Potamopyrgus Antipodarum (Gray, 1843) (Gastropoda, Tateidae) in Chile, and a Summary of Its Distribution in the Country
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16 3 NOTES ON GEOGRAPHIC DISTRIBUTION Check List 16 (3): 621–626 https://doi.org/10.15560/16.3.621 Range extension of the invasive Potamopyrgus antipodarum (Gray, 1843) (Gastropoda, Tateidae) in Chile, and a summary of its distribution in the country Gonzalo A. Collado1, 2, Carmen G. Fuentealba1 1 Departamento de Ciencias Básicas, Facultad de Ciencias, Universidad del Bío-Bío, Avenida Andrés Bello 720, Chillán, 3800708, Chile. 2 Grupo de Biodiversidad y Cambio Global, Universidad del Bío-Bío, Avenida Andrés Bello 720, Chillán, 3800708, Chile. Corresponding author: Gonzalo A. Collado, [email protected] Abstract The New Zealand mudsnail Potamopyrgus antipodarum (Gray, 1843) has been considered as one of the most invasive mollusks worldwide and recently was listed among the 50 most damaging species in Europe. In the present paper, we report for the first time the presence ofP. antipodarum in the Maule river basin, Chile. The identity of the species was based on anatomical microdissections, scanning electron microscopy comparisons, and DNA barcode analysis. This finding constitutes the southernmost record of the species until now in this country and SouthAmerica. Keywords Alien species, DNA barcode, cryptic species, invasive mollusks, Maule River, range distribution. Academic editor: Rodrigo Brincalepe Salvador | Received 05 February 2020 | Accepted 23 March 2020 | Published 22 May 2020 Citation: Collado GA, Fuentealba CG (2020) Range extension of the invasive Potamopyrgus antipodarum (Gray, 1843) (Gastropoda, Tateidae) in Chile, and a summary of its distribution in the country. Check List 16 (3): 621–626. https://doi.org/10.15560/16.3.621 Introduction the 50 most damaging species in Europe (Nentwig et al. 2017). The native range of this species is New Zealand Biological invasions may cause a series of effects on and adjacent islands (Winterbourn 1970, 1972; Ponder invaded ecosystems such as economic damage, altera- 1988). Now, the NZMS has invaded brackish and fresh- tions of habitats and biotopes, threats to biodiversity, and water ecosystems in several countries in Asia, Austra- harm to human health. Although habitat loss is the main lia, Europe, and North and South America (e.g. Ponder cause of species extinctions in the modern age (Tollef- 1988; Bowler 1991; Shimada and Urabe 2003; Levri et al. son 2019), biological invasions nowadays represent one 2007; Radea et al. 2008; Butkus et al. 2012; Hamada et of the main causes of biodiversity loss (e.g. Gordon 1998; al. 2013; Collado 2014). Wilcove et al. 1998; Bax et al. 2003; Lodge and Shrader- The first records of the NZMS in North America were Frechette 2003; Juliano and Lounibos 2005). made in the Snake River, Idaho, in late 1980s and early The New Zealand mudsnail (NZMS), Potamopyrgus 1990s (Bowler 1991; Bowler and Frest 1992). In South antipodarum (Gray, 1843), is one of the most success- America, Collado (2014) first discovered NZMS in two ful and widespread invasive freshwater mollusks in the places in Choapa river basin and two others in Maipo world (Son 2008; Alonso and Castro-Díez 2008; But- river basin in the central-north part of Chile. However, kus et al. 2012), and in fact, it was recently listed among NZMS was present earlier in Chile but it was overlooked © The authors. This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. 622 Check List 16 (3) by Collado et al. (2011) and Collado and Méndez (2011), Taxonomic account who ascribed part of their samples to the genus Heleobia Superfamily Truncatelloidea Gray, 1840 Stimpson, 1865. Subsequently, NZMS has been reported Family Tateidae Thiele, 1925 from additional localities in Chile, with the southern- Genus Potamopyrgus Stimpson, 1865 most record from Lo Carreño irrigation canal in the Rapel river basin (Collado 2016; Collado et al. 2019a, Potamopyrgus antipodarum (Gray, 1843) 2019b). Materials examined. Chile • 1♀, 4.7 mm; Maule Re- The NZMS can spread to new habitats through pas- gion, Maule river basin, Maule River; 35°33′12.69″S, sive and active dispersal mechanisms and, although it 071°41′57.04″W; 96 m a.s.l., 3 Mar. 2019; G.A. Collado is highly tolerant to a variety of physicochemical water leg.; GenBank: MG779236; PaMR1-LMSM-UBB; MC- conditions (Dorgelo 1987; Poirier 2013), it prefers fresh- NPPRF-CC 157-2 (radula), MCNPPRF-CC 157-4 (pro- water environments rather than brackish water. In lab- toconch) • 2♀, 2.8 mm; same collection data as for oratory experiments, the NZMS exhibited avoidance preceding; GenBank: MG779236; PaMR2-LMSM- behaviors to predatory fishes, a trait that can help the UBB; MCNPPRF-CC 157-3 (operculum) • 3♀, 2.6 mm; spread of the species (Levri et al. 2017). The objective of this paper is to report a new record same collection data as for