Manuel Lopes-Lima

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.

Biology and conservation of freshwater bivalves: past, present and future perspectives

Freshwater bivalves have been highly threatened by human activities, and recently their global decline has been causing conservational and social concern. In this paper, we review the most important research events in freshwater bivalve biology calling attention to the main scientific achievements. A great bias exists in the research effort, with much more information available for bivalve species belonging to the Unionida in comparison to other groups. The same is true for the origin of these studies, since the publishing pattern does not always correspond to the hotspots of biodiversity but is concentrated in the northern hemisphere mainly in North America, Europe and Russia, with regions such as Africa and Southeast Asia being quite understudied. We also summarize information about past, present and future perspectives concerning the most important research topics that include taxonomy, systematics, anatomy, physiology, ecology and conservation of freshwater bivalves. Finally, we introduce the articles published in this Hydrobiologia special issue related with the International Meeting on Biology and Conservation of Freshwater Bivalves held in 2012 in Bragança, Portugal.

Impacts of climate change and land-use scenarios on Margaritifera margaritifera, an environmental indicator and endangered species

In this study, we assess the impacts of future climate and land-use in the Beça River (northern Portugal) under different scenarios and how this will translate into the conservation status of the endangered pearl mussel Margaritifera margaritifera (Linnaeus, 1758). This species is currently present in several stretches of the Beça River that still hold adequate ecological conditions. However, the species is threatened by projected declines in precipitation for the 21st century, with implication on the river flows and water depths that might decrease below the species requisites. This situation could be especially critical during summer conditions since the ecological flows may not be assured and several river stretches may be converted into stagnant isolated pools. The habitat connectivity will also be affected with reverberating effects on the mobility of Salmo trutta, the host of M. margaritifera, with consequences in the reproduction and recruitment of pearl mussels. In addition, human-related threats mostly associated with the presence of dams and an predicted increases in wildfires in the future. While the presence of dams may decrease even further the connectivity and river flow, with wildfires the major threat will be related to the wash out of burned areas during storms, eventually causing the disappearance of the mussels, especially the juveniles. In view of future climate and land-use change scenarios, conservation strategies are proposed, including the negotiation of ecological flows with the dam promoters, the replanting of riparian vegetation along the water course and the reintroduction of native tree species throughout the catchment.

Phylogeny of the most species-rich freshwater bivalve family (Bivalvia: Unionida: Unionidae): Defining modern subfamilies and tribes

Freshwater mussels of the order Unionida are key elements of freshwater habitats and are responsible for important ecological functions and services. Unfortunately, these bivalves are among the most threatened freshwater taxa in the world. However, conservation planning and management are hindered by taxonomic problems and a lack of detailed ecological data. This highlights the urgent need for advances in the areas of systematics and evolutionary relationships within the Unionida. This study presents the most comprehensive phylogeny to date of the larger Unionida family, i.e., the Unionidae. The phylogeny is based on a combined dataset of 1032bp (COI+28S) of 70 species in 46 genera, with 7 of this genera being sequenced for the first time. The resulting phylogeny divided the Unionidae into 6 supported subfamilies and 18 tribes, three of which are here named for the first time (i.e., Chamberlainiini nomen novum, Cristariini nomen novum and Lanceolariini nomen novum). Molecular analyses were complemented by investigations of selected morphological, anatomical and behavioral characters used in traditional phylogenetic studies. No single morphological, anatomical or behavioral character was diagnostic at the subfamily level and few were useful at the tribe level. However, within subfamilies, many tribes can be recognized based on a subset of these characters. The geographical distribution of each of the subfamilies and tribes is also presented. The present study provides important advances in the systematics of these extraordinary taxa with implications for future ecological and conservation studies.

Factors driving changes in freshwater mussel (Bivalvia, Unionida) diversity and distribution in Peninsular Malaysia.

