Limnoperna siamensis, Limnoperna lacustris

Habitat
The climate in Limnoperna fortunei’s native range is humid subtropical, with warm summers and no dry season (Darrigran and Damborenea 2005). L. fortunei is able to inhabit a variety of aquatic habitats (i.e. lakes, rivers, streams) but requires a hard substrate for byssal attachment, though it can attach to aquatic plants. However, it can also attach to soft substrates if it is sufficiently compacted (Boltovskoy et al. 2006). L. fortunei has a wide environmental tolerance: see the table below for a description of physiological tolerances.

The mussel can survive (90%) up to a salinity shock of 2 ppt for periods of at least 10 days (Angonesi et al. 2008). This species overwinters in South Korea, with water temperatures as low as 0°C (Oliveira et al. 2010). In Japan, the minimum temperature in a reservoir with mussels was 4.2°C (Nakano et al. 2011). Experimental research supports the 5°C threshold for prolonged exposure (Oliveira et al. 2010). Experiments to examine L. fortunei overwintering survival found that populations at the northern invasion front can survive 6 days, 41 days, and 108 days at <1°C, <2°C, and <5°C respectively. Overall survival was 27% at these temperatures. An accompanying species distribution model implies suitable habitats at higher latitudes than previously considered (Xia et al. 2021). Compared to the zebra mussel Dreissena polymorpha, Limnoperna fortunei has higher resistance to anoxia, pollution (including eutrophication), pH, and high temperatures, longer reproduction periods and lower calcium requirements (3-4mg/L) (Karatayev et al. 2007). This broader tolerance indicates this species could have an even broader distribution in the Great Lakes than D. polymorpha, except for depth as zebra mussels can inhabit depths up to 50 meters while L. fortunei has been noted to inhabit depths of 0.5 to 40 meters with an optimum depth of 10 meters (Darrigran 2022).

Food Web
Limnoperna fortunei consumes a variety of phytoplankton and zooplankton (Rojas Molina et al. 2010, Rojas Molina et al. 2012, Frau et al. 2012). Adults do well despite low food availability (Oliveira et al. 2011). This species negatively affects burrowing invertebrates and unionids (Karatayev et al. 2010) in South America, and may do the same in the Great Lakes given its high densities, such competitive exclusion is also seen in a similar species, the zebra mussel Dreissena polymorpha. L. fortunei modifies nutrient concentrations and proportions, and promotes aggregation of solitary Microcystis spp. cells into colonies; both these effects can favor blooms of this often noxious cyanobacteria (Cataldo et al. 2012).

Limnoperna fortunei negatively impacts zooplankton, and part of zooplankton decline may be due to starvation (i.e., mussel outcompetes zooplankton for food resources) (Rojas Molina et al. 2012). Limnoperna fortunei has increased food availability in the benthic zone, which in part has increased invertebrate (excluding mussels) density 1.9 to 22 times and biomass 1.7 to 19 times (Burlakova et al. 2012). Limnoperna fortunei has homogenized benthic communities (Darrigran and Damborenea 2011, Sardiña et al. 2011); e.g., in one study 99.9% of community biomass consisted of the filtering collector trophic group (Burlakova et al. 2012). Limnoperna fortunei has shunted the dominant nutrient cycling from the pelagic to the benthic zone (Darrigran and Damborenea 2011, Cataldo et al. 2012, Rojas Molina 2012). Limnoperna fortunei has significantly reduced phytoplankton densities (>60%) and changed composition of the algae assemblages, most notably an increase in the flagellate group, relative to the diatom, single-celled and colonial groups (Frau et al. 2012).

Limnoperna fortunei filters water substantially faster than D. polymorpha (Karatayev et al. 2010). Limnoperna fortunei brings increases in water transparency, and a decrease in suspended matter, chlorophyll a, and primary production (Boltovskoy et al. 2009). It also brings a decrease in turbidity and an increase in dissolved nitrogen in mussel presence (Rojas Molina 2012). Increased habitat complexity led to significant (e.g., threefold) increase in community taxonomic richness. Shells increase surface area for settling organisms, and also provide refuges from predation and physical stressors (Darrigran et al. 1998, Darrigran and Damborenea 2011, Burlakova et al. 2012, Spaccesi and Capitulo 2012). This species transforms sand or mostly bare sediment into reef-like druses (Burlakova et al. 2012).

