Abstract
An updated overview of the marine alien and cryptogenic species recorded in the Egadi Islands Marine Protected Area (Tyrrhenian Sea, Italy), based on relevant publications, grey literature and unpublished data, is presented and discussed. Altogether, 17 species (14 aliens and 3 cryptogenic) belonging to five taxa are present in the area: Rhodophyta (Antithamnionella elegans, Asparagopsis armata, Asparagopsis taxiformis, Bonnemaisonia hamifera, Botryocladia madagascariensis, Ceramium strobiliforme, Laurencia caduciramulosa, Lophocladia lallemandii, Neosiphonia harveyi, Womersleyella setacea), Chlorophyta (Caulerpa cylindracea and Caulerpa taxifolia), Mollusca (Aplysia dactylomela), Arthropoda (Percnon gibbesi) and Cordata (Fistularia commersonii, Kyphosus vaigiensis and Stephanolepis diaspros). The overall Mediterranean presence of one further taxon recorded from the area, Zygochlamys patagonica (Mollusca), is here confuted since recent findings of living specimens with certain data are missing. One loose valve of “Pinctada imbricata radiata (Mollusca)” was found in 2010 at Favignana, but we did not include it in the list of alien species, pending further finding of living or dead specimens. Unpublished distributional data are reported for some of these species, and their known distribution in the Aegadian Archipelago is mapped. Records of P. gibbesi (a conspicuous number of specimens) constitute the first for the archipelago. All the species included in the present paper were recorded after the Egadi Islands Marine Protected Area was established, with the first record dating back to 2000. This is presumably due to the recent increase in research programs on marine reserves. Finally, we provide the establishment status of all the recorded species updated to 2015, and discuss why unaided spread (whether alien or native) and/or transport-stowaway constitute the more plausible vectors of introduction.
Similar content being viewed by others
References
Abelló P, Visauta E, Bucci A, Demestre M (2003) Noves dades sobre l’expansió del cranc Percnon gibbesi (Brachyura: Grapsidae: Plagusiinae) a la Mediterrània occidental. Boll Soc Hist Nat Balears 46:73–77
Andreakis N, Procaccini G, Kooistra W (2004) Asparagopsis taxiformis and Asparagopsis armata (Bonnemaisoniales, Rhodophyta): genetic and morphological identification of Mediterranean populations. Eur J Phycol 39:273–283
Andreakis N, Procaccini G, Maggs C, Kooistra WHCF (2007) Phylogeography of the invasive seaweed Asparagopsis (Bonnemaisoniales, Rhodophyta) reveals cryptic diversity. Mol Ecol 16:2285–2299
Andreakis N, Kooistra WHCF, Procaccini G (2009) High genetic diversity and connectivity in the polyploid invasive seaweed Asparagopsis taxiformis (Bonnemaisoniales) in the Mediterranean, explored with microsatellite alleles and multilocus genotypes. Mol Ecol 18:212–226
Azzurro E, Soto S, Garofalo G, Maynou F (2013) Fistularia commersonii in the Mediterranean Sea: invasion history and distribution modeling based on presence-only records. Biol Invasions 15(5):977–990
Barone R, Di Martino V, Mannino AM (2003a) Asparagopsis taxiformis (Delile) Trevisan in Sicily: distribution and reproductive strategies. Third European Phycological Congress (EPC3, Belfast, Ireland)
