The freshwater pearl mussel <Emphasis Type="Italic">Margaritifera margaritifera</Emphasis> in Bavaria,Germany—Population status,conservation efforts and challenges

The freshwater pearl mussel Margaritifera margaritifera is a highly specialized, sensitive and critically endangered freshwater bivalve with a complex life cycle. An overview on the population status in Bavaria, Germany, one of the species’ main areas of distribution in Central Europe, is presented. Using the example of the freshwater pearl mussel and a Bavarian conservation project for this species, a scheme for the development of site-specific conservation concepts is discussed.     

Results of testing the comparatory method: The curvature of the shell valve frontal section is inappropriate as a systematic character for the freshwater pearl mussel of the genus Margaritifera

This paper continues a discussion on the number of pearl mussel species of the genus Margaritifera in northern Europe. A biometric study of 1711 pearl mussel Margaritifera margaritifera shells from 15 rivers in Russia and Latvia (basins of the White and Baltic seas) has been conducted. All the examined samples fall into two groups: the northern group (with the shells more flattened on average, f. margaritifera) and the southern one (with more convex shells, f. elongata); the boundary between these groups is at 63° N. Analysis of intrapopulation variation has shown that the samples contain individuals that correspond to f. margaritifera, f. elongata, and f. borealis. However, any hiatus between these forms is absent in all the samples, and individuals belonging to two intermediate forms are rather frequent. The hypothesis on the species specificity of the shell valve frontal section has not been confirmed based on examination of large shell samples. The pearl mussels inhabiting rivers of Northern Europe belong to a single species, M. margaritifera.     

Strong genetic differentiation and low genetic diversity of the freshwater pearl mussel (<Emphasis Type="Italic">Margaritifera margaritifera</Emphasis> L.) in the southwestern European distribution range

Genetic diversity of European freshwater pearl mussel, Margaritifera margaritifera (L.), appears exceptional with highest genetic variability found in the northernmost European populations of Scandinavia and lower genetic variability in central and southern Europe. The objective of this study was to investigate genetic diversity and differentiation of 14 southernmost populations on the Iberian Peninsula which greatly differ in terms of life span and habitat conditions from the rest of central and northern European populations. The analyses of ten microsatellite loci revealed a pronounced level of genetic divergence and very low genetic diversity. These results match the expectations of geographically peripheral populations with respect to their genetic composition. The life history strategy, the narrow ecological niche of the species, and anthropogenic habitat modifications have most likely shaped the genetic pattern of Iberian pearl mussel populations. The peripheral position with less optimal habitat conditions may increase the extinction risk of these populations and thus effective conservation strategies for the Iberian M. margaritifera are needed. The successful conservation of the species at its southwestern margin requires inclusion of genetically different conservation units which may reveal local adaptation.     

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.     

Drainage-independent genetic structure and high genetic diversity of endangered freshwater pearl mussels (<Emphasis Type="Italic">Margaritifera margaritifera</Emphasis>) 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.     

Variation in the <Emphasis Type="Italic">COI</Emphasis> gene of the freshwater pearl mussel <Emphasis Type="Italic">Margaritifera margaritifera</Emphasis> 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.     

Irregularity of the linear growth of the <Emphasis Type="Italic">Margaritifera margaritifera</Emphasis> (Bivalvia: Margaritiferidae) population of the Nemina River,Karelia

The dependence of shell growth in length and height during ontogeny has been studied in the pearl mussel Margaritifera margaritifera inhabiting the Nemina River (basin of Lake Onega, Karelia). It has been shown that the population is heterogenous based on the height-to-length ratio. It has been found that during ontogeny M. margaritifera from the studied population undergoes a constant change in the relative growth of the shell leading to either lengthening or rounding of the shell.     

Modelling distributional trends to inform conservation strategies for an endangered species

