Invasive ecology of corbicula fluminea (müller, 1774)

  1. Noé Ferreira Rodríguez
Dirixida por:
  1. Isabel Pardo Gamundi Director

Universidade de defensa: Universidade de Vigo

Ano de defensa: 2016

  1. Caryn Vaughn Presidente/a
  2. Rafael Araújo Armero Secretario/a
  3. José Prenda Marín Vogal
  1. Ecoloxía e bioloxía animal

Tipo: Tese

Teseo: 431675 DIALNET


Between the worst invasive species in Europe, the Asian clam Corbicula fluminea (Müller, 1774) represents an important threat to aquatic environments. The species started its worldwide dispersion at the beginning of the twentieth century associated with human activities such as global trade, fishing bait, recreational activities and so on. In addition to the native range in Asia, at current the species is present in North and South America, North Africa and Europe. In Europe, C. fluminea was first record as invasive exotic species in 1980. Since then, the species has greatly expanded its distribution range being present in almost all European river basins, from Iberia in the southwest to Ireland and UK in the North and to Bulgaria and Romania in the East. Given this wide distribution range, in the first part of this thesis we aim to 1) actualize the distribution of C. fluminea in Galicia and draw an ecosystem approach to biological invasions in freshwaters from the region and to C. fluminea invasion in particular. To achieve these objectives we designed a survey campaign covering sixteen river systems and one pond system (total of 65 sampled localities) in Galicia. Additionally, field data were complemented with a series of interviews and a revision of scientific and grey literature. As a result of our field research we actualized C. fluminea distribution in Galicia. Nowadays, C. fluminea is present in three river basins (Miño-Sil, Ulla and Mero). Additionally, grey literature signaled its presence at Lagoa de Antela and Pontiña river. Our data indicated a mean upstream spread of 3.6 km yr-1. Regarding spread vectors of C. fluminea in Galicia, the ecosystem approach revealed that the area occupied by the species may be related with loss of native biodiversity, economy and implementation of legislative instruments regarding invasive species. These results are of value to address introductory pathways and dispersal vectors of invasive species in the region. An example is the involvement of different stakeholders (e.g. fishermen) in order to early identify the presence of new invasive species. In particular, the River Miño estuary was invaded by C. fluminea since late 80’s. This invasive bivalve has colonized all the international section of the river between Spain and Portugal, reaching more than 150 km upstream from the river mouth. Corbicula within this time has become the dominant species of the benthic fauna in the estuary. In general, the variation of environmental factors in brackish and freshwaters determines its natural biodiversity and constitutes important environmental barriers for invasive species establishment. In this regard, estuaries act as filters transferring exotic species between marine and freshwater ecosystems due to the salinity gradient. Once in freshwaters, calcium is a key physiological compound for invertebrates. It is required for shell formation, muscle contraction, mediates gene expression, and allows counteracting acidosis during stress periods, among other functions. In the second part of this doctoral thesis, we aimed to obtain a complete characterization of the River Miño estuary, focused upon the study of the environmental factors of relevance for the distribution of C. fluminea in the area. According to these results we tested the capacity of C. fluminea to cope with osmotic stress conditions previously to invade new freshwater habitats through estuaries. Secondly, we aimed to decipher whether the environmental calcium concentration might hamper C. fluminea invasiveness in the upstream colonization process from the estuary. To achieve these objectives we designed two sampling campaigns. Firstly, a quantitative survey campaign completed at 47 sites along the 15 km in the River Miño estuary where the species was known to occur. Secondly, environmental factors and C. fluminea populations were studied at twelve rivers and two lagoons (total of 22 sites) located in the Northwestern Iberian Peninsula, between the Ulla River (Galician, Spain) and the Mira River (Central Portugal). Additionally, laboratory experiments were performed to assess the ability of C. fluminea to cope with estuarine osmotic stress conditions and to grow under different environmental calcium concentrations. Further, we used a multidisciplinary and integrative approach in order to decipher whether the environmental calcium concentration might hamper C. fluminea invasiveness. In this regard, field surveys were complemented with in situ Ca2+ content assessment in soft tissues and molecular biology analyses as well as growth laboratory experiments. At local scale (River Miño estuary), density and biomass were positively related to coarse sediments and to sedimentary organic matter that can be taken as a food supplement. The study of size frequency