Barone R, Mannino AM, Marino M (2003b) Asparagopsis taxiformis (Bonnemaisoniales, Rhodophyta): first record of gametophytes on the Italian coast. Bocconea 16(2):1021–1025
Bax N, Williamson A, Aguero M, Gonzales E, Geeves W (2003) Marine invasive alien species: a threat to global biodiversity. Mar Policy 27:313–323
Belton GS, Prud’homme van Reine WF, Huisman JM, Draisma SGA, Gurgel CFD (2014) Resolving phenotypic plasticity and species designation in the morphologically challenging Caulerpa racemosa–peltata complex (Chlorophyta, Caulerpaceae). J Phycol 50:32–54
Benedetti-Cecchi L, Cinelli F (1989) Note on a Polysiphonia sp. (Rhodohyta, Ceramiales) collected at Rosignano Solvay (Western Mediterranean). Giorn Bot Ital 123:49–54
Berthold G (1882) Die Bangiaceen des Golfes von Neapel und der angrenzenden Meeres-Abschnitte. Fauna Flora Golfes Neapel, Monographie 8. Englemann, Leipzig
Bianchi CN (2007) Biodiversity issues for the forthcoming tropical Mediterranean Sea. Hydrobiology 580:7–21
Bouchet P (2015) Pinctada imbricata radiata (Leach, 1814). In: MolluscaBase (2015) World register of marine species. http://marinespecies.org/aphia.php?p=taxdetails&id=564660
Boudouresque CF, Verlaque M (2002) Biological pollution in the Mediterranean Sea: invasive versus introduced macrophytes. Mar Pollut Bull 44:32–38
Britton-Simmons KH, Abbott KC (2008) Short- and long-term effects of disturbance and propagule pressure on a biological invasion. J Ecol 96:68–77
Burfeind DD, Pitt KA, Connolly RM, Byers JE (2013) Performance of invasive species within marine reserves. Biol Invasions 15:17–28
Byers JE (2005) Marine reserves enhance abundance but not competitive impacts of a harvested nonindigenous species. Ecology 86:487–500
Carefoot TH (1987) Aplysia: its biology & ecology. Oceanogr Mar Biol Annu Rev 25:167–284
Carlton JT (1996) Biological invasions and cryptogenic species. Ecology 77(6):1653–1655
Carlton JT (2009) Deep invasion ecology and the assembly of communities in historical time. In: Rilov G, Crooks J (eds) Biological invasions in marine ecosystems. Springer, Berlin, pp 13–56
Castriota L, Falautano M, Battaglia P, Oddo A, Andaloro F (2014) New biological data on Fistularia commersonii in the central Mediterranean Sea. Cybium 38(1):15–21
Catra M, Alongi G, Serio D, Cormaci M, Furnari G (2006) The benthic algal flora on rocky substrata of the Egadi Islands, a marine protected archipelago off the western coast of Sicily (Italy, Mediterranean Sea). Nova Hedwigia 82:489–538
[CBD] Convention on Biological Diversity (2014) Pathways of Introduction of Invasive Species, Their Prioritization, and Management. CBD (5 May 2014; www.cbd.int/doc/meetings/sbstta/sbstta-18/official/sbstta-18-09-add1-en.pdf)
Coll M, Piroddi C, Steenbeek J, Kaschner K, Ben Rais Lasram F, Aguzzi J, Ballesteros E, Bianchi CN, Corbera J, Dailianis T, Danovaro R, Estrada M, Froglia C, Galil BS, Gasol JM, Gertwagen R, Gil J, Guilhaumon F, Kesner-Reyes K, Kitsos MS, Koukouras A, Lampadariou N, Laxamana E, López-Fé de la Cuadra CM, Lotze HK, Martin D, Mouillot D, Oro D, Raicevich S, Rius-Barile J, Saiz-Salinas JI, San Vicente C, Somot S, Templado J, Turon X, Vafidis D, Villanueva R, Voultsiadou E (2010) The biodiversity of the Mediterranean Sea: estimates, patterns and threats. PLoS ONE 5(8):e11842. doi:10.1371/journal.pone.0011842
