Freshwater Pearl Mussel Populations Research Articles

Discovery of a freshwater pearl mussel population from the Kushereka River, White Sea drainage, Northern European Russia

In this paper we present the results of our field survey in the Kushereka River and preliminary data concerning the size structure, age composition, and population density of the freshwater pearl mussel M. margaritifera in the studied sites.

The Wullowitz-Lakes theory: Periglacial impacts on river morphology and habitat suitability for the endangered freshwater pearl mussel

The Malše River, on the border between Austria and the Czech Republic, contains one of the last remaining freshwater pearl mussel (Margaritifera margaritifera) populations on the Bohemian Massif. Evidence from field studies indicated that landscape evolutionary processes changed the boundary conditions for river channel formations, especially in those parts where the remaining mussels, probably also self-reproducing to a limited extent, were documented. The aim of the present work was to study these possible palaeo-impacts through (i) the analysis of the terrain data and accompanying hydrodynamic-numerical modelling and (ii) sediment sampling of the main channel and the surrounding floodplains at the reach and catchment scales. The results indicated that solifluction caused a historic blockage in the drainage area with consequent formation of lakes in the upstream part of these obstructions. At least two sites where this “Wullowitz-Lakes Theory” can be applied were identified. The occurrence of these lakes was validated by sediment analysis. The findings further indicated that the later fluvial processes in these deposits of a former stagnant water body forced the formation of an anabranching channel in the system, which would not have occurred in a solely freely developed fluvial system. In conclusion, it could be determined that the consideration of palaeo-processes might be important even for present onsite assessments of aquatic habitats and species such as the endangered freshwater pearl mussel.

Assessment of endangered freshwater pearl mussel populations in the Northern Iberian Plateau in relation to non–native species: xenodiversity as a threat

In the last two decades, small populations of freshwater pearl mussels, Margaritifera margaritifera, have been recorded in Mediterranean rivers of the Iberian Northern Plateau. A survey was carried out in Castilla and León in 2018 to assess the development of populations of this species in all the rivers of known distribution and to update the threat classification. Thirty sections in the rivers Negro, Tera, Alberche and Águeda were positive for its presence, and another 50 stretches of seven rivers were negative. The species is currently distributed over about 22.5 km. Águeda and Tera populations have decreased dramatically in the last 14 years and are on the threshold of extinction. The Negro river supports the largest population, although the species has now disappeared in at least 61 % of the stretches that were inhabited in 2004. All populations showed very low densities and an ageing population structure, with no recruitment for decades. The presence of non-native invasive alien species (NIS) was higher than in a previous regional survey, with the signal crayfish representing the greatest threat. We observed changes in benthic microhabitats and direct predation of adults and glochidia conglutinates. In the Alberche River, in strict syntopy with M. margaritifera and two other mussel species, 10 NIS were detected. The current hydrological and ecological conditions in the Duero watershed support the settlement of exotic species to the disadvantage of native mollusks, which are more demanding in terms of microhabitats.

Assessing remote sensing as a tool to monitor hydrological stress in Irish catchments with Freshwater Pearl Mussel populations

The West Coast of Ireland hosts many of the few populations of Freshwater Peal Mussels (FPM) left in Europe. The decline of this keystone species is strongly related to deteriorating hydrological conditions, specifically to the threat of low flows during dry summers. Populations still capable of reproducing require a minimum discharge and flow velocity to support juvenile mussels, or else stress builds up and an entire generation may be lost. Monitoring environmental and hydrological conditions in small and remote FPM catchments is difficult due to the lack of infrastructure. Indices derived from remote sensing imagery can be used to assess hydrological variables at the catchment scale. Here, five indices are tested as possible surrogates for soil moisture and evapotranspiration, based on two relevant land-cover types: open peat habitats (OPH) and forestry. Selected indices are then assessed in their ability to reproduce seasonal patterns and in their response to a severe drought event. The moisture stress index (MSI) and normalized difference vegetation index (NDVI) were found to be the best surrogates for soil moisture and evapotranspiration respectively. Both indices showed seasonality patterns in the two land-cover types, although the variability of MSI was significantly higher. During the 2018 drought, MSI visibly increased only in OPH, while NDVI rose only for forestry. The results suggest that OPH enhances the long-term hydrological resilience of a catchment by conserving water in the peat substrate, while industrial forestry plantations exacerbate the pressure on water during drier periods. This has consequences for river discharge, freshwater biodiversity and specifically for FPM. Implementing these surrogates have the potential to identify land-use management strategies that reduce and even avert the effects of drought on FPM. Such strategies are increasingly necessary in a climate change context, as recurring summer droughts are expected in most of Europe.

