Tarebia granifera
Encyclopedia
Tarebia granifera, common name
in the aquarium industry the quilted melania, is a species
of freshwater snail
with an operculum
, an aquatic
gastropod mollusk in the family Thiaridae
. This snail is native to south-eastern Asia, but it has become an invasive species
in numerous countries.
in 1952 together with notes on its biology and bionomics. A dissection guide was provided by Malek (1962).
The maximum height of adult shells of this species from South Africa is from 18.5 mm to 25.1 mm, while in Puerto Rico they can reach up to 35 mm.
Two color forms of Tarebia granifera are found, one has a pale brown body whorl
and a dark spire
(see photo on the right) and in the other the shell is entirely dark brown to almost black (see photo on the left). Intermediate forms exist.
, Taiwan, Hong Kong, Thailand.
Americas:
Africa:
This spread will doubtless continue into northern South Africa, Moçambique, Zimbabwe and beyond. It has not been possible to calculate the rate of dispersal.
Asia:
of the natural waterbodies of the region – more so than any other invasive freshwater invertebrate known from the South Africa. The South African indigenous thiarids Thiara amarula, Melanoides tuberculata, and Cleopatra ferruginea
are considered particularly vulnerable.
Most localities in South Africa (93%) lie below an altitude of 300 m above sea level where an estimated area of 39 500 km2 has been colonized. The only known localities outside this area are the Umsinduzi River in Pietermaritzburg
and its confluence with the Umgeni River which lie closer to 500 m. R. Tucker Abbott
(1952) noted that on Guam
Island, Tarebia granifera occurred in streams and rivers at 983 m altitude but that these watercourses were consistently above 24°C indicating that temperature may be an important determinant of distribution.
Tarebia granifera also occurs in several estuaries along the KwaZulu-Natal coast. Prominent among these is the dense population (±6038 m2) found at a salinity
of 9.98‰ (28.5% sea water) in Catalina Bay, Lake St Lucia, iSimangaliso Wetland Park, KwaZulu-Natal. These records show that Tarebia granifera is able to colonize brackish and moderately saline habitats and reach high densities there. From observations in Puerto Rico
it was suggested that snails could survive temporarily saline conditions for several weeks by burying themselves in the substratum
, emerging when fresh water returned.
In common with other Thiaridae, Tarebia granifera is primarily a benthic species and in South Africa has been collected on a variety of substrata in both natural and artificial waterbodies, e.g. sand, mud, rock, concrete bridge foundations and the concrete walls and bottoms of reservoirs, irrigation canals and ornamental ponds. Many of these habitats were vegetated and the associated vegetation included many types of emergent
monocotyledons (e.g. Cyperus papyrus
, Scirpus
sp., Typha
sp., Phragmites
sp.) and dicotyledons (e.g. Ceratophyllum demersum
, Potamogeton crispus, Nymphaea nouchali
). Where densities are high, Tarebia granifera may also occur on marginal, trailing vegetation and the floating Common Water Hyacinth Eichhornia crassipes
as well. It favours turbulent water and tolerates current speeds up to 1.2m.s−1 and possibly greater. This habitat range is similar to that recorded for Tarebia granifera in Puerto Rico.
The major interest in Tarebia granifera outside Asia today is its invasive ability and its impact on indigenous benthic communities
in colonized waterbodies.
Typically half or more of these snails were buried in the sediment
s and were not visible from the surface. This was also noticed in aquaria
where they actively buried themselves in sand. Exact proportion of population of Tarebia granifera that is buried at any time is not known. There is also not known how long can snails remain buried.
Tarebia granifera will die at the temperature 7 °C in aquaria, but they do not live in water temperature under 10 °C in the wild.
of Tarebia granifera from one waterbody or river catchment to another occurs passively via birds, notably waterfowl
, which eat them and void them later, perhaps in another habitat. Evidence for this comes from the finding of many small Tarebia granifera 5–7 mm in height and still containing the soft parts in unidentified bird droppings from the bank of the Mhlali River, South Africa. Even though the shell of Tarebia granifera is thick, most of these juveniles had been partially crushed with only a few still intact. Both the intact and damaged specimens could have been alive when passed and perhaps survived had they been deposited in water. None was large enough to have been reproductively mature (see below) and would have needed to survive in any new habitat for several months before reproducing.
Passive dispersal may also occur via weed on boats and boat trailers and via water pumped from one waterbody to another for industrial and irrigation purposes. In the Nseleni River juvenile Tarebia granifera were commonly found with another invasive snail, Pseudosuccinea columella
, on floating clumps of water hyacinth Eichhornia crassipes which provide a vehicle for rapid downstream dispersal.
Once established in a particular waterbody Tarebia granifera is likely to disperse actively, both up and downstream in the case of flowing systems, as far as environmental factors like current speed and food availability will allow. The snail’s tolerance of turbulent, flowing water was demonstrated by Prentice (1983) who reported it migrating upstream on the Caribbean island of Saint Lucia
at a rate of 100 m month−1 in streams discharging up to 50 l.s−1. In KwaZulu-Natal it has been collected in water flowing at up to 1.2 m.s−1 which is likely to exceed the current speeds of at least the lower and middle reaches of many rivers and streams in South Africa making these watercourses open to colonization.
The sole
of Tarebia granifera is proportionally small when compared to other thiarids and smaller snails with their higher coefficients were less able to grip the substratum in the face of moving water and so not did disperse as effectively as larger ones.
of Tarebia granifera 4444 m−2 which falls within the range of densities measured with a Van Veen grab in a number of sites in northern KwaZulu-Natal, where was measured desnsities 843.6 ±320.2 m−2 to 20764.4 ±13828.1 m−2. The site with such high density was non-flowing, devoid of rooted vegetation but it was shaded by trees (Barringtonia racemosa
) and by floating Eichhornia crassipes
. This between-site variability may be positively correlated to habitat heterogeneity
and food availability. Despite the very high densities recorded in the Nseleni River, indigenous invertebrates were still present in the sediments including: bivalve Chambardia wahlbergi, chironomids, oligochaetes (tubificids) and burrowing polychaetes were also found but in very low numbers.