Freshwater mussels (Bivalvia, Unionida) fulfil important ecosystem functions and are one of the most threatened freshwater taxa globally. Knowledge of freshwater mussel diversity, distribution and ecology in Peninsular Malaysia is extremely poor, and the conservation status of half of the species presumed to occur in the region has yet to be assessed. We conducted the first comprehensive assessment of Peninsular Malaysias freshwater mussels based on species presence/absence and environmental data collected from 155 sites spanning all major river catchments and diverse habitat types. Through an integrative morphological-molecular approach we recognised nine native and one widespread non-native species, i.e. Sinanodonta woodiana. Two species, i.e. Pilsbryoconcha compressa and Pseudodon cambodjensis, had not been previously recorded from Malaysia, which is likely a result of morphological misidentifications of historical records. Due to their restriction to single river catchments and declining distributions, Hyriopsis bialata, possibly endemic to Peninsular Malaysia, Ensidens ingallsianus, possibly already extinct in the peninsula, and Rectidens sumatrensis, particularly require conservation attention. Equally, the Pahang, the Perak and the north-western river catchments are of particular conservation value due to the presence of a globally unique freshwater mussel fauna. Statistical relationships of 15 water quality parameters and mussel presence/absence identified acidification and nutrient pollution (eutrophication) as the most important anthropogenic factors threatening freshwater mussel diversity in Peninsular Malaysia. These factors can be linked to atmospheric pollution, deforestation, oil-palm plantations and a lack of functioning waste water treatment, and could be mitigated by establishing riparian buffers and improving waste water treatment for rivers running through agricultural and residential land.

Diversity, biogeography and conservation of freshwater mussels (Bivalvia: Unionida) in East and Southeast Asia

Recent research efforts have significantly advanced our knowledge on Asian freshwater mussel (Bivalvia: Unionida) diversity and distribution. Here we provide a modern consensus of the diversity, biogeography and conservation of Unionida in the region comprising East and Southeast Asia (excluding Wallacea) and Asian Russia. A data review confirmed the presence of 228 native and 3 non-native Unionida (98% Unionidae, 2% Margaritiferidae), rendering the region a global hotspot of freshwater mussel diversity. Species richness was highest in China (particularly Yangtze basin) in absolute numbers and Cambodia when correcting for country area, and decreased gradually towards the south and steeply towards the north and east. Six of the seven unionid subfamilies are native to the region, with species richness peaking in Southeast Asia for Rectidentinae, Gonideinae, Parreysiinae and Modellnaiinae, China for Anodontinae and Unioninae, and Asian Russia for Margaritiferidae. Conservation status and data collected after 1980 were not available for 61 and 24% of species, respectively. Dams, deforestation and pollution are likely the major threats to mussels in the region, though data in this respect are scarce. The Philippines, Laos, Indonesia, Myanmar and Malaysia are among the countries with the poorest data availability and urgently require research.

Effects of Cd2+ on the calcium metabolism and shell mineralization of bivalve Anodonta cygnea

The survival of freshwater mussels is affected by cadmium ions because they accumulate in tissues and fluids and displace calcium ions in transport and regulation mechanisms. A preliminary study of the freshwater bivalve Anodonta cygnea under enriched Ca2+ (2 mM) water for different periods (3, 4, and 18 days), showed significant increase in calcium levels (p < 0.05) in the ventricular fluid with concentration proportional to time of exposure. Groups of A. cygnea were then exposed to different treatments for 4 days: Group 1 to Ca2+ (2 mM) enriched water as a control; Group 2 to a sub-lethal concentration (10−6 M) of Cd2+; Group 3 to an injection of vitamin D (1340 IU mL−1); Group 4 to an injection of SEA0400 (950 µg mL−1), a sodium/calcium exchanger (NCX) inhibitor. Fluid samples from different compartments of the animals were analyzed for Ca2+ and Cd2+ composition as well as for other ions relevant to the osmoregulation (Na+, Mg2+, K+, and Cl−) and their osmolarity. The treatment groups had significantly higher calcium concentrations in their ventricular fluid (p < 0.05) under Cd2+ and vitamin D, also in pericardium fluid under Cd2+, vitamin D, and SEA0400. We infer a specific transport mechanism from the intestinal to the ventricular fluid that may be induced by vitamin D. A general internal acidosis by Cd2+, releasing calcium from the calcareous concretions and a specific inhibition of calcium resorption, by the SEA0400, from the pericardium towards the ventricle is discussed. Cd2+ incubation significantly augmented (p < 0.05) the cadmium contents of all experimental fluids and tissues. Scanning electron microscope (SEM) imaging of the border regions of the shell showed clear ultrastructural changes in respone to Cd2+ incubation, suggesting a direct influence of this ion on the shell biomineralization mechanisms.