Life History
Limnoperna fortunei requires external fertilization to reproduce and is considered a dioecious spawner with an equal ratio of males to females (Darrigran 2022). After fertilization, the oocyte develops into the first trochophore stage after six hours. This is the first active larval stage and at this point these larvae are capable of coordinated swimming and disperse in the water column. Larvae then develop into the veliger stages where the shell begins to form and they begin to consume plankton. External fertilization and the development of planktonic larvae support the rapid spread of golden mussel (Boltovskoy et al. 2015), similar to other successful invaders in the Great Lakes (i.e. Dreissena polymorpha and D. bugensis). The veliger larvae gradually transition into a plantigrade stage, at this stage movement becomes restricted and an adhesive foot is formed. The plantigrade stage involves exploration for suitable substrate and ends with the attachment of byssal threads. Once byssal attachment is complete, the larvae develop into juveniles and remain in place through adulthood (Boltovskoy 2015).

No data was found on natural Limnoperna fortunei fecundity, though very high rates of colonization suggest it is high (Karatayev et al. 2007). L. fortunei can reach densities of 5000-250,000 individuals/m² on hard substrate, and 90-2000 individuals/m² on soft substrate (Frau et al. 2012). Analysis of a L. fortunei population in Brazil found a high annual growth rate (K = 1.22) and estimated that 62.920 juveniles/m² will be recruited annually (Ayroza et al. 2021). L. fortunei spawns continually in suitable conditions, as opposed to batch spawning that is observed in similar species (i.e. zebra mussel) (Boltovskoy et al. 2006).

Limnoperna fortunei has a moderate probability of introduction to the Great Lakes (Confidence level: High).

Potential pathway(s) of introduction: Transoceanic Shipping

Limnoperna fortunei has a high tolerance to fluctuating salinities; no significant mortality was observed in mussels exposed to a salinity cycle with abrupt salinity changes ranging 1–23% (mean 2.68%) over a month (Sylvester et al. 2013). This will affect the probability of uptake (many ports located in estuarine environments with fluctuating salinity) and survival after ballast exchange (Sylvester et al. 2013). Though tolerance of larvae has not been specifically examined, larval survival is likely due to presence of colonies in saline regions (unlikely formed by drifting adults) (Sylvester et al. 2013). Ship traffic to the Great Lakes includes areas already invaded by L. fortunei, such as South America and Asia (Boltovskoy 2015, EPA 2015). While ship traffic from these regions is not frequent, the potential for introduction exists.

Limnoperna fortunei has a High probability of establishment if introduced to the Great Lakes (Confidence level: High).

Limnoperna fortunei is already found in regions with climates similar to the Great Lakes, and shows the ability to survive overwinter in temperatures as low as 0°C. L. fortunei consumes a variety of phytoplankton and zooplankton, making it able to adjust its diet based on prey availability in the Great Lakes if introduced.

The native and introduced ranges of Limnoperna fortunei include extremes of pollution, water temperature, pH, and nutrient levels, making it able to adapt to the many microhabitats throughout the Great Lakes. L. fortunei attaches well to hard substrate (including of biological origin), macrophytes and reeds (Karatayev et al. 2007), and plastic bottles (Karatayev et al. 2010). L. fortunei attaches minimally to soft substrate, but can attach if the substrate is sufficiently compacted (Boltovskoy et al. 2006).

Summary of species impacts derived from literature review. Click on an icon to find out more...

