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Home , Cranchia scabra, Cranchiinae, Cycloteuthidae, Cycloteuthis, Cycloteuthis sirventi, Megalocranchia

ISSN: 0001-5113 ACTA ADRIAT., REVIEW PAPER AADRAY 61 (2): 113 - 134, 2020

Non-indigenous in the : a review

Giambattista BELLO1, Franco ANDALORO2 and Pietro BATTAGLIA3

1 Via C. Colombo 34, 70042 Mola di Bari, Italy

2 SZN, Stazione Zoologica Anton Dohrn, Centro Interdipartimentale della Sicilia, Lungomare Cristoforo Colombo 4521, 90149 Palermo, Italy

3 SZN, Stazione Zoologica Anton Dohrn, Centro Interdipartimentale della Sicilia, Villa Pace, Contrada Porticatello 29, 98167 Messina, Italy

*Corresponding author, e-mail:[email protected], [email protected]

The present review critically assesses the records of cephalopods that have entered the Mediterranean Sea in the last few decades. It includes 13 species, namely Sepia dollfusi, leucoptera, Sepioteuthis lessoniana, Architeuthis dux, , pavo, sp., megalops, sirventi, Taningia danae, Octopus cyanea, Amphioctopus sp. and Tremoctopus gracilis. The presence of Sepia pharaonis needs to be confirmed, whereas that of Sepia gibba and Spirula spirula is excluded. The arrivals from the through the Strait of Gibraltar are related to the entrance surface current, which either carried passively planktonic paralarvae or favoured in some other way the entrance of subadult and adult stray specimens. As a matter of fact, all Atlantic cephalopods are pelagic oegopsid , with the exception of the nekto-benthic sepiolid S. leucoptera; all of them have been found only in the western Mediterranean basin. None of them seemingly established a stable population there, apart the latter species. On the contrary, the cephalopods entering the Mediterranean from the Red Sea through the Suez Canal (Lessepsian migrants) lead a benthic mode of life. At least two of them, namely S. lessoniana and Amphioctopus sp., set up stable populations in the eastern basin. Lastly the occurrences of the pelagic octopod T. gracilis are ascribed, in the literature, to human-mediated transfer.