Stable isotopes reveal the importance of terrestrially derived resources for the diet of the freshwater pearl mussel (Margaritifera margaritifera)

Abstract The freshwater pearl mussel (FPM) is among the most endangered freshwater species worldwide. The few remaining populations suffer from low recruitment rates and are subject to habitat fragmentation, pollution, siltation, decline or loss of host fish populations, and climate change. Successful conservation strategies for FPM require a holistic understanding of its ecological requirements, life history, population dynamics, and habitat prerequisites. Although habitat requirements are well described, food requirements at different life stages have received less attention. Stable isotope analyses of FPM and potential food resources in three German streams were combined with mixing model analysis to quantify organic matter resources assimilated by juvenile (first year after encystment from host fish) and semi‐adult (10 years old, immature) individuals. There were only slight differences in dietary contributions between the two life stages, and terrestrial particulate organic matter and benthic organic matter contributed substantially to the diet. Tissue type was more important in explaining variation in dietary contributions than individual variation for semi‐adult FPM. The strong reliance on terrestrial resources sheds new light on the functional role of unionid mussels and the connection of streams to their riparian area. The dependence of FPM on terrestrial resources also emphasizes the need for a stronger focus on the restoration and protection of intact riparian areas, including wetlands with their specific vegetation, when planning conservation and management strategies for threatened FPM populations.

Time travelling through local ecological knowledge regarding an endangered species

European freshwater pearl mussel (Margaritifera margaritifera) populations are declining despite a growing effort to conserve them. Here we used a combination of local ecological knowledge (LEK) and field sampling to assess past and current distribution and conservation status of this endangered species in Cávado and Neiva Rivers (Portugal). We performed face-to-face interviews in both rivers and sampled the entire area where the respondents confirmed the historical presence of this species. Abiotic characterization, water quality and fish diversity were also assessed in both rivers. We found that freshwater pearl mussels are now possibly extinct in Cávado River but almost 50% of the respondents confirm its presence in the past, especially elders that lived in villages near its historical distribution. To the contrary, and although the species is still present in Neiva River, only 3.8% of the respondents remembered its presence in the past. In both rivers, respondents suggested pollution as the most important explanation for the freshwater pearl mussels decline. However, nowadays both rivers present excellent water quality and trout Salmo trutta (the freshwater pearl mussel fish host) is still abundant. Since we identified the areas where the species was present in a recent past, this information is vital for possible management actions with the aim of re-introduce or increase the abundance of M. margaritifera populations and/or for the rehabilitation of habitats in both rivers. We also highlight the vital importance of getting LEK, mainly from elders, in order to avoid shifting baseline syndromes and to get qualitative accurate information of past references and/or experience with historical conditions. Results reported here reinforce concern about the conservation status of freshwater pearl mussel populations in Portugal and can be used to guide future research and management initiatives to better conserve this species.

Mass Mortality Events in Freshwater Pearl Mussel (Margaritifera margaritifera) Populations in Sweden: An Overview and Indication of Possible Causes

The freshwater pearl mussel Margaritifera margaritifera is an endangered species in Sweden with more than 600 known populations distributed in 16 out of 21 counties. Only approximately one-third of these populations are considered viable and healthy with signs of recent juvenile recruitment. From 2011 to 2017, research documented an increased mortality in this species, of up to 100% in some populations, but no etiological cause of these mortalities has been identified. With this paper, we provide current knowledge of locations where mass mortality of freshwater pearl mussel has been found in Sweden and discuss possible causes. Postmortem sampling and histopathological findings from two counties in 2016–17 detected lesions in digestive glands indicating a reduced capacity for nutrient uptake. Results from these macroscopic and microscopic investigations also indicate a reduction in, or a lack of, reproductive output compared with reference populations.

Host specificity drives genetic structure in a freshwater mussel

Parasites often depend on their hosts for long distance transport, and genetic population structure can be strongly affected by host specificity and dispersal. Freshwater pearl mussel (Margaritifera margaritifera) populations have previously been found to naturally infest either primarily Atlantic salmon (‘salmon-mussel’) or exclusively brown trout (‘trout-mussel’) across a wide geographic range. Here, we experimentally test whether this intraspecific variation in natural infestation can be explained by host specificity in freshwater pearl mussel. Our experiments show that when both host species were exposed to larvae from salmon- and trout-mussel respectively, salmon-mussel larvae almost never infested brown trout and vice versa. This suggests that host specificity can explain variation in natural infestation among the studied freshwater pearl mussel populations. Host specificity provides a link to the species’ variable population genetic structure, as mussel populations limited to Atlantic salmon, the host with stronger dispersal, show higher genetic diversity and weaker differentiation than populations limited to brown trout as host.