The low densities of Tarebia granifera reported for the Mhlatuze River, South Africa may have been influenced by nearby sand-mining activities or, more likely, high flows and mobile sediments, but they nevertheless approach those recorded by Dudgeon (1980) for Tarebia granifera in its native Hong Kong
(18–193 m−2).
Little is known of the long term population fluctuations of Tarebia granifera and findings seem to be contradictory. Studies in Cuba (Yong et al. (1987), Ferrer López et al. (1989), Fernández et al. (1992)) indicate that the snail lives for more than a year though maximum densities were recorded at different times of the year in different habitats. Using a catch per unit effort
netting technique, Yong et al. (1987) and Ferrer López et al. (1989) found highest densities in summer when temperatures reached their maximum whereas Fernández et al. (1992) found highest densities in November (late autumn) when temperatures reached their minimum. Fernández et al. (1992) also suggested that Tarebia granifera density was positively correlated with Ca2+
concentrations and negatively with NH4
concentrations.
Recent surveys by Vázquez et al. (2010) of Pinar del Río Province
, Cuba have reported population densities of Tarebia granifera of 85 individuals/m2, well above those of its endemic relatives (5 individuals/m2).
.
and ovoviviparous, although males have been reported. These are characteristics which are undoubtedly key to its success as an invader. For example no males have been found amongst hundreds dissected from KwaZulu-Natal, it is probable that a few are present. Males were found in most (6/7) populations examined in Puerto Rico
but were generally uncommon at up to 22.7% of the population (mean 4.6%). Live sperm were present in the testes of these males but the genitalia
were apparently non-functional. R. Tucker Abbott (1952) failed to find sperm in the gonads of male Tarebia granifera from Florida. Most Tarebia granifera are therefore clones
of the female parent.
Embryo
s develop in a brood pouch. This pouch is a compartmentalized structure lying immediately above the oesophagus and develops only after the snail has reached maturity. Its size expands as the number of embryos increases. Tarebia granifera has 1-77 embryos in its brood pouch.
Tucker Abbott (1952), Chaniotis et al. (1980) and WHO (1981) cite the same statistic that females can give birth to one juvenile every 12 hours! Young snails emerge through a birth pore on the right side of the head. The newborn shell is <1–2 mm in height with between 1.5 and 4.8 whorls. The size of juveniles at birth is 0.7-2.1 mm. According to Chen (2003) these newborns have a high survival rate in the field.
Attainment of sexual maturity
in Tarebia granifera is generally indicated by the size of the smallest snail observed to give birth rather than a histological assessment of the development of the gonad and associated reproductive structures. Appleton & Nadasan (2002) estimated onset of maturity at 10–12 mm shell height but unpublished data suggest a height closer to 8 mm in line with other published studies. Tucker Abbott (1952) estimated sexual maturity at between 5.5 and 8.0 mm at different stations over a short stretch of river in Florida. Chaniotis et al. (1980) gave a similar estimate of 6.0-7.0 mm from a cohort of laboratory-bred snails in Puerto Rico.
Appleton et al. (2009) extrapolated data by Yong et al. (1987), Ferrer López et al. (1989) and by Fernández et al.(1992) and they resulted that sexual maturity is reached at an age of about five months. Reported variation in maturation period varies from 97–143 days (3.2-4.8 months) under the laboratory conditions to 6–12 months, also from laboratory data. It is difficult to relate shell size at the onset of maturity to age since the size structure of populations vary over time and from one locality to another.
Dissection of Tarebia granifera showed blastula
stage embryos in the brood pouches of snails as small as 8 mm shell height. Small numbers of shelled embryos, including veliger
s, were found in snails of 10–14 mm but became more plentiful in snails >14 mm and especially those >20 mm. Importantly, unshelled embryos (blastula, gastrula and trochophore
stages) were not found in snails >16 mm and the numbers of shelled embryos themselves decreased in the largest snails, >24 mm. This suggests that differentiation of germinal cells
in the ovary and their subsequent arrival in the brood pouch as blastulae is not a continuous process over a breeding season but occurs as one or more ‘cohorts’ or ‘pulses’ which stop before the birth rate of young snails reaches its maximum. So it seems that while the first birth may occur in snails as small as 8 mm, these are few and most juveniles are born to snails >14 mm. The size of the shell of the parent at peak release of juveniles is 24.0 mm.
The reproductive biology
of Tarebia granifera needs to be investigated in detail before its population dynamics
can be properly interpreted from quantitative sampling.
for a variety of trematodes in its native south east Asia. Amongst these are several species of the family Heterophyidae
some of which have been reported as opportunistic infections in people, and another, Centrocestus formosanus
(Nishigori, 1924), is an important gill parasite of fish. Tarebia granifera also serves as intermediate host for the philopthalmid eyefluke Philopthalmus gralli Mathis & Ledger, 1910 which has recently (2005) been reported affecting ostrich
es Struthio camelus on farms in Zimbabwe. The snail host implicated in this outbreak was Melanoides tuberculata but the rapid spread and high population densities achieved by Tarebia granifera, which appears to be replacing Melanoides tuberculata in South Africa, may exacerbate the problem in the future.
For many years Tarebia granifera was believed to be an intermediate host for the Asian lungfluke Paragonimus westermani
(Kerbert, 1878), but Michelson showed in 1992 that this was erroneous.
and have displaced the vegetation-associated pulmonate Biomphalaria glabrata
from streams and ponds on several Caribbean islands. Although the responsible mechanism is not understood, this has led to suggestions that it could be useful as a biocontrol
agent in snail control operations within integrated schistosomiasis
control programmes. They probably also compete
for space and resources (e.g. food) with indigenous infaunal and epifaunal invertebrates, especially where its densities are high. Under such conditions it is likely to alter the structure and biodiversity
of the entire benthic communities of invaded habitats and perhaps the vegetation-associated communities as well.
