Unio Mancus Research Articles

Captive breeding of European freshwater mussels as a conservation tool: A review

Abstract Freshwater mussels are declining throughout their range. Their important ecological functions along with insufficient levels of natural recruitment have prompted captive breeding for population augmentation and questions about the usefulness and applicability of such measures. This article reviews the current state of captive breeding and rearing programmes for freshwater mussels in Europe. It considers the various species, strategies, and techniques of propagation, as well as the different levels of effort required according to rearing method, highlighting the key factors of success. Within the last 30 years, 46 breeding activities in 16 European countries have been reported, mainly of Margaritifera margaritifera and Unio crassus. Some facilities propagate species that are in a very critical situation, such as Pseudunio auricularius, Unio mancus, and Unio ravoisieri, or multiple species concurrently. In some streams, the number of released captive‐bred mussels already exceeds the size of the remaining natural population. Rearing efforts range from highly intensive laboratory incubation to lower intensity methods using in‐river mussel cages or silos. Most breeding efforts are funded by national and EU LIFE(+) grants, are well documented, and consider the genetic integrity of the propagated mussels. Limited long‐term funding perspectives, the availability of experienced staff, water quality, and feeding/survival during early life stages are seen as the most important challenges. Successful captive breeding programmes need to be combined with restoration of the habitats into which the mussels are released. This work will benefit from an evidence‐based approach, knowledge exchange among facilities, and an overall breeding strategy comprising multiple countries and conservation units.

Microplastic intake of Unio mancus Lamarck 1819 collected from Ataturk Dam Lake, Türkiye

Microplastic intake of Unio mancus Lamarck 1819 collected from Ataturk Dam Lake, Türkiye

Streams in the Mediterranean Region are not for mussels: Predicting extinctions and range contractions under future climate change

Climate change is becoming the leading driver of biodiversity loss. The Mediterranean region, particularly southwestern Europe, is already confronting the consequences of ongoing global warming. Unprecedented biodiversity declines have been recorded, particularly within freshwater ecosystems. Freshwater mussels contribute to essential ecosystem services but are among the most threatened faunal groups on Earth. Their poor conservation status is related to the dependence on fish hosts to complete the life cycle, which also makes them particularly vulnerable to climate change. Species Distribution Models (SDMs) are commonly used to predict species distributions, but often disregard the potential effect of biotic interactions. This study investigated the potential impact of future climate on the distribution of freshwater mussel species while considering their obligatory interaction with fish hosts. Specifically, ensemble models were used to forecast the current and future distribution of six mussel species in the Iberian Peninsula, including environmental conditions and the distribution of fish hosts as predictors. We found that climate change is expected to severely impact the future distribution of Iberian mussels. Species with narrow ranges, namely Margaritifera margaritifera and Unio tumidiformis, were predicted to have their suitable habitats nearly lost and could potentially be facing regional and global extinctions, respectively. Anodonta anatina, Potomida littoralis, and particularly Unio delphinus and Unio mancus, are expected to suffer distributional losses but may gain new suitable habitats. A shift in their distribution to new suitable areas is only possible if fish hosts are able to disperse while carrying larvae. We also found that including the distribution of fish hosts in the mussels' models avoided the underprediction of habitat loss under climate change. This study warns of the imminent loss of mussel species and populations and the urgent need of management actions to reverse current trends and mitigate irreversible damage to species and ecosystems in Mediterranean regions.

Collapse of native freshwater mussel populations: Prospects of a long-term study

Freshwater biodiversity is under threat, but long-term quantitative studies showing major demographic declines in invertebrate species are still scarce. Here we focus on a long-term study (2004 to 2019) using four native freshwater mussel species (Order Unionida) colonizing two canals of the Ebro River (Spain). Special attention was given to Pseudunio auricularius (Spengler, 1793), a critically endangered species. Generalized linear mixed models results showed significant temporal effects on mussel densities, with a continuous decline in all species present, being Anodonta anatina, Potomida littoralis and Unio mancus now considered locally extinct. Pseudunio auricularius is still present in the studied canals, but at very low densities (0.01 ind/m2). Capture-recapture data on P. auricularius show a progressive decline in its survival probability, down to 0.15 in 2020 in the Canal Imperial de Aragón, although in the Canal de Tauste it remains close to 1. Based on these results, we discuss several hypotheses that may explain this rapid collapse of unionid populations. Given the precarious conservation status of freshwater mussels in both canals, effective management measures should be urgently applied, including habitat restoration and captive breeding.

