alterado para:  “Combining phylogeny, systematics and ecology to advance the conservation of freshwater mussels Bivalvia: Unionida”  Under the surface: combining ecological and evolutionary analysis to conserve freshwater mussels in the Iberian Peninsula

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Lifting the curtain on the freshwater mussel diversity of the Italian Peninsula and Croatian Adriatic coast

Publication . Froufe, Elsa; Lopes-Lima, Manuel; Riccardi, Nicoletta; Zaccara, Serena; Vanetti, Isabella; Lajtner, Jasna; Teixeira, Amílcar; Varandas, Simone; Prié, Vincent; Zieritz, Alexandra; Sousa, Ronaldo; Bogan, Arthur E.

Freshwater mussels of the order Unionida have been dramatically declining globally. Despite their ecological importance, conservation of these animals has been hindered by unresolved taxonomy and a lack of data on the distribution and status of populations, especially in southern Europe. Although the Italian Peninsula has been noted as a centre of endemism and one of the major refugia of the glacial ages for several taxa, few studies have been performed on the genetic diversity of Unionida. Most importantly, the taxonomic status of several freshwater mussel populations of the Italian Peninsula is still unresolved. Here we present the first comprehensive dataset for the Unionida of the region spanning Italy and the coastal Croatian region (west of the Dinaric Alps). In total, 191 specimens were collected (85 Anodonta, 64 Unio, 17 Microcondylaea bonellii and 25 Sinanodonta woodiana) from 34 sites across the Italian Peninsula and coastal Croatian river basins for molecular identification (COI, 16S and 28S). Genetic analyses were performed to understand major phylogenetic and phylogeographic patterns. Seven species were detected: three Anodonta species (A. anatina, A. cygnea and A. exulcerata), two Unio species (U. mancus and U. elongatulus), Microcondylaea bonellii, and the invasive Sinanodonta woodiana. The presence of three endemic species (A. exulcerata, U. elongatulus and M. bonellii) confirms the importance of the region as a centre of endemism for freshwater mussels. The Apennine Mountains act as an important biogeographic barrier.

2017Journal article

Open access

Invasive crayfishes as a threat to freshwater bivalves: Interspecific differences and conservation implications

Publication . Meira, Alexandra; Lopes-Lima, Manuel; Varandas, Simone; Teixeira, Amílcar; Arenas-Arenas, Francisco José; Sousa, Ronaldo

Freshwater bivalves have suffered major global declines, being the introduction of invasive alien species (IAS) an important, but not well studied, mechanism of threat. This study assessed the predator-prey relationship between two non-native crayfish species (Procambarus clarkii and Pacifastacus leniusculus) and three native (Anodonta anatina, Potomida littoralis and Unio delphinus) and one non-native (Corbicula fluminea) freshwater bivalve species through experiments in laboratory and validation under natural conditions (Sabor River basin, Portugal). All native bivalve species were preyed both in laboratory and in the field; however, both crayfish species were unable to prey C. fluminea. Predation was dependent on crayfish and bivalve species but was not affected neither by crayfish nor bivalve sizes. In the laboratory, the most preyed species by both crayfishes was A. anatina. On average, this species was preyed at least 12% more than other species, when crayfishes had a choice. Similar results were found in the field. We also found signs of competition between both crayfishes, being P. clarkii more dominant and aggressive as this species, on average, manipulated the bivalves 63.6% more times and 24:33 min longer than P. leniusculus, and initiated 55.8% more agnostic bouts. Our results support the idea that P. clarkii and P. leniusculus can affect native freshwater bivalves, but clear interspecific differences were detected. Both crayfishes may have direct and indirect impacts on bivalve populations by increasing mortality or by reducing their fitness. In addition, since both crayfishes do not prey C. fluminea, they offer this IAS another advantage over native bivalves. Given the widespread distribution of both P. clarkii and P. leniusculus and the threatened status of many freshwater bivalves, the dynamics and impacts of this relationship should be taken in account in the implementation of management measures devoted to the conservation of native freshwater bivalves.