distributions indicated that individuals of size 20 mm dominated the River Miño estuarine population, with at least two annual cohorts. Smaller individuals preferred coarse sediments in combination with high organic matter contents, allowing us to identify the estuary recruitment areas. Downstream, osmotic stress exposure compromised the establishment and survival of C. fluminea. Under osmotic stress exposure, great mortality rates were reached after 19 days. The species tolerance range, measured by individual maintained activity, was at salinity ̴20 when exposed to winter temperatures, while when animals were exposed to summer ones its tolerance was reduced to salinity lower than 15. Results revealed that C. fluminea shows a great physiological flexibility to cope with salinity variations in estuaries. In summer, the temperature increases the metabolic rate making the species more vulnerable to osmotic stress exposure. Upstream, calcium may determine invasiveness of ecosystems. A Principal Component Analysis of different environmental factors at 22 sampling stations within C. fluminea distribution area identified environmental Ca2+ concentration as one of the variables that majorly explains variations among sampling station. Calcium content in animal’s body from two representative rivers was dependent on the environmental calcium concentration of freshwater basins; the lower the concentration, the lower the body’s content. Expression of stress- and calcium homeostasis-related genes was higher in C. fluminea from low calcium concentration environments than in those from calcium rich freshwater basins. Finally, under experimental conditions, low water calcium concentrations decreased C. fluminea’s growth rates. Our results identify important ecological features of C. fluminea and provide valuable information to improve exotic invasive species management in the region. Firstly, the identification of environmental factors controlling C. fluminea distribution and recruitment areas in the River Miño estuary aims to be the basis for management plans designed to prevent and control the species in Atlantic estuaries, at a time that allowed us the design of experimental assays to validate the observations resulting from this study. Our experiments designed to assess C. fluminea resistance to osmotic stress may be of valuable concern to prevent new invasions through ship ballast waters ensuring complete mortality if individuals are retained for >26 days. In addition, for the first time, present data suggests environmental calcium concentration as a determinant factor of invasive success of C. fluminea in freshwater environments; and provides new clues for freshwater basins management allowing the identification of areas with great invasion risk. Following, if invasive species are able to cope with environmental barriers and establish self-sustaining populations may cause environmental harm, economic harm and impact to human health. Environmental harm involves negative impacts over native fauna related to already damaged populations. Conversely, invasion of successional mature and undisturbed communities usually requires that the alien taxon overcomes a different category of barriers that increases ecological resistance of the environment. The global decline of freshwater mussels is related with a great variety of threats, including the introduction of invasive species. In this regard, C. fluminea may compete with freshwater bivalves for space and/or food resources. In addition, the negative impact on native freshwater mussels is also likely to occur through other mechanisms, such as possible ingestion of unionid sperm, glochidia or newly metamorphosed juveniles by C. fluminea, massive mortalities which result in unionid mortality by ammonia toxicity, and bioturbation activities and organic matter enrichment due to production of faeces and pseudofaeces, which may alter sediment biochemistry and impair the survival of unionids. But, in a general context, the worldwide decline of freshwater biodiversity (including freshwater mussels) is attributed to global change. Global warming, eutrophication or invasive species introduction are some components of the ongoing global change. Namely, global warming influences species migration and distribution, abundance and population dynamics, and functional variation in aquatic and terrestrial organisms. In this regard, most studies to date conclude that climate changes increase the distribution range and will promote the establishment of the most invasive aquatic invertebrates in new areas. Given this global change context, the third part of this thesis aim to determine if C. fluminea interacts negatively with native freshwater mussels (i.e. Unio delphinus), potentially competing for food resources and/or space. In addition, we aim to determine if the successful biological traits of C. fluminea may enhance its competitive ability compared to native mussels in a global change context (increased temperatures and/or nutrient enrichment). Concerning the negative impact of C. fluminea over native freshwater mussels, we perform field and laboratory experiments. Namely, inter-specific assays using the