Potential utilization of mussel meals as an alternative fish feed raw material for aquaculture

Increasing the target of aquaculture production will increase the need for feed which an increase will follow in the need for fish meal. The constraint in aquaculture fish feed dependence on a fish meal import is known. In efforts to find local raw materials to reduce dependence on fish meals, one source of quality animal protein from marine resources as raw material for feed that needs to be studied and developed is mollusks or mussels. This review summarizes the use of mussel meal in aquaculture feed and is expected to provide a comprehensive overview of the existing studies’ potential on mussels meal used as a feed ingredient in fish feed. Many species of mussel have been tested for raw material in fish feed such as blue mussel (Mytilus galloprovincialis), Freshwater mussels (Anodonta anatina & Unio mancus), Mytilus edulis L and Green mussel (Perna viridis). Mussels contain high levels of nutrients and bio-actives which were utilized in the form of mussel meals for feed ingredients. The constraint mussels have high heavy metals such as Pb, Hg and Pb. The utilization of mussel meals as a source of protein feed could increase the growth of several types of cultured fish. One alternative used organic acid as a feed additive to reduce toxicity of heavy metals in fish. The conclusion is that mussel meals have the potential as raw material and an alternative protein source to reduce dependence on a fish meal in aquaculture fish feed.

The gill transcriptome of threatened European freshwater mussels

Genomic tools applied to non-model organisms are critical to design successful conservation strategies of particularly threatened groups. Freshwater mussels of the Unionida order are among the most vulnerable taxa and yet almost no genetic resources are available. Here, we present the gill transcriptomes of five European freshwater mussels with high conservation concern: Margaritifera margaritifera, Unio crassus, Unio pictorum, Unio mancus and Unio delphinus. The final assemblies, with N50 values ranging from 1069–1895 bp and total BUSCO scores above 90% (Eukaryote and Metazoan databases), were structurally and functionally annotated, and made available. The transcriptomes here produced represent a valuable resource for future studies on these species’ biology and ultimately guide their conservation.

Clearance and persistence of Escherichia coli in the freshwater mussel Unio mancus

The excessive use of antibiotics has led to the emergence of resistant bacteria, mainly from the Enterobacterales group, with high pathogenic/zoonotic potentials that can lead to problems in public health. The increasing presence in freshwater ecosystems highlights the need to evaluate potential sentinel species as risk indicators for both ecosystem and human health. The freshwater mussels provide several ecosystem services, may represent potential sentinel species due to their ability to filter water and retain both organic and inorganic particles. We tested the capability of U. mancus to retain Escherichia coli as a model bacterial organism. Under experimental conditions, the mussels could clear suspended E. coli, facilitating its rapid elimination from water within the first 24 h after exposure. The species also presented a maximum retention time of 4 days. We also provide allometric equations correlating the filtering capacity with the length and the weight of mussel body parts often used in biometric studies. We provide a first assessment of the potential of the bivalve Unio mancus to act as a sentinel species for the detection of Enterobacterales and demonstrate the ability to act as a water cleaner.

