Endangered Freshwater Pearl Mussel Margaritifera Research Articles

Effects of multiple stressors on recruitment of long‐lived endangered freshwater mussels

Abstract Multiple stressors can affect populations interactively. However, the process by which they affect recruitment remains unclear, especially in long‐lived organisms with complex life cycles. This study explored the bottleneck stages of juvenile recruitment in the endangered freshwater pearl mussel Margaritifera togakushiensis and the interactive effects of nutrients and fine sediments on these stages. The proportion of M. togakushiensis juveniles aged ≤10 years was investigated in 24 rivers from north‐eastern Japan. Margaritifera togakushiensis has a complex life cycle with an obligate parasitic larval stage. Gravid female density, glochidia density (the number of glochidial infections per stream area), and juvenile survival rate, used as indices for adult, parasitic, and post‐parasitic juvenile stages, respectively, were obtained from 11 of these rivers. Twenty‐four population status assessments showed that the proportion of juveniles aged ≤10 years ranged from 0.00 to 0.23, and that they were absent in 12 rivers. Parasitic and post‐parasitic juvenile stages were bottlenecks for recruitment; juvenile survival rates had a stronger positive effect on recruitment in rivers with high glochidia density. Juvenile survival rate was negatively associated with the synergistic effects of nutrients and fine sediments, although factors limiting glochidia density were not identified. These findings suggest that the interaction between nutrients and fine sediments can synergistically reduce the recruitment of M. togakushiensis, indicating an underestimated impact of stressors on mussel recruitment if treated individually. Future mitigation measures should consider both nutrient levels and fine sediments to restore mussel recruitment. These results also emphasize the importance of considering both parasitic and post‐parasitic juvenile stages of mussels to maximize the success of future restoration actions.

Substratum Raking Can Restore Interstitial Habitat Quality in Swedish Freshwater Pearl Mussel Streams

Functional and oxygenated stream beds provide crucial habitat for multiple endangered stream taxa, including endangered freshwater mussels, fishes, and insect larvae. Stream bed restoration measures such as substrate raking are often applied to mitigate excess fine sediment introductions and stream bed colmation, yet such measures are controversial. In this study, we conducted a systematic experiment in which sites with stream bed raking and removal of macrophytes were monitored over two years and compared with before-treatment conditions and untreated reference sites in the Swedish Brånsån stream, which still contains a population of the endangered freshwater pearl mussel Margaritifera margaritifera. The stream bed restoration resulted in improved habitat quality, as evident from decreased substrate compaction, increased redox potential, and oxygen supply into the stream bed. In contrast to previous studies in Central European catchments with more intensive agricultural catchment uses, the effects of the restoration measure were much longer, extending over two years. Consequently, stream bed raking and macrophyte removal can be considered a useful and more long-lasting restoration measure than currently assumed, especially in streams where excess input of fine sediment has already been mitigated, where catchment land use is rather extensive, and where near-natural flow regimes still prevail.

Spatiotemporal variation of streambed quality and fine sediment deposition in five freshwater pearl mussel streams, in relation to extreme drought, strong rain and snow melt

Oxygenated streambeds are considered a key requirement for the successful recruitment of stream fauna, including highly endangered freshwater pearl mussel Margaritifera margaritifera. Excessive amounts of fines impede exchange between open water and interstitial, leading to colmation and low oxygen levels in the juvenile habitat. Understanding the dynamic relationship between sediment delivery, transport, deposition and remobilization in relation to anthropogenic drivers is still poorly understood, yet is essential for conservation and restoration.This study analysed spatiotemporal sediment dynamics and interstitial habitat quality in five pearl mussel streams at the border region between Bavaria, Saxony and the Czech Republic during 2018 and 2019, comparing extremely dry periods with higher discharge events caused by snow melt and rainfall. Physicochemical habitat conditions within the streambed and sediment deposition were recorded in high spatial resolution along the stream courses, with a particular focus on the effects of tributaries and outflows of man-made fishponds.Habitat conditions were unsuitable for juvenile pearl mussels at the majority of sites, indicated by pronounced differences in physicochemical parameters between open water and the substrate, independent of discharge conditions. Sediment deposition varied markedly between discharge events, in terms of both the quality and quantity of deposits. Snow melt resulted in the highest sedimentation rates, but the smallest proportion of fine particles. During low flow conditions, fine sediment deposition was highly variable, ranging from 0.048 to 4.170 kg/week/m², mostly independent of flow velocity. High spatiotemporal variation was observed within and amongst stream systems, revealing different longitudinal patterns of fine sediment deposition, with catchment land use as the main driver. Temporal variability in sediment deposition was mainly associated with the discharge condition while abiotic parameters varied mainly with season.The high site-specificity of sedimentation rates and substrate conditions in response to different discharge events highlights the importance of an adapted conservation management which considers anthropogenic effects at the local scale.

