Progress in Mediterranean Bioinvasions Two Years After the Suez Canal Enlargement

ISSN: 0001-5113 AADRAY ACTAADRIAT., 58(2): 347 - 358, 2017 ORIGINAL SCIENTIFIC PAPER Progress in Mediterranean bioinvasions two years after the Suez Canal enlargement Argyro ZENETOS Hellenic Centre for Marine Research, Institute of Marine Biological Resources and Inland Waters, 19003 Anavissos, Greece Corresponding author, e-mail: [email protected] The possibility that the recent expansion of the Suez Canal could trigger an entirely new twenty first century wave of invasions was investigated. Results showed that only 19 new alien species were detected after August 2015 (date of the last Suez Canal enlargement). Five of the newcomers have already established viable populations. Between August 2015 and August 2017 approximately 9,5 new species (mostly fish) entered the Mediterranean annually, 7 of them via the Suez Canal unaided. The next most important pathway is Transport - Stowaway: Shipping, while intentional releases from aquaria appear to play an important role. Our results confirm previous findings on the decreasing rate of introductions, which is not affected by the recent expansion of the Suez Canal. Conclusively, the rate of bio invasions via the Suez Canal has not “doubled” as anticipated but rather decreased in relation to previous years. Key words: Alien species, Suez Canal, Internet screening However, a recent study revealed that from 2011 to 2016, the annual rate of MAS introductions in the Mediterranean has decreased regardless of the pathway (ZENETOS et al., 2017). GALIL et al. (2015) claimed that the recent expansion of the Suez Canal could trigger an entirely new twenty first century wave of invasions through a nextgeneration Suez Canal. INTRODUCTION It has been well documented that the Suez Canal is the main pathway of Marine Alien species (MAS) introductions into the Mediterra- nean Sea (POR, 1978; GALIL, 2006; RILOV & GALIL, 2009; ZENETOS et al., 2012; KATSANEVAKIS et al., 2013; NUNES et al., 2013). The aim of the present work is to examine the rate of introductions in relation to the pathway/vector after the latest enlargement of the Suez Canal. The successive enlargements of the Suez Canal have raised concern over increasing propagule pressure resulting in introductions of additional MAS and associated degradation and loss of native populations, habitats and ecosystem services (THORSON, 1971; GALIL et al., 2017). The trend in introduction of alien species via the Suez Canal has been increasing over the last MATERIAL AND METHODS The Google scholar searches were made, decades (ZENETOS et al., 2012; GALIL et al., 2016). with a combination of the key words: new spe- 348 ACTAADRIATICA, 58(2): 347 - 358, 2017 T a ble 1. New MAS reported in the period August 2015 to November 2017. Taxon: F=Fish Mol=Mollusca, Cru=Crustacea, Alg=macroalgae, Cni =Cnidaria, Asc=Ascidiacea, Bry-Bryozoa, Pol=Polychaeta, Dia= Diatoms. In bold, species described from the Mediterranean publication year online/in <ul style="display: flex;"><li style="flex:1">TAXON Species </li><li style="flex:1">Source </li><li style="flex:1">country </li></ul>Tunisia Italy press 2017 2016 2016 coll Year time lapse Date Alg Alg Alg <ul style="display: flex;"><li style="flex:1">(Montagne) A. Gepp & ES Gepp </li><li style="flex:1">Verlaque et al., 2017 </li></ul>Kawai et al., 2016 Hoffman & Wynne, 2016 2015 1960s 2015 2 >50 1 26.07.2015 Avrainvillea amadelpha (Turner) Greville Cutleria multifida <ul style="display: flex;"><li style="flex:1">Børgesen </li><li style="flex:1">Israel </li><li style="flex:1">Dec 2015 </li></ul>Monosporus indicus Halim & Abdel <ul style="display: flex;"><li style="flex:1">Messeih, 2016 </li><li style="flex:1">Asc </li></ul>Bry Bry Cni Cni Cru Cru Cru Cru Cru <ul style="display: flex;"><li style="flex:1">Savigny, 1816 </li><li style="flex:1">Egypt </li></ul>Egypt 1994/2016 2017 1994 2015 2010 2015 2003 2016 2015 2014 2013 2012 02Polyclinum