Current status of the non-indigenous molluscs in Chile, with the first record of Otala punctata (Müller, 1774) (Gastropoda: Helicidae) in the country and new records for Cornu aspersum (Müller, 1774) and Deroceras laeve (Müller, 1774)

A new introduced species, Otala punctata (Müller, 1774) and new records in Chile for Cornu aspersum (Müller, 1774) and Deroceras laeve (Müller, 1774) are documented based on surveys carried out in northern and central areas of the country. The presence and distribution of these alien species are complemented with a comprehensive compilation of all 34 non-indigenous species of marine, freshwater and terrestrial Mollusca in Chile; until 1999, only 16 alien species were known in Chile. Most of these alien species are found exclusively in transformed habitats, few exist in natural environments. The mechanism of introduction for the majority of these non-indigenous species is unknown; however, horticultural development, urban and suburban transformation of original natural habitats, and the aquarium trade are the most likely pathways of introduction. The highest threat of alien species is direct competition and predation of native molluscs, especially the small native land gastropods. Education and continuous field surveys are vital to detect and prevent their propagation as well as to avoid introduction of additional alien taxa.


Introduction
The introduction of non-indigenous species (NIS) of molluscs to Chile almost certainly began with the arrival of the Spanish colonists in the late fifteenth century. However, the oldest confirmed record of introduced molluscs in the country was made by Philippi (1885), who listed three introduced land snail species; Helix aspersa (= Cornu aspersum), Helix costata and Helix pulchella, the latter two with no subsequent records in the literature. The last comprehensive review on the distribution of Chilean molluscan species (Valdovinos 1999), listed 13 nonindigenous taxa, with nine terrestrial and four marine species, representing approximately 3% of all the molluscs recorded in the country. Further studies have added 20 new entries to this NIS list, most of them terrestrial gastropods (Kirch et al. 2009;Cádiz et al. 2013), with a few marine and freshwater species most probably associated with El Niño Southern Oscillation (ENSO) events and with the aquarium trade, respectively (Letelier et al. 2007). Regarding the direct impact of those NIS; it has been established that some alien molluscs, for example species of the genus Oxychilus Fitzinger, 1833, can compete with or feed on local native species, especially microgastropods. Alien species can also be invasive or agricultural pests (species of the genera Deroceras Rafinesque, 1820;Otala Schumacher, 1817 andLimax Linnaeus, 1758), and some introduced freshwater mollusc species (species of the genera Pomacea Perry, 1811 andMelanoides Olivier, 1804) can act as hosts for the parasitic nematode Angiostrongylus cantonensis (Chen, 1933) or the parasitic human lung fluke Paragonimus westermani Kerbert, 1878. Some introduced molluscan species have indirect impacts on the ecosystem, due to the exploitation of native algae for their aquaculture (species of the genus Haliotis Linnaeus, 1758).
Besides documenting for the first time the presence of Otala punctata (Müller, 1774) in Chile, and extending the records of Cornu aspersum (Müller, 1774) and Deroceras laeve (Müller, 1774) for the country, this paper synthesizes all the available records of alien Mollusca recorded so far in the country. This list includes marine, terrestrial and freshwater species that have been introduced into natural environments, species introduced for aquaculture, species whose reports are associated with ENSO events, and species whose introduction was accidental or for which the pathway is unknown. Because little has been published on this group in Chile, information regarding the presence, distribution and possible impacts of these species is crucial for future biodiversity studies.

Methods
A survey of 12 localities in the regions of Iquique, Antofagasta and Atacama, northern Chile, and in the region Metropolitana, central Chile, was made in the southern summer and winter of 2012 and 2013 (Table 1). This information was complemented by an extensive bibliographic compilation on the occurrence of NIS in Chile, compiled from Boyko and Cordeiro (2001), Castilla et al. (2005), Letelier et al. (2007), Ashton et al. (2008), Kirch et al. (2009), Rumi et al. (2010, Landler and Nuñez (2012), Cádiz et al. (2013) and references therein. All the material collected in the field surveys was deposited in the collections of the Museo de Zoología de la Universidad de Concepción (MZUC) and of the Museo Paleontológico de Caldera (MPC).
The systematic affinity, geographical range, ecosystems affected, possible impacts, mode of entry and year of first record are indicated for each species included in this review. The taxonomic status of the 33 species follows the latest published systematic work on each corresponding group; however, no formal taxonomic changes are proposed here. The terminology on bioinvasion follows the definitions proposed by Occhipinti-Ambrogi and Galil (2004), Appendix C. Abbreviations by scale and impact include: EA, Established Alien; IA, Invasive Alien; NA, Noxious Alien; UA, Unestablished Alien. Abbreviations by mode of entry include: I, Introduced Alien; II, Intentional Introduction; SI, Secondary Introduction; SA, Spreading Alien; UI, Unintentional Introduction.

