AN İNVENTORY OF NON-İNDİGENOUS SPECİES (NIS) İNSİDE AND OUTSİDE THREE TOURİST MARİNAS FROM THE SOUTHERN MEDİTERRANEAN COAST
04/01/2019An inventory of non-indigenous species (NIS) inside and outside three tourist marinas from the southern Mediterranean coast
Yassine Ramzi Sghaier, Rym Zakhama-Sraieb, Ahmed Ben Hmida, Faouzia Charfi
Laboratory of Diversity, Management and Conservation of Biological Systems, Faculty of Sciences of Tunis, University of Tunis El Manar, LR18ES06, Tunis, TUNISIA
Regional Activity Centre for Specially Protected Areas (RAC/SPA), Boulevard du Leader Yasser Arafat, BP 337, 1080 Tunis Cedex, TUNISIA
University of Manouba, High Institute of Biotechnology of Sidi Thabet, BiotechPôle, BP-66, 2020 Sidi Thabet, Ariana, TUNISIA
Abstract
In December 2013, three marinas in the southern Mediterranean coasts, El Kantaoui and Cap Monastir in the central east coast of Tunisia and Marina El Alamein in the central coast of Egypt, were surveyed for the presence of non-indigenous species (NIS). In order to maximize the number of collected species and to sample the full range of biotic assemblages and microhabitats inside and outside the marinas, diverse survey methods were employed. These include rapid assessment surveys of epibiota on artificial structures in harbors, with standardized one-hour transects used for snorkeling and diving to observe infra-littoral species and traps for catching small crabs and shrimps. Other data were obtained from the catch composition of coastal fishing boats operating in the area. A total of 26 NIS originating from Indo-Pacific Ocean/Red Sea were identified as 6 macrophyte, 11 invertebrate and 9 fish species. The results highlight the role of marinas in the introduction of NIS into the Mediterranean. Further and regular surveys in risk areas are recommended to provide an effective early warning system for NIS.
Keywords: Biofouling, non-indigenous species, marina, Tunisia, Egypt, Mediterranean Sea
References
Antit, M., Gofas, S., Salas, C., Azzouna, A. (2011) One hundred years after Pinctada: an update on alien Mollusca in Tunisia. Medit Mar Sci 12(1): 53-73.
Balls, H. (1936) Decapoda. Part VII. The fisheries grounds near Alexandria. Fisheries Research Directorate Notes and Memoirs (Cairo) 15:1-67.
Bazairi, H., Sghaier, Y.R., Benamer, I., Langar, H., Pergent, G., Bourass, E.M., Verlaque, M., Ben Soussi, J., Zenetos, A. (2013) Alien marine species of Libya: first inventory and new records in El-Kouf National Park (Cyrenaica) and the neighbouring areas. Medit Mar Sci 14(2): 451-462.
Bitar, G., Kouli-Bitar, S. (2001) Nouvelles données sur la faune et la flore benthiques de la côte Libanaise. Migration Lessepsienne. Thalassia Salent 25: 71-74.
Carlton, J.T. (1989) Man’s role in changing the face of the ocean: biological invasions and implications for conservation of near-shore environments. Conserv Biol 3(3): 265-273.
Cattaneo-Vietti, R., Chemello, R., Giannuzzi-Savelli, R. (1990) Atlas of Mediterranean Nudibranchs. La Conchiglia, Roma, Italy.
Clarke Murray, C., Therriault, T.W., Martone, P.T. (2012) Adapted for invasion? Comparing attachment, drag and dislodgment of native and nonindigenous hull fouling species. Biol Invasions 14: 1651-1663.
Cohen, A.N., Carlton, J.T. (1998) Accelerating invasion rate in a highly invaded estuary. Science 279: 555-558.
Cvitković, I., Despalatović, M., Grubelić, I., Nikolić, V., Pleše, B., Žuljević, A. (2013) Occurrence of Paraleucilla magna (Porifera: Calcarea) in the eastern Adriatic Sea. Acta Adriatica: Int J Mar Sci 54(1): 93-99.
Çinar, M.E., Bilecenoglu, M., Öztürk, B., Can, A. (2006) New record of alien species on the Levantine coast of Turkey. Aquat Invasions 1: 84-90.