constellatum Calyptotheca alexandriensis Hayward, 2001 Abdelsalam et al., 2017 Sokolover et al., 2016 Yilmaz et al., 2017 Galil et al., 2016 Dec 2015 24.6.2015 Israel Turkey Israel Israel <ul style="display: flex;"><li style="flex:1">2016 </li><li style="flex:1">6</li></ul>Conopeum ponticum <ul style="display: flex;"><li style="flex:1">Gosse, 1853 </li><li style="flex:1">2017 </li><li style="flex:1">2</li></ul>Aequorea vitrina <ul style="display: flex;"><li style="flex:1">Stiasny, 1920 </li><li style="flex:1">2016 </li><li style="flex:1">13 </li></ul>1Cotylorhiza erythraea <ul style="display: flex;"><li style="flex:1">s Chen, 1989 </li><li style="flex:1">Galil et al., 2017 </li><li style="flex:1">2017 </li></ul>Arcania brevifron <ul style="display: flex;"><li style="flex:1">(Randall, 1840) </li><li style="flex:1">Ounifi-Amor et al, 2016 Tunisia </li><li style="flex:1">2015 </li><li style="flex:1">0</li><li style="flex:1"><May 2015 </li></ul>Calcinus latens Grandidierella bonnieroides Stephensen, 1947 (Herbst, 1783) Lo Brutto et al., 2016 Moussa et al., 2016 Marchini et al., 2016 Israel Egypt Italy <ul style="display: flex;"><li style="flex:1">2016 </li><li style="flex:1">2</li></ul><ul style="display: flex;"><li style="flex:1">2015 </li><li style="flex:1">2</li></ul>Halimede ochtodes Ianiropsis serricaudis Gurjanova, 1936 (Poppe, 1889) <ul style="display: flex;"><li style="flex:1">2016 </li><li style="flex:1">4</li></ul>Terbıyık Kurt & Polat, in <ul style="display: flex;"><li style="flex:1">press </li><li style="flex:1">Cru </li></ul>Cru Turkey Turkey 2017 2016 2012 2014 52Pleopis schmackeri <ul style="display: flex;"><li style="flex:1">(Olivier, 1811) </li><li style="flex:1">Patania & Mutlu, 2016 </li></ul>Sicyonia lancifer Fernandez-González & <ul style="display: flex;"><li style="flex:1">Sanchez-Jerez, 2017 </li><li style="flex:1">Cru </li></ul>Dia F<ul style="display: flex;"><li style="flex:1">Bynum & Fox, 1977 </li><li style="flex:1">Spain </li></ul>Croatia Malta Turkey Israel 2016 2017 2016 2016 2017 2010 2015 2014 2015 2017 62210Stenothoe georgiana Nielsen, 1931 Čalić et al., 2017 13.12.2015 Chaetoceros pseudosymmetricus <ul style="display: flex;"><li style="flex:1">(Steindachner, 1881) </li><li style="flex:1">Vella et al., 2016 </li></ul>Gürlek et al., 2016 Fricke et al., in press Abudefduf hoefleri <ul style="display: flex;"><li style="flex:1">F</li><li style="flex:1">(Valenciennes, 1830) </li><li style="flex:1">28.10.2015 </li></ul>Argyrops filamentosus FArnoglossus nigrofilamentosus 05.05.2017 Akel in Stamouli et al., <ul style="display: flex;"><li style="flex:1">in press </li><li style="flex:1">F</li><li style="flex:1">(Cuvier & Valenciennes 1837) </li><li style="flex:1">Egypt </li><li style="flex:1">2017 </li><li style="flex:1">2017 </li><li style="flex:1">0</li></ul>10.08.2017 Bathygobius cyclopterus Evans & Schembri, 2017a Cephalopholis hemistiktos (Rüppell, 1830) Malta Malta Italy 2017 2016 2017 2016 2016 2016 2015 2017 2016 2016 2016 2016 2015 2017 2015 2016 2009 2016 2017 2016 2009 2014 2015 2016 2016 2016 2010 2015 2015 2014 2015 2015 8000720100610301 F<ul style="display: flex;"><li style="flex:1">F</li><li style="flex:1">(Günther, 1859) </li><li style="flex:1">Vella et al., 2016 </li><li style="flex:1">July, 2016 </li></ul>18.2.2017 26.8.2016 Cephalopholis nigri <ul style="display: flex;"><li style="flex:1">F</li><li style="flex:1">Randall & Anderson, 1997 </li><li style="flex:1">Insacco & Zava, 2017 </li></ul>Seyhan et al., 2017 Hata & Motomura, 2016 Çiftçi et al., 2017 Chlorurus rhakoura <ul style="display: flex;"><li style="flex:1">F</li><li style="flex:1">Fricke, 1983 </li><li style="flex:1">Turkey </li></ul>Israel Turkey Israel Israel Turkey Syri a Diplogrammus randalli Encrasicholina gloria Encrasicholina punctifer Epinephelus areolatus F<ul style="display: flex;"><li style="flex:1">F</li><li style="flex:1">Fowler, 1938 </li></ul><ul style="display: flex;"><li style="flex:1">F</li><li