Open Access

Out of New Zealand: molecular identification of the highly invasive freshwater mollusk Potamopyrgus antipodarum (Gray, 1843) in South America

Zoological Studies201453:70

DOI: 10.1186/s40555-014-0070-y

Received: 20 June 2014

Accepted: 10 September 2014

Published: 18 September 2014

Abstract

Background

The New Zealand mud snail Potamopyrgus antipodarum (Gray, 1843) is among the most widespread non-indigenous mollusk in the world. Based on a comprehensive phylogenetic analysis, the invasion of this species to central Chile, which is also the first record of this species from South America, is reported.

Results

Molecular analysis identified four populations of P. antipodarum in central Chile, Parque O'Higgins and Estero La Dehesa in Santiago city, and Estero Consuelo and the Chalinga River in Salamanca, a town located in a different basin. No sequence divergence was found among populations in the cytochrome c oxidase subunit I (COI) gene. Morphological and reproductive evidence is in agreement with these findings.

Conclusions

This is the first record of P. antipodarum in the Neotropical region. All populations contained only females with embryos or juvenile snails in their brood pouches suggesting that they are viable and well established. It is important to prevent the spread of P. antipodarum to other localities in Chile and other South American countries.

Keywords

Biological invasions Caenogastropoda Chile COI gene Tateidae

1 Background

The widespread introduction of non-native species has been considered as one of the major threats to biodiversity (Lodge and Shrader-Frechette [2003]). The mud snail Potamopyrgus antipodarum is a caenogastropod originated from New Zealand and adjacent islands (Winterbourn [1970], [1972]). This snail has become among the most widespread non-indigenous aquatic invertebrates in the world (Butkus et al. [2012]). Several transport methods have been reported as responsible for propagation of this global exotic species, which include both active and passive dispersal (Alonso and Castro-Diez [2008]). This species has invaded brackish and freshwater habitats in several countries in Europe, Australia, Asia, and North America (e.g. Ponder [1988]; Bowler [1991]; Shimada and Urabe [2003]; Radea et al. [2008]; Butkus et al. [2012]; Hamada et al. [2013]).

Potamopyrgus antipodarum is a minute snail highly variable in size, shape and ornamentation. Adults range from 3 to 6 mm in length in USA, but they reach 11 mm in their native habitat (Richards [2002]). Winterbourn ([1970]) reported considerable variation in the shell ornamentation of the species in its native range, even within a single population. Shell polymorphism in P. antipodarum would be influenced by environmental and genetics bases (Winterbourn [1970]; Haase [2003]). Recently, Butkus et al. ([2012]) reported regular (smooth) and carinate morphotypes from Lake Vilkokšnis, suggesting two independent invasion events. However, this should be taken with caution since the presence of a keel-like ridge can be a phenotypically plastic trait.

Potamopyrgus antipodarum is a generalist species, feeding on aquatic plants, green algae and detritus (Haynes and Taylor [1984]), being able to tolerate a broad range of physicochemical aquatic conditions (Dorgelo [1987]; Proctor et al. [2007]; Poirier [2013]). In the rivers of Wyoming, USA, the species dominates secondary production, even reaching one of the highest values of productivity ever reported for a stream invertebrate (Hall et al. [2006]). Zaranko et al. ([1997]) reported its densities in Lake Ontario being as high as 5,600 snails per square meter, which is a value close to that found in native populations (4,000/m2, see Collier et al. [1998]). However, in other invaded habitats, P. antipodarum can achieve densities as high as 500,000 snails per square meter (Hall et al. [2003]; Richards [2002]; Richards et al. [2001]), and even more (800,000/m2, see Dorgelo [1987]).

Because frequently there are no obvious morphological characters to distinguish different components of invertebrate fauna, DNA barcoding and molecular phylogenetic analysis are increasingly used to identify aquatic invaders in a variety of taxa (e.g. Geller et al. [1997]; Facon et al. [2003]; Albrecht et al. [2009]; Duggan et al. [2012]; Porco et al. [2013]; Wetterer [2014]). In 2010, an investigation of the small freshwater gastropod of the superfamily Rissooidea Gray, 1847 sensu lato of Chile was initiated by the author, sampling snails from a number of locations. In a previous morphological work, Collado et al. ([2011a]) assigned snails from the Chalinga River and Estero Consuelo to the genus Heleobia Stimpson, 1865 following Biese ([1944], [1947]). Here, I perform a comprehensive phylogenetic analysis to evidence that these snails actually represent the non-native species P. antipodarum. I also report the occurrence of this species in other two watersheds from central Chile, Estero La Dehesa east of Santiago, and a spring located within the Parque O'Higgins, also in this city. Additionally, I evaluate the reproductive performance of populations studied.