Despalatovic, M., Antolic, B., Grubelic, I., Uljevic, A. (2002) First record of the Indo-Pacific gastropod Melibe fimbriata in the Adriatic Sea. J Mar Biol Assoc UK 82: 923-924.
Dorgham, M.M., Hamdy, H., El-Rashidy, H.H., Atta, M.M. (2013) First records of polychaetes new to Egyptian Mediterranean waters. Oceanologia 55(1): 235- 267.
Engl, W. (1995) Specie prevalentemente Lessepsiane attestate lungo le coste turche. Bollettino Malacologico 31(1-4): 43-50.
European Environment Agency (2012) The Impacts of Invasive Alien Species in Europe. Luxembourg: EEA. 114 Technical Report 16. Publications Office of the European Union.
Ferrario, J., Caronni, S., Occhipinti-Ambrogi, A., Marchini, A. (2017) Role of commercial harbours and recreational marinas in the spread of non-indigenous fouling species. Biofouling 33(8): 651-660.
Galil, B.S. (1993) Lessepsian migration: New findings on the foremost anthropogenic change in the Levant Basin fauna. In: Symposium Mediterranean Seas 2000, (ed. DellaCroce, N.F.R.) Istituto Scienze Ambientali Marine- Santa Margherita Ligure, pp. 307-318.
Galil, B.S., Zenetos, A. (2002) A sea change-exotics in the eastern Mediterranean. In: Invasive Aquatic Species of Europe: Distributions, Impacts and Management, (eds., Leppäkoski, E., Olenin, S., Gollasch, S.), Kluwer Scientific Publications, pp. 325-336.
Gerovasileiou, V., Akel, E.H.K.h., Akyol, O., Alongi, G., Azevedo, F., Babali, N., Bakiu, R., Bariche, M., Bennoui, A., Castriota, L., Chintiroglou, C.C., Crocetta, F., Deidun, Α., Galinou-Mitsoudi, S., Giovos, Ι., Gökoğlu, M., Golemaj, Α., Hadjioannou, L., Hartingerova, J., Insacco, G., Katsanevakis, S., Kleitou, P., Korun, J., Lipej, L., Malegue, M., Michailidis, N., Mouzai Tifoura, A., Ovalis, P., Petović, S., Piraino, S., Rizkalla, S.I., Rousou, M., Savva, I., Şen, H., Spinelli, A., Vougioukalou, K.G., Xharahi, E., Zava, B., Zenetos, A. (2017) New Mediterranean biodiversity records (July, 2017). Medit Mar Sci 18(2): 179- 207.
Grosholz, E. (2002) Ecological and evolutionary consequences of coastal invasions. Trends in Ecology and Evolution 17:22-27.
Guardiola, M., Frotscher, J., Uriz, M.J. (2012) Genetic structure and differentiation at a short-time scale of the introduced calcarean sponge Paraleucilla magna to the western Mediterranean. Hydrobiologia 687: 71-84.
Haas, G. (1948) Sur l’immigration de mollusques de l’Indo-Pacifique dans les eaux côtières de la Palestine. J Conchyliologie 88: 141-144.
Halim, Y., Rizkalla, S. (2011) Aliens in Egyptian Mediterranean waters. A check-list of Erythrean fish with new records. Medit Mar Sci 12: 479-490.
Hoffman, R. (2013) Alien benthic algae and seagrasses in the Mediterranean Sea and their connection to global warming. In: The Mediterranean Sea: Its History and Present Challenges, (eds., Goffredo, S., Dubinsky, Z.), Springer Publishers, Netherlands, pp. 159-181.
Hoffman, R., Shemesh, E., Ramot, M., Dubinsky, Z., Pinchasov-Grinblat, Y., Iluz, D. (2011) First record of Codium arabicum Küt (Bryopsidales, Chlorophyta) in the Mediterranean Sea. Bot Mar 54: 487-495.
Jancic, G. (2004) Melibe from the Adriatic. [Message in] Sea Slug Forum. Australian Museum, Sydney. Available at: http://www.seaslugforum.net/find/12104 (accessed 7 May 2016).
