Is the trend in new introductions of marine non-indigenous species a reliable criterion for assessing good environmental status? Τhe case study of Greece

Published: Dec 2, 2020
Non-indigenous species biological invasions range expansion pathways monitoring Mediterranean Sea.

This study presents the updated status of marine non-indigenous species (NIS) distribution in Greece and investigates trends in new NIS introductions, at both national and subnational level, during 1970-2017. The overall picture shows an increase in new introductions from the 1970s to 2017. The number of unaided introduced species (mainly Lessepsian immigrants) followed an upward trend in the South Aegean Sea until 2017. Similarly, the number of NIS associated with transport-stowaway (NIS introduced mainly via ballast and boat hulls) followed an upward until 2017 in the South Aegean Sea, but also in the Hellenic Levantine coasts. However, these results are greatly affected by a monitoring bias, which appears to be the main factor influencing the number of new NIS introductions reported from Greece and its subnational areas. This monitoring bias, as well as the continuous influx of Lessepsian NIS into the Aegean Sea, constitutes a challenge for Greece as regards setting exact boundaries for areas with or without Good Environmental Status (GES), based on Descriptor 2, primary criterion C1 (D2C1), of the Marine Strategy Framework Directive (MSFD). Dedicated monitoring of marine NIS should be established and be constant in space, time and across taxonomic groups. Prioritization should be given to hot-spot areas of new NIS introductions, such as ports, aquaculture units and marine protected areas. This should be a prerequisite for applying the primary criterion D2C1 of the MSFD properly, at both national and subnational level. Finally, as regards the implementation of D2C1 of the MSDF and setting exact threshold values, we highlight the need for subregional and regional coordination in the Mediterranean.

Article Details
  • Section
  • Review Article
Download data is not yet available.
Angelidis, A., Polyzoulis, G., 2018. New distributional records of four Indo-Pacific species from Astypalaia Island, south Aegean Sea, Greece. Xenophora Taxonomy, 21, 3-10.
Armon, R.H., Zenetos, A., 2015. Invasive alien species and their indicators. p. 147-173. In: Environmental indicators. Armon, R., Hänninen, O. (Eds). Springer, Dordrecht.
Bariche, M., Al-Mabruk, S., Ateş, M., Büyük, A., Crocetta, F. et al., 2020. New Alien Mediterranean Biodiversity Records (March 2020). Mediterranean Marine Science, 21 (1), 129- 145.
Boon, P.J., Clarke, S.A., Copp, G.H., 2020. Alien species and the EU Water Framework Directive: a comparative assessment of European approaches. Biological Invasions, 22, 1497-1512.
Cavallo, M., Elliot, M., Quintino, V., Touza, J., 2018. Can national management measures achieve good status across international boundaries? - A case study of the Bay of Biscay and Iberian coast sub-region. Ocean and Coastal Management, 160, 93-102.
CBD, 2014. Pathways of introduction of invasive species, their prioritization and management. UNEP/CBD/SBSTTA/ 18/9/Add.1. Secretariat of the Convention on Biological Diversity, Montréal.
Chartosia, N., Anastasiadis, D., Bazairi, H., Crocetta, F., Deidun, A. et al., 2018. New Mediterranean Biodiversity Records (July 2018). Mediterranean Marine Science, 19, 398-415.
Crocetta, F., Gofas, S., Salas, C., Tringali, L.P., Zenetos, A., 2017. Local ecological knowledge versus published literature: a review of non-indigenous Mollusca in Greek marine waters. Aquatic Invasions, 12, 415-434.
Dailianis, T., Akyol, O., Babali, N., Bariche, M., Crocetta, F. et al., 2016. New Mediterranean Biodiversity Records (July 2016). Mediterranean Marine Science, 17, 608-626.
Delliou, A., Antoniadou, C., Almpanakis, K., Tsoukala, E., Chintiroglou, C., 2015. Biodiversity of sublittoral foraminiferan assemblages in the northeast Aegean Sea: preliminary results. p. 569-572. In: 11th Panhellenic Symposium on Oceanography & Fisheries, Mytilene, 13-17 May 2015. HCMR, Greece.
Dimitriadis, C., Fournari-Konstantinidou, I., Di Franco, A., Corsini-Foka, M., 2019. First record of the Red Sea Mantis shrimp Erugosquilla massavensis (Kossmann, 1880) in the Greek Ionian Sea. Acta Adriatica, 60, 187-191.
