, Trishal, Mymensingh. Twenty apparently healthy live snails and mussels from each population collected at the same date were selected for haemolymph analysis. A non-lethal sampling technique was adopted for collecting haemolymph from the snails and mussels. The haemolymph parameters Na+, K+, Cl−, glucose concentrations and pH levels were determined for each specimen. Significant differences (P < 0.05) were found in almost all the haemolymph parameters among the sampled snail and mussel populations. This study provided reference ranges for some vital haemolymph parameters of the two freshwater snail species and four unionid mussel species. These ranges are measurable non-lethally and could be applied to biological monitoring of environmental stressors using the molluscs as indicator species.

The reproductive costs of bitterling fish and zebra mussel parasitism to a unionid mussel

Unionid mussels are one of the most vulnerable groups of animals, with multitude of factors responsible for the decline of their populations in the freshwater ecosystems. Many of those causes stem from interspecific relationships. Direct data on the reproductive costs incurred to unionids through parasitism by fish and other mussel species are incomplete. We used field experiments to test whether reproduction of the swollen river mussel (Unio tumidus) is affected by parasitism by the European bitterling fish (Rhodeus amarus) and zebra mussel (Dreissena polymorpha). We documented that bitterling brood can develop in the gills of female, male and hermaphrodite mussels. Our research showed that male mussels carried more fish offspring than female U. tumidus and bitterling embryo survival appeared higher in the outer gill demibranchs. Parasitised female U. tumidus suffered reduced fecundity in terms of a reduced number of mature ovulated oocytes and increased oocyte degeneration. Our data lend clear support to the hypothesis that bitterling fish embryos parasitizing mussel gills and epibiont zebra mussel fouling unionid shells represent a major cost to the reproductive success of their host mussels. Extended gonadal activity (multiple spawning) of U. tumidus spreads their spawning time over a longer period, which may mitigate the costs of parasitism.

Impact of habitat engineering by invasive Corbicula clams on native European unionid mussels

Biological invasions cause biodiversity erosion on a global scale. Invasive species spreading beyond their natural range compete with native fauna for food and space, push native species to suboptimal habitats, impairing their behaviour and thus limiting their occurrence. Freshwater ecosystems are especially vulnerable to biological invasions and their ecological and economic impacts. The invasive Asian clams (Corbicula spp.), due to their opportunistic life style, can occur at densities of thousands ind. m−2. They act as ecosystem engineers transforming bottom substrata through accumulation of shells. Our goal was to determine the effect of substratum modification by living Corbicula and their shells on substratum choice and behaviour of Unio tumidus and Anodonta anatina, two European freshwater mussel species of the highly imperilled Unionidae family. We assessed their substratum selection in pairwise choice tests (pure sand vs. sand modified by living Corbicula or their shells, sand modified by shells vs. living Corbicula). Next, we tested locomotion and burrowing of unionids on pure substratum and substrata modified by Corbicula. Unionids avoided sand modified by living Corbicula and their empty shells, not distinguishing between these two types of substratum modification. In the presence of Corbicula, their burrowing was shallower or it took them longer to obtain the same depth as in the pure sand. Additionally, on sand modified by Corbicula shells, we observed a locomotion increase (U. tumidus) or slowing down (A. anatina). Our research showed a novel mechanism of negative impact of Corbicula on unionids, consisting in pushing them away from their optimal habitats. This may contribute to their habitat loss and future declines in invaded ecosystems.

Behavioral and Biochemical Effects of Glyphosate-Based Herbicide Roundup on Unionid Mussels: Are Mussels Good Indicators of Water Pollution with Glyphosate-Based Pesticides?

The behavioral (filtration activity) and biochemical (oxidative stress) effects of Roundup 360 Plus (active substance glyphosate) herbicide on two species of unionid mussels, Unio tumidus (Philipsson, 1788) and Anodonta anatina (L.), were evaluated at concentrations ranging from 15 to 1500 μg L−1 of glyphosate for five days. During all experiments, we did not record the mortality of the studied mussel species. Exposure to Roundup herbicide induced dose-dependent filtration disruptions in both U. tumidus and A. anatina. Exposure of the mussels to a low and environmentally relevant concentration 15 µg glyphosate L−1 resulted in a slight (&lt;20%) and temporary decrease in mean valve dilation. Exposure of the mussels to Roundup at relatively high concentrations caused drastic and prolonged shell closure and a reduction in the mussel shell opening rate. Exposure of both mussel species to herbicide resulted in oxidative stress; an increase in superoxide dismutase enzymatic activity was detected. The most significant increase in SOD activity was observed after the exposure to the highest Roundup concentration. However, no correlation between the Roundup concentration and enzymatic activity was found. The use of unionid mussels to detect environmentally relevant concentrations of Roundup, as a part of biological early warning system for pollution, is limited, but they can serve to detect the incidental pollution of aquatic ecosystems with high concentrations of this herbicide.