Cormaci M, Furnari G, Alongi G, Dinaro R, Pizzuto F (1992) On the occurrence in Sicily of three Florideophyceae new to the Mediterranean Sea. Bot Mar 35:447–450
Cormaci M, Furnari G, Giaccone G, Serio D (2004) Alien macrophytes in the Mediterranean Sea: a review. Recent Res Devel Environ Biol 1:153–202
Crocetta F, Renda W (2008) Further record of Chlamys lischkei (Bivalvia: Pectinoidea) in the Mediterranean Sea. Mar Biodiv Rec 1:e57. doi:10.1017/S1755267207006045
Deidun A, Castriota L, Falautano M, Maraventano G, Prazzi E, Andaloro F (2015) Documenting the occurrence of the Lessepsian fish Stephanolepis diaspros within the Strait of Sicily, central Mediterranean. J Black Sea/Medit Environ 21(1):1–11
Delile AR (1813) Florae Aegyptiacae illustratio. In: Anon (ed) Description de l’Egypte ou recueil des observations et des recherches qui ont été faites en Egypte pendant l’expédition de l’armée française (1798–1801), Histoire naturelle, Vol. 2, Paris: France (Commission d’Egypte), pp 49–82
Dijoux L, Viard F, Payri C (2014) The more we search, the more we find: discovery of a new lineage and a new species complex in the genus Asparagopsis. PLoS ONE 9(7):e103826. doi:10.1371/journal.pone.0103826
Dixon PS, Irvine LM (1977) Seaweeds of the British Isles. Volume 1 Rhodophyta. Part 1 Introduction, Nemaliales, Gigartinales. The Natural History Museum, London
EC (European Commission) (2008) Developing an EU framework for invasive alien species discussion paper (Final). http://ec.europa.eu/environment/nature/invasivealien/docs/ias_discussion_paper.pdf.
Evans J, Barbara J, Schembri PJ (2015) Updated review of marine alien species and other ‘newcomers’ recorded from the Maltese Islands (Central Mediterranean). Mediterr Mar Sci 16(1):225–244
Feldman J, Feldman G (1942) Récherches sur les Bonnemaisoniacées et leur alternance de génération. Ann Sci Nat Bot Ser 11(3):75–175
Furnari G, Cormaci M, Serio D (2001) The Laurencia complex (Rhodophyta, Rhodomelaceae) in the Mediterranean Sea: on overview. Cryptogamie, Algol 22:331–373
Galil BS (2007) Loss or gain? Invasive aliens and biodiversity in the Mediterranean Sea. Mar Pollut Bull 55:314–322
Galil BS, Goren M (2014) Metamorphoses: bioinvasions in the Mediterranean Sea. In: Goffredo S, Dubinsky Z (eds) The Mediterranean Sea. Springer, Dordrecht, pp 463–478
Galil B, Boero F, Fraschetti S, Piraino S, Campbell M, Hewitt C, Carlton J, Cook E, Jelmert A, Macpherson E, Marchini A, Occhipinti-Ambrogi A, Mckenzie C, Minchin D, Ojaveer H, Olenin S, Ruiz G (2015) The enlargement of the Suez Canal and introduction of non-indigenous species to the Mediterranean Sea. Bull Limnol Oceanog 24(2):25–64
Galil BS, Marchini A, Occhipinti-Ambrogi A (2016) East is east and West is west? Management of marine bioinvasions in the Mediterranean Sea. Estuar Coast Shelf S. doi:10.1016/j.ecss.2015.12.021
Gianguzza P, Zava B, Bonaviri C, Monteverde G, Palmeri A, Riggio S (2006) First record of Caulerpa taxifolia (Caulerpales, Ulvophyceae) in the western Sicilian waters (Italy). Biol Mar Medit 13(1):591–592
Golani D (2000) First record of the bluespotted cornetfish from the Mediterranean Sea. J Fish Biol 56:1545–1547
