Regional impacts of warming on biodiversity and biomass in high latitude stream ecosystems across the Northern Hemisphere.

Warming can have profound impacts on ecological communities. However, explorations of how differences in biogeography and productivity might reshape the effect of warming have been limited to theoretical or proxy-based approaches: for instance, studies of latitudinal temperature gradients are often conflated with other drivers (e.g., species richness). Here, we overcome these limitations by using local geothermal temperature gradients across multiple high-latitude stream ecosystems. Each suite of streams (6-11 warmed by 1-15°C above ambient) is set within one of five regions (37 streams total); because the heating comes from the bedrock and is not confounded by changes in chemistry, we can isolate the effect of temperature. We found a negative overall relationship between diatom and invertebrate species richness and temperature, but the strength of the relationship varied regionally, declining more strongly in regions with low terrestrial productivity. Total invertebrate biomass increased with temperature in all regions. The latter pattern combined with the former suggests that the increased biomass of tolerant species might compensate for the loss of sensitive species. Our results show that the impact of warming can be dependent on regional conditions, demonstrating that local variation should be included in future climate projections rather than simply assuming universal relationships.

Freshwater mussel conservation: A global horizon scan of emerging threats and opportunities.

We identified 14 emerging and poorly understood threats and opportunities for addressing the global conservation of freshwater mussels over the next decade. A panel of 17 researchers and stakeholders from six continents submitted a total of 56 topics that were ranked and prioritized using a consensus-building Delphi technique. Our 14 priority topics fell into five broad themes (autecology, population dynamics, global stressors, global diversity, and ecosystem services) and included understanding diets throughout mussel life history; identifying the drivers of population declines; defining metrics for quantifying mussel health; assessing the role of predators, parasites, and disease; informed guidance on the risks and opportunities for captive breeding and translocations; the loss of mussel-fish co-evolutionary relationships; assessing the effects of increasing surface water changes; understanding the effects of sand and aggregate mining; understanding the effects of drug pollution and other emerging contaminants such as nanomaterials; appreciating the threats and opportunities arising from river restoration; conserving understudied hotspots by building local capacity through the principles of decolonization; identifying appropriate taxonomic units for conservation; improved quantification of the ecosystem services provided by mussels; and understanding how many mussels are enough to provide these services. Solutions for addressing the topics ranged from ecological studies to technological advances and socio-political engagement. Prioritization of our topics can help to drive a proactive approach to the conservation of this declining group which provides a multitude of important ecosystem services.

A roadmap for the conservation of freshwater mussels in Europe.

Europe has a long history of human pressure on freshwater ecosystems. As pressure continues to grow and new threats emerge, there is an urgent need for conservation of freshwater biodiversity and its ecosystem services. However, whilst some taxonomic groups, mainly vertebrates, have received a disproportionate amount of attention and funds, other groups remain largely off the public and scientific radar. Freshwater mussels (Bivalvia, Unionida) are an alarming example of this conservation bias and here we point out six conceptual areas that need immediate and long-term attention: knowledge, threats, socioeconomics, conservation, governance and education. The proposed roadmap aims to advance research, policy and education by identifying the most pressing priorities for the short- and long-term conservation of freshwater mussels across Europe.

Cryptic taxonomic diversity and high-latitude melanism in the glossiphoniid leech assemblage from the Eurasian Arctic.

The family Glossiphoniidae is a diverse and widespread clade of freshwater leeches, playing a significant role in functioning of aquatic ecosystems. The taxonomy and biogeography of leeches from temperate, subtropical, and tropical regions attracted much attention of zoologists, while their taxonomic richness and distribution in the Arctic are poorly understood. Here, we present an overview of the Eurasian Arctic Glossiphoniidae based on the most comprehensive occurrence and DNA sequence datasets sampled to date. This fauna contains 14 species, belonging to five genera and three subfamilies. One genus and five species are new to science and described here. The world's northernmost occurrences of glossiphoniids are situated on the Taymyr Peninsula at 72° N, although further records at higher latitudes are expected. Most Arctic leeches are characterized by broad ranges crossing several climatic zones (e.g., Glossiphonia balcanica and G. nebulosa), although the distribution of two new species may be confined to the high-latitude areas. The Taymyr Peninsula with the nearby Putorana Plateau represents the most species-rich area (totally 9 species), while the European Arctic, Iceland, Kolyma Highland, and Chukotka Peninsula house depleted faunas (2-4 species per subregion). Finally, we show that the high-latitude melanism is a common phenomenon in glossiphoniid leeches.

Is the South African leech Barbronia gwalagwalensis Westergren amp; Siddall, 2004 (Hirudinida: Erpobdelliformes: Salifidae) a Paleotropical species?