2 Methods

In this study, four localities in two regions from central Chile, Región de Coquimbo and Región Metropolitana, were sampled from prospective sites for snail collection (Figure 1). In Región de Coquimbo, two watersheds were sampled, both in the town of Salamanca, the Chalinga River (31° 46′ 15.61″ S; 70° 59′ 05.09″ W), which is a small, intermittent watercourse north of the town, and Estero Consuelo (31° 46′ 48.61″ S; 70° 57′ 37.33″ W), a stream east of the town. In Región Metropolitana, two watersheds were sampled in Santiago city; Estero La Dehesa (33° 22′ 02.00″ S; 70° 31′ 15.00″ W), a stream located in the eastern suburbs of the city, and Parque O'Higgins (33° 28′ 06.22″ S; 70°39′ 38.31″ W), an urban park that offers recreation, fishing, and open green space to residents and whose southern section includes a spring that flows about 300 m into an small artificial lagoon. In this spring, P. antipodarum co-occur with a snail species of the genus Physa Draparnaud, 1801, platyhelminthes, and other invertebrates. The snails were obtained from macrophytes of the spring using a sieve and preserved in absolute ethanol prior to molecular and morphological analyses. The snails were photographed at the same magnification with a Motic SMZ-168 Stereo Microscope (Motic, Richmond, BC, Canada) with a Moticam 2000 (Motic, Xiamen, China) integrated digital camera. The shell of adult snails was broken and the mantle tissue was removed to determine the sex by the presence/absence of a penis. In the case of the females, the oviduct wall was dissected to determine the presence of embryos or juveniles. The measurements of animals were performed under a stereo microscope. The author is authorized to the removal of animals from watersheds in Chile (Resolution N° 3285, Subsecretaria de Pesca y Acuicultura, Ministerio de Economía, Fomento y Turismo, República de Chile). Voucher specimens of P. antipodarum were deposited in the Colección Malacológica del Servicio Agrícola y Ganadero de Chile (CMSAG 3651 and 3652).
Figure 1

Sampling sites of Potamopyrgus antipodarum in central Chile (black dots).

A small piece of tissue from the mantle and gill was cut off from the snails to extract genomic DNA using the cetyl trimethylammonium bromide (CTAB) method (Winnepennickx et al. [1993]). A fragment of the mitochondrial gene, cytochrome c oxidase subunit I (COI) was amplified by polymerase chain reaction (PCR) using the primers LCO1490 (5′-GGTCAACAAATCATAAAGATATTGG-3′) and HCO2198 (5′-TAAACTTCAGGGTGACCAAAAAATCA-3′) (Folmer et al. [1994]); PCR conditions were the same as those in [Collado et al. (2011b)]. Amplified products were sequenced by Macrogen Inc., South Korea. The sequences were edited and aligned with BioEdit (Hall [2001]) using default parameters. Phylogenetic analyses were performed using maximum parsimony (MP) and Bayesian inference (BI) methods. The MP analysis was carried out with the program PAUP* 4.0 (Swofford [2003]) using a heuristic search with the tree bisection and reconnection branch swapping algorithm and the addition of random sequences. Character states were treated as unordered, assuming equal weight. The statistical confidence of the nodes was evaluated using 100 bootstrap pseudoreplicates (Felsenstein [1985]). The BI was performed with MrBayes v. 3.1.2 (Ronquist and Huelsenbeck [2003]) after selecting the best evolutionary model in jModelTest (Posada [2008]). The analysis was run three times for 3 million generations, sampling trees every 1,000 generations and using a burn-in period of 10%.

As Chilean rissooidean snails have been assigned to different families (Collado et al. [2011a]), original sequences were aligned with sequences of snails obtained from GenBank covering a wide range of taxa within this superfamily (see Wilke et al. [2013]) (Table 1). After ascertaining the family of the Chilean snails, original sequences were aligned with sequences of different genera within the particular family to determine the genus and species to which the snails belong, in this case P. antipodarum. Original sequences were deposited in GenBank (Table 2).
Table 1

Classification and GenBank accession numbers for the rissooidean taxa studied

Family

Species

GenBank accession

Source

Barleeiidae

Barleeia oldroydi (Bartsch 1920)

JX970602

Wilke et al. ([2013])

Amnicolidae

Amnicola limosa (Say, 1817)

AF213348

Wilke et al. ([2000a])

Assimineidae

Assiminea grayana Fleming, 1828

HQ623170

Wilke et al. ([2013])

Beddomeia group

Beddomeia paludinella (Reeve, 1857)

JX970603

 

Bithyniidae

Bithynia tentaculata (Linnaeus, 1758)

JX970605

 

Bythinellidae

Bythinella austriaca (Frauenfeld, 1856)

AF213349

Wilke et al. ([2000a])

Iravadiidae

Clenchiella sp.