Key words: , Cephalopoda, exotic species, Lessepsian migrants, cryptic species

INTRODUCTION change (THIÉBAULT et al., 2016), resource over- exploitation (e.g. VASILAKOPOULOS et al., 2014; In recent years, the invasion of Mediterrane- TSIKLIRAS et al., 2015), pollution (e.g. DANOVARO, an by non-indigenous species (NIS) has 2003; FOSSI et al., 2018) and other anthropogenic represented a growing and concerning problem stressors (e.g. DURRIEU DE MADRON et al., 2011) because of their impact on marine ecosystems. is threatening the equilibrium of Mediterra- The introduction of NIS together with climate nean ecosystems and its biodiversity. Recent 114 ACTA ADRIATICA, 61 (2): 113 - 134, 2020 reviews have recorded the presence of little less tively (see Results). However, the first monitor- than a thousand NIS in the Mediterranean Sea ing experiences on NIS in the Mediterranean (BONANNO & ORLANDO-BONACA, 2019; ROTTER Sea paid little attention to the presence of alloch- et al., 2020). NIS have entered this basin either thonous cephalopods. For instance, the CIESM through one of its two openings, i.e. the Strait Atlas of Exotic Molluscs in the Mediterranean of Gibraltar and the Suez Canal, or by other (ZENETOS et al., 2004) and its web updates did not pathways depending on anthropic transport (e.g. mention any species belonging to Cephalopoda. shipping, aquaculture, aquarium trade, live food/ In this respect, the ISPRA project Identification bait trade, colonized floating man-made objects) and distribution of non-indigenous species in or other human-mediated causes (ROTTER et al., Italian Seas represented the first opportunity 2020). A closer attention has been paid to the to provide an overall revision of allochthonous entrances from the Red Sea via the Suez Canal, Mediterranean cephalopods (ANDALORO, 2011; which date since its man-made opening in 1869 ANDALORO et al., 2012). Today, in light of pre- (GALIL, 2007). The recent enlargement of this vious considerations, an update of the current canal has further accelerated and facilitated the status of non-indigenous cephalopods in the introduction of Red Sea species into the Medi- Mediterranean basin is definitely required. terranean Sea (GALIL et al., 2015, 2017; QUEIROZ & Therefore, the main aim of the present paper POOLEY, 2018). is to review and discuss the matter of non-indig- Only a fraction of these species is capable of enous cephalopods sensu lato in the Mediter- spreading, settling and establishing stable popu- ranean Sea; that is to say all species recorded in lations in the Mediterranean Sea (SERVELLO et the last few decades irrespective of their origin. al., 2019), whereas other invasions are limited to some areas near their basin of origin, as in the HISTORICAL OVERVIEW case of molluscan pseudo-populations in the Alboran Sea described by BOUCHET & TAVIANI As mentioned in the Introduction, allochtho- (1992). Since the ’90s the phenomenon of NIS nous cephalopods have three ways to enter the arrivals was seemingly accelerated because of Mediterranean basin: i) crossing the only natural the warming up of the Mediterranean waters, passage, the Strait of Gibraltar, from the Atlantic which has favoured the entrance and survival Ocean; ii) passing through the Suez Canal from of mainly tropical and sub-tropical fauna and the Red Sea; iii) being transported by humans in flora elements (ANDALORO & RINALDI, 1998; various ways (ROTTER et al., 2020) from anywhere THIÉBAULT et al., 2016). in the world oceans. As the opening of the Suez As regards Cephalopoda, apparently no NIS Canal is dated to comparatively recent times had been recorded in the Mediterranean up to (1869), the first colonization of the Mediter- the ’80s: MANGOLD & BOLETZKY (1988) reported ranean by Atlantic cephalopods (as well as all no exotic in their review. How- other taxa) through the Gibraltar opening has ever, it was afterwards shown that allochthonous been dated back to the aftermath of the Messin- cephalopods had been already collected, though ian salinity crisis, which was not survived by misidentified, in the Mediterranean Sea as early any Mediterranean cephalopods (MANGOLD & as the middle ’30s (MIENIS, 2005; ORSI RELINI et BOLETZKY, 1988). The present Mediterranean al., 2009). biodiversity, including its teuthodiversity, origi- In the last two decades, the occurrence of nated when the Strait of Gibraltar re-opened non-indigenous cephalopods in the Mediterra- to the ocean waters and their load of living nean has been recognized not to be at all negli- organisms during the Zanclean flood (5.3 MYA) gible, thanks to the increasing attention on both (BLANC, 2002). In the following ages, several Atlantic and Lessepsian migrant species, above speciation events occurred within the Mediter- all by Spanish and Italian scientists as well as ranean Sea, through which new cephalopod Greek, Turkish and Israeli researchers, respec- species were born (BELLO, 2003, 2019). Obviously, Bello et al: Non-indigenous species of cephalopods in the Mediterranean Sea: a review 115 the timing of Mediterranean colonization by so that the checklist includes now 13 document- individual species is not known. What is known ed species. In addition, three more species have is that this basin was colonized by cephalopods been reported whose Mediterranean presence of both Mauretanic (i.e. warm) and Lusitanic was not sufficiently supported. (i.e. temperate) affinities, most probably in dif- ferent periods (BELLO, 2003). The process of the MATERIAL AND METHODS entrance and establishment of Atlantic species in the Mediterranean has seemingly occurred Information on the Mediterranean non-indig- through all the time since the opening of the enous cephalopods was gathered from the avail- Gibraltar gate in the post-Messinian period able literature. and is still occurring. Hence, it may be rather In this paper the following terminology was difficult, in some cases, to decide whether an used: Atlantic cephalopod, newly discovered in the § Geographical distribution outside the Medi- Mediterranean, is actually a recently arrived terranean: current geographical distribution species or just one previously overlooked. This outside the Mediterranean. is particularly true for those cephalopods that § First Mediterranean documented occurrence: escape most common sampling devices and date and place of first occurrence (the first man’s notice, mostly because of their fully documented occurrence may not coincide pelagic mode of life as well as for other reasons, with the first literature record). including their poorly explored habitat, their § First Mediterranean literature record: first diminutive size and lack of commercial interest. piece of literature recording the Mediterrane- To the purpose of assembling a list of the an occurrence of the NIS, whether correctly non-indigenous cephalopods sensu lato found identified or not, together with the year and in the Mediterranean, while taking into account place of occurrence. the just mentioned caveats, we set as a baseline § Notes on the species: additional available the cephalopod catalogue by BELLO (1986), who information on the biology and ecology of critically reviewed all previous Mediterrane- the NIS, as well as taxonomic comments an cephalopod records. Accordingly, SÁNCHEZ when pertinent. (1985) was the first one to document a non-indig- § NIS category: whether the entrance into enous cephalopod, an early juvenile Teuthowe- the Mediterranean was due to natural range nia megalops collected in the Balearic Sea and expansion or was human-mediated. deemed of Atlantic origin. Few years later, a § Status: whether established or not. second purported Atlantic cephalopod species, , was caught in the west- Definitions of the terms used in the present ern basin (ORSI RELINI & MASSI, 1991). As for paper: Lessepsian cephalopod, the first one, “Octopus § NIS a non-indigenous species sensu RELINI aegina”, was reported in the year 1999 (SALMAN (2008); it includes cephalopods originating et al., 1999). from either the Red Sea through the Suez However, it became evident later that some Canal (Lessepsian species) or anthropic non-indigenous cephalopods, namely Amphioc- causes (including climate warming) or recent topus “aegina” and Tremoctopus gracilis, had range expansion from the Atlantic Ocean. been collected in the Mediterranean Sea as early § Vagrant: an Atlantic species found only once as in the years 1934 and 1936, respectively, or very few times in the Mediterranean Sea. but had been misidentified (MIENIS, 2005; ORSI § Lessepsian: Red Sea/ species RELINI et al., 2004). that entered the Mediterranean Sea through Afterwards several other exotic cephalopods the Suez Canal. were recorded in Mediterranean waters, coming § Human-mediated: directly or indirectly car- from either the Atlantic Ocean or the Red Sea, ried by man. 116 ACTA ADRIATICA, 61 (2): 113 - 134, 2020