Katsanevakis, S., Wallentinus, I., Zenetos, A., Leppäkoski, E., Çinar, M.E., Oztürk, B., Grabowski, M., Golani, D., Cardoso, A.C. (2014) Impacts of marine invasive alien species on ecosystem services and biodiversity: a pan European review. Aquat Invasions 9(4): 391-423.
Klautau, M., Monteiro, L. Borojevic, R. (2004) First occurrence of the genus Paraleucilla (Calcarea, Porifera) in the Atlantic Ocean: P. magna sp. nov. Zootaxa 710: 1-8.
Lambert, C.C., Lambert G. (1998) Non-indigenous ascidians in southern California harbours and marinas. Mar Biol 130: 675-688.
Longo, C., Mastrototaro, F., Corriero, G. (2007) Occurrence of Paraleucilla magna (Porifera: Calcarea) in the Mediterranean Sea. J Mar Biol Assoc UK 87: 1749-1755.
Lopez-Legentil S., Legentil M.L., Erwin P.M., Turon X. (2015) Harbor networks as introduction gateways: contrasting distribution patterns of native and introduced ascidians. Biol Invasions 17(6): 1623-1638.
Mačić, V., Petović, S. (2016) New data on the distribution of the alien sponge Paraleucilla magna Klautau, Monteiro & Borojević, 2004 in the Adriatic Sea. Studia Marina 29(1): 63-68.
Maurice, A.P., Lockyear B.E. (1983) A Bridge and Galley Guide to Tunisia. McMillan Graham.
Minchin, D., Floerl, O., Savini, D., Occhipinti-Ambrogi, A. (2006) Small craft and the spread of exotic species. In: The Ecology of Transportation: Managing Mobility for The Environment, (eds., Davenport, J. Davenport, J.L.), Springer, The Netherlands, pp. 99-118.
Molnar, J.L., Gamboa, R.L., Revenga, C., Spalding, M.D. (2008) Assessing the global threat of invasive species to marine biodiversity. Front Ecol Environ 6: 458-492.
Moosleitner, H. (1986) Note on the occurrence of Melibe sp. (?) in the Mediteranean (Opisthobranchia: Fimbriidae). La Conchiglia 18(202-203): 20.
Nunes, A.L., Katsanevakis, S., Zenetos, A., Cardoso, A.C. (2014) Gateways to alien invasions in the European Seas. Aquatic Invasions 9: 133-144.
Occhipinti-Ambrogi, A., Marchini, A., Cantone, G., Castelli, A., Chimenz, C., Cormaci, M., Froglia, C., Furnari, G., Gambi, M.C., Giaccone, G., Giangrande, A., Gravili, C., Mastrototaro, F., Mazziotti, C., Orsi-Relini, L. Piraino, S. (2011) Alien species along the Italian coasts: an overview. Biol Invasions 13: 215-237.
Occhipinti-Ambrogi, A., Savini, D. (2003) Biological invasions as a component of global change in stressed marine ecosystems. Mar Poll Bull 46: 542-551.
Otero, M., Cebrian, E., Francour, P., Galil, B., Savini, D. (2013) Monitoring Marine Invasive Species in Mediterranean Marine Protected Areas (MPAs): A Strategy and Practical Guide for Managers. IUCN, Malaga, Spain.
Ounifi-Ben Amor, K., Rifi, Μ., Ghanem, R., Draeif, I., Zaouali, J., Ben Souissi, J. (2016) Update of alien fauna and new records from Tunisian marine waters. Medit Mar Sci 17(1): 124-143.
Pederson, J., Bullock, R., Carlton, J., Dijkstra, J., Dobroski, N., Dyrynda, P., Fisher, R., Harris, L., Hobbs, N., Lambert, G., Lazo-Wasem, E., Mathieson, A., Miglietta, M.P., Smith, J., Smith, III J., Tyrell, M. (2003) Marine Invaders in the Northeast; Rapid assessment survey of non-native and native marine species of floating dock communities. MIT, Sea Grant College Program, Cambridge, Massachusetts, Publication No. 05-3.
Rilov, G., Crooks, J. (2009) Biological Invasions in Marine Ecosystems. Springer, Berlin, Heidelberg.
Ruiz, G.M., Fofonoff, P.W., Carlton, J.T., Wonham, M.J., Hines, A.H. (2000) Invasion of coastal marine communities in North America: apparent patterns, processes and biases. Annu Rev Ecol Evol Syst 31: 481-531.
