Invasion History

First Non-native North American Tidal Record: 1949
First Non-native West Coast Tidal Record:
First Non-native East/Gulf Coast Tidal Record: 1949

General Invasion History:

Tarebia granifera is a predominantly freshwater snail native to regions of Southeast Asia and Oceania, including India and Sri Lanka east to Indonesia, the Philippines, and Papua New Guinea (Poss et al. 2008; Academy of Natural Sciences 2013; US National Museum of Natural History 2013). This snail occurs widely in fresh waters of Pacific Islands, including Guam, French Polynesia, and Hawaii, where populations may have been introduced by early Polynesians (Abbott 1952; Cowie 1998; Myers et al. 2000). It is found in a variety of habitats, including ponds, lakes, rivers, ditches, and swamps, but seems to prefer the riffles of streams. It is reported to prefer flowing, upland streams (McCann et al. 1996; Thompson 2004), but occurs in tidal oligohaline to mesohaline tributaries of Tampa Bay, Florida (Baker et al. 2004). In Hawaii and South Africa, it occurs in estuaries with salinities up to 30 PSU (Englund et al. 2000; Miranda et al. 2010).

Tarebia granifera has been widely introduced outside its native range, including freshwaters in Florida, interior springs and streams in Texas, and a pond in Idaho (Abbott 1952; Baker et al. 2004; Karatayev et al. 2009; USGS Nonindigenous Aquatic Species Program 2013). It is also known from many Caribbean islands (Chaniotis 1980a; Pointier 2001), and freshwaters in Mexico (López-López et al. 2009), South America (Venezuela-Brazil, Pointier et al. 2007), Israel (Ben-Ami 2006), South Africa (Appleton and Nadasan 2002), and Hawaii (Cowie 1998). It is a popular aquarium animal (Abbott 1952), which may have led to its introduction around the globe. In the Caribbean and South America, it was introduced to control native snails which host disease-causing trematode parasites (Pointier 2001).

North American Invasion History:

Invasion History on the East Coast:

Tarebia granifera occurs in Coral Gables and Miami, on the East Coast of Florida (Chaniotis et al. 1980b), but has not been reported from tidal waters.

Invasion History on the Gulf Coast:

In North America, Tarebia granifera was reportedly first imported by an aquarium dealer in 1937 in Tampa, Florida (FL). In 1947, it was collected in Lithia Springs, Hillsborough County, FL in headwaters of the Alafia River. It subsequently spread into tidal waters, where it can occur in high abundances in fresh-oligohaline tributaries (Poss 1999; Baker et al. 2004; Gulf States Marine Fisheries Commission 2009). It has been collected in interior springs and streams in nine Florida counties and in central Texas (Karatayev et al. 2009; Florida Museum of Natural History 2013; USGS Nonindigenous Aquatic Species Program 2013).

Invasion History in Hawaii:

Tarebia granifera was collected in Maui in 1856, but it could have been introduced in Prehistoric times by Polynesian settlers as food or in the roots of cultivated Taro plants. It is now found in streams of all the major Hawaiian Islands (Cowie 1998; Carlton and Eldredge 2009). On Oahu, it is abundant in two brackish streams at 15 and 30 PSU (Englund et al. 2000).

Invasion History Elsewhere in the World:

Tarebia granifera was first found in Puerto Rico in 1945 (Chaniotis et al. 1980b) and is now widespread (USGS Nonindigenous Aquatic Species Program 2013). It also occurs in Cuba, Jamaica (by 1988), the Virgin Islands (by 1987), Martinique (in 1991), Haiti (by 1979), the Dominican Republic (in 1968), Trinidad (by 1944), the Gulf Coast of Mexico (by 2007), and the Caribbean coast of Guatemala and Venezuela (in 1975) (Chanitois 1980b; Pointier et al. 1994; Pointier 2001; López-López et al. 2010; Florida Museum of Natural History 2013). In two Mexican rivers, its range extends to the upper estuarine zone (López-López 2010). The aquarium industry is probably the primary vector of introduction, but some of its later spread in the Caribbean region has resulted from its use for biocontrol of the native snail Biomphalaria glabrata, a host of the disease-causing trematode Schistosoma mansoni (blood-fluke) (Pointier et al. 1994; Pointier 2001).