§ Cryptogenic: “a species that is not demon- S. dollfusi was expected to enter the Mediter- strably native or introduced” (CARLTON, 1996: ranean basin. 1653). § Established: a NIS that originated a self- Stoloteuthis leucoptera (Verrill, 1878) sustaining population. (Decapodiformes: Sepiolida: : Het- § Questionable NIS: a NIS whose presence eroteuthinae) in the Mediterranean Sea is not sufficiently § Geographical distribution outside the Medi- warranted. terranean: subtropical and temperate amphi- Atlantic, from the Gulf of St. Lawrence to the The supra-systematics adopted in this paper Straits of Florida in the western side of the is that proposed in ALLCOCK et al. (2014). As for ocean and from the to Namibia the nomenclature, we followed that of the Italian in the eastern side, also in the southern Indian checklist of marine species (BELLO, 2017a). Ocean (REID & JEREB, 2005; VECCHIONE & YOUNG, 2013). RESULTS § First Mediterranean documented occurrence: 1986, north of Gorgona Island, Non-indigenous cephalopods (VOLPI et al., 1995). § First Mediterranean literature record: 1988, Here below the non-indigenous cephalopods Ligurian Sea (ORSI RELINI & MASSI, 1991). reported in the Mediterranean Sea are listed fol- § Notes on the species: bentho-pelagic small- lowing a systematic order. The overall system- sized sepiolid, living in the lower sublittoral atic list is reported in Table 1. and upper bathyal, from 160 to 700 m (REID & JEREB, 2005). Sepia dollfusi Adam, 1941 (Decapodiformes: § NIS category and status: natural range expan- Sepiida: Sepiidae) sion from the Atlantic Ocean or native; estab- § Geographical distribution outside the Medi- lished. terranean: Red Sea and southern part of Suez The specimens first reported in the literature Canal (REID et al., 2005); according to NESIS were found in the Ligurian Sea: one male, ML (1987), it is widely distributed in the Indo- = 11.5 mm, collected by IKMT (Isaacs-Kidd Pacific. Mid- Trawl) at 270-400 m of depth off § First Mediterranean documented occurrence Ventimiglia (Liguria), and two juveniles, ML = and literature record: 2014, at 100 m depth 8.5 and 9.5 mm respectively, trawled at 250 m of off Alexandria (Egypt), eastern Mediterra- depth off Sestri Levante (Liguria). However, one nean Sea (RIAD, 2015). specimen of this species had been collected two § Notes on the species: a small-sized , years earlier, in summer 1986, by trawling at reaching about 15 cm ML ( length) 461 m depth north of Gorgona Island, Ligurian (GABR et al., 1998). It occurs in benthic habitats Sea; it was a male, 18 mm ML (VOLPI et al., 1995). of the neritic zone (GABR et al., 1998), down to A range extension of this sepiolid was noted about 100 m (RIAD, 2015). shortly after: one specimen netted off the Gulf § NIS category and status: Lessepsian; not of Naples () on the sea bottom established. at 387 m depth, during one of the 1990-92 The only specimen collected was a female autumn bottom trawl surveys (WÜRTZ et al., 1995); measuring 12.2 cm ML, caught by trawling dur- GIORDANO & CARBONARA (1999) reported the ing commercial fishing operations. capture of one specimen in the Gulf of Naples This cephalopod is well known in the Suez during the 1990-95 bottom trawl surveys, which Canal where it established a thriving popula- might be the same specimen reported by WÜRTZ tion that represents a main target for the canal et al. (1995); 13 additional specimens have been fishery (GABR et al., 1998). Therefore, in a sense, collected on bathyal grounds of the Tyrrhe- Bello et al: Non-indigenous species of cephalopods in the Mediterranean Sea: a review 117

