Francisco Sylvester

Dispersion and Ecological Impact of the Invasive Freshwater Bivalve Limnoperna fortunei in the Río de la Plata Watershed and Beyond

Limnoperna fortunei is a freshwater bivalve that invaded South America through Río de la Plata estuary in 1989 and has since become a major macrofouling pest. Along the Paraná-Paraguay waterway, which hosts intense boat traffic, L. fortunei has moved upstream at an average rate of of 250 km per year. In contrast, along the Uruguay river, where boat traffic is restricted to the lowermost 200 km section, upstream colonization is almost 10-times slower. This suggests that attachment to vessels is by far the most important dispersion mechanism. It is suggested that the Amazon, Orinoco and Magdalena basins are under high risk of invasion by this mussel, especially through their estuarine gateways. All South American basins host innumerable water bodies with favorable conditions for L. fortunei’s colonization. Known ecological tolerance limits of the mussel also suggest that it may colonize much of the area from Central America to Canada, including waters that due to their low calcium contents, high temperature and pollution levels, and low oxygen are inadequate for the survival of Dreissena polymorpha. Despite it’s remarkable geographic expansion and its extremely high population densities, L. fortunei’s ecological effects have received very little attention so far. It is suggested that the 2.4-fold increase in Argentine landings of freshwater fish between 1992–1993 and 2000–2001 may be associated with the introduction of this prey species.

Filtration rates of the invasive pest bivalve Limnoperna fortunei as a function of size and temperature

Clearance rates of Limnoperna fortunei (Bivalvia) were investigated in laboratory experiments using monocultures of the alga Chlorella vulgaris. Experimental conditions included two mollusc sizes (15 and 23 mm), and three water temperatures (15, 20 and 25 °C) covering the normal seasonal range in the lower Paraná river and Río de la Plata estuary. Filtration rates obtained were, for the larger mussels: 9.9, 13.1 and 17.7 ml mg tissue dry weight−1 h−1 at 15, 20 and 25 °C, respectively; and for the smaller ones: 17.7, 20.8 and 29.5 ml mg−1 h−1. Differences between sizes and between temperatures (except 15 vs. 20 °C) were statistically significant. In absolute terms larger animals have higher clearance rates, but as a function of body mass smaller individuals feed more actively. Within the range of experimental values used, filtration rates were positively associated with water temperature. These clearance rates (125–350 ml individual−1 h−1) are among the highest reported for suspension feeding bivalves, including the invasive species Dreissena polymorpha, D. bugensis and Corbicula fluminea. High filtration rates, associated with the very high densities of this mollusc in the Paraná watershed (up to over 200,000 ind m−2) suggest that its environmental impact may be swiftly changing ecological conditions in the areas colonized.

The invasive bivalve Limnoperna fortunei enhances benthic invertebrate densities in South American floodplain rivers

We assessed the effects of the introduced bivalve L. fortunei on the abundance and biomass of associated benthic invertebrates in South American large floodplain rivers. The survey was based on comparisons of L. fortunei-covered and L. fortunei-barren areas in five artificial cages from where large predators were excluded, exposed to colonization by the mussel for a total of 17 months in the lower Paraná river delta. Accompanying invertebrates were dominated by Oligochaeta, Nematoda, Rotifera, Copepoda, Gastropoda, Hirudinea, Chironomidae and nauplii. Also present in minor numbers were Tardigrada, Turbellaria, Cladocera, Ostracoda, Insecta, Hydracarina and Decapoda. Dominant invertebrates were 27–100% more numerous (and hosted 43–100% more biomass) in areas with L. fortunei than in areas barren of the mussel. In areas with L. fortunei, total invertebrate biomass (excluding the bivalve) was positively correlated with mussel biomass, and increased with time of exposure under water. No such trend was observed in areas barren of L. fortunei. It is suggested that higher invertebrate growth is associated with enhanced substrate complexity and, probably, the transfer of organic matter from the plankton to the sediments due to the mussels’ feces and pseudofeces. Some of the adverse ecosystem-wide effects of filter-feeding invasive mussels observed in European and North American water bodies may be offset in the Paraná by the extremely high loads of organic matter in these turbid waters.

Genetic Diversity in Introduced Golden Mussel Populations Corresponds to Vector Activity

We explored possible links between vector activity and genetic diversity in introduced populations of Limnoperna fortunei by characterizing the genetic structure in native and introduced ranges in Asia and South America. We surveyed 24 populations: ten in Asia and 14 in South America using the mitochondrial cytochrome c oxidase subunit I (COI) gene, as well as eight polymorphic microsatellite markers. We performed population genetics and phylogenetic analyses to investigate population genetic structure across native and introduced regions. Introduced populations in Asia exhibit higher genetic diversity (H E = 0.667–0.746) than those in South America (H E = 0.519–0.575), suggesting higher introduction effort for the former populations. We observed pronounced geographical structuring in introduced regions, as indicated by both mitochondrial and nuclear markers based on multiple genetic analyses including pairwise ФST, F ST, Bayesian clustering method, and three-dimensional factorial correspondence analyses. Pairwise F ST values within both Asia (F ST = 0.017–0.126, P = 0.000–0.009) and South America (F ST = 0.004–0.107, P = 0.000–0.721) were lower than those between continents (F ST = 0.180–0.319, P = 0.000). Fine-scale genetic structuring was also apparent among introduced populations in both Asia and South America, suggesting either multiple introductions of distinct propagules or strong post-introduction selection and demographic stochasticity. Higher genetic diversity in Asia as compared to South America is likely due to more frequent propagule transfers associated with higher shipping activities between source and donor regions within Asia. This study suggests that the intensity of human-mediated introduction vectors influences patterns of genetic diversity in non-indigenous species.

