| More

A Preliminary inventory of alien and cryptogenic species in Monastir Bay, Tunisia: spatial distribution, introduction trends and pathways

Views: 637 Downloads: 310
SAHAR CHEBAANE (http://orcid.org/0000-0003-3700-8930), JUAN SEMPERE-VALVERDE (https://orcid.org/0000-0001-5856-9214), SAHBI DORAI (http://orcid.org/0000-0001-9050-0022), ADNEN KACEM, YASSINE RAMZI SGHAIER


The Mediterranean Sea is a marine biodiversity hotspot under threat. One of the major impacts on its biological resources and services comes from the invasiveness of non-indigenous species (NIS). Nevertheless, NIS monitoring programs in the south basin of the Mediterranean Sea are in an early implementation stage. This study aims to describe NIS and cryptogenic species distribution in Monastir Bay (Tunisia) and to identify risk areas for the introduction and spread of invasive species, providing a baseline for future monitoring programs. To this end, a series of Rapid Assessment Surveys were carried out to identify NIS and cryptogenic species in one marina, five fishing ports, two aquaculture farms and the Special Conservation Area of the Kuriat islands. 24 species were found, of which 11 constitute new records for Monastir Bay, which represent a 33.3% of the total NIS reported in this Bay. Assemblages differed between substrata types, being NIS more abundant in artificial than in natural substrata. Regarding locations, Cap Monastir Marina was the most invaded site, the most transited by vessels and the only one visited by international sailing. Hence, this marina constitutes the main risk area to be monitored, although the fishing ports and fishing farms in the semi-enclosed coastal lagoon of Monastir Bay can also be considered as risk areas. Nevertheless, more research effort is needed in Monastir Bay in order to update the records of NIS and cryptogenic species and increase insight on the ecological evolution of these species and their related impacts on natural communities and marine resources.


Non-indigenous Species; Introduction Vectors; Risk Areas; Monastir Bay, Tunisia

Full Text:



Aissi, M., Ben Amer, IB., Moslah S., Sghaier, YR., 2018. First record of the spotted sea hare Aplysia dactylomela Rang, 1828 in the south Mediterranean coast (Kuriat Islands, Tunisia). Journal of the Black Sea / Mediterranean Environment, 24 (2), 163‑68.

Anderson, M.J., Gorley, R.N., Clarke, K.R., 2008. PERMANOVA + for PRIMER. Guide to software and statistical methods. PRIMER-E Ltd, Plymouth, UK.

Bdioui, M., 2016. Premier signalement du crabe bleu Portunus segnis (forskål, 1775) dans le sud du golfe de Hammamet (centre-est de la Tunisie). Bulletin de l’Institut National des Sciences et Tecnologies de la Mer de Salammbô, 43,183‑87.

Ben Mustapha, K., Komatsu, T., Hattour, A., Sammari, Ch., Zarrouk, S. et al., 2002. Tunisian mega benthos from infra (Posidonia meadows) and circalittoral (coralligenous) sites. Bulletin de l’Institut National des Sciences et Tecnologies de la Mer de Salammbô. 29, 23–36.

Bethoux, J.P., Gentili, B., Morin, P., Nicolas, E., Pierre, C. et al., 1999. The Mediterranean Sea: a miniature ocean for climatic and environmental studies and a key for the climatic functioning of the North Atlantic. Progress in Oceanography, 44 (1-3), 131-146.

Boudouresque, C.F., Verlaque, M., 2010. Is global warming involved in the success of seaweed introductions in the Mediterranean Sea?. p. 31-50. In Seaweeds and their role in globally changing environments. Cellular Origin, Life in Extreme Habitats and Astrobiology, vol 15. Seckbach, J., Einav, R., Israel, A. (eds). Springer, Dordrecht.

Bradai, M.N., Quignard, J.P., Bouain, A., Jarboui, O., Ouannes- Ghorbel, A. et al., 2004. Ichtyofaune autochtone et exotique des côtes tunisiennes: recensement et biogeography. Cybium, 28 (4), 315-328.

