M. tuberculata is a tropical freshwater gastropod, native to eastern Africa and the Middle East, that has established widely throughout the tropics. It has demonstrated that it can rapidly colonize many types of...
Live individual of M. tuberculata in a field situation.
Copyright
Jean-Pierre Pointier
Individual in the field
Live individual of M. tuberculata in a field situation.
Jean-Pierre Pointier
Title
Aggregation
Caption
Example of population density that can be reached in natura.
Copyright
Jean-Pierre Pointier
Aggregation
Example of population density that can be reached in natura.
Jean-Pierre Pointier
Title
Colour morphs
Caption
Different colour morphs of Melanoides tuberculata which can be found in the French West Indies.
Copyright
Jean-Pierre Pointier
Colour morphs
Different colour morphs of Melanoides tuberculata which can be found in the French West Indies.
Jean-Pierre Pointier
Title
Colour morphs
Caption
Different colour morphs of Melanoides tuberculata which can be found in the French West Indies.
Copyright
Jean-Pierre Pointier
Colour morphs
Different colour morphs of Melanoides tuberculata which can be found in the French West Indies.
Jean-Pierre Pointier
Title
Colour morphs
Caption
Different colour morphs of Melanoides tuberculata which can be found in the French West Indies.
Copyright
Jean-Pierre Pointier
Colour morphs
Different colour morphs of Melanoides tuberculata which can be found in the French West Indies.
Jean-Pierre Pointier
Title
Biomphalaria glabrata
Caption
Biomphalaria glabrata, the intermediate snail hosts of schistosomiasis, for which M. tuberculata was used in 1970's and 1980's for biocontrol programs in several islands of the Carribean area as competitor.
Copyright
Jean-Pierre Pointier
Biomphalaria glabrata
Biomphalaria glabrata, the intermediate snail hosts of schistosomiasis, for which M. tuberculata was used in 1970's and 1980's for biocontrol programs in several islands of the Carribean area as competitor.
M. tuberculata is a tropical freshwater gastropod, native to eastern Africa and the Middle East, that has established widely throughout the tropics. It has demonstrated that it can rapidly colonize many types of habitat. It can reach very high densities up to several thousands of individuals per m2 (Dundee and Paine, 1977). It is a ubiquitous species and can tolerate a broad spectrum of environmental conditions. It is able to colonize disturbed habitats (especially man-made habitats) such as garden ponds, artificial lakes and irrigation systems. Reproduction is mainly by parthenogenesis (Jacob, 1957) but sexual reproduction does occur, with a resulting increase in genetic variance and/or heterosis effect (Facon et al., 2005). These recombination events can produce new genotypes that may invigorate the invasive ability (Facon et al., 2008). In its introduced range, there are reports of M. tuberculata outcompeting native species, however, the consequences are not always negative. In the Neotropical region, especially on some Caribbean islands, this snail has reduced populations of Biomphalaria glabrata, the main snail host of intestinal schistosomiasis.
Melanoides tuberculata is a tropical freshwater gastropod belonging to the Thiaridae family which is placed in clade Sorbeoconcha of the Caenogastropoda according to the classification of Bouchet and Rocroi (2005). It was described in the eighteenth century by Müller (1774) from the Coromandel region, India. Since its first description, many new species names have been given, as a consequence of substantial morphological variability, and subsequently synonymized with M. tuberculata (Starmühlner, 1976b). However, the shell of M. tuberculata exhibits an amazing morphological variation (general shape, background colour, ornaments and sculptures) that can simply be revealed by bleaching shells and which allows defining discrete morphs (several dozen described morphs), (Pointier, 1989; Facon et al., 2003). This variation has been shown to be heritable in the morphs studied (Pointier et al., 1992). These different morphs display very different life-history traits (Pointier et al., 1992; Facon et al., 2008).
