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Unraveling cryptic invasion of a freshwater snail in Chile based on molecular and morphological data

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Abstract

Cryptic species may cause biological invasions to be overlooked leading to underestimation of the potential impacts of invaders on the new ecosystems. Identification of freshwater snails is challenging because of the scarcity of discriminative morphological characters and the limited taxonomic knowledge of some taxa. Here, molecular and morphological analyses were performed to investigate the identity of viable populations of the genus Physa in aquatic ecosystems of different basins in northern and central Chile, including habitats where the native species Physa chilensis and Physa nodulosa have been traditionally recognized. Molecular analyses based on mitochondrial DNA sequences from the small subunit 16S rDNA and cytochrome c oxidase subunit 1 identified all specimens sequenced as belonging to the globally invasive species Physa acuta. Microscopic examination of the radula and morphological observations of the reproductive system were congruent with these findings. Highly divergent haplotypes found in El Salto suggest multiple introductions of different lineages of the invader in this locality. It is clear that for future management planning a more reliable assessment of the status of P. chilensis and P. nodulosa is required.

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References

  • Albrecht C, Schultheiss R, Kevrekidis T, Streit B, Wilke T (2007) Invaders or endemics? Molecular phylogenetics, biogeography and systematics of Dreissena in the Balkans. Freshw Biol 52:1525–1536

    Article  Google Scholar 

  • Albrecht C, Kroll O, Terrazas EM, Wilke T (2009) Invasion of ancient Lake Titicaca by the globally invasive Physa acuta (Gastropoda: Pulmonata: Hygrophila). Biol Invasions 11:1821–1826

    Article  Google Scholar 

  • Albrecht C, Föller K, Hauffe T, Clewing C, Wilke T (2014) Invaders versus endemics: alien gastropod species in ancient Lake Ohrid. Hydrobiologia 739:163–174

    Article  Google Scholar 

  • Appleton CC (2003) Alien and invasive fresh water Gastropoda in South Africa. Afr J Aquat Sci 28:69–81

    Article  Google Scholar 

  • Araya JF (2015) 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). J Nat His 49:1731–1761

    Article  Google Scholar 

  • Armstrong KF, Ball SL (2005) DNA Barcodes for biosecurity: invasive species identification. Philos Trans R Soc B 360:1813–1823

    Article  CAS  Google Scholar 

  • Bennett CE, Wilson BS, DeSalle R (2011) DNA barcoding of an invasive mammal species, the small Indian mongoose (Herpestes javanicus; E. Geoffroy Saint-Hillaire 1818) in the Caribbean and Hawaiian Islands. Mitochondrial DNA 22:12–18

    Article  CAS  PubMed  Google Scholar 

  • Biese WA (1948) Revisión de los moluscos terrestres y de agua dulce provistos de concha de Chile. Familia Ancylidae y Physidae. Bol Mus Nac Hist Nat 24:217–239

    Google Scholar 

  • Brown DS (1994) Freshwater snails of Africa and their medical importance, 2nd edn. Taylor and Francis, London

    Google Scholar 

  • Clench WJ (1930) Notes on Physidae with descriptions of new species. Occas Pap Boston Soc Nat Hist 5:301–315

    Google Scholar 

  • Collado GA (2014) Out of New Zealand: molecular identification of the highly invasive freshwater mollusk Potamopyrgus antipodarum (Gray, 1843) in South America. Zool Stud 53:70

    Article  Google Scholar 

  • Cope NJ, Winterbourn MJ (2004) Competitive interactions between two successful molluscan invaders of freshwaters: an experimental study. Aquat Ecol 38:83–91

    Article  Google Scholar 

  • Crawford AJ, Alonso R, Jaramillo C, Sucre S, Ibáñez R (2011) DNA barcoding identifies a third invasive species of Eleutherodactylus (Anura: Eleutherodactylidae) in Panama City, Panama. Zootaxa 2890:65–67

    Google Scholar 

  • de Kock KN, Wolmarans CT (2007) Distribution and habitats of the alien invader freshwater snail Physa acuta in South Africa. Water SA 33:717–722

