L. fortunei is an epifaunal mytilid, native to Chinese and south-eastern Asian rivers and creeks. It became established in Hong Kong in 1965 and in Japan and Taiwan in the 1990s. In 1991, it invaded America throu...
L. fortunei is an epifaunal mytilid, native to Chinese and south-eastern Asian rivers and creeks. It became established in Hong Kong in 1965 and in Japan and Taiwan in the 1990s. In 1991, it invaded America through the Plata basin (Río de la Plata, Argentina, South America). It spreads up stream in the main rivers of the Plata basin (240 km/year), using different vectors (e.g. commercial and tourist ships, fixed to nets, buoys). It has several invasive characteristics such as gregariousness, rapid growth, short life span; it has a planktonic larval stage, and great adaptive and reproductive capacity. It modifies the presence and abundance of native macro invertebrate fauna, fish diets, and their high filtration rates cause environmental impact, changing ecological conditions in the areas colonized. It causes great economic damage to water intakes and cooling systems.
L. fortunei is listed as an invasive species in ISSG and other databases.
The generic name Limnoperna Rochebrune 1888 was erected to distinguish this monotypic genus from the other mytilids. Limnoperna fortunei has been cited under a variety of names (Morton, 1973; Ricciardi, 1998). One species and its subspecies of the genus Limnoperna was recognized from Japan: Limnoperna fortunei fortunei (Dunker, 1857) and Limnoperna fortunei kikuchii Habe, 1981 (Habe, 1981). Kimura et al. (1999) confirmed that L. fortunei kikuchii isa synonym of Xenostrobus securis Lamarck, 1819.
L. fortunei is a bivalve mollusc that belongs to the Mytilidae. Adult L. fortunei are sessile and are generally found in clumps on hard substrates.
The shells of adult L. fortunei are equivalve and heteromyarian. It is dark-brown above the umbonal keel and paler yellow-brown below.This is caused by the nacre of the interior of the shell being purple above and white below the keel. The presence of a nacreous layer in L. fortunei removes this genus from all contact with Dreissenacea.
The outer periostracal layer of the shell is smooth and shiny, and thick where it curls inwards at the shell margin. The umbones are very nearly terminal and the dorsal ligamental margin is straight or, at most, only slightly curved. The ventral margin of the shell is the most variable feature and in different specimens varied between the two extremes of being either straight or distinctly arcuate. There are no hinge teeth or byssal notches.
The shells are yellow-brown. In clear water, for example in northern Argentina, they look golden; so it is called the ‘golden mussel’.
Its longevity is variable. In the natural environment of Bagliardi Beach, Argentina, longevity was recorded as 3.2 years (Maroñas et al., 2003). Boltovskoy and Cataldo (1999) estimated it as 3 years in Cuenca del Plata, Argentina. Iwasaki and Uryu (1998) suggested a longevity of 2 years in the Uji River, Japan, from 4 to 5 years in Korea and over 10 years in central China.
It is dioecious and reaches sexual maturity in the first year of its life span. Spawning occurs at temperatures of 16-28°C. After spawning and fertilization, the trocophore is the first planktonic stage. Several stages of free-swimming planktonic veliger (D-larvae about 7 days, between 80 and 146 mm; veliconcha between 90 and 237 mm and pediveliger or umbonate, more than 256 mm). Then the larvae settle as plantigrade mussels and attach to the substrate as juveniles. These larvae are free-swimming and planktonic and live in the water column. These stages of the mussel’s life cycle are the most vulnerable to environmental fluctuations.
The larvae settle to the bottom and securely attach to a hard substrate by byssal threads, which are secreted from a gland at the base of the mussel’s muscular foot.
L. fortunei are epifaunal, unlike most other South American native freshwater bivalves, and not overly selective, therefore they colonize almost any solid, submerged surface such as buoys, water intake pipes, rocks, rooted aquatic plants, boat hulls, and the shells of other molluscs. Its eurioic status allows a quick and effective distribution in water bodies. The juveniles differentiate into males and females; with lengths of 5 mm in the spring and 9 mm in the summer, and can reach sexual maturity after 6 mm total length (Darrigran et al., 2003).