Bulleri, F., Airoldi, L., 2005. Artificial marine structures facilitate the spread of a non-indigenous green alga, Codium fragile ssp. tomentosoides, in the north Adriatic Sea. Journal of Applied Ecology, 42 (6), 1063–1072.

Bulleri, F., Chapman, M.G., 2010. The introduction of coastal infrastructures as a driver of change in marine environments. Journal of Applied Ecology, 47 (1), 26–35.

Campbell, M.L., Gould, B., Hewitt, C.L., 2007. Survey evaluations to assess marine bioinvasions. Marine Pollution Bulletin, 55 (7-9), 360-378.

Campbell, M.L., King, S., Heppenstall, L.D., van Gool, E., Martin, R. et al., 2017. Aquaculture and urban marine structures facilitate native and non-indigenous species transfer through generation and accumulation of marine debris. Marine pollution bulletin, 123 (1-2), 304-312.

Carlton, J.T., Geller, J.B., 1993. Ecological roulette: the global transport of nonindigenous marine organisms. Science, 261, 78–82.

Challouf, R., Hamza, A., Mahfoudhi, M., Ghozzi, K., Bradai, M.N., 2017. Environmental assessment of the impact of cage fish farming on water quality and phytoplankton status in Monastir Bay (eastern coast of Tunisia). Aquaculture International, 25 (6), 2275-2292.

Chebaane, S., Kacem, A., Sghaier, Y.R., 2019. Contribution to the setting up of a monitoring programme for non-indigenous species in Monastir Bay, Tunisia. p. 34-39. In: 1st Mediterranean Symposium on the Non-Indigenous Species, Antalya, Turkey, 18 Jan 2019. Langar, H., Ouerghi, A. (Eds). SPA/RAC publi, Tunis.

Clarke, K.R., Gorley, R.N., 2006. PRIMER v6: User manual/tutorial. PRIMER-E Ltd, Plymouth, UK.

Coll, M., Piroddi, C., Steenbeek, J., Kaschner, K., Ben Rais Lasram, F. et al., 2010. The biodiversity of the Mediterranean Sea: estimates, patterns, and threats. PLoS ONE, 5 (8), e11842.

Corsini-Foka, M., Zenetos, A., Crocetta, F., Çinar, M.E., Koçak, F. et al., 2015. Inventory of alien and cryptogenic species of the Dodecanese (Aegean Sea, Greece): collaboration through COST action training school. Management of Biological Invasions, 6 (4), 351-366.

Crooks, J.A., Chang, A.L., Ruiz, G.M., 2011. Aquatic pollution increases the relative success of invasive species. Biological Invasions, 13 (1), 165-176.

Coutts, A.D., Valentine, J.P., Edgar, G.J., Davey, A., Burgess-Wilson, B., 2010. Removing vessels from the water for biofouling treatment has the potential to introduce mobile non-indigenous marine species. Marine pollution bulletin, 60 (9), 1533-1540.

Damak, M., Frontalini, F., Elleuch, B., Kallel, M., 2018. Benthic foraminiferal assemblages as pollution proxies along the coastal fringe of the Monastir Bay (Tunisia). Journal of African Earth Sciences, 150, 379-388.

Deidun, A., Gauci, A., Azzopardi, J., Camilleri, C., Cutajar, D. et al., 2018. Development of a Novel Tool for the Monitoring of Shipping Traffic within the Strait of Sicily (Central Mediterranean): the BIODIVALUE AIS Vessel Tracker. Journal of Coastal Research, 85 (sp1), 1356 – 1360.

Ferrario, J., Ulman, A., Marchini, A., Saracino, F. Ambrogi, A.O., 2016. Non-indigenous fouling species in the marina of Rome. Biologia Marina Mediterranea, 23 (1), 224-225.

Floerl, O., Norton, N., Inglis, G., Hayden, B., Middleton, C. et al., 2005. Efficacy of hull cleaning operations in containing biological material I. Risk assessment. MAF Biosecurity New Zealand Technical Paper, 8 (12).

