Endangered Freshwater Pearl Mussel Research Articles

A review of the physical habitat requirements and research priorities needed to underpin conservation of the endangered freshwater pearl mussel Margaritifera margaritifera

Abstract The freshwater pearl mussel Margaritifera margaritifera has declined across its range but current knowledge of its physical habitat requirements falls short of that needed to confidently guide habitat management and conservation programmes. This paper critically reviews knowledge of the physical habitat requirements of M. margaritifera and sets out a research agenda to address existing knowledge gaps. Present information on the hydraulic, sedimentary and oxygen requirements of M. margaritifera is based largely on descriptive or correlative field studies. Consequently, little is known of the processes that control the correlations observed between habitat conditions and pearl mussel abundance. Furthermore, a pressing concern is the need for standardization of field and laboratory techniques, notably in the context of sediment and hyporheic dissolved oxygen, where the variety of field and analytical techniques applied to date limits transferability. The review identifies nine important research questions and outlines approaches from environmental hydraulics, fluvial geomorphology and fisheries ecology that can be used to address them. Research specifically focused on the role of high and low discharges may help elucidate the hydrological, fluvial and bio‐energetic processes that influence M. margaritifera distribution and recruitment. Research is also needed to assess the role of mussels as engineers. The review outlines opportunities to apply new approaches to improve characterization of physical habitat conditions and assess how these conditions influence mussels. Improved characterization will provide a firm evidence base for habitat management and mussel conservation. Copyright © 2014 John Wiley & Sons, Ltd.

Host-dependent genetic variation in freshwater pearl mussel (Margaritifera margaritifera L.)

The endangered freshwater pearl mussel (Margaritifera margaritifera) requires brown trout or Atlantic salmon as a host to complete its life cycle. In Norway, populations have been identified using almost exclusively either salmon or trout as hosts, even when both hosts are present. In this study we tested the hypothesis that the genetic variation in freshwater pearl mussel is host-dependent. A total of 587 specimens from 25 different localities were assayed for genetic variation at eight microsatellite loci. Within populations, the trout-mussel populations had significantly lower allelic richness and expected heterozygosity than the salmon-mussel populations. The genetic differentiation among trout-mussel populations was very large (FST = 0.332), and significantly larger than among salmon-mussel populations (FST = 0.023). Host affiliation explained more of the genetic differentiation among freshwater pearl mussel populations (FCT = 0.150) than geographical location (FCT = 0.013). Collectively these results suggest that there is strong reproductive isolation between freshwater pearl mussel populations. More importantly, our results indicate that trout- and salmon-mussel populations are differently genetically structured. Because of the mandatory parasitic larval stage on trout and salmon, the host-dependent genetic variation has implications for restoration and management plans for this species.

Practical experience in the rearing of freshwater pearl mussels (Margaritifera margaritifera): advantages of a work-saving infection approach, survival, and growth of early life stages

The critically endangered freshwater pearl mussel (Margaritifera margaritifera Linnaeus 1758) is the target species of an Austrian conservation project that involves captive breeding. In order to optimize the operational procedure, controls were conducted at several decisive stages, including infec- tion of host fish (for which a time- and work-saving enclosure approach was tested), larval growth during the parasitic stage, growth of juvenile mussels in climate chambers at different temperatures, and growth and survival of re-introduced juveniles in field cages. High infection rates could be attained under near natural conditions. Distinctive patterns in the way the gill arches of the host fish were infected could be detected. Encysted glochidia showed significantly different successive growth stages, related to water temperature. In all, five distinctive growth stages could be detected in the course of the first 562 days of observation. The stages are described and the respec- tive daily increments given. Very high survival rates were achieved during hibernation in the field as well as at the laboratory. The study suggests a way for saving time in the infection procedure that can more effec- tively be invested in an intensive maintenance of juveniles at the laboratory and during hibernation in the field.