First observation of a spawning mantle display in a European unionid mussel.

Freshwater bivalve mussels in the order Unionida are highly endangered ecosystem engineers with a parasitic lifecycle necessitating a fish host to metamorphose from larval glochidia to juvenile mussel. While many species are broadcast spawners and release a large number of glochidia into the water column, many other species have a variety of highly evolved lure mechanisms and mantle displays to attract hosts to ensure a more targeted infestation. Almost all lure mussels are found exclusively in North America, with only one European species (Unio crassus) occasionally displaying a host attraction behaviour referred to as larval spurting. Here, I present evidence that the depressed river mussel (Pseudanodonta complanata) exhibits mantle displays to attract fish to gravid mussels for a targeted infestation, the first description of mantle displays in Europe.

Biofiltering capacity of Chambardia rubens (Bivalvia: Unionidae) may modulate expression of stress and growth genes inhibited by the neonicotinoid insecticide acetamiprid in zebrafish

Neonicotinoid insecticides specifically target insect subtypes of nicotinic acetylcholine receptors. Acetamiprid (ACE: C10H11ClN4), the neonicotinoid insecticide, is used to control crop insect pests worldwide. It is a nitrile, monochloropyridine, and carboxamidine that is highly soluble and accessible to waterways. There, it causes neurotoxic and oxidative perturbance to non-target organisms. The unionid mussel Chamabradia rubens is a common Northern River Nile suspension feeder. The current study aimed to assess ACE filtration from waters by C. rubens, and whether this biological power can reduce ACE effects on fish. Removal of ACE by C. rubens was assessed using LC-MS/MS. Zebrafish Danio rerio adults were exposed to different sublethal doses of ACE in the presence or absence of C. rubens in their aquaria. The results showed that mussels could remove significant ACE amounts from water, where it accumulated mostly in the digestive gland. The presence of C.rubens in zebrafish aquaria having ACE was accompanied by significant upregulation of antioxidant enzyme gene transcripts and total H2O2 scavenging, in contrast to mussel-free ACE-exposed groups. Meanwhile, liver triglycerides rose 5-6-fold in response to ACE in the “Fish-Only” groups, indicating an ACE-induced hepatotoxicity. Also, Insulin-like growth factor 1 (igf1) and fish body mass increased more in “Fish + Mussel” groups than in the “Fish-Only” ones. In aggregate, these findings suggest that the Nile mussel could reduce the oxidative stress and metabolic changes induced in fish by ACE. This can contribute valuable environmental and economic benefits upon the use of this mussel as a biofilter.

Freshwater mussels prefer a diet of stramenopiles and fungi over bacteria

Freshwater mussels (Mollusca: Unionidae) play a crucial role in freshwater river environments where they live in multi-species aggregations and often serve as long-lived benthic ecosystem engineers. Many of these species are imperiled and it is imperative that we understand their basic needs to aid in the reestablishment and maintenance of mussel beds in rivers. In an effort to expand our knowledge of the diet of these organisms, five species of mussel were introduced into enclosed systems in two experiments. In the first, mussels were incubated in water from the Clinch River (Virginia, USA) and in the second, water from a manmade pond at the Commonwealth of Virginia’s Aquatic Wildlife Conservation Center in Marion, VA. Quantitative PCR and eDNA metabarcoding were used to determine which planktonic microbes were present before and after the introduction of mussels into each experimental system. It was found that all five species preferentially consumed microeukaryotes over bacteria. Most microeukaryotic taxa, including Stramenopiles and Chlorophytes were quickly consumed by all five mussel species. We also found that they consumed fungi but not as quickly as the microalgae, and that one species of mussel, Ortmanniana pectorosa, consumed bacteria but only after preferred food sources were depleted. Our results provide evidence that siphon feeding Unionid mussels can select preferred microbes from mixed plankton, and mussel species exhibit dietary niche differentiation.

Comparison of three unionid mussel species in removing green microalgae grown in recirculating aquaculture system effluent

Global increase in aquaculture production has created a need to reduce its environmental impacts. Nutrients could be recycled especially at land-based recirculating aquaculture systems (RAS) by cultivating green microalgae in aquaculture effluent. However, microalgae are difficult to harvest. As a multi-trophic solution, mussels could be used in harvesting microalgae. We tested three European freshwater mussels (duck mussel Anodonta anatina, swan mussel A. cygnea, and swollen river mussel Unio tumidus) for filtering two common green microalgae (Monoraphidium griffithii and Selenastrum sp.) grown in RAS effluent. Mussels decreased microalgal concentrations in the tanks 42–83% over three consecutive trials. Algal concentrations at the end of each trial were lowest for both microalgae in tanks containing Anodonta mussels. Clearance rates were higher for Anodonta mussels than for U. tumidus. Mussels biodeposited more microalgae to tank bottoms when M. griffithii was filtered. Ammonium concentration decreased or did not change in tanks with M. griffithii, but increased in tanks containing Selenastrum sp. These results suggest that of the tested species Anodonta mussels and M. griffithii show best potential for RAS effluent bioremediation application. We conclude that a co-culture of microalgae and unionid mussels could be used for recycling nutrients in aquaculture.