The freshwater leech family Salifidae Johansson has a Paleotropical range, with a hotspot of species richness in the Oriental Region, and a few species endemic to Africa, Madagascar, and Reunion. Barbronia gwalagwalensis Westergren Siddall, 2004 was thought to be a characteristic example of the latter group being a lineage endemic to South Africa. However, we found that this species also occurs in Asia (Myanmar and Korea). Our time-calibrated phylogeny based on the mitochondrial cytochrome c oxidase subunit I (COI) gene reveals that the split between the African and Asian populations of this species occurred in the mid-Pleistocene, approximately 1.3 Ma ago (95% HPD 0.7-2.1 Ma). The statistical biogeographic modeling indicates that a B. gwalagwalensis population in South Africa most likely originated due a long-distance dispersal event with a subsequent vicariance (probability = 88.9%). A Late Quaternary range extension towards South Africa is known to occur in some other freshwater taxa (e.g. the freshwater mussel Unio caffer Krauss species group), which agrees with our hypothesis on the ancient origin of the South African B. gwalagwalensis population. Conversely, we can assume that the African population of this species was recently introduced from Asia. If so, the high levels of genetic divergence between African and Asian populations could be a part of a more general phylogeographic pattern historically originated within the Asian subcontinent due to the isolation by orographic or marine barriers. These two alternative hypotheses need further research efforts, i.e. sampling and sequencing of other Barbronia taxa, the ranges of which are situated between South Africa and Southeast Asia, as well as of topotypes of B. weberi (Blanchard, 1897) from Indonesia. Finally, our results highlight that the salifid genus Barbronia Johansson originated in the Oriental Region and that these leeches share both recently and historically high potential for long-distance dispersal events.

The role of anthropogenic habitats in freshwater mussel conservation.

Anthropogenic freshwater habitats may provide undervalued prospects for long-term conservation as part of species conservation planning. This fundamental, but overlooked, issue requires attention considering the pace that humans have been altering natural freshwater ecosystems and the accelerated levels of biodiversity decline in recent decades. We compiled 709 records of freshwater mussels (Bivalvia, Unionida) inhabiting a broad variety of anthropogenic habitat types (from small ponds to large reservoirs and canals) and reviewed their importance as refuges for this faunal group. Most records came from Europe and North America, with a clear dominance of canals and reservoirs. The dataset covered 228 species, including 34 threatened species on the IUCN Red List. We discuss the conservation importance and provide guidance on how these anthropogenic habitats could be managed to provide optimal conservation value to freshwater mussels. This review also shows that some of these habitats may function as ecological traps owing to conflicting management practices or because they act as a sink for some populations. Therefore, anthropogenic habitats should not be seen as a panacea to resolve conservation problems. More information is necessary to better understand the trade-offs between human use and the conservation of freshwater mussels (and other biota) within anthropogenic habitats, given the low number of quantitative studies and the strong biogeographic knowledge bias that persists.

Does differential phosphorus processing by plankton influence the ecological state of shallow lakes?

Shallow lakes have a tendency to settle into turbid or clear-water states, the latter having lower concentrations of total phosphorus (TP). However, how P-cycling is affected by and perhaps contributes to maintaining the different states is not well understood, in part because quantifying the processes involved by traditional methods is difficult. To elucidate these processes, we conducted experiments using 32P-PO4 as a tracer on samples collected from the unrestored, unvegetated sections of Huizhou West Lake where turbid water prevails as well as the restored, clear-water, macrophyte-rich waters of the lake. We measured PO4 uptake rates, 32P-PO4 accumulation by various plankton size-fractions (picoplankton (0.2-2 µm), nanoplankton (2-20 µm) and microplankton (>20 µm)) as well as release rates of 32P-PO4 by labelled plankton. Our results revealed slow PO4 uptake in the turbid state due to low PO4 concentration, slow recycling of the high particulate P, and high levels of particulate 32P which may allow for continuous high growth and biomass of phytoplankton. In contrast, in the clear water state, the uptake of PO4 was rapid due to a higher PO4 concentration, the recycling rates of particulate 32P were high and the levels of particulate 32P were low, potentially constraining the phytoplankton growth. A greater proportion of particulate 32P was in the microplankton fraction in clear waters, suggesting that grazing by microplankton may play an important role in the rapid P recycling in clear-waters. Our results provide some evidence for a reinforcement of the turbid conditions (low recycling rate) when the lake is in a turbid state and vice versa when in the clear water state. The results add new knowledge to the understanding of P cycling in shallow lakes and illustrate the utility of using P-kinetics in contrasting states in plankton communities.