Microstructural characterization of inner shell layers in the freshwater bivalve Anodonta cygnea.

ABSTRACT The shell microstructure of freshwater bivalve Anodonta cygnea was observed from the ventral margin toward the intrapallial regions by scanning electronic microscopy during the spring/summer period. The three main structures—the periostracum, prismatic, and nacreous layers—were visualized in a sequential path from the ventral margin toward the intrapallial regions. Although with always the same calcium carbonate polymorph (aragonite), A. cygnea presented composites of aragonite crystals embedded within an organic matrix displaying varied morphologies and structural arrangements. The prisms of the prismatic shell layer are composed of single-crystal fibers radiating from spheruliths, whereas in the nacreous layer the structure is similar to that of a brick wall, with tablets in each layer offset with respect to those in the layers above and below them. From the shell ventral margin, the last nacreous lamina formed exhibit crystals with rounded forms, followed by rhombic and hexagonal shapes toward the interior with irregular microstructure. There are gradual intermediate forms between these distinct shapes. This study offers a description of the inner calcareous mineralized layers of A. cygnea and will be useful for future comparative studies in several research areas such as phylogenetic evolution, ecotoxicology, and the influence of environmental and physicochemical factors on the shell formation process in freshwater bivalves.

The male and female complete mitochondrial genome sequences of the Endangered freshwater mussel Potomida littoralis (Cuvier, 1798) (Bivalvia: Unionidae)

Abstract Freshwater mussels of the family Unionidae exhibit a particular form of mitochondria inheritance called double uniparental inheritance (DUI), in which the mitochondria are inherited by both male and female parents. The (M)ale and (F)emale mitogenomes are highly divergent within species. In the present study, we determine and describe the complete M and F mitogenomes of the Endangered freshwater mussel Potomida littoralis (Cuvier, 1798). The complete M and F mitogenomes sequences are 16 451 bp and 15 787 bp in length, respectively. Both F and M have the same gene content: 13 protein-coding genes (PCGs), 22 transfer RNA (trn) and 2 ribosomal RNA (rrn) genes. Bayesian analyses based on the concatenated nucleotide sequences of 12 PCGs and 2 rrn genes of both genomes, including mitogenome sequences available from related species, were performed. Male and Female lineages are monophyletic within the family, but reveal distinct phylogenetic relationships.

Reproductive Cycle and Strategy of Anodonta anatina (L., 1758): Notes on Hermaphroditism

Freshwater mussels have decreased dramatically in Iberia over the last decades. These animals are responsible for important ecosystem services such as recycling nutrients and improving water clarity. Under this view a better knowledge on the biological features of these animals is extremely important for future conservation and management actions. In this study the reproductive and gametogenic cycle of Anodonta anatina were studied during 2 years in one population as well as the sex ratio and hermaphroditism in six distinct populations, using standard histology. Gametogenesis was continuous in both sexes and germinal epithelium in early stages of development. Gametes were present throughout the reproductive cycle. Oogenesis and spermatogenesis occurred mainly between January and May. Larvae brooding occurred between September and March and main glochidia discharge occurred over a short period (2-3 weeks) in March. For the sex-ratio and hermaphroditism assessments a variable number of individuals were collected from several populations from lakes and rivers. Previous studies described A. anatina as mainly dioecious with only a few populations presenting occasional hermaphroditism. However, the present study indicates that A. anatina sexual behavior is influenced by environmental conditions, being mainly dioecious in rivers with increased hermaphroditism in standing waters. Although self-fertilization was not confirmed, additional studies with molecular characterization of larvae using fast evolving markers should be used in future studies to enlighten this process. Overall, this study indicates that for more efficient conservation actions and management plans, freshwater mussel reproductive biology should be studied at the population level mainly in the subfamily Anodontinae.