style="flex:1">(Forsskål, 1775) </li><li style="flex:1">Rothman et al., 2016 </li></ul>Stern et al., in press Yucel et al., 2017 30.08.2015 11.12.2016 24.1.2016 15.5.2016 FLacepède, 1803 Fistularia petimba Himantura leoparda Leiognathus berbis <ul style="display: flex;"><li style="flex:1">F</li><li style="flex:1">Manjaji-Matsumoto & Last, 2008 </li></ul><ul style="display: flex;"><li style="flex:1">(Valenciennes, 1835) </li><li style="flex:1">F</li><li style="flex:1">Alshawy et al., 2016 </li></ul>Zenetos et al., 2016 <ul style="display: flex;"><li style="flex:1">F</li><li style="flex:1">(Cuvier, 1816) </li><li style="flex:1">Greece </li></ul>Israel Italy Lutjanus sebae <ul style="display: flex;"><li style="flex:1">F</li><li style="flex:1">(Linnaeus, 1766) </li></ul>(Blyth, 1852) Marcelli et al., 2017 Guidetti et al., 2016 02.09.2015 03.08.2015 Paracanthurus hepatus Zebrasoma xanthurum FAslan & Ovalis, 2017 Mol Mol Mol <ul style="display: flex;"><li style="flex:1">T. Cossignani, 1997 </li><li style="flex:1">Turkey </li></ul>Israel Israel Crithe cossinea <ul style="display: flex;"><li style="flex:1">(Rüppell & Leuckart, 1830) </li><li style="flex:1">Halevy et al., 2015 </li></ul>Mienis et al., 2016 24.05.2015 12.11.2015 Goniobranchus obsoletus (Gmelin, 1791) Isognomon legumen Lottia sp. Scuderi & Eernisse, 2016 Jan. 2015 Mol Mol Mol Mol Mol Mol Pol <ul style="display: flex;"><li style="flex:1">Italy </li><li style="flex:1">2016 </li></ul>2015 2017 2015 2017 2017 2016 2015 2012 2016 1986 2016 2016 2015 1<ul style="display: flex;"><li style="flex:1">3</li><li style="flex:1">(Lamarck, 1816) </li><li style="flex:1">Ounifi-Amor et al., 2016 Tunisia </li></ul>Morula aspera <ul style="display: flex;"><li style="flex:1">(Alder & Hancock, 1864) </li><li style="flex:1">Rothman et al., 2017 </li></ul>Mienis & Rittner, 2015 Öztürk et al., 2017 Micali et al., 2017 Goren et al., 2017 Israel Israel Turkey Greece Israel <ul style="display: flex;"><li style="flex:1">1</li><li style="flex:1">05.10.2016 </li></ul>Phidiana militaris Sclerodoris apiculata Varicopeza pauxilla (Alder & Hancock, 1864) (A. Adams, 1855) 29 <ul style="display: flex;"><li style="flex:1">1</li><li style="flex:1">18.08.2016 </li></ul>Sept. 2016 May 2015 <ul style="display: flex;"><li style="flex:1">sp. [cf. </li><li style="flex:1">(Hinds, 1843)] </li><li style="flex:1">1</li></ul><ul style="display: flex;"><li style="flex:1">Viriola </li><li style="flex:1">corrugata </li></ul><ul style="display: flex;"><li style="flex:1">(Lamarck, 1818) </li><li style="flex:1">1</li></ul>Iphione muricata Zenetos.: Progress in Mediterranean bioinvasions two years after the Suez Canal enlargement. 349 cies, first record, marineintroduced species, alien for the species observed/collected after January species, Mediterranean, Suez Canal, Lessepsian. 2015 following the CBD classification (ANONY- In addition, taxonomic studies were screened for MOUS, 2014). mentions of new MAS. Cryptogenic species and questionable cases were not considered. As the exact publication date is not always clear, the literature addressing new marine alien species RESULTS Screening of the internet search results led in the Mediterranean was searched for the period to 44 new alien species reported in the period 2015-2017. Publications in press were also con- August 2015 to October 2017 (Table 1). These sidered while literature published either online belong to: Fish (17 species); Mollusca (9), Aor in a published issue prior to August 15, 2015 Crustacea (8), macroalgae (3), Cnidaria (2), were not taken into account. The year of first Ascidiacea (1), Bryozoa (2), Polychaeta (1), detection was retrieved from each publication. Diatoms (1). Twenty six of these were detected However, the exact date was extracted only for in the period January 2015 to August 2017, of the species detected in the period August 2015 which 19 species appear to have been detected <ul style="display: flex;"><li style="flex:1">to August 2017. </li><li