Golani D, Orsi-Relini L, Massutí E, Quignard JP, Dulčić J, Azzurro E (2015) CIESM atlas of exotic fishes in the Mediterranean. http://www.ciesm.org/atlas/appendix1.html
Gubbioli F, Nofroni I (1985) Note malacologiche dal mare di Alboran (Mediterraneo occidentale). Contributo 1. La Conchiglia 17(200–201):20–21
ISPE (2007) Monitoraggio dei popolamenti ittici presenti nei caulerpeti alloctoni siciliani. ISPE ed., Palermo
Jongma DN, Campo D, Dattolo E, D’Esposito D, Duchi A, Grewe P, Huisman J, Verlaque M, Yokes MB, Procaccini G (2013) Identity and origin of a slender Caulerpa taxifolia strain introduced into the Mediterranean Sea. Bot Mar 56:27–39
Jousson O, Pawlowski J, Zaninetti L, Meinesz A, Boudouresque CF (1998) Molecular evidence for the aquarium origin of the green alga Caulerpa taxifolia introduced to the Mediterranean Sea. Mar Ecol Progr Ser 172:275–280
Katsanevakis S, Poursanidis D, Yokes MB, Mačić V, Beqiraj S, Kashta L, Sghaier YR, Zakhama-Sraieb R, Benamer I, Bitar G, Bouzaza Z, Magni P, Nike Bianchi C, Tsiakkiros L, Zenetos A (2011) Twelve years after the first report of the crab Percnon gibbesi (H. Milne Edwards, 1853) in the Mediterranean: current distribution and invasion rates. J Biol Res-Thessalon 16:224–236
Katsanevakis S, Bogucarskis K, Gatto F, Vandekerkhove J, Deriu I, Cardoso AC (2012) Building the European Alien Species Information Network (EASIN): a novel approach for the exploration of distributed alien species data. BioInvasions Rec 1(4):235–245
Katsanevakis S, Zenetos A, Belchior C, Cardoso AC (2013) Invading European Seas: assessing pathway of introduction of marine aliens. Ocean Coast Manag 76:64–74
Katsanevakis S, Coll M, Piroddi C, Steenbeek J, Ben Rais Lasram F, Zenetos A, Cardoso AC (2014) Invading the Mediterranean Sea: biodiversity patterns shaped by human activities. Front Mar Sci 1:32. doi:10.3389/fmars.2014.00032
Klinger T, Padilla DK, Britton-Simmons K (2006) Two invaders achieve higher densities in reserves. Aquat Conserv-Mar Freshw Eco 16:30–311
Lauret M (1967) Morphologie, Phenologie, repartition des Polysiphonia marins du littoral languedocien. I. Section Oligosiphonia. Nat Monspel ser Bot 18:347–373
Lejeusne C, Chevaldonne P, Pergent-Martini C, Boudouresque CF, Perez T (2010) Climate change effects on a miniature ocean: the highly diverse, highly impacted Mediterranean Sea. Trends Ecol Evol 25:250–260
Lipej L, Mavrič B, Dulčić J (2014) Northernmost record of the reticulated leatherjacket Stephanolepis diaspros Fraser-Brunner, 1940 in the Mediterranean Sea. Mediterr Mar Sci 15(1):198–212
Mannino AM, Balistreri P, Yokeş MB (2014) First record of Aplysia dactylomela (Opisthobranchia, Aplysiidae) from the Egadi Islands (western Sicily). Mar Biodiv Rec 7:e22. doi:10.1017/S1755267214000190
Mannino AM, Balistreri P, Iaciofano D, Galil BS, Lo Brutto S (2015) An additional record of Kyphosus vaigiensis (Quoy & Gaimard, 1825) (Osteichthyes, Kyphosidae) from Sicily clarifies the confused situation of the Mediterranean kyphosids. Zootaxa 3963(1):045–054
Marchini A, Galil BS, Occhipinti-Ambrogi A (2015) Recommendations on standardizing lists of marine alien species: lessons from the Mediterranean Sea. Mar Poll Bull 101:267–273
Meinesz A, Hesse B (1991) Introduction et invasion de l’algue tropicale Caulerpa taxifolia en Méditerranée Nord occidentale. Oceanol Acta 14(4):415–426