M. tuberculata has a turreted shell with rounded body whorls that are ornamented with spiral grooves and sometimes axial undulating ribs well marked on the middle and upper whorls. The shells are pale to dark brown with numerous reddish brown flames and spots. However, characteristics of the shell (general shape, background colour, ornaments and sculptures) can vary according to the morphs considered (Facon et al., 2003). The spire is usually twice the length of the aperture or more (Morrison, 1954). The aperture is oval-shaped and the operculum is paucispiral, with the nucleus near the base (Morrison, 1954; Thompson, 1984). The head is tongue-like and constricted on its ventral side to give rise to the foot. The tentacles arise from just above this constricted area and are long and slender. M. tuberculata can reach up to a mean adult size of 20-40 mm depending on the morphs considered and environmental conditions (Pointier, 1989), but Murray (1975) reported individuals 70-80 mm in shell length in Texas.
M. tuberculata may have originated in eastern Africa and the Middle-East, although determining its distributional area prior to the increase in human trade (its main vector) a few thousand years ago remains problematic. Plio-Pleistocene fossils have been found in eastern Africa (Williamson, 1981). Based on a review of the available chorological and fossil evidence, Glaubrecht (1996) suggests that Melanoides colonized eastern Africa during the Miocene from the oriental region via land bridges forming in the area of the Arabian Peninsula. A first description of its distributional area included the inter-tropical belt of the Old World, from Africa to southeastern Asia (Pilsbry and Bequaert, 1927). It has since then invaded the whole inter-tropical area (Glaubrecht, 2000).
In addition to the countries listed, M. tuberculata is also found in:
Brunei Darussalam and Nigeria (P David, CEFE-CNRS, Montpellier, France, personal communication, 2008)
West Bengal (S Raut, Dept. of Zoology, University of Calcutta, India, personal communication, 2008)
Sulawesi (M Glaubrecht, Inst. Zool. Mus. Nat., Berlin, personal communication, 2008)
Laos (G Dreyfuss, Faculty of Pharmacie, Limoges, France, personal communication, 2008)
Vietnam (P Jarne, CEFE-CNRS, Montpellier, France, personal communication, 2008)
Benin (M Ibikounlé, Dept. of Zoology, University of Cotonou, Benin, personal communication, 2008)
Democratic Republic of Congo (L Tcheum-Tchuenté, Faculty of Science, University of Yaondé, Cameroon, personal communication, 2008)
Cote D’Ivoire (Y Bony, University of Abobo-Adjame, Cote D’Ivoire, personal communication, 2008)
Mauritania (M Aminetou, Faculty of Medicine, University of Antilles-Guyane, personal communication, 2008)
Mexico (D Amaya-Huerta, Universidad Autonoma, Mexico, personal communication, 2008)
Trinidad & Tobago (S Snider, Dept. of Zoology, North Caroline State University, USA, personal communication, 2008)
Ecuador (P Morin, private shell collector, personal communication, 2008)
Wallis & Funtuna Islands (R Galzin, CRIOBE CNRS-EPHE, Moorea, French Polynesia, personal communication, 2008).
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.
In 1927, M. tuberculata was found in various regions of Asia and Africa. Since then, it quickly invaded the whole inter-tropical belt mainly as a result of the trade in aquatic plants used in aquariophily (Madsen and Frandsen, 1989; Glaubrecht, 2000). Its invasion history in the Neotropics is well documented. Accidental introduction was first mentioned in America (Texas) in 1964 (Murray, 1964), and this was followed by rapid expansion. It was reported in Puerto-Rico and Florida in 1966, Panama in 1971, Venezuela in 1972, the Lesser Antilles (Dominique Island) and Louisiana in 1975, Honduras, Martinique and Guadeloupe Islands in 1979, Mexico and Dominican Republic in 1980 (Pointier and McCullough, 1989; Pointier, 1999). Later, other South-American countries were colonized, including Colombia, Peru, Ecuador, Brazil and Argentina (Fernandez et al., 2003). Today, most of the Neotropical area must be considered as either invaded or on the way to be so (Pointier, 1999; Quintana et al., 2000). Invasion dynamics have been thoroughly studied in some areas, such as the French West Indies (for further information, see Pointier, 1989, 1993, 1999; Pointier and Guyard, 1992; Pointier and Jourdane, 2000; Pointier et al., 1989, 1992,1993). Its expansion in the Australian and Pacific areas is more poorly documented. For instance, Riech (1937) recorded M. tuberculata in the Pacific islands in 1937, but its absence is not certain before this date.