Galil, B., 2018. Poisonous and venomous: marine alien species in the Mediterranean Sea and human health. p. 1-15. In: Invasive Species and Human Health. Mazza, G., Tricarico, E. (Eds). CABI, Wallingford, UK.

GDFA, 2018. Statistics of fisheries and aquaculture in Tunisia for the year 2017. Official Journal of the Ministry of Agriculture, Water Resources and Fisheries, General Directorate of Fisheries and Aquaculture, Tunisia.

Glasby, T.M., Connell, S.D., Holloway, M.G., Hewitt, C.L., 2007. Nonindigenous biota on artificial structures: could habitat creation facilitate biological invasions?. Marine Biology, 151 (3), 887–895.

Hopkins, G.A., Forrest, B.M., 2008. Management options for vessel hull fouling: an overview of risks posed by in-water cleaning. ICES Journal of Marine Science, 65 (5), 811-815.

Horton, T., Kroh, A., Ahyong, S., Bailly, N., Boyko, C.B. et al., 2019. World Register of Marine Species. http://www.marinespecies.org (Accessed 13 February 2019).

Katsanevakis, S., Coll, M., Piroddi, C., Steenbeek, J., Lasram, F. et al., 2014. Invading the Mediterranean Sea: Biodiversity patterns shaped by human activities. Frontiers in Marine Science, 1, 32.

Katsanevakis, S., Zenetos, A., Belchior, C., Cardoso, A.C., 2013. Invading European Seas: assessing pathways of introduction of marine aliens. Ocean & Coastal Management, 76, 64-74.

Kenworthy, J.M., Rolland, G., Samadi, S., Lejeusne, C., 2018. Local variation within marinas: Effects of pollutants and implications for invasive species. Marine pollution bulletin, 133, 96-106.

Lejeusne, C., Chevaldonné, P., Pergent-Martini, C., Boudouresque, C.F., Pérez, T., 2010. Climate change effects on a miniature ocean: the highly diverse, highly impacted Mediterranean Sea. Trends in ecology & evolution, 25 (4), 250-260.

Leung B., Lodge D., Finnoff D., Shogren F., Lewis M., Lamberti G., 2002. An ounce of prevention or a pound of cure: bioeconomic risk analysis of invasive species. Proceedings of the Royal Society of London. Series B: Biological Sciences, 269 (1508), 2407‑2413.

Mangos A., Claudot M.A., 2013. Economic study of the impacts of marine and coastal protected areas in the Mediterranean. Plan Bleu, Valbonne, Plan Bleu 13, 58 pp.

Marchini, A., Ferrario, J., Sfriso, A., Occhipinti-Ambrogi, A., 2015. Current status and trends of biological invasions in the Lagoon of Venice, a hotspot of marine NIS introductions in the Mediterranean Sea. Biological invasions, 17 (10), 2943-2962.

Martínez-Laiz, G., Ulman, A., Ros, M., Marchini, A., 2019. Is recreational boating a potential vector for non-indigenous peracarid crustaceans in the Mediterranean Sea? A combined biological and social approach. Marine Pollution Bulletin, 140, 403-415.

Mesel, I.D., Kerckhof, F., Norro, A., Rumes, B., Degraer, S., 2015. Succession and seasonal dynamics of the epifauna community on offshore wind farm foundations and their role as stepping stones for non-indigenous species. Hydrobiologia, 756 (1), 37-50.

Micheli, F., Halpern, B.S., Walbridge, S., Ciriaco, S., Ferretti, F. et al., 2013. Cumulative human impacts on Mediterranean and Black Sea marine ecosystems: assessing current pressures and opportunities. PloS one, 8 (12), e79889.

Minchin, D., Gollasch, S., Cohen, A.N., Hewitt, C.L., Olenin, S., 2009. Characterizing vectors of marine invasion. p. 109-116. In: Biological invasions in marine ecosystems. Springer, Berlin, Heidelberg.

Molina, S., Ros, M., Guerra-García, J.M., 2017. Distribution of the Invasive Caprellid Caprella scaura (Crustacea: Amphipoda) in Cádiz Marina, Southern Spain: Implications for its Dispersal. Thalassas: An International Journal of Marine Sciences, 33(2), 81-86.