L. fortunei is a freshwater mytilid of South East Asia; native to China, and also found in Laos, Cambodia, Vietnam, Indonesia and Thailand (Oliveira et al., 2006), typically found in freshwater systems; both rivers and lakes.
This species has been found in Hong Kong, Taiwan and Japan. In South America it is found in the Plata Basin and Guaiba Basin:
The distribution in this summary table is based on all the information available. When several references are cited, they may give conflicting information on the status. Further details may be available for individual references in the Distribution Table Details section which can be selected by going to Generate Report.
Morton (1975) first recorded it in Hong Kong where it had been introduced from China via supplied potable water. The species has been recorded in Taiwan, fouling potable water supply systems (Tan et al.,1987). In Japan, L. fortunei was first recorded in the ancient Lake Biwa in 1991 (Kimura, 1994) and has subsequently invaded associated potable water treatment systems (Nakai, 1995). It was first recorded in South America in the 1990s (Pastorino et al., 1993).
L. fortunei was first found in South America in 1991 at Bagliardi Beach (Argentina) (Pastorino et al., 1993). In 1994 and 1995, it was found in water intakes of Bernal town (Museo de La Plata Collection) and Retiro, and in Buenos Aires Harbour. Sacarabino and Verde (1994) reported presence of the species in the town of Colonia Sacramento, Uruguay. All these localities are on the Río de la Plata Estuary.
The species has expanded up through the Paraná River. During 1996, the species spread to the town of Goya (29º10’S-59º16’W), in Corrientes Province (Di Persia and Bonetto, 1997), and was collected in the middle Paraná River, near the city of Santa Fe, where the river has a very wide alluvial plain. L. fortunei was first collected in Paraná River, at Vuelta del Este, Zárate, on the Paraná de las Palmas River, and at Paso Burghi, city of Rosario, on the lower Paraná River toward the end of 1995. It was found in the main channel, on the left bank at the town of Paraná and associated alluvial plain, in San Javier and Correntoso rivers, near the city of Santa Fe. It was also found on the right bank of the lower Salado del Norte River in the town of Santo Tomé (31º40’S-60º45’W). In 1996, this species was collected from “fouling” samples in Cerrito Island (27º20’S-58º43’W) near the confluence of the Paraguay and Paraná rivers.
The dispersion continued along the Paraguay River. In April 1997, it was collected in Asuncion Harbour (25º17’S-57º38’W). In 1998, L. fortunei was observed for the first time in Mato Grosso do Sul State, Brazil, in samples taken from the bottom of a lake, connected to the Paraguay River, called ‘baia do Tuiuiu´ ’ (18º49’S-57º39’W), next to the city of Corumbá. In January of 1999, L. fortunei was found in the Paraguay River in the vicinity of Forte Coimbra (19º53’S-57º46’W) and in the northern part of the Paraguay River, in the vicinity of Bela Vista do Norte (17º38’S-57º41W). Limnoperna has also been found in Castelo Lake (18º34’S-57º34’W) and the Tamengo Channel (10º59’S-57º40’W) Mato Grosso, Brazil (Oliveira et al., 2006).
The species is found throughout the Paraná River. It was collected during the last month of 1998, at Posadas Harbour, on the upper Paraná River, and in the Itaipú Reservoir in April of 2001 (Zanella and Marenda, 2002). In November 2002, it was found in Paranapanema River, near Rosana City, (22°31’S-53°00’W) Sao Paulo State, Brazil (Avelar et al., 2004). Other records for that region are: in August 2004, Río Paranaíba, Porto Alencastro (19º39’S-55º08’W), junction of Paranaíba and Claro rivers (19º19’S-50º50’W) and the Paranaíba and Verde rivers (19º11’S-50º08’W) (Campos et al., 2005).