Table 1. Check-list of non-indigenous cephalopods recorded in the Mediterranean Sea. Origin: AO = Atlantic Ocean; RS = Red Sea; HT = human-mediated transport. Status: S = Stray specimen(s); E = Established; C = Cryptogenic

Taxon Species Origin Status References DECAPODIFORMES

Sepiida Sepia dollfusi Sepiidae RS S riad (2015) Adam, 1941

Sepiolida orsi relini & massi (1991); volpi et al. (1995); voliani (pers. comm.); orsi relini (pers. comm.); würtz et al. Stoloteuthis (1995); sanchez et al. (1998); giordano Sepiolidae leucoptera (Verrill, AO C & carbonara (1999); biagi et al. (2002); 1878) corsini-foka et al. (2010); cuccu et al. (2010); fanelli et al. (2012); quetglas et al. (2013); zaragoza et al. (2015); keller et al. (2017)

Myopsida salman & katağan (2002); mienis (2004); riad (2008); lefkaditou et al. Sepioteuthis (2009); tzomos et al. (2010); waheed & Loliginidae lessoniana Férussac, RS C gareb (2010); hattour (2011); crocetta 1830 et al. (2014); shakman et al. (2017); ammar & maaroof (2019); dragičević et al. (2019); katsanevakis et al. (2020)

Oegopsida gonzález et al. (2000); guerra (2006); Architeuthis dux Architeuthidae AO S bustamante et al. (2008); anonymous Steenstrup, 1857 (2020)

Cranchia scabra quetglas et al. (1999); zaragoza et al. AO S Leach, 1817 (2015) Megalocranchia sp. (cf. maxima Pfeffer, AO S bello & biagi (1999) 1884) AO S quetglas et al. (2013) (Lesueur, 1821) (Prosch, AO S sánchez (1985) 1849)

Cycloteuthis sirventi AO C guerra (1992; pers. comm.) Joubin, 1919

Taningia danae Octopoteuthidae AO S quetglas et al. (2006) Joubin, 1931

OCTOPODIFORMES

Octopoda Octopus cyanea Octopodidae RS E? mienis (2003a) Gray, 1849 Amphioctopus sp. RS E salman et al. (1999, 2005); mienis (2005)

Tremoctopus kramer (1937); belluscio et al. (2003); Tremoctopodidae gracilis (Eydoux & HT? E? orsi relini et al. (2004); rifi & ben Souleyet, 1852) souissi (2014) 118 ACTA ADRIATICA, 61 (2): 113 - 134, 2020 nian Sea, from November 1992 to July 2002 To sum up, the present Mediterranean range (one reported by SANCHEZ et al. (1998); 12 by of S. leucoptera extends in the western basin, VOLIANI (pers. comm.)). Several others were net- from the Alboran and Catalan Seas to the Ligu- ted in the Ligurian Sea in the last twenty years rian and Tyