Invasive freshwater gastropods in South America: Physa acuta and its expansion to Austral Patagonia in Argentina

. Physa acuta is a freshwater snail of North American origin that has spread to all continents. In South America it was detected for the first time in 1966 (Brazil) and is currently present in Argentina, Brazil, Peru, Chile, Colombia, Ecuador and Uruguay, occupying 13 of the 52 South American freshwater eco-regions. Its introduction would be related to the import and transportation of aquatic plants. Here we update the distribution of P. acuta in Argentina based on a review of scientific collections, published works and new collections. Our review expands the distribution of the species from 11/23 Argentine provinces (until 2010) to 19/23, and we report the first record for the province of Santa Cruz, this being the southernmost site of the species. This new discovery in the province of Santa Cruz (Austral Patagonia), with an established and reproducing population in an urban area, poses a potential threat to local biodiversity (where there are no records of other non-native mollusks) and to human and animal health. This is due to the finding of populations in southern Argentina that are naturally infested by Fasciola hepatica. The record of P. acuta in aquatic environments of southern Patagonia makes it necessary to generate monitoring and control plans with the objective of identifying the dispersion vectors and preventing the spread of the species in other water bodies in the region.


INTRODUCTION
Biological invasions represent an important ecological and economic problem in the globalized world, leading to noteworthy consequences such as the decrease and/or loss of biodiversity, disruption of ecosystem natural cycles, and the spread of diseases (Alonso & Castro-Díez, 2012;Diagne et al., 2021;Carranza et al., 2023).Globalization has played a crucial role in increasing the dispersal of these species by facilitating the movement of goods, people, and living organisms across borders.This is particularly evident in aquatic ecosystems, where the incidence of invasive species has surged in recent decades due to their close association with human activities (Hulme et al., 2008;Hulme, 2009;Clusa et al., 2017).Mollusks are not exempt from these dis-persals, and in South America, 86 non-native species have been detected, including 16 freshwater species (11 gastropods and 5 bivalves) (Darrigran et al., 2020).Among these species Physa acuta Draparnaud, 1805 [= Physella acuta (Draparnaud, 1805); = Physa cubensis Pfeiffer, 1839; = Physella cubensis (Pfeiffer, 1839); = Physella venustula (A.Gould, 1847)], snail of the family Physidae, of North American origin, has profusely invaded all continents, except Antarctic (e.g., Vinarski, 2017;Ebbs et al., 2018).Physa acuta has been called "the sewage snail" because it can live in highly polluted water (Appleton, 2003).This species has also been considered of medical importance since it can potentially act as an intermediate host of human trematodes (Kanev, 1994;Dreyfuss et al., 2002).However, invasive populations have a lower number of trematodes than populations in their range of origin (Ebbs et al., 2018).In addition, impacts on native species have been reported in at least South Africa, New Zealand and Australia (Winterbourn, 1980;Brackenbury & Appleton, 1993;Zukowski & Walker, 2009).
Physa acuta exhibits a sinistral shell (like all species in the Physidae), thin and generally opaque, allowing it to be distinguished from native species, Stenophysa marmorata (Guilding, 1828), in South America (Núñez, 2011).According to Núñez (2011), shell characteristics alone are insufficient for species determination, and anatomical features are required, among which the following stand out: mantle not folded over the shell; triangular projections of the mantle in varying numbers; light pigmentation without a dark line at the level of the foot; absence of papilla in the female gonopore; presence of preputial gland; penis typically slender, with a decreasing diameter towards its free end.
In South America, Physa acuta is currently dispersed in 7 countries (Argentina, Brazil, Chile, Colombia, Ecuador, Peru and Uruguay), occupying 13 of the 52 ecoregions of South America (Darrigran et al., 2020).The first record of this species in South America was in Brazil in 1966 (Leme, 1966), being cited as Physella cubensis.Later it was cited in Chile (Te et al., 1978, as Physella venustula), Argentina (Miquel, 1985, both as P. cubensis and P. venustula) and Peru (Larrea et al., 1990, as P. venustula).The first records in Colombia, Ecuador and Uruguay are not precisely defined (Darrigran et al., 2020).
In Argentina, the first record refers to the Ciudad Autónoma de Buenos Aires and the province of Buenos Aires (as P. cubensis) and the province of Río Negro (as P. venustula) (Miquel, 1985), based on records of 1970 and 1981 respectively (Fig. 1B).Miquel & Parent (1996), cite it for the province of Santa Fe, and subsequently, Miquel & Zelaya (1999), expand its distribution to the provinces of Córdoba (with records from the 80's), Tucumán, Salta (as P. cubensis) and San Juan (as P. venustula, with records from the 80's).Núñez & Pelichotti (2003) first mention it for the provinces of Corrientes, Jujuy and San Luis, and Paraense (2005), without providing precise collection dates, cites it for Mendoza.The latest review of the Physidae family in Argentina, conducted by Núñez (2009), confirms the presence of P. acuta in 11 of the 23 Argentine provinces (plus the Ciudad Autónoma de Buenos Aires).
In this work, we update the distribution of this species in Argentina, since 2010, based on new collections, review of scientific collections and publications.