In Brazil, the invasion of L. fortunei has also been documented in the Guaíba Lake Basin, in the state of Rio Grande do Sul in 1999 (Mansur et al., 1999). In November 1998, it was detected in Brazil on Itapua Beach, Rio Grande do Sul State. In January 1999, in Guaíba Lake, near Strait of Itapuã, which communicates with Lagoa dos Patos (Mansur et al., 1999). Then it was found in Arambaré (30º54’S-51º30’W), Lagoa dos Patos. In 2001, it was found in São Lourenço River (31º20’S-51º58’W) and in Logoa dos Patos, near its junction with the Atlantic Ocean (Capítole and Benvenuti, 2004), Rio Grande city and the San Gonzalo channel.
In Uruguay, the species has been recorded in five of the six main hydrographical basins: Río de la Plata, Santa Lucía, Negro and Uruguay rivers (Scarabino and Verde, 1994; Brugnoli et al., 2005) and recently in the Merín Lagoon and Río Branco River (Langone, 2005).
In 2001, the L. fortunei was detected at the Salto Grande Hydroelectric Power Plant (Argentina-Uruguay), in the Uruguay River (Leites and Bellagamba, 2002). The most northerly location where L. fortunei has been found is Monte Caseros, Corrientes Province (G Darrigran, personal communication, Facultad Ciencias Naturales y Museo, Argentina, 2008).
Darrigran and Pastorino (1995) proposed the non-intentional introduction of L. fortunei into the Río de la Plata, through ballast water of ocean vessels
At present the pathways are under study. Up to now, the main identified pathway is the commercial trade in the big rivers of the Plata basin (Paraná and <_st13a_country-region _w3a_st="on">Paraguay rivers), and the tourist/sporting activities in the <_st13a_place _w3a_st="on">Uruguay River (Darrigran, 2002). There are no governmental controls of the pathways.
In South America, L. fortunei first occupied environments with freshwater temperatures of 14-24ºC. At a later stage it invaded areas with shorter winters and temperatures of 15-33ºC. It can also inhabit brackish waters (salinity <3 ppt), and tolerates pH values of 6.2-7.4 and calcium ion concentrations of 3.96 mg/L (Darrigran, 2002). The species needs hard substrates to attach to with byssal threads.
The genetic studies of L. fortunei are scarce. Kimura et al. (2003) carried out comparative genetic studies of L. fortunei from native and invaded localities. The results show that characteristics of morphology and isozymes of specimens collected from mainland China were similar to those from Japan rather than to those from Argentina. These differences might be explained by one or two alternative scenarios: the difference may simply reflect genetic characteristics of their provenance or may be generated due to a bottleneck effect at each country. DNA damage and repair in the haemolymph cells of L. fortunei exposed to environmental contaminants was reported. The results suggest L. fortunei is a potential biomonitor organism (Vianna Villela et al., 2006).
Boeger et al. (2007) tested a molecular method to detect larvae of L. fortunei in plankton samples. This method promises to become an important way to monitor the expansion of L. fortunei populations.
Reproductive Biology
L. fortunei is a dioecious spawner, and exhibits an equal ratio of males to females. After external fertilization, planktonic larvae live for several weeks before settling and attaching to a hard substrate. Optimal conditions for spawning occur when water temperature reaches 18°C. Morton (1982) studied a population from Hong Kong, where the spawning takes place between May and June, and from November to December.
In South America, Darrigran et al. (1999) studied the reproductive biology of L. fortunei in temperate areas, for the first time. This study differentiated numerous spawning events (five were recorded), many of them of low magnitude. Darrigran et al. (2003) carried out another reproductive study, after 10 years of settlement in America. The observed pattern was similar to the one described by Morton (1982). Only two major spawnings were observed through the year; one when summer temperature was recorded and the other with spring temperatures. A small winter spawning was also observed.
Santos and Mansur (2002) suggested that L. fortunei populations in the Gauíba Lake (a subtropical area in Brazil) have the ability to reproduce all year, with a peak in spring.
Nutrition
L. fortunei filters a wide range of particles, such as algae, zooplankton and organic matter. The larval stages feed on bacteria.
Associations
Associations between L. fortunei and other species have not been described. In South America, there are no records of L. fortunei as a vector of symbiotic organisms (commensals or parasites).