Tarebia granifera was discovered near Durban, South Africa, in a freshwater reservoir in 1996 (Appleton and Nadasan 2002). It has now colonized freshwater drainages, lagoons, and estuaries along ~330 km of coastline, from Durban, nearly to the border with Mozambique (Appleton et al. 2009). In 2005, it was found in a freshwater stream flowing into the St. Lucie estuary in Kruger National Park, and soon established dense populations at salinities of 10-20 PSU (Appleton et al. 2009; Miranda et al. 2010). In 2004, T. granifera was found at several sites along the Jordan River estuary (Ben-Ami 2008).


Description

Tarebia granifera is a predominantly freshwater snail, but has colonized estuaries with near-marine salinities in South Africa and Hawaii (Englund et al. 2000; Miranda and Perissinotto 2012). It has a dextrally coiled, elongate-conical shell, with 8-12 whorls. The apex of the spire is usually eroded and the sides are concave in outline. The shell is sculptured with prominent nodes overlapping the suture between whorls and forming crenulations. It is marked with vertical and spiral ribs and threads. The base is marked with prominent spiral ridges. The operculum has a small nucleus near the basal margin and rapidly expands towards the top of the aperture. Adults range from 6 to 40 mm, but more normally reach 20-35 mm. This is about 0.4 X as wide as it is tall. Description from: Abbott 1952, Chaniotis 1980b, Baker et al. 2004, and Thompson 2004.

There are at least four named species of Tarebia in Southeast Asia, and many synonyms (Galli 2013). Populations show great morphological variation, and it is possible that more than one species is present in Florida (Thompson 2004).


Taxonomy

Taxonomic Tree

Kingdom:   Animalia
Phylum:   Mollusca
Class:   Gastropoda
Order:   Neotaenioglossa
Family:   Thiaridae
Genus:   Tarebia
Species:   granifera

Synonyms

Melania granifera (Lamarck, 1822)
Tarebia lateritia. (Lea, 1850)
Thiara granifera (Lamarck, 1822)
Tarebia batana (Gould, 1843)
Tarebia broti (Reeve, 1859)
Tarebia celebensis (Quoy & Gaimard, 1834)
Tarebia chocolatum (Brot, 1860)
Tarebia coffea (Philippi, 1843)
Tarebia lineata (Gray in Wood, 1828)
Tarebia lirata (Menke, 1843)
Tarebia verrucosa (Hinds, 1844)

Potentially Misidentified Species

Melanoides tuberculatus
None

Tarebia granifera
None

Ecology

General:

Tarebia granifera is a freshwater snail which occasionally invades brackish habitats (Englund et al. 2000; Baker et al. 2004; Appleton et al. 2009). This snail has separate sexes, but reproduces primarily by parthenogenetic reproduction (without fertilization), with only occasional sexual reproduction, resulting in populations that are largely or completely clonal. Males are rare or absent (Abbott 1952; Myers et al. 2000; Miranda et al. 2010). Reproduction is ovoviviparous, with eggs being incubated in the female's brood pouch in the last (largest) whorl of the shell and hatching out as small snails, 2.0 - mm in length with 4-5 shell whorls. Estimated annual fecundity is 213 embryos per year (Keller et al. 2007). The snails reach maturity at about 6 mm shell length in 3-6 months (Abbott 1952; Chaniotis et al. 1980b).

Tarebia granifera is a snail of warm-temperate to tropical distribution. Habitats include springs, streams, lakes, rivers, and estuaries (Abbott 1952; Pointier et al. 1994; Thompson 2004; Appleton et al. 2009). It has a preference or tolerance for stronger currents than its relative Melanoides tuberculata (Red-Rim Melania) (Pointier et al. 1994). Snails from Puerto Rico died after 24 hr exposure to 7°C, but specimens from South Africa tolerated 0°C (Chaniotis et al. 1980a; Miranda et al. 2010). The Quilted Melania is predominantly a freshwater species, but some populations have colonized brackish or nearly marine waters. In estuaries on Oahu, Hawaii, and in KwaZulu, South Africa the snail occurred from freshwater to 30 and 34 PSU, respectively (Englund et al. 2000; Miranda et al. 2010). This snail, though aquatic, is quite tolerant of desiccation – individuals survived 2-3 days of air exposure at 25-30°C at 76-92% relative humidity (Chaniotis et al. 1980a).