Nouira, T., Tagorti, M. A., Budzinski, H., Etchebert, H., Boussetta, H., 2013. Polycyclic aromatic hydrocarbons (PAHs) in surface sediments of Monastir Bay (Tunisia, Central Mediterranean): distribution, origin and seasonal variations. International Journal of Environmental Analytical Chemistry, 93 (14), 1470-1483.

Occhipinti Ambrogi, A., 2001. Transfer of marine organisms: a challenge to the conservation of coastal biocoenoses. Aquatic Conservation: marine and freshwater Ecosystems, 11 (4), 243-251.

Occhipinti-Ambrogi, A., Savini, D., 2003. Biological invasions as a component of global change in stressed marine ecosystems. Marine Pollution Bulletin, 46 (5), 542-551.

Ostalé-Valriberas, E., Sempere-Valverde, J., Coppa, S., García-Gómez, J.C., Espinosa, F., 2018. Creation of microhabitats (tidepools) in ripraps with climax communities as a way to mitigate negative effects of artificial substrate on marine biodiversity. Ecological engineering, 120, 522-531.

Ounifi-Amor, K.O.B., Rifi, Μ., Ghanem, R., Draeif, I., Zaouali, J., et al., 2016. Update of alien fauna and new records from Tunisian marine waters. Mediterranean Marine Science.17 (1), 124-143.

Piola, R.F., Johnston, E.L., 2008. Pollution reduces native diversity and increases invader dominance in marine hard‐substrate communities. Diversity and Distributions, 14 (2), 329-342.

Piola, R.F., Johnston, E.L., 2009. Comparing differential tolerance of native and non-indigenous marine species to metal pollution using novel assay techniques. Environmental Pollution, 157 (10), 2853-2864.

PNUE-PAM-CAR/ASP, 2017. Programme National de surveillance de la biodiversité marine et des espèces non indigènes en Tunisie. CAR/ASP – Projet EcApMEDII. Ben Haj S. (Ed.), Tunis, 49 pp.

Ramalhosa, P., Gestoso, I., Duarte, B., Caçador, I., Canning-Clode, J., 2019. Metal pollution affects both native and non-indigenous biofouling recruitment in a subtropical island system. Marine Pollution Bulletin, 141, 373-386.

Ramos-Espla, A.A., Ben Mustapha, K., 2010. Rapport de la mission d’tude des habitats marins et des principales espèces des Iles Kuriat (Tunisie) (octobre 2008). APAL-CAR/ASP- INSTM Salammbô-UA/UBM, 86 pp.

Rech, S., Salmina, S., Pichs, Y.J.B., García-Vazquez, E., 2018. Dispersal of alien invasive species on anthropogenic litter from European mariculture areas. Marine pollution bulletin, 131 (A), 10-16.

Rilov, G., Crooks, J.A., 2009. Marine bioinvasions: conservation hazards and vehicles for ecological understanding. p. 3-11. In: Biological invasions in marine ecosystems. Rilov. G., Crooks, J.A. (Eds). Springer, Berlin.

Ros, M., Vázquez-Luis, M., Guerra-García, J.M., 2013. The role of marinas and recreational boating in the occurrence and distribution of exotic caprellids (Crustacea: Amphipoda) in the Western Mediterranean: Mallorca Island as a case study. Journal of Sea Research, 83, 94-103.

Ros, M., Vázquez-Luis, M., Guerra-García, J.M., 2015. Environmental factors modulating the extent of impact in coastal invasions: the case of a widespread invasive caprellid (Crustacea: Amphipoda) in the Iberian Peninsula. Marine pollution bulletin, 98(1-2), 247-258.

Ruiz, G.M., Freestone, A.L., Fofonoff, P.W., Simkanin, C., 2009. Habitat distribution and heterogeneity in marine invasion dynamics: the importance of hard substrate and artificial structure. p. 321-332. In: Marine hard bottom communities. Springer, Berlin, Heidelberg.