Distribution
Native to the Mediterranean Sea, this mussel now shows a worldwide distribution (Westfall and Gardner 2010). In Chile, it was recorded for the first time in 2000 (Daguin and Borsa 2000), and it has been recorded from Dichato (36°33ʹ S, 72°56ʹ W) to Punta Arenas (53°10ʹ S, 70°56ʹ W) (Tarifeño et al. 2012).

Remarks
Filter feeder, species of commercial importance (Poppe and Goto 2000). UA, II.

Distribution
Native to America, Amazon Basin (Brazil, Peru, Bolivia) (Cowie and Thiengo 2003). In Chile, this species was found for the first time in the country in 2000 (Letelier et al. 2007) and has been recorded only in Santiago (33°27ʹ S, 70°38ʹ W).

Remarks
Omnivorous, invasive, may predate native species (Cazzaniga 1990;Kwong et al. 2009). This species can also act as an intermediate host of the parasitic nematode Angiostrongylus cantonensis (Yang et al. 2013

Possible mechanism of introduction/Status
Aquarium trade/established (Letelier et al. 2007).

Possible mechanism of introduction/Status
Aquarium trade/established.

Remarks
Herbivore, detritivore, invasive (parthenogenetic species). This is a common aquarium snail and it has been cited as an intermediate host of the human liver fluke (Dundee and Paine 1977). EA, NA, I.

Possible mechanism of introduction/Status
Associated with ENSO events/unestablished (Castilla et al. 2005).

Remarks
This is a large herbivorous marine slug, feeding almost exclusively on the alga Ulva lactuca (Frings and Frings 1965). UA, SA.

Distribution
Native to Henderson Island (Preece 1995), widespread in the South Pacific Islands from Western Polynesia (Samoa, Tonga) throughout southeastern Polynesia to Easter Island (Kirch et al. 2009). In Chile this species has been recorded only in Easter Island (39°48ʹ S, 73°14ʹ W) (Stuardo and Vega 1985;Stuardo and Vargas-Almonacid 2000), and it was found for the first time in Chile by Odhner (1922).

Remarks
Although this species was described as native to Easter Island (Odhner 1922), it is probably native to Henderson Island, where some fossil shells are present in sedimentary deposits pre-dating human settlement (Preece 1995). EA, UI.

Distribution
Native range uncertain; this species is currently widespread in the tropics (Rowson et al. 2010). In Chile this species has been reported only from Easter Island (39°48ʹ S, 73°14ʹ W) (Boyko and Cordeiro 2001).

Possible mechanism of introduction/Status
Human transportation/probably established (Boyko and Cordeiro 2001).

Distribution
Europe, Mediterranean basin/Cosmopolitan (Cowie 2001), invasive in Far East and South America (Miquel et al. 1995). The first and only record for Chile does not give precise data (Rumi et al. 2010).

Possible mechanism of introduction/Status Human transportation/unestablished
Remarks Omnivorous and invasive species, minor plant pest, it may prey on other gastropods (Barker 2004). UA, I.

Possible mechanism of introduction/Status
Human transportation/established.

Distribution
Native to North America and introduced in Europe, New Zealand and South America (Faberi et al. 2006). In Chile this species has been recorded from Caldera (27°S), northern Chile (new records in this work, Table 1), to latitude 46°S, in the Región de Aysén del General Carlos Ibáñez del Campo (Letelier and Ramos 2002). The first record of this species in Chile was by Stuardo and Vega (1985).

Possible mechanism of introduction/Status
Human transportation/established (Landler and Nuñez 2012) Remarks This species has been cited as a pest of crops, feeding on seeds and seedlings (Faberi et al. 2006). EA, I.