Environmental Requirements
L. fortunei inhabits rivers, streams, lakes, dams and estuaries. In Asia, it is found between 8-32°C, with confirmed occurrences up to 35°C. In South America, in a temperate area, Limnoperna populations can develop between 11 and 28ºC (approximately) (Darrigran et al., 2003). In a subtropical area, the reported temperatures are 17-29ºC (Mansur et al., 2004). It is intolerant to extended anaerobic conditions. Mansur et al. (2004) reported the pH tolerance range of 5.8-9.3. L. fortunei is a freshwater species that can inhabit brackish waters and maintain substantial populations in estuarine habitats. It is tolerant to polluted and contaminated waters with low calcium and pH levels.
There are no records of natural enemies in its native area. In the introduced area, enemies include the following species of fishes: Leporinus obtusidens; Schizodon borellii; Piaractus mesopotámicus; Pterodoras granulosus; Rhinodoras dorbignyi; Oxydoras kneri; Pimelodus maculatus; Pimelodus albicans; Pimelodus argenteus; Brochiloricaria chauliodon; Hypostomus laplatae; Hypostomus uruguayensis; Paraloricaria vetula; Megalancystrus parananus; Pseudohemiodon laticeps; Cyprinus carpio; Potamotrygon brachyurus; Micropogonias furnieri (García and Montalto, 2006).
Cesar et al. (2003) described the predation of L. fortunei by the blue crab, Callinectes sapidus in Rio de la Plata Estuary.
The natural dispersal of L. fortunei is passive, and occurs as veliger larvae that are passively transported from colonized areas through connected streams. The natural dispersal is downstream and dependent on water currents.
Vector Transmission (Biotic)
There is little information about biotic vector transmission. The specimens could be eaten and carried in the gut of fishes (Belz, 2006) birds, etc.
Accidental Introduction L. fortunei has been accidentally introduced in South America. Darrigran and Pastorino (1995) proposed the non-intentional introduction of L. fortunei into the Río de la Plata in 1991, through ballast water of ocean vessels. At that time an increase of trade between Argentina and two countries that L. fortunei inhabits occurred. In Guaíba Basin, it was also probably introduced via ballast water (Mansur et al., 1999) and in the Itaipu reservoir (Zanella and Marenda, 2002) probably via boats used for sport.
In South America, the identified vectors are commercial and sport ships and boats, live bait, nets, and buoys that spread the species through the basin. Other vectors are the trucks that transport sand from an invaded beach to other areas (Darrigran, 2002; Belz, 2006).
Magara et al. (2001) proposed that L. fortunei arrived in Japan before 1987 possibly with the Asian clam imported as food from mainland China.
Freshwater macrofouling is a new economic/environmental problem for South America. Until the beginning of the 1990s, macrofouling in the neotropical region occurred only in marine and mixohaline waters. Since the introduction of L. fortunei, macrofouling also extended to freshwaters in Argentina, Brazil, Paraguay and Uruguay (Darrigran and Damborenea, 2005). This kind of problem (freshwater macrofouling) is caused by the appearance of larvae or juveniles of L. fortunei. It impacts the sources of water supply of many water-treatment plants, industrial refrigeration systems, and power stations. Among the usual problems involved, the following are the most significant: pipe obstruction; reduction in flow velocity in pipes due to friction loss (turbulent flows); accumulation of empty valves and pollution of water ways by massive mortality; filter occlusion; and increase in the corrosion of surfaces due to mussel infestation. This new economical and environmental problem for the neotropical regions produces unexpected expenses, for example, due to system shutdowns, the need for chemical or mechanical cleaning, and pipe and filter replacement.
The large biomass associated with high densities of L. fortunei impacts on aquatic food chains. Several species of native fish consume L. fortunei (López Armengol and Casciotta, 1998; Montalto et al., 1999) and it has become the main food source for Leporinus obtusidens (Anostomidea) in the Río de la Plata (Penchaszadeh et al., 2000).
However, many other aspects of the biology of L. fortunei are poorly understood (Sylvester et al., 2005), including its filtering capacity. Because of its high density in the Plata basin, L. fortunei could increase water clarity in a manner similar to that caused by Dreissena polymorpha in North America (Darrigran and Damborenea, 2005).