An Initial Survey of Unionid Mussels in Lakes East of the Missouri River in South Dakota, USA

This study surveyed freshwater mussels (family Unionidae) in 116 lakes and reservoirs east of the Missouri River in South Dakota, USA, during 2017. Using two-person–hour/site timed searches, evidence of a total of 1789 mussels, including 1053 live mussels, was obtained from 50 waters. Nine species, from two different orders, were found in lakes and reservoirs throughout five of the six major river drainages east of the Missouri River. The native species observed included Giant Floater Pyganodon grandis, Fatmucket Lampsilis siliquoidea, Threeridge Amblema plicata, White Heelsplitter Lasmigona complanata, Wabash Pigtoe Fusconaia flava, Deertoe Truncilla truncata, and Pink Heelsplitter Potamilus alatus. Giant Floater was the most widespread and abundant species observed, representing 63.3% of the live mussels sampled. Two non-native species, Zebra Mussel Dreissena polymorpha and Chinese Basket Clam Corbicula fluminea, were also documented from three water bodies in the lower Missouri River drainage. Overall, mussel abundance was negatively correlated with lake water conductivity and positively correlated with turbidity. No significant correlations were observed between species abundance and water temperature, pH, dissolved oxygen, or substrate particle size.

Correction to “Short‐term effects on Unionid mussel density and distribution before and after low‐head dam removal in northern New York”

Correction to “Short‐term effects on Unionid mussel density and distribution before and after low‐head dam removal in northern New York”

Environmental DNA dynamics of three species of unionid freshwater mussels

AbstractNorth American freshwater mussels are of special conservation concern due to their high endemism and the multiple anthropogenic stressors affecting them. Of the over 300 species in North America, nearly one third of these species are federally listed as threatened or endangered. Environmental DNA (eDNA) analysis has been successful in detecting freshwater mussels and could aid in monitoring their populations. Production and degradation rates of eDNA for the species of interest are needed to inform interpretation of eDNA detections, allow possible modeling of relative abundance and population location, and aid in mussel conservation through population identification. Here, we designed and tested qPCR assays for three freshwater mussel species, mucket (Ortmanniana ligamentina), fatmucket (Lampsilis siliquoidea), and the federally endangered spectaclecase (Cumberlandia monodonta). We performed laboratory experiments under controlled conditions to measure eDNA shedding and degradation rates for each species. Different biomasses, temperatures, and food regimens were tested independently to determine if these factors influence the amount of DNA produced by the mussels. Degradation rates of eDNA were measured from experimental tank water after mussels were removed. Overall, we observed low eDNA shedding rates for freshwater mussels compared to previous studies of fish eDNA shedding rates. Furthermore, temperature and feeding showed limited or no significant effects in the species studied. Environmental DNA degradation rates were consistent with those reported in the literature for other taxa. Collectively, our results will be useful for designing eDNA monitoring studies, modeling eDNA dispersal, and interpreting eDNA results to help inform freshwater mussel conservation efforts.

A test of the loose-equilibrium concept with long-lived organisms: Evaluating temporal change in freshwater mussel assemblages.

The loose-equilibrium concept (LEC) predicts that ecological assemblages change transiently but return towards an earlier or average structure. The LEC framework can help determine whether assemblages vary within expected ranges or are permanently altered following environmental change. Long-lived, slow-growing animals typically respond slowly to environmental change, and their assemblage dynamics may respond over decades, which transcends most ecological studies. Unionid mussels are valuable for studying dynamics of long-lived animals because they can live >50 years and occur in dense, species-rich assemblages (mussel beds). Mussel beds can persist for decades, but disturbance can affect species differently, resulting in variable trajectories according to differences in species composition within and among rivers. We used long-term data sets (10-40 years) from seven rivers in the eastern United States to evaluate the magnitude, pace and directionality of mussel assemblage change within the context of the LEC. Site trajectories varied within and among streams and showed patterns consistent with either the LEC or directional change. In streams that conformed to the LEC, rank abundance of dominant species remained stable over time, but directional change in other streams was driven by changes in the rank abundance and composition of dominant species. Characteristics of mussel assemblage change varied widely, ranging from those conforming to the LEC to those showing strong directional change. Conservation approaches that attempt to maintain or create a desired assemblage condition should acknowledge this wide range of possible assemblage trajectories and that the environmental factors that influence those changes remain poorly understood.