Anecdotal reports and observations suggest that in KwaZulu-Natal
the indigenous thiarid Melanoides tuberculata is becoming less common and pressure from the spread of Tarebia granifera, particularly at high densities, is a possible explanation. Like Tarebia granifera, Melanoides tuberculata is parthenogenetic and ovoviviparous, grows to a similar size, are similar in size at first birth and juvenile output. Data from several habitats where the species occur sympatrically show however that in all such situations Tarebia granifera becomes numerically dominant.
Tarebia granifera is likely to impact on another South-African indigenous thiarid, the poorly known Thiara amarula in the saline St. Lucia estuary system.
Studies on the ecological impact of Tarebia granifera are urgently needed.
s, dams and ponds on the premises of three large industrial plants in northern KwaZulu-Natal and been pumped out of at least one of them, blocking water pipe
s and damaging equipment. This generally happens when snail densities are high and the damage is due to individuals being crushed so that pieces of shell and soft tissue are carried into machinery. Details of the nature and extent of this damage and the costs incurred are not available. There is no doubt that Tarebia granifera is able to pass unharmed through pumps, probably as juveniles.
Common name
A common name of a taxon or organism is a name in general use within a community; it is often contrasted with the scientific name for the same organism...
in the aquarium industry the quilted melania, is a species
Species
In biology, a species is one of the basic units of biological classification and a taxonomic rank. A species is often defined as a group of organisms capable of interbreeding and producing fertile offspring. While in many cases this definition is adequate, more precise or differing measures are...
of freshwater snail
Freshwater snail
A freshwater snail is one kind of freshwater mollusc, the other kind being freshwater clams and mussels, i.e. freshwater bivalves. Specifically a freshwater snail is a gastropod that lives in a watery non-marine habitat. The majority of freshwater gastropods have a shell, with very few exceptions....
with an operculum
Operculum (gastropod)
The operculum, meaning little lid, is a corneous or calcareous anatomical structure which exists in many groups of sea snails and freshwater snails, and also in a few groups of land snails...
, an aquatic
Aquatic animal
An aquatic animal is an animal, either vertebrate or invertebrate, which lives in water for most or all of its life. It may breathe air or extract its oxygen from that dissolved in water through specialised organs called gills, or directly through its skin. Natural environments and the animals that...
gastropod mollusk in the family Thiaridae
Thiaridae
Thiaridae, common name thiarids, is a family of tropical freshwater snails with an operculum, aquatic gastropod mollusks in the superfamily Cerithioidea....
. This snail is native to south-eastern Asia, but it has become an invasive species
Invasive species
"Invasive species", or invasive exotics, is a nomenclature term and categorization phrase used for flora and fauna, and for specific restoration-preservation processes in native habitats, with several definitions....
in numerous countries.
Subspecies
Subspecies of Tarebia granifera include:- Tarebia granifera granifera (Lamarck, 1822)
- Tarebia granifera mauiensis Brot, 1877
Description
A detailed account of the anatomy of Tarebia granifera was given by R. Tucker AbbottR. Tucker Abbott
Robert Tucker Abbott was an American conchologist and malacologist . He was the author of more than 30 books on malacology, which have been translated into many languages....
in 1952 together with notes on its biology and bionomics. A dissection guide was provided by Malek (1962).
The maximum height of adult shells of this species from South Africa is from 18.5 mm to 25.1 mm, while in Puerto Rico they can reach up to 35 mm.
Two color forms of Tarebia granifera are found, one has a pale brown body whorl
Body whorl
Body whorl is part of the morphology of a coiled gastropod mollusk.- In gastropods :In gastropods, the body whorl, or last whorl, is the most recently-formed and largest whorl of a spiral or helical shell, terminating in the aperture...
and a dark spire
Spire (mollusc)
A spire is a descriptive term for part of the coiled shell of mollusks. The word is a convenient aid in describing shells, but it does not refer to a very precise part of shell anatomy: the spire consists of all of the whorls except for the body whorl...
(see photo on the right) and in the other the shell is entirely dark brown to almost black (see photo on the left). Intermediate forms exist.
Indigenous distribution
The indigenous distribution of this species includes the general area of these countries: India, Sri Lanka, Philippines, Hawaii, southern Japan, Society IslandsSociety Islands
The Society Islands are a group of islands in the South Pacific Ocean. They are politically part of French Polynesia. The archipelago is generally believed to have been named by Captain James Cook in honor of the Royal Society, the sponsor of the first British scientific survey of the islands;...
, Taiwan, Hong Kong, Thailand.
Nonidigenous distribution
Tarebia granifera has become invasive on at least three continents:North and South America and Africa. Initial introductions were presumably via the aquarium trade.Americas:
- It occurs in several southern states of the U.S.A.: Puerto Rico, Florida, Texas and IdahoIdahoIdaho is a state in the Rocky Mountain area of the United States. The state's largest city and capital is Boise. Residents are called "Idahoans". Idaho was admitted to the Union on July 3, 1890, as the 43rd state....
- Hawaii
- Many Caribbean islands:
- Cuba - also with Physella acutaPhysella acutaPhysella acuta, common name the European physa, is a species of small, left-handed or sinistral, air-breathing freshwater snail, an aquatic gastropod mollusk in the family Physidae.-Shell description:...
it is the most common freshwater snail in Cuba - The Dominican Republic
- Saint LuciaSaint LuciaSaint Lucia is an island country in the eastern Caribbean Sea on the boundary with the Atlantic Ocean. Part of the Lesser Antilles, it is located north/northeast of the island of Saint Vincent, northwest of Barbados and south of Martinique. It covers a land area of 620 km2 and has an...