Tarebia granifera grazes on microalgae and detritus, but does not feed on the leaves of larger plants (Miranda and Perissinotto 2012). It is eaten by crabs, fishes, and birds, as indicated by a diversity of parasites which use it as an intermediate host. Many trematode species and many more undescribed larval forms have been reported from this snail (Abbott 1952; Appleton et al. 2009). This snail was widely believed to be an intermediate host of the lung-fluke Paragonimus westermanni (Abbott 1952; Chaniotis 1980b), but this has been shown to be incorrect (Michelson 1992).

Food:

Algae; Aquatic plants

Trophic Status:

Herbivore

Herb

Habitats

General HabitatNontidal FreshwaterNone
General HabitatUnstructured BottomNone
General HabitatGrass BedNone
General HabitatCoarse Woody DebrisNone
General HabitatFresh (nontidal) MarshNone
General HabitatSwampNone
General HabitatTidal Fresh MarshNone
General HabitatMarinas & DocksNone
General HabitatRockyNone
General HabitatCanalsNone
Salinity RangeLimnetic0-0.5 PSU
Salinity RangeOligohaline0.5-5 PSU
Salinity RangeMesohaline5-18 PSU
Salinity RangePolyhaline18-30 PSU
Tidal RangeSubtidalNone
Vertical HabitatEpibenthicNone


Tolerances and Life History Parameters

Minimum Temperature (ºC)0Experimental (Miranda et al. 2010 et al. 1980a, direct transfer, 32 hr exposure).
Maximum Temperature (ºC)40Experimental, 32 h exposure, 100% survival (Miranda et al. 2010)
Minimum Salinity (‰)0This is a freshwater species.
Maximum Salinity (‰)30Collected at up to 30 PSU in Hawaii (Englund et al. 2000). However, in Florida, it appears to avoid saline waters (Baker et al. 2005). In experimental studies, snails from South Africa survived up to a month at 30 PSU (Miranda et al. 2010)
Minimum pH7.1Field, Puerto Rico (Chaniotis et al. 1980b)
Maximum pH8.5Field, Puerto Rico (Chaniotis et al. 1980b)
Minimum Reproductive Salinity0This is a freshwater species.
Maximum Reproductive Salinity20Experimental (Miranda et al. 2010)
Minimum Length (mm)6Minimum size at reproduction, Abbott 1952; Thompson 2004
Maximum Length (mm)40A more normal maximum size is 20-35 mm (Abbott 1952; Thompson 2004).
Broad Temperature RangeNoneSubtropical-Tropical
Broad Salinity RangeNoneNontidal Limnetic-Polyhaline

General Impacts

Tarebia granifera, a popular aquarium snail, reaches high densities in Tampa Bay tributaries and inland Florida fresh waters (Abbott 1952; Baker et al. 2004; Thompson 2004). However, no major ecological or economic impacts have been reported from US waters, to our knowledge. This snail was once widely studied as the putative first intermediate host of the Oriental Lung Fluke Paragonimus westermanni (Abbott 1952; Chaniotis et al. 1980b). However, later research showed that this was incorrect (Michelson 1992). Instead T. granifera came to be regarded as a parasite fighter in the Caribbean, against the Blood Fluke Schistosoma mansoni, by competition with the native host snail Biomphalaria glabrata. It has been introduced to many streams as a biocontrol agent (Perez et al. 1991; Pointier et al. 1994).

Economic Impacts

Health: Tarebia granifera was found to have benefits in controlling another trematode parasite, the Blood Fluke Schistosoma mansoni, by competition and egg-predation on the native host snail Biomphalaria glabrata, and has been introduced to many streams as a biocontrol agent (Perez et al. 1991; Pointier et al. 1994).

Ecological Impacts

Competition: Tarebia granifera is known to compete with, and sometimes replace, native gastropods in its introduced range. In the West Indies and Venezuela, it, together with M. tuberculata, spread rapidly and replaced the native Biomphalaria glabrata, a major host of Schistosoma mansoni (Perez et al. 1991; Pointier et al. 1994; Pointier 2001). Tarebia granifera is considered a threat to native freshwater snails in springs and streams of central Texas (Karatayev et al. 2009) and South Africa (Appleton et al. 2009).

Predation: This snail did eat the egg masses of an endangered central Texas fish, Etheostoma fonticola (Fountain Darter), but at rates lower than those of most other native and introduced snails (Phillips et al. 2010).