Meinesz A, Belsher T, Thibaut T, Antolic B, Mustapha KB, Boudouresque CF, Chiaverini D, Cinelli F, Cottalorda JM, Djellouli A, El Abed A, Orestano C, Grau AM, Ivesa L, Jaklin A, Langar H, Massuti-Pascual E, Peirano A, Tunesi L, De Vaugelas J, Zavodnik N, Zuljevic A (2001) The introduced green alga Caulerpa taxifolia continues to spread in the Mediterranean. Biol Invasions 3:201–210
Meusnier I, Valero M, Olsen JL, Stam WT (2004) Analysis of rDNA ITS1 indels in Caulerpa taxifolia (Chlorophyta) supports a derived, incipient species status for the invasive strain. Eur J Phycol 39:83–92
Minchinton TE, Bertness MD (2003) Disturbance-mediated competition and the spread of Phragmites australis in a coastal marsh. Ecol Appl 13:1400–1416
Nizamuddin M (1991) The green marine algae of Libya. Elga, Bern
Occhipinti-Ambrogi A, Marchini A, Cantone G, Castelli A, Chimenz C, Cormaci M, Froglia C, Furnari G, Gambi MC, Giaccone G, Giangrande A, Gravili C, Mastrototaro F, Mazziotti C, Orsi-Relini L, Piraino S (2011a) Alien species along the Italian coasts: an overview. Biol Invasions 13:215–237
Occhipinti-Ambrogi A, Marchini A, Cantone G, Castelli A, Chimenz C, Cormaci M, Froglia C, Furnari G, Gambi MC, Giaccone G, Giangrande A, Gravili C, Mastrototaro F, Mazziotti C, Orsi-Relini L, Piraino S (2011b) Erratum to: alien species along the Italian coasts: an overview. Biol Invasions 13:531–532
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)
Paula J, Hartnoll RG (1989) The larval and post-larval development of Percnon gibbesi (Crustacea, Brachyura, Grapsidae) and the identity of the larval genus Pluteocaris. J Zool Lond 218:17–37
Pennings SC (1991) Spatial and temporal variation in recruitment of Aplysia californica Cooper: patterns, mechanisms and consequences. J Exp Mar Biol Ecol 146:253–274
Petersen HE (1918) Algae (excluding calcareous algae). Rep Danish Oceanog Biology (Exped. 1908–1910 Medit. adj. seas) 2:1–20
Piazzi L, Meinesz A, Verlaque M, Akçali B, Antolić B, Argyrou M, Balata M, Ballesteros E, Calvo S, Cinelli F, Cirik S, Cossu A, D’Archino F, Djellouli AS, Javel F, Lanfranco E, Mifsud C, Pala D, Panayotidis P, Peirano A, Pergent G, Petrocelli A, Ruitton S, Žuljević A, Ceccherelli G (2005) Invasion of Caulerpa racemosa var. cylindracea (Caulerpales, Chlorophyta) in the Mediterranean Sea: an assessment of the spread. Cryptogamie, Algol 26(2):189–202
Por FD (1978) Lessepsian migration. The influx of Red Sea biota into Mediterranean by way of the Suez Canal. Ecological Studies, 23. Springer, Berlin
Relini M, Orsi L, Puccio V, Azzuro E (2000) The exotic crab Percnon gibbesi (H. Milne-Edwards, 1853) (Decapoda, Grapsidae) in the Central Mediterranean. Sci Mar 64:337–340
Repetto G (1989) Nuovo ritrovamento in Mediterraneo di Chlamys lischkei (Bunker, 1850). Boll Malacol 25:261–262
Schembri PJ, Barbara J, Deidun A, Lanfranco E, Lanfranco S (2015) It was only a matter of time: occurrence of Caulerpa taxifolia (Vahl) C. Agardh var. distichophylla (Sonder) Verlaque, Huisman and Procaccini in the Maltese Islands (Chlorophyta, Ulvophyceae, Caulerpaceae). BioInvasions Rec 4(1):9–16
Steinitz W (1927) Beiträge zur Kenntnis der Küstenfauna Palästinas. I. Pubbl Staz Zool Napoli 8(3–4):311–353