New phylogenetic insights on some species of Unionidae from Switzerland (Bivalvia, Palaeoheterodonta, Unionidae)

Switzerland’s drainage systems are divided into three major European river basins, i.e. the Po, the Rhône, and the Rhine basins. Until recently 32 species of freshwater mussel species (i.e. belonging to the genera Anodonta and Unio) were recognized for the country, albeit their identity and number remain uncertain especially, given the recent recognition of Unio mancus Lamarck, 1819 from the Rhône in France, and Unio elongatulus C. Pfeiffer, 1825 and Anodonta exulcerata Porro, 1838 from the Po basin in Italy. In this study, we molecularly assess Swiss populations of freshwater mussels to understand the identity and number of species as well as to characterize their distributions within this geologically differentiated Alpine country. We collected 125 specimens in 42 lakes and rivers representing the three major basins and performed a phylogenetic investigation of the collected specimens using two mitochondrial markers (COI & 16S) and one nuclear marker (28S). COI Haplotype networks are then presented for the identified species. Our new findings show that Unio elongatulus inhabits water bodies north of the main Alpine arc. No living populations of Unio mancus could be detected in Switzerland. Anodonta exulcerata is recorded from two localities north of Lake Maggiore and in the Swiss part of Lake Lugano. Anodonta anatina (Linnaeus, 1758) shows genetic differences between southern alpine and northern alpine populations. Our genetic data from Swiss populations of unionid species provides new records and knowledge concerning freshwater mussels from Central Europe and specifically from the Alpine region.

Oxidative stress response as biomarker of exposure of a freshwater invertebrate model organism (Unio mancus Lamarck, 1819) to antifouling copper pyrithione

Sublethal effects of copper pyrithione (CuPT) on an invertebrate model organism, freshwater mussel (Unio mancus), were assessed using oxidative stress parameters and histopathology. The environmentally relevant concentration of 5 ?g/l copper pyrithione was applied as a 96 h semi-static exposure. MDA levels in digestive gland (DG) significantly increased, compared to a control group (p < 0.001). Gill MDA levels also increased, but not significantly (p > 0.05). GSH level in DG increased significantly (p < 0.05), and gill tissue levels also increased but not significantly (p > 0.05). Levels of SOD, GPx activities, and AOPP levels did not change significantly (p > 0.05). The most prominent histopathological alterations in the gills were haemocyte infiltration, lipofuscin aggregates and lamellar deformations with tubule degeneration and accumulated lipofuscin aggregates in DG tubules. CuPT impacts antioxidant defense systems even during sublethal exposure of Unio mancus as the freshwater model organism.

Investigation of toxic effects of fungicide tebuconazole on freshwater mussels (Unio mancus) with multiple biomarkers

Triazol fungusitler, geniş spektrumlu, steroidal olmayan antiöstrojenler ve çeşitli endüstriyel uygulamalar için yaygın olarak kullanılmaktadır. Toprak, su gibi çevresel ortamlarda ve canlı organizmaların dokularında bu fungusitlerin kalıntılarına rastlanmaktadır. Giderek artan toksisite raporları, triazol fungusitlerin çevre ve halk sağlığı açısından endişe verici kirleticiler olarak ortaya çıkmasına neden olmuştur. Bu çalışmada, triazol grubu fungusitlerden en yaygın kullanılan türlerinden biri olan tebukonazolün (TEB) hedef dışı organizmalar olan tatlı su midyeleri (Unio mancus) üzerindeki toksik etkileri incelenmiştir. Çalışmada, 96 saat boyunca dört TEB konsantrasyonuna (1.5, 15, 150 ve 1500 µg Aİ L-1) maruz bırakılan midyelerin solungaç ve sindirim bezlerinde çeşitli oksidatif stres parametreleri [toplam antioksidan konsantrasyonu (TAC), toplam oksidan konsantrasyonu (TOC), oksidatif stres indeksi (OSI), glutatyon (GSH), malondialdehit (MDA)], antioksidan enzimler [(süperoksit dismutaz (SOD), glutatyon peroksidaz (GPx), glutatyon S-transferaz (GST), glutatyon redüktaz (GR)] ve biyotransformasyon enzimlerinden karboksil esteraz (CaE) aktivitesi değerlendirilmiştir. TEB’e maruz kalmanın, hem solungaçta hem de sindirim bezinde kontrole göre önemli oranda TAC, OSI, MDA seviyelerini arttırdığı, TOC ve GSH düzeylerini düşürdüğü, SOD, GPx, GST aktivitelerini arttırdığı, GR ve CaE’yi ise inhibe ettiği gözlenmiştir. Sonuç olarak, TEB’in U. mancus’da önemli toksik etkiler oluşturduğu ve tatlı su ekosistemlerinde yaşayan midyelerin TEB’e maruz kalma tehdidi altında olabileceği söylenebilir.