JX970606

Wilke et al. ([2013])

Cochliopidae

Heleobops carrikeri Davis and McKee, 1989

AF213347

Wilke et al. ([2000a])

Falsicingulidae

Falsicingula athera Bartsch, 1936

HQ623172

Wilke et al. ([2013])

Hydrobiidae

Hydrobia acuta (Draparnaud, 1805)

AF278808

Wilke et al. ([2000b])

Lithoglyphidae

Lithoglyphus naticoides (Pfeiffer, 1828)

AF367642

Wilke et al. ([2001])

Moitessieriidae

Moitessieria cf. puteana Coutagne, 1883

AF367635

 

Pomatiopsidae s.s.

Pomatiopsis lapidaria (Say, 1817)

AF367636

 

Rissooidae

Setia turriculata Monterosato, 1884

AF253084

Davis et al. ([1998])

Stenothyridae

Stenothyra cf. glabra A. Adams, 1861

HQ623177

Wilke et al. ([2013])

Tateidae

Tatea huonensis (Tenison-Woods, 1876)

JX970619

Wilke et al. ([2013])

Hydrobiidae

Ascorhis tasmanica Martens, 1858

AF129329

Hershler et al. ([1999])

Truncatellidae

Geomelania inornata Chitty, 1853

AF367629

Wilke et al. ([2001])

Table 2

GenBank accession numbers for the taxa studied of the family Tateidae

Species

GenBank accession number

Source

Fluviopupa sp.

JX970615

Wilke et al. ([2013])

Halopyrgus pupoides (Hutton, 1882)

JX970616

 

Hemistomia winstonefi (Haase and Bouchet, 1998)

JX970617

 

Obtusopyrgus alpines Haase, 2008

AY631088

 

Opacuincola delira Haase, 2008

AY631090

 

Potamolithus ribeirensis Pilsbry, [1911]

JX970618

Wilke et al. ([2013])

Potamopyrgus antipodarum (Gray, 1843)

EU573983

Ponder et al. ([2008])

 

AB703675

Hamada et al. ([2013])

 

AB703676

 
 

AB703677

 
 

AY631101

Haase ([2005])

 

AY631102

 

Potamopyrgus estuarinus (Winterbourn, 1971)

AY631103

 
 

AY631104

 

Potamopyrgus kaitunuparaoa Haase, 2008

AY631105

 
 

AY631106

 

Potamopyrgus oppidanus Haase, 2008

AY631112

 

Sororipyrgus kutukutu Haase, 2008

AY631108

 

Catapyrgus matapango Haase, 2008

AY631072

 

Hadopyrgus ngataana Haase, 2008

AY631073

 

Leptopyrgus melbourni Haase, 2008

AY631075

 

Rakiurapyrgus cresswelli (Climo, 1974)

AY631081

 

Meridiopyrgus muaupoko Haase, 2008

AY631083

 

Paxillostium nanum Gardner, 1970

AY631111

 

Halopyrgus pagodulus Haase, 2008

AY631113

 

Tongapyrgus kohitatea Haase, 2008

AY631124

 

Tatea huonensis (Tenison-Woods, 1876)

JX970619

Wilke et al. ([2013])

Tatea rufilabris (A. Adams, 1862)

EU151940

Colgan and da Costaa

Edgbastonia alanwillsi Ponder et al. [2008]

EU580440

Ponder et al. ([2008])

Spring from Parque O'Higgins

KJ616603

Present study

 

KJ616604

Present study

 

KJ616605

Present study

 

KJ616606

Present study

Chalinga River

KJ616607

Present study

 

KJ616608

Present study

 

KJ616609

Present study

 

KJ616610

Present study

Estero Consuelo

KJ616611

Present study

 

KJ616612

Present study

 

KJ616613

Present study

 

KJ616614

Present study

Estero La Dehesa

KJ616615

Present study

 

KJ616616

Present study

 

KJ616617

Present study

 

KJ616618

Present study

aUnpublished data.

