Physical microhabitat requirements of freshwater pearl mussels,Margaritifera margaritifera (L.)

Surface sediment diatoms from the east coast of Lake Tanganyika were analysed using ordination and classification techniques, and compared with assemblages previously described from the northern part of the lake. Grain-size analyses were performed on subsamples. Four groups of diatom assemblages were recognised. The first group clusters samples taken in the north, far from the Rusizi river mouth. The second group comprises samples taken on silty sediment along the Tanzanian coast, including one sample taken near the mouth of the Malagarazi river and those from the northernmost part of the lake. The third group comprises surface sediments along the Burundian coast (near Ramba and Magara), and the fourth is characterised by epipsammic taxa. A sample taken near the central arm of the Malagarazi river is included in the latter group. The impact of small rivers on the diatom assemblages in the surface sediments is restricted to the mouth area.     

Timing of spawning and glochidial release in Scottish freshwater pearl mussel (Margaritifera margaritifera) populations

1. The timing of reproduction was investigated in six Scottish freshwater pearl mussel populations from 1993 to 2002. Gravid females were examined and the release of mussel larvae (glochidia) was monitored. 2. Annual spawning (oviposition) and spat (glochidial release) events occurred during June to July and June to September, respectively. 3. Between‐river differences in timing seem to be related to water temperature. Mussels in the warmest rivers tend to spawn and spat first, and vice‐versa. 4. Thermal variations also seem to influence the timing of reproduction within rivers, which can be delayed by several weeks during cold years. At least 3000°‐days occur between annual episodes of glochidial release. 5. The timing of spawning is determined gradually, probably by a thermal summation effect. 6. The release stage occurs as a sudden, synchronised event, with most of the glochidia spat over 1–2 days, indicating that it is triggered by an environmental cue. Sudden changes in water temperature and/or river level often result in spats, and the underlying mechanism may be respiratory.     

Length‐specific growth rates in freshwater mussels (Bivalvia: Unionidae): extreme longevity or generalized growth cessation?

1. North American lacustrine freshwater mussels (Bivalvia: Unionidae) are one of the world's most imperilled groups of organisms. Knowledge of their age structure and longevity is needed for the understanding and management of mussels. Current methods for age estimation in freshwater mussels are insufficient and may have resulted in an erroneous view of the ages of lacustrine freshwater mussels.
2. We collected growth data through mark-recapture in Minnesota and Rhode Island, U.S.A., examining four lentic populations of three of the most common species of freshwater mussels, Elliptio complanata , Lampsilis siliquoidea , and Pyganodon grandis . Using an inversion of the von Bertalanffy growth equation, we estimated age at length from length-specific growth relationships.
3. In some populations, lacustrine mussels may be much older than previously predicted. Ages predicted from actual growth rates suggest that individuals in some populations frequently reach ages in excess of a century, placing unionid mussels among the Earth's longest-lived animals. Alternatively, if growth has only recently slowed in these populations, generalized growth cessation may be occurring over a broad distributional range of some common North American lacustrine mussels.     

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

Freshwater fishes are vulnerable to changes in water quality, physical habitat and connectivity resulting from drought, particularly in regulated rivers. When adequate river flows return, the recovery of populations might depend on the duration and consequences of drought. Rivers of the highly regulated Murray–Darling Basin in south-eastern Australia terminate at two large, shallow lakes that are separated from the estuary by tidal barrages. Over-abstraction of water and widespread prolonged drought (1997–2010) placed the lakes under severe environmental stress, culminating in critical water level recession from 2007 to 2010. Concurrently, most freshwater fish populations collapsed. We investigate shifts in fish assemblages resulting from habitat inundation in the lakes following the drought. The inundation and re-connection of the lakes and fringing habitats led to a substantial reduction of salinity throughout the region, and aquatic vegetation shifted from salt-tolerant to freshwater species. Fish assemblages became increasingly characterized by common freshwater taxa (ecological generalists), including high proportions of alien species. There were no indications of population recovery for three threatened species. The findings emphasize that short-lived fishes with specialized habitat requirements are vulnerable to severe population declines during prolonged drought in regulated rivers, which might restrict their recovery when adequate flows return.     