First freshwater mussel-associated piscicolid leech from East Asia.

Parasites and symbionts of freshwater mussels are poorly understood, although a diverse assemblage of mussel-associated leeches (Glossiphoniidae) was recently described. Here, we report on the discovery of a fish leech (Piscicolidae) in the mantle cavity of the freshwater mussel Cristaria plicata (Unionidae) in the Russian Far East. It is the first member of this leech family being associated with freshwater molluscs. This leech does not match any known genus and species both morphologically and genetically, and is described here as Alexandrobdella makhrovi gen. & sp. nov. It uses mussels as shelter (and probably as a secondary host), while the Amur catfish Silurus asotus (Siluridae) seems to be the primary host. These novel findings indicate that mussel-associated leech assemblage contains at least one piscicolid species. Our fossil-calibrated phylogeny suggests that the crown group of Piscicolidae was originated in the Early Cretaceous. This primarily marine family shares at least five independent colonization events into freshwater environments.

Integrative taxonomy, biogeography and conservation of freshwater mussels (Unionidae) in Russia.

Freshwater mussels are ecosystem engineers and keystone species in aquatic environments. Unfortunately, due to dramatic declines this fauna is among the most threatened globally. Here, we clarify the taxonomy and biogeography of Russian Unionidae species based on the most comprehensive multi-locus dataset sampled to date. We revise the distribution and assess the conservation status for each species. This fauna comprises 16 native species from 11 genera and 4 tribes: Anodonta, Pseudanodonta (Anodontini); Amuranodonta, Beringiana, Buldowskia, Cristaria, Sinanodonta (Cristariini); Middendorffinaia, Nodularia, Unio (Unionini); and Lanceolaria (Lanceolariini). No country-level endemic species are known in Russia, except for Buldowskia suifunica that may also occur in China. Sinanodonta woodiana, a non-native species, was introduced from China. Russia comprises the northern parts of Western and Eastern Palearctic subregions. The first subregion with six species encompasses a huge area from the western boundary of Russia to the Lena Basin in Siberia. The second subregion with 10 species covers the Amur Basin, rivers east of the Lena Basin, coastal basins of the Japan Sea, and the North Pacific Islands. The fauna of Russia primarily includes widespread generalist species that are here considered Least Concern (LC). However, Buldowskia suifunica and Sinanodonta lauta have restricted distributions and are assessed here as Vulnerable (VU) and Endangered (EN), respectively.

Freshwater mussels house a diverse mussel-associated leech assemblage.

Freshwater mussels (Unionida) are one of the most imperiled animal groups worldwide, revealing the fastest rates of extinction. Habitat degradation, river pollution and climate change are the primary causes of global decline. However, biological threats for freshwater mussels are still poorly known. Here, we describe a diverse ecological group of leeches (Hirudinea: Glossiphoniidae) inhabiting the mantle cavity of freshwater mussels. So far, examples of mussel-associated leech species are recorded from East Asia, Southeast Asia, India and Nepal, Africa, and North America. This group comprises a dozen glossiphoniid species with a hidden life style inside the mantle cavity of their hosts largely overlooked by researchers. We show that the association with freshwater mussels evolved independently in three leech clades, i.e. Batracobdelloides, Hemiclepsis, and Placobdella, at least since the Miocene. Seven mussel-associated leech species and two additional free-living taxa are described here as new to science.

An example of a possible leech-bryozoan association in freshwater.

Associations of various invertebrate species with bryozoans and sponges are a well-known marine phenomenon but such epizooic communities are far less diverse in freshwater environments. Here an occurrence of numerous leeches Alboglossiphoniacf.papillosa (Braun, 1805), in interstitial spaces between zooids of a colony of the freshwater bryozoan species Plumatellaaff.fungosa (Pallas, 1768) in Eastern Siberia is described. To the best of our knowledge, this record appears to be the first known example of a leech-bryozoan association, although such relationships deserve further research.

Species Richness, Molecular Taxonomy and Biogeography of the Radicine Pond Snails (Gastropoda: Lymnaeidae) in the Old World.