- Martinique since 1991
- Cuba - also with Physella acuta
- Central America: Mexico
- El Hatillo Municipality, Miranda, Venezuela
Africa:
- South Africa The Tarebia granifera was reported from South Africa (and Africa) for the first time in 1999 in northern KwaZulu-NatalKwaZulu-NatalKwaZulu-Natal is a province of South Africa. Prior to 1994, the territory now known as KwaZulu-Natal was made up of the province of Natal and the homeland of KwaZulu....
though it was probably introduced sometime prior to 1996. In the 10 years since its discovery it has spread rapidly, particularly northwards, into MpumalangaMpumalangaMpumalanga , is a province of South Africa. The name means east or literally "the place where the sun rises" in Swazi, Xhosa, Ndebele and Zulu. Mpumalanga lies in eastern South Africa, north of KwaZulu-Natal and bordering Swaziland and Mozambique. It constitutes 6.5% of South Africa's land area...
province, the Kruger National ParkKruger National ParkKruger National Park is one of the largest game reserves in Africa. It covers and extends from north to south and from east to west.To the west and south of the Kruger National Park are the two South African provinces of Limpopo and Mpumalanga. In the north is Zimbabwe, and to the east is...
and SwazilandSwazilandSwaziland, officially the Kingdom of Swaziland , and sometimes called Ngwane or Swatini, is a landlocked country in Southern Africa, bordered to the north, south and west by South Africa, and to the east by Mozambique...
.
This spread will doubtless continue into northern South Africa, Moçambique, Zimbabwe and beyond. It has not been possible to calculate the rate of dispersal.
Asia:
- Israel (non-indigenous)
Habitat
In the South Africa, the snail has colonized different types of habitat, from rivers, lakes and irrigation canals to concrete lined reservoirs and ornamental ponds. It reaches very high densities, up to 21 000 m², and is likely to impact on the entire indigenous benthosBenthos
Benthos is the community of organisms which live on, in, or near the seabed, also known as the benthic zone. This community lives in or near marine sedimentary environments, from tidal pools along the foreshore, out to the continental shelf, and then down to the abyssal depths.Many organisms...
of the natural waterbodies of the region – more so than any other invasive freshwater invertebrate known from the South Africa. The South African indigenous thiarids Thiara amarula, Melanoides tuberculata, and Cleopatra ferruginea
Cleopatra ferruginea
Cleopatra ferruginea is a species of freshwater snails with an operculum, aquatic gastropod molluscs in the family Paludomidae.This species is found in Burundi, Egypt, Ethiopia, Kenya, Sudan, Tanzania, Uganda and South Africa....
are considered particularly vulnerable.
Most localities in South Africa (93%) lie below an altitude of 300 m above sea level where an estimated area of 39 500 km2 has been colonized. The only known localities outside this area are the Umsinduzi River in Pietermaritzburg
Pietermaritzburg
Pietermaritzburg is the capital and second largest city in the province of KwaZulu-Natal, South Africa. It was founded in 1838, and is currently governed by the Msunduzi Local Municipality. Its "purist" Zulu name is umGungundlovu, and this is the name used for the district municipality...
and its confluence with the Umgeni River which lie closer to 500 m. R. Tucker Abbott
R. Tucker Abbott
Robert Tucker Abbott was an American conchologist and malacologist . He was the author of more than 30 books on malacology, which have been translated into many languages....
(1952) noted that on Guam
Guam
Guam is an organized, unincorporated territory of the United States located in the western Pacific Ocean. It is one of five U.S. territories with an established civilian government. Guam is listed as one of 16 Non-Self-Governing Territories by the Special Committee on Decolonization of the United...
Island, Tarebia granifera occurred in streams and rivers at 983 m altitude but that these watercourses were consistently above 24°C indicating that temperature may be an important determinant of distribution.
Tarebia granifera also occurs in several estuaries along the KwaZulu-Natal coast. Prominent among these is the dense population (±6038 m2) found at a salinity
Salinity
Salinity is the saltiness or dissolved salt content of a body of water. It is a general term used to describe the levels of different salts such as sodium chloride, magnesium and calcium sulfates, and bicarbonates...
of 9.98‰ (28.5% sea water) in Catalina Bay, Lake St Lucia, iSimangaliso Wetland Park, KwaZulu-Natal. These records show that Tarebia granifera is able to colonize brackish and moderately saline habitats and reach high densities there. From observations in Puerto Rico
Puerto Rico
Puerto Rico , officially the Commonwealth of Puerto Rico , is an unincorporated territory of the United States, located in the northeastern Caribbean, east of the Dominican Republic and west of both the United States Virgin Islands and the British Virgin Islands.Puerto Rico comprises an...
it was suggested that snails could survive temporarily saline conditions for several weeks by burying themselves in the substratum
Substratum
In linguistics, a stratum or strate is a language that influences, or is influenced by another through contact. A substratum is a language which has lower power or prestige than another, while a superstratum is the language that has higher power or prestige. Both substratum and superstratum...
, emerging when fresh water returned.
In common with other Thiaridae, Tarebia granifera is primarily a benthic species and in South Africa has been collected on a variety of substrata in both natural and artificial waterbodies, e.g. sand, mud, rock, concrete bridge foundations and the concrete walls and bottoms of reservoirs, irrigation canals and ornamental ponds. Many of these habitats were vegetated and the associated vegetation included many types of emergent
Emergent
It may also mean:* Emergent , Neural Simulation Software* Emergent , a 2003 album by Gordian Knot* emergent plant, a plant which grows in water but which pierces the surface so that it is partially in air...
monocotyledons (e.g. Cyperus papyrus
Cyperus papyrus
Cyperus papyrus is a monocot belonging to the sedge family Cyperaceae. It is a herbaceous perennial native to Africa, and forms tall stands of reed-like swamp vegetation in shallow water....