It has to be noted that the invasion of the New World has been proven to be due to multiple introductions of different morphs from different parts of the native areas thanks to molecular phylogeography (Facon et al., 2003, 2008). This multiplicity of invasions suggests that the species level might not be appropriate to count invasive entities in such a parthenogenetic taxon. Moreover, it implies that invasions of new morphs in the Old World would certainly often remain cryptic because the presence of M. tuberculata, not of any particular morph, is usually reported and/or checked for (Genner et al., 2004).
M. tuberculata recently invaded the whole inter-tropical belt, mainly as a result of the trade in aquarium plants. Further invasions are therefore likely, especially of ‘improved’ morphs, in relation to the increase of trade in aquarium fishes and plants. Indeed, this common aquarium snail is often found as a ’hitch-hiker‘ on aquarium plants. They are often considered a beneficial addition to most aquariums, cleaning up leftover food and eating algae.
Besides these accidental introductions, it has to be noticed that M. tuberculata was subsequently used in 1970s and 1980s for biocontrol programmes in several islands of the Caribbean area (such as St Lucia, Martinique and Guadeloupe) as a competitor of Biomphalaria spp., the intermediate snail hosts of schistosomiasis (Prentice, 1983; Pointier et al., 1989; Pointier and Guyard, 1992; Pointier, 1993; Pointier and Jourdane, 2000).
M. tuberculata may resist a broad spectrum of environmental conditions. Typically it is found in shallow slow running water (0.6-1.2 m in depth), on a substratum consisting of soft mud, or soft mud and sand. But it has also been reported from relatively deep portions of freshwater pools (3 m deep) with substrata composed largely of rocks (Murray, 1975). It can inhabit very varied natural freshwater habitats such as rivers, streams, ponds and marshes, but also several anthropized aquatic environments such as garden ponds, irrigation systems or artificial lakes.
Cytological studies have indicated that M. tuberculata exhibits various levels of ploidy depending of the morphs considered (Jacob, 1958, 1959). The creation of polyploidy forms would result from complex events, including polyploidization and fertilization of gametes with a different ploidy level (Samadi et al., 1999). For instance, the pentaploid form may have been formed through the fertilization of apomictic autotetraploid ova by haploid sperm (Jacob, 1958, 1959).
The molecular diversity and phylogenetic relationships within the genus Melanoides have been studied by von Sørensen et al. (2005).
Reproductive Biology
M. tuberculata reproduces mainly through apomictic parthenogenesis, ova being produced mitotically (Jacob, 1958; 1959). This species is viviparous and juveniles are incubated in the brooding pouch (located in the head) of females, which have a wider last shell whorl than males (Heller and Farstay, 1989). The number of young within the brood pouch ranges from one to 70 depending on the size of the adult and on the morph considered (Livshits and Fishelson, 1983). The new-borns measure between 1 and 4 mm (depending on the morph considered (Facon et al., 2008) and their shells consist of a small protoconch and the first two whorls. Reproduction rates are poor when compared with pulmonate snails, but the survival of young snails tends to be very high (Pointier et al., 1991).
Besides its usual reproduction through parthenogenesis, M. tuberculata can make some rare events of sexual reproduction (Samadi et al., 1999). Some bisexual populations have been detected in Israel (Heller and Farstay, 1990) and Martinique (Samadi et al., 1997). Indeed, the ratios of shell-diameter / shell-height and penultimate-whorl diameter / shell-diameter differ significantly between males and females due to the absence of the brooding pouch in males (Heller and Farstay, 1989).