Duration of the parasitic phase determines subsequent performance in juvenile freshwater pearl mussels (Margaritifera margaritifera)

Host–parasite systems have been useful in understanding coevolutionary patterns in sympatric species. Based on the exceptional interaction of the long‐lived and highly host‐specific freshwater pearl mussel (FPM; Margaritifera margaritifera) with its much shorter‐lived host fish (Salmo trutta or Salmo salar), we tested the hypotheses that a longer duration of the parasitic phase increases fitness‐related performance of mussels in their subsequent post parasitic phase, and that temperature is the main factor governing the duration of the parasitic phase. We collected juvenile mussels from naturally and artificially infested fish from eight rivers in Norway. Excysted juvenile mussels were maintained separately for each collection day, under similar temperature and food regimes, for up to 56 days. We recorded size at excystment, post excystment growth, and survival as indicators of juvenile fitness in relation to the duration of the parasitic phase. We also recorded the daily average temperatures for the entire excystment period. We observed strong positive relationships between the length of the parasitic phase and the post parasitic growth rate, size at excystment and post parasitic survival. Temperature was identified as an important factor governing excystment, with higher temperatures decreasing the duration of the parasitic phase. Our results indicate that juvenile mussels with the longest parasitic phase have better resources (larger size and better growth rate) to start their benthic developmental phase and therefore to survive their first winter. Consequently, the parasitic phase is crucial in determining subsequent survival. The temperature dependence of this interaction suggests that climate change may affect the sensitive relationship between endangered FPMs and their fish hosts.     

Development of microsatellite markers for the endangered freshwater pearl mussel Margaritifera margaritifera L. (Bivalvia: Unionoidea)

Freshwater pearl mussels (Margaritifera margaritifera L.) are among the most critically endangered freshwater invertebrates. We describe the isolation and characterization of the first microsatellite markers for this species, which were obtained by screening 4900 recombinant clones from two genomic libraries. Thirteen loci revealed polymorphisms as demonstrated on 42 tested individuals from four river drainages. Allelic richness ranged from two to 12 alleles and averaged 6.8 alleles per locus with heterozygosity levels varying from 0 to 0.850 for observed heterozygosity (H_O) and from 0.174 to 0.850 for expected heterozygosity (H_E). Deficiency of heterozygous genotypes was observed in eight of 13 loci.     

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.     

Growth and longevity in freshwater mussels: evolutionary and conservation implications

The amount of energy allocated to growth versus other functions is a fundamental feature of an organism's life history. Constraints on energy availability result in characteristic trade‐offs among life‐history traits and reflect strategies by which organisms adapt to their environments. Freshwater mussels are a diverse and imperiled component of aquatic ecosystems but little is known about their growth and longevity. Generalized depictions of freshwater mussels as ‘long‐lived and slow‐growing’ may give an unrealistically narrow view of life‐history diversity which is incongruent with the taxonomic diversity of the group and can result in development of inappropriate conservation strategies. We investigated relationships among growth, longevity, and size in 57 species and 146 populations of freshwater mussels using original data and literature sources. In contrast to generalized depictions, longevity spanned nearly two orders of magnitude, ranging from 4 to 190 years, and the von Bertalanffy growth constant, K, spanned a similar range (0.02–1.01). Median longevity and K differed among phylogenetic groups but groups overlapped widely in these traits. Longevity, K, and size also varied among populations; in some cases, longevity and K differed between populations by a factor of two or more. Growth differed between sexes in some species and males typically reached larger sizes than females. In addition, a population of Quadrula asperata exhibited two distinctly different growth trajectories. Most individuals in this population had a low‐to‐moderate value of K (0.15) and intermediate longevity (27 years) but other individuals showed extremely slow growth (K = 0.05) and reached advanced ages (72 years). Overall, longevity was related negatively to the growth rate, K, and K explained a high percentage of variation in longevity. By contrast, size and relative shell mass (g mm^?1 shell length) explained little variation in longevity. These patterns remained when data were corrected for phylogenetic relationships among species. Path analysis supported the conclusion that K was the most important factor influencing longevity both directly and indirectly through its effect on shell mass. The great variability in age and growth among and within species shows that allocation to growth is highly plastic in freshwater mussels. The strong negative relationship between growth and longevity suggests this is an important trade‐off describing widely divergent life‐history strategies. Although life‐history strategies may be constrained somewhat by phylogeny, plasticity in growth among populations indicates that growth characteristics cannot be generalized within a species and management and conservation efforts should be based on data specific to a population of interest.     