Short-term breeding: releasing post-parasitic juvenile Margaritifera into ideal small-scale receptor sites: a new technique for the augmentation of declining populations

The aim of this research was to assess the potential for augmentation of freshwater pearl mussel populations Margaritifera margaritifera through short-term captive breeding to early juvenile stage and thus avoiding the growing-on stage of juveniles in captivity, which can have a high mortality rate. Fish encysted with Margaritifera glochidia were transferred to a tank lined with a thin layer of river gravels. Juvenile mussels were left to drop-down into these gravels and were then transferred, with the gravels, into suitable habitat in their native river. Redox potential measurements and near bed flow velocities were measured in the tops and tails of riffles to determine the best potential areas to transfer the juveniles. Following a year in the wild, juvenile mussels were found to be living in the areas in which they had been placed. This technique is recommended for rivers with populations of Margaritifera that have lost habitat quality, but where preferential flows maintain some areas that are still capable of juvenile survival.

Regional monitoring of freshwater pearl mussel Margaritifera margaritifera in the County of Norrbotten, Sweden

A total of 16 freshwater pearl mussel Margaritifera margaritifera rivers out of 64 known freshwater pearl mussel rivers are included in the Administrative County of Norrbotten regional monitoring program. First surveys were done in 1994 and the results show that only three rivers have viable populations according to national criteria despite little visible human impact and that juvenile mussels (<50 mm in length) have been found in all rivers at every occasion. The results also indicate that there might be “missing years” for juvenile recruitment suggesting that freshwater pearl mussel populations at the extreme end of the species range might be dependent on “golden moments” in order to keep up viable populations. Deeper knowledge and better tools for determining viable populations might be necessary in order to make the right decisions on how to manage the rivers and the freshwater pearl mussel populations.

Variation in the COI gene of the freshwater pearl mussel Margaritifera margaritifera from River Vuokkijoki

The freshwater pearl mussel Margaritifera margaritifera L. is one of the most endangered freshwater mussels in the world. Effective conservation of threatened species requires not only ecological, but also genetic information from the target species and populations. Since low genetic diversity can reduce the ability of a species to adapt to environmental changes, maintaining genetic diversity has been identified as one of the key elements in successful conservation programs. We examined genetic variation of the freshwater pearl mussel from the River Vuokkijoki, Karelia, Russia. We sequenced a fragment of the cytochrome c oxidase subunit I gene (COI) from 22 individuals and compared the data to 32 previously published COI sequences available in GenBank. We identified 10 different COI haplotypes in the sequenced samples, three of which had not been previously reported. Our results show that the River Vuokkijoki has high genetic diversity and suggest that the colonization of this northern freshwater pearl mussel population might have occurred from multiple and even distant refugia. Therefore, the freshwater pearl mussel population of the River Vuokkijoki is valuable for the conservation of the whole species.

The ecology of the freshwater form of the Atlantic salmon Salmo salar L., the brown trout Salmo trutta L., and the freshwater pearl mussel Margaritifera margaritifera L. in Syuskyuyanyoki River (Basin of Lake Ladoga)

The locations and the area of the spawning–growing grounds have been assessed in the Syuskyuyanyoki River (the basin of Lake Ladoga), as has the population density of the juveniles of the freshwater form of the Atlantic salmon and the brown trout. The Atlantic salmon spawns at present on the rapids downstream of the hydroelectric power plant because of the insurmountable dam; the population density of this species has decreased dramatically. Only the landlocked form of the brown trout was found; the anadromous form was not. The brown trout has resettled along the major part of the river. We suggest that there are two subpopulations of the freshwater pearl mussel that differ with regard to the host for their larvae. The intensity of invasion of the juveniles of salmonids by the larvae of the freshwater pearl mussel and the survivability of glochidia did not depend on the host species. The growth rate of the mollusks and the age–size structure of the freshwater pearl mussel population have been assessed.

