Environmental factors affect the condition of critically endangered freshwater pearl mussels by disrupting terrestrial–aquatic resource connectivity

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.

Multiple paternity is an important characteristic of the genetic mating system and common across a wide range of taxa. Multiple paternity can increase within‐population genotypic diversity, allowing selection to act on a wider spectre of genotypes, and potentially increasing effective population size. While the genetic mating system has been studied in many species with active mating behavior, little is known about multiple paternity in sessile species releasing gametes into the water. In freshwater mussels, males release sperm into the water, while eggs are retained and fertilized inside the female (spermcast mating). Mature parasitic glochidia are released into the water and attach to the gills of fish where they are encapsulated until settling in the bottom substrate. We used 15 microsatellite markers to detect multiple paternity in a wild population of the freshwater pearl mussel (Margaritifera margaritifera). We found multiple paternity in all clutches for which more than two offspring were genotyped, and numbers of sires were extremely high. Thirty‐two sires had contributed to the largest clutch (43 offspring sampled). This study provides the first evidence of multiple paternity in the freshwater pearl mussel, a species that has experienced dramatic declines across Europe. Previous studies on other species of freshwater mussels have detected much lower numbers of sires. Multiple paternity in freshwater pearl mussels may be central for maintaining genetic variability in small and fragmented populations and for their potential to recover after habitat restoration and may also be important in the evolutionary arms race with their fish host with a much shorter generation time.

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 COMMUNICATION WIDER RIPARIAN BUFFER STRIPS: A COSTEFFECTIVE CONSERVATION MEASURE FOR FRESHWATER PEARL MUSSELS IN IRELAND? D. Ó hUallacháin INTRODUCTION The freshwater pearl mussel Margaritifera margaritifera (FPM) is a long-lived invertebrate that is found in coarse sand or fine gravel in clean, well-oxygenated, fast-flowing and unpolluted freshwater (Moorkens 1999; 2000; Skinner et al. 2003). The species has undergone a dramatic decline in the sizes of most meta-populations and in the size of its range over the twentieth century (Young 1991; Reid et al. 2012), with an estimated reduction of over 90% in the FPM population in central Europe over this time (Bauer 1988). The species is in very serious decline throughout its range and is listed in the IUCN red data book as endangered worldwide (Baillie and Groombridge 1996) and in the most recent IUCN Irish Red List of non-marine molluscs as critically endangered (Byrne et al. 2009). Ireland is considered a stronghold for the FPM and is believed to support approximately 46% of FPM individuals in the EU (DAFF 2008). However, the NPWS (2008; 2013) concluded that recruitment levels were insufficient in all Irish FPM populations, resulting in all FPM populations, including the populations in designated Special Areas of Conservation (SAC), having unfavourable conservation status. A number of factors are believed to be responsible for the decline in European FPM populations, including organic pollution; sedimentation ; a decline in fish stocks; over-exploitation; and habitat degradation (Beasley and Roberts 1999; Cosgrove and Hastie 2001; Englund et al. 2008). Freshwater pearl mussels have a complex life cycle (Moorkens 1999), and in order to successfully recruit juveniles, they require well-oxygenated rivers that are low in nutrients and have riverbeds containing clean gravel and sand (Curtis et al. 2009). They are particularly sensitive to environmental pressures that cause habitat degradation (e.g. sedimentation and pollution). In Ireland, the principal threat to the species is believed to be poor substrate quality as a result of physical siltation/sedimentation and excess growth of algae and macrophytes (due to nutrient enrichment) (NPWS 2008; 2013; DEHLG 2009). As agriculture is the dominant land-use in Ireland, it is unsurprising that it is also one of the predominant pressures on FPM catchments; for example, restructuring of agricultural land holdings and diffuse pollution to surface waters due to agricultural and forestry activities are believed to be among the most significant threats to FPM in Ireland (NPWS 2013). In an effort to halt the continued decline, the FPM has been protected under Irish and international legislation. The species is listed in Annexes II and V of the European Habitats Directive (EEC 1992) and Appendix III of the Bern Convention (Council of Europe 1979). In 2009, the European Communities Environmental Objectives (Freshwater Pearl Mussel) (EC 2009) were established to support the achievement of favourable conservation status for FPMs. In Ireland, the species is also protected under the Wildlife Act 2000. However, designation alone has proven inadequate in ensuring the sustainability of FPM populations in Ireland. The national population of mature FPM declined by approximately 8% between 2006 and 2012 (NPWS 2013), despite the most-densely populated FPM sites being protected. The report concluded that the conservation status of the FPM was ‘unfavourable bad’ and that the overall trend in the conservation status was ‘declining’. The most urgent challenge therefore for the conservation FPM in Ireland is reducing losses of sediment and nutrients from forestry and agriculture through the development and implementation of cost-effective mitigation measures. WHAT ARE RIPARIAN BUFFER STRIPS AND WHAT ROLE DO THEY PLAY IN NUTRIENT/SEDIMENT REMOVAL? The Habitats Directive (Article 6) requires Member States to avoid the deterioration of natural habitats within SACs and establish conservation measures for annexed species. To date, many measures have been proposed in an effort to reduce the catchment pressures on FPM (for example, see DEHLG 2010). Received 5 May 2014. Accepted 5 April 2014. Published 15 October 2014. D. Ó hUallacháin (email: daire.ohuallachain @teagasc.ie) Teagasc, Johnstown Castle Research Centre, Wexford. Cite as follows: D. Ó hUallacháin 2014 Wider riparian buffer strips: A cost-effective conservation measure for freshwater pearl mussels in Ireland? Biology and Environment: Proceedings of the Royal...

