Tracing the westward front: molecular and morphological evidence of the expansion of the non-native oyster Dendostrea cf. crenulifera (Ostreidae) in the Mediterranean Sea

Daniele Salvi; Matteo Garzia; Salvatore Giacobbe; Marina Morabito; Nathan Delcour; Giulia Furfaro; Paolo Mariottini; Paolo G.  Albano

doi:10.3989/scimar.05730.122

Authors

Daniele Salvi Department of Health, Life & Environmental Sciences, University of L’Aquila https://orcid.org/0000-0002-3804-2690
Matteo Garzia Department of Health, Life & Environmental Sciences, University of L’Aquila https://orcid.org/0000-0002-0918-9925
Salvatore Giacobbe CNR-IRBIM https://orcid.org/0000-0002-4619-4862
Marina Morabito Department Chemical, Biological, Pharmaceutical and Environmental Sciences, University of Messina https://orcid.org/0000-0002-0224-2113
Nathan Delcour Department of Health, Life & Environmental Sciences, University of L’Aquila https://orcid.org/0000-0001-8203-9301
Giulia Furfaro Department of Biological and Environmental Sciences and Technologies - DiSTeBA, University of Salento https://orcid.org/0000-0001-8184-2266
Paolo Mariottini Department of Science, University of “Roma Tre” https://orcid.org/0000-0003-1044-7108
Paolo G. Albano Department of Marine Animal Conservation and Public Engagement, Stazione Zoologica Anton Dohrn https://orcid.org/0000-0001-9876-1024

DOI:

https://doi.org/10.3989/scimar.05730.122

Keywords:

Mediterranean Sea, Biological invasions, Ostreidae, Dendostrea cf. crenulifera, Molecular identification, Range expansion, Vessel-mediated transport, cox1

Abstract

The Mediterranean Sea is a major hotspot of non-indigenous species, many of which arrive through the Suez Canal and spread via vessel-mediated transport. Among them, the tropical oyster Dendostrea cf. crenulifera has long been affected by taxonomic uncertainty. By integrating morphological characters with mitochondrial cox1 sequences from 38 specimens collected in nine localities of Greece, Croatia and Italy, we provide the first molecularly validated evidence of its occurrence outside the Levantine basin. New records from the Aegean Sea, Libyan Sea, Ionian Sea, Adriatic Sea and southern Tyrrhenian Sea extend the known range by more than 1000 km westwards. Specimens from Crete were found on natural rocky substrates, whereas those from all western localities occurred exclusively on artificial structures in harbours and marinas, supporting hull fouling as the primary vector of spread. The ability of this tropical oyster to establish in environmentally diverse basins, including areas where native oysters occur, suggests the potential for spatial overlap and competitive interactions. The early detection of this range expansion offers opportunities for monitoring and for the assessment of its ecological implications.

Downloads

Download data is not yet available.

References

Albano P.G., Steger J., Bakker P.A.J., et al. 2021a. Numerous new records of tropical non-indigenous species in the Eastern Mediterranean highlight the challenges of their recognition and identification. ZooKeys 1010: 1–95.

Albano P.G., Steger J., Bošnjak M., et al. 2021b. Native biodiversity collapse in the eastern Mediterranean. Proc. Biol. Sci. 288: 1–9.

Albano P.G., Hong Y., Steger J., et al. 2024a. New records of non-indigenous species from the eastern Mediterranean Sea (Crustacea, Mollusca), with a revision of genus Isognomon (Mollusca: Bivalvia). PeerJ 12: e17425.

Albano P.G., Schultz L., Wessely J., et al. 2024b. The dawn of the tropical Atlantic invasion into the Mediterranean Sea. Proc. Natl. Acad. Sci. 121: e2320687121.

Azzola A., Furfaro G., Trainito E., et al. 2022. Seawater warming favours the northward range expansion of Lessepsian species in the Mediterranean Sea: the cephalaspidean Lamprohaminoea ovalis. J. Mar. Biol. Assoc. U.K. 102: 167–173.

Azzurro E., Ben Soussi J., Andaloro F. 2013. The yellowstripe barracuda Sphyraena chrysotaenia reaches the central Mediterranean: a new record from Lampedusa Island. Mar. Biodivers. Rec. 6.