Dimitriadis, C., Galanidi, M., Zenetos, A., Corsini-Foka, M., Giovos, I. et al., 2020. Updating the occurrences of Pterois miles in the Mediterranean Sea, with considerations on thermal boundaries and future range expansion. Mediterranean Marine Science, 21, 62-69.
Dragičević, B., Anadoli, O., Angel, D., Benabdi, M., Bitar, G. et al., 2019. New Mediterranean Biodiversity Records (December 2019). Mediterranean Marine Science, 20, 645-656.
EC, 2008. European Commission Directive 2008/56/EC of the European Parliament and of the Council of 17 June 2008, establishing a framework for community action in the field of marine environmental policy (Marine Strategy Framework Directive). Official Journal of the European Union L164, 19-40.
EC, 2014. European Commission Regulation (EU) No 1143/2014 of the European Parliament and of the Council on the prevention and management of the introduction and spread of invasive alien species. Official Journal of the European Union L315, 35-55.
EC, 2017a. European Commission Directive (EU) 2017/845 of 17 May 2017 amending Directive 2008/56/EC of the European Parliament and of the Council as regards the indicative lists of elements to be taken into account for the preparation of marine strategies. Official Journal of the European Union L125, 27-33.
EC, 2017b. European Commission Decision (EU) 2017/848 of 17 May 2017 laying down criteria and methodological standards on good environmental status of marine waters and specifications and standardized methods for monitoring and assessment, and repealing Decision 2010/477/
EU. Official Journal of the European Union L125, 43-74. Eurostat, 2018. Top 20 ports handling containers, 2008-2018 (thousand TEUs). explained/index.php?title=File:Top_20_ports_handling_ containers,_2008-2018_(thousand_TEUs).png (Accessed 15 September 2020)
Evagelopoulos, A., Poursanidis, D., Papazisi, E., Gerovasileiou, V., Katsiaras, N. et al., 2015. Records of alien marine species of Indo-Pacific origin at Sigri Bay (Lesvos Island, Northeastern Aegean Sea). Marine Biodiversity Records, 8, e35.
Gerakaris, V., Lardi, P.L., Issaris, Y., 2020. First record of the tropical seagrass species Halophila decipiens Ostenfeld in the Mediterranean Sea. Aquatic Botany, 160, 103151.
Gerovasileiou, V., Akel, E.H.Kh., Akyol, O., Alongi, G., Azevedo, F. et al., 2017. New Mediterranean Biodiversity Records (July, 2017). Mediterranean Marine Science, 18, 179-207.
Giovos, I., Bernardi, G., Romanidis-Kyriakidis, G., Marmara, D., Kleitou, P., 2018. First records of the fish Abudefduf sexfasciatus (Lacepède, 1801) and Acanthurus sohal (Forsskål, 1775) in the Mediterranean Sea. BioInvasions Records, 7, 205-210.
Giovos, I., Kleitou, P., Poursanidis, D., Batjakas, I., Bernardi, G. et al., 2019. Citizen-science for monitoring marine invasions and stimulating public engagement: a case project from the eastern Mediterranean. Biological Invasions, 21, 3707-3721.
Giovos, I., Tiralongo, F., Langeneck, J., Kaminas, A., Kleitou, P. et al., 2020. First record of the Atlantic spadefish Chaetodipterus faber (Broussonet, 1782) in the Mediterranean Sea: is it a new aquarium release? Bioinvasions Records, 9, 89-95.
Gkargkavouzi, A., Halkos, G., Matsiori, S., 2019. Assessing values, attitudes and threats towards marine biodiversity in a Greek coastal port city and their interrelationships. Ocean and Coastal Management, 167, 115-126.
Gómez, F., 2019. Comments on the non-indigenous microalgae in the European seas. Marine Pollution Bulletin, 148, 1-2. HELCOM, 2018. Trends in arrival of new non-indigenous species HELCOM core indicator 2018. HELCOM core indicator report. Available at: holistic-assessments/state-of-the-baltic-sea-2018/ reports-and-materials
Katsanevakis, S., Poursanidis, D., Hoffman, R., Rizgalla, J., Rothman, S.B-S. et al., 2020 Unpublished Mediterranean records of marine alien and cryptogenic species. Bioinvasions Records, 9, 165-182.