Variable development and excystment of freshwater pearl mussel (Margaritifera margaritifera L.) at constant temperature

The highly endangered freshwater pearl mussel ( Margaritifera margaritifera L.) has strongly declined throughout Europe and is a priority species in aquatic conservation. The complex life cycle of M. margaritifera includes an obligate development phase of glochidia larvae on a suitable host fish. Knowledge on the progression of the parasitic phase and on the factors governing excystment of juvenile mussels are particularly crucial for artificial breeding and conservation measures. The core objective of this study was to study excystment of M. margaritifera after maintaining the infested hosts under constant water temperatures between 11 and 12 °C and to determine the sum of daily water temperatures (day degrees) required by M. margaritifera for completion of metamorphosis. In a standardized laboratory experiment, excystment of juvenile mussels from brown trout ( Salmo trutta ) was found between 1700 and 3400 day degrees post infestation, indicating highly variable development times of individual glochidia and the absence of a previously postulated threshold temperature of ≥15 °C for successful excystment of living juveniles. Consequently, the parasitic phase does not seem to limit the current distribution range and reintroduction of the species into cool headwater areas, as well as the culturing under constant water temperature conditions in typical salmonid fish hatchery setups. The concept of day degrees of development may also be useful to test the ecological implications of observed genetic differences among different populations.

Conservation status and reproduction of the critically endangered freshwater pearl mussel (Margaritifera margaritifera) in Northern Ireland

ABSTRACTFreshwater unionoids are one of the most threatened animal groups worldwide and the freshwater pearl mussel Margaritifera margaritifera is currently listed as critically endangered in Europe. The EC Habitats Directive requires that EU Member States monitor the distribution and abundance of this species and report regularly on its conservation status.The pearl mussel meta‐population in Northern Ireland was surveyed to assess temporal population trends in Special Areas of Conservation (SACs) and mussel reproduction throughout its range.Mussels occurred in six rivers and numbers within three SAC designated sites remained stable between 2004–2007 and 2011. The discovery of more than 8000 previously unknown individuals in the Owenreagh River contributed to an overall increase (+56.8%) in the total known population. All populations actively reproduced during 2010 with approximately half of all individuals gravid. Moreover, suitable salmonid hosts occurred at all sites with 10.7% of salmon and 22.8% of trout carrying encysted glochidia. Populations were composed entirely of aged individuals with little evidence of recent recruitment.It is inferred that the break in the life cycle must occur during the juvenile stage when glochidia metamorphose and settle into the interstitial spaces within the substrate. Water quality parameters, most notably levels of suspended solids, exceeded the recommended maximum thresholds in all rivers.It is posited that the deposition of silt may be the main cause of juvenile mortality contributing to a lack of recruitment. Consequently, all populations were judged to be in ‘unfavourable’ conservation status. Catchment‐level management plans are urgently needed to reduce siltation with the aim of improving recruitment. These results have implications for the success of ex situ conservation programmes; specifically, the size at which captive‐bred juveniles are released into the wild. Further research is required to assess the vulnerabilities of early life‐stages of M. margaritifera to siltation. Copyright © 2012 John Wiley & Sons, Ltd.

Impacts of flow regulation on freshwater pearl mussel (Margaritifera margaritifera) habitat in a Scottish montane river

The River Moriston in NW Scotland is a cobble–gravel bedded river that has been dammed and regulated for hydroelectric power (HEP) since 1956. The river supports a functional population of the critically endangered freshwater pearl mussel (Margaritifera margaritifera) in the lower part. In contrast the population in the upper reach is sparse and shows no signs of juvenile recruitment, leading to speculation that hydrological and geomorphic changes associated with HEP have degraded the habitat they depend on. A combination of historical analysis, field mapping and geomorphic survey of channel and active bar sites was used to assess habitat changes and current quality. During the post-dam period, the naturally stability of much of the channel has increased, active bars have been stabilised through vegetation colonisation, riparian tree cover has increased and the active channel width has significantly reduced locally (>50%); adjustments that are indicative of a reduction in the incidence of competent flows caused by flow regulation. However area and stability of habitat for freshwater pearl mussels have not been reduced greatly. The channel sites examined are characterised by mixed cobble–gravel substrates (D50 range=46–188mm), predicted to be highly stable, that provide suitable habitat for adult freshwater pearl mussels. However a degree of bed compaction at one site was observed that could be limiting the recruitment of juvenile mussels. It is hypothesised that the sparse, non-functional status of the freshwater pearl mussel population reflects significant historical pearl fishing and the limitation of recovery due to HEP related pressures of fish migration obstruction and bed compaction. The implications of these factors for conservation of the species are 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.

A critical reflection on the success of rearing and culturing juvenile freshwater mussels with a focus on the endangered freshwater pearl mussel (Margaritifera margaritifera L.)