Habitat Change: Tarebia granifera has a generalist diet, but feeds mostly on filamentous microlalgae (Miranda and Perissinotto 2012). In Trinidad streams, the snail was much more abundant (2-8 X) in open areas, with direct sunlight and denser algal populations, compared with forested areas. The high snail abundance and intense grazing led to a 3-9-fold increase in nitrogen export, contributing to eutrophication downstream (Moslemi et al. 2012). An unusual habitat effect was found at the mouth of streams in Tobago, where abundant shells of M. tuberculata (Red-Rim Melania) and Tarebia granifera were washed down streams into coastal waters during storms, providing a new empty-shell resource for hermit crabs (Clibanarius tricolor and C. vittatus) and drastically changing the patterns of shell use (van Oosterhout et al. 2013).

Regional Distribution Map

Bioregion Region Name Year Invasion Status Population Status
G070 Tampa Bay 1949 Def Estab
SP-XXI None 1856 Def Estab
WA-V None 2005 Def Estab

Occurrence Map

OCC_ID Author Year Date Locality Status Latitude Longitude

References

Abbott, R. Tucker (1952) A study of an intermediate snail host (Thiara granifera) of the Oriental lung fluke (Paragonimus), Proceedings of the United States National Museum 102(3292): 71-116

Abe, Naoya (1983) Proceeding of the second international conference on the malacofauna of Hong Kong and southern China, Hong Kong University Press, Hong Kong. Pp. 381-392

Appleton, C. C.; Forbes, A. T.; Demetriades, N. T. (2009) The occurrence, bionomics and potential impacts of the invasive freshwater snail Tarebia granifera (Lamarck, 1822) (Gastropoda: Thiaridae) in South Africa, Zoologische Mededelingen 83(4): 525-536

Appleton, C. C.; Nadasan, D. S. (2002) First report of Tarebia granifera (Lamarck, 1816) (Gastropoda: Thiaridae) from Africa, Journal of Molluscan Studies 68: 399-402

Baker, Patrick; Baker, Shirley M.; Fajans, Jon (2004) Nonindigenous marine species in the greater Tampa Bay ecosystem., Tampa Bay Estuary Program, Tampa FL. Pp. <missing location>

Ben-Ami, Frida (2008) First report of the invasive freshwater snail Tarebia granifera (Lamarck, 1816) (Gastropoda : Thiaridae) from Israel, Nautilus 120(4): 156-161

Chaniotis, Byron N.; Butler, J. Miles Jr.; Ferguson, Frederick F.; Jobin, William R. (1980a) Thermal limits, dessication tolerance, and humidity reactions of Thiara (Tarebia) granifera mauiensis (Gastropoda: Thiaridae) host of the Asiatic lung fluke disease, Caribbean Journal of Science 16(1-4): 91-93

Chaniotis, Byron N.; Butler, J. Miles Jr.; Ferguson, Frederick F.; Jobin, William R. (1980b) Bionomics of Tarebia granifera (Gastropoda: Thiaridae) in Puerto Rico, an Asiatic vector of Paragonimus westermanni, Caribbean Journal of Science 16(1-4): 81-90

Concepcion, Georgette B.; Nelson, Stephen G. (1999) Effects of a dam and reservoir on the distributions and densities of macrofauna in tropical streams of Guam (Marianas Islands), Journal of Freshwater Ecology 14(4): 447-454

Cowie, Robert H. (1998) Patterns of introduction of non-indigenous non-marine snails and slugs in the Hawaiian Islands., Biodiversity and Conservation 7: 349-368

Englund, R.A.; Arakaki, K.; Preston, D.J.; Coles, S.L.; Eldredge, L.G. (2000) <missing title>, Hawaii Biological Survey, Bishop Museum, Honolulu. Pp. <missing location>

Facon, Benoit; David, Patrice (2006) Metapopulation dynamics and biological invasions: a spatially explicit model applied to a freshwater snail., The American Naturalist 168(6): 769-783

2009-2013 Invertebrate Zoology Master Database. http://www.flmnh.ufl.edu/scripts/dbs/malacol_pub.asp

2013 WMSDB- Worldwide Molluscan Species Database. http://www.bagniliggia.it/WMSD/WMSDhome.htm

Karatayev, Alexander Y.; Burlakova, Lyubov E.; Karatayev, Vadim A; Padilla, Dianna K. (2009) Introduction, distribution, spread, and impacts of exotic freshwater gastropods in Texas, Hydrobiologia 619: 181-194

Keller, Reuben P.; Drake, John M.; Lodge, David M. (2007) Fecundity as a basis for risk assessment of nonindigenous freshwater molluscs, Conservation Biology 21(1): 191-200

Ladd, Hallie L. A.; Rogowski, David L. (2012) Egg predation and parasite prevalence in the invasive freshwater snail, Melanoides tuberculata (Müller, 1774) in a west Texas spring system, Aquatic Invasions 7(2): 287-290

López-López, Eugenia; Sedeño-Díaz, J. Elías; Vega, Perla Tapia; Oliveros, Eloiza (2010) Invasive mollusks Tarebia granifera Lamarck, 1822 and Corbicula fluminea Müller, 1774 in the Tuxpam and Tecolutla rivers, Mexico: spatial and seasonal distribution patterns, Aquatic Invasions 5(S1): 435-450

McCann, James A.; Arkin, Lori; Williams, James D. (1996) <missing title>, University of Florida, Center for Aquatic Plants, Gainesville. Pp. unpaged

Mead, A.; Carlton, J. T.; Griffiths, C. L. Rius, M. (2011b) Introduced and cryptogenic marine and estuarine species of South Africa, Journal of Natural History 39-40: 2463-2524

Michelson, E. H. (1992) Thiara granifera, a victim of authoritarianism, Malacological Review 25: 67-71

Miranda, Nelson A. F.; Perissinotto, Renzo (2012) Stable isotope evidence for dietary overlap between alien and native gastropods in coastal lakes of northern Kwazulu-Natal, South Africa, PLOS ONE 7(2): e31897

Miranda, Nelson A. F.; Perissinotto, Renzo; Appleton, Christopher C. (2011) Population structure of an invasive parthenogenetic gastropod in coastal lakes and estuaries of northern Kwazulu-Natal, South Africa, PLOS ONE 6(8): e24337

Miranda, Nelson A.F.; Perissinotto, Renzo; Appleton, Christopher C. (2010) Salinity and temperature tolerance of the invasive freshwater gastropod Tarebia granifera, South African Journal of Science 106(3/4): 1-7

Moslemi, Jennifer M.; Snider, Sunny B.; MacNeill, Keeley; Gilliam, James F.; Flecker, Alexander S. (2012) Impacts of an invasive snail (Tarebia granifera) on nutrient cycling in tropical streams: the role of riparian deforestation in Trinidad, West Indies, PLOS ONE 7(6): e38806

Myers, Marilyn J.; Meyer, Chris, P.; Resh, Vincent H. (2000) Neritid and thiarid gastropods from French Polynesian streams: How reproduction (sexual, parthenogenetic) and dispersal (active, passive) affect population structure, Freshwater Biology 44: 535-545

Perez, Jose Gomez; Vargas, Mercedes; Malek, Emile A. (1991) Displacement of Biomphalaria glabrata by Thiaria granifera under natural conditions in the Dominican Republic, Memorias do Instituto Oswaldo Cruz Rio de Janeiro 88: 341-347

Phillips, C. T.; Alexander, M. L.; Howard, R. (2010) Consumption of eggs of the endangered fountain darter (Etheostoma fonticola) by native and nonnative snails, Southwestern Naturalist 55: 115-117

Pointier, J. P., Incani, R. N., Balzan, C., Chrosciechowski, P., Prypchan, S. (1994) Invasion of the rivers of the littoral central region of Venezuela by Thiara granifera and Melanoides tuberculata (Mollusca: Prosobranchia: Thiaridae) and the absence of Biomphalaria glabrata, snail host of Schistosoma mansoni, Nautilus 107(4): 124-128

Pointier, Jean-Pierre (2001) Invading freshwater snails and biological control in Martinique Island, French West Indies, Memorias do Instituto Oswaldo Cruz Rio de Janeiro 96: 67-74

1999 Nonindigenous species in the Gulf of Mexico. <missing description>

Raw, Jacqueline L.; Miranda, Nelson A. F.; Perissinotto, Renzo (2013) Chemical cues released by an alien invasive aquatic gastropod drive its invasion success, PLOS ONE 5: e64071

2004 An identification manual for the freshwater snails of Florida an identification manual for the freshwater snails of florida an identification manual for the freshwater snails of florida an identification guide for the freshwater sn. http://www.flmnh.ufl.edu/malacology/fl-snail/snails1.htm

2003-2015 Nonindigenous Aquatic Species Database. Gainesville, FL. http://nas.er.usgs.gov

van Oosterhout, Cock and 7 authors (2013) Invasive freshwater snails provide resource for native marine hermit crabs, Aquatic Invasions 8: in press