Conservation of freshwater bivalves at the global scale: diversity, threats and research needs
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Bivalves are ubiquitous members of freshwater ecosystems and responsible for important functions and services. The present paper revises freshwater bivalve diversity, conservation status and threats at the global scale and discusses future research needs and management actions. The diversity patterns are uneven across the globe with hotspots in the interior basin in the United States of America (USA), Central America, Indian subcontinent and Southeast Asia. Freshwater bivalves are affected by multiple threats that vary across the globe; however, pollution and natural system (habitat) modifications being consistently found as the most impacting. Freshwater bivalves are among the most threatened groups in the world with 40% of the species being near threatened, threatened or extinct, and among them the order Unionida is the most endangered. We suggest that global cooperation between scientists, managers, politicians and general public, and application of new technologies (new generation sequencing and remote sensing, among others) will strengthen the quality of studies on the natural history and conservation of freshwater bivalves. Finally, we introduce the articles published in this special issue of Hydrobiologia under the scope of the Second International Meeting on Biology and Conservation of Freshwater Bivalves held in 2015 in Buffalo, New York, USA.
KeywordsBivalvia Unionida Venerida IUCN Red List Freshwater mussels Conservation
Freshwater ecosystems are among the most threatened on the planet facing unprecedented pressures related to the increase of human population and socioeconomic development (Dudgeon et al., 2006; Vörösmarty et al., 2010). Increasing anthropogenic pressure worldwide results in habitat loss, habitat modification and fragmentation, overexploitation of natural resources (including water), pollution, introduction of invasive alien species (IAS) and climate change (Malmqvist & Rundle, 2002; Strayer & Dudgeon, 2010). Biodiversity crisis is one of the major consequences of steeply rising human demands, and among the animals with high extinction rates are freshwater bivalves (FB) (Strayer et al., 2004; Lydeard et al., 2004; Régnier et al., 2009; Lopes-Lima et al., 2014, 2017a). The future survival of FB is highly impaired and considering the large suite of ecosystem services they provide (Vaughn, 2017) scientists, managers, politicians and the general public need to strengthen their cooperation in order to conserve these species.
Whereas over the last years multiple studies have been published concerning the biology, ecology and conservation of FB, the majority of them were carried out in North America and Europe (Lopes-Lima et al., 2014). Consequently, a great ignorance about basic aspects (e.g. distribution, diversity, abundance, population structure and life cycle) concerning species inhabiting South America, Africa and Asia still persists and much more information is needed for these continents.
In the present paper, we compile data on FB diversity patterns, conservation status and threats from the International Union for Conservation of Nature (IUCN) database using a species list adapted from Graf & Cummings (2017) and mapped them in ecoregions adapted from Graf & Cummings (2007) and Haag (2010). We also briefly discuss research needs and urgent management actions that may help conserve these animals, and introduce the articles published in this special issue resulting from the Second International Meeting on Biology and Conservation of Freshwater Bivalves held in 2015 in Buffalo, United States of America (USA).
Diversity patterns at the global scale
We would like to stress that diversity patterns described above may be underestimated and may change substantially as a result of ongoing and future surveys in the less studied regions of Southeast Asia, Africa, NT and AU. For example, Bolotov et al. (2017) studying the FB of a poorly known and remote basin (Sittaung) in Myanmar described two new genera and seven new species. Also, even in Europe and NA, which are the most well-studied continents, the knowledge of the diversity of Unionida is still undergoing considerable changes (e.g. Froufe et al., 2016a, b, 2017; Araujo et al., 2017; Lopes-Lima et al., 2017a; Williams et al., 2017; Smith et al., 2018).
Conservation status and major threats
The global pattern is more or less similar in all ecoregions, with the exception of the NT and AF (Fig. 6). While the NT pattern may not be very representative of the ecoregion due to the few assessed species, in AF it reflects the poor knowledge about the population size and trends. This is due to the lack of research that is being done in the AF, where survey and monitoring studies are almost non-existent (Lopes-Lima et al., 2014; Sousa et al., 2016, 2017).