ABSTRACT Freshwater mussels are in decline throughout their range. The lack of natural recruitment in freshwater pearl mussel populations and other freshwater molluscs has led to controversies about the usefulness and applicability of captive breeding techniques for their conservation. The current state of rearing and culturing programmes for freshwater mussels in Europe and North America is reviewed here with a focus on the endangered freshwater pearl mussel (Margaritifera margaritifera). Different strategies of propagation and the key factors of success are addressed and conservation management decisions are discussed with respect to risk reduction and the intensity of the culturing system. Based on the rearing techniques applied for multiple species in North America, and for the genus Margaritifera in European countries, sufficient numbers of juveniles can be produced to sustain selected populations. However, captive breeding and stocking should be carefully documented and must not replace the restoration of functional stream habitats. From a conservation point of view, captive breeding of endangered mussel species can be a last‐minute rescue tool in order to retain the evolutionary potential of priority populations which would not persist long enough to benefit from habitat restoration practices. Copyright © 2011 John Wiley & Sons, Ltd.

Suitability of different salmonid strains as hosts for the endangered freshwater pearl mussel (Margaritifera margaritifera L.)

Abstract The complex life cycle of endangered European freshwater pearl mussel Margaritifera margaritifera L. involves an obligatory parasitic phase on a host fish. Knowledge on the host–parasite interaction and on the suitability of different host fish species and strains is required both for the management of wild fish and mussel populations as well as for improving the efficiency of captive breeding methods. In this study, the suitability of different salmonid strains for hosting glochidia was tested, including Danube salmon (Hucho hucho L.) and three brown trout (Salmo trutta L.) strains from inside and outside the freshwater pearl mussel distribution range. All brown trout strains as well as Danube salmon were successfully infected with freshwater pearl mussel glochidia and encystment of mussel larvae was detected. One brown trout strain originating from the natural pearl mussel distribution range was identified as the most suitable host, revealing the highest fish‐weight‐normalized infection rates and highest glochidial growth rates, whereas endemic Danube salmon was least suitable. Under natural conditions, the role of Danube salmon may be attributed to the long‐distance dispersal of glochidia in the Danube system, whereas sedentary brown trout appear to be the most important hosts at a local scale. Successful infection of suitable hosts and the maintenance of these host–parasite systems in calcareous water were demonstrated in this study. These results indicate that neither the infection process nor the encystment phase of freshwater pearl mussels is dependent on low lime concentrations. The results of this study suggest that careful selection and management of appropriate host fish strains is mandatory for sustainable conservation management of freshwater pearl mussel populations. Copyright © 2010 John Wiley & Sons, Ltd.

Strategies for the conservation of endangered freshwater pearl mussels (Margaritifera margaritifera L.): a synthesis of Conservation Genetics and Ecology

Freshwater pearl mussels (Margartifera margaritifera L.) are among the most critically threatened freshwater bivalves worldwide. The pearl mussel simultaneously fulfils criteria of indicator, flagship, keystone and umbrella species and can thus be considered an ideal target species for the process conservation of aquatic ecosystem functioning. The development of conservation strategies for freshwater pearl mussels and for other bivalve species faces many challenges, including the selection of priority populations for conservation and strategic decisions on habitat restoration and/or captive breeding. This article summarises the current information about the species’ systematics and phylogeny, its distribution and status as well as about its life history strategy and genetic population structure. Based on this information, integrative conservation strategies for freshwater mollusc species which combine genetic and ecological information are discussed. Holistic conservation strategies for pearl mussels require the integration of Conservation Genetics and Conservation Ecology actions at various spatial scales, from the individual and population level to global biodiversity conservation strategies. The availability of high resolution genetic markers for the species and the knowledge of the critical stages in the life cycle, particularly of the most sensitive post-parasitic phase, are important prerequisites for conservation. Effective adaptive conservation management also requires an evaluation of previous actions and management decisions. As with other freshwater bivalves, an integrative conservation approach that identifies and sustains ecological processes and evolutionary lineages is urgently needed to protect and manage freshwater pearl mussel diversity. Such research is important for the conservation of free-living populations, as well as for artificial culturing and breeding techniques, which have recently been or which are currently being established for freshwater pearl mussels in several countries.