Azzurro E., D’Amen M. 2022. Climate change paves the way for a new inter-ocean fish interchange. Front. Ecol. Environ. 20: 558–563.

Battiata M., Curatolo T., Naser M.D., et al. 2024. The State of the Art of the Global Distribution of the Invasive Mytilid Species Brachidontes pharaonis (P. Fischer, 1870). Diversity 16: 381.

Bottacini D., Pollux B.J.A., Nijland R., et al. 2024. Lionfish (Pterois miles) in the Mediterranean Sea: a review of the available knowledge with an update on the invasion front. NeoBiota 92: 233–257.

Çeviker D. 1999. Lessepsians from Indian Ocean and the Red Sea. Sualtı Dünyasi 45: 22–27.

Çeviker D. 2001. Recent immigrant bivalves in the northeastern Mediterranean off Iskenderun. La Conchiglia. 298: 39–46

Coll M., Piroddi C., Steenbeek J., et al. 2010. The Biodiversity of the Mediterranean Sea: Estimates, Patterns, and Threats. PLOS ONE 5: e11842.

Coutts A.D.M., Taylor, M.D. 2004. A preliminary investigation of biosecurity risks associated with biofouling on merchant vessels in New Zealand. N. Z. J. Mar. Freshw. Res. 38: 215–229.

Crocetta F., Mariottini P., Salvi D., et al. 2015. Does GenBank provide a reliable DNA barcode reference to identify small alien oysters invading the Mediterranean Sea? J. Mar. Biol. Assoc. U. K. 95: 111–122.

Daly-Yahia M.N. Daly-Yahia O.K., Gueroun S.K.M., et al. 2013. The invasive tropical scyphozoan Rhopilema nomadica Galil, 1990 reaches the Tunisian coast of the Mediterranean Sea. BioInvasions Rec. 2: 319–323.

Davidson I., Zabin C., Chang A., et al. 2010. Recreational boats as potential vectors of marine organisms at an invasion hotspot. Aquat. Biol. 11: 179–191.

Delcour N., Garzia M., Oliver P.G., et al. 2025. High genetic diversity and lack of structure underlie the invasion history of the non-indigenous oyster Dendostrea cf. crenulifera (Mollusca, Ostreida, Ostreidae) spreading in the eastern Mediterranean Sea. NeoBiota 101: 277–302.

Doyle J.J., Doyle J.L. 1987. A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem. Bull. 19: 11-15.

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

Furfaro G., Fumarola L.M., Toso A., et al. 2025. A Mediterranean melting pot: native and non-indigenous sea slugs (Gastropoda, Heterobranchia) from Lebanese waters. BioInvasions Rec. 14. 197-221.

Galil B.S. 2007. Loss or gain? Invasive aliens and biodiversity in the Mediterranean Sea. Mar. Pollut. Bull., Marine Bioinvasions: A collection of reviews 55: 314–322.

Garzia M., Doneddu M., Giacobbe S., et al. 2024. Molecular and morphological data provide evidence for only one alien species of pearl oyster in the Mediterranean Sea. Sci. Mar. 88: e085–e085.

Golani D. 2010. Colonization of the Mediterranean by Red Sea fishes via the Suez Canal - Lessepsian migration. In: Golani D., B. Appelbaum-Golani (eds). Fish Invasions in the Mediterranean Sea: Change Renew. Pensoft, Sofia, pp. 145–188.

Johnson M., Zaretskaya I., Raytselis Y., et al. 2008. NCBI BLAST: a better web interface. Nucleic Acids Res. 36: W5-9. https://doi.org/10.1093/nar/gkn201

Lam K., 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: 1–13.

Liu J., Li Q., Kong L., et al. 2011. Identifying the true oysters (Bivalvia: Ostreidae) with mitochondrial phylogeny and distance-based DNA barcoding. Mol. Ecol. Resour. 11: 820–830.

Lockwood J.L., Hoopes M.F., Marchetti M.P. 2013. Invasion ecology. WileyBlackwell, Chichester, 456 pp.

Miladi R. 2018. DNA barcoding identification of the macroalgal flora of Tunisia.

Oliver P.G., Garzia M., Paulay G., et al. 2025. On the species identity of a tropical oyster (Bivalvia, Ostreidae, Dendostrea) invading the eastern Mediterranean Sea. ZooKeys 1243: 207–224.

Peleg O., Guy-Haim T., Yeruham E., et al. 2020. Tropicalization may invert trophic state and carbon budget of shallow temperate rocky reefs. J. Ecol. 108: 844–854.

Piazzi L., Cinelli F. 2003. Evaluation of benthic macroalgal invasion in a harbour area of the western Mediterranean Sea. Eur. J. Phycol. 38: 223-231.

Png-Gonzalez L., Aguilo-Arce J., Vázquez-Luis M., et al. 2021. New occurrence of Pinctada imbricata radiata (Leach, 1814) in the Balearic Archipelago (NW Mediterranean Sea). BioInvasions Rec. 10: 853–858.

Por F.D. 1978. Lessepsian migration: the influx of Red Sea biota into the Mediterranean by way of the Suez Canal. Springer-Verlag, Berlin, Heidelberg, New York, 228 pp.

QGIS Development Team 2022. QGIS Geographic Information System. QGIS Association.

Rilov G. 2016. Multi-species collapses at the warm edge of a warming sea. Sci. Rep. 6: 36897.

Salvi D., Mariottini P. 2017. Molecular taxonomy in 2D: A novel ITS2 rRNA sequence structure approach guides the description of the oysters’ subfamily Saccostreinae and the genus Magallana (Bivalvia: Ostreidae). Zool. J. Linn. Soc. 179: 263–276.

Salvi D., Mariottini P. 2021. Revision shock in Pacific oysters taxonomy: the genus Magallana (formerly Crassostrea in part) is well-founded and necessary. Zool. J. Linn. Soc. 192: 43–58.

Salvi D., Bellavia G., Cervelli M., et al. 2010. The analysis of rRNA sequence-structure in phylogenetics: An application to the family Pectinidae (Mollusca: Bivalvia). Mol. Phylogenet. Evol. 56: 1059–1067.

Salvi D., Macali A., Mariottini P. 2014. Molecular phylogenetics and systematics of the bivalve family Ostreidae based on rRNA sequence-structure models and multilocus species tree. PLOS ONE 9: e108696.

Salvi D., Al-Kandari M., Oliver P.G., et al. 2022. Cryptic Marine Diversity in the Northern Arabian Gulf: An integrative approach uncovers a new species of oyster (Bivalvia: Ostreidae), Ostrea oleomargarita. J. Zool. Syst. Evol. Res. 2022: e7058975.

Sambrook J., Fritsch E.F., Maniatis T., et al. 1989. Molecular cloning: a laboratory manual. Cold spring harbor laboratory press. Cold Spring Harbor, New York.

Steger J., Bogi C., Lubinevsky H., et al. 2024. Ecological baselines in the Eastern Mediterranean Sea shifted long before the availability of observational time series. Glob. Change Biol. 30: e17272.

Toso A., Solca M., Trainito E., et al. 2025. Arrivals and departures: exploring sea slug diversity (Mollusca, Gastropoda) in the Salento Peninsula harbours. Mar. Biodivers. 55: 80.

Ulman A., Ferrario J., Occhpinti-Ambrogi A., et al. 2017. A massive update of non-indigenous species records in Mediterranean marinas. PeerJ 5: e3954.

Ulman A., Ferrario J., Forcada A., et al. 2019. Alien species spreading via biofouling on recreational vessels in the Mediterranean Sea. J. Appl. Ecol. 56: 2620–2629.

Winters G., Beer S., Willette D.A., et al. 2020. The Tropical Seagrass Halophila stipulacea: Reviewing What We Know From Its Native and Invasive Habitats, Alongside Identifying Knowledge Gaps. Front. Mar. Sci. 7: 300.

Zenetos A., Gofas S., Verlaque M., 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. Mediterr. Mar. Sci. 11: 381–381.

Zenetos A., Albano P.G., Garcia E.L., et al. 2022a. Established non-indigenous species increased by 40% in 11 years in the Mediterranean Sea. Mediterr. Mar. Sci. 23(1): 196-212.

Zenetos A., Tsiamis K., Galanidi M., et al. 2022b. Status and Trends in the Rate of Introduction of Marine Non-Indigenous Species in European Seas. Diversity 14: 1077.