MATERIAL AND METHODS
As an initial foundation, we used the distribution data partially published in Rumi et al. (2008) and Núñez (2009), which included the latest revision of malacological collections in Argentina (Museo de La Plata: MLP, Museo Argentino de Ciencias Naturales: MACN, Fundación Miguel Lillo: FML) and works published until 2008.
The databases were updated through the revision of the mentioned collections, including the collection at the Instituto de Biodiversidad Neotropical -IBN, data published in scientific journals from 2009 onwards, and our records obtained through fieldwork in the provinces of Buenos Aires, Chubut, Entre Ríos, Mendoza, Neuquén, San Luis, and Santa Cruz, among which are the completion of two doctoral theses (de Lucía, 2022;Torres, 2022).Specimen identification followed the methodology outlined by Núñez (2011).To search for published works, we utilized several search engines: CONICET Digital, Biblioteca electrónica de Ciencia y Tecnología, Biodiversity Heritage Library, Naturalis, Google Scholar, SEDICI (Servicio de Difusión de la Creación Intelectual-UNLP), Sistema Nacional de Repositorios Digitales, and GBIF.The keywords used included Argentina, Physidae, Physa, Physella, acuta, cubensis, venustula, and combinations thereof.

RESULTS
The review of publications, scientific collections, and new collections shows the expansion time and space of Physa acuta in Argentina.Until 1990, it was found in four provinces (Buenos Aires, Córdoba, Río Negro, and San Juan) in addition to the Ciudad Autónoma de Buenos Aires (Fig. 1B).Until 2000 it had expanded northward, including the provinces of Salta, Tucumán, Jujuy and Santa Fe (Fig. 1C); while ten years later it added the provinces of Corrientes, Mendoza and San Luis (Fig. 1D).By 2020, the presence expanded in seven more provinces (Chaco, Catamarca, Chubut, La Rioja, Entre Ríos, Neuquén, and La Pampa) (Fig. 1E).Finally, in 2023, the province of Santa Cruz was added, to complete the current distribution of this species, present in 19 of the 23 provinces of Argentina, which allowed the creation of a database with 229 records of this species (see Table S1, Fig. 1F).It was observed that the provinces that presented the greatest number of records are Buenos Aires, Tucumán, Salta, and Córdoba, while four other provinces only have one record each (Chaco, La Pampa, La Rioja, and Santa Cruz) (Fig. 2).
Based on the publications by Rumi et al. (2008), Núñez (2009) and Núñez et al. (2010), the review of scientific collections yields new records for the provinces of Chaco (no collection date), Catamarca (since 2011), La Rioja (since 2012), La Pampa (since 2013) and Neuquén (since 2013).Regarding the bibliographic review, this provided new records in the province of Chubut (Esquel and surrounding areas, since 2012) (Assef et al., 2014).
From the new collections carried out in the central region of the country, the species has been recorded in the provinces of Buenos Aires, Chubut, Mendoza, Neuquén and San Luis, where it was already documented (Fig. 3).Additionally, it was recorded for the first time in the province of Entre Ríos (since 2010, MLP 13507, 13863).In the south of Argentina, specifically in the province of Santa Cruz, it was found in the city of Caleta Olivia (MLP-Ma 16102), in the March of 2023 (Fig. 3).