, Scirpus
Scirpus
The plant genus Scirpus consists of a large number of aquatic, grass-like species in the family Cyperaceae , many with the common names club-rush or bulrush . Other common names are deergrass or grassweed.The genus has a cosmopolitan distribution, and grows in wetlands and moist soil...
sp., Typha
Typha
Typha is a genus of about eleven species of monocotyledonous flowering plants in the family Typhaceae. The genus has a largely Northern Hemisphere distribution, but is essentially cosmopolitan, being found in a variety of wetland habitats...
sp., Phragmites
Phragmites
Phragmites, the Common reed, is a large perennial grass found in wetlands throughout temperate and tropical regions of the world. Phragmites australis is sometimes regarded as the sole species of the genus Phragmites, though some botanists divide Phragmites australis into three or four species...
sp.) and dicotyledons (e.g. Ceratophyllum demersum
Ceratophyllum demersum
Ceratophyllum demersum is a species of Ceratophyllum. It is a submerged, free-floating aquatic plant, native to North America but nowadays having a cosmopolitan distribution in temperate and tropical regions...
, Potamogeton crispus, Nymphaea nouchali
Nymphaea nouchali
Nymphaea nouchali, commonly known as the Red and blue water lily, Blue star water lily, Star lotus, or by its synonym Nymphaea stellata, is a water lily of genus Nymphaea.-Distribution and habitat:...
). Where densities are high, Tarebia granifera may also occur on marginal, trailing vegetation and the floating Common Water Hyacinth Eichhornia crassipes
Eichhornia crassipes
Eichhornia crassipes, commonly known as Common Water Hyacinth, is an aquatic plant native to the Amazon basin, and is often considered a highly problematic invasive species outside its native range.-Ecology:...
as well. It favours turbulent water and tolerates current speeds up to 1.2m.s−1 and possibly greater. This habitat range is similar to that recorded for Tarebia granifera in Puerto Rico.
The major interest in Tarebia granifera outside Asia today is its invasive ability and its impact on indigenous benthic communities
Benthos
Benthos is the community of organisms which live on, in, or near the seabed, also known as the benthic zone. This community lives in or near marine sedimentary environments, from tidal pools along the foreshore, out to the continental shelf, and then down to the abyssal depths.Many organisms...
in colonized waterbodies.
Typically half or more of these snails were buried in the sediment
Sediment
Sediment is naturally occurring material that is broken down by processes of weathering and erosion, and is subsequently transported by the action of fluids such as wind, water, or ice, and/or by the force of gravity acting on the particle itself....
s and were not visible from the surface. This was also noticed in aquaria
Aquarium
An aquarium is a vivarium consisting of at least one transparent side in which water-dwelling plants or animals are kept. Fishkeepers use aquaria to keep fish, invertebrates, amphibians, marine mammals, turtles, and aquatic plants...
where they actively buried themselves in sand. Exact proportion of population of Tarebia granifera that is buried at any time is not known. There is also not known how long can snails remain buried.
Tarebia granifera will die at the temperature 7 °C in aquaria, but they do not live in water temperature under 10 °C in the wild.
Dispersal
It is probable that dispersalBiological dispersal
Biological dispersal refers to species movement away from an existing population or away from the parent organism. Through simply moving from one habitat patch to another, the dispersal of an individual has consequences not only for individual fitness, but also for population dynamics, population...
of Tarebia granifera from one waterbody or river catchment to another occurs passively via birds, notably waterfowl
Waterfowl
Waterfowl are certain wildfowl of the order Anseriformes, especially members of the family Anatidae, which includes ducks, geese, and swans....
, which eat them and void them later, perhaps in another habitat. Evidence for this comes from the finding of many small Tarebia granifera 5–7 mm in height and still containing the soft parts in unidentified bird droppings from the bank of the Mhlali River, South Africa. Even though the shell of Tarebia granifera is thick, most of these juveniles had been partially crushed with only a few still intact. Both the intact and damaged specimens could have been alive when passed and perhaps survived had they been deposited in water. None was large enough to have been reproductively mature (see below) and would have needed to survive in any new habitat for several months before reproducing.
Passive dispersal may also occur via weed on boats and boat trailers and via water pumped from one waterbody to another for industrial and irrigation purposes. In the Nseleni River juvenile Tarebia granifera were commonly found with another invasive snail, Pseudosuccinea columella
Pseudosuccinea columella
Pseudosuccinea columella, common name the "American ribbed fluke snail", is a species of air-breathing freshwater snail, an aquatic pulmonate gastropod mollusk in the family Lymnaeidae, the pond snails....
, on floating clumps of water hyacinth Eichhornia crassipes which provide a vehicle for rapid downstream dispersal.
Once established in a particular waterbody Tarebia granifera is likely to disperse actively, both up and downstream in the case of flowing systems, as far as environmental factors like current speed and food availability will allow. The snail’s tolerance of turbulent, flowing water was demonstrated by Prentice (1983) who reported it migrating upstream on the Caribbean island of Saint Lucia
Saint Lucia
Saint Lucia is an island country in the eastern Caribbean Sea on the boundary with the Atlantic Ocean. Part of the Lesser Antilles, it is located north/northeast of the island of Saint Vincent, northwest of Barbados and south of Martinique. It covers a land area of 620 km2 and has an...
at a rate of 100 m month−1 in streams discharging up to 50 l.s−1. In KwaZulu-Natal it has been collected in water flowing at up to 1.2 m.s−1 which is likely to exceed the current speeds of at least the lower and middle reaches of many rivers and streams in South Africa making these watercourses open to colonization.
The sole
Sole
Sole may refer to:* Sole , the bottom of the foot* Sole , the bottom supporting member of the shoe-Business:* Sole proprietorship, a business which legally has no separate existence from its owner...
of Tarebia granifera is proportionally small when compared to other thiarids and smaller snails with their higher coefficients were less able to grip the substratum in the face of moving water and so not did disperse as effectively as larger ones.