style="flex:1">after August 15, 2015 (Table 2). </li></ul><ul style="display: flex;"><li style="flex:1">For the analysis of the annual rate of intro- </li><li style="flex:1">The countries of first records are in decreas- </li></ul>ductions attributed to the Suez Canal (Lessep- ing order Israel (15 species), Turkey (9), Italy sian immigrants), the pan-European inventory (5), Egypt (4), Malta (3), Tunisia (3), Greece (2), of MAS provided by the European Alien Spe- Spain (1), Croatia (1), Syria (1). <ul style="display: flex;"><li style="flex:1">cies Information Network (EASIN; <a href="/goto?url=http://easin" target="_blank">http://easin. </a></li><li style="flex:1">The time lapse between finding and publica- </li></ul>jrc.ec.europa.eu/) and updated up to March 2017 tion is on average 2.76 years exempting records (EASIN Catalogue version 5.6) was used. The of species hitherto considered as native such as pathway/vector of introduction was assigned the macroalgae Cutleria multifida or overlooked T a ble 2. MAS detected in the period 2015-2017. In bold the species after 15.08.2015. ES=Establishment success: cas=casual, est=established, unk=unknown observation/ collection date Jan. to Aug. 2015 24.06.2015 <ul style="display: flex;"><li style="flex:1">Species </li><li style="flex:1">ES </li><li style="flex:1">Potential pathway </li></ul>est? cas cas est TRANSPORT- STOWAWAY: Ship/boat hull fouling TRANSPORT- STOWAWAY: Ship/ballasts CORRIDORS-Suez canal Lottia sp. Aequorea vitrina Calcinus latens Goniobranchus obsoletus <May 2015 <ul style="display: flex;"><li style="flex:1">24.05.2015 </li><li style="flex:1">CORRIDORS-Suez canal </li></ul>unk est cas May 2015 26.07.2015 03.08.2015 CORRIDORS-Suez canal TRANSPORT- STOWAWAY: other RELEASE IN NATURE: Other intentional release Iphione muricata Avrainvillea amadelpha Zebrasoma xanthurum Epinephelus areolatus Paracanthurus hepatus cas cas 30.08.2015 02.09.2015 CORRIDORS-Suez canal RELEASE IN NATURE: Other intentional release Argyrops filamentosus Isognomon legumen cas est unk est est cas cas cas cas cas cas 28.10.2015 12.11.2015 13.12.2015 Dec. 2015 Dec. 2015 24.01.2016 July 2016 CORRIDORS-Suez canal CORRIDORS-Suez canal Chaetoceros pseudosymmetricus Monosporus indicus TRANSPORT- STOWAWAY: Ship/ballasts TRANSPORT- STOWAWAY: Ship/boat hull fouling CORRIDORS-Suez canal Calyptotheca alexandriensis Himantura leoparda CORRIDORS-Suez canal Cephalopholis nigri RELEASE IN NATURE: Other intentional release CORRIDORS-Suez canal Leiognathus berbis 15.05.2016 26.08.2016 Sept. 2016 18.08.2016 Diplogrammus randalli Viriola sp. [cf. corrugata ] Varicopeza pauxilla CORRIDORS-Suez canal CORRIDORS-Suez canal CORRIDORS-Suez canal Phidiana militaris Arcania brevifrons Fistularia petimba cas unk est 05.10.2016 11.12.2016 11.12.2016 CORRIDORS-Suez canal CORRIDORS-Suez canal CORRIDORS-Suez canal Chlorurus rhakoura Arnoglossus nigrofilamentosus Bathygobius cyclopterus cas cas cas 18.02.2017 05.05.2017 10.08.2017 TRANSPORT- STOWAWAY: Shipping CORRIDORS-Suez canal CORRIDORS-Suez canal 350 ACTAADRIATICA, 58(2): 347 - 358, 2017 because of their similarity to natives. The period between detection and publication drops to 0.73 year for species observed in the 2015-2017 period. Based on the results of Table 2, the 19 species reported in the 2 years period correspond to a rate of 9.5 new species per year, regardless of the pathway of introduction. Suez Canal is suspected responsible for seven per year, while shipping and Aquarium trade appear to be responsible for the introduction of the rest. cies (ABDEL-SALAM, TAYLOR, & DORGHAM, 2017). 2. The fish Encrasicholina gloria was described from the Persian Gulf (Khasab, Oman), the Red Sea (Egypt and Saudi Arabia) and the eastern Mediterranean (Israel) (HATA & MOTOMURA, 2016). The distribution of specimens in the Mediterranean is considered to represent a Lessepsian migration. 