Impact on Biodiversity
The impact caused by L. fortunei it is not restricted to the economic aspect. Darrigran et al. (1998) showed that since the introduction of L. fortunei at Bagliardi Beach, two gastropods commonly found have been displaced: one of them, Chilina fluminea, is no longer found; whereas the other, Gundlachia concentrica, is becoming rare. In contrast, several benthic species, uncommon or absent before the occurrence of L. fortunei in this microenvironment, are now present, including the Annelids: Oligochaeta (eight species), Aphanoneura (one species) and Hirudinea (eight species). In addition, several species of crustaceans and insects never cited at the invaded areas are now present (Darrigran et al., 1998).
The most direct and severe ecological impact has been the epizoic colonization of native naiads (Hyriidae and Mycetopodidae) by L. fortunei, similar to the impact of D. polymorpha on native bivalves in North America (Ricciardi et al., 1997).The displacement of the native naiads resulted from their inability to open and shut their valves because of the byssally-attached mussels on their shells. The quantitative impact of L. fortunei on native naiads in South America is unknown. L. fortunei alsosettles on other native fauna, such as Pomacea canaliculata (Gastropoda, Ampullariidae) and Aegla platensis (Anomura, Aeglidae), as well as on the introduced Corbicula fluminea (Bivalvia, Corbiculidae) (Darrigran et al., 2000; Darrigran, 2002).
- Dreissena polymorpha (zebra mussel): tan, brown, and black striped; adult shell length of 1-2 cm common; lacks projection on the lateral margin of its myophore plate; dorsally tapered shell valves; umbone located at the front; bottom of shell is flat or concave; acutely angled ventral shell margin.
- Mytilopsis leucophaeata (false dark mussel): typically solid coloration not striped; adult shell length of 1-2 cm common; has projection on the lateral margin of its myophore plate; dorsally tapered shell valves; umbone located at the front; bottom of organism is convex and lacking an acute angle.
- Mytella charruana is the only species that is very similar to L. fortunei, and the species have overlapping habitats (Rio de la Plata Esturary, brackish habitat). It can be distinguished from L. fortunei, because it has a resilial ridge pitted in the hinge area.
The Secretaria de Ambiente y Desarrollo Sustentable de la Nación (Jefatura de Gabinete de Ministerios – http://www.ambiente.gov.ar ) in Argentina, and the Ministerio de Medio Ambiente de Brasil (http://www.mma.gov.br/), are the government organizations that manage invasive species. Both ratified international events related to bio-invasions topics, such as:
- Convention of Naciones Unidas sobre el Derecho del Mar. - Agreement about Biological Diversity (CDB).
Brazil and Argentina head the lists of South American countries that create the legislation about ballast water for invasive species control (e.g. Ordenanza 12-98, Prefectura Naval Argentina).
Public awareness
Through NGOs in Brazil and Argentina, and State Universities (e.g. Universidad Nacional de La Plata, Facultad de Ciencias Naturales y Museo), educational programmes are carried out, both about bio-invasion in general and L. fortunei in particular.
Projects to increase information to the public in general are:
- Informative pamphlets on the economic-environmental problems resulting from the invasion of L. fortunei (freshwater macrofouling), and the production of documents and courses.
- A book about L. fortunei and its invasion in South America has recently been published (Darrigran and Damborenea, 2006).
Control
There is no single safety technique to control macrofouling due to L. fortunei in freshwater intake structures, screens, pumps, and fire protection systems of industries. There is a set of techniques suitable for each water system, in relation to the structure and the environmental features of the area. These techniques are a combination of physical/mechanical and chemical methods.
It would be of great value to generate knowledge about several topics, such as: predictive models for dispersion patterns; research about the more important vectors in each area; and research about control and preventive strategies with scarce environmental impact. This information is relevant because L. fortunei appears to be capable of colonizing waters from South America to the lower North American Great Lakes region (Ricciardi, 1998; Darrigran and Damborenea, 2005).
G Darrigran, Universidad Nacional de La Plata, Facultad de Ciencias Naturales y Museo, División Zoología de Invertebrados, Paseo del bosque, La Plata (1900), Buenos Aires, Argentina