Sempere-Valverde, J., Ostalé-Valriberas, E., Farfán, G.M., Espinosa, F., 2018. Substratum type affects recruitment and development of marine assemblages over artificial substrata: A case study in the Alboran Sea. Estuarine, Coastal and Shelf Science, 204, 56-65.

Sghaier, Y.R., Zakhama-Sraieb, Ben Hmida, A., Charfi-Cheikhrouha, F., 2019. An inventory of non-indigenous species (NIS) inside and outside three tourist marinas from the southern Mediterranean coast. Journal of the Black Sea / Mediterranean Environment, 25(1), 29-48.

Sghaier, Y.R., Zakhama-Sraieb, R., Mouelhi, S., Vazquez, M., Valle-Pérez, C. et al., 2016. Review of alien marine macrophytes in Tunisia. Mediterranean Marine Science, 17 (1), 109-123.

Sghaier, Y.R., Zakhama-Sraieb, R., Benamer, I., Charfi-Cheikhrouha, F., 2011a. Occurrence of the seagrass Halophila stipulacea (Hydrocharitaceae) in the southern Mediterranean Sea. Botanica Marina, 54 (6), 575‑582.

Sghaier, Y.R., Zakhama-Sraieb, R., Charfi-Cheikhrouha, F., 2011b. On the distribution of Percnon gibbesi (H. Milne Edwards, 1853) (Crustacea, Decapoda, Plagusiidae) along the Tunisian coast. Mediterranean Marine Science, 12 (1), 233-237.

Streftaris, N., Zenetos. A., 2006. Alien marine species in the Mediterranean – the 100 ‘worst invasive’ and their impact. Mediterranean Marine Science, 7 (1), 87-118.

Tilman, D., 1997. Community invasibility, recruitment limitation, and grassland biodiversity. Ecology, 78 (1), 81–92.

Tlig-Zouari, S., Rabaoui, L., Irathni, I., Ben Hassine, OK., 2009. Distribution, habitat and population densities of the invasive species Pinctada radiata (Molluca: Bivalvia) along the Northern and Eastern coasts of Tunisia. Cahiers de Biologie Marine. 50 (2), 131‑142.

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

UNEP/MAP, 2016a. Integrated Monitoring and Assessment Programme of the Mediterranean Sea and Coast and Related Assessment Criteria. United Nations Environment Programme Mediterranean Action Plan. Athens, Greece. 22 (7), 1-162.

UNEP/MAP, 2016b. Integrated Monitoring and Assessment Guidance. United Nations Environment Programme Mediterranean Action Plan. Athens, Greece.

UNEP/MAP, 2018. Agenda items 3: Progress Report for April - September 2018. Compilation of Project Fiches. United Nations Environment Programme Mediterranean Action Plan. Athens, Greece. 87 (5), 53-56.

Verlaque, M., 2001. Checklist of the macroalgae of Thau Lagoon (Hérault, France), a hot spot of marine species introduction in Europe. Oceanologica acta, 24 (1), 29-49.

Vitousek, P.M., D’Antonio, C.M., Loope, L.L., Rejmanek, M., Westbrooks, R., 1997. Introduced species: a significant component of human caused global change. New Zealand Journal of Ecology, 21 (1), 1–16.

Woods, C.M., Floerl, O., Jones, L., 2012. Biosecurity risks associated with in-water and shore-based marine vessel hull cleaning operations. Marine pollution bulletin, 64 (7), 1392-1401.

Zaafrane, S., Maatouk, K., 2016. Note sur la présence de l’espèce Siganus rivulatus (Forsskål, 1775) au niveau des côtes–Est de la Tunisie. Bulletin de l’Institut National des Sciences et Tecnologies de la Mer de Salammbô, 43, 169‑177.

Zenetos, A., Gofas, S., Morri, C., Rosso, A., Violanti, D. et al., 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 (2), 328–352.

Zenetos, A., Gofas, S., Verlaque, M., Çinar, M. E., García Raso, E. et al., 2010. Alien species in the Mediterranean 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.


  • There are currently no refbacks.