Nutrient Recycling, Phytoplankton Grazing, and Associated Impacts of Limnoperna fortunei

Laboratory and field experiments indicate that the presence of Limnoperna fortunei decreases concentrations of particulate organic matter and increases ammonia, nitrate, and especially phosphate. Long-term series of field data partially confirm these results. After having been colonized by the mussel, a 47 km2 reservoir developed higher concentrations of ammonia and phosphates, a higher P:N ratio, more transparency, less seston, and less phytoplankton and primary production. Phytoplankton clearance rates by the mussel vary widely, suggesting that “normal” values for adult organisms are around 100 mL/ind./h, or ca. 2–4 mL/mg DW/h. Data on grazing selectivity are inconclusive, but seem to indicate highest impacts on small (< 1 mm) particles. Large plankton are negatively selected, but they may account for greater proportions of total biomass in the diet. Studies on consumption of toxic cyanobacteria yield conflicting results, but large golden mussel populations significantly enhance blooms of colonial Microcystis spp. through changes in nutrient availability, size-selective grazing, promotion of colony formation, and reduced grazing of toxic cells. These toxic blooms, in turn, suppress reproduction of the mussel, most probably killing the larvae. Growth of periphyton and aquatic macrophytes are enhanced significantly by the golden mussel.

Relationships of Limnoperna Fortunei with Benthic Animals

Similar to other invasive bivalves, Limnoperna fortunei has a variety of effects on other benthic animals. These effects have been studied in the Parana-Paraguay-Uruguay river system, Rio de la Plata estuary, and in the reservoir Embalse Rio Tercero since the invasion of South America by the bivalve. The bulk of information accumulated indicates that L. fortunei has predominantly positive effects on meiofaunal groups. Increases in the abundance, biomass, and richness of many groups are attributed to substrate enrichment from the bivalve’s feces and pseudofeces as well as refugia provision amid the valves. Nonetheless, negative impacts on some groups (gastropods) and the homogenization of benthic fauna following colonization by the mussel have also been reported. Large-sized invertebrates can also be detrimentally affected by this mussel’s biofouling, as severe cases of epifaunal growth have been reported for native crabs and mussels, including the invasive clam Corbicula fluminea. However, consequences to affected individuals and impacts at the population level have not yet been assessed. A variety of animals, including fish, crabs, turtles, waterfowl, and some mammals, may benefit from predation on this new abundant prey item, although the consequences to predator populations remain unstudied. Despite marked similarities with Dreissena polymorpha, there are a number of differences regarding the effects of the two bivalves arising from differences in their biology and ambient dissimilarities between their respective environments. The extrapolation of results obtained for Dreissena species, abundant in the L. fortunei literature, can be misleading due to these differences.

Reproductive Output and Seasonality of Limnoperna fortunei

Young Limnoperna fortunei mature sexually from 5–6 to ~15 mm. The species is generally dioecious, with approximately equal numbers of males and females and very small (< 0.6 %) proportions of hermaphrodites. The gametogenic cycle has been described for both Asian and South American populations, recognizing between four and five reproductive phases. Gonadal cycles based on histological sections yielded somewhat dissimilar results for different areas. In Hong Kong, two yearly peaks in reproductive output were detected. In South America, mature sperm and ova have been recorded year round and several irregularly spaced spawning events have been observed, as well as more or less continuous breeding punctuated by peaks in spring and at the end of the summer. Reproductive studies based on changes in the abundance of larvae in the water column have been carried out in South America and in Japan. In tropical and subtropical South America, larval output is more or less continuous for 6–10 months of the year, often with a major peak in spring–early summer, and a smaller one in the late summer–autumn. In Japan, at considerably lower water temperatures, larval production is limited to 1–2 months centered around summer. Apparent disagreements between results based on histological data and on larval counts stem from the fact that while the latter integrate the reproductive output of extensive mussel beds dispersed over large areas, histological evidence pinpoints with high precision the ripening and spawning of isolated mussel clusters. Aside from water temperature, several other factors (pH, salinity, dissolved oxygen, suspended solids, chlorophyll a, flood–drought cycles) have been proposed as reproductive triggers, but actual associations have not been demonstrated. Peak larval densities can exceed 20,000 ind./m3, but, normally, values range around 6000 ind./m3, showing major fluctuations within short periods, as well as changes as a function of time elapsed post colonization, and availability of substrata suitable for adult occupation. Microcystin-producing cyanobacterial blooms can kill L. fortunei larvae.