Unambiguous evidence of sexual reproduction has been reported in Martinique only (Samadi et al., 1999), and concerns two morphs detected in the 1990s. Morphological and micro satellite data showed that these two morphs are hybrids between pre-existing invasive morphs in Martinique (Samadi et al., 1999). These hybridization events involved unreduced female gametes from one morph and reduced (meiotic products) male gametes from the other one, inducing an increase of the ploidy level of the hybrids. After these sporadic sexual events, both hybrid morphs reproduce asexually and form new parthenogenetic lines (Samadi et al., 1999).
Physiology and Phenology
Studies in Martinique and Guadeloupe Islands (Pointier et al., 1989, 1993) allowed investigating life patterns of M. tuberculata under natural conditions. It showed that this snail has a demographic strategy characterized by a slow growth and a long life span (up to three years in some habitats). They revealed also that maximum reproduction took place during the rainy season between June and November (Pointier et al., 1993), but reproduction did not completely stop during the dry season. The estimated intrinsic rate of natural increase ‘r’ ranges from 0.12 to 0.27 and is similar to those obtained under laboratory conditions (Pointier et al., 1989). This species is active mostly at night, hiding beneath decaying plants and stones or burying themselves in the mud during the day (Livshits and Fishelson, 1983).
Nutrition
M. tuberculata is a polyphagous species. It is an aquatic herbivorous snail that feeds on periphyton, fine detritus, diatoms, epiphytic algae and decaying plants (Madsen, 1992).
Associations
This species is ubiquitous and thus does not show any specific association.
Environmental Requirements
M. tuberculata can inhabit very varied natural freshwater habitats such as rivers, streams, ponds and marshes, but also several anthropized aquatic environments such as garden ponds, irrigation systems or artificial lakes. It has also been found in marshy areas near mangroves and estuaries. However, it prefers physicochemical stability of the water through the year and homogeneity of the habitat. Thus it reaches higher densities in permanent water habitats than in temporary ones and population dynamics tend to be regulated mostly by floods during the rainy season and desiccation during dry season (Pointier et al., 1993). It supports a wide range of salinity conditions. Russo (1974) and Roessler et al. (1977) reported this species from both fresh and estuarine waters in south Florida. Roessler et al. (1977) found this species in waters up to 30ppt. It lives usually in water between 18 and 25°C (Murray, 1971), but Livshits and Fishelson (1983) reported individuals that bury themselves in the mud and hibernate in the winter in Israel.
Favourable ecological conditions for M. tuberculata are permanent and shallow waters, emergent plants and well-oxygenated niches (Pointier and McCullough, 1989). In rivers, M. tuberculata is mainly present along the riverbanks where it can find refuge from water turbulence (Samadi et al., 1997).
M. tuberculata may play the role of intermediate host of several trematode parasites. These parasites may have a harmful impact on the snail reproduction, some of which have a sterilizing effect on their snail host. Several trematode species infecting M. tuberculata have been found in some invaded countries such as Mexico (Amaya-Huerta and Almeyda-Artigas, 1994) and Colombia (Velasquez et al., 2000). Predators of M. tuberculata are absent in invaded areas except for rats and aquatic birds. Other freshwater snails belonging to the Buccinidae family are predators in native areas, such as Clea helena in South-East Asia.
Flooding may be a local dispersal agent but it has not been properly identified.
Vector Transmission (Biotic)
Some local dispersal agents include aquatic birds or cattle.
Accidental Introduction
M. tuberculata recently invaded the whole inter-tropical belt mainly as a result of the trade in aquarium plants. Further invasions are therefore likely, especially of ‘improved’ morphs, in relation to the increase of trade in aquarium fishes and plants. M. tuberculata individuals are now for sale on the Internet due to the fact that they are often considered a beneficial addition to most aquariums, cleaning up leftover food and eating algae. This could soon increase the risk of accidental introductions.
