Hostname: page-component-7c8c6479df-xxrs7 Total loading time: 0 Render date: 2024-03-26T23:21:19.871Z Has data issue: false hasContentIssue false

Does GenBank provide a reliable DNA barcode reference to identify small alien oysters invading the Mediterranean Sea?

Published online by Cambridge University Press:  08 August 2014

F. Crocetta
Affiliation:
Stazione Zoologica Anton Dohrn, Villa Comunale, I-80121 Napoli, Italy
P. Mariottini
Affiliation:
Dipartimento di Scienze, Università ‘Roma Tre’, Viale G. Marconi 446, I-00146 Rome, Italy
D. Salvi
Affiliation:
CIBIO, Centro de Investigação em Biodiversidade e Recursos Genéticos, Campus Agrário de Vairão, 4485-661 Vairão, Portugal
M. Oliverio*
Affiliation:
Dipartimento di Biologia e Biotecnologie ‘Charles Darwin’, Università di Roma ‘La Sapienza’, Viale dell'Università 32, I-00185 Rome, Italy
*
Correspondence should be addressed to: M. Oliverio, Dipartimento di Biologia e Biotecnologie ‘Charles Darwin’, Università di Roma ‘La Sapienza’, Viale dell'Università 32, I-00185 Rome, Italy email: marco.oliverio@uniroma1.it

Abstract

The Mediterranean Sea is currently under siege by a conspicuous alien pressure, and, within some families (e.g. the Ostreidae), the number of native species seems to be remarkably outnumbered by that of the alien ones. We wanted to test the reliability of the molecular data currently available on the small alien oysters recently invading the Mediterranean Sea. Samples from Greece and Turkey, encompassing the known species-specific morphological variation, were sequenced for the markers with the widest taxonomic coverage in the group of small oysters (i.e. the 16S rDNA and the COI). The sequences obtained have been compared with those available in GenBank, and a possible identification at the species level has been finally tested in a DNA-barcoding fashion. The present results clearly demonstrated that our samples belong to a single, morphologically highly variable species. Their 16S sequences were closely related to a sequence registered under the name Dendostrea folium, with a genetic distance which does not warrant conspecificity. Additionally, a remarkable number of sequences retrieved from the GenBank (of both genes) did not form a monophyletic group according to the published classification of the vouchers, suggesting—at least in part—an origin from specimens not properly identified. Both genes seem promising for use as DNA-barcode, although the COI will probably prove more effective. Therefore, we urge the availability of a baseline of oyster pedigreed DNA barcode sequences in the public databases, to allow the use of such genetic data to reliably monitor bio-invasions in the Mediterranean Sea.

Type
Research Article
Copyright
Copyright © Marine Biological Association of the United Kingdom 2014 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Albano, P.G., Rinaldi, E., Evangelisti, F., Kuan, M. and Sabelli, B. (2009) On the identity and origin of Anadara demiri (Bivalvia: Arcidae). Journal of the Marine Biological Association of the United Kingdom 89, 12891298.Google Scholar
Albayrak, S. (2011) Alien marine bivalve species reported from Turkish seas. Cahiers de Biologie Marine 52, 107118.Google Scholar
Antit, M., Gofas, S., Salas, C. and Azzouna, A. (2011) One hundred years after Pinctada: an update on alien Mollusca in Tunisia. Mediterranean Marine Science 12, 5373.Google Scholar
Barash, A. and Danin, Z. (1986) Further additions to the knowledge of Indo-Pacific Mollusca in the Mediterranean Sea (Lessepsian migration). Spixiana 9, 117141.Google Scholar
Bianchi, C.N., Morri, C., Chiantore, M., Montefalcone, M., Parravicini, V. and Rovere, A. (2012) Mediterranean Sea biodiversity between the legacy from the past and a future of change. In Stambler, N. (ed.) Life in the Mediterranean Sea: a look at habitat changes. New York: Nova Science Publishers, Chapter 1, pp. 155.Google Scholar
Blundo, C., Castagnolo, L. and Lumare, F. (1972) Nota sull'accrescimento di Crassostrea angulata (Lmk) e Crassostrea gigas (Thun) nella laguna di Varano e primi tentativi di fecondazione artificiale. Bollettino di Pesca, di Piscicoltura e di Idrobiologia 27, 297315.Google Scholar
Bosch, D.T., Dance, S.P., Moolenbeek, R.G. and Oliver, P.G. (1995) Seashells of Eastern Arabia. Dubai: Motivate Publishing.Google Scholar
Boudry, P., Heurtebise, S. and Lapègue, S. (2003) Mitochondrial and nuclear DNA sequence variation of presumed Crassostrea gigas and C. angulata specimens: a new oyster species in Hong Kong? Aquaculture 228, 1525.Google Scholar
Cesari, P. (1994) I molluschi della laguna di Venezia. Venezia: Arsenale Editrice.Google Scholar
Cesari, P. and Pellizzato, M. (1985) Molluschi pervenuti in laguna di Venezia per apporti volontari o casuali. Acclimatazione di Saccostrea commercialis (Iredale & Roughley, 1933) e di Tapes philippinarum (Adams & Reeve, 1850). Bollettino Malacologico 21, 237274.Google Scholar
Çevik, C., Öztürk, B. and Buzzurro, G. (2001) The presence of Crassostrea virginica (Gmelin, 1791) and Saccostrea commercialis (Iredale and Roughley, 1933) in the eastern Mediterranean Sea. La Conchiglia 298, 2528.Google Scholar
Çeviker, D. (1999) Lessepsians from Indian Ocean and the Red Sea. Sualti Dűnyasi 45, 2227.Google Scholar
Çeviker, D. (2001) Recent immigrant bivalves in the north-eastern Mediterranean off Iskenderun. La Conchiglia 298, 3946.Google Scholar
Çinar, M.E., Bilecenoğlu, M., Őztűrk, B., Katağan, T., Yokeş, M.B., Aysel, V., Dağli, E., Açik, S., Őzcan, T. and Erdoğan, H. (2011) An updated review of alien species on the coasts of Turkey. Mediterranean Marine Science 12, 257315.Google Scholar
Cossignani, T. and Ardovini, R. (2011) Malacologia Mediterranea. Atlante delle conchiglie del Mediterraneo—7.500 foto a colori. Ancona: L'Informatore Piceno.Google Scholar
Cossignani, T., Cossignani, V., Di Nisio, A. and Passamonti, M. (1992) Atlante delle conchiglie del medio Adriatico. Ancona: L'Informatore Piceno.Google Scholar
Crocetta, F. (2011) Marine alien Mollusca in the Gulf of Trieste and neighbouring areas: a critical review and state of knowledge (updated in 2011). Acta Adriatica 52, 247260.Google Scholar
Crocetta, F. (2012) Marine alien Mollusca in Italy: a critical review and state of the knowledge. Journal of the Marine Biological Association of the United Kingdom 92, 13571365.CrossRefGoogle Scholar
Crocetta, F., Bitar, G., Zibrowius, H. and Oliverio, M. (2013b) Biogeographical homogeneity in the eastern Mediterranean Sea. II. Temporal variation in Lebanese bivalve biota. Aquatic Biology 19, 7584.CrossRefGoogle Scholar
Crocetta, F., Macali, A., Furfaro, G., Cooke, S., Villani, G. and Valdés, Á. (2013a) Alien molluscan species established along the Italian shores: an update, with discussions on some Mediterranean “alien species” categories. ZooKeys 277, 91108.Google Scholar
Dantan, J.L. and Heldt, H. (1932) L'ostréiculture en Tunisie. Résultats acquis dans le lac de Porto Farina. Bulletin—Station Océanographique de Salammbô 30, 130.Google Scholar
Delongueville, C. and Scaillet, R. (2006) Mollusques associés à Spondylus spinosus Schreibers, 1793 dans le golfe d'Iskenderun (Turquie). Novapex 7, 2933.Google Scholar
Fabioux, C., Huvet, A., Lapègue, S., Heurtebise, S. and Boudry, P. (2002) Past and present geographical distribution of populations of Portoguese (Crassostrea angulata) and Pacific (C. gigas) oysters along the European and North African Atlantic coasts. Haliotis 31, 3344.Google Scholar
Folmer, O., Black, M., Hoeh, W., Lutz, R. and Vrijenhoek, R. (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3, 294299.Google Scholar
Galil, B.S. (2007) Seeing red: alien species along the Mediterranean coast of Israel. Aquatic Invasions 2, 281312.Google Scholar
Galil, B.S. and Goren, M. (2014) Metamorphoses: bioinvasions in the Mediterranean Sea. In Goffredo, S. and Dubinsky, Z. (eds) The Mediterranean Sea: its history and present challenges. Dordrecht: Springer, Chapter 27, pp. 463478.Google Scholar
Giannuzzi-Savelli, R., Pusateri, F., Palmeri, A. and Ebreo, C. (2001) Atlante delle conchiglie marine del Mediterraneo. Volume 7. (BIVALVIA: ProtobranchiaPteriomorpha). Roma: Edizioni Evolver srl.Google Scholar
Gunter, G. (1950) The generic status of living oysters and the scientific name of the common American species. American Midland Naturalist 43, 438449.Google Scholar
Haas, G. (1948) Sur l'immigration de Mollusques Indo-Pacifiques dan les eaux côtières de la Palestine. Journal de Conchyliologie 88, 141144.Google Scholar
Huber, M. (2010) Compendium of bivalves. A full-color guide to 3,300 of the world's marine bivalves. A status on Bivalvia after 250 years of research. Hackenheim: ConchBooks.Google Scholar
Jozefowicz, C.J. and Ó Foighil, D. (1998) Phylogenetic analysis of southern hemisphere flat oysters based on partial mitochondrial 16S rDNA gene sequences. Molecular Phylogenetics and Evolution 10, 426435.Google Scholar
Katsanevakis, S., Tsiamis, K., Ioannou, G., Michailidis, N. and Zenetos, A. (2009) Inventory of alien marine species of Cyprus (2009). Mediterranean Marine Science 10, 109133.CrossRefGoogle Scholar
Keller, C. (1883) Die Fauna im Suez-Kanal und die Diffusion der Mediterranen und Erythräischen Thierwelt. Eine thiergeographische Untersuchung. Neue Denkschriften der Allgemeinen Schweizerischen Gesellschaft für die gesammten Naturwissenschaften 28, 139.Google Scholar
Korringa, P. (1952) Recent advances in oyster biology. Quaterly Review of Biology 27, 266308, 339–365.Google Scholar
Krŭić, P. (2014) Bioconstructions in the Mediterranean: present and future. In Goffredo, S. and Dubinsky, Z. (eds) The Mediterranean Sea: its history and present challenges. Dordrecht: Springer, Chapter 25, pp. 435447.Google Scholar
Kumar, S., Tamura, K. and Nei, M. (2004) MEGA 3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Briefings in Bioinformatics 5, 150163.Google Scholar
Lam, K. and Morton, B. (2003) Mitochondrial DNA and morphological identification of a new species of Crassostrea (Bivalvia: Ostreidae) cultured for centuries in the Pearl River Delta, Hong Kong, China. Aquaculture 228, 113.Google Scholar
Lam, K. and Morton, B. (2004) The oysters of Hong Kong (Bivalvia: Ostreidae and Gryphaeidae). Raffles Bulletin of Zoology 52, 1128.Google Scholar
Lapègue, S., Batista, R.M., Heurtebise, S., Yu, Z.N. and Boudry, P. (2004) Evidence for the presence of the Portuguese oyster, Crassostrea angulata, in Northern China. Journal of Shellfish Research 23, 759763.Google Scholar
Liu, J., Li, Q., Kong, L., Yu, H. and Zheng, X. (2011) Identifying the true oysters (Bivalvia: Ostreidae) with mitochondrial phylogeny and distance-based DNA barcoding. Molecular Ecology Resources 11, 820830.Google Scholar
Lόpez-Flores, I., de la Herrán, R., Garrido-Ramos, M.A., Boudry, P., Ruiz-Rejón, C. and Ruiz-Rejón, M. (2004) The molecular phylogeny of oysters based on a satellite DNA related to transposons. Gene 339, 181188.Google Scholar
Lόpez-Flores, I., Ruiz-Rejόn, C., Cross, I., Rebordinos, L., Robles, F., Navajas-Pérez, R. and de la Herrán, R. (2010) Molecular characterization and evolution of an interspersed repetitive DNA family of oysters. Genetica 138, 12111219.Google Scholar
Lubinevsky, H. and Mienis, H.K. (2005) A first record of Nanostrea exigua Harry, 1985, another exotic mollusc species from the eastern Mediterranean Sea. Triton 12, 34.Google Scholar
Manzi, V., Gennari, R., Hilgen, F., Krijgsman, W., Lugli, S., Roveri, M. and Sierro, F.J. (2013) Age refinement of the Messinian salinity crisis onset in the Mediterranean. Terra Nova 25, 315322.Google Scholar
Matta, F. (1969) Sull'acclimatazione e l'accrescimento di Gryphea angulata Lmk. in alcune regioni adriatiche. Bollettino di Pesca, di Piscicoltura e di Idrobiologia 23, 171258.Google Scholar
Mazzarelli, G. (1936) L'ostrica portoghese (Gryphaea angulata Lam.) nel lago Fusaro (Napoli). Memorie di Biologia Marina ed Oceanografia 4, 311.Google Scholar
Mienis, H.K. (2004) New data concerning the presence of Lessepsian and other Indo-Pacific migrants among the molluscs in the Mediterranean Sea with emphasis on the situation in Israel. Turkish Journal of Aquatic Life 2, 117131.Google Scholar
Mienis, H.K. (2008) Marine mollusken uit het oostelijk dell van de Middellandse Zee, 29. Een bevestiging van het voorkomen van Nanostrea exigua Harry, 1985. Spirula 363, 67.Google Scholar
Mienis, H.K., Rittner, O., Rilov, G. and Almog, O. (2012a) Some additional records of two hardly known lessepsian migrants among the molluscs from the Mediterranean coast of Israel. Triton 26, 13.Google Scholar
Mienis, H.K., Zaslow, R.B.-D. and Rittner, O. (2012b) First records of Alectryonella plicatula from the Mediterranean coast of Israel (Mollusca, Bivalvia, Ostreidae). Triton 26, 45.Google Scholar
Mizzan, L. (1999) Le specie alloctone del macrozoobenthos della Laguna di Venezia: il punto della situazione. Bollettino del Museo Civico di Storia Naturale di Venezia 49, 145177.Google Scholar
Monterosato, T.A. (1915) Ostreae ed Anomiae del Mediterraneo. Annali del Museo Civico di Storia Naturale di Genova 47, 716.Google Scholar
Nei, M. and Kumar, S. (2000) Molecular evolution and phylogenetics. New York: Oxford University Press.Google Scholar
Nunes, A.L., Katsanevakis, S., Zenetos, A. and Cardoso, A.C. (2014) Gateways to alien invasions in the European seas. Aquatic Invasions 9, 133144.Google Scholar
Ojaveer, H., Galil, B.S., Minchin, D., Olenin, S., Amorim, A., Canning-Clode, J., Chainho, P., Copp, G.H., Gollasch, S., Jelmert, A., Lehtiniemi, M., McKenzie, C., Mikuš, J., Miossec, L., Occhipinti-Ambrogi, A., Pećarević, M., Pederson, J., Quilez-Badia, G., Wijsman, J.W.M. and Zenetos, A. (2014) Ten recommendations for advancing the assessment and management of non-indigenous species in marine ecosystems. Marine Policy 44, 160165.Google Scholar
Oliver, P.G. (1992) Bivalved seashells of the Red Sea. Cardiff: Christa Hemmen, Verlag and The National Museum of Wales.Google Scholar
Oliverio, M. and Mariottini, P. (2001) A molecular framework for the phylogeny of Coralliophila and related muricoids. Journal of Molluscan Studies 67, 215224.Google Scholar
Pallary, P. (1912) Catalogue des mollusques du littoral Méditerranéen de l'Égypte. Mémoires de l'Institut Égyptien 7, 69205.Google Scholar
Palumbi, S., Martin, A., Romano, S., McMillan, W.O., Stice, L. and Grabowski, G. (2001) The simple fool's guide to PCR Version 2.0. Honolulu, HI: Department of Zoology and Kewalo Marine Laboratory, University of Hawaii.Google Scholar
Pascoal, S., Carvalho, G., Creer, S., Rock, J., Kawaii, K., Mendo, S. and Hughes, R. (2012) Plastic and heritable components of phenotypic variation in Nucella lapillus: an assessment using reciprocal transplant and common garden experiments. Plos ONE 7, e30289. doi:10.1371/journal.pone.0030289.Google Scholar
Pećarević, M., Mikuš, J., Bratoš Cetinić, A., Dulčić, J. and Čalić, M. (2013) Introduced marine species in Croatian waters (Eastern Adriatic Sea). Mediterranean Marine Science 14, 224237.Google Scholar
Polson, M.P., Hewson, W.E., Eernisse, D.J., Baker, P.K. and Zacherl, D.C. (2009) You say conchaphila, I say lurida: molecular evidence for restricting the olympia oyster (Ostrea lurida Carpenter 1864) to temperate western North America. Journal of Shellfish Research 28, 1121.Google Scholar
Reece, K.S., Cordes, J.F., Stubbs, J.B., Hudson, K.L. and Francis, E.A. (2008) Molecular phylogenies help resolve taxonomic confusion with Asian Crassostrea oyster species. Marine Biology 153, 709721.Google Scholar
Sabelli, B. and Taviani, M. (2014) The making of the Mediterranean molluscan biodiversity. In Goffredo, S. and Dubinsky, Z. (eds) The Mediterranean Sea: its history and present challenges. Dordrecht: Springer, Chapter 16, pp. 285396.Google Scholar
Salvi, D., Bellavia, G., Cervelli, M. and Mariottini, P. (2010) The analysis of rRNA sequence-structure in phylogenetics: an application to the family Pectinidae (Mollusca: Bivalvia). Molecular Phylogenetics and Evolution 56, 10591067.Google Scholar
Salvi, D. and Mariottini, P. (2012) Molecular phylogenetics in 2D: ITS2 rRNA evolution and sequence-structure barcode from Veneridae to Bivalvia. Molecular Phylogenetics and Evolution 65, 792798.Google Scholar
Seilacher, A., Matyla, B.A. and Wierzbowski, A. (1985) Oyster beds: morphologic response to changing substrate conditions. In Bayer, U. and Seilacher, A. (eds) Sedimentary and evolutionary cycles. New York: Springer-Verlag, pp. 421435.CrossRefGoogle Scholar
Sharabati, D. (1984) Red Sea shells. London, Boston, Melbourne, Henley: KPI.Google Scholar
Sharon, Y., Benayahu, Y. and Mienis, H.K. (2005) First record of an exotic oyster: Alectryonella crenulifera, from the Mediterranean coast of Israel. Triton 12, 56.Google Scholar
Solas, M.R., Sepúlveda, R.D. and Brante, A. (2013) Genetic variation of the shell morphology in Acanthina monodon (Gastropoda) in habitats with different wave exposure conditions. Aquatic Biology 18, 253260.Google Scholar
Tamura, K., Peterson, D., Peterson, N., Steker, G., Nei, M. and Kumar, S. (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution 28, 27312739.Google Scholar
Tavaré, S. (1986) Some probabilistic and statistical problems in the analysis of DNA sequences. Lectures on Mathematics in the Life Sciences 17, 5786.Google Scholar
Taviani, M. (2002) The Mediterranean benthos from late Miocene up to present: ten million years of dramatic climatic and geologic vicissitudes. Biologia Marina Mediterranea 9, 445463.Google Scholar
Thompson, J.D., Gibson, T.J., Plewniak, F., Jeanmougin, F. and Higgins, D.G. (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research 25, 48764882.Google Scholar
Valdés, Á., Alexander, J., Crocetta, F., Baki Yokeş, M., Giacobbe, S., Poursanidis, D., Zenetos, A., Cervera, J.L., Caballer, M., Galil, B.S. and Schembri, P.J. (2013) The origin and dispersal pathway of the spotted sea hare Aplysia dactylomela (Mollusca: Opisthobranchia) in the Mediterranean Sea. Aquatic Invasions 8, 427436.Google Scholar
Wang, H.Y., Guo, X.M., Zhang, G.F. and Zhang, F.S. (2004) Classification of jingjiang oysters Crassostrea rivularis (Gould, 1861) from China, based on morphology and phylogenetic analysis. Aquaculture 242, 137155.Google Scholar
Wang, H.Y., Zhang, G.F., Liu, X. and Guo, X.M. (2008) Classification of common oysters from north China. Journal of Shellfish Research 27, 495503.Google Scholar
Zenetos, A., Gofas, S., Morri, C., Rosso, A., Violanti, D., Garcia Raso, J.E., Çinar, M.E., Almogi-Labin, A., Ates, A.S., Azzurro, E., Ballesteros, E., Bianchi, C.N., Bilecenoglu, M., Gambi, M.C., Giangrande, A., Gravili, C., Hyams-Kaphzan, O., Karachle, P.K., Katsanevakis, S., Lipej, L., Mastrototaro, F., Mineur, F., Pancucci-Papadopoulou, M.A., Ramos-Esplà, A., Salas, C., San Martin, G., Sfriso, A., Streftaris, N. and Verlaque, M. (2012) Alien species in the Mediterranean Sea by 2012. A contribution to the application of European Union's Marine Strategy Framework Directive (MSFD). Part 2. Introduction trends and pathways. Mediterranean Marine Science 13, 328352.Google Scholar
Zenetos, A., Gofas, S., Russo, G. and Templado, J. (2004) CIESM Atlas of exotic species in the Mediterranean. Volume 3. Molluscs, Monaco: CIESM Publishers.Google Scholar
Zenetos, A., Gofas, S., Verlaque, M., Çinar, M.E., Garcia Raso, J.E., Bianchi, C.N., Morri, C., Azzurro, E., Bilecenoglu, M., Froglia, C., Siokou, I., Violanti, D., Sfriso, A., San Martin, G., Giangrande, A., Katağan, T., Ballesteros, E., Ramos-Esplà, A., Mastrototaro, F., Ocaña, O., Zingone, A., Gambi, M.C. and Streftaris, N. (2010) Alien species in the Mediterranean Sea by 2010. A contribution to the application of European Union's Marine Strategy Framework Directive (MSFD). Part I. Spatial distribution. Mediterranean Marine Science 11, 381493.Google Scholar
Zenetos, A., Katsanevakis, S., Poursanidis, D., Crocetta, F., Damalas, D., Apostolopoulos, G., Gravili, C., Vardala-Theodorou, E. and Malaquias, M. (2011) Marine alien species in Greek Seas: additions and amendments by 2010. Mediterranean Marine Science 12, 95120.Google Scholar
Zenetos, A., Konstantinou, F. and Konstantinou, G. (2009) Towards homogenization of the Levantine alien biota: additions to the alien molluscan fauna along the Cypriot coast. Marine Biodiversity Records 2, e156. doi: http://dx.doi.org/10.1017/S1755267209990832.Google Scholar
Zenetos, A., Koutsogiannopoulos, D., Ovalis, P. and Poursanidis, D. (2013) The role played by citizen scientists in monitoring marine alien species in Greece. Cahiers de Biologie Marine 54, 419426.Google Scholar
Supplementary material: Image

Crocetta et al. supplementary material

Figure 1

Download Crocetta et al. supplementary material(Image)
Image 412.8 KB
Supplementary material: Image

Crocetta et al. supplementary material

Figure 2

Download Crocetta et al. supplementary material(Image)
Image 437.5 KB
Supplementary material: Image

Crocetta et al. supplementary material

Figure 3

Download Crocetta et al. supplementary material(Image)
Image 601.9 KB
Supplementary material: Image

Crocetta et al. supplementary material

Figure 4

Download Crocetta et al. supplementary material(Image)
Image 1.1 MB
Supplementary material: Image

Crocetta et al. supplementary material

Figure 5

Download Crocetta et al. supplementary material(Image)
Image 625.2 KB
Supplementary material: Image

Crocetta et al. supplementary material

Figure 6

Download Crocetta et al. supplementary material(Image)
Image 613 KB
Supplementary material: File

Crocetta et al. supplementary material

Figure legends

Download Crocetta et al. supplementary material(File)
File 21 KB