The status of the freshwater pearl mussel Margaritifera margaritifera in Scotland: extent of change since 1990s, threats and management implications

All known rivers in Scotland with recent records of freshwater pearl mussels Margaritifera margaritifera were surveyed in 2013–2015 using a standard methodology. Freshwater pearl mussel populations were classed as: (i) apparently extinct in 11 rivers, (ii) not successfully recruiting in 44 rivers, and (iii) evidence of recent successful recruitment in 71 rivers. On a regional basis, a high proportion of extant populations were located in North and West Scotland. In all regions extant populations were characterised by low pearl mussel densities, with 97 of 115 extant Scottish populations defined as ‘rare’ (0.1–0.9 mussels per 1 m 2) or ‘scarce’ (1.0–9.9 mussels per 1 m 2). Only 18 Scottish rivers now hold pearl mussel populations in densities that are considered to be ‘common’ (10–19.9 mussels per 1 m 2) or ‘abundant’ (>20 mussels per 1 m 2). Based on survey evidence, the number of apparently extinct pearl mussel populations in Scottish rivers is now 73. The decline is particularly pronounced in the West Highlands and Western Isles strongholds. The key threats are: (i) pearl fishing, (ii) low host fish densities, (iii) pollution/water quality, (iv) climate change and habitat loss, (v) hydrological management/river engineering and (vi) ‘other factors’, such as non-native invasive species. Over the last 100 years this endangered species has been lost from much of its former Holarctic range. Scotland’s extant M. margaritifera populations continue to be of international importance, but their continued decline since the first national survey in 1998 is of great concern.

Using genetic monitoring to inform best practice in a captive breeding programme: inbreeding and potential genetic rescue in the freshwater pearl mussel Margaritifera margaritifera

Freshwater pearl mussel (Margaritifera margaritifera) populations are declining in Northern Ireland to the extent that a captive breeding programme was established on the Upper Ballinderry river in 1998. Previous genetic analysis of the hatchery broodstock and their first cohort of offspring showed significant levels of inbreeding (F IS = 0.166). The broodstock, which currently numbers ca. 90 individuals, was supplemented with new individual mussels, whilst in 2013, a previously unknown population was discovered on the Lower Ballinderry river. The aim of the present study was to determine whether the rotation of the broodstock has led to a decrease in the levels of inbreeding in the second cohort of juveniles, and to determine whether the new population found in the Lower Ballinderry was genetically distinct from the captive bred population and populations from the Upper Ballinderry, which represent the source of the hatchery broodstock. Genotyping using eight microsatellite markers indicated that levels of inbreeding in the second cohort of captive-bred mussels were high, (F IS = 0.629), and were comparable to those sampled from the original cohort and the hatchery broodstock (F IS = 0.527 and 0.636 respectively). Bayesian analysis of population structure indicated that the newly discovered Lower Ballinderry population was genetically distinct from the broodstock and its source populations on the Upper Ballinderry. The observed differentiation was primarily due to differences in allele frequencies, and was most likely a result of genetic drift. The occurrence of ten alleles, albeit at low frequency, in the Lower Ballinderry population, including four private alleles, suggests that this new population could be incorporated into the broodstock with the aim of decreasing levels of inbreeding in the future.

Influence of flow diversions on giant freshwater pearl mussel populations in the Ebro River, Spain

Abstract Freshwater mussels, historically a component of freshwater benthic invertebrate biomass, are one of the most imperilled animal groups on the planet. Margaritifera auricularia was once a common freshwater mussel inhabiting large rivers throughout Western Europe. It was believed to be extinct until 1996 when a few small populations were found in Spain and France. Currently M. auricularia is one of the most endangered species in the world. The current status of this mollusc in the Ebro River was surveyed, finding a few adult specimens at only two localities, and many old, empty shells throughout the river. Using a simple analysis of historical hydrological data, dramatic changes in water flow might have led to localized extirpation of this freshwater mussel. Other factors contributing to the slow extirpation of this long‐lived invertebrate from other areas of the Ebro Basin include the continuous reduction of water levels during the reproductive season, overharvesting for nacre, construction of impoundments, extinction of fish hosts, and impaired water quality. Copyright © 2016 John Wiley &amp; Sons, Ltd.

