Bayesian posterior probabilities are listed locality of P. For spe- cific locality information see Additional file 1. Introduced populations of Pomacea canaliculata are genet- ically distinct from those of P. The egg masses of P. California, Hawaii, and Buenos Aires. The Arizona Clutches of Pomacea insularum often exceed 1, eggs sequence differed from the Argentinean one by a single Fig.
The variability in clutch size reported for P. The source of the introduced populations of P. There is some prelimi- the Buenos Aires area [K. Hayes, R. Joshi, S. Cowie, in prep.
In the continental U. The East and West coast populations of apple 1. We found very little genetic variation in P. We have also found populations in ecologically sensitive areas includ- ing Everglades National Park and Loxahatchee National Wildlife Refuge. Pomacea insularum has not been reported previously in the continental U. Specimens identified as P. When, then, did P. Winner [23] reported ampullariids with pink egg masses in Florida fish farms in SPomacea canaliculata col- insularum.
At present, the earliest genetically confirmed Shells of Pomacea insularum and Pomacea canaliculata specimen that is from the location of an extant population collected within the continental U. Pomacea insularum Many populations were discovered in Florida from from Lake Tohopekaliga, Florida; b.
Pomacea canaliculata from Mecca, California. The establishment of P. Howells et al. Pomacea canaliculata was reported in Florida and Texas in insularum as "Pomacea canaliculata-group" in Texas. The the late s, probably based on misidentification of P. The earliest was discovered in in Houston Harris County [33]. The history of other populations in California and Bend, and Chambers [10]. Arizona was reviewed recently [10]. In Georgia, P. Other populations, some established, have since P.
Pomacea insu- been discovered in ponds and streams of the Alabaha larum is reported from Argentina, Brazil [12], and Bolivia River, on St. We sampled a specimen of P. Statistical parsimony analysis showed that responded closely to sequences from several populations the Argentina haplotype was nested within the network of of introduced P. Although the majority of introduced snails sampled were most closely Based on our analyses to date, P. It has been recorded from a formed a distinct well-supported clade Fig.
Bayesian posterior probabilities are listed above branches, bootstrap proportions below. Taxon labels of speci- mens collected from outside the continental U. Relative branch lengths are illustrated in the phylo- gram shown in the inset. Abbreviations are: P. For specific locality infor- mation refer see Additional file 1.
In areas where many populations are in close proximity, a larger circle encompasses the area. Figure 9 network within Pomacea insularum Parsimony In the analysis of all P. Statisti- nested, although not robustly, between two clades made cal parsimony analysis was undertaken using TCS [version up of native-range samples from Brazil Fig.
We do not 1. Shown are the 10 unique know yet whether these two clades differ in ecologically haplotypes listed by locality and identity code see Figure 7; relevant traits. Additional file 1. For specific locality information refer to the corresponding numbered specimen of P. Note that a native range haplotype of P. It lacks a channeled North American haplotypes. The egg masses have an irregular honey- combed appearance, like those of P. Pomacea diffusa out the Amazon Basin.
Pain [19] argued that P. Basin Brazil, Peru, Bolivia. Cowie and Thiengo [12] sug- gested that the latter might deserve full species status, and Thompson [8] recorded this species as P.
Thiengo and Pinellas Counties. We have also collected Cruz, Bolivia, although the species is widespread through- this species in Hillsborough and Collier Counties. It should be sii by Clench [18]. This lack of concern may be unwarranted. The U. Marisa cornuarietis Linnaeus, Department of Agriculture considered it as P. Its egg masses are unique among introduced cluded that it feeds primarily on aufwuchs, not macro- ampullariids in being gelatinous throughout develop- phytes [38].
The potential effects of Pomacea diffusa in ment and in being laid in water [34]. It is widespread in natural habitats are unknown, but a conflicting study northern South America, although the type locality is reports that, in addition to macrophytes, it will feed read- unknown. There are currently two recognized species in ily on animal carcasses, live worms, and the eggs of the genus, M. We planorbid snails [39]. It may therefore have direct effects included samples of both species in our analysis: non- on both aquatic vegetation and native snails and compete native M.
We also included Asolene spixii, which clustered within the Marisa clade, thereby Pomacea insularum and P. The introduced Marisa we threat to agriculture and native wetland ecosystems in the sampled fell within a well-supported clade of Marisa cor- U.
One of the better predictors of the effect of an inva- nuarietis. The poten- Marisa cornuarietis was first discovered in Coral Gables, tial of P. It has spread to many other counties Southeast Asia where its introduction into a tropical wet- in southern Florida [[8], Rawlings and Collins, pers.
Its potential eco- by its devastating effects on agriculture, especially wetland logical impacts have been reviewed recently [10]. Currently, the occurrence of P.
However, it has the potential to Pomacea haustrum is currently of relatively minor concern spread into other areas, including the rice-growing parts in the U. Some of the ecological and agricultural impacts in Asia associated with P. This species is also wide- spread in the region [[27,43], K. Thiengo, and R. Pomacea insularum may therefore be likely to have a significant impact on aquatic ecosystems and pose a threat to crops in the southeastern U. The match of introduced haplotypes of P.
Moreover, P. The species, which seems possible given the close phyloge- average minimum monthly temperature in Buenos Aires netic relationship of P. There is is 4—6 degrees Celsius 39—43 degrees Fahrenheit from also the possibility of competitive interactions between May to September, slightly lower than the average mini- native and non-native snails [49]. Introduced Pomacea mum winter monthly temperatures in Charleston, South spp. Consequently, P. We spread at least this far north on the Atlantic Coastal Plain, have anecdotally noted a decline in abundance or the and through parts of Alabama, Mississippi, Louisiana, and apparent disappearance of P.