2019Journal article

Open access

Die-offs of the endangered pearl mussel Margaritifera margaritifera during an extreme drought

Publication . Sousa, Ronaldo; Ferreira, André; Carvalho, Francisco; Lopes-Lima, Manuel; Varandas, Simone; Teixeira, Amílcar

Droughts may be responsible for important ecological impacts in freswater ecosystems, including the death of rare species. This study assessed the mortality of the endadgered pearl mussel Margaritifera margarififera (Linnaeus, 1758) in the Mente, Rabaçal and Tuela rivers (north west of the Iberian Peninsula) during the extreme summer drought of 2017. Mortality ocuurred as a result of the low river flow, which led to mussel stranding near the banks and consumption (by predation of scavenging) by wild boar Sus scrofa (Linnaeus, 1758). Mortality differed across sites. The shell length of live mussels (measured before the drougt( and dead mussels significantly differed in the Rabaçal River, but not in the Mente and Tuela rivers. Extreme droughts are predicted to increase in number and intensity i the future, and possible impacts on rare species such as M. margaritifera populations in Iberia (and elsewhere) may now be at increased risk, and measures should be implemented in order to mitigate the impacts of future extreme droughts.

2018Journal article

Open access

Oued Bouhlou: a new hope for the Moroccan pearl mussel

Publication . Sousa, Ronaldo; Teixeira, Amílcar; Santos, André; Benaissa, Hassan; Varandas, Simone; Ghamizi, Mohamed; Prié, Vincent; Froufe, Elsa; Lopes-Lima, Manuel

The freshwater pearl mussel Margaritifera marocana (Pallary,) is an endemic species of Morocco being listed as critically endangered and it stands among the world's 100 most threatened species. An extensive survey was performed in the Sebou basin (total area of approximately 40,000 km2), covering 26 different sites. Margaritifera marocana was found only in four sites limited to a small tributary (Oued (=River) Bouhlou). This population has a very restricted distribution (no more than 4 km of river length) but appears stable with recent recruitment, since small specimens were found. Genetic analyses were performed, showing that this population has a similar diversity to that found in the River Laabid (Oum Er Rbia basin), but represents a distinct conservation unit that should be managed independently. Although this study adds a new population to the current known distribution of M. marocana, urgent conservation measures (e.g. extension of the Tazzekka National Park; better management of river flow; increase of the riparian vegetation in some stretches; establishment of national and international legislation, and engagement of local citizens) are needed given the species' restricted distribution, its rarity, and the numerous threats that impair its future survival.

2018Journal article

Open access

A tale of shells and claws: The signal crayfish as a threat to the pearl mussel Margaritifera margaritifera in Europe

Publication . Sousa, Ronaldo; Nogueira, Joana Garrido; Ferreira, André; Carvalho, Francisco; Lopes-Lima, Manuel; Varandas, Simone; Teixeira, Amílcar

The freshwater pearl mussel Margaritifera margaritifera is a highly threatened species in Europe. Several mechanisms may be responsible for the decline in distribution and abundance of European pearl mussel populations, but almost no quantitative data exists about the possible negative impacts of invasive alien species (IAS). In this study, we clearly demonstrate that the invasive signal crayfish Pacifastacus leniusculus predates pearl mussels, using a laboratorial experiment followed by in situ validation in four rivers in the North of Portugal (Mente, Rabaçal, Tuela and Baceiro Rivers; Douro Basin). In the laboratory, the crayfish had a clear preference for small-sized pearl mussels but no differences in predation were found in mesocosms with and without sediment. In addition, we clearly demonstrated that the signal crayfish predates pearl mussels in natural conditions and detected a significant density dependent effect (i.e., sites with more crayfish presented higher number of pearl mussel shells with marks of predation). Given the recent introduction of the signal crayfish and the potential negative impacts on pearl mussel populations we also investigated its autoecology (distribution, abundance, size structure and sex-ratio) in the four studied rivers. Significant differences in average abundance and size of the crayfish were detected between sites and the sex-ratio was highly skewed to females. In view of the widespread distribution of signal crayfish (and other invasive crayfish species) in Europe, future management actions devoted to the conservation of pearl mussels should take in consideration the possible negative effects of these predators, especially on juveniles.

2019Journal article

Open access