The characteristics of the infection of juvenile Atlantic salmon with glochidia of the freshwater pearl mussel in rivers of Northwest Russia

The decline of freshwater pearl mussel (Margaritifera margaritifera L.) populations is globally well documented, but there is a lack of knowledge concerning the status of the species and its interaction with host fishes in the rivers of the White and Baltic Seas. This study aimed to identify the host fish of pearl mussel in four rivers of Karelia (Northwest Russia), to analyse the duration of the parasitic phase, and the susceptibility of fish hosts to the infestation. Juvenile sea-migrating and land-locked Atlantic salmon (Salmo salar L.) were identified as the most important hosts. In the Keret’ River, reduced numbers of juvenile Atlantic salmon are likely to result in a decline of pearl mussel. This problem does not appear to be present for the other three studied rivers. Pearl mussel glochidia were mostly found in yearlings (0+), whereas older fish were infected less, suggesting a more complex pattern of host use than commonly expected. The remote location of Karelian pearl mussel rivers, the high number of pearl mussels in them, and their rather pristine state all suggest that these rivers have a high conservation priority. The importance of Atlantic salmon as a host fish and the emerging declines of Atlantic salmon populations, e.g. , in the Keret’ River, suggest that the sustaining of this host species should have a high conservation priority.

Quantification of Freshwater Pearl Mussel Entrainment Velocities and Controlling Factors; a Flume Study

Increased flood frequency and magnitude are predicted for Scotland, and the country contains several of the world's largest recruiting populations of freshwater pearl mussel (Margaritifera margaritifera). This study provides a unique flume experiment to measure the near-bed velocities required for freshwater pearl mussel entrainment and factors affecting their movement. It represents the first quantitative attempt at examining the precise water velocities at which freshwater pearl mussel become vulnerable to displacement during high flow events. Measurement of the near-bed velocities at which the mussels moved was undertaken using an indoor recirculating flume. The effect of the different parameters (bed substrate, mussel burial depth, mussel curvature, mussel alignment, shell curvature and the presence of a simulated foot) on entrainment velocity was tested in the flume and their significance was verified using Kruskal–Wallis and Mann Whitney tests. Bed substrate was found to have the biggest influence on mussel entrainment velocities with averages of 0.86 ms−1, 0.95 ms−1, 1.01 ms−1 and 1.42 ms−1 for sand, gravel, mixed bed and boulder beds respectively. Stepwise logistic regression showed that bed substrate, foot presence, mussel length, mussel burial depth and shell curvature were sufficient to explain mussel entrainment velocity. These findings provide valuable information for the modelling of freshwater pearl mussel dynamics in streams systems and assessing the vulnerability of endangered mussel populations to higher flows associated with climate change in Scotland. Copyright © 2015 John Wiley & Sons, Ltd.

Impacts of invasive crayfish (Pacifastacus leniusculus) on endangered freshwater pearl mussels (Margaritifera laevis and M. togakushiensis) in Japan

The invasive alien crayfish Pacifastacus leniusculus is considered harmful to freshwater pearl mussels Margaritifera laevis and M. togakushiensis. It also often colonises mussel habitats in Japan. In order to test the negative effects of alien crayfish on mussels, we evaluated the predation impact of signal crayfish on freshwater pearl mussels in vitro. We tested the relationship between the survival/injury rates of mussels and crayfish predation with respect to different sizes of mussels (four classes based on shell length: 10, 30, 50 and 70 mm). Crayfish selectively fed on the flesh of the 10-mm size class mussels after breaking their shells. The shell margins of mussels in all size classes were injured by crayfish. Results also showed that crayfish particularly injured the 50-mm size class of mussels. This observation could be attributed to this mussel size being the most suitable shell size (29.56–37.73 mm in carapace length) that the crayfish can effectively hold. This study shows that the presence of invasive crayfish reduces freshwater pearl mussel populations by damaging the shell margins and/or killing the mussels. This negative impact of invasive crayfish not only decreases the mussel population but could also limit mussel recruitment, growth and reproduction.

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.

The impact of land use on the mussel Margaritifera margaritifera and its host fish Salmo trutta

Today, land use impacts a major proportion of all streams. Here, landscape features in corridors along streams and water chemical factors were analyzed in relation to recruitment of the threatened freshwater pearl mussel (Margaritifera margaritifera) and its host fish the brown trout (Salmo trutta). Mussel recruitment and trout density were negatively related to forest clear-cuts. Mussel recruitment was negatively related to water color and turbidity. Therefore, the threats to the mussel may be severe, as low mussel recruitment may be caused by direct effects on the juvenile mussels and indirect effects on the host fish. High proportions of lakes and ponds were found to be positive for recruitment and for trout, and deciduous forest was positively related to trout. The combination of investigations at different scales at the landscape level and at in-stream levels may be applicable to find threats to other threatened species. The results indicate that forestry activities may negatively affect recruitment of freshwater pearl mussels and its host fish. Reductions of forestry activities and the retaining of intact quantity and quality of the riparian zones next to streams, both for the mussel and its host fish may be important conservation measures to restore freshwater pearl mussel populations.