Thermal tolerance exceedances of an endangered unionid mussel in the Rio Grande Basin, with implications for river management

Abstract Freshwater mussels are globally imperilled, which is attributed to their sensitivity to changes in streamflow and temperature. The Black River in south‐eastern New Mexico, USA, harbours a stronghold population of the federally endangered unionid Popenaias popeii (Texas hornshell). Decreasing discharge and elevated water temperatures are considered the primary factors responsible for the species’ decline. However, the impact of these factors has not been quantified directly, which may hinder conservation efforts. The upper thermal tolerances (LT05 and LT50) of Black River P. popeii larvae (glochidia) and newly transformed juveniles were evaluated. Individuals were acclimated to 27°C and then immersed at five experimental temperatures (28, 30, 32, 34 and 36°C) for 24 h (glochidia) or 96 h (juveniles). The thermal tolerances of P. popeii and its presumed host fishes were then overlain onto in situ water temperature and discharge data to determine thermal exceedances in the past 15 years. Temperature was hindcast back to 2007 using machine learning (random forest model) and coupled with discharge. For glochidia, LT05 was exceeded frequently (41%) and LT50 was exceeded occasionally (13%) during spring and summer periods, whereas juvenile thresholds were never exceeded. Upper continuous duration above threshold (UCAT) analysis revealed periods of catastrophic high temperature, which were used to determine discharge bottlenecks. This study demonstrates how laboratory‐derived physiological thresholds can be used in conjunction with environmental data to evaluate the hydrological needs of aquatic organisms, which is useful in efforts to maintain flow regimes that protect native ecosystems.

Investigating biodiversity patterns across scales in freshwater mussels.

Hypotheses relating genomic diversity to community attributes such as abundance and species diversity attract attention from a wide and varied audience because their applications are twofold. First, testing such hypotheses can further a theoretical-and hopefully generalizable-understanding of the forces that assemble communities and create observed patterns of biodiversity. Second, relationships that hold true could ease the burden of data collection for conservation or other urgent applications; for example, a strong correlation between species diversity and genetic diversity could make it possible to use one as a proxy for the other, and focus limited resources on measuring the easier of the two without sacrificing information gained. In a From the Cover article in this issue of Molecular Ecology, Bucholz etal.(2023) explore the relationships between within-species genomic diversity, community relative abundance and community species richness, testing three types of ecological hypotheses in the freshwater mussel communities of the southeastern United States. They find positive relationships between mussel density and species richness, and between genomic diversity within a species and density of that species, but no robust support for the expectation of correlated genomic and species diversity. Their analyses highlight the among-species variability in relationships among these different levels of organization and also the complex ways in which interactions with the broader ecosystem (i.e. unionid mussels require fish hosts for maturation) affect these quantitative relationships, nonetheless pushing forward into the important frontier of community-wide genomic assessment for theoretical and conservation applications.

'Phototaxis' in the absence of light? Locomotory patterns in unionid mussels.

Locomotion in benthic invertebrates can strongly affect habitat selection and ecosystem nutrient cycling. In the case of freshwater mussels, the drivers of locomotion are largely unresolved. Our aim was to assess the influence of light presence and intensity on the locomotory behaviour of freshwater mussels in controlled laboratory experiments. The species investigated in our study were Anodonta anatina and Unio pictorum, two widely distributed mussels in European lentic and lotic inland waters. At low algal concentrations, known to be associated with more frequent locomotory activities, we found that both species moved primarily in the absence of light (72.7% of all movements across experiments). However, the movements of both species were directed towards the light source, resembling a net-positive 'phototactic' response but in the absence of light. The distance to the light source, which was negatively correlated to light intensity, had a positive effect on the distance covered in locomotory activities by A. anatina but not by U. pictorum. Intraspecific variation in shell size had no impact on movement distance, indicating that the energetic costs of movement were not a limiting factor. We suggest that the observed movement towards brighter locations helps to enhance food quantity and quality, whilst movement in darkness mitigates predation risks.

Molecular phylogenetic position and the life cycle of Phyllodistomum cyprini Feng et Wang, 1995 in Japan, with a note of a larval Phyllodistomum sp. from unionid mussels in North America

A gorgoderid species, Phyllodistomum cyprini Feng et Wang, 1995 obtained from ureters of common carp, Cyprinus carpio in Japan is described both morphologically and molecularly. Its larval stage is a macrocercous cercaria found in a unionid mussel, Nodularia nipponensis first described by Urabe et al. (2015). A molecular phylogenetic study revealed that P. cyprini is not closely related to rhopalocercous cercariae from unionid mussels both in Europe and North America. This result indicates that there are several distinct clades in Phyllodistomum species that use unionid mussels as a first intermediate host, and suggests that the cercarial morphology may be a more accurate indicator of the phylogeny of Phyllodistomum than molluscan host identity.