DISCUSSION
Physa acuta has proven to be a successful non-native species in South America, adapting to different climates (Darrigran et al., 2020).Our review results of collections, publications, and new records reaffirm this condition of invasive species since we communicate the expansion of the distribution of this species from 11 provinces in 2010 (Núñez, 2009) to 19 in almost a decade.Among these revisions, the expansion to three provinces from Argentine Patagonia stands out, Chubut (Assef et al., 2014), Neuquén, and Santa Cruz.The new record for the city of Caleta Olivia, Santa Cruz, is the southernmost for the species worldwide.The environment where this species was found consists of a small, shallow stream with a sandy bed that goes through farmlands and runs along roadsides, hosting eggs, juveniles, and adults.The closest previous records are from the town of Esquel (42°S) (Assef et al., 2014), Chubut province, in an area of lakes and mountain rivers surrounded by abundant vegetation.The presence of P. acuta in this area is generally related to environments with a high degree of anthropogenic impact, such as agriculture, urbanization and sewage effluents (Horak et al., 2023) (Fig. 4).In Chile, the nearest record is at latitude 41°S (Llanquihue Lake) (Collado et al., 2020), about 5 degrees north of the one found in Caleta Olivia (46°S), the closest site to Esquel.
The review carried out by Torres (2022) shows that in the province of Santa Cruz, 13 species of freshwater mollusks are recorded, 10 belonging to gastropods and three to bivalves.All of these species are native, and here we have recorded the presence of the first invasive species of freshwater mollusks in the province.The introduction of this new entity to the province cannot be precisely determined, but it is generally attributed to the dispersion of this species through the trade of aquatic plants used in aquariums.The aquarium trade has been shown to be a source not only of introduction of non-native aquatic macrophyte species (June-Wells et al., 2012), but also of fauna associated with them.These species are distributed throughout the world through a generally unregulated industry (Padilla & Williams, 2004).In Argentina, Physa acuta is in Category 1: Restricted and mandatory control species (EEI-1), according to MAyDS (2021).However, it continues to be sold in physical and virtual commercial aquariums.This dispersion route in general does not have exhaustive control.
Physa acuta is a species characterized by being present in disturbed environments (Miyahira et al., 2023;Tchakonte et al., 2023).Even recent studies (Cieplok & Spira, 2020;Collado et al., 2023) demonstrate that, in this type of environment, the density of P. acuta is dominant, displacing native species.In the Argentine Patagonia, it has been recorded in the Esquel area (Chubut), where it has been observed in urban streams with high levels of nutrients, including phosphorus and nitrogen com-  pounds (Assef et al., 2014).Horak et al. (2023) evaluated the activity of the multi-xenobiotic defense mechanism in P. acuta specimens in highly impacted environments in Patagonia (Chubut).The authors determined that P. acuta specimens from environments impacted by agriculture and urbanization showed more detoxifying activity than organisms from reference sites with low impact of anthropic origin, indicating a higher degree of tolerance than native species.Laboratory studies carried out in Argentina by Núñez (2010) revealed that the growth of this species was not affected by reproduction, exhibiting a more extended reproductive period and deposit-ing a greater quantity of eggs compared to Stenophysa marmorata (Guilding, 1828), a native species of the same family.In the southern part of the Buenos Aires province, in natural environments, it was determined that P. acuta (identified as P. venustula) has a semelparous and subannual life cycle, with two or three loosely defined cohorts per year, featuring almost continuous oviposition and recruitment (Martín, 2001).Both in the laboratory (Núñez, 2010) and in natural environments (Martín, 2001), they conclude that this species has a high juvenile mortality of up to 3.5 mm in length and decreases in subadults and adults.The presence of a new potential intermediate host of Fasciola hepatica could complicate the situation of fascioliasis in the province of Santa Cruz, which directly impacts livestock in the center and north of the province (Aguilar & Olaechea, 2014).Recently, Larroza et al. (2023) have detected, in the northwest of Santa Cruz, resistance of F. hepatica to Triclabendazole (TCBZ), one of the few anthelmintics available to treat fasciolosis for ruminants.This could significantly increase livestock mortality in establishments that do not have adequate sanitary controls, or indirectly through metabolic disorders that affect milk production and quality or with effects on the reproductive capacity of cattle and sheep.
The expansion of the distribution range of Physa acuta in water bodies in southern Patagonia represents not only a risk to biodiversity but also a health concern.The presence of this invasive species in Santa Cruz constitutes the first record of an invasive exotic mollusk for the province, making it necessary to develop monitoring and control plans.The objective is to identify vectors of dispersion and prevent the species from spreading to other water bodies in the region.These understandings serve as tools for the prevention of the introduction and establishment of invasive species, according to NISC (2001) andELI (2002).They include risk assessment, early detection, rapid response, and public education.Public education, along with the dissemination of high-quality scientific information, is fundamentally important for making the management of biological invasions sustainable.Society must be aware of specific cases, their environmental impacts, and social effects to encourage governments to implement the necessary mechanisms for the prevention of bioinvasions (Darrigran et al., 2012).

SUPPLEMENTARY MATERIAL
Table S1.Localities where Physa acuta was recorded in Argentina, with information on the year of collection and reference to scientific collection or publication.In red, lots deposited as a result of our sampling efforts.

Figure 2 .
Figure 2. Number of records of Physa acuta per province.
Merlo et al. (2022)) in the Esquel area (Chubut),Sanero et al. (2018)conducted a parasitological study using different species of native and non-native gastropods, recording specimens identified as Physa spp.(found in the same sites as Physa acuta byAssef et al. (2014)infested with cercariae from the family Notocotylidae and Fasciola hepatica (Fasciolidae).According toMerlo et al. (2022), P. acuta records cercariae from the families Echinostomatidae and Plagiorchioidae in Salta, and Gorgoderoidea and Schistosomatidae in Buenos Aires.If the specimens in Chubut belong to P. acuta (as there are no other Physidae registered in the area), these are the first records of infection in the Argentine Patagonia in anthropized environments, representing a new vector for fascioliasis that could potentially spread throughout southern Patagonia.