Trainito E (2003) Mediterranean harlequins, a field guide to Mediterranean sea slugs. Taphros, Olbia (Italy)
Tsiamis K, Aydogan Ö, Bailly N, Balistreri P, Bariche M, Carden-Noad S, Corsinifoka M, Crocetta F, Davidov B, Dimitriadis C, Dragičević B, Drakulić M, Dulčić J, Escánez A, Fernández-Álvarez FA, Gerakaris V, Gerovasileiou V, Hoffman R, Izquierdo-Gómez D, Izquierdo-Muñoz A, Kondylatos G, Latsoudis P, Lipej L, Madiraca F, Mavrič B, Parasporo M, Sourbès L, Taşkin E, Tűrker A, Yapici S (2015) New Mediterranean biodiversity records (July 2015). Mediterr Mar Sci 16(2):472–488
Valdés A, Alexander J, Crocetta F, Yokes B, Giacobbe S, Poursanidis D, Zenetos A, Cervera JL, Caballer M, Galil B, Schembri P (2013) The origin and dispersal pathway of the spotted sea hare Aplysia dactylomela (Mollusca: Opisthobranchia) in the Mediterranean Sea. Aquat Invasions 8:427–436
Verlaque M (1989) Contribution à la flore des algues marines de Méditerranée: espèces rares ou nouvelles pour les côtes françaises. Bot Mar 32:101–113
Wallentinus I, Nyberg CD (2007) Introduced marine organisms as habitats modifiers. Mar Pollut Bull 55:323–332
West EJ, Barnes P, Wright J, Davis A (2007) Anchors aweigh: fragment generation of invasive Caulerpa taxifolia by boat anchors and its resistance to desiccation. Aquat Bot 87:196–202
Zenetos A, Gofas S, Russo G, Templado J (2004) Molluscs. In: Briand F (ed) CIESM atlas of exotic species in the Mediterranean, vol 3. CIESM Publishers, Monaco, pp 1–380
Zenetos A, Gofas S, Verlaque M, Çinar ME, García Raso JE Bianchi CN, Morri C, Azzurro E, Bilecenoglu M, Froglia C, Siokou I, Violanti D, Sfriso A, San Martìn G, Giangrande A, Katağan T, Ballesteros E, Ramos Espla A, Mastrototaro F, Ocaña O, Zingone A, Gambi MC, Streftaris N (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(2):381–493
Zenetos A, Gofas S, Morri C, Rosso A, Violanti D, García Raso JE, Çinar ME, Almogi-Labin A, Ates AS, Azzurro E, Ballesteros E, Bianchi CN, Bilecenoglu M, Gambi MC, Giangrande A, Gravili C, Hyams-Kaphzan O, Karachle PK, Katsanevakis S, Lipej L, Mastrototaro F, Mineur F, Pancucci-Papadopoulou MA, Ramos Esplá A, Salas C, San Martín G, Sfriso A, Streftaris N, Verlaque M (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. Patterns in introduction trends and pathways. Mediterr Mar Sci 13(2):328–352
Acknowledgments
The authors thank Ernesto Azzurro, Luca Castriota, Stefano Melchioni, Gabriele Sercia, Vito Vaccaro and Bruno Zava for providing photos, information and records. They also thank Dr. Elisabetta Oddo for improving the English text. The study of the alien species from Italy was partially funded by the East and South European Network for Invasive Alien Species—a tool to support the management of alien species in Bulgaria (ESENIAS-TOOLS) (EEA funded: Contract No. Д-33-51/30.06.2015) (FC).
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by P. Martinez Arbizu
Rights and permissions
About this article
Cite this article
Mannino, A.M., Parasporo, M., Crocetta, F. et al. An updated overview of the marine alien and cryptogenic species from the Egadi Islands Marine Protected Area (Italy). Mar Biodiv 47, 469–480 (2017). https://doi.org/10.1007/s12526-016-0496-z
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12526-016-0496-z