3 Results

The snails collected in central Chile have ovate to conical shell shape, smooth, with a deep suture, and with up to six whorls (Figure 2). The aperture is oval, sometimes thickened, and with a thin brown operculum. The external shell morphology of these snails is consistent with the drawings and photographs of P. antipodarum shown in other studies (Winterbourn [1970], [1972]; Gangloff [1998]; Butkus et al. [2012]; Poirier [2013]). All the snails examined in the present study were females. The largest snail belonged to the population from Estero La Dehesa (Table 3). The presence of embryos or juveniles in the breeding pouches was detected in every studied population (Figure 3). In a previous study, Collado and Méndez ([2011]) demonstrated that the species treated as Heleobia choapaensis (Biese, [1944]) from Estero Consuelo was ovoviviparous.
Figure 2

Living representative adult snails of Potamopyrgus antipodarum in central Chile. Shell length and shell width are given in millimeters. (A) Parque O'Higgins (3.8 × 2.1) (B) Estero La Dehesa (4.0 × 2.1). (C) Estero Consuelo (2.9 × 1.5). (D) Chalinga River (2.9 × 1.6).

Table 3

Number of snails collected, and size of specimens used in the present study; all specimens collected were females

Locality

Specimens observed

Shell size of the smallest specimen (length-wide)

Shell size of the largest specimen (length-wide)

Parque O'Higgins

20

3.5 × 1.7 mm

4.4 × 2.2 mm

Estero La Dehesa

15

2.8 × 1.5 mm

5.1 × 2.6 mm

Chalinga River

39

2.7 × 1.4 mm

4.2 × 1.9 mm

Estero Consuelo

24

2.5 × 1.3 mm

4.4 × 1.9 mm

Figure 3

Adult ovoviviparous female (<5 mm) of Potamopyrgus antipodarum from Estero La Dehesa, Santiago, Chile. The pallial oviduct brood pouch was dissected to show several shelled juveniles.

A COI fragment of 639 bp was amplified in the snail sampled in the present study. No sequence variation was found within the four populations. The MP and BI analyses indicated that these snails fell in a clade integrated by snails that belong to the family Tateidae Thiele, 1925 (Figure 4). In both analyses, the Tateidae node was highly supported. A subsequent phylogenetic analysis included 20 species of this family (Table 2) using Ascorhis tasmanica as an outgroup (see also Wilke et al. [2013] for the sister group of the Tateidae). In this analysis, the matrix was composed of 638 nucleotide sites. The relationships among these species were well resolved by the MP and BI analyses (selected model: TPM2uf + I + G). Both analyses located the snails studied here within the genus Potamopyrgus (MP: 96% bootstrap support), specifically within the clade composed by the sequences of the species P. antipodarum (MP: 100% bootstrap support). The same systematic position was inferred in the BI analysis (1.00 posterior probability) (Figure 5).
Figure 4

Bayesian consensus tree of rissooidean snails based on COI gene sequences. The phylogenetic position of the Chilean snails is shown in the gray box. The taxa represent the families (or family-level assignments) within the rissooidean (see Wilke et al. [2013]). Numbers above the nodes indicate posterior probability values obtained in the BI (only values equal to or above 0.95 are shown). The outgroup in this analysis was chosen following Wilke et al. ([2013]).

Figure 5

Bayesian consensus tree showing the systematic position of the Chilean COI sequences among lineages of the family Tateidae. The Chilean snails integrated the Potamopuygus antipodarum clade. Numbers above the nodes indicate posterior probability values obtained in the BI (only values equal to or above 0.95 are shown) followed by the bootstrap values obtained under the MP analysis (only values equal to or above 50% are shown). The outgroup in this analysis was chosen following Wilke et al. ([2013]) and results obtained in the present study.

The haplotype of the invader tateid snails from Chile was identical with the haplotype of the European invader from West India Dock, London (GenBank: EU573983) (Ponder et al. [2008]), Chitose River in Japan (GenBank: AB703675) (Hamada et al. [2013]), and those obtained in Lake Superior, USA (GenBank: GQ996433) and Lake Alexandrina, New Zealand (GenBank: GQ996432) (Neiman et al. [2010], personal communication).

4 Discussion

The morphological survey, reproductive features, and the COI gene markers data showed that the populations surveyed in central Chile belong to the highly invasive clonal snail P. antipodarum. Although several native hydrobioid species have been named or assigned to the genus Potamopyrgus Stimpson, 1865 on the South American continent (Pilsbry [1911], [1944], [1952]; Doello Jurado [1916]; Haas [1938], [1949], [1952]; Lima and Pereira de Souza [1990]), at present all of them are allocated in different genera (Gaillard [1973]; Gaillard and de Castellanos [1976]; Hershler and Thompson [1992]; Wesselingh [2000]; Pons da Silva [2003]). Thus until now, there was no evidence of the presence of the genus Potamopyrgus neither in Chile nor any other South American country.

In the present study, only a single haplotype was identified in the four Chilean localities, although this may be not conclusive because only four snails were sequenced in each location. In North America, Dybdahl and Drown ([2011]) found four genotypes of P. antipodarum from the whole USA. Different haplotypes of this species were also identified in Japan as a consequence of more than one colonization event (Hamada et al. [2013]). At present, it is impossible to know the origin and exact time of the arrival of P. antipodarum to Chile considering that the same haplotype is found in Japan, England, New Zealand, and USA (Ponder et al. [2008]; Neiman et al. [2010]; Hamada et al. [2013], present study). A microsatellite analysis could reveal more informative results due to the higher mutation rates than COI gene.

It has been suggested that at high densities P. antipodarum may compete with native macroinvertebrates for food or space (Kerans et al. [2005]) and alter the nutrient cycles, especially nitrogen and carbon (Hall et al. [2003]), with significant effects on higher and lower trophic levels (Kerans et al. [2005]). Potamopyrgus antipodarum is extremely abundant in the spring from Parque O'Higgins, where it reaches thousands of animals per square meter (unpublished data). The snails also are relatively abundant in the other localities, except in Estero La Dehesa, where in one hour of sampling using a sieve, only 15 snails were obtained. This, together with the observation of viable breeding snails and similar size range reported in other invaded regions, suggest that the populations of these animals are well established in central Chile. It is unknown whether the species is more widespread in this country.

Ovoviviparity seems to be an important factor for successful invasions. With this type of reproductive strategy (Winterbourn [1970]; Ponder [1988]), P. antipodarum females brood embryos in a brood pouch and release from 20 to 120 free crawling juveniles (Cheng and LeClair [2011]). Native P. antipodarum populations contain both abundant parthenogenetic females and sexual females and males at a relatively lower proportion (Winterbourn [1970]). However, non-native populations mostly consist of parthenogenetic females, males being rare or absent (Gangloff [1998]; Butkus et al. [2012]). Thus, colonization may have occurred from the introduction of a single female (Proctor et al. [2007]; Cheng and LeClair [2011]; Poirier [2013]). Like P. antipodarum, the exotic ovoviviparous snail Sinotaia quadrata (Benson 1842) (Viviparidae Gray, 1847) was also introduced into South America and is now established in Argentina (Ovando and Cuezzo [2012]).

Potential natural vectors of P. antipodarum include fish, birds, water flow, and floating algae or macrophytes (Vareille-Morel [1983]; Ribi [1986]; Zaranko et al. [1997]; Proctor et al. [2007]). Regarding transport by animals, these snails can survive passage through the digestive system of fish and birds (Haynes et al. [1985]; Ribi [1986]). Non-natural vectors include ship ballast water, freshwater tanks, aquaculture products, aquatic ornamental plants, domestic livestock, firefighting machinery, recreational watercraft and trailers, transport of mud, and sport fishing equipment (Ribi [1986]; Bowler [1991]; Richards et al. [2001]; Proctor et al. [2007]; Ponder et al. [2008]; Alonso and Castro-Diez [2008]); it is unknown how the species came to Chile.

The NZ Mudsnail Management Plan Working Group in USA was established in 2003 to prevent and delay the spread of the introduced P. antipodarum to new areas into the United States (Proctor et al. [2007]). Some of the objectives proposed were identify foci, pathways and vectors of P. antipodarum, develop methods of detecting new populations of this species and develop strategies to control introduced populations. In Chile, exotic freshwater snails have increased in recent times; the main route of introduction has probably been freshwater commercial aquarium trade (Jackson and Jackson [2009]; Letelier et al. [2007]). The procedures proposed by Proctor et al. ([2007]) may be implemented in Chile as a control measure against these species and P. antipodarum.

5 Conclusions

The phylogenetic analysis of COI gene supports the inclusion of the snail sequences from Parque O'Higgins, Estero La Dehesa, Estero Consuelo, and the Chalinga River in central Chile into the Potamopyrgus antipodarum lineage. Thus, the snails studied belong to the family Tateidae. In all locations, sexually mature females were found. Ecological studies are needed to understand the impact of this invasive species on aquatic ecosystems in Chile.

Declarations

Acknowledgements

This study was supported by the Project FONDECYT No. 11130697. I am grateful to anonymous referees for valuable comments to the original manuscript.

Authors’ Affiliations

(1)
Departamento de Ciencias Básicas, Facultad de Ciencias, Universidad del Bío-Bío
(2)
Fundación Chile Natura

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