Density
In Florida Tucker Abbott (1952) recorded a densityPopulation density
Population density is a measurement of population per unit area or unit volume. It is frequently applied to living organisms, and particularly to humans...
of Tarebia granifera 4444 m−2 which falls within the range of densities measured with a Van Veen grab in a number of sites in northern KwaZulu-Natal, where was measured desnsities 843.6 ±320.2 m−2 to 20764.4 ±13828.1 m−2. The site with such high density was non-flowing, devoid of rooted vegetation but it was shaded by trees (Barringtonia racemosa
Barringtonia racemosa
Barringtonia racemosa is a tree in the family Lecythidaceae. It is commonly known as the Powder-puff Tree. It is found in coastal swamp forests and on the edges of estuaries in the Indian Ocean, starting at the east coast of Mozambique and KwaZulu-Natal to Madagascar, India, Sri Lanka, Malaysia,...
) and by floating Eichhornia crassipes
Eichhornia crassipes
Eichhornia crassipes, commonly known as Common Water Hyacinth, is an aquatic plant native to the Amazon basin, and is often considered a highly problematic invasive species outside its native range.-Ecology:...
. This between-site variability may be positively correlated to habitat heterogeneity
Spatial heterogeneity
Spatial heterogeneity is a property generally ascribed to a landscape or to a population. It refers to the uneven distribution of various concentrations of each species within an area. A landscape with spatial heterogeneity has a mix of concentrations of multiple species of plants or animals , or...
and food availability. Despite the very high densities recorded in the Nseleni River, indigenous invertebrates were still present in the sediments including: bivalve Chambardia wahlbergi, chironomids, oligochaetes (tubificids) and burrowing polychaetes were also found but in very low numbers.
The low densities of Tarebia granifera reported for the Mhlatuze River, South Africa may have been influenced by nearby sand-mining activities or, more likely, high flows and mobile sediments, but they nevertheless approach those recorded by Dudgeon (1980) for Tarebia granifera in its native Hong Kong
Hong Kong
Hong Kong is one of two Special Administrative Regions of the People's Republic of China , the other being Macau. A city-state situated on China's south coast and enclosed by the Pearl River Delta and South China Sea, it is renowned for its expansive skyline and deep natural harbour...
(18–193 m−2).
Little is known of the long term population fluctuations of Tarebia granifera and findings seem to be contradictory. Studies in Cuba (Yong et al. (1987), Ferrer López et al. (1989), Fernández et al. (1992)) indicate that the snail lives for more than a year though maximum densities were recorded at different times of the year in different habitats. Using a catch per unit effort
Catch per unit effort
In fisheries and conservation biology, the catch per unit effort is an indirect measure of the abundance of a target species. Changes in the catch per unit effort are inferred to signify changes to the target species' true abundance...
netting technique, Yong et al. (1987) and Ferrer López et al. (1989) found highest densities in summer when temperatures reached their maximum whereas Fernández et al. (1992) found highest densities in November (late autumn) when temperatures reached their minimum. Fernández et al. (1992) also suggested that Tarebia granifera density was positively correlated with Ca2+
Calcium in biology
Calcium plays a pivotal role in the physiology and biochemistry of organisms and the cell. It plays an important role in signal transduction pathways, where it acts as a second messenger, in neurotransmitter release from neurons, contraction of all muscle cell types, and fertilization...
concentrations and negatively with NH4
Ammonium
The ammonium cation is a positively charged polyatomic cation with the chemical formula NH. It is formed by the protonation of ammonia...
concentrations.
Recent surveys by Vázquez et al. (2010) of Pinar del Río Province
Pinar del Río Province
Pinar del Río is one of the provinces of Cuba. It is at the western end of the island of Cuba.-Geography:The Pinar del Río province is Cuba's westernmost province and contains one of Cuba's three main mountain ranges, the Cordillera de Guaniguanico, divided into the easterly Sierra del Rosario and...
, Cuba have reported population densities of Tarebia granifera of 85 individuals/m2, well above those of its endemic relatives (5 individuals/m2).
Feeding habits
Tarebia granifera feeds on algae, diatoms and detritusDetritus
Detritus is a biological term used to describe dead or waste organic material.Detritus may also refer to:* Detritus , a geological term used to describe the particles of rock produced by weathering...
.
Life cycle
Tarebia granifera is both parthenogeneticParthenogenesis
Parthenogenesis is a form of asexual reproduction found in females, where growth and development of embryos occur without fertilization by a male...
and ovoviviparous, although males have been reported. These are characteristics which are undoubtedly key to its success as an invader. For example no males have been found amongst hundreds dissected from KwaZulu-Natal, it is probable that a few are present. Males were found in most (6/7) populations examined in Puerto Rico
Puerto Rico
Puerto Rico , officially the Commonwealth of Puerto Rico , is an unincorporated territory of the United States, located in the northeastern Caribbean, east of the Dominican Republic and west of both the United States Virgin Islands and the British Virgin Islands.Puerto Rico comprises an...
but were generally uncommon at up to 22.7% of the population (mean 4.6%). Live sperm were present in the testes of these males but the genitalia
Reproductive system of gastropods
The reproductive system of gastropods varies greatly from one group to another within this very large and diverse taxonomic class of animals...
were apparently non-functional. R. Tucker Abbott (1952) failed to find sperm in the gonads of male Tarebia granifera from Florida. Most Tarebia granifera are therefore clones
Cloning
Cloning in biology is the process of producing similar populations of genetically identical individuals that occurs in nature when organisms such as bacteria, insects or plants reproduce asexually. Cloning in biotechnology refers to processes used to create copies of DNA fragments , cells , or...
of the female parent.
Embryo
Embryo
An embryo is a multicellular diploid eukaryote in its earliest stage of development, from the time of first cell division until birth, hatching, or germination...
s develop in a brood pouch. This pouch is a compartmentalized structure lying immediately above the oesophagus and develops only after the snail has reached maturity. Its size expands as the number of embryos increases. Tarebia granifera has 1-77 embryos in its brood pouch.
Tucker Abbott (1952), Chaniotis et al. (1980) and WHO (1981) cite the same statistic that females can give birth to one juvenile every 12 hours! Young snails emerge through a birth pore on the right side of the head. The newborn shell is <1–2 mm in height with between 1.5 and 4.8 whorls. The size of juveniles at birth is 0.7-2.1 mm. According to Chen (2003) these newborns have a high survival rate in the field.