Investigation of metallothionein level, reduced GSH level, MDA level, and metal content in two different tissues of freshwater mussels from Atatürk Dam Lake coast, Turkey

ABSTRACTAtatürk Dam Lake is one of the important freshwater ecosystems in the world in terms of the size of the surface area and the biodiversity. The objective of this study was to determine the effects of metal pollution in the Atatürk Dam Lake on some biochemical markers in the gills and digestive glands of mussels (Unio mancus). Mussel samples were collected in July-2018 from four stations. The metal residues (Cd, Cu, Pb, Zn, and Ni) in the tissues were determined by ICP-MS. The MT, reduced GSH, and MDA levels were analysed using the proposed spectrophotometric methods. According to the results, toxic metals such as Cd and Pb in both tissues were determined mostly in mussels collected from St1. The highest MT and MDA levels in the gills were determined in St3 and St2 respectively, while the highest MT and MDA levels in the digestive glands were determined in St1. Although there was no significant difference in the reduced GSH level in the gills among the stations, the highest reduced GSH level in the digestive glands was determined in St4. These results indicated that mussels are appropriate sentinel organisms for metal contamination with effects on oxidative stress and metal exposure biomarkers.

Diversity and taxonomy of the genus Unio Philipsson in Italy, with the designation of a neotype for Unio elongatulus C. Pfeiffer (Mollusca, Bivalvia, Unionidae).

Novel Unio spp. populations from Slovenia, the Italian peninsula, Sardinia and Sicily were genetically analysed in order to define the distribution and diversity of the genus Unio in Italy and neighbouring areas. The presence of two primarily allopatric autochtonous species, Unio elongatulus Pfeiffer, and Unio mancus Lamarck, is confirmed for the Italian peninsula, Corsica, Sardinia, and Sicily.Autochthonous populations of Unio elongatulus are present in the peri-Adriatic drainages of the Italian and Balkan peninsulas, south as far as the Ofanto River (Apulia, Italy) and Lake Skadar (Albania), while its presence in the Tyrrhenian rivers of Tuscany is likely due to anthropogenic introduction events. Conversely, Unio mancus turtonii Payraudeau, an endangered peri-Tyrrhenian taxon, was found with autochthonous populations in the Apennine-Tyrrhenian drainages of peninsular Italy, eastern Mediterranean France, Corsica, Sardinia and Sicily, while the actual autochthony of the single population found in the Ionian basin of the Italian peninsula (Bradano River, Basilicata) deserves further investigation. The Italian population of U. mancus requienii Michaud, reported from Lake Montepulciano is to be considered allochthonous.The binomen U. elongatulus, although widely used in the recent scientific literature, was, to date, assigned to a doubtful species, because its type locality includes a large area inhabited by different Unio taxa, which are not clearly distinguishable by their shell alone; furthermore, no type material is present in historical collections. To retain the recently-used name, a new restricted type locality is established, where only U. elongatulus lives, and a neotype is designated. The validity of the subspecies of Unio mancus is also discussed and confirmed.Finally, hypotheses on the origin of Italian mussels, and considerations on their conservation status are discussed.

Metal accumulation and biochemical variations in the freshwater mussels (Unio mancus) collected from Atatürk Dam Lake, Turkey