Katsanevakis, S., Zenetos, A., Belchior, C., Cardoso, A.C., 2013. Invading European Seas: Assessing pathways of introduction of marine aliens. Ocean and Coastal Management, 76, 64-74.
Kondylatos, G., Corsini-Foka, M., 2017. Penaeus hathor (Burkenroad, 1959) (Crustacea: Decapoda: Penaeidae) in Rhodian waters (Aegean Sea). Cahier de Biologie Marine, 58, 491-495.
Kondylatos, G., Corsini-Foka, M., Perakis, E., 2018. First record of the isopod Idotea hectica (Pallas, 1772) (Idoteidae) and of the brachyuran crab Matuta victor (Fabricius, 1781) (Matutidae) in the Hellenic waters. Mediterranean Marine Science, 19, 656-661.
Kondylatos, G., Kampouris, T., Kouloumperis, V., Foka, M.C., 2017. The Indo-Pacific brachyuran Charybdis (Gonioinfradens) paucidentatus (A. Milne-Edwards, 1861) (Brachyura, Portunidae) in the Cyclades, Aegean Sea. Turkish Journal of Zoology, 41, 1118-1120.
Kousteni, V., Bakiu, R., Benhmida, A., Crocetta, F., Di Martino, V. et al., 2019. New Mediterranean Biodiversity Records (April, 2019). Mediterranean Marine Science, 20, 230-247.
Küpper, F.C., Tsiamis, K., Johansson, N.R., Peters, A.F., Salomidi, M. et al., 2019. New records of the rare deep-water alga Sebdenia monnardiana (Rhodophyta) and the alien Dictyota cyanoloma (Phaeophyceae) and the unresolved case of deep-water kelp in the Ionian and Aegean Seas (Greece). Botanica Marina, 62, 577-586.
Langeneck, J., Lezzi, M., Del Pasqua, M., Luigi, M., Gambi, M.C. et al., 2020. Non-indigenous polychaetes along the coasts of Italy: a critical review. Mediterranean Marine Science, 21, 238-275.
Lipej, L., Acevedo, I., Akel, E.H.K., Anastasopoulou, A., Angelidis, A. et al., 2017. New Mediterranean Biodiversity Records (March 2017) Mediterranean Marine Science, 18, 179-201.
Manousis, T., Kontadakis, C., Mpazios, C., Galinou-Mitsoudi, S., 2020. New records of Cimidae, Murchisonellidae and Pyramidellidae (Mollusca: Gastropoda: Heterobranchia) for the Mediterranean Sea and the Hellenic Waters. Xenophora Taxonomy, 28, 3-27.
Manousis, T., Kontadakis, C., Polyzoulis, G., Mbazios, G., Galinou- Mitsoudi, S., 2018. New marine gastropod records for the Hellenic waters. Journal of Biological Research-Thessaloniki, 25, 6.
Micali, P., Siragusa, F., Agamennone, F., Germanà, A., Sbrana, C., 2017. Karpathos Island (Greece) and its Indo-Pacific alien species. Part 1. Bolletino Malacologico, 53, 40-49.
Ministry of Environment and Energy (MinEnv), Greece (2012) Technical report for the preparation stage of action plan for marine strategies in Greece, for the implementation of marine strategy framework Directive 2008/56/EC.
APC Advanced planning-consulting SA. University of the Aegean – OSPAR, 2018. CEMP Guideline: Common Indicator - Changes to non-indigenous species communities (NIS3). Paris, Agreement 2018-04e, 8 pp.
Palialexis, A., Cardoso, A.C., Tsiamis, K., Alemany, F. et al., 2015. Report of the JRC’s Descriptor 2 workshop in support to the review of the Commission Decision 2010/477/ EU concerning MSFD criteria for assessing Good Environmental Status for NIS. EUR 27714; doi:10.2788/486618.
Pirkenseer, C.M., 2020. Alien species in southern Laconia, Kythira Island and southern Messenia (Greece): new and additional records and updated record maps. Journal of the Black Sea/Mediterranean Environment, 26, 145-175.
Ragkousis, M., Abdelali, N., Azzurro, E., Badreddine, A., Bariche M. et al., 2020. New Alien Mediterranean Biodiversity Records (October 2020). Mediterranean Marine Science, 21, 631-652.
Rohde, S., Schupp, P.J., Markert, A., Wehrmann, A., 2017. Only half of the truth: Managing invasive alien species by rapid assessment. Ocean and Coastal Management, 146, 26-35.