3. The fish Arnoglossus nigrofilamentosus was described from four specimens collected in the southeastern Mediterranean near Tel-Aviv, Israel (FRICKE et al., 2017). Though the species has not yet been observed in the northern Red Sea, it probably originates from the Gulf of Suez, so this finding represents a probable new case of Lessepsian migration. DISCUSSION Most of the internet search results addressed local or review studies. Some new records referredtonewspeciesforsciencedescribedfrom the Mediterranean i.e. the fish Diplecogaster umutturali Bilecenoğlu et al, 2017 in Turkey; some to Atlantic species extending their distribution range i.e the sea star Luidia atlantidea Madsen, 1950 in Spain reported by GALLARDO- ROLDAN et al. (2015); while a lot more included species whose alien or native status is debatable and should be provisionally classified as cryp- togenics i.e. the sea star Coronaster briareus (Verrill, 1882) in Malta (EVANS et al., 2017) and many others. Two fish species reported as aliens in the study period were excluded as misidentifica- tions: Pomacanthus asfur (Forsskål, 1775) reported by DEIDUN & BONNICI in KARACHLE et al., 2016, refuted by EVANS & SCHEMBRI (2017b), as misidentification of Pomacanthus imperator (Bloch, 1787), and/or questionable cases such as the fish Plectorhinchus gaterinus (Forsskål, 1775) reported by CORSINI-FOKA & SARLIS (2016) with reservation. Among the 44 validated newly reported species as MAS are three species described in the Mediterranean. These are: 1. The bryozoan Calyptotheca alexandrien- siswhosecolonies began to appear in the Eastern Harbour of Alexandria, Egypt in December 2015. The species was identified as belonging to the predominantly IndoPacific cheilostome genus Calyptotheca Harmer, 1957 and described as a new spe- The reports of most MAS detected after August 2015 are based on casual records, while the following five species are established, as follows: 1. Calyptotheca alexandriensis: The bryozoan exhibits intensive growth sporadically on different hard substrata, including rocks, submerged concrete walls, ropes, ships’ hulls, and metal pipes supporting marina piers in Alexandria (ABDELSALAM et al., 2017) 2. Isognomon legumen: the first record of this mollusk in Israel was based on an empty shell (MIENIS et al., 2016). However subsequent findings in Greece MICALI et al. (2017); ANGELIDIS in LIPEJ et al. (2017) as Malleus regula (Forsskål in Niebuhr, 1775) confirm its establishment success in the eastern Med- iterranean (CROCETTA et al., 2017). 3. Monosporus indicus: this epiphytic red alga has established healthy populations in the warm Levant Mediterranean Sea of Israel (HOFFMAN & WYNNE, 2016). 4. Avrainvillea amadelpha: This alga was common and was growing gregariously in colonies, between 20-22 m depth, in sunny places (sub-horizontal substrates), in Cymo- docea nodosa (Ucria) Ascherson meadows, Posidonia oceanica beds, on dead mattes of P. o ceanica meadows and coarse sand bot- toms (VERLAQUE et al., 2017). Zenetos.: Progress in Mediterranean bioinvasions two years after the Suez Canal enlargement. 351 5. Fistularia petimba: following the first find- Canal enlargement. In fact only 7 species per year seem to enter via the Suez Canal after the latest enlargement (Table 2), a figure less than in previous decades. This figure will substantially increase as new records will be published in the following months/years that may have been detected during the study period, although the time lapse between detection and publication of an alien species has dropped significantly over the last decade (results not shown here). ing in of this cornet fish in December 2011, off the coast of Ashdod, five additional juve- nile specimens of F . p etimba were caught on November 26, 2017, in the southern coast of Israel, from a shallow depth of 20m. This finding confirms the establishment of this species along the Israeli Mediterranean coast

Progress in Mediterranean Bioinvasions Two Years After the Suez Canal Enlargement

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