preceding; PaMR3-LMSM- of the invasive NZMS in Maule River, central Chile, the UBB; MCNPPRF-CC 157-1 (shell). southernmost record known, until now, in this country Identification. NZMS are similar in shell morphology and in South America. to species of the genus Heleobia and Potamolithus (Col- lado et al. 2019a, 2019b), which include several native species in Chile. Species-specific identification was per- Methods formed after observation of the protoconch and radula, In March 2019, five localities were prospected to col- which differ among genera (Collado et al. 2019a). lect freshwater snails in central Chile: Claro River (35° Morphology. The shell of the NZMS is ovate-conic 25′12.03″S, 071°40′57.36″W) and Maule River (35°33′ (Fig. 1A–D), not umbilicated, with 5–6 whorls, aper- 12.69″S, 071°41′56.45″W) in Maule river basin, Maule ture ovate. Protoconch having ca 1.2 whorls (Fig. 1E, F). Region, and Cato River (36°33′26.68″S, 072°02′39.87″W), Operculum corneous, bright brown-orange, solid, with the irrigation canal La Luz (36°35′31.64″S, 072°04′ white smear (Fig. 1G–J). Radula taenioglossan (general 13.31″W), and Las Toscas stream (36°35′34.89″S, 072° formula: 3-1-3), composed by seven teeth on each row: 03′38.62″W) in Itata river basin, Ñuble Region. The two marginal teeth (external and internal) and a lateral snails were sampled using a hand sieve and stored in tooth located on each side of the central tooth (Fig. 1K, absolute ethanol. The shell and operculum were photo- L). Central tooth with five lateral cusps on each side of graphed and measured using a Motic SMZ-168 Stereo- a larger median cusp and three decreasing pairs of basal microscope equipped with a Moticam 2000 camera. cusps (Fig. 1L). Distal section of the external marginal For taxonomic identification, morphological and micro- teeth free (flange well developed). structural features were studied following Collado et al. Two identical partial COI sequences of (2019a), including protoconch, operculum and radula, DNA barcoding. which were observed using scanning electron micros- 639 bp from PaMR1-LMSM-UBB and PaMR2-LMSM- copy (SEM) (Hitachi SU3500). The reproductive strat- UBB were obtained. The BLASTn analysis compar- egy of snails was studied by microdissections. A DNA ing this haplotype against GenBank database found barcode analysis (Hebert et al. 2003) was performed 100% identity with sequences of P. antipodarum pre- in the BLASTn section of the GenBank database after viously published (Ponder et al. 2008; Neiman et al. sequencing the cytochrome c oxidase 1 (COI) gene 2010; Hamada et al. 2013; Collado et al. 2014, 2019a, based on the molecular methods performed by Collado 2019b), confirming the taxonomic assignment based on (2014). Voucher specimens of the NZMS were deposited morphology. at the collection housed in Laboratorio de Malacología y Distribution. Although the distribution of the NZMS Sistemática Molecular, Universidad del Bío-Bío, Chillán, in Chile is not continuous regarding its absence in some Chile (LMSM–UBB) and at Museo de Ciencias Natura- contiguous basins, the species is present in five political les Profesor Pedro Ramírez Fuentes (MCNPPRF), Chil- regions of the country, specifically from the Coquimbo lán, Chile (Acta de Ingreso 157). to Maule regions. With the new record provided here, the occurrence of the NZMS in Chile reaches 19 localities Results (Collado 2014, 2016; Collado et al. 2019a, 2019b; present study) (Fig. 2, Table 1). Sampling was positive for the NZMS Potamopyrgus antipodarum only in Maule River. The species was found in syntopy with specimens of the gastropod genera Pota Discussion molithus Pilsbry, 1896 (Tateidae), Chilina Gray, 1828 Our integrative study using freshwater snails collected (Chilinidae), and Physa Draparnaud, 1801 (Physidae). in Maule River, central Chile, revealed the occurrence of Collado and Fuentealba | Spread of Potamopyrgus antipodarum in Chile 623 Figure 1. Potamopyrgus antipodarum (Gray, 1843), Maule River, central Chile. A. Shell of specimen PaMR1-LMSM-UBB observed with SEM. B–D. Shells of specimens PaMR1-LMSM-UBB, PaMR2-LMSM-UBB and PaMR3-LMSM-UBB, respectively, observed with stereomicroscope. E, F. Protoconchs of two individuals. G, H. Operculum observed with stereomicroscope (internal and external view, respectively). I, J. Operculum observed with SEM (internal and external view, respectively). K. Anterior section of the radula. L. Three central teeth of the radula. Abbreviations: c = central tooth; e = external marginal tooth; i = internal marginal tooth; l: lateral tooth. Scale bars: A–D = 1 mm; E, F= 300 µm; G–J = 500 µm; K = 50 µm; L = 20 µm. 624 Check List 16 (3) Figure 2. Geographic records of the invasive freshwater snail Potamopyrgus antipodarum (Gray, 1843) in Chile. Square: new record of the species; circle: previous records obtained from the literature (Collado 2014, 2016; Collado et al. 2019a, 2019b); triangles: localities where P.