Using a multi‐model ensemble approach to determine biodiversity hotspots with limited occurrence data in understudied areas: An example using freshwater mussels in México

Species distribution models (SDMs) are an increasingly important tool for conservation particularly for difficult‐to‐study locations and with understudied fauna. Our aims were to (1) use SDMs and ensemble SDMs to predict the distribution of freshwater mussels in the Pánuco River Basin in Central México; (2) determine habitat factors shaping freshwater mussel occurrence; and (3) use predicted occupancy across a range of taxa to identify freshwater mussel biodiversity hotspots to guide conservation and management. In the Pánuco River Basin, we modeled the distributions of 11 freshwater mussel species using an ensemble approach, wherein multiple SDM methodologies were combined to create a single ensemble map of predicted occupancy. A total of 621 species‐specific observations at 87 sites were used to create species‐specific ensembles. These predictive species ensembles were then combined to create local diversity hotspot maps. Precipitation during the warmest quarter, elevation, and mean temperature were consistently the most important discriminatory environmental variables among species, whereas land use had limited influence across all taxa. To the best of our knowledge, our study is the first freshwater mussel‐focused research to use an ensemble approach to determine species distribution and predict biodiversity hotspots. Our study can be used to guide not only current conservation efforts but also prioritize areas for future conservation and study.     

Effects of dams and their environmental impacts on the genetic diversity and connectivity of freshwater mussel populations in Poyang Lake Basin,China

1. Habitat fragmentation is one of the main threats to biodiversity. Barriers to dispersal caused by anthropogenic habitat alteration may affect phylogeographic patterns in freshwater mussels. Knowledge of the phylogenetic and phylogeographic patterns of unionoids is vital to inform protection of their biodiversity.
2. Here, we assessed influences of dams and their environmental effects on the genetic diversity and population connectivity of a broadly distributed freshwater mussel, Nodularia douglasiae, in Poyang Lake Basin.
3. The results showed high genetic diversity in areas without dams and low genetic diversity in areas with dams. High genetic differentiation and low gene flow were found among the 11 populations. Genetic variation was significantly correlated with dissolved oxygen levels.
4. The observation of low genetic diversity in populations separated by dams indicated that those populations were subjected to genetic erosion and demographic decline because they are disconnected from other populations with higher diversity. High genetic differentiation and low gene flow among the 11 populations could be correlated with anthropogenic habitat alteration.
5. These results indicated that anthropogenic habitat alterations have led to the decline in freshwater mussel diversity. Therefore, we recommend maintaining favourable habitat conditions and connectivity of rivers or lakes, and strengthening study of life histories with host-test experiments to identify potential host fish species to strengthen the knowledge base underpinning freshwater mussel conservation.

     

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.     

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.     

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.     

The effects of flow and stream characteristics on the variation in freshwater mussel growth in a Southeast US river basin

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Do hotspots fall within protected areas? A Geographic Approach to Planning analysis of regional freshwater biodiversity

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Imperiled freshwater mussels in drainage channels associated with rare agricultural landscape and diverse fish communities

Identification of landscape structures that predict the distribution of aquatic organisms has the potential to provide a practical management tool for species conservation in agricultural drainage channels. We tested the hypothesis that sites with imperiled freshwater mussels have distinct rural landscape structures and are characterized by the presence of diverse fish communities. In central Japan, the proportion of developed land use in surrounding areas was compared among sites with mussel populations (mussel sites) and randomly chosen sites (random sites) across multiple spatial scales (with a radius ranging from 100 to 3,000 m). Mussel sites were characterized by a much lower proportion of developed land (mean 5–18 %) compared with random sites (mean 32–35 %) at a scale of ≤300 m. The areas that met the landscape criteria for mussel sites across multiple scales constituted only 0.23 % of the area that was presumed to have suitable slope and elevation as a mussel habitat. Landscape metrics derived from mussel sites to locate unknown populations had a low predictability (16.7 %). Sites with mussels were located close to each other and had fish communities with higher taxonomic diversity than in sites without mussels. In addition, mussel taxonomic richness was a good predictor of fish community diversity. The quantitative measures of landscape structure may serve as a useful tool when prioritizing or identifying areas for conservation of mussels and fish if spatially autocorrelated distribution of habitat and other critical environmental factors such as habitat connectivity are also considered.     

BIODIVERSITY PATTERN AND CONSERVATION OF AQUATIC VASCULAR PLANTS IN THE YANGTZE RIVER BASIN,CHINA北大核心CSCD

The Yangtze River is the largest river in China. It is a priority conservation area for biodiversity of the world, with its main river, branches and wetlands. As an essential part of freshwater ecosystem, aquatic vegetation has been well studied by Chinese researchers since 1950s, but large-scaled analysis on the biodiversity pattern is lacked. Based on published studies, we analyzed spatial and temporal pattern of aquatic plant diversity in the Yangtze River Basin, and calculated the suitable habitat area and underlying influence of environmental factors using MaxEnt software. A total of 298 species are recognized, belonging to 121 genera in 52 families, which is 57.6% of the total aquatic vascular plants in China. The Yangtze River Basin is the key area for aquatic plant diversity of China, especially the subregions of middle reaches. The elevation and land use are the key environmental variables to the spatial pattern of aquatic plants. The separation among water systems have weak influence on the spatial pattern of diversity in aquatic vascular plants, but potamo-lacustrine habitats facilitated the species homogenization of the flora in a sub-basin scale. The network consists of Poyang Lake, Dongting Lake, Tai Lake, and the middle and lower mainstream is the suitable area for the aquatic plants based on the MaxEnt model. In the past half century, the decline or loss of aquatic vegetation occurred in plenty of lakes in the Yangtze River Basin. We suggested that the protection of aquatic vegetation should be incorporated into the integrated conservation of the middle and lower Yangtze River. © 2019, Institute of Hydrobiology, Chinese Academy of Sciences. All rights reserved.     

Species traits and catchment‐scale habitat factors influence the occurrence of freshwater mussel populations and assemblages

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Freshwater mussel (Mollusca: Bivalvia: Unionoida) richness and endemism in the ecoregions of Africa and Madagascar based on comprehensive museum sampling

The objective of this study was to assess freshwater mussel (Mollusca: Bivalvia: Unionoida) species distributions among the freshwater ecoregions of Africa and Madagascar to discover areas of high richness and endemism. These are among the top criteria for identifying biodiversity hotspots and establishing conservation priorities. Distributions were determined from museum specimens in 17 collections. In total, 5,612 records for 87 unionoid species could each be assigned to one of 90 freshwater ecoregions. The majority of species (55%) are known from only one (34 spp.) or two (14) ecoregions. Only three are known from more than 20 ecoregions: Etheria elliptica (38 ecoregions), Chambardia wahlbergi (25), and Mutela rostrata (21). The most species-rich ecoregions are Lake Victoria Basin (17 spp.), Upper Nile (16), Upper Congo (14), Senegal–Gambia (13), and Sudanic Congo–Oubangi (13). Those with the most endemic species are Lake Tanganyika (8 spp.), Lake Victoria Basin (6), Bangweulu–Mweru (4), and Lake Malawi (3). Twenty-five ecoregions have no known freshwater mussels. These patterns are significantly correlated with fish and general freshwater mollusk richness. Unionoid richness also varies significantly among major habitat types. These patterns are relevant to biogeography and conservation and indicate areas in need of further research. We argue that freshwater mussels are valuable as focal species for conservation assessments, and they themselves merit management consideration for their ecosystem functions and distributions in imperiled habitats. It is recommended that field surveys be conducted to determine the current status of species in all areas of Africa and Madagascar.     

Impending extinctions of North American freshwater mussels (Unionoida) following the zebra mussel (Dreissena polymorpha) invasion

1. Freshwater mussels (Order Unionoida) are the most imperiled faunal group in North America; 60% of described species are considered endangered or threatened, and 12% are presumed extinct. Widespread habitat degradation (including pollution, siltation, river channelization and impoundment) has been the primary cause of extinction during this century, but a new stress was added in the last decade by the introduction of the Eurasian zebra mussel, Dreissena polymorpha , a biofouling organism that smothers the shells of other molluscs and competes with other suspension feeders for food. Since the early 1990s, it has been spreading throughout the Mississippi River basin, which contains the largest number of endemic freshwater mussels in the world. In this report, we use an exponential decay model based on data from other invaded habitats to predict the long-term impact of D. polymorpha on mussel species richness in the basin.
2. In North American lakes and rivers that support high densities (>3000 m⁻²) of D. polymorpha , native mussel populations are extirpated within 4–8 years following invasion. Significant local declines in native mussel populations in the Illinois and Ohio rivers, concomitant with the establishment of dense populations of D. polymorpha , suggest that induced mortality is occurring in the Mississippi River basin.
3. A comparison of species loss at various sites before and after invasion indicates that D. polymorpha has accelerated regional extinction rates of North American freshwater mussels by 10-fold. If this trend persists, the regional extinction rate for Mississippi basin species will be 12% per decade. Over 60 endemic mussels in the Mississippi River basin are threatened with global extinction by the combined impacts of the D. polymorpha invasion and environmental degradation.     

Extensive allozyme monomorphism in a threatened species of freshwater mussel, Margaritifera hembeli Conrad (Bivalvia: Margaritiferidae)

A threatened but under-studied component offreshwater biodiversity in North America is thenative freshwater mussels (Bivalvia:Unionoidea: Margaritiferidae and Unionidae). Genetic data suggest that these mussel speciesgenerally exhibit levels of variability similarto other invertebrates. We surveyed allozymevariation in the Louisiana Pearlshell, Margaritifera hembeli (Margaritiferidae), athreatened freshwater mussel. Five examinedpopulations are monomorphic for 25 allozymeloci, the first report of a native freshwatermussel species with extensive allozymemonomorphism. Low genetic diversity appears tobe characteristic of margaritiferids, as anANOVA indicated that mussels of the familyMargaritiferidae have significantly lowerlevels of heterozygosity than the mussels ofthe family Unionidae. Margaritiferids havestrong habitat preferences and modification ofhabitat leads to rapid loss of populations.Although bottlenecks are known to cause lowgenetic variability, margaritiferids mayexhibit meta-population structure withextinction/re-colonization dynamics leading tolow genetic variability. Margaritiferidsgenerally exhibit a patchy distribution with acolonization rate that is approximately twicethat of extinction. Tests of themetapopulation hypothesis will requireadditional allozyme population genetic data aswell as hypervariable microsatellite loci.     

Evaluating the influence of land use,drought and reach isolation on the occurrence of freshwater mussel species in the lower Flint River Basin,Georgia (U.S.A.)

1. North American freshwater mussels have been subjected to multiple stressors in recent decades that have contributed to declines in the status and distribution of many species. However, considerable uncertainty exists regarding the relative influence of these factors on observed population declines. 2. We used an occupancy modelling approach to quantify relationships between mussel species occurrence and various site‐ and catchment‐level factors, including land cover, stream size, the occurrence of drought and reach isolation due to impoundment for 21 mussel species native to the lower Flint River Basin, Georgia, U.S.A. 3. Our modelling approach accounted for potential biases associated with both incomplete detection and misidentification of species, which are frequently not accommodated as sources of bias in freshwater mussel studies. 4. Modelling results suggested that mussel species were, on average, four times less likely to be present following severe drought, but the negative effects of drought declined rapidly with increasing stream size. Similarly, mussel species were 15 times less likely to occupy small streams that were isolated from mainstem tributaries by impoundments. 5. This study provides insight into the effects of natural and anthropogenic factors on freshwater mussel species. Our findings add to a growing body of literature aimed at improving understanding of the predominant factors influencing freshwater mussel populations and fostering the development of more informed and effective conservation strategies.     

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.     

Spatio-temporal patterns of the decline of freshwater mussels in the Little South Fork Cumberland River,USA

The Little South Fork Cumberland River, Kentucky and Tennessee, USA, was a globally important conservation refugium for freshwater mussels (Mollusca: Unionidae) because it supported an intact example (26 species) of the unique Cumberland River mussel fauna including imperiled species. We used previous surveys and our 1997–1998 survey to reconstruct the historical fauna, to describe spatio-temporal patterns of density and number of species, and to evaluate the probable sequence and cause of observed mussel declines. We were specifically interested in better understanding how mussel assemblages respond to chronic disturbances, and how these changes manifest in persistence patterns. Density and numbers of species declined steadily from 1981 to 1998, but declines occurred first in the lower river (early 1980s), followed by declines in the upper river (late 1980s to early 1990s). Of the total species recorded from the Little South Fork, 17 (65%) are seemingly extirpated and five others appear near extirpation. Declines are associated with at least two, temporally distinct major insults. Lower river declines are associated with surface mining, whereas, oil extraction activities are implicated in upper river declines. Regardless of causal factors, species persistence was primarily a function of predecline population size with only the most numerous and widespread species surviving. At this time, the river appears lost as a conservation refugium for mussels despite its remoteness, predominantly forested watershed, and several layers of existing statutory and regulatory environmental safeguards. We suggest that the river could be restored and mussels reintroduced if an interagency task force is formed to identify and mitigate specific stressors now affecting most mussel species in the river.Nomenclature: Turgeon et al. (1998).     

Population structure and gene flow in the Sheepnose mussel (Plethobasus cyphyus) and their implications for conservation

North American freshwater mussel species have experienced substantial range fragmentation and population reductions. These impacts have the potential to reduce genetic connectivity among populations and increase the risk of losing genetic diversity. Thirteen microsatellite loci and an 883 bp fragment of the mitochondrial ND1 gene were used to assess genetic diversity, population structure, contemporary migration rates, and population size changes across the range of the Sheepnose mussel (Plethobasus cyphyus). Population structure analyses reveal five populations, three in the Upper Mississippi River Basin and two in the Ohio River Basin. Sampling locations exhibit a high degree of genetic diversity and contemporary migration estimates indicate that migration within river basins is occurring, although at low rates, but there is no migration is occurring between the Ohio and Mississippi river basins. No evidence of bottlenecks was detected, and almost all locations exhibited the signature of population expansion. Our results indicate that although anthropogenic activity has altered the landscape across the range of the Sheepnose, these activities have yet to be reflected in losses of genetic diversity. Efforts to conserve Sheepnose populations should focus on maintaining existing habitats and fostering genetic connectivity between extant demes to conserve remaining genetic diversity for future viable populations.     

Population genetics of the freshwater mussel, <Emphasis Type="Italic">Amblema plicata</Emphasis> (Say 1817) (Bivalvia: Unionidae): Evidence of high dispersal and post-glacial colonization

Over 70% of North American freshwater mussel species (families Unionidae and Margaritiferidae) are listed as threatened or endangered. Knowledge of the genetic structure of target species is essential for the development of effective conservation plans. Because Ambelma plicata is a common species, its population genetic structure is likely to be relatively intact, making it a logical model species for investigations of freshwater mussel population genetics. Using mtDNA and allozymes, we determined the genotypes of 170+ individuals in each of three distinct drainages: Lake Erie, Ohio River, and the Lower Mississippi River. Overall, within-population variation increased significantly from north to south, with unique haplotypes and allele frequencies in the Kiamichi River (Lower Mississippi River drainage). Genetic diversity was relatively low in the Strawberry River (Lower Mississippi River drainage), and in the Lake Erie drainage. We calculated significant among-population structure using both molecular markers (A.p. Φ_st = 0.15, θ_st = 0.12). Using a hierarchical approach, we found low genetic structure among rivers and drainages separated by large geographic distances, indicating high effective population size and/or highly vagile fish hosts for this species. Genetic structure in the Lake Erie drainage was similar to that in the Ohio River, and indicates that northern populations were founded from at least two glacial refugia following the Pleistocene. Conservation of genetic diversity in Amblema plicata and other mussel species with similar genetic structure should focus on protection of a number of individual populations, especially those in southern rivers.     

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.     

Genetic distinctiveness of Ligumia recta, the black sandshell, in the Mobile River Basin and implications for its conservation

North America’s freshwater mussels are widely regarded as one of the most diverse and imperiled groups on earth, and many of the continent’s ~ 300 Unionidae and Margaratiferidae are drainage or regional endemics. Although Ligumia recta is currently widespread and stable in the Mississippi Basin, recent surveys suggest it is extirpated from the Pearl River drainage and only small populations persist in isolated Mobile River Basin tributaries. We compared 504 base pairs of the cytochrome c oxidase 1 mitochondrial gene from two Mobile Basin L. recta specimens and found that the Mobile Basin appears to support an evolutionarily significant genotype that could warrant recognition as a cryptic and highly imperiled taxon. Genetic data are beginning to reveal the extent and magnitude of recent biodiversity losses in the southeastern US, and moreover, these data will be critical to tailoring conservation and management strategies.