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.     

The Crown Pearl: a draft genome assembly of the European freshwater pearl mussel Margaritifera margaritifera (Linnaeus, 1758)

Since historical times, the inherent human fascination with pearls turned the freshwater pearl mussel Margaritifera margaritifera (Linnaeus, 1758) into a highly valuable cultural and economic resource. Although pearl harvesting in M. margaritifera is nowadays residual, other human threats have aggravated the species conservation status, especially in Europe. This mussel presents a myriad of rare biological features, e.g. high longevity coupled with low senescence and Doubly Uniparental Inheritance of mitochondrial DNA, for which the underlying molecular mechanisms are poorly known. Here, the first draft genome assembly of M. margaritifera was produced using a combination of Illumina Paired-end and Mate-pair approaches. The genome assembly was 2.4 Gb long, possessing 105,185 scaffolds and a scaffold N50 length of 288,726 bp. The ab initio gene prediction allowed the identification of 35,119 protein-coding genes. This genome represents an essential resource for studying this species’ unique biological and evolutionary features and ultimately will help to develop new tools to promote its conservation.     

Genetic diversity and differentiation of central European freshwater pearl mussel (Margaritifera margaritifera L.) populations: implications for conservation and management

Despite the fact that mollusc species play an important role in many aquatic ecosystems, little is known about their biodiversity and conservation genetics. Freshwater pearl mussel (Margaritifera margaritifera L.) populations are seriously declining all over Europe and a variety of conservation programs are being established to support the remaining endangered central European populations. In order to provide guidelines for conservation strategies and management programs, we investigated the genetic structure of 24 freshwater pearl mussel populations originating from five major central European drainages including Elbe, Danube, Rhine, Maas and Weser, representing the last and most important populations in this area. We present a nondestructive sampling method of haemolymph for DNA analyses, which is applicable for endangered bivalves. The analyses of nine microsatellite loci with different levels of polymorphism revealed a high degree of fragmented population structure and very different levels of genetic diversity within populations. These patterns can be explained by historical and demographic effects and have been enforced by anthropogenic activities. Even within drainages, distinct conservation units were detected, as revealed from high F(ST) values, private alleles and genetic distance measures. Populations sampled close to contact zones between main drainage systems showed lowest levels of correct assignment to present-day drainage systems. Populations with high priority for conservation should not only be selected by means of census population size and geographical distance to other populations. Instead, detailed genetic analyses are mandatory for revealing differentiation and diversity parameters, which should be combined with ecological criteria for sustainable conservation and recovery programs.     

Glochidium metamorphosis in the endangered freshwater mussel Margaritifera auricularia (Spengler, 1793): a histological and scanning electron microscopy study

The metamorphosis of the glochidium of the critically endangered Margaritifera auricularia in the gills of a host is studied here for the first time. Siberian sturgeon, Acipenser baeri, were infected with glochidia and regularly inspected using scanning and optical microscopy. The mature glochidia immediately attach to the epithelium of the sturgeon gill filaments, piercing the secondary lamellae and the connective tissues, blood cells, and vessels within the lamellae. Once the epithelium is pierced, overlapping host lamellae cover the glochidium and form a cyst. Metamorphosis takes place inside the cyst. Sixteen days after infection the glochidium becomes spherical in shape and the larval muscle is reabsorbed. The two adductor muscles of the juvenile are observed 34 days after infection at 16-20 degrees C. Metamorphosis is complete in approximately 51 days at 18-22 degrees C and in 65 days at 16-17 degrees C. Released juveniles have a spherical shell with a thin rim of new shell material and a finely ciliated foot. Juvenile mean measurements are: length = 190 microm, width = 193 microm, and height = 210 microm.     

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.     