Molecular Markers Reveal Genetic Contamination of Endangered Freshwater Pearl Mussels in Pearl Culture Farms in Japan

Molecular Markers Reveal Genetic Contamination of Endangered Freshwater Pearl Mussels in Pearl Culture Farms in Japan

Drainage-independent genetic structure and high genetic diversity of endangered freshwater pearl mussels (Margaritifera margaritifera) in northern Europe

Freshwater pearl mussels (Margaritifera margaritifera) are among the most critically threatened bivalve molluscs worldwide. An understanding of spatial patterns of genetic diversity is crucial for the development of integrative conservation strategies. We used microsatellites to study the genetic diversity and differentiation of 14 populations of M. margaritifera in central Sweden, an area which was described as a major secondary contact zone in postglacial colonisation for other species. Genetic diversity of Swedish pearl mussel populations was much greater than in central and southern Europe but similar to the genetic diversity observed in the northeastern portion of their European range. Genetic differentiation among populations was pronounced but to a large extent independent from present-day drainage systems. The complex patterns of genetic diversity and differentiation in pearl mussel seem to be strongly influenced by the species’ high degree of specialisation and extraordinary life history strategy which involves facultative hermaphrodism and an obligatory encystment stage on a host fish. Genetic drift effects and anthropogenic disturbances resulting in reduction of population size and loss of connectivity are less pronounced in northern pearl mussel populations compared to those in central and southern Europe.

Use of mollusc shells for DNA-based molecular analyses

Genetic approaches are increasingly being considered for investigations into the systematics and the conservation biology of molluscs. Here, we investigate the potential of using shell material for DNAbased analyses, using the example of endangered freshwater pearl mussels (Margaritifera margaritifera). Tissue and shells from 15 dead specimens were sampled. Their shells were split into four-quarters and re-exposed to original stream water for zero (unexposed), 1, 3 and 6 months. The influences of exposure time and resulting shell degradation, different grinding procedures and different DNA extraction methods on the quantity and quality of extractable DNA were assessed, using tissue samples as a reference. A combination of short shell-exposure time, medium grinding size and phenol–chloroform extraction procedures resulted in the most robust PCR and in lowest microsatellite genotyping errors. Amplification of nine microsatellite loci was successful in 89% of samples derived from fresh shell DNA. Genotyping errors were mostly the result of false alleles (7.8%), whereas allelic dropout only occurred at a rate of 5.7%. Shell material re-exposed to stream water for 1 month did not produce reliable genotyping results but amplification of mitochondrial COI was still successful. Real-time quantitative PCR of microsatellite-flanking DNA regions was shown to be an effective tool for pre-assessing DNA-quantity in shell material. These results suggest that fresh shell material may be a useful source of DNA for genetic analyses in mollusc species if the increased risk of errors compared to the use of soft tissues is adequately addressed.

Relationship of biotic and abiotic factors to recruitment patterns in Margaritifera margaritifera

We investigated relationships of biotic and abiotic factors to recruitment patterns of the endangered freshwater pearl mussel (Margaritifera margaritifera) in 10 Swedish streams. We found that the maximum proportion of gravid mussels did not differ between streams with and without recent recruitment. Moreover, the mean glochidial load on trout (Salmo trutta), which was positively related to adult mussel density, did not differ significantly between these stream types. Thus, the larval stages of the freshwater pearl mussel were not related to recruitment failure. Instead, recruitment is probably hindered at the next stage in the life history of the mussels, the benthic stage, and may be related to sedimentation as turbidity was four times greater in streams lacking recent recruitment than in streams with recent recruitment. Furthermore, we found that juvenile mussel density was positively related to the number of glochidial infections per stream area in streams with ongoing recruitment, indicating that successful recruitment in these streams may depend on both mussel and trout density. Future research should thus examine biotic interactions between mussels and trout as well as the effects of sedimentation on benthic-living mussels.

Stable carbon isotopes in freshwater mussel shells: Environmental record or marker for metabolic activity?

Mussel shells have been used in a number of paleoecological and environmental studies. The interpretation of stable carbon isotopic composition of shell material is still controversial. The carbon for shell carbonate precipitation can either be derived from ambient dissolved inorganic carbon (DIC), with shells recording environmental signals, or from metabolic CO 2, with the potential to disguise environmental signals. To gain insight into this question, we investigated four nearly 100-yr long-term records of aragonite shells from an extant freshwater bivalve species, the endangered freshwater pearl mussel ( Margaritifera margaritifera L.). Single growth increments of the outer prismatic and the inner nacreous zones were successfully and easily separated with a simple heat treatment for chronological analyses of δ 13C in single layers of each zone. Autocorrelation and semivariance statistical methods reveal that mussels show distinct individual signal patterns, which extend up to 25 yr. Signal patterns are reliably reproduced with replicate samples from defined layers within one shell and show similar patterns with a slight offset for inner nacreous and outer prismatic layers for individual animals. Mussels exposed to the same environmental conditions exhibit distinct and contradictory signature patterns, which do not match between individuals. This observation can only be explained by strong metabolic influences on shell precipitation. Environmental changes in pH, temperature, electric conductivity and atmospheric carbon signature had no or little (<5%) influence, whereas body tissue protein and body tissue δ 13C signatures negatively correlated with the youngest produced shell δ 13C signatures, indicating that respiration causes a preferential loss of light isotopes from body mass and an inverse enrichment in shell aragonite. Hence, the shells of the freshwater pearl mussel yield a long-term record of metabolic activity, whereas the use of δ 13C in these shells as recorder for environmental signals is questionable. This may also be true for shells from other species, for which metabolic carbon incorporation has been acknowledged.