Sparrow, A., Badalamenti, F., Pipitone, C., 2001. Contribution to the knowledge of Percnon gibbesi (Decapoda, Grapsidae), an exotic species spreading rapidly in Sicilian waters. Crustaceana, 74(10), 1009-1017.
Stamouli, C., Akel, E.H.Kh., Azzurro, E., Bakiu, R., Bas, A.A. et al., 2017. New Mediterranean Biodiversity Records (December 2017). Mediterranean Marine Science, 18, 534- 556.
Stefani, F., Aquaro, G., Azzurro, E., Colorni, A., Galli, P., 2012. Patterns of genetic variation of a Lessepsian parasite. Biological Invasions, 14, 1725-1736.
Steger, J., Stockinger, M., Ivkić, A., Galil, B.S., Albano, P.G., 2018. New records of non-indigenous molluscs from the eastern Mediterranean Sea. BioInvasions Records, 7, 245- 257.
Stulpinaite, R, Hyams-Kaphzan, O., Langer M.R., 2020. Alien and cryptogenic Foraminifera in the Mediterranean Sea: A revision of taxa as part of the EU 2020 Marine Strategy Framework Directive. Mediterranean Marine Science, 21 (3), 719-758.
Thessalou-Legaki, M., Zenetos, A., Kambouroglou, V., Corsini- Foka, M., Kouraklis, P. et al., 2006. The establishment of the invasive crab Percnon gibbesi (H. Milne Edwards, 1853) (Crustacea: Decapoda: Grapsidae) in Greek waters. Aquatic Invasions, 1 (3), 133-136.
Tsiamis, K., Palialexis, A., Stefanova, K. Ničević Gladan, Z., Skejić, S. et al., 2019. Non-indigenous species refined national baseline inventories: a synthesis in the context of the European Union’s Marine Strategy Framework Directive. Marine Pollution Bulletin, 145, 429-435.
Ulman, A., 2018. Recreational boating as a vector of spread of alien species around the Mediterranean. PhD thesis. University of Pavia (Italy) and Université Pierre et Marie Curie (UPMC, France).
Ulman, A., Ferrario, J., Occhpinti-Ambrogi, A., Arvanitidis, Ch., Bandi, A. et al., 2017. A massive update of non-indigenous species records in Mediterranean marinas. Peer J, 5, e3954.
Yokeş, M., Andreou, V., Bakiu, R., Bonanomi, S., Camps, J. et al., 2018. New Mediterranean Biodiversity Records (November 2018). Mediterranean Marine Science, 19, 673-689.
Zenetos, A., 2019. Mediterranean Sea: 30 Years of Biological Invasions (1988-2017). p. 13-19. In: Proceedings of the 1st Mediterranean Symposium on the Non-Indigenous Species, 18 January 2019, Antalya, Turkey. Langar, H., Ouerghi, A. (Eds). SPA/RAC, Tunis.
Zenetos, A., Miliou, A., 2020. Abudefduf cf. saxatilis in Saronikos Gulf. Unaided introduction or human aided transfer? Annales, Series Historia Naturalis, in press.
Zenetos, A., Apostolopoulos, G., Crocetta, F., 2016. Aquaria kept marine fish species possibly released in the Mediterranean Sea: First confirmation of intentional release in the wild. Acta Ichthyologica et Piscatoria, 46, 255-262.
Zenetos, A., Arianoutsou, M., Bazos, I., Balopoulou, S., Corsini- Foka, M. et al., 2015. ELNAIS: A collaborative network on Aquatic Alien Species in Hellas (Greece). Management of Biological Invasions, 6, 185-196.
Zenetos, A., Corsini-Foka, M., Crocetta, F., Gerovasileiou, V., Karachle, P.K. et al., 2018. Deep cleaning of alien species records in the Greek Seas (2018 update). Management of Biological Invasions, 9, 209-226.
Zenetos, A., Gratsia, E., Cardoso, A.C., Tsiamis, K., 2019. Time lags in reporting of biological invasions: the case of Mediterranean Sea. Mediterranean Marine Science, 20, 469-475.
Zenetos, A., Ovalis, P., Giakoumi, S., Kontadakis, C., Lefkaditou, E. et al., 2020. Saronikos Gulf: a hotspot area for alien species in the Mediterranean Sea. BioInvasions Records 9 (4), 873-889.
Most read articles by the same author(s)