Freshwater pearl mussels (family Margaritiferidae) are sensitive to human impact and environmental changes. Large declines in their abundance have prompted studies of distribution and estimations of population densities. Iturup Island, a part of Kuril Islands, Russia, is considered to be within the distribution area of freshwater pearl mussels, but this information is based on only two specimens collected several decades ago. Detailed survey of the island is challenging as most of its territory is nearly impassable. A preliminary analysis of island rivers was carried out prior to the surveys to discover potential freshwater pearl mussel habitats. Based on previous experience from European Russia, freshwater pearl mussel habitat was expected to occur in rivers flowing out of lowland lakes. Live individuals of Margaritifera laevis were found during surveys in one river together with the unionid Beringiana beringiana, which were also found in two other rivers where the predicted habitat occurred. Based on prediction and surveys, the occurrence of freshwater pearl mussels in other rivers of Iturup Island is unlikely. Pearl mussels were concentrated in a small section of the Zmeika River with a population of about 100,000 mussels. Present threats to the population include overharvest of host fish masou salmon (Oncorhynchus masou). Surveys using similar methods can help to reveal unknown freshwater mussel populations on other Kuril Islands and on the mainland.

ABSTRACTThe freshwater pearl mussel (genus Margaritifera) has shown severe declines, while the mussels play important roles in the translocation of nutrients and materials in river water ecosystems. We hypothesized that the biofilm bacterial composition and nutrient flow may reflect the differences in the existence of mussels. We analyzed water from 14 rivers from in multiple regions of Japan, including eight rivers, where the two species of freshwater pearl mussels (Margaritifera laevis and Margaritifera togakushiensis) are predominantly found, to analyze the microbial and nutritional nature of the biofilm artificially formed in the river. Field-produced biofilms, including the bacterial community structure, were examined, using next-generation sequencing of bacterial 16S rRNA gene amplicons followed by analyzing the genomic DNA extracted from the samples, inorganic nitrogen compounds, and chlorophyll a concentration. Compared to those in the control river without freshwater pearl mussels, biofilms of the existing river contained less inorganic nitrogen (ammonia and nitrate), suggesting the involvement of mussels in regulating the river water nutrient flow. Distinct changes were found in biofilms, depending on mussel existence, particularly in biofilms containing fewer photosynthetic bacterial groups, such as Betaproteobacteria and Cyanobacteria. Conversely, bacteria belonging to Bacteroidales in Bacteroidetes and Clostridiales in Firmicutes were predominantly found in biofilm samples where the mussels existed. Mussels alleviated strict nitrogen limitation in streams and possibly caused a concomitant change in the bacterial communities, where populations of bacterial groups exchanging inorganic nitrogen were low. We demonstrate the profound influence of freshwater mussel species on ecosystem processes and community dynamics across rivers.IMPORTANCE The abundance of freshwater unioid mussels exhibited more diverse patterns of inorganic nitrogen flow and bacterial communities than the areas without mussels. This study demonstrates the effect of mussels on different freshwater ecosystem processes with variable organismal densities and biogeochemical factors. Freshwater unionid mussels significantly affect the ecosystem and community dynamics by modulating the relationships, altering nutrient availability, and indirectly manipulating the downstream ecological members, eventually expanding their role in the river ecosystems.

Environmental DNA (eDNA) from water samples is increasingly used to detect the presence and distribution of species in aquatic ecosystems. However, before implementing eDNA in monitoring programmes, various species‐specific sampling or analytical issues remain to be resolved in order to minimize frequencies of false‐positive and ‐negative results. For example, empty shells from freshwater pearl mussels (Margaritifera margaritifera) contain extractable DNA (chemical extraction from ground‐up shells) suggesting a risk of false‐positive samples at stream sites with extinct populations but with empty shell material remaining. The aim of this study was to investigate whether empty and naturally degrading shells from M. margaritifera can cause false‐positive eDNA signals in water samples. Water samples were collected from outdoor stream channels (in Lemming, Denmark) with living freshwater pearl mussels or empty shell material (density ~10 individuals m−2) during a 3‐week experimental period. Living freshwater pearl mussels were collected from Hemgravs stream in Sweden and transported to Denmark according to permissions granted by the Swedish and Danish authorities. All water samples from stream channels containing empty shells were negative for eDNA indicating that eDNA traces in stream water are most likely to originate from living individuals located upstream of the sampling site. Water samples collected from stream channels containing living individuals of M. margaritifera were consistently positive for eDNA except for one sample (interpreted as a false negative). The study shows that positive eDNA signals for freshwater pearl mussels most likely reflect the presence of living individuals. Consequently, we suggest that eDNA should be used to locate remaining population fragments of M. margaritifera in deep and turbulent streams, providing a platform for faster and more efficient decision making when launching investigative and mitigation initiatives.