    Google Scholar 

  • Dillon RT, Wethington A, Rhett J, Smith T (2002) Populations of the European freshwater pulmonate Physa acuta are not reproductively isolated from American Physa heterostropha or Physa integra. Inverteb Biol 121:226–234

    Article  Google Scholar 

  • Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791

    Article  Google Scholar 

  • Fernández D (1981) Mollusca, Gasteropoda, Physidae. Fauna Agua Dulce Repúb Argent 15:83–98

    Google Scholar 

  • Fernández-Álvarez FÁ, Machordom A (2013) DNA barcoding reveals a cryptic nemertean invasion in Atlantic and Mediterranean waters. Helgol Mar Res 67:599–605

    Article  Google Scholar 

  • Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol 3:294–299

    CAS  PubMed  Google Scholar 

  • Früh D, Haase P, Stoll S (2015) Temperature drives asymmetric competition between alien and indigenous freshwater snails (Physa acuta vs. Physa fontinalis). PeerJ 3:e1227. Available at https://dx.doi.org/10.7287/peerj.preprints.997v1

  • Fuentealba C, Figueroa R, Morrone JJ (2010) Análisis de endemismo de moluscos dulceacuícolas de Chile. Rev Chil Hist Nat 83:289–298

    Article  Google Scholar 

  • Gates KK, Kerans BL, Keebaugh J, Kalinowski S, Vu N (2013) Taxonomic identity of the endangered Snake River physa, Physa natricina (Pulmonata: Physidae) combining traditional and molecular techniques. Conserv Genet 14:159–169

    Article  Google Scholar 

  • Germain L (1913) Une nouvelle espèce de Physe du Chili. Rev Chil Hist Nat 17:161–166

    Google Scholar 

  • Gould AA (1847) Dr. Gould read descriptions of species of Physa, from the collection of the Exploring Expedition. Proc Boston Soc Nat Hist 2:214–215

    Article  Google Scholar 

  • Gray JE (1828) Spicilegia zoologica; or original figures and short systematic descriptions of new and unfigured animals. Treüttel, Würtz & Co & Wood, London

    Google Scholar 

  • Gustafson KD, Kensinger BJ, Bolek MG, Luttbeg B (2014) Distinct snail (Physa) morphotypes from different habitats converge in shell shape and size under common garden conditions. Evol Ecol Res 16:77–89

    Google Scholar 

  • Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analyses. Nucl Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  • Hamilton-Attwell VL, De Kock KN, Van Eeden JA (1970) The occurrence and distribution of Physa acuta Draparnaud in the Republic of South Africa. Wetenskap Byd Potchefst Univ CEO B 26:1–11

    Google Scholar 

  • Ibáñez M, Alonso MR (2003) Physella (Costatella) acuta (Draparnaud, 1805) en las islas Canarias (Pulmonata Basommatophora: Planorboidea: Physidae). Vieraea 31:133–144

    Google Scholar 

  • Küster HK, Dunker W, Clessin S (1841–1886) Die Familie der Limnaeiden enthaltend die Genera Planorbis, Limnaeus, Physa und Amphipeplea. Systematisches Conchylien-Cabinet von Martini und Chemnitz. Ersten Bandes siebenzehnte Abtheilung. Bauer & Raspe, Nürnberg

  • Letelier S, Ramos AM, Huaquín L (2007) Moluscos dulceacuícolas exóticos en Chile. Rev Mex Biodivers 78:9–13

    Google Scholar 

  • Lowe S, Browne M, Boudlejas S (2000) 100 of the world’s worst invasive alien species. Invasive Species Specialist Group, Auckland

    Google Scholar 

  • Madsen H, Frandsen F (1989) The spread of freshwater snails including those of medical and veterinary importance. Acta Trop 46:139–146

    Article  CAS  PubMed  Google Scholar 

  • Manganelli G, Bodon M, Cianfanelli S, Favilli L, Giusti F (2000) Conoscenza e conservazione dei molluschi non marini italiani: lo stato delle ricerche. Boll Malacol 36:5–42

    Google Scholar 

  • Miquel SE (1985) Presencia del género Physella Haldeman, 1842 en la República Argentina (Mollusca Pulmonada Physidae). Neotrópica 31:38

    Google Scholar 

  • Miquel SE, Zelaya DG (1999) Nuevos hallazgos de Physella cubensis y P. venustula en la Argentina (Mollusca: Physidae). Physis Secc B 57:9–10

    Google Scholar 

  • Mouthon J, Daufresne M (2010) Long-term changes in mollusc communities of the Ognon river (France) over a 30-year period. Fundam Appl Limnol 178:67–79

    Article  CAS  Google Scholar 

  • Núñez V (2011) Revisión de dos especies de Physidae. Rev Mex Biodivers 82:93–108

    Google Scholar 

  • Núñez V, Pelichotti PE (2003) Sinopsis y nuevas citas para la distribución de la familia Physidae en la Argentina (Gastropoda: Basommatophora). Comun Soc Malacol Urug 8:259–261

    Google Scholar 

  • Paetel F (1888). Catalog der Conchylien-sammlung von Fr. Paetel. Vierte Neubearbeitung. Zweite Abtheilung: die Land- und Süsswasser-Gastropoden. Gebrüder Paetel, Berlin

  • Palumbi SR (1996) Nucleic acids II: the polymerase chain reaction. In: Hillis DM, Moritz C, Mable BK (eds) Molecular systematics. Sinauer Associates, Sunderland, pp 205–247

    Google Scholar 

  • Paraense WL (1987) Physa cubensis Pfeiffer, 1839 (Pulmonata: Physidae). Mem Inst Oswaldo Cruz 82:15–20

    Article  Google Scholar 

  • Paraense W (2003) Planorbidae, Lymnaeidae and Physidae of Peru (Mollusca: Basommatophora). Mem Inst Oswaldo Cruz 98:767–771

    Article  PubMed  Google Scholar 

  • Paraense WL (2005) Planorbidae, Lymnaeidae and Physidae of Argentina (Mollusca: Basommatophora). Mem Inst Oswaldo Cruz 100:491–493

    Article  PubMed  Google Scholar 

  • Paraense WL, Pointier J-P (2003) Physa acuta Draparnaud, 1805 (Gastropoda: Physidae): a study of topotypic specimens. Mem Inst Oswaldo Cruz 98:513–517

    Article  PubMed  Google Scholar 

  • Parodiz JJ (1956) Notas sobre Physa (Gastr. Pulm. Basom.). Neotropica 2:19–21

    Google Scholar 

  • Pastorino G, Darrigan (2011) Haitia venustula. The IUCN Red List of Threatened Species 2011: e.T189126A8689055. http://dx.doi.org/10.2305/IUCN.UK.2011-2.RLTS.T189126A8689055.en. Downloaded on 17 April 2016

  • Pip E, Frank JPC (2008) Molecular phylogenetics of central Canadian Physidae (Pulmonata: Basommatophora). Can J Zool 86:10–16

    Article  CAS  Google Scholar 

  • Posada D (2008) jModelTest: phylogenetic model averaging. Mol Biol Evol 25:1253–1256

    Article  CAS  PubMed  Google Scholar 

  • Remigio EA (2002) Molecular phylogenetic relationships in the aquatic snail genus Lymnaea, the intermediate host of the causative agent of fascioliasis: insights from broader taxon sampling. Parasitol Res 88:687–696

    Article  CAS  PubMed  Google Scholar 

  • Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574

    Article  CAS  PubMed  Google Scholar 

  • Rozas J, Sánchez-DelBarrio JC, Messeguer X, Rozas R (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496–2497

    Article  CAS  PubMed  Google Scholar 

  • Semenchenko V, Laenko T, Razlutskij V (2008) A new record of the North American gastropod Physa acuta (Draparnaud 1805) from the Neman River Basin, Belarus. Aquat Invasions 3:359–360

    Article  Google Scholar 

  • Sielfeld W (2001) Phylum Mollusca. Guías de identificación y biodiversidad fauna chilena. Apuntes de Zoología. Universidad Arturo Prat, Iquique

    Google Scholar 

  • Smith KF, Thia J, Gemmill CEC, Cary SC, Fidler AE (2012) Barcoding of the cytochrome oxidase I (COI) indicates a recent introduction of Ciona savignyi into New Zealand and provides a rapid method for Cion species discrimination. Aquat Invasions 7:205–313

    Article  Google Scholar 

  • Sowerby GB, I (1821–1834) The genera of recent and fossil shells, for the use of students in conchology and geology. Published by the author, London

  • Stuardo J (1961) Contribución a un catálogo de los moluscos chilenos de agua dulce. Con una clave adicional de generos. Gayana Zool 1:7–32

    Google Scholar 

  • Swofford DL (2003) PAUP*: Phylogenetic analysis using parsimony (*and other methods). Ver. 4. Sinauer Associates, Sunderland

    Google Scholar 

  • Taylor DW (2003) Introduction to Physidae (Gastropoda: Hygrophila); biogeography, classification, morphology. Rev Biol Trop 51:1–263

    CAS  PubMed  Google Scholar 

  • Thompson JD, Gibson TJ, Plewnia KF, Jeanmougin F, Higgins DG (1997) The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucl Acid Res 25:4876–4882

    Article  CAS  Google Scholar 

  • Valdovinos C (1999) Biodiversidad de moluscos chilenos: Base de datos taxonómica y distribucional. Gayana 63:111–164

    Google Scholar 

  • Valdovinos C (2006) Estado de conocimiento de los gastrópodos dulceacuícolas de Chile. Gayana 70:88–95

    Google Scholar 

  • Velásquez LE, Escobar JS (2001) Physa cubensis Pfeiffer, 1839 (Pulmonata: Physidae) en la sabana de Bogotá (Cundinamarca, Colombia). Actual Biol 23:75–80

    Google Scholar 

  • von Beeren C, Stoeckle MY, Xia J, Burke G, Kronauer DJC (2015) Interbreeding among deeply divergent mitochondrial lineages in the American cockroach (Periplaneta americana). Sci Rep 5:1–7

    Google Scholar 

  • Wethington AR, Lydeard C (2007) A molecular phylogeny of Physidae (Gastropoda: Basommatophora) based on mitochondrial DNA sequences. J Molluscan Stud 73:241–257

    Article  Google Scholar 

  • Wethington AR, Wise J, Dillon RT (2009) Genetic and morphological characterization of the Physidae of South Carolina (Pulmonata: Basommatophora), with description of a new species. Nautilus 123:282–292

    Google Scholar 

  • Wilcove DS, Rothstein D, Dubow J, Phillips A, Losos E (1998) Quantifying threats to imperiled species in the United States. Bioscience 48:607–615

    Article  Google Scholar 

  • Winnepennickx B, Backeljau T, De Wachter R (1993) Extraction of high molecular weight DNA from molluscs. Trends Genet 9:407

    Article  Google Scholar 

  • Yong Cong M, Ferrer Lopez JR, Perera de Puga G (1994) Anatomía y morfometría de Physa cubensis Pfeiffer, 1839 (Pulmonata: Physidae) en Cuba. Rev Cuba Med Trop 46:37–41

    Google Scholar 

  • Zukowski S, Walker KF (2009) Freshwater snails in competition: alien Physa acuta (Physidae) and native Glyptophysa gibbosa (Planorbidae) in the River Murray, South Australia. Mar Freshw Res 60:999–1005

    Article  CAS  Google Scholar 

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Acknowledgements

I thank the staff of the Museo de Ciencias Naturales Profesor Pedro Ramírez Fuentes, Chillán, Chile. I am also grateful to Francis Miño and Nicolás Villalobos for field assistance and Cristian Suárez for technical support. This study was supported by the project DIUBB 153309 2/R and FONDECYT No. 11130697. I also thank the CONICYT-FONDEQUIP Program (No. EQM-140088) for acquisition of the Hitachi Scanning Electron Microscope and the anonymous referees for valuable comments on the original manuscript. The author is authorized to collect snails in Chile (Resolution No. 3285, Subsecretaría de Pesca y Acuicultura, Ministerio de Economía, Fomento y Turismo, República de Chile).

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Correspondence to Gonzalo A. Collado.

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Communicated by Robert Cowie.

This article belongs to the Topical Collection: Invasive species.

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Collado, G.A. Unraveling cryptic invasion of a freshwater snail in Chile based on molecular and morphological data. Biodivers Conserv 26, 567–578 (2017). https://doi.org/10.1007/s10531-016-1255-y

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