Environmental	Socioeconomic	Beneficial

Limnoperna fortunei is an ecosystem engineer that significantly alters invaded habitats by altering habitat complexity, sedimentation, and accelerating eutrophication (Burlakova et al. 2012, Tokumon et al. 2018, Gattas et al. 2020). L. fortunei reach large densities (5000-250,000 individuals/m² on hard substrate, and 90-2000 individuals/m² on soft substrate; Frau et al. 2012) shifting productivity in the nutrient cycle from the pelagic zone to the benthic zone. This species filters water quickly, clarifying water causing a reduction in primary production occurring within the water column. Nutrient concentrations and proportion are shifted to promote aggregation of solitary Microcystis spp. cells; this favors blooms of the noxious cyanobacteria (Cataldo et al. 2012). L. fortunei bioaccumulates heavy metals and pesticides and may facilitate the transfer of these substances to existing fauna (Besen and Marengoni 2021, Sene et al. 2021).

Limnoperna fortunei has been shown to physically foul living unionids and naiads through settlement on their shells. This impairs movement and restricts their ability to open their valves, thus depriving them of food and oxygen (Darrigan and Damborenea 2005, Weigand 2019). This species also significantly impacts benthic fauna, with changes in invertebrate and plankton abundance well-documented (Rojas Molina et al. 2012, Frau et al. 2012, Bertao et al. 2021, Silva et al. 2021).

Limnoperna fortunei has the potential for high socio-economic impact if introduced to the Great Lakes.

Limnoperna fortunei can clog/foul water intake sieves and filters, pipes, heat exchangers, and condensers. This species has become a common difficulty for industrial and power plants that use raw water, chiefly for cooling purposes (Cataldo et al. 2003, Goto 2002, Boltovskoy et al. 2009). Their biofouling leads to increased abrasive wear and significant economic costs for their cleaning and maintenance (Yao et al. 2017, de Castro et al. 2019, Boltovskoy et al. 2022). L. fortunei biofouls 38% of the hydropower plants in Brazil and is responsible for estimated annual losses of 120 million dollars (US$) (SPIC Brasil 2021).

Limnoperna fortunei modifies nutrient concentrations and proportions, and promotes aggregation of solitary Microcystis spp. cells into colonies; both these effects can favor blooms of this often noxious cyanobacteria (Cataldo et al. 2012). Gazulha et al. (2012) found that while single cells of cyanobacteria were accepted, filamentous and colonial cyanobacteria were rejected as pseudofeces. L. fortunei has been shown to increase the growth of Microcystis spp. through the alteration of P:N ratios, selective grazing, competitor exclusion, and increasing nutrient supply (Boltovskoy et al. 2017, Silva and Giani 2018, Gangi et al. 2020).

The current solutions implemented in the Great Lakes to control dreissenid mussels are expected to be effective against Limnoperna fortunei. As such, there are many control measures in place to mitigate socio-economic impact from golden mussel invasion. The potential for increased impacts exists if L. fortunei is resistant to existing control measures or able to occupy areas where dreissenids are excluded due to their increased physiological tolerances.

Limnoperna fortunei has the potential for high beneficial impact if introduced to the Great Lakes.

In its invasive range outside the Great Lakes, Limnoperna fortunei has had similar impacts to Dreissena polymorpha, i.e., has led to a dramatic shift in the benthic trophic structure and a homogenization of freshwater communities, regardless of original substrate and community structure (Burlakova et al. 2012, Darrigran and Damborenea 2011, Sardiña et al. 2011). Also, this species has led to an increase in water transparency, a decrease in suspended matter, chlorophyll a, and primary production (Boltovskoy et al. 2009). L. fortunei promotes glyphosate degradation and reduces the concentration of herbicides in freshwater systems (Di Fiori et al. 2012, Vargas et al. 2019). The structure of functional feeding groups in the new community, including invasive bivalves, is overwhelmingly dominated by collectors-filterers (Burlakova et al. 2012). Predictive models for the Lake Erie food web suggest Limnoperna fortunei will positively impact piscivores, most omnivores (except juvenile yellow perch), and most benthic invertebrates (except dreissenids), negative effects are predicted for planktivores and plankton (Zhang et al. 2019).