A multi-scale, integrative modeling framework for setting conservation priorities at the catchment scale for the Freshwater Pearl Mussel Margaritifera margaritifera

The identification and prioritization of sites for conservation actions to protect biodiversity in lotic systems is crucial when economic resources or available areas are limited. Challenges include the incorporation of multi-scale interactions, and the application of species distribution models (SDMs) to rare organism with multiple life stages. To support the planning of conservation actions for the highly endangered Freshwater Pearl Mussel Margaritifera margaritifera (FPM), this paper aims at developing an ecohydrological modeling cascade including a hydrological model (SWAT) and a hydraulic model (HEC-RAS). Building on hydrology and hydraulics, Random Forest models for potential risk to juveniles due to sand accumulation, SDMs for adults habitat niche, and a landscape connectivity assessment of dispersal potential were developed. The feasibility of such models integration was tested in the Aist catchment (630 km2) in Austria. The potential FPM habitat and the sand accumulation risk for the whole catchment were predicted with good accuracy. Results show that while the potentially suitable habitats for adults FPM cover 34% of the river network, only few habitat patches can maximize the dispersal potential (4% of the river network) and even less are showing limited impact of accumulations (3.5% of river network). No habitat patch that meets all the three criteria is available, suggesting approaches that target the patch-specific critical life stage-factors are promising for conservation.

Sensitivity to cadmium of the endangered freshwater pearl mussel Margaritifera margaritifera from the Dronne River (France): experimental exposure.

Margaritifera margaritifera is a critically endangered species in Europe. Among the causes explaining its decline, metal pollution had never been deeply studied. Thus, an ecotoxicological investigation was developed on this species which comes from the Dronne River (South-West of France). Cadmium (Cd) exposure of mussels at 2 and 5μg/L for 7days was conducted to test their vulnerability to this metal, and also the potential endocrine disruption power of Cd. Morphometric analyses, gonad histological observations, metal bioaccumulation, metallothionein (MTs) production, measures of malondialdehyde (MDA), and finally quantitative relative expression analysis of genes involved in various metabolic functions were performed.The main results showed Cd accumulation increasing in a dose-dependent manner, especially in the gills. The same trend was observed for gene expression relative to oxidative stress. Histological analysis of the gonads highlighted a predominance of hermaphrodite individuals, but after 7days of exposure to Cd, the percentage of female was largely increased compared with controls, from 17 to 33%. These results demonstrate the endocrine disruption effect of Cd on freshwater pearl mussels.The pearl mussel Margaritifera margaritifera is sensitive to cadmium since the metallothioneins are poorly induced, gene expression reveals oxidative stress, and gonads tend to be feminized.

A qPCR MGB probe based eDNA assay for European freshwater pearl mussel (Margaritifera margaritifera L.)

Abstract1. Environmental (e)DNA assays are becoming increasingly used to detect rare or invasive aquatic species.2. The Critically Endangered freshwater pearl mussel Margaritifera margaritifera is undergoing range‐wide reduction in population numbers and distribution.3. An eDNA assay to detect the presence of M. margaritifera was developed, based on the mitochondrial cytochrome oxidase I gene, utilizing species‐specific primers, a minor groove binding (MGB) probe and quantitative (q)PCR approaches.4. The results from this pilot study demonstrated high sensitivity both in laboratory and field trials, and provide a valuable non‐invasive tool for detecting M. margaritifera.

Interaction between the endangered freshwater pearl mussel Margaritifera margaritifera, the duck mussel Anodonta anatina and the fish host (Salmo): acquired and cross-immunity

The common duck mussel Anodonta anatina can live in sympatry with—and use the same host, brown trout (Salmo trutta)—as the endangered freshwater pearl mussel Margaritifera margaritifera. Since the glochidia release of A. anatina takes place seasonally earlier than that of M. margaritifera, brown trout can be sequentially exposed first to A. anatina and then to M. margaritifera. Cross-immunity, an immune reaction induced in fish host against glochidia after the infection with glochidia of another mussel species, is possible. Thus, it was studied experimentally if brown trout can be cross immunized against M. margaritifera by earlier infection with A. anatina. In addition, the hypothesis that consecutive exposures of same glochidial species in different years in the same host may create acquired immunity was tested in brown trout against M. margaritifera. Furthermore, the dose dependence of acquired immunity against M. margaritifera glochidia in the Atlantic salmon (S. salar) was also studied. Cross-immunity was not found; suggesting that occurrence of A. anatina does not pose a threat to M. margaritifera. Instead, acquired immunity and its dose dependence were evident, emphasizing the significance of availability of 0+ age group immunologically naive Atlantic salmon/brown trout for efficient conservation of M. margaritifera.