Aim Species loss has increased significantly over the last 1000 years and is ultimately attributed to the direct and indirect consequences of increased human population growth across the planet. A growing number of species are becoming endangered and require human intervention to prevent their local extirpation or complete extinction. Management strategies aimed at mitigating a species loss can benefit greatly from empirical approaches that indicate the rate of decline of a species providing objective information on the need for immediate conservation actions, e.g. captive breeding; however, this is rarely employed. The current study used a novel method to examine the distributional trends of a model endangered species, the freshwater pearl mussel, Margaritifera margaritifera (L.). Location United Kingdom and Republic of Ireland. Methods Using species presence data within 10‐km grid squares since records began three‐parameter logistic regression curves were fitted to extrapolate an estimated date of regional extinction. Results This study has shown that freshwater pearl mussel distribution has contracted since known historical records and outlier populations were lost first. Within the United Kingdom and Republic of Ireland, distribution loss has been greatest in Scotland, Northern Ireland, Wales and England, respectively, with the Republic of Ireland containing the highest relative proportion of M. margaritifera distribution, in 1998. Main conclusions This study provides empirical evidence that this species could become extinct throughout countries within the United Kingdom within 170 years under the current trends and emphasizes that regionally specific management strategies need to be implemented to prevent extirpation of this species.     

The populations of the freshwater pearl mussel, <Emphasis Type="Italic">Margaritifera margaritifera</Emphasis> (Linnaeus, 1758), and the thick shelled river mussel, <Emphasis Type="Italic">Unio crassus</Emphasis> Philipsson, 1788, in Latvia

The populations of two endangered species—the freshwater pearl mussel Margaritifera margaritifera and the thick shelled river mussel Unio crassus in Latvia were studied. The specimens were counted, measured, population density and age structure were calculated. The possible host fish presence was found.     

Irregularity of the linear growth of the <Emphasis Type="Italic">Margaritifera margaritifera</Emphasis> (Bivalvia: Margaritiferidae) population of the Syskyanjoki River,Karelia

The interdependence of shell growth in length and height during ontogeny has been studied in the pearl mussel Margaritifera margaritifera, inhabiting the Syskyanjoki River (basin of Lake Ladoga, Karelia). It was shown that by the height-to-length ratio of the shell the population is heterogeneous. The question of whether this is due to the heterogeneity of genetic variability or due to variations in the environmental conditions remains unclear. It was found that during the ontogeny of the M. margaritifera from the population there is a constant change in the relative growth of the shell, leading to lengthening or rounding of the shell. Conventionally, all mussels can be divided into two groups, different by the periods of change in the relative growth. A comparison of the results with the data obtained previously for pearl mussels of the Varzuga River (basin of the White Sea, Murmansk oblast) was performed.     

The status of the freshwater pearl mussel <Emphasis Type="Italic">Margaritifera margaritifera</Emphasis> 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.     

The relationship between the freshwater pearl mussel (<Emphasis Type="Italic">Margaritifera margaritifera</Emphasis>) 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.     

Regional monitoring of freshwater pearl mussel <Emphasis Type="Italic">Margaritifera margaritifera</Emphasis> 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.     

Population dynamics of glochidia of the freshwater pearl mussel Margaritifera margaritifera L., parasitizing on juvenile Salmonidae fishes in northern water reservoirs

This paper presents data on the population dynamics of glochidia of the freshwater pearl mussel Margaritifera margaritifera L. (1758) (a declining species of European fauna), parasitizing on juvenile Salmonidae fishes in rivers of northern Europe. It was found that the number of glochidia parasitizing on gills of juvenile salmon and trout in explored water reservoirs are stimulated by negative binomial distribution. Estimation of the distribution parameter allows us to obtain statistically valid data on the population number of pearl mussel and to judge the stable character of interactions in the host-parasite system (balance of host specimens that are resistant and nonresistant to infection).     

Strategies for the conservation of endangered freshwater pearl mussels (<Emphasis Type="Italic">Margaritifera margaritifera</Emphasis> 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.     

Physicochemical stream bed characteristics and recruitment of the freshwater pearl mussel (Margaritifera margaritifera)

1. The freshwater pearl mussel (Margaritifera margaritifera) is endangered and of conservation importance. We used its survival/mortality during the critical post‐parasitic phase as a biological indicator for the habitat quality of the stream substratum. 2. We established and tested biological, physical and chemical methods of assessing the stream bed in 26 streams from seven European countries. We analysed penetration resistance, texture, the concentrations and ratios of C, N, S, P, Fe, Mn in fine material <100 μm, and redox, pH and electric conductivity at the surface and at 5 and 10 cm into the substratum. 3. Sites with high stream bed quality (promoting pearl mussel populations with good juvenile recruitment) had coarser and better sorted substrata with significantly lower quantities of fines, and a higher Mn concentration in the fines, than poor quality sites. Redox potential (Eh) at sites without recruitment differed markedly between the free‐flowing water at the surface and at 5 and 10 cm in the bed, whereas no differences were detectable at good quality sites. This was also true of electric conductivity and, to a lesser extent, pH. The stream bed at sites lacking pearl mussel recruitment had a more variable and higher penetration resistance, indicating clogging of the interstitial macropore system by the deposition of mud and compaction of the stream bed. 4. Our results show that habitat quality for pearl mussels depends strongly on the exchange between the surface and the interstices, which is governed by physicochemical characteristics of the stream substratum. Combined measurements of penetration resistance, depth gradients of Eh and texture were most suitable for assessing stream bed quality, while water chemistry was insufficient because of the decoupling of interstitial and free‐flowing water at poor quality sites.     