In this study, we aimed to determine the toxic effects of metals on mussels (Unio mancus) selected as biomonitor organisms in the Atatürk Dam Lake. The effect of metal pollution was evaluated using some biochemical markers [glutathione-S-transferase (GST), acetylcolinesterase (AChE), carboxylesterase (CaE), glutathione reductase (GR), metallothionein (MT)] in the digestive gland of the mussels. Mussels were collected from four sampling sites of dam lake in the winter and summer of 2016. The metal levels in the mussel samples varied significantly across the sites and seasons (p < 0.05). Fe was the most accumulated metal, followed by Zn, Cu, and As, while Hg was the least accumulated metal. There were significant differences among sites and between seasons for enzyme activities and MT levels (p < 0.05). Although AChE was inhibited in summer at all sites, the lowest level of AChE was determined for the Sitilce site. Our results showed that there were statistical differences for CaE, GR, and GST activities among sites and between seasons. MT levels were statistically higher in summer than in winter at all sites (p < 0.05). The highest MT level was detected at the Sarısu site in summer, while the lowest MT level was detected at Sitilce in winter. According to the results of correlation analysis, we observed strong correlations between MT and some metal concentrations in both winter and summer (p < 0.05). Our data suggest that industrial activities and domestic wastes along the coast of Atatürk Dam Lake are the main sources of metal pollutants at these sites.

Who wins in the weaning process? Juvenile feeding morphology of two freshwater mussel species.

The global decline of freshwater mussels can be partially attributed to their complex life cycle. Their survival from glochidium to adulthood is like a long obstacle race, with juvenile mortality as a key critical point. Mass mortality shortly after entering into a juvenile state has been reported in both wild and captive populations, thus weakening the effective bivalve population. A similar phenomenon occurs during metamorphosis in natural and hatchery populations of juvenile marine bivalves. Based on a morphological analysis using scanning electron microscopy of newly formed juveniles of the freshwater species Margaritifera margaritifera (L.) (Margaritiferidae) and Unio mancus Lamarck (Unionidae), we show that a second metamorphosis, consisting of drastic morphological changes, occurs that leads to suspension feeding in place of deposit feeding by the ciliated foot. We hypothesize that suspension feeding in these two species improves due to a gradual development of several morphological features including the contact between cilia of the inner gill posterior filaments, the inner gill reflection, the appearance of the ctenidial ventral groove and the formation of the pedal palps. Regardless of the presence of available food, a suspension feeding mode replaces deposit feeding, and juveniles unable to successfully transition morphologically or adapt to the feeding changes likely perish.

Uptake from water, internal distribution and bioaccumulation of selenium in Scenedesmus obliquus, Unio mancus and Rattus norvegicus: part B.

(75)Se-selenite transfer was investigated in a phytoplankton-mussel-rat food chain model consisting of Scenedesmus obliquus (Turpin) Kützing, Unio mancus Lamark and Rattus norvegicus Berkenhout. (75)Se-metabolized forms were investigated in order to identify potential critical steps in the food chain, as well as its relative bioavailability looking also at intracellular, cellular and organ partitioning. Tissue and intracellular distribution of (75)Se in mussels fed with (75)Se-S. obliquus was different compared to those exposed only to inorganic (75)Se-selenite. The intracellular distribution of (75)Se in the hepatopancreas and mantle of mussels fed (75)Se-microalgae was similar to hepatic and renal distributions in rats, suggesting that their stomach dissociated larger (75)Se-containing molecules. The (75)Se partitioned from water (culture medium) to microalgae showing a bioconcentration factor of 435. The bottleneck in the trophic transfer of (75)Se occurred between S. obliquus-U. mancus. From microalgae to mussels and subsequently to rats no bioaccumulation was verified.

Uptake from water, internal distribution and bioaccumulation of selenium in Scenedesmus obliquus, Unio mancus and Rattus norvegicus: part A.

The (75)Se internal bioavailability was investigated in microalgae, mussels and rats as biological experimental models. The (75)Se accumulation from freshwater to microalgae [Scenedesmus obliquus (Turpin) Kützing], from freshwater to mussels (Unio mancus Lamark) and, finally, per os to rats (Rattus norvegicus Berkenhout) was followed using (75)Se-labelled selenite looking at (75)Se uptake, retention, intracellular distribution and binding with cellular biocomplexes. After exposure to 10, 50 and 500 μg Se L(-1), the microalgae showed an inhibitory effect on population growth only at the highest concentration. Mussels exposed to 105 μg Se L(-1) showed an accumulation of the element with time in all tissues. Intracellularly, Se was present in all subcellular fractions, especially in the cytosol. Rats were treated via oral administration with 5 μg Se rat(-1). After 24 h, liver and kidney showed the highest Se concentration.