Similarly, P. Everglade Snail Kite [52], and an important food for other Ecological niche modeling based on the native and intro- birds, including the limpkin, as well as fish, turtles, and duced range of these species [e.
At Lake Tohopekaliga Collins and Rawlings, refined estimate of potential introduced ranges. An pers. Finally, introduction of all non-native ampullariids is a P. We know nothing at present about the parasites height , low spire, absence of a channel at the suture, and of introduced ampullariids in the continental U. Amp- distinctive egg masses [8]. Mature egg masses have an ullariids, including Pomacea canaliculata, are intermediate average of thirty round pale pink to white eggs averaging hosts of important vertebrate parasites [53], most notably 4 mm in size in grape-like clusters [47] Fig.
Those planning cephalitis [54], and P. Transmission of ida must ensure they have not inadvertently targeted the Parastrongylus infections to mammalian hosts requires native apple snails or their eggs. The spread of Pomacea species may therefore In addition to collateral damage from control of non- facilitate the spread of Parastrongylus species by complet- native species, "extinction by hybridization" [48] could ing the life cycle required to infect mammalian hosts.
In result from hybridization of P. Conclusion Clarification of species identifications, introduced ranges, and native ranges provides a more accurate picture of the tempo of apple snail invasions in the continental U.
The situation is dynamic: during the time in which this paper was written, a new population of apple snails with channeled sutures has been discovered in New Orleans S. Longman, pers. Collins and J. Bernatis, unpublished data Maturation of Pomacea paludosa eggs. Maturation from suggest that a population of P. Considerable work remains to be done. We left , to the mature pinkish white eggs in calcified shells have sampled only about one quarter of the Florida pop- right.
Other species may yet be discovered in introduced chemistry following the manufacturer's protocol PE- populations. At present, a combination of genetic data, ABI. Sequencing reactions were analyzed on an ABI morphological characters, and egg mass morphology is Prism Genetic Analyzer. All samples were sequenced the best strategy for definitive identification.
Higher resolution markers such as microsatellites may be useful in indicat- COI sequences were generated for snails. The 12SS ing the pathways by which non-native snails are spreading region was sequenced for representatives of each unique rapidly through parts of the U.
COI haplotype and locality combination, for a data set of individuals. For some specimens, primarily museum Methods specimens, amplification did not work for all gene Sampling, DNA extraction, and sequencing regions, and different gene regions failed to amplify in dif- We sampled native Pomacea paludosa in Florida and non- ferent snails, resulting in snails with no sequence in com- native apple snails in Florida, Georgia, Texas, California, mon.
This resulted in significant degradation of support Arizona, Hawaii, Cuba, and Guadeloupe in the Lesser values. We therefore selected the 95 individuals with both Antilles [see Additional file 1].
These included taxa identi- gene regions completely sequenced, representing 46 fied as Pomacea canaliculata or Pomacea canaliculata-group, unique haplotypes, for the among-species phylogenetic Pomacea bridgesii, Pomacea haustrum, Marisa cornuarietis, analysis. Nevertheless, some individuals with a great deal Pila conica and Pila polita.
We also sampled native-range of missing data were important for matching introduced populations of Pomacea canaliculata-group snails, Pomacea haplotypes to native ranges, and were therefore used for haustrum, Pomacea diffusa, Pomacea camena, Asolene spixii, within-species analyses and haplotype networks.
Marisa planogyra, and Pila polita. Pila conica was used as an outgroup for phylogenetic analyses [60,61]. The polymerase chain reaction PCR was We used maximum parsimony and Bayesian methods for used to amplify two portions of the mitochondrial phylogenetic analyses.
Maximum parsimony bootstrap genome. This region was gaps treated as missing data. The the cytochrome c oxidase subunit I COI gene amplified COI sequence was divided into 3 partitions by codon using slightly degenerate versions of standard primers position.
We employed 4 the manuscript. We also thank the following inferred when the average standard deviation of split fre- museum staff for assistance with accessing material: Philippe Bouchet and quencies approached 0. To explore further the relationships among introduced haplotypes of P.
We Marisa cornuarietis, Ampullariidae in South Florida. Some museum specimens did not 2. Mochida O: Spread of freshwater Pomacea snails Pilidae, Mol- amplify for all regions, resulting in significant missing lusca from Argentina to Asia.
Micronesica Suppl , Because missing data may cause 3. J Med problems related to calculated distances and collapsing of Appl Malacol , Cowie RH: Apple snails as agricultural pests: their biology, impacts and management. Wallingford: CAB International; University of Science and Technology; Padilla DK, Williams SL: Beyond ballast water: aquarium and the majority of the native-range and the Hawaiian sam- ornamental trades as sources of invasive species in aquatic ecosystems.
Front Ecol Environ , Thompson FG: Freshwater snails of Florida: A manual for sequences and contributed the majority of the continental identification. Gainesville: University of Florida Press; TC and TR 9.
Hubricht L: Pomacea paludosa in Alabama. Nautilus , All authors All authors read and approved the final man- lusca: Gastropoda: Ampullariidae: Asolene, Felipponea, uscript. Marisa, Pomacea, Pomella : a nomenclatural and type cata- log.
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