The relationship between the freshwater pearl mussel (Margaritifera margaritifera) and its hosts

Endangered freshwater pearl mussels Margaritifera margaritifera reveal a complex life cycle with an obligate host-dependent phase. Only two species, Atlantic salmon Salmo salar and brown trout S. trutta, are important hosts in Europe, indicating a high degree of specialization. Whilst freshwater pearl mussels with their filtering activity can provide important ecosystem services and indirectly improve the habitat quality for their salmonid hosts, their direct effects on physiological stress, reduced swimming performance, and increased mortality at high rates of infestation all support a parasitic character of the mussel during its hostdependent phase. From an evolutionary perspective, both the much greater generation time of the parasite compared to the host, as well as the great distribution ranges of M. margaritifera and its hosts should favour local adaptation patterns. The variable suitability of different salmonid strains and species as hosts for M. margaritifera and the resulting differences in the performance of larvae during the host-dependent phase indicate that host-management strategies should focus on maintaining high quality hosts at a regional scale to avoid selection or genetic drift effects which could erode the genetic and evolutionary potential for adaptation to changing environmental conditions.

Impacts of small scale flow regulation on sediment dynamics in an ecologically important upland river.

Flow regulation is widely recognized as affecting fluvial processes and river ecosystems. Most impact assessments have focused on large dams and major water transfer schemes, so relatively little is known about the impacts of smaller dams, weirs and water diversions. This paper assesses sediment dynamics in an upland river (the Ehen, NW England) whose flows are regulated by a small weir and tributary diversion. The river is important ecologically due to the presence of the endangered freshwater pearl mussel Margaritifera margaritifera, a species known to be sensitive to sedimentary conditions. Fine sediment yield for the 300-m long study reach was estimated to be 0.057tkm(-2)year(-1), a very low value relative to other upland UK rivers. Mean in-channel storage of fine sediment was also low, estimated at an average of around 40gm(-2). Although the study period was characterized by frequent high flow events, little movement of coarser bed material was observed. Data therefore indicate an extremely stable fluvial system within the study reach. The implication of this stability for pearl mussels is discussed.

Effect of pH, iron and aluminum on survival of early life history stages of the endangered freshwater pearl mussel, Margaritifera margaritifera

Glochidium larvae and juveniles of the endangered freshwater pearl mussel Margaritifera margaritifera may be sensitive to low pH and metal exposure, but to our knowledge, no tolerance tests have been performed. Therefore, we exposed glochidia, fish-attached glochidia, and juveniles of the pearl mussel to low pH and increased iron (Fe) and aluminum (Al) by using realistic pH (6.0–4.5), Fe (0.5–2.0 mg L−1), and Al (0.25–1.0 mg L−1) levels periodically observed in this study site. Survival of glochidia decreased with decreasing pH, increasing Fe, and increasing Al, as well as with increasing Fe + Al concentration in a 72 h exposure. All glochidia died within 24 h in pH 4.5 and Fe 2.0 mg L−1. When infected trout, Salmo trutta, were exposed to increased Fe and Al from 4 days before to 76 days after infection, the numbers of encysted glochidia did not differ from unexposed control fish. In juvenile mussels, a slight decrease in survival was observed in lowered pH and increased Al and a combination of Al + Fe in a 168 h experiment. Results indicate that episodes of low pH and high metal concentrations may harm glochidia and potentially contribute to local decline of M. margaritifera.

Threats to the freshwater pearl mussel Margaritifera margaritifera L. in Central Europe

Data on threats affecting the life cycle of the endangered freshwater pearl mussel Margaritifera margaritifera L. are presented. There was no evidence to suggest that a change in density or age structure of host fish (brown trout) populations has contributed to the decline of mussels. The factor of greatest impact was pollution. Mortality of the adult stage exhibited a positive correlation with the concentration of nitrate in the water and, in particular, phosphate, calcium and BOD 5 were correlated with decreasing survival and establishment of juvenile mussels. As fertility (i.e. production of glochidia) is maintained even in sparse populations, and in polluted rivers, the populations should recover if the causes of decline are removed. Eutrophication should therefore be prevented. It might accelerate recovery of sparse populations if the numbers of young mussels released by the hosts were increased by introducing artificially infected fish.