Presence of organic layers in shells of fossil and recent Unionoida (Bivalvia) and their implications

The presence of thin organic layers embedded in the nacreous layer in the shell of several species of Unionoida has been widely considered to be largely a reaction to prevent further shell dissolution once part of the shell has been corroded. Their microstructural characteristics have also been used as taxonomic characters to separate the families Margaritiferidae and Unionidae. This paper focuses on the description and interpretation of these organic layers in samples of four extant species of European Unionidae coming from acidic and alkaline waters, six extant species of Margaritiferidae, one Cretaceous Unionidae and two Cretaceous Margaritiferidae species. Our results demonstrate that organic layers have characterized species of Unionoidea at least since the Cretaceous and occur in specimens coming from both acidic and alkaline waters. Moreover, the presence of these layers in noncorroded shells can be interpreted as a preventative or ‘prophylactic’ measure against corrosion. Their thickness is the only useful character verified to separate the two families. In the Margaritiferidae, organic layers were found to be present in Margaritifera margaritifera, M. valdensis, M. idubedae, M. laosensis, M. laevis and M. monodonta, and absent in M. auricularia and M. marocana. In Unionidae, they appear in Protopleurobema numantina, Potomida littoralis and in some individuals of Unio mancus, U. delphinus and U. tumidiformis. We argue that organic layers played a fundamental role in shell protection during the invasion of freshwater by the earliest Unionoida, while today they function to improve fitness in acidic water in some species.

Bad taxonomy can kill : molecular reevaluation ofUnio mancusLamarck, 1819 (Bivalvia : Unionidae) and its accepted subspecies

Key-words: COI gene, conservation genetics, freshwater mussel, molecular systematics, species delimitation The conservation status of European unionid species rests on the scientific knowledge of the 1980s, before the current revival of taxonomic reappraisals based on molecular characters. The taxonomic status of Unio mancus Lamarck, 1819, superficially similar to Unio pictorum (Linnaeus, 1758) and often synonymized with it, is re-evaluated based on a random sample of major French drainages and a systematic sample of historical type localities. We confirm the validity of U. mancus as a distinct species occurring in France and Spain, where it is structured into three geographical units here ranked as subspecies: U. m. mancus [Atlantic drainages, eastern Pyrenees, Spanish Mediterranean drainages], U. m. turtonii Payraudeau, 1826 [coastal drainages East of the Rhone and Corsica] and U. m. requienii Michaud, 1831 [Seine, Saone-Rhone, and coastal drainages West of the Rhone]. Many populations of Unio mancus have been extirpated during the 20th century and the remaining populations continue to be under pressure; U. mancus satisfies the criteria to be listed as “Endangered” in the IUCN Red List.

The identity and biology of unio mancus laMarck, 1819 (=U. Elongatulus) (bivalvia: unionidae) in the Iberian Peninsula

Genetic variability, shell morphology, anatomy, reproductive season, glochidium morphology and host fish of several Iberian populations of Unio mancus Lamarck, 1819 (=U. elongatulus C. Pfeiffer, 1825) were examined. The genetics of three allopatric populations were studied, including two ‘races’ previously described for this species on the Iberian Peninsula. All shared the same haplotype of the COI mitochondrial gene. It is proposed that all known Iberian Mediterranean populations of the genus Unio correspond to Unio mancus. All mature specimens studied were dioecious. Glochidial release occurred between March and August. The barbel Barbus graellsii was the natural host of the U. mancus glochidia in the studied area. In artificial infestations performed in aquaria, seven fish species, all native, carried the glochidia throughout their complete metamorphosis. This process occurred in 141 degree/days. Newly released juveniles were spherical and had a thin marginal rim of new shell.

The elemental (C, H, N, O, S) and biochemical composition of Unio mancus (Pfeiffer) and Anodonta cygnea L.

The elemental (C, H, N, O, S) and biochemical composition of <i>Unio mancus</i> (Pfeiffer) and <i>Anodonta cygnea</i> L.