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 infection 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 respective 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 effectively be invested in an intensive maintenance of juveniles at the laboratory and during hibernation in the field.     

Population density and age structure of the freshwater pearl mussel, Margaritifera margaritifera, in two Iberian rivers

1. The European freshwater pearl mussel, Margaritifera margaritifera (Bivalvia: Unionoida), is one of the most threatened mussels. The Iberian populations of this species are considered peripheral because their distinct characters such as growth rate and longevity, and require development of effective conservation strategies. 2. We assessed population density and age structure of pearl mussels in two Galician rivers (Eo and Masma in north‐west Spain). Four sampling sites were selected in each river to cover stretches of 100 m. The mean density of mussels in each of these sampling transects was estimated using the adaptive sampling technique, given that mussels occur at low densities and are highly aggregated in these rivers. 3. Age structure was inferred for each population using length–age keys. The empty shells encountered during sampling were used to determine the length of the specimens at different ages (years), together with length‐at‐age data from shells previously analysed for computing growth rates from the same rivers. Water samples from both rivers were analysed for typical physicochemical parameters. 4. Mean densities were very variable, even within the same river (from 0.27 to 6.55 m^?2 in the River Eo and from 0.98 to 2.38 m^?2 in the River Masma). Individuals in the 0‐ to 5‐year age class were scarce in both rivers. 5. Margaritifera margaritifera showed a preference for the strip of river bed within 1.5 m from the river bank and avoided sites at greater distances. The species also showed a preference for sites with more than 80% tree cover and avoided sites with <50% cover. 6. Iberian populations exhibit the highest growth rate, together with the lowest maximum age and maximum length known for M. margaritifera. Detailed knowledge about these peripheral Iberian populations will contribute to developing strategies for conservation and management of this endangered species.     

Reach- and catchment-scale determinants of the distribution of freshwater mussels (Bivalvia: Unionidae) in south-eastern Michigan, U.S.A.

1. We investigated the diversity and distribution of freshwater mussels at 40 sites in an agricultural catchment, the River Raisin in south‐eastern Michigan, to relate mussel assemblages and individual taxa to reach and catchment‐scale variables. Unionids were surveyed by timed searches in 100‐m reaches, and in‐stream and riparian habitat were quantified as well as flow, water chemistry and channel morphology. Land use/cover and surficial geology were determined for site subcatchments and riparian buffers. 2. Some 21 mussel species were found overall; richness ranged from 0 to 12 living species per site. From the upper to middle to lower catchment, the number of individuals, number of species, Shannon–Weaver diversity and relative abundance of intolerant unionids all declined significantly. 3. Four groupings based on overall mussel diversity and abundance were significantly related to reach‐scale habitat variables. The richest mussel assemblages were associated with sites with higher overall habitat quality, greater flow stability, less fine substratum, and lower specific conductance. 4. Stepwise multiple regressions revealed that the distribution and abundance of the total mussel assemblage, as well as the most common species, could be predicted from a combination of reach‐ and catchment‐scale variables (R² = 0.63 for total mussels, R² = 0.51–0.86 for individual species). 5. Flow stability, substratum composition and overall reach habitat quality were the most commonly identified reach‐scale variables, and measures of surficial geology were the most effective catchment‐scale variables. The spatial pattern of geology is likely to be responsible for the diversity gradient from the upper to the lower catchment. 6. Prior studies, attempting to explain mussel distributions from local habitat features alone, have found relatively weak relationships. By employing a combination of reach‐ and catchment‐scale habitat variables, this study was able to account for a substantial amount of the spatial variability in mussel distributions.     

Feeding and growth of the pearl oyster Pinctada margaritifera (L.) in Dongonab Bay,Red Sea

Plankton samples and gut contents of P. margaritifera were analysed monthly from April 1972 to March 1973. Coscinodiscus sp. was the most ingested food by pearl oysters of all ages. However, food variety increased as the oyster grew older. Experiments confirmed the absence of food selectivity in P. margaritifera. Unlike the young ones, the adult showed reduced growth during summer (July–September), which coincides with its spawning season.     

Assessment of nutritional subsidies to freshwater mussels using a multiple natural abundance isotope approach

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