Application of plate-tectonic concepts to sedimentary basin development has been important in petroleum geology. Physical aspects have been stressed, but a complete classification must include the amount, type, and distribution of organic matter because this is the material that generates petroleum. Organic matter can be classified into two broad categories: (1) land-derived (terrestrial) organic matter that may include major amounts of lignin and surface coatings which give gas or waxy crudes respectively, and (2) aquatic organic matter which commonly is dominantly of algal origin and generates normal crudes. The relative amounts of these two types of organic matter, and hence the relative amounts of oil and gas, depend on the depositional environment and this can be r lated to plate-tectonic setting. Rifts that form in the early stages of continental breakup receive high percentages of terrestrially derived organic matter initially, but aquatic organic matter becomes quantitatively more significant as the rift widens and marine conditions develop. Thus pull-apart continental margins develop a vertical profile from terrestrial organic matter deep to aquatic organic matter shallow. The deeper continentally derived sedimentary sections of these margins produce waxy crudes, gas, and some condensate reflecting the character of the organic matter. Pull-apart margins and rifts with waxy crudes were within 20° of the equator at the time of rifting. They include the Sirte, Cambay, Reconcavo, Gabon, and Cuanza basins. When rifting occurred farther from the equator, gas-dominated provin es were developed, such as northwest Australia, offshore Newfoundland, Baltimore Canyon, and the central Viking graben. Rivers transport continental sediments and organic matter to continental margins, and the association of transported terrestrial organic matter with clastic sediments makes deltas one of the most gas-prone depositional environments. Organic materials are not distributed uniformly in deltas because terrestrial organic matter has its highest concentration nearshore whereas aquatic material is also produced in large amounts offshore. This separation and distribution lead to gas fields near paleoshorelines and oil farther out. As the delta progrades, terrestrial organic matter is deposited over the previously deposited aquatic organic matter. This profile of organic matter type is exactly the opposite of that developed on passive continental margins and leads to the opposite trend for the distribution of oil and gas with depth. Although organic-matter type exercises initial control over the nature of the hydrocarbons generated, the composition may be changed later by maturation and migration. Maturation is the thermally induced trend from oil to gas and the depth for this conversion will depend on geothermal gradient. Migration distance is also controlled by plate-tectonic setting with distances in excess of 100 km being well documented for structurally simple interior basins. In contrast, migration distances are much shorter when migration pathways are interrupted, for example, by block faulting in rifts and growth faults in deltas. End_of_Article - Last_Page 1356------------

Transport and deposition of terrestrial organic matter in marine littoral deltas: New evidence from flume experiments and 3D laser scanning

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.

Water mill canals as habitat for Margaritifera margaritifera: Stable refuge or an ecological trap?

Exploring the optimal integrated multi-trophic aquaculture (IMTA) patterns benefiting culture animals and natural water environment

Freshwater pearl mussels (Margaritifera margaritifera) in the River Dee (north-east Scotland) are in decline, and now occur at low densities with poor recruitment levels. The population's deterioration has been attributed to reduced water quality, degraded river-bed habitat and pearl fishing but the specific importance of each of these impacts has not previously been investigated. This study focused on the impacts of artificial structures on the River Dee's freshwater pearl mussel population. Natural hydromorphological features were also included in the analysis. Relationships between the spatial distribution of the freshwater pearl mussel population and 31 explanatory variables were investigated using logistic regression. Three different model selection strategies were compared and contrasted. An absence of freshwater pearl mussels was found to be significantly associated with the following factors: (1) presence of bank protection; (2) proximity of the nearest upstream bridge; (3) presence of a wastewater treatment works; (4) number of upstream tributaries; (5) proximity of the nearest upstream tributary; and (6) presence of sediment deposition. The results strongly suggest that artificial structures on the main stem of the River Dee have contributed to the decline of its freshwater pearl mussel population. Hypotheses are proposed for the causal relationships involved. Requirements for further exploratory analyses, model testing, and experimentation are discussed. This work opens a new line of investigation into the causes of the decline of freshwater pearl mussel populations, providing formal support at a catchment scale for an impact previously identified only on a site-by-site basis. Copyright © 2012 John Wiley & Sons, Ltd.

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.

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