The radicine pond snails represent a species-rich and widely distributed group, many species of which are key vectors of human and animal trematodoses. Here we clarify the taxonomy, distribution and evolutionary biogeography of the radicine lymnaeids in the Old World based on the most comprehensive multi-locus molecular dataset sampled to date. We show that the subfamily Amphipepleinae is monophyletic and contains at least ten genus-level clades: Radix Montfort, 1810, Ampullaceana Servain, 1881, Peregriana Servain, 1881, Tibetoradix Bolotov, Vinarski & Aksenova gen. nov., Kamtschaticana Kruglov & Starobogatov, 1984, Orientogalba Kruglov & Starobogatov, 1985, Cerasina Kobelt, 1881, Myxas G. B. Sowerby I, 1822, Bullastra Bergh, 1901, and Austropeplea Cotton, 1942. With respect to our phylogeny, species-delimitation model and morphological data, the Old World fauna includes 35 biological species of radicines. Tibet and Eastern Europe harbor the richest faunas, while East Asia and Africa appear to be the most species-poor areas. The radicine clade could have originated near the Cretaceous - Paleocene boundary. The Miocene great lakes in Eurasia seems to be the most important evolutionary hotspots shaping spatial patterns of recent species richness. Finally, we present the first DNA barcode reference library for the reliable molecular identification of species within this group.

Climate Warming as a Possible Trigger of Keystone Mussel Population Decline in Oligotrophic Rivers at the Continental Scale.

The effects of climate change on oligotrophic rivers and their communities are almost unknown, albeit these ecosystems are the primary habitat of the critically endangered freshwater pearl mussel and its host fishes, salmonids. The distribution and abundance of pearl mussels have drastically decreased throughout Europe over the last century, particularly within the southern part of the range, but causes of this wide-scale extinction process are unclear. Here we estimate the effects of climate change on pearl mussels based on historical and recent samples from 50 rivers and 6 countries across Europe. We found that the shell convexity may be considered an indicator of the thermal effects on pearl mussel populations under warming climate because it reflects shifts in summer temperatures and is significantly different in viable and declining populations. Spatial and temporal modeling of the relationship between shell convexity and population status show that global climate change could have accelerated the population decline of pearl mussels over the last 100 years through rapidly decreasing suitable distribution areas. Simulation predicts future warming-induced range reduction, particularly in southern regions. These results highlight the importance of large-scale studies of keystone species, which can underscore the hidden effects of climate warming on freshwater ecosystems.

Ancient River Inference Explains Exceptional Oriental Freshwater Mussel Radiations.

The concept of long-lived (ancient) lakes has had a great influence on the development of evolutionary biogeography. According to this insight, a number of lakes on Earth have existed for several million years (e.g., Baikal and Tanganyika) and represent unique evolutionary hotspots with multiple intra-basin radiations. In contrast, rivers are usually considered to be variable systems, and the possibility of their long-term existence during geological epochs has never been tested. In this study, we reconstruct the history of freshwater basin interactions across continents based on the multi-locus fossil-calibrated phylogeny of freshwater mussels (Unionidae). These mussels most likely originated in Southeast and East Asia in the Jurassic, with the earliest expansions into North America and Africa (since the mid-Cretaceous) following the colonization of Europe and India (since the Paleocene). We discovered two ancient monophyletic mussel radiations (mean age ~51-55 Ma) within the paleo-Mekong catchment (i.e., the Mekong, Siam, and Malacca Straits paleo-river drainage basins). Our findings reveal that the Mekong may be considered a long-lived river that has existed throughout the entire Cenozoic epoch.

Conservation status of freshwater mussels in Europe: state of the art and future challenges.

Freshwater mussels of the Order Unionida provide important ecosystem functions and services, yet many of their populations are in decline. We comprehensively review the status of the 16 currently recognized species in Europe, collating for the first time their life-history traits, distribution, conservation status, habitat preferences, and main threats in order to suggest future management actions. In northern, central, and eastern Europe, a relatively homogeneous species composition is found in most basins. In southern Europe, despite the lower species richness, spatially restricted species make these basins a high conservation priority. Information on freshwater mussels in Europe is unevenly distributed with considerable differences in data quality and quantity among countries and species. To make conservation more effective in the future, we suggest greater international cooperation using standardized protocols and methods to monitor and manage European freshwater mussel diversity. Such an approach will not only help conserve this vulnerable group but also, through the protection of these important organisms, will offer wider benefits to freshwater ecosystems.

Multi-locus fossil-calibrated phylogeny, biogeography and a subgeneric revision of the Margaritiferidae (Mollusca: Bivalvia: Unionoida).

The taxonomy and biogeographic history of the bivalve family Margaritiferidae are controversial because previous molecular studies did not provide a well-resolved phylogenetic framework for these enigmatic freshwater mussels that have extensive but disjunct distribution in North America, Eurasia and North Africa. In this study, we present a new, fossil-calibrated phylogenetic hypothesis based on five molecular markers (∼4kb of total length) for ten species. Our results indicate that all recent margaritiferids are in the single genus, Margaritifera Schumacher, 1816. Additionally, we identified three relatively well-supported phylogenetic clades that are valid subgenera, i.e., Margaritifera s. str. (Holarctic), Margaritanopsis (=Cumberlandia) (southeast North America-southeast Asia disjunct) and Pseudunio (Mediterranean). We suggest that the crown lineage of the Margaritiferidae most likely originated in the Cretaceous (mean age 93Ma, 95% CI 66-126Ma). The combined results of ancestral area reconstructions based on the three different approaches (S-DIVA, DEC and S-DEC) showed that ancient vicariance events could have played an important role in speciation within the family. The rates of mitochondrial evolution of margaritiferids are notably slow, which may be associated with their longevity, long generation time and low metabolic rates. Our findings highlight the complex biogeographic history of the Margaritiferidae as an intermixing of ancient vicariance and dispersal events, which were most likely associated with some inland barriers, continental movements and a sea level dynamic.

First molecular identification of Australapatemon burti (Miller, 1923) (Trematoda: Digenea: Strigeidae) from an intermediate host Radix labiata (Rossmaessler) (Gastropoda: Lymnaeidae) in Europe.

The strigeid digenean species Australapatemon burti (Miller, 1923) (Trematoda: Digenea: Strigeidae) was originally described from North America, but recorded in the Neotropical region (Drago et al. 2007; Hernández-Mena et al. 2014; Blasco-Costa et al. 2016) and in Central Europe (Faltýnková et al. 2007). In Europe, this species is rare, and there is not much information about its range (Faltýnková et al. 2007; Soldánová et al. 2012). Australapatemon burti has a complex life cycle with three larval stages, two of which (sporocyst and cercaria) use several species of freshwater snails, and the third stage (metacercaria) use non-specific host hirudineans (Dubois 1968; Davies & Ostrowski de Núñez 2012; Blasco-Costa et al. 2016). Adult flukes are parasitic in the intenstines of various waterfowl species, such as ducks and swans (Drago et al. 2007; Hernández-Mena et al. 2014). Currently, the molecular data on this parasite species includes only nucleotide sequences of four adult specimens from Mexico (Hernández-Mena et al. 2014). Their hosts were Mexican duck, Anas diazi Ridgway, American Wigeon, Anas americana Gmelin, Cinnamon Teal, Anas cyanoptera Vieillot, and Ruddy Duck, Oxyura jamaicensis (Gmelin) (Anserformes: Anatidae).

Radix dolgini: The integrative taxonomic approach supports the species status of a Siberian endemic snail (Mollusca, Gastropoda, Lymnaeidae).

The molecular techniques are the standard tool for the study of the taxonomic position and phylogenetic affinities of the lymnaeid genus Radix Montfort, 1810, and the majority of the European representatives of this taxon have been studied in this respect. However, a plethora of nominal species of Radix described from Northern Asia (Siberia and the Russian Far East) are still characterized only morphologically, raising some doubts concerning their validity. In this paper, we present the triple (morphological, molecular, and zoogeographical) evidence that there is at least one endemic species of Radix, Radix dolgini (Gundrizer and Starobogatov, 1979), widely distributed in Siberia and Western Mongolia. Phylogenetically, it is a sister species to the European R. labiata (Rossmaessler, 1835) [=R. peregra auct.], and their common ancestor most probably lived in the Pliocene, nearly 3.25Myr ago. Our results assume the existence of an extended dispersal barrier for freshwater hydrobionts between Europe and Siberia in the Late Pliocene that may be important for biogeographical explanations. Three other nominal Siberian species of Radix: R. kurejkae (Gundrizer and Starobogatov, 1979), R. gundrizeri (Kruglov and Starobogatov, 1983), and R. ulaganica (Kruglov and Starobogatov, 1983) proved to be the junior synonyms of R. dolgini.

Reproduction of Pisidium casertanum (Poli, 1791) in Arctic lake.

Freshwater invertebrates are able to develop specific ecological adaptations that enable them to successfully inhabit an extreme environment. We investigated the brooding bivalve of Pisidium casertanum in Talatinskoe Lake, Vaigach Island, Arctic Russia. Here, quantitative surveys were conducted, with the collection and dissections of 765 molluscs, on the basis of which analyses on the brood sacs length (marsupia) and the number and size of embryos, were performed. In this study, the number of brooded embryos was positively correlated with the parent's shell length. The number of extramarsupial embryos was much lower than the number of intramarsupial embryos. Our research also showed that the brood sac length and embryos within one individual can vary significantly. Thus, we detected that P. casertanum has a specific brooding mechanism, accompanied by asynchronous development and embryos release by the parent. We suggest that such a mode could result in the coin-flipping effect that, presumably, increases the population breeding success in the harsh environment of the Arctic lake.