Applications of extensive survey techniques to describe freshwater pearl mussel distribution and macrohabitat in the River Spey, Scotland

AbstractThe spatial distribution and associated physical habitat of endangered freshwater pearl mussels (Margaritifera margaritifera) in a 145 km stretch of the River Spey, northeast Scotland, were investigated. The overall size of the Spey M. margaritifera population was estimated to be in the order of 10 million. Mussel distributions were compared with River Corridor Survey (RCS) macrohabitat data and found to be positively associated with coarse riverbed substrata, ‘fast‐flowing’ waters, riparian woodland, and river bends; and negatively associated with shingle bars, flood barriers, ‘slow‐flowing’ waters, eroding cliffs and aquatic macrophytes. Significant positive relationships between mussel density and channel slope, width and bank height, were also observed. Binary logistic regression models (based on four to six features) were used to predict the presence/absence of mussels or the occurrence of ‘optimal’ mussel habitat (i.e. mussel density &gt;1 m−2) at any given site. Overall predictive success rates of 79% and 78% were achieved, respectively. Discriminant function models (based on five variables) were also used, with predictive success rates of 78% and 88%, respectively. Copyright © 2004 John Wiley &amp; Sons, Ltd.

The threat of climate change to freshwater pearl mussel populations.

Changes in climate are occurring around the world and the effects on ecosystems will vary, depending on the extent and nature of these changes. In northern Europe, experts predict that annual rainfall will increase significantly, along with dramatic storm events and flooding in the next 50-100 years. Scotland is a stronghold of the endangered freshwater pearl mussel, Margaritifera margaritifera (L.), and a number of populations may be threatened. For example, large floods have been shown to adversely affect mussels, and although these stochastic events were historically rare, they may now be occurring more often as a result of climate change. Populations may also be affected by a number of other factors, including predicted changes in temperature, sea level, habitat availability, host fish stocks and human activity. In this paper, we explain how climate change may impact M. margaritifera and discuss the general implications for the conservation management of this species.

Conservation of threatened freshwater pearl mussel populations: river management, mussel translocation and conflict resolution

River engineering work has historically been responsible for the decline and extinction of a number of endangered freshwater pearl mussel [ Margaritifera margaritifera (L.)] populations and potentially remains a significant threat. The impact of different types of river engineering work on a number of Scottish M. margaritifera populations is examined and discussed. M. margaritifera is now fully protected under law in most countries and guidance is urgently needed so that river managers can integrate ecological and socio-economic factors when considering the impact of proposed activities on M. margaritifera populations. To safeguard the remaining important populations, a simple conflict resolution framework is suggested for the appraisal of proposed developments in rivers with pearl mussel populations. Operations likely to harm mussels and permanently damage their river bed habitat should not proceed. In exceptional circumstances (outlined), the translocation of small numbers of adult mussels may possibly be considered as a potential management tool, but mussel translocation has been little used and should be considered experimental and last resort.

Does electrofishing harm freshwater pearl mussels?

Abstract1. Two experiments were carried out in a Scottish river to test the effects of electrofishing on endangered freshwater pearl mussels (Margaritifera margaritifera).2. In the first experiment, two areas of mussel bed were marked out as treatment and control sites and the former was electrofished using standard equipment. The mussels were examined 10 min, 24 h and 35 days after treatment and their shell valve closure responses, burrowing capabilities and gravidities were recorded as signs of normal ‘functioning’.3. In the second experiment, individual mussels were marked as treatments and controls and the former were electrofished. These mussels were examined as before.4. No mortalities occurred and no significant differences in ‘functioning’ between treatments and controls were observed in either experiment.5. Since no measurable treatment effect could be demonstrated, it appears that electrofishing did not adversely affect the short‐term survival of M. margaritifera. Copyright © 2001 John Wiley &amp; Sons, Ltd.

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.