Intentional Introduction
Besides accidental introductions, it has to be noticed that M. tuberculata was subsequently used in 1970s and 1980s for bio control programmes in several islands of the Caribbean area (such as St Lucia, Martinique and Guadeloupe) as a competitor of Biomphalaria spp., the intermediate snail hosts of schistosomiasis (Prentice, 1983; Pointier et al., 1989; Pointier and Guyard, 1992; Pointier and Jourdane, 2000).
Besides its positive consequences concerning schistosomiasis, M. tuberculata may play the role of intermediate host for several trematode parasites of medical or veterinary importance (Murray, 1971; Jacobson, 1975; Dundee and Paine, 1977). The most important parasite infecting M. tuberculata is Centrocestus formasanus (Amaya-Huerta and Almeyda-Artigas, 1994), which is responsible for a food-borne disease in Asia. This parasite has also been recently introduced into Mexico and Colombia (Amaya-Huerta and Almeyda-Artigas, 1994; Velasquez et al., 2000).
Impact on Biodiversity
M. tuberculata has no negative impact on aquatic macrophytes (Madsen, 1992) although it has been reported to displace several gastropods where introduced (Murray, 1971; Jacobson, 1975; Pointier, 1999). Roessler et al. (1977) reported competition for trophic resources with Neritina virginea in Florida. M. tuberculata was also shown to outcompete Biomphalaria glabrata and B. straminea in Martinique and Guadeloupe Islands (especially in stable aquatic habitats) (Pointier and McCullough, 1989), and B. havanensis and Pachychilus largillierti in Honduras (Clarke, 1987).
The consequences of the invasion of the Neotropical area, especially in some Caribbean islands, may be considered as a benefit for public health, because this snail has eliminated or strongly reduced populations of Biomphalaria glabrata, the main snail host of intestinal schistosomiasis (Pointier and Théron, 2006). However, it has to be noted that the impact of M. tuberculata on B. glabrata is variable according to the type of aquatic habitat (Pointier et al., 1993). Positive results have been obtained in dasheen-marshes (Prentice, 1983), water-cress beds (Pointier and Guyard, 1992), ponds (Pointier, 1989) and springs (Pointier et al., 1991) where B. glabrata was eliminated but the biological control failed in the marshy forest located behind mangroves in Guadeloupe and this area is still an active focus of schistosomiasis (Pointier and Jourdane, 2000; Pointier and Théron, 2006).
Two aspects of the invasion of M. tuberculata should be more thoroughly studied. Firstly, investigation into whether the serial replacement of morphs observed in Martinique (see case studies) recurs in other regions of the invaded area. Secondly, a more precise knowledge is needed of the locations and the interactions between the different morphs in the native area.
Gutiérrez Gregoric DE, Vogler RE, 2010. Risk of establishment of the invasive freshwater gastropod Melanoides tuberculatus in the Rio de la Plata (Argentina - Uruguay). (Riesgo de establecimiento del gasterópodo dulceacuícola invasor Melanoides tuberculatus en el Río de la Plata (Argentina - Uruguay).) Revista Mexicana de Biodiversidad 81, 81:573-577
Peso JG, Vogler RE, Pividori ND, 2010. First record of the invasive gastropod Melanoides tuberculata (Gastropoda, Thiaridae) in the Uruguay River (Argentina-Brazil). (Primer registro del gasterópodo invasor Melanoides tuberculata (Gastropoda, Thiaridae) en el río Uruguay (Argentina-Brasil).) Comunicaciones de la Sociedad Malacológica del Uruguay, 9(93):231-235
Jean Pierre Pointier, Laborat. Ecosystemes Aquatiques Tropicaux et Mediterraneens, UMR 5244 CNRS-EPHE-UPVD, Biologie et Ecologie Tropicale et Medit., 52 avenue Paul Alduy, 66860 Perpignan cedex, France