Distribution
Native to Europe and currently found in most of North America and many temperate and subtropical countries (Boyko and Cordeiro 2001). In Chile this species has been found from Valparaíso to Tierra del Fuego (Valdovinos 1999) and in the Juan Fernández Archipelago and Easter Island (Boyko and Cordeiro 2001.). The first record of this species in Chile was by Stuardo and Vega (1985).

Distribution
Native to the Iberian Peninsula, Europe, now Cosmopolitan (Thomas et al. 2010). In Chile this species has been found from Valparaíso to Chiloé and in the Juan Fernández Archipelago and Easter Island (Stuardo and Vega 1985;Boyko and Cordeiro 2001). It was recorded for the first time in the country as Limax arborum Bouchard-Chantereaux, 1837 (Odhner 1922).

Possible mechanism of introduction/Status
Human transportation/probably established (Valdovinos 1999).

Distribution
Native to Europe; introduced to Australia, New Zealand, and North and South America (Thomas et al. 2010). In Chile this species has been cited from Valdivia (39°48ʹ S, 73°14ʹ W) to northern Chile (Landler and Nuñez 2012). The first record of this species for Chile was by Stuardo and Vega (1985).

Remarks
Highly invasive species, pest of stored agricultural products (Thomas et al. 2010 Description Thomas et al. (2010).

Distribution
Western Palaearctic, introduced into North and South America, South Africa, Pacific Islands, Australia and New Zealand (Gaitán-Espitia et al. 2012). In Chile this species has been cited from 30°to 46° (Valdovinos 1999;Letelier and Ramos 2002).

Remarks
Herbivorous terrestrial gastropod (Bohan et al. 2000). According to Hausdorf (2002), there are no obvious effects on native land snail fauna after the introduction of this species. EA, I.

Distribution
Native to Western Europe and Mediterranean region, now cosmopolitan (Cowie 2000). This is the NIS with the oldest occurrence records in Chile (Philippi 1885) and the introduced species with the largest distribution in the country, found in this work (Tables 1, 2) from Iquique (20°S) to Chiloé Island (43°S).

Possible mechanism of introduction/Status
Human transportation/established (Araya and Catalán 2014).

Distribution
Native to countries bordering the western Mediterranean Sea (Iberian Peninsula and northwest Africa) (Herbert and Sirgel 2001). The first and only record for Chile did not give precise data (Rumi et al. 2010).

Possible mechanism of introduction/Status
Human transportation/unestablished.

Distribution
Western Mediterranean: northwest Algeria, eastern Spain and the Balearic Islands (De Mattia and Mascia 2011). This is the first record for this species in the country: Buin, Santiago (33°43ʹ59ʹʹ S; 70°45ʹ00ʹʹ W) (Tables 1, 2).

Possible mechanism of introduction/Status
Human transportation/unestablished.

Remarks
Herbivore, invasive. This species is widely raised in heliciculture (De Mattia and Mascia 2011). UA, I.

Distribution
Native to Europe, Mediterranean basin. Introduced in North America, Australia, New Zealand, Japan, South America, and numerous Atlantic and Pacific Islands (Thomas et al. 2010). In Chile this species has been cited from latitude 30°S to 45°S and in the Juan Fernández Archipelago and Easter Island (Valdovinos 1999). The first record of this species for Chile was by Stuardo and Vega (1985).

Remarks
Herbivore, invasive and common in areas associated with humans; it is predominantly a subterranean species and a pest of root crops (Barker 1999). EA, I.

Remarks
Carnivore, facultative predator of other small snails (Meyer and Cowie 2010). This species is known as the "garlic snail" because of its ability to emit a strong smell of garlic when irritated . EA, I.

Distribution
Native to western and central Europe and the western Mediterranean, introduced to Scandinavia, North and South America, the Philippines, South Africa, St Helena, Australia and New Zealand (Barker 1999). In Chile this species has been recorded between 30°S and 45°S (Letelier and Ramos 2002), and in the Juan Fernandez Archipelago (Stuardo and Vega 1985). The first record of this species for Chile was by Stuardo and Vega (1985).

Possible mechanism of introduction/Status
Human transportation/established (Kirch et al. 2009).

Distribution
Widely distributed among tropical Pacific islands, probably native to Indonesia and the tropical western Pacific (Brook et al. 2010). In Chile, this species has been reported only from Easter Island (39°48ʹ S, 73°14ʹ W), Región de Valparaiso (Boyko and Cordeiro 2001).

Journal of Natural History 1749
Possible mechanism of introduction/Status Human transportation/unestablished (Boyko and Cordeiro 2001).

Distribution
Probably native to the Caribbean, Central America and Brazil (Brook et al. 2010). In Chile this species has been reported only from Easter Island (39°48ʹ S, 73°14ʹ W), Región de Valparaiso (Kirch et al. 2009).

Remarks
Cryptogenic freshwater gastropod species, it may represent a native species. EA, UI.

Distribution
Native to coastal waters of East Asia (Geiger and Owen 2012). In Chile this species is commercially harvested, with aquaculture farms in Caldera (27°S), northern Chile (Valdovinos 1999). It was first introduced to the country in 1982 (Flores-Aguilar et al. 2007).
Possible mechanism of introduction/Status Imported to Chile for aquaculture (Castilla et al. 2005;Flores-Aguilar et al. 2007).

Remarks
Herbivorous species, this species has an indirect impact on the communities of the native rocky kelp Lessonia nigrescens and Lessonia trabeculata, which are used as abalone food in Chilean aquaculture facilities (Castilla et al. 2005;Flores-Aguilar et al. 2007). This species is also a primary introduction vector for the non-indigenous boring polychaete species Polydora uncinata Sato-Okoshi, 1998 (Radashevsky and Olivares 2005). UA, II.

Distribution
East coast of the Pacific Ocean from Sunset Bay, Oregon, USA, to El Rosario, Baja California, Mexico (Mardones et al. 2013). In Chile this species is found around Caldera (27°S) and in the Región de Los Lagos (41°S to 46°S), only in aquaculture farms (Valdovinos 1999), with the first introduction to the country in 1977 (Flores-Aguilar et al. 2007).
Possible mechanism of introduction/Status Imported to Chile for aquaculture (Flores-Aguilar et al. 2007).

Remarks
Herbivorous species, this species has an indirect impact on the communities of the native rocky kelp Lessonia nigrescens and Lessonia trabeculata, which are used as abalone food in the local aquaculture facilities (Castilla et al. 2005;Flores-Aguilar et al. 2007). This species is also a primary and secondary introduction vector in Chile for the non-indigenous boring polychaete species Dipolydora huelma Sato-Okoshi and Takatsuka, 2001; Dodecaceria cf. opulens Gravier, 1908;Polydora rickettsi Woodwick, 1961and Terebrasabella heterouncinata Fitzhugh and Rouse, 1999(Moreno et al. 2006. UA, II.

Discussion
A total of 34 introduced species in 19 families are documented, including 20 terrestrial gastropods, eight marine species (gastropods and bivalves) and six freshwater gastropods (Table 2). Taxa in the families Haliotidae, Ostreidae and Pectinidae include species that are cultivated for export, with no records in natural environments in Chile (Castilla et al. 2005;Castilla and Neill 2009). Mytilus galloprovincialis, the only marine NIS in Bivalvia, is found in natural environments associated with banks of the native species Mytilus edulis in the Bay of Concepción, central Chile (Tarifeño et al. 2012). Other marine species include the gastropods Aplysia juliana, Monoplex keenae and Monoplex wiegmanni, all of which are associated with ENSO events (Castilla et al. 2005) and whose records may represent natural southern range extensions of their corresponding natural tropical distributions. All of the 20 recorded introduced terrestrial Gastropoda species are grounddwellers, and they are all associated (together with freshwater species) with humandisturbed habitats ( Table 2). Ten of these terrestrial species have been recorded in Easter Island alone (Boyko and Cordeiro 2001;Kirch et al. 2009) which, however, has a single species of native land mollusc: the subfossil snail species Hotumatua anakenana Kirch, Christensen and Steadman, 2009; now extinct (Kirch et al. 2009). The remaining invasive species are distributed in continental Chile, mostly in specific locations along the southern part of the country (Cádiz and Gallardo 2007;Rumi et al. 2010;Landler and Nuñez 2012). Among these, species of the genus Oxychilus have been cited as particularly dangerous to native micromolluscs, preying selectively on them (Cádiz et al. 2013). Freshwater species include six gastropods, five of them widely known as invasive molluscs (Olivares and Gálvez 2008;Jackson and Jackson 2009;Collado 2014) and a cryptogenic species of Physidae, Haitia venustula, recently transferred from genus Physa Draparnaud, 1801, and which may possibly constitute a native species (Miquel 1985;Taylor 2003). Dubious records include the species Otala lacteaa species easily misidentified with the congeneric Otala punctataand Rumina decollata, both species listed from Chile but without any geographic reference or further information (Rumi et al. 2010).
The first record of Otala punctata is made here from two locations near agricultural land in the commune of Buin, Region Metropolitana, in central Chile ( Table 1). The species is widespread worldwide and is a minor plant pest. Even when only a pair of specimens was collected, the potential proliferation of this species may approach that of Cornu aspersum in Chile. Cornu aspersum and Deroceras laeve were found in gardens, greenhouses, and monoculture plantations in the cities of Vallenar, Tierra Amarilla, Copiapó, Caldera, Antofagasta and Iquique, in northern Chile (Table 2). Cornu aspersum was previously recorded in Chile only from Caldera (27°S) to Chiloé Island (42°S), including Easter Island and the Juan Fernández Archipelago (Araya and Catalán 2014), whereas Deroceras laeve had been recorded from latitudes 30°S to 40°S (Valdovinos 1999). The northern distribution in Chile for C. aspersum and D. laeve is therefore extended here by about 1084 km. Fortunately, both of these species (C. aspersum and D. laeve) have never been recorded in natural environments and it seems that they are restricted to transformed habitats in general.
Regarding impacts by NIS, apart from the obvious invasive threats, the aquaculture of Haliotis species in particular has an indirect negative impact on communities of indigenous algae (Lessonia trabeculata, Macrocystis pyrifera and Gracilaria chilensis) which are collected and processed to feed these abalone species (Flores-Aguilar et al. 2007). These haliotid species also constitute introduction vectors for non-indigenous boring polychaete species (Radashevsky and Olivares 2005;Moreno et al. 2006). Regarding freshwater NIS, the introduction of the snails Pomacea canaliculata and Melanoides tuberculata poses a risk as both of these species have been documented as potential vectors for trematode parasites (Letelier et al. 2007) and P. canaliculata in particular has been listed as a predator of amphibian eggs (Karraker and Dudgeon 2014). The only positive impact of non-indigenous molluscan species relies on the primary production and commercialization of Crassostrea gigas, Haliotis discus and Haliotis rufescens (2138 tons in 2012) (Servicio Nacional de Pesca 2012).
As a result of this revision, a new record for a molluscan NIS -Otala punctataand new distribution records for the species Cornu aspersum and Deroceras laeve are given for the Chilean territory, resulting in a total at present of 34 invasive molluscan species recorded in the country. Most (61%) of the molluscan NIS constitute terrestrial taxa, and most (about 45%) of the new arrivals have a European origin. More than half (52%) of all these molluscan NIS were first recorded after the year 2000, doubling the 13 species recorded by Valdovinos (1999), indicating a large increase in the introduction (or recognition) of these species in Chile. Results indicate that the majority of the molluscan NIS in the country are associated with humandominated/disturbed habitats, with comparatively few species found in natural environments. Among these, the gastropods Pomacea, Melanoides and Oxychilus have the largest potential negative impact as invasive species and could greatly affect native biota. Taking into account that this is the first comprehensive study compiling all the records of freshwater, marine and terrestrial non-indigenous molluscs in Chileand that the results indicate a rapid increase in this group in the countryan in-depth study of the distribution, ecological characteristics and impacts of these alien species is of utmost importance. Particularly, it is necessary to study and test their direct effects on the native freshwater and terrestrial species, to eradicate alien species already established in the country, and to prevent further NIS from establishing in the Chilean territory.
New Zealand) for his comments and correction of an early version of the manuscript. I am indebted also to two anonymous reviewers and to the academic editor for their commentaries, corrections and suggestions, which greatly improved the quality of the manuscript. I thank also Daniel Geiger (Santa Barbara Museum of Natural History, Santa Barbara, CA, USA) who kindly checked the language and corrected a final version of the manuscript. This work is dedicated to Professor Cecilia Osorio (Universidad de Chile, Santiago, Chile) for her long contribution to the knowledge of Chilean molluscs and for her long friendship and personal support.