The relative percentage of recorded threats is generally similar across the main ecoregions with a few notable exceptions. For instance, in the NA and PA species seem to be less threatened by climate change than the tropical and southern hemisphere ecoregions. Conversely, in the more developed areas of the NA and the PA, habitat modifications seem to negatively affect more species in these ecoregions than in the AF and IN. Exploitation is a much more detrimental threat in the IN than elsewhere (Fig. 7). In fact, harvesting of mussels for human consumption in East and Southeast Asia is a major economic activity; for example, in Vietnam it may reach up to 50,000 tons per year in each major basin (Köhler et al., 2012). Furthermore, the ratio of agriculture related threats is higher in AU and PA, mainly due to water diversion and extraction.
Research and conservation actions needs
Although many research gaps and conservation needs have been identified in the last years, many recent technological advances can provide us with new insights that are needed for FB research. For example, new remote sensing techniques like underwater video and side-scan sonars may help survey FB populations, and identify more favourable habitats (Powers et al., 2014; Mehler et al., 2016). Use of drones in semi-arid regions can aid in tracking and identifying the remaining pools after droughts where mussels take refuge. These technologies and also the use of environmental DNA analyses may help gathering basic biological and ecological data on distribution and abundance, which are still missing for many species (Stoeckle et al., 2016). More powerful genetics and morphometric tools are also increasingly available, for instance, new statistical tools for species delimitation using molecular and/or other types of data such as morphometry and anatomical traits (e.g. Froufe et al., 2016b; Pfeiffer et al., 2016). These tools are particularly important owing to the fact that many species present hidden cryptic diversity (Froufe et al., 2016b; Pfeiffer et al., 2016). Additionally, next-generation sequencing is now allowing for quicker and less expensive robust phylogenies using methods like whole-transcriptome and whole-mitogenome analyses with a wide range of markers (Guerra et al., 2017; Lopes-Lima et al., 2017c). Furthermore, using reduced genome representations or snip analyses, it is now possible to get more information on the phylogeographic patterns of species and on the definition of conservation units (Catchen et al., 2017; Desalle & Amato, 2017).
While most of the global protected areas network is aimed at protecting essentially terrestrial vertebrates, the identification of sites to conserve freshwater vertebrates and invertebrates such as FB is also of crucial importance (Darwall et al., 2011; Maceda-Veiga et al., 2017). Using the IUCN Key Biodiversity Areas (KBAs) network (IUCN, 2016) or new systematic conservation planning approaches (e.g. Hermoso et al., 2015) may help to promote a better FB representation within protected area networks.
The proceedings of the Second International Meeting on Biology and Conservation of Freshwater Bivalves
All the research and conservation needs summarised above make the facilitation of cooperation among scientists from different countries and continents particularly important. For example, recent reviews published by multinational teams of scientists provided vital baseline information about FB on different continents (e.g. Pereira et al., 2014 for South America, Walker et al., 2014 for Australia; Lopes-Lima et al., 2017a for Europe; Williams et al., 2017 for North America, and Zieritz et al., 2017 for East and Southeast Asia). Additionally, intercontinental cooperative research is also becoming increasingly common (see for example Zieritz et al., 2016; Lopes-Lima et al., 2017b). In order to discuss the current and future research challenges and needs, the Second International Meeting on Biology and Conservation of Freshwater Bivalves was hosted by the Great Lakes Centre at SUNY Buffalo State College in Buffalo, New York, USA, from 4 to 8 October 2015, bringing together over 80 scientists from 19 countries and four continents (Europe, North America, South America and Australia) (Burlakova et al., 2017).