Introduction of Limnoperna fortunei into habitats outside of its native range provided a new food resource to be exploited by the fish community. This species has become an important food resource for native fish, including those of commercial value (Paolucci et al. 2017, de Ávila-Simas et al. 2019, Gonzalez-Bergonzoni et al. 2020). An increase in mussel densities have been associated with a threefold increase in Argentina's freshwater fish landings in the Rio do la Plata basin after 1995, due to its status as a new, abundant food source (Boltovskoy et al. 2006). Positive impacts of L. fortunei are not limited to fishes that directly consume mussels, but there are also indirect positive effects on ichthyophagous and detritivorous fish species. See Burlakova et al. (2023) for a comprehensive review of ecosystem services provided by L. fortunei.

Parallels with the Dreissena polymorpha highlight several important differences, including Limnoperna fortunei’s higher resistance to anoxia, pollution, pH, and high temperatures, longer reproduction periods and lower calcium requirements (Karatayev et al. 2007), suggesting that, should L. fortunei reach North America or Europe, it will become an even more aggressive invader, especially in regions dominated by acidic, soft and contaminated waters (Boltovskoy et al. 2009). L. fortunei, given its enhanced physiological tolerances, has the potential to displace D. polymorpha in nearshore areas if introduced to the Great Lakes.

It is illegal to import, possess, deposit, release, transport, breed/grow, buy, sell, lease or trade L. fortunei in Ontario (Invasive Species Act 2015). Ohio lists L. fortunei as an injurious aquatic invasive species and therefore it is unlawful for any person to possess, import, or sell live individuals within the state. Dead golden mussels can only be possessed in Ohio if they are preserved in ethanol or formaldehyde, or eviscerated (internal organs removed) (OH ADM. Code, 1501:31-18-01).  In Michigan, it is illegal to possess, import, sell, or offer to sell L. fortunei (NREPA Part 413 as amended, MCL 324.41302). Illinois lists L. fortunei as an injurious species as defined by 50 CFR 16.11-15. Therefore, L. fortunei cannot be possessed, propagated, bought, sold, bartered or offered to be bought, sold, bartered, transported, traded, transferred or loaned to any other person or institution unless a permit is first obtained from the Department of Natural Resources. Illinois also prohibits the release of any injurious species, including L.fortunei (17 ILL. ADM. CODE, Chapter 1, Sec. 805). It is prohibited to transport, possess, or introduce L. fortunei in Wisconsin (Wisconsin Chapter NR 40). There are no regulations on L. fortunei in Minnesota, Indiana, Pennsylvania, or New York.

Note: Check federal, state, and local regulations for the most up-to-date information.

Control

Biological

Previous studies conducted in South America have shown that L. fortunei was prominent in the diet of several species of native fish (Oliveira et al. 2010; Isaac et al. 2012). The ability of native predators to adapt to exotic prey is not uncommon (Carlsson et al. 2009; Oliveira et al. 2010; Isaac et al. 2012). Given the physical similarities between dreissenid mussels and L. fortunei it is likely that predators of Dreissena spp. would also feed on L. fortunei if it were to become established in the Great Lakes. Dreissenid predators such as Freshwater drum (Aplodinotus grunniens), Common carp (Cyprinus carpio), Round goby (Neogobius melanostomus), Pumpkinseed (Lepomis gibbosus), Lake whitefish (Coregonus clupeaformis), Channel catfish (Ictalurus punctatus), and Diving duck (Aythya spp.), which are common in Great Lakes coastal wetlands (Herdendorf 1987, Bookhout et al. 1989, Johnson 1989 in Bowers and de Szalay 2007) could potentially reduce population densities of L. fortunei. However, predation by species maladapted to digest L. fortunei could also aid in its dispersal. Oliveira et al. (2010) found intact mollusks in several fish species suggesting that the mollusks could not be digested and therefore could be passed through alive.