Historical geography of pearl harvesting and current status of populations of freshwater pearl mussel Margaritifera margaritifera (L.) in the western part of Northern European Russia

This paper summarises data on the occurrence of freshwater pearl mussel Margaritifera margaritifera in the western part of Northern European Russia adjacent to White Sea, Barents Sea, Onega Lake and Ladoga Lake basins. Also, this article provides an overview of the literature-based data and archive materials on the history of pearl harvesting. We include a list of rivers of Northwestern Russia, where pearls were harvested during the period of the sixteenth to twentieth centuries. The pearl mussel populations at the present time exist in at least 24 water streams in Northwestern Russia. Many of these populations are in high abundance and are able to reproduce normally. Data on the status of populations are given in this paper. Data indicate that the pearl mussel population in Russia contains >143.5 million individuals, but this estimation is certainly undervalued. Timber floating (timber floating is the transport of timber on waterways), hydro-engineering construction, pollution of rivers by industrial wastes and introduction of alien species, as well as a reduction in host fish species numbers can all be cited as the main factors that transformed the ecosystems inhabited by pearl mussel of Northern Russia. In addition, methods used in the Russian Federation for decreasing the anthropogenic load on pearl mussel populations were considered.     

Parasitic freshwater pearl mussel larvae (Margaritifera margaritifera L.) reduce the drift-feeding rate of juvenile brown trout (Salmo trutta L.)

In this paper we describe, for the first time, the effects of freshwater pearl mussel (Margaritifera margaritifera L.) encystment on the drift-feeding behavior of juvenile brown trout (Salmo trutta L.). Because both mussel and salmonid populations are often threatened, this study not only adds knowledge to the understanding of host-parasite systems, but it is also of conservation value. Individual trout, mussel-encysted (25.1?±?5.7 larvae?·?g^?1 body weight, n?=?5) or non-encysted (n?=?5), were fed with chironomid larvae in a flow-through stream aquarium. Feeding trials were filmed and analyzed by counting the numbers of chironomid larvae each individual ate, and by estimating the prey-capture distance. Non-encysted trout had a significantly higher drift-foraging rate than did encysted trout, and they captured significantly more prey further away from their focal point. The reduced foraging success of encysted trout was mainly due to their failure to catch prey relatively further from their focal point. This suggests that reduced foraging success of encysted trout may be due to poorer energetic status, but the physical effects of mussel larvae on prey handling time cannot be ruled out. Encysted trout caught approximately 20 % fewer prey, which would result in a reduction in growth potential during the period of mussel encystment. Reduced energetic status might also result in reduced competitive ability or in increased exposure to predation risk.     

Threatened freshwater pearl mussel <Emphasis Type="Italic">Margaritifera margaritifera</Emphasis> L. in NW Spain: low and very structured genetic variation in southern peripheral populations assessed using microsatellite markers

A genetic analysis of freshwater pearl mussel Margaritifera margaritifera populations from NW Spain, a peripheral area of its European distribution, was carried out using microsatellite markers. These populations were formerly reported as genetically differentiated on the basis of growth and longevity studies. Ten loci previously characterized in populations from central Europe were used to comparatively analyze the genetic variability at the southern edge of the species’ range. Iberian pearl mussel populations showed very low genetic variability and significant high genetic differentiation. Half of the total genetic diversity observed appeared to be distributed between populations, which suggested a highly structured adaptive potential in pearl mussel at the southern peripheral distribution of the species. Population distinctiveness was evidenced by assignment tests, which revealed a high accuracy of individual assignments to their population of origin. All data suggested low effective population size and major effects of genetic drift on population genetic structure. In order to avoid further loss of genetic variation in biologically distinctive populations from NW Spain, prioritization of genetic resources of this species is required for conservation and management.