Sala, E., Kizilkaya, Z., Yildirim, D., Ballesteros, E. (2011) Alien marine fishes deplete algal biomass in the eastern Mediterranean. Plos One 6(2): e17356,
Sanchez Villarejo, F. (2007) Melibe ‘fimbriata’ from Cyprus. [Message in] Sea Slug Forum. Australian Museum, Sydney. Available at: http://www.seaslugforum.net/showall/melifimb (accessed 7 May 2016).
Sghaier, Y.R., Zakhama-Sraieb, R., Benamer, I., Charfi-Cheikhrouha, F. (2011) Occurrence of the seagrass Halophila stipulacea (Hydrocharitaceae) in the southern Mediterranean Sea. Bot Mar 54: 575-582.
Sghaier, Y.R., Zakhama-Sraieb, R., Mouelhi, S., Vazquez, M., Valle, C., Ramos-Espla, A.A., Astier J.M., Verlaque, M., Charfi-Cheikhrouha, F. (2016) Review of alien marine macrophytes in Tunisia. Medit Mar Sci 17(1): 109-123.
Shenkar, N., Loya, Y. (2009) Non-indigenous ascidians (Chordata: Tunicata) along the Mediterranean coast of Israel. Mar Biodiv Rec 2: 1-7
Steinitz, W. (1929) Die Wander ung indopazifischer Arten ins Mittelmeer seit Beginn der Quartärperiode. Int Rev Gesamten Hydrobiol 22: 1-90.
Topaloğlu, B., Evcen, A., Cinar, M.E. (2016) Sponge fauna in the Sea of Marmara. Turk J Fis Aquat Sci 16(1): 51-5.
Ulman, A., Ferrario, J., Occhipinti-Ambrogi, A., Arvanitidis, C., Bandi, A., Bertolino, M., Bogi, C., Chatzigeorgiou, G., Çiçek, B.A., Deidun, A., RamosEsplá, A., Koçak, Ç., Lorenti, M., Martínez-Laiz, G., Merlo, G., Princisgh, E., Scribano, G., Marchini, A. (2017) A massive update of non-indigenous species records in Mediterranean marinas. Peer J 5: e3954. http://dx.doi.org/10.7717/peerj.3954
UNEP/MAP (2017) Integrated Monitoring and Assessment Programme of the Mediterranean Sea and Coast and Related Assessment Criteria Athens, Greece.
UNEP-MAP-RAC/SPA (2015) Marine Mediterranean Invasive Alien Species. http://www.mamias.org (accessed 16 Jun 2018).
Verlaque, M. (2001) Checklist of the macroalgae of Thau Lagoon (Hérault, France), a hot spot of marine species introduction in Europe. Oceanol Acta 24(1): 29-49.
Yokes, B., Rudman, W.B. (2004) Lessepsian opisthobranchs from the southwestern coast of Turkey; five new records for the Mediterranean. Rapport Comm int Mer Médit 37: 557.
Zakhama-Sraieb, R., Sghaier, Y.R., Ben Hmida, A., Cappai, G., Carucci, A., Charfi-Cheikhrouha, F. (2016) Variation along the year of trace metal levels in the compartments of the seagrass Posidonia oceanica in Port El Kantaoui, Tunisia. Environ Sci Poll Res 23: 1681-1690.
Zammit, P.P., Longo, C., Schembri, P.J. (2009) Occurrence of Paraleucilla magna Klautau et al., 2004 (Porifera: Calcarea) in Malta. Medit Mar Sci 10(2): 135-138.
Zenetos, A., Gofas, S., Morri, C., Rosso, A., Violanti, D., García 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., HyamsKaphzan, O., Karachle, P.K., Katsanevakis, S., Lipej, L., Mastrototaro, F., Mineur, F., Pancucci-Papadopoulou, M.A., Ramos-Esplá, A., Salas, C., San Martín, G., Sfriso, A., Streftaris, N., Verlaque M. (2012) Alien species in the Mediterranean Sea by 2010. A contribution to the application of European Union’s Marine Strategy Framework Directive (MSFD). Part 2. Introduction trends and pathways. Medit Mar Sci 13(2): 328-352.