The use of biocides to control L. fortunei has been examined. The commercial biocide Bulab 6002®, a quaternary ammonium polymer, rendered all L. fortunei larvae inactive after 24 hours at low concentrations (1 mg/L). This biocide may be effective in preventing larval settlement since inactive larvae do not secrete the byssus necessary to attach to substrate (Darrigran et al. 2007).  The use of the bacterium Pseudomonas flourescens CL145A, commercially known as Zequanox®, is highly lethal to dreissenid mussels and can affect L. fortunei (GLMRIS 2012; Rackl et al., 2012).

Physical

Physical control methods for Dreissena polymorpha could be implemented for L. fortunei control. These methods include thermal treatments, mechanical filtration, mechanical cleaning (scraping, brushing, and pigging), high-pressure jet cleaning, carbon dioxide pellet blasting, freezing, desiccation, acoustics, electric fields and UV light (Boelman et al. 1997). The tolerance of L. fortunei to desiccation is pertinent to the control of this species. One study found that golden mussels exposed to air without humidity control (49 to 63% relative humidity) did not survive more than 120 hours whereas mussels in more humid environments survived up to 168 hours. Therefore, desiccation is a viable option to reduce biofouling but water must be periodically removed for at least six days and this should be accompanied by procedures to reduce the relative humidity of the environment (Darrigran et al. 2004). High frequency turbulent flow (>30 Hz) is an effective way of killing L. fortunei veligers, but the energy required to create this turbulence may restrict its practical application (Xu et al. 2015).

Chemical

Chemical treatments such as chlorination or the use of commercial, non-oxidizing molluscicides can be effective against L. fortunei but water temperature and concentration can affect the efficiency of these chemical agents (Cataldo et al. 2008). The life stage of the mussels often dictates the control strategy. Targeting juveniles (5-8 mm in size) is often the most effective strategy because they are less tolerant than adults (thus requiring lower toxicant concentrations and exposure times), they detach more readily from surfaces, and they do not require continuous application throughout the reproductive period as do planktonic larvae.  It is beneficial to prevent juveniles from reaching the next stage because adults can form dense mats and significantly impact water flow. Therefore, in order to maximize the overall effectiveness of these treatments while minimizing environmental impact it is imperative to understand the timing of reproduction of L. fortunei (Boltovskoy et al. 2009).  Limnoperna begin reproducing in spring and cease reproducing in fall at temperatures around 16-17 °C, providing an extended period of reproduction in warm ecosystems. The mussels are dioecious and reproduce via external fertilization. Larvae undergo several pelagic development stages before settling and attaching to the substrate 11-20 days after spawning (Cataldo et al. 2005)

Other

Xu et al. (2015) studied the effectiveness of an ecological integrated approach to control L. fortunei biofouling in water transfer tunnels. The authors developed a prevention pool that aimed at reducing living veligers entering and attaching onto a water transfer tunnel. In the experiment water entered through a fore bay and into the pool that consisted of three attachment sections. The first two sections consisted of bamboo rafts that served as suitable material for mussel attachment and the third section contained geotextile frames used to absorb veligers that were not capable of stable attachment to the bamboo. In order to limit the mussel density in the bamboo sections these areas were filled with predators of L. fortunei: Carassius auratus (Common name: Goldfish) and Channa argus (Common name: Northern snakehead). Pipes in the end section of the prevention pool created high frequency turbulent flows as a final measure to guarantee the reduction of living veligers. The authors noted that the use of the predatory fish played an important role in restraining the attachment density and shell length of the golden mussel in the prevention pool. The experiment yielded an 80% reduction rate of living veligers in water that passed through the pool and a sharp decrease in mussel attachment density was observed as distance from the pool entrance increased. This method was tested at a pump station on the Xizhijiang River in China where the construction of an integrated ecological prevention pool yielded an 80% reduction in attachment density from 2012 to 2013. Using prevention pools on water intake structures in the Great Lakes could be an effective way to reduce biofouling, but the use of the Carassius auratus and Channa argus is not preferable since these species are not indigenous to the basin.

Note: Check state and local regulations for the most up-to-date information regarding permits for pesticide/herbicide/piscicide/insecticide use.