Spread of the non-indigenous ascidian Aplidium accarense (Millar, 1953) in the Eastern Mediterranean Sea: morphological and molecular tools for an accurate identification


Published: Mar 8, 2021
Keywords:
Ascidiacea NIS Mediterranean Sea COI integrative taxonomy.
FEDERICA MONTESANTO
https://orcid.org/0000-0001-6328-7596
GIOVANNI CHIMIENTI
https://orcid.org/0000-0002-4890-2949
CARMELA GISSI
https://orcid.org/0000-0002-2269-079X
FRANCESCO MASTROTOTARO
https://orcid.org/0000-0002-4890-2949
Abstract

The aplousobranch ascidian Aplidium accarense (Millar, 1953) was first described on the western coast of Africa, where it is considered native. Afterwards, this species was introduced along south-American Atlantic coasts, where it affected local shellfish farms through a massive colonization of both natural and artificial substrata. Aplidium accarense has been recently reported along Catalan coasts and in the Tyrrhenian Seas (Western Mediterranean) where it represents a non-indigenous species, only recorded in harbours and aquaculture farms thus far. These Mediterranean records support the hypothesis that A. accarense is currently expanding within the basin, representing a potential invasive species. In this study, several colonies of A. accarense were found for the first time on artificial substrata within the semi-enclosed basin of the Mar Piccolo of Taranto (Italy, Ionian Sea), in the Eastern Mediterranean. Here we provide an updated description of A. accarense combining both morphological and molecular approaches, in order to allow an accurate and reliable identification of this expanding species. Comparing the morphology of the specimens collected from Taranto with the previous descriptions, a slight intra-specific variability has been noticed. Therefore, we provide detailed comparisons of the specimens found in Taranto with all the other A. accarense sampled in other areas of the world, in order to highlight the intra-species variability. The correct identification of a potentially-dangerous species such as A. accarense, represents a needed step for environmental monitoring purposes and for implementing management strategies to mitigate the effects of non-indigenous species on natural ecosystems and human activities.

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Adams, C.M., Shumway, S.E., Whitlatch, R.B., Getchis, T., 2011. Biofouling in marine molluscan shellfish aquaculture: a survey assessing the business and economic implications of mitigation. Journal of the World Aquaculture Society, 42 (2), 242-252.
Altschul, S.F., Gish, W., Miller, W., Myers, E.W., Lipman, D.J., 1990. Basic local alignment search tool. Journal of Molecular Biology, 215 (3), 403-10.
Bouzon, J.L., Brandini, F.P., Rocha, R.M., 2012. Biodiversity of sessile fauna on rocky shores of coastal islands in Santa Catarina, Southern Brazil. Marine Science, 2 (5), 39-47.
Bracchi, V.A., Marchese, F., Savini, A., Chimienti, G., Mastrototaro, F. et al., 2016. Seafloor integrity of the Mar Piccolo Basin (Southern Italy): quantifying anthropogenic impact. Journal of Maps, 12, 1-11.
Brunetti, R., Manni, L., Mastrototaro, F., Gissi, C., Gasparini, F., 2017. Fixation, description and DNA barcode of a neotype for Botryllus schlosseri (Pallas, 1766) (Tunicata, Ascidiacea). Zootaxa, 4353 (1), 29-50.
Brunetti, R., Mastrototaro, F., 2017. Ascidiacea of the European Waters. Edagricole - New Business Media II, Milano, 447 pp.
Carman, M.R., Grunden, D.W., 2010. First occurrence of the invasive tunicate Didemnum vexillum in eelgrass habitat. Aquatic Invasions, 5 (1), 23-29.
Casso, M., Navarro, M., Ordóñez, V., Fernández-Tejedor, M., Pascual, M., et al., 2018. Seasonal patterns of settlement and growth of introduced and native ascidians in bivalve cultures in the Ebro Delta (NE Iberian Peninsula). Regional Studies in Marine Science, 23, 12-22.
Fletcher, C.S., Westcott, D.A., 2013. Dispersal and the design of effective management strategies for plant invasions: matching scales for success. Ecological Applications, 23 (8), 1881-1892.
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. Molecular Marine Biology and Biotechnology, 3 (5), 294-299.
Gravili, C., Belmonte, G., Cecere, E., Denitto, F., Giangrande, A. et al., 2010. Non-indigenous species (NIS) along the Apulian coast, Italy. Chemistry & Ecology, 26 (S1), 121-142.
Guerra-Castro, E., Cruz-Motta, J.J., Conde, J.E. 2011. Cuantificación de la diversidad de especies incrustantes asociadas a las raíces de Rhizophora mangle L. en el Parque Nacional Laguna de la Restinga. Interciencia, 36 (12), 923-930.
Hirose, M., Hirose, E., 2009. DNA barcoding in photosymbiotic species of Diplosoma (Ascidiacea: Didemnidae), with the description of a new species from the southern Ryukyus, Japan. Zoological Science, 26 (8), 564-8.
Hulme, P.E., 2006. Beyond control: wider implications for the management of biological invasions. Journal of Applied Ecology, 43 (5), 835-847.
Hulme, P.E., Bacher, S., Kenis, M., Klotz, S., Kühn, I. et al., 2008. Grasping at the routes of biological invasions: a framework for integrating pathways into policy. Journal of Applied Ecology, 45 (2), 403-414.
Izquierdo-Muñoz, A., Diaz Valdes, M., Ramos-Esplà, A.A., 2009. Recent non-indigenous ascidians in the Mediterranean Sea. Aquatic Invasions, 4, 59-64.
Kearse, M., Moir, R., Wilson, A., Stones-Havas, S., Cheung, M. et al., 2012. Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics, 28 (12), 1647-9.
Lambert, G., 2002. Non-indigenous ascidians in tropical waters. Pacific Science, 56 (3), 291-298.
Lambert, G., 2007. Invasive sea squirts:a growing global problem. Journal of Experimental Marine Biology and Ecology, 342 (1), 3-4.
Longo, C., Mastrototaro, F., Corriero, G., 2007. Occurrence of Paraleucilla magna (Porifera: Calcarea) in the Mediterranean Sea. Journal of the Marine Biological Association of the United Kingdom, 87 (6), 1749-1756.
López-Legentil, S., Legentil, M.L., Erwin, P.M., Turon, X., 2015. Harbor networks as introduction gateways: contrasting distribution patterns of native and introduced ascidians. Biological Invasions, 17(6), 1623-1638.
Marchini, A., Ferrario, J., Occhipinti-Ambrogi, A., 2013. Recent additions to the alien marine biota along Italian coasts. Rapport Commission Internationale Mer Méditeranée, 40, 887.
Mastrototaro, F., Matarrese, A., D’Onghia, G., 2003. Occurrence of Musculista senhousia (Mollusca: Bivalvia) in the Taranto seas (eastern-central Mediterranean Sea). Journal of Marine Biology Association of the United Kingdom, 83 (6), 1279-1280.
Mastrototaro, F., Brunetti, R., 2006. The non-indigenous ascidian Distaplia bermudensis in the Mediterranean: comparison with the native species Distaplia magnilarva and Distaplia lucillae sp. nov. Journal of the Marine Biological Association of the United Kingdom, 86 (1), 181-185.
Mastrototaro, F., Chimienti, G., Matarrese, A., Gambi, M.C., Giangrande, A., 2015. Growth and population dynamics of the non-indigenous species Branchiomma luctuosum Grube (Annelida, Sabellidae) in the Ionian Sea (Mediterranean Sea). Marine Ecology, 36 (3), 517-529.
Mastrototaro, F., Montesanto, F., Salonna, M., Grieco, F., Trainito, E. et al., 2019. Hitch-hikers of the sea: concurrent morphological and molecular identification of Symplegma brakenhielmi (Tunicata: Ascidiacea) in the western Mediterranean Sea. Mediterranean Marine Science, 20 (1), 197-207.
Mastrototaro, F., Montesanto, F., Salonna, M., Viard, F., Chimienti, G. et al., 2020. An integrative taxonomic frame work for the study of the genus Ciona (Ascidiacea) and description of a new species, Ciona intermedia. Zoological Journal of the Linnean Society, 190 (4), 1193-1216.
Millar, R.H., 1953. On a collection of ascidians from the Gold Coast. In: Proceedings of the Zoological Society of London. Blackwell Publishing Ltd, UK, Oxford.
Monniot, C., Monniot, F., 1967. Campagne de la Calypso aux iles du Cap Vert (1959). Tuniciers benthiques. In : Annales del’Institut Océanographique, France, Paris.
Monniot, F., 1969. Sur une collection d’Ascidies composées de Dakar. Bulletin du Muséum National D’Histoire Naturelle, 41 (2), 426-457.
Monniot, F., Dettai, A., Eleaume, M., Cruaud, C., Ameziane, N., 2011. Antarctic Ascidians (Tunicata) of the French-Australian survey CEAMARC in Terre Adélie. Zootaxa, 2817 (1), 1-54.
Occhipinti-Ambrogi, A., Marchini, A., Cantone, G., Castelli, A., Chimenz, C. et al., 2011. Alien species along the Italian coasts: an overview. Biological Invasions, 13 (1), 215-237.
Ojaveer, H., Galil, B.S., Minchin, D., Olenin, S., Amorim, A. et al., 2014. Ten recommendations for advancing the assessment and management of non-indigenous species in marine ecosystems. Marine Policy, 44, 160-165.
Rocha, R.M., Bonnet, N.Y., 2009. Ascídias (Tunicata, Ascidiacea) introduzidas no Arquipélago de Alcatrazes, São Paulo. Iheringia Series Zoologie, 99 (1), 27-35.
Rocha, R.M., Moreno, T.R., Metri, R., 2005. Ascídias (Tunicata, Ascidiacea) da Reserva Biológica Marinha do Arvoredo, Santa Catarina, Brasil Ascidians (Tunicata, Ascidiacea) from the Arvoredo Marine Biological Reserve, Santa Catarina, Brazil. Revista Brasileira de Zoologia, 22 (2), 461-476.
Rocha, R.M., Kremer, L.P., Baptista, M.S., Metri, R., 2009. Bivalve cultures provide habitat for exotic tunicates in southern Brazil. Aquatic Invasions, 4 (1), 195-205.
Rocha, R.M., Guerra-Castro, E., Lira, C., Pauls, S.M., Hernández, I. et al., 2010. Inventory of ascidians (Tunicata, Ascidiacea) from the National Park La Restinga, Isla Margarita, Venezuela. Biota Neotropica, 10 (1), 209-218.
Rocha, R.M., Salonna, M., Griggio, F., Ekins, M., Lambert, G. et al., 2019. The power of combined molecular and morphological analyses for the genus Botrylloides: identification of a potentially global invasive ascidian and description of a new species. Systematics and Biodiversity, 17 (5), 509-526.
Rodrigues, S.A., Rocha, R.M., Lotufo, T.M.C., 1998. Guia ilustrado para identificação das ascídias do Estado de São Paulo. FAPESP, São Paulo, 190 pp. Roman, J., 2006. Diluting the founder effect: cryptic invasions expand a marine invader’s range. Proceedings of the Royal Society B: Biological Sciences, 273 (1600), 2453-2459.
Salonna, M., Gasparini, F., Huchon, D., Montesanto, F., Haddas- Sasson, M. et al., 2021. An elongated COI fragment to discriminate botryllid species and as an improved ascidian DNA barcode. Scientific reports, 11 (1), 1-19.
Servello, G., Andaloro, F., Azzurro, E., Castriota, L., Catra, M. et al., 2019. Marine alien species in Italy: a contribution to the implementation of descriptor D2 of the Marine Strategy Framework Directive. Mediterranean Marine Science, 20 (1), 1-48.
Schlick-Steiner, B.C., Seifert, B., Stauffer, C., Christian, E., Crozier, R.H., Steiner, F.M., 2007. Without morphology, cryptic species stay in taxonomic crypsis following discovery. Trends in Ecology & Evolution, 22 (8), 391-392.
Tursi, A., Corbelli, V., Cirpiano, G., Capasso, G., Velardo, R. et al., 2018. Mega-litter and remediation: the case of Mar Piccolo of Taranto (Ionian Sea). Rendiconti Lincei. Scienze Fisiche e Naturali, 29 (4), 817-824.
Vandepas, L.E., Oliveira, L.M., Lee, S.S., Hirose, E., Rocha, R.M., et al., 2015. Biogeography of Phallusia nigra: is it really black and white? The Biological Bulletin, 228 (1), 52-64.
Zenetos, A., Gofas, S., Verlaque, M., Çinar, M., Garcia Raso, J. et al., 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 (2), 381-493.
Zenetos, A., Çinar, M.E., Crocetta, F., Golani, D., Rosso, A. et al., 2017. Uncertainties and validation of alien species catalogues: The Mediterranean as an example. Estuarine, Coastal and Shelf Science, 191, 171-187.
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