invasive species C. fluminea and the native species U. delphinus comprised two different approaches: i) a field experiment to determine possible negative effects on growth and physiological condition of U. delphinus under different C. fluminea density and ii) a laboratory experiment to assess possible alteration on the activity pattern of U. delphinus in sympatry with C. fluminea. In a global change context, we experimentally simulated the effect of increasing temperatures during summer heatwaves to assess strengths and weaknesses of U. delphinus in coexistence with C. fluminea. We measured several physiological parameters (clearance rate, oxygen consumption and absorption efficiency) and the energetic balance to determine the potential effects of increasing temperatures on mussel physiological activity. In addition, the effect of C. fluminea presence was evaluated by measuring U. delphinus faeces production, as a response variable to food consumption. Faeces production was measured under fixed evacuation times, and under three temperatures and three trophic conditions, using phytoplankton concentrations as a proxy for trophic condition. Our results showed that U. delphinus exhibited lower growth, lower physiological condition and greater locomotor activity at higher C. fluminea density, which may suggest that this unionid is negatively affected by C. fluminea and may be displaced to less favorable habitats. In a global change context, U. delphinus responded to high temperatures with higher respiration rates, showing an increase in energy expenditure. U. delphinus faeces production, a proxy for food consumption, varied significantly with each factor analyzed (temperature, food availability and C. fluminea presence) and there was an interactive effect between these factors; increasing with temperature and trophic condition, and declining in the presence of the invasive clam. Results showed that heatwaves will negatively influence the physiology of native mussels and suggest that C. fluminea will advantageously outcompete U. delphinus in warmer and highly productive freshwater environments. Although we were not able to establish the main mechanisms responsible for these results our experiments identified important clues for native freshwater mussel conservation. Possibilities may include competition for food resources, competition for space which may result in mussel displacements and/or changes in microhabitat features, as a result of bioturbation and production of faeces and pseudofaeces by C. fluminea. Given that results, in a global change context, we confirm that warming is likely to worsen the scenario when invasive species are present. C. fluminea can negatively affect unionids by a more efficient food uptake in warmer and nutrient enriched freshwaters, limiting food availability at time that native mussels depend on food quantity to compensate for the metabolic demand from increasing temperatures. Hence, the early identification of areas that are threatened by invasive species is crucial for planning effective control measures or conservation actions (e.g. mussel translocation from highly invaded areas). Those might be based on the relative impact of each factor and considering the possible ‘interactive effects’ as driving forces of native species decline. Besides, biological invasions can yield substantial benefits for native biodiversity. There is a large literature on the rapid adaptation of native species to an introduced species. Interactions among native and exotic fauna involve facilitative interactions, cascading effects across trophic levels, community re-structuration or evolutionary changes. In this regard faeces and pseudafaeces produced by C. fluminea increases organic matter content and food resources for some macrozoobenthic species; and empty shell accumulation and bioturbation in the sediments create conditions for the establishment of other invertebrates. Concerning benefits across trophic levels, the concept of ‘invasional meltdown’ was introduced to describe the synergistic interactions among invaders that may increase the susceptibility of ecosystems to future invasions. Between predator-prey interactions, the establishment of one species may facilitate in a reciprocal way further introductions. In the fourth part of this thesis we aim to assess if native populations trend (i.e. Haematopus ostralegus) was related to global change drivers, namely temperature and C. fluminea introduction. In addition, we aim to examine the facilitation process on native and exotic terrapin species by the invasive clam C. fluminea in Iberian inland waters. Finally, we aim to determine if two invasive bivalves, the Asian clam C. fluminea and the Eurasian zebra mussel Dreissena polymorpha (Pallas 1771), could be potential food items for Acipenser sturio Linnaeus, 1758 and assess the potential of sturgeons as biological control of invasive bivalves. To investigate how global change affects oystercatcher population, winter temperature data in the Rive Miño, average Autumn temperature data from the North Sea, North Atlantic Oscillation and Asian clam invasion as a potential ‘perturbation factor’ were included