Invertebrate Systematics Invertebrate Systematics Society
Systematics, phylogeny and biogeography
RESEARCH ARTICLE

Morphology and DNA barcodes reveal the presence of the non-native land planarian Obama marmorata (Platyhelminthes : Geoplanidae) in Europe

Domingo Lago-Barcia A , Fernando A. Fernández-Álvarez A B F , Lisandro Negrete C D , Francisco Brusa C D , Cristina Damborenea C D , Cristina Grande E and Carolina Noreña A
+ Author Affiliations
- Author Affiliations

A Departamento de Biodiversidad y Biología Evolutiva, Museo Nacional de Ciencias Naturales (CSIC), Madrid, Spain.

B Institut de Ciències del Mar (CSIC), Passeig Maritim 37–49, 08003 Barcelona, Spain.

C División Zoología Invertebrados, Museo de La Plata (FCNyM-UNLP), Paseo del Bosque s/n, La Plata, Buenos Aires, Argentina.

D CONICET – Consejo Nacional de Investigaciones Científicas y Técnicas (Argentina).

E Departamento de Biología Molecular and Centro de Biología Molecular ‘Severo Ochoa’ (Consejo Superior de Investigaciones Científicas), Universidad Autónoma de Madrid, 28049 Madrid, Spain.

F Corresponding author. Email: f.a.fernandez.alvarez@gmail.com

Invertebrate Systematics 29(1) 12-22 https://doi.org/10.1071/IS14033
Submitted: 9 July 2014  Accepted: 20 October 2014   Published: 20 March 2015

Abstract

We report for the first time the occurrence of Obama marmorata in the Iberian Peninsula as an introduced species from the Neotropical Region. The species is also reported for the first time in Argentina. The identification was made on the basis of morphological evidence. The divergence levels of a fragment of the mitochondrial cytochrome c oxidase I gene from Argentinean and Iberian samples were studied. The morphology of samples from the two regions was the same and matched the original description of the species. A DNA barcoding matrix was constructed using new sequences from O. marmorata and sequences of related species taken from GenBank. Among the Geoplanidae, interspecific divergence ranged between 3.3 and 14.4%, while intraspecific divergence percentages were 0–1.2%, signalling the presence of a DNA barcoding gap. All O. marmorata sequences, irrespective of their geographic origin, form a well supported clade with an intraspecific divergence of 0–0.9 (average = 0.4%). These results indicate the utility of DNA barcoding to discover allochthonous species in this group of organisms.

Additional keywords: Argentina, exotic species, Geoplaninae, Spain, terrestrial flatworm.


References

Akaike, H. (1974). A new look at the statistical model identification. IEEE Transactions on Automatic Control 19, 716–723.
A new look at the statistical model identification.CrossRef |

Álvarez-Presas, M., and Riutort, M. (2014). Planarian (Platyhelminthes, Tricladida) diversity and molecular markers: a new view of an old group. Diversity 6, 323–338.
Planarian (Platyhelminthes, Tricladida) diversity and molecular markers: a new view of an old group.CrossRef |

Álvarez-Presas, M., Baguñà, J., and Riutort, M. (2008). Molecular phylogeny of land and freshwater planarians (Tricladida, Platyhelminthes): from freshwater to land and back. Molecular Phylogenetics and Evolution 47, 555–568.
Molecular phylogeny of land and freshwater planarians (Tricladida, Platyhelminthes): from freshwater to land and back.CrossRef | 18359250PubMed |

Álvarez-Presas, M., Mateos, E., Vila-Farré, M., Sluys, R., and Riutort, M. (2012). Evidence for the persistence of the land planarian species Microplana terrestris (Müller, 1774) (Platyhelminthes, Tricladida) in microrefugia during the Last Glacial Maximum in the northern section of the Iberian Peninsula. Molecular Phylogenetics and Evolution 64, 491–499.
Evidence for the persistence of the land planarian species Microplana terrestris (Müller, 1774) (Platyhelminthes, Tricladida) in microrefugia during the Last Glacial Maximum in the northern section of the Iberian Peninsula.CrossRef | 22587911PubMed |

Álvarez-Presas, M., Mateos, E., Tudó, À., Jones, H., and Riutort, M. (2014). Diversity of introduced terrestrial flatworms in the Iberian Peninsula: a cautionary tale. PeerJ 2, e430.
Diversity of introduced terrestrial flatworms in the Iberian Peninsula: a cautionary tale.CrossRef | 24949245PubMed |

Baptista, V., and Leal-Zanchet, A. M. (2005). Nova espécie de Geoplana Stimpson (Platyhelminthes, Tricladida, Terricola) do sul do Brasil. Revista Brasileira de Zoologia 22, 875–882.
Nova espécie de Geoplana Stimpson (Platyhelminthes, Tricladida, Terricola) do sul do Brasil.CrossRef |

Bessho, Y., Ohama, T., and Osawa, S. (1992a). Planarian mitochondria I. Heterogeneity of cytochrome c oxidase subunit I gene sequences in the freshwater planarian, Dugesia japonica. Journal of Molecular Evolution 34, 324–330.
Planarian mitochondria I. Heterogeneity of cytochrome c oxidase subunit I gene sequences in the freshwater planarian, Dugesia japonica.CrossRef | 1:CAS:528:DyaK38XitVyqur0%3D&md5=947a46097c2bb2dd5704e54ac1adca82CAS | 1314908PubMed |

Bessho, Y., Ohama, T., and Osawa, S. (1992b). Planarian mitochondria II. The unique genetic code as deduced from cytochrome c oxidase subunit I gene sequences. Journal of Molecular Evolution 34, 331–335.
Planarian mitochondria II. The unique genetic code as deduced from cytochrome c oxidase subunit I gene sequences.CrossRef | 1:CAS:528:DyaK38XitVyquro%3D&md5=37a215758681f574b82233f685b971d1CAS | 1314909PubMed |

Breugelmans, K., Quintana Cardona, J., Artois, T., Jordaens, K., and Backeljau, T. (2012). First report of the exotic blue land planarian, Caenoplana coerulea (Platyhelminthes, Geoplanidae), on Menorca (Balearic Islands, Spain). ZooKeys 199, 91–105.
First report of the exotic blue land planarian, Caenoplana coerulea (Platyhelminthes, Geoplanidae), on Menorca (Balearic Islands, Spain).CrossRef | 22711997PubMed |

Carbayo, F., Álvarez-Presas, M., Olivares, C. T., Marques, F. P. L., Froehlich, E. M., and Riutort, M. (2013). Molecular phylogeny of Geoplaninae (Platyhelminthes) challenges current classification: proposal of taxonomic actions. Zoologica Scripta 42, 508–528.
Molecular phylogeny of Geoplaninae (Platyhelminthes) challenges current classification: proposal of taxonomic actions.CrossRef |

Darriba, D., Taboada, G. L., Doallo, R., and Posada, D. (2012). jModelTest 2: more models, new heuristics and parallel computing. Nature Methods 9, 772.
jModelTest 2: more models, new heuristics and parallel computing.CrossRef | 1:CAS:528:DC%2BC38XhtFWmsbfP&md5=f0463a1a372a25c49bc206a93dc6de15CAS | 22847109PubMed |

Darwin, C. (1844). Brief descriptions of several terrestrial planariae and of some remarkable marine species, with an account of their habits. Annals & Magazine of Natural History 14, 241–251.
Brief descriptions of several terrestrial planariae and of some remarkable marine species, with an account of their habits.CrossRef |

Dendy, A. (1895). Notes on New Zealend land planarians. Part I. Transactions of the New Zealand Institute 27, 177–189.

Fernández-Álvarez, F. Á., and Machordom, A. (2013). DNA barcoding reveals a cryptic nemertean invasion in Atlantic and Mediterranean waters. Helgoland Marine Research 67, 599–605.
DNA barcoding reveals a cryptic nemertean invasion in Atlantic and Mediterranean waters.CrossRef |

Filella-Subirà, E. (1983). Nota sobre la presencia de la planària terrestre Bipalium kewense Moseley, 1878 a Catalunya. Butlleti de la Institució Catalana d’Història Natural 49, 151.

Fiore, C., Tull, J. T., Zehner, S., and Ducey, P. K. (2004). Tracking and predation on earthworms by the invasive terrestrial planarian Bipalium adventitium (Tricladida, Platyhelminthes). Behavioural Processes 67, 327–334.
Tracking and predation on earthworms by the invasive terrestrial planarian Bipalium adventitium (Tricladida, Platyhelminthes).CrossRef | 15518983PubMed |

Froehlich, C. G. (1955). Sôbre espécies brasileiras do gênero Geoplana. Boletim da Faculdade de Filosofia, Ciências e Letras da Universidade de São Paulo. Série Zoologia, São Paulo 19, 289–369.

Froehlich, C. G. (1959). On geoplanids from Brazil. Boletim da Faculdade de Filosofia, Ciências e Letras da Universidade de São Paulo. Série Zoologia, São Paulo 22, 201–242.

Graff, L. v. (1896). Ueber das System und die geographische Verbreitung der Landplanarien. Verhandlungen der Deutschen Zoologischen Gesellschaft 6, 75–93, 61–93.

Graff, L. (1899). ‘Monographie der Turbellarien. II. Tricladida Terricola.’ Leipzig: Verlag von Wilhelm Engelmann 1, XII+574 pp.; 2: 58t. 574 pp.

Haria, A. H., McGrath, S. P., Moore, J. P., Bell, J. P., and Blackshaw, R. P. (1998). Impact of the New Zealand flatworm Artioposthia triangulata on soil structure and hydrology in the UK. The Science of the Total Environment 215, 259–265.
Impact of the New Zealand flatworm Artioposthia triangulata on soil structure and hydrology in the UK.CrossRef | 1:CAS:528:DyaK1cXis1yit7g%3D&md5=bc73b2e3b8d04d8fe61f5ae54d0a6767CAS | 9606946PubMed |

Hutton, F. W. (1880). Additions to the list of New Zealand worms. Transactions of the New Zealand Institute 12, 277–278.

Hyman, L. H. (1939). Land planarians from the Hawaiian Islands. Archives de zoologie expérimentale et génerale. Notes et Revué 80, 116–124.

Iwai, N., Sugiura, S., and Chiba, S. (2010). Prey-tracking behavior in the invasive terrestrial planarian Platydemus manokwari (Platyhelminthes, Tricladida). Naturwissenschaften 97, 997–1002.
Prey-tracking behavior in the invasive terrestrial planarian Platydemus manokwari (Platyhelminthes, Tricladida).CrossRef | 1:CAS:528:DC%2BC3cXhtlaiu7%2FI&md5=2fa28715bbe1a8e439a588e33aa35a67CAS | 20853096PubMed |

Justine, J., Winsor, L., Gey, D., Gros, P., and Thevenot, J. (2014). The invasive New Guinea flatworm Platydemus manokwari in France, the first record for Europe: time for action is now. PeerJ 2, e297.
The invasive New Guinea flatworm Platydemus manokwari in France, the first record for Europe: time for action is now.CrossRef | 24688873PubMed |

Kraepelin, K. (1901). Über die durch den Schiffverkehr in Hamburg eingeschleppten Tiere. Jahrbuch der Hamburgischen Wissenschaftlichen Anstalten 18, 183–209.

Kvist, S., Oceguera-Figueroa, A., Siddall, M. E., and Erséus, C. (2010). Barcoding, types and the Hirudo files: using information content to critically evaluate the identity of DNA barcodes. Mithocondrial DNA 21, 198–205.
Barcoding, types and the Hirudo files: using information content to critically evaluate the identity of DNA barcodes.CrossRef | 1:CAS:528:DC%2BC3cXhsFyksr7J&md5=13b2bca58d0c9d81b89456d2ad3a8a52CAS |

Lang, A. (1881). Untersuchungen zur vergleichenden Anatomie und Histologie des Nervensystemes der Plathelminthen. IV. Das Nervensystem der Tricladen. V. Vergleichende Anatomie des Nervensystemes der Plathelminthen. Mittheilungen aus der Zoologische Station in Neapel, III Bd. Leipzig.

Leal-Zanchet, A. M., and Carbayo, F. (2001). Two new species of land planarians (Platyhelminthes, Tricladida, Terricola) of South Brazil. Journal of Zoology 253, 433–446.
Two new species of land planarians (Platyhelminthes, Tricladida, Terricola) of South Brazil.CrossRef |

Marcus, E. (1951). Turbellaria brasileiros (9). Boletim da Faculdade de Filosofia, Ciências e Letras. Zoologia 16, 5–215.

Mateos, E., Tudó, A., Álvarez-Presas, M., and Riutort, M. (2013). Planàries terrestres exòtiques a la Garrotxa. Annals de la delegació de la Garrotxa de la Institució Catalana d’Història Natural 6, 67–73.

Moseley, H. N. (1877). Notes on the structure of several forms of land planarians, with a description of two new genera and several new species, and a list of all species at present known. Quarterly Journal Microscopical Science. New Series 18, 273–292.

Moseley, H. N. (1878). Description of a new species of land-planarian from the hothouses at Kew Gardens. Annals & Magazine of Natural History 1, 237–239.
Description of a new species of land-planarian from the hothouses at Kew Gardens.CrossRef |

Ogren, R. E. (1995). Predation behavior of land planarians. Hydrobiologia 305, 105–111.
Predation behavior of land planarians.CrossRef |

Pantin, C. F. A. (1953). On the name of the ground fluke Fasciola terrestris O. F. Müller, on Othelosoma symondsi Gray, and on the genus Amblyplana von Graff. Journal of the Linnean Society of London. Zoology (Jena, Germany) 42, 207–218.

Rambaut, A., and Drummond, A. J. (2007). ‘Tracer v1.4.’ Available at: http://beast.bio.ed.ac.uk/Tracer/

Riester, A. (1938). Beiträge zur Geoplaniden-Fauna Brasiliens. Abhandlungen Senckenbergischen Naturforschenden Gesellschaft 441, 1–88.

Riutort, M., Álvarez-Presas, M., Lázaro, E., Solá, E., and Paps, J. (2012). Evolutionary history of the Tricladida and the Platyhelminthes: an up-to-date phylogenetic and systematic account. The International Journal of Developmental Biology 56, 5–17.
Evolutionary history of the Tricladida and the Platyhelminthes: an up-to-date phylogenetic and systematic account.CrossRef | 22450992PubMed |

Romeis, B. (1989). ‘Mikroskopische Technik.’ (17th revised and expanded edition, ed. P. Böck.) (Urban & Schwarzenberg: München, Wien, Baltimore.) 697 pp, 49 Fig., 40 Tab.

Sambrook, J., Fritsch, E., and Maniatis, T. (1989). ‘Molecular Cloning: A Laboratory Manual.’ (Cold Spring Harbor Laboratory: New York.)

Sanna, D., Lai, T., Francalacci, P., Curini-Galletti, M., and Casu, M. (2009). Population structure of the Monocelis lineata (Proseriata, Monocelididae) species complex assessed by phylogenetic analysis of the mitochondrial cytochrome c oxidase subunit I (COI) gene. Genetics and Molecular Biology 32, 864–867.
Population structure of the Monocelis lineata (Proseriata, Monocelididae) species complex assessed by phylogenetic analysis of the mitochondrial cytochrome c oxidase subunit I (COI) gene.CrossRef | 1:CAS:528:DC%2BC3cXpvFyrug%3D%3D&md5=a7a2208c483a3ee8b8b13ee1a27c43d5CAS | 21637466PubMed |

Schultze, M., and Müller, F. (1857). Beiträge zur Kenntniss der Landplanarien nach Mittheilungen des Dr. Fritz Müller in Brasilien und nach eigenen Untersuchungen von Dr. Max Schultze. Abhandlungen der naturforschenden Gesellschaft zu Halle 4(1), 19–38, 61–74 [1856].

Stimpson, W. (1857). Prodromus descriptionis animalium evertebratorum, quae in Expeditione ad Oceanum Pacificum Septentrionalem a Republica Federata missa, Johanne Rodgers Duce, observavit et descripsit. Pars I, Turbellaria Dendrocoela. Proceedings. Academy of Natural Sciences of Philadelphia 9, 19–31.

Sugiura, S. (2010). Prey preference and gregarious attacks by the invasive flatworm Platydemus manokwari. Biological Invasions 12, 1499–1507.
Prey preference and gregarious attacks by the invasive flatworm Platydemus manokwari.CrossRef |

Tamura, K., Stecher, G., Peterson, D., Filipski, A., and Kumar, S. (2013). MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Molecular Biology and Evolution 30, 2725–2729.
MEGA6: Molecular Evolutionary Genetics Analysis version 6.0.CrossRef | 1:CAS:528:DC%2BC3sXhvVKhurzP&md5=a47bf66f019c07034bb59ce53749111aCAS | 24132122PubMed |

Vila-Farré, M., Sluys, R., Mateos, E., Jones, H. D., and Romero, R. (2011). Land planarians (Platyhelminthes: Tricladida: Geoplanidae) from the Iberian Peninsula: new records and description of two new species, with a discussion on ecology. Journal of Natural History 45, 869–891.
Land planarians (Platyhelminthes: Tricladida: Geoplanidae) from the Iberian Peninsula: new records and description of two new species, with a discussion on ecology.CrossRef |

Ward, R. D., Hanner, R., and Hebert, P. D. N. (2009). The campaign to DNA barcode all fishes, FISH-BOL. Journal of Fish Biology 74, 329–356.
The campaign to DNA barcode all fishes, FISH-BOL.CrossRef | 1:CAS:528:DC%2BD1MXjvVWrsbw%3D&md5=7c956a4a711ccfb43ebeca2926c3c223CAS | 20735564PubMed |



Rent Article (via Deepdyve) Export Citation Cited By (3)

View Altmetrics