Attainment of sexual maturity
Sexual maturity
Sexual maturity is the age or stage when an organism can reproduce. It is sometimes considered synonymous with adulthood, though the two are distinct...
in Tarebia granifera is generally indicated by the size of the smallest snail observed to give birth rather than a histological assessment of the development of the gonad and associated reproductive structures. Appleton & Nadasan (2002) estimated onset of maturity at 10–12 mm shell height but unpublished data suggest a height closer to 8 mm in line with other published studies. Tucker Abbott (1952) estimated sexual maturity at between 5.5 and 8.0 mm at different stations over a short stretch of river in Florida. Chaniotis et al. (1980) gave a similar estimate of 6.0-7.0 mm from a cohort of laboratory-bred snails in Puerto Rico.
Appleton et al. (2009) extrapolated data by Yong et al. (1987), Ferrer López et al. (1989) and by Fernández et al.(1992) and they resulted that sexual maturity is reached at an age of about five months. Reported variation in maturation period varies from 97–143 days (3.2-4.8 months) under the laboratory conditions to 6–12 months, also from laboratory data. It is difficult to relate shell size at the onset of maturity to age since the size structure of populations vary over time and from one locality to another.
Dissection of Tarebia granifera showed blastula
Blastula
The blastula is a hollow sphere of cells formed during an early stage of embryonic development in animals . The blastula is created when the zygote undergoes the cell division process known as cleavage. The blastula is preceded by the morula and is followed by the gastrula in the developmental...
stage embryos in the brood pouches of snails as small as 8 mm shell height. Small numbers of shelled embryos, including veliger
Veliger
A veliger is the planktonic larva of many kinds of marine and freshwater gastropod molluscs, as well as most bivalve mollusks.- Description :...
s, were found in snails of 10–14 mm but became more plentiful in snails >14 mm and especially those >20 mm. Importantly, unshelled embryos (blastula, gastrula and trochophore
Trochophore
A trochophore is a type of free-swimming planktonic marine larva with several bands of cilia.By moving their cilia rapidly, a water eddy is created. In this way they control the direction of their movement...
stages) were not found in snails >16 mm and the numbers of shelled embryos themselves decreased in the largest snails, >24 mm. This suggests that differentiation of germinal cells
Germ cell
A germ cell is any biological cell that gives rise to the gametes of an organism that reproduces sexually. In many animals, the germ cells originate near the gut of an embryo and migrate to the developing gonads. There, they undergo cell division of two types, mitosis and meiosis, followed by...
in the ovary and their subsequent arrival in the brood pouch as blastulae is not a continuous process over a breeding season but occurs as one or more ‘cohorts’ or ‘pulses’ which stop before the birth rate of young snails reaches its maximum. So it seems that while the first birth may occur in snails as small as 8 mm, these are few and most juveniles are born to snails >14 mm. The size of the shell of the parent at peak release of juveniles is 24.0 mm.
The reproductive biology
Reproductive biology
Reproductive biology is a study mainly involving the reproductive system and sex organs. It is closely related to reproductive endocrinology and infertility. also is miotosis and miosis...
of Tarebia granifera needs to be investigated in detail before its population dynamics
Population dynamics
Population dynamics is the branch of life sciences that studies short-term and long-term changes in the size and age composition of populations, and the biological and environmental processes influencing those changes...
can be properly interpreted from quantitative sampling.
Parasites
Tarebia granifera serves as the first intermediate hostIntermediate host
A secondary host or intermediate host is a host that harbors the parasite only for a short transition period, during which some developmental stage is completed. For trypanosomes, the cause of sleeping sickness, humans are the primary host, while the tsetse fly is the secondary host...
for a variety of trematodes in its native south east Asia. Amongst these are several species of the family Heterophyidae
Heterophyidae
Heterophyidae is a family of intestinal flukes of the class trematoda.Tegument covered by spines. Oral sucker not armed or armed by cyrcumoral spines. Pharynx presented. Genital synus presented. Ventral and genital suckers ussualy not combined. Cirrus and bursa absent. Two testes located in...
some of which have been reported as opportunistic infections in people, and another, Centrocestus formosanus
Centrocestus formosanus
Centrocestus formosanus is a trematode parasite of Asian origin that has found its way in to North American streams and rivers. It not only affects the fountain darter but many species of commercially important fishes....
(Nishigori, 1924), is an important gill parasite of fish. Tarebia granifera also serves as intermediate host for the philopthalmid eyefluke Philopthalmus gralli Mathis & Ledger, 1910 which has recently (2005) been reported affecting ostrich
Ostrich
The Ostrich is one or two species of large flightless birds native to Africa, the only living member of the genus Struthio. Some analyses indicate that the Somali Ostrich may be better considered a full species apart from the Common Ostrich, but most taxonomists consider it to be a...
es Struthio camelus on farms in Zimbabwe. The snail host implicated in this outbreak was Melanoides tuberculata but the rapid spread and high population densities achieved by Tarebia granifera, which appears to be replacing Melanoides tuberculata in South Africa, may exacerbate the problem in the future.
For many years Tarebia granifera was believed to be an intermediate host for the Asian lungfluke Paragonimus westermani
Paragonimus westermani
Paragonimus westermani is a lung fluke and is most prominent in Asia and South America. It was discovered from two Bengal tigers that died in zoos in Europe in 1878...
(Kerbert, 1878), but Michelson showed in 1992 that this was erroneous.
Other interspecific relationships
Tarebia granifera have been associated with the disappearance of two indigenous benthic gastropod species from rivers in Puerto RicoPuerto Rico
Puerto Rico , officially the Commonwealth of Puerto Rico , is an unincorporated territory of the United States, located in the northeastern Caribbean, east of the Dominican Republic and west of both the United States Virgin Islands and the British Virgin Islands.Puerto Rico comprises an...
and have displaced the vegetation-associated pulmonate Biomphalaria glabrata
Biomphalaria glabrata
Biomphalaria glabrata is a species of air-breathing freshwater snail, an aquatic pulmonate gastropod mollusk in the family Planorbidae, the ram's horn snails....
from streams and ponds on several Caribbean islands. Although the responsible mechanism is not understood, this has led to suggestions that it could be useful as a biocontrol
BioControl
BioControl is a peer-reviewed scientific journal published by Springer Science+Business Media covering all aspects of basic and applied research in biological control of invertebrate, vertebrate, and weed pests, and plant diseases. The journal was established in 1956 as Entomophaga and published by...
agent in snail control operations within integrated schistosomiasis
Schistosomiasis
Schistosomiasis is a parasitic disease caused by several species of trematodes , a parasitic worm of the genus Schistosoma. Snails often act as an intermediary agent for the infectious diseases until a new human host is found...
control programmes. They probably also compete
Competition (biology)
Competition is an interaction between organisms or species, in which the fitness of one is lowered by the presence of another. Limited supply of at least one resource used by both is required. Competition both within and between species is an important topic in ecology, especially community ecology...
for space and resources (e.g. food) with indigenous infaunal and epifaunal invertebrates, especially where its densities are high. Under such conditions it is likely to alter the structure and biodiversity
Biodiversity
Biodiversity is the degree of variation of life forms within a given ecosystem, biome, or an entire planet. Biodiversity is a measure of the health of ecosystems. Biodiversity is in part a function of climate. In terrestrial habitats, tropical regions are typically rich whereas polar regions...
of the entire benthic communities of invaded habitats and perhaps the vegetation-associated communities as well.
Anecdotal reports and observations suggest that in KwaZulu-Natal
KwaZulu-Natal
KwaZulu-Natal is a province of South Africa. Prior to 1994, the territory now known as KwaZulu-Natal was made up of the province of Natal and the homeland of KwaZulu....
the indigenous thiarid Melanoides tuberculata is becoming less common and pressure from the spread of Tarebia granifera, particularly at high densities, is a possible explanation. Like Tarebia granifera, Melanoides tuberculata is parthenogenetic and ovoviviparous, grows to a similar size, are similar in size at first birth and juvenile output. Data from several habitats where the species occur sympatrically show however that in all such situations Tarebia granifera becomes numerically dominant.
Tarebia granifera is likely to impact on another South-African indigenous thiarid, the poorly known Thiara amarula in the saline St. Lucia estuary system.
Studies on the ecological impact of Tarebia granifera are urgently needed.
Human importance
In addition to its role as intermediate host for several economically important trematode species, Tarebia granifera has colonized water reservoirWater reservoir
A reservoir , artificial lake or dam is used to store water.Reservoirs may be created in river valleys by the construction of a dam or may be built by excavation in the ground or by conventional construction techniques such as brickwork or cast concrete.The term reservoir may also be used to...
s, dams and ponds on the premises of three large industrial plants in northern KwaZulu-Natal and been pumped out of at least one of them, blocking water pipe
Water pipe
Water pipes are pipes or tubes, frequently made of polyvinyl chloride , ductile iron, steel, cast iron, polypropylene, polyethylene, or copper, that carry pressurized and treated fresh water to buildings , as well as inside the building.-History:For many centuries, lead was the favoured material...
s and damaging equipment. This generally happens when snail densities are high and the damage is due to individuals being crushed so that pieces of shell and soft tissue are carried into machinery. Details of the nature and extent of this damage and the costs incurred are not available. There is no doubt that Tarebia granifera is able to pass unharmed through pumps, probably as juveniles.
Further reading
- Butler J. M., Ferguson F. F., Palmer J. R. & Jobin W. R. (1980). "Displacement of a colony of Biomphalaria glabrata by an invading population of Tarebia granifera in a small stream in Puerto Rico". Caribbean Journal of ScienceCaribbean Journal of ScienceThe Caribbean Journal of Science is a peer-reviewed scientific journal publishing articles, research notes, and book reviews related to science in the Caribbean, with an emphasis on botany, zoology, ecology, conservation biology, geology, archaeology, and paleontology...
16: 73-79. PDF. - Chaniotis B. N., Butler J. M., Ferguson F. F. & Jobin W. R. (1980). "Thermal limits, desiccation tolerance, and humidity reactions of Thiara (Tarebia) granifera mauiensis (Gastropoda: Thiaridae) host of the asiatic lung fluke disease". Caribbean Journal of ScienceCaribbean Journal of ScienceThe Caribbean Journal of Science is a peer-reviewed scientific journal publishing articles, research notes, and book reviews related to science in the Caribbean, with an emphasis on botany, zoology, ecology, conservation biology, geology, archaeology, and paleontology...
16: 91-93. PDF. - Ferguson et al. (1958). "Potential for Biological Control of Australorbis Glabratus, the Intermediate Host of Puerto Rican Schistosomiasis". The American Journal of Tropical Medicine and Hygiene 7: 491-493.
- Miranda N., Perissinotto R. & Appleton C. (2010). "Salinity and temperature tolerance of the invasive freshwater gastropod Tarebia granifera". South African Journal of ScienceSouth African Journal of ScienceThe South African Journal of Science is a peer-reviewed multidisciplinary academic journal and the official publication of the Academy of Science of South Africa. It covers research in any field of interest to more than one discipline and with a regional focus on Africa. According to the Journal...
106(3/4): 7 pages. doi:10.4102/sajs.v106i3/4.156. - Miranda N. A. F., Perissinotto R. & Appleton C. C. (2011). "Population Structure of an Invasive Parthenogenetic Gastropod in Coastal Lakes and Estuaries of Northern KwaZulu-Natal, South Africa". PLoS ONEPLoS ONEPLoS ONE is an open access peer-reviewed scientific journal published by the Public Library of Science since 2006. It covers primary research from any discipline within science and medicine. All submissions go through an internal and external pre-publication peer review but are not excluded on the...
6(8): e24337. doi:10.1371/journal.pone.0024337.