The present special issue in Hydrobiologia comprises a total of 34 papers (including this introductory note) summarising some of the information presented in this meeting. These papers cover a wide variety of topics, from a review of ecosystem services provided by freshwater mussels (Vaughn, 2017) to papers describing the diversity patterns and conservation of Unionida in East and Southeast Asia (Zieritz et al., 2017) as a result of international collaboration. Seven papers focus on different biological aspects of invasive bivalve species, including diversity changes by species substitution (Karatayev et al., 2017), physiological aspects (Labecka & Domagala, 2016), dispersion (Collas et al., 2016), ecological effects on native bivalve species (Ferreira-Rodríguez et al., 2016), low palatability to distinct predators (Castro et al., 2017), metabolite emission suppression in zebra mussels exposed to predation stress (Antoł et al., 2017) and the use of a new sonar technology and underwater imagery analysis for the survey of FB in rivers (Mehler et al., 2016). Propagation as a conservation tool was the subject of three studies: one about an improved method of in vitro culture of glochidia (Ma et al., 2016), one introducing short-term breeding of the Endangered freshwater pearl mussel Margaritifera margaritifera (Linnaeus, 1758) as a new technique for the augmentation of declining populations (Moorkens, 2017) and one revising the challenges in the conservation progress of Margaritifera auricularia (Spengler, 1793) (Prié et al., 2017). Six papers used molecular tools to describe genetic structure or phylogeographic patterns of European (Feind et al., 2017), North American (Hewitt et al., 2016; Mathias et al., 2016) and South American species (da Cruz Santos-Neto et al., 2017); to reveal the uncommon doubly uniparental inheritance of mitochondria in a European species (Soroka and Burzynski, 2017) and the sequencing of transcriptomic resources for an invasive species (Soroka et al., 2017). The interaction between mussels and their host fishes was addressed in three papers that evaluate the effects of stress (Douda et al., 2016), cross-immunity (Chowdhury et al., 2017) and temperature (Schneider et al., 2017) on the reproduction of freshwater mussels. Three papers describe distribution patterns with distinct spatial and temporal scales: the population trends of Unionidae in Romania (Sîrbu and Benedek, 2017), the distribution of freshwater mussels and their host fishes in Texas (Dascher et al., 2017) and a study that reconstructs the historical range and population size of the threatened species Popenaias popeii (Karatayev et al., 2015). On a smaller scale, a study on the longitudinal variation in freshwater mussel assemblages within two rivers is presented by Chambers & Woolnough (2016), while Dittman et al. (2017) evaluate the microhabitat and biology of the poorly studied pea clam Sphaerium striatinum. Two papers assess the growth of M. auricularia (Nakamura et al., 2017) and of juvenile freshwater pearl mussels M. margaritifera at the river scale (Černá et al., 2017). One paper assesses the shell phenotypic plasticity of Unio crassus (Zając et al., 2017). The influence of the flood pulses and of near-bed hydrodynamics on freshwater mussels is evaluated by Callil et al. (2017) and Sansom et al. (2017), respectively. Finally, toxicology and archaeology are represented by a study of the effects of polycyclic aromatic hydrocarbons on unionid mussels (Archambault et al., 2017) and the conservation implications of freshwater mussel remains in a Texan river (Popejoy et al., 2016).
Conservation of FB requires urgent collaboration between scientists, managers, politicians and the general public, in order to share knowledge and efforts. An example of this collaboration is the International Meeting on Biology and Conservation of Freshwater Bivalves, but more efforts are necessary for the transfer of knowledge between scientists and the general public in order to raise awareness about the importance of FB conservation. These efforts can include, but not be limited to the increase in visibility of FB conservation issues in the media, better engagement with local communities and stakeholders (e.g. providing training and lifelong learning opportunities like workshops for public, better information dissemination and accessibility of collaborative research even integrating participants from civil society into surveys and research projects), publications and additions to national collections.
We thank the Editor-in-Chief Prof. Dr. Koen Martens for his help and support and the coordinator of Springer Journals Editorial Office, Deepan Selvaraj, for his hard work and assistance in the editorial process of this Special Issue. This work was supported by FCT—Foundation for Science and Technology, Project 3599—Promote the Scientific Production and Technological Development and Thematic 3599-PPCDT by FEDER as part of the project FRESHCO: multiple implications of invasive species on Freshwater Mussel co-extinction processes (Contract: PTDC/AGRFOR/1627/2014). FCT also supported MLL under Grant (SFRH/BD/115728/2016).
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