in an Auto-Regressive Integrated Moving Average model (ARIMA) to analyze the average number of wintering oystercatchers for a 30-years period (1985 – 2014). Regarding the possibility of future facilitation processes among terrapin species, we compare the predation rate and size selection with native and alien freshwater turtles. We run multiple experimental trials to estimate turtles predation rates on C. fluminea using native and exotic terrapins established in the Iberian Peninsula. Finally, a pilot study was designed to determine if the invasive bivalves, C. fluminea and D. polymorpha, could be potential food items for A. sturio and to describe sturgeon predator – bivalve prey relationship in order to determine the potential of sturgeon’s reintroduction plans as biological control in invaded ecosystems. Facilitative interactions analysis has shown an adaptation of native waterbird species to C. fluminea invasion. Results showed that wintering waterbirds declined since the mid-1980s. In contrast, oystercatchers doubled its wintering effectives within the study area. The ARIMA model showed that relative abundance is partially dependent of C. fluminea density in the River Miño estuary. Additionally, warming at the study area and in North Sea had a significantly relation with oystercatcher population. Regarding terrapin diet, our results evidenced great similarities between native and exotic emidid species. Meanwhile there were different feeding capabilities among terrapins. In general, the ability to feed upon C. fluminea was correlated with terrapin’s mouth kinematics and differed greatly between native and exotic species. In this regard, the opportunistic behavior of exotic species contrasts with the adaptive pattern of native species. Finally, the pilot study designed to explore the potential of juvenile European Atlantic sturgeon to feed upon C. fluminea and D. polymorpha shown that, the potential to control both invasive species may be restricted to initial invasion stages. In this final part of the thesis we discus facilitative interaction with native and exotic species. As shown, results presented in this work indicate that at the study site, the Eurasian oystercatcher population increased its wintering effectives in response to C. fluminea invasion. The species provide a novel exploitable food resource that may favors both, oystercatcher´s movements from adjacent coastal areas to the inner estuary and the establishment of a resident population. Hence, control measures applied to long term invasions must be carefully analyzed since invasion has created a dependent native community. In other side, we discuss the plausible scenario where the introduced C. fluminea can aid the invasion of non-native terrapins while having negative effects over threatened native species. Namely, C. fluminea may facilitate the establishment of new exotic terrapin species (e.g. Graptemys pseudogeographica, Sternotherus odoratus) in Europe, and promote the spreading expansion of the Slider turtle Trachemys scripta. Since the prohibition of T. scripta importation in the European Union, the pet industry shifted to new species that already inhabit water courses. In this regard, our results indicated the necessity to assess invasion risks before importation of new species to address future conservation problems due to invasive species introduction. Previous studies have demonstrated that fish predation in lentic environments could prevent the establishment of C. fluminea at high densities and could serve as a useful tool in C. fluminea management programs. Our results suggest that A. sturio reintroduction programs may be limited but of value in prevent the establishment of high invasive bivalve densities during early invasion stages. Additionally, this new food items will provide valuable information for the setting of conservation priorities for sturgeon reintroduction plans. To conclude, the vast river network becomes Galician region particularly susceptible to secondary spread processes of freshwater invasive species once introduced. Hence, the invasion risk assessment of new species imported with commercial purposes, establishment of preventive measures and development of more specific legislative instruments may be effective tools to avoid new introductions and slow the spread of existing ones. Present results provide new clues for freshwater basins management regarding their invasion by C. fluminea. Since some rivers from NW Iberian Peninsula presented high calcium levels, our research may help to identify such basins where the colonization by C. fluminea may reveal a potential of invasion. In management terms, since a single individual of C. fluminea can found a new population, its eradication is impossible in most of cases. In this regard, preventive measures are of primary importance. We highlight the importance of collaborating efforts between stakeholders with academic institutions to early detect new invasions and to develop management strategies jointly with decision-makers specifically designed to address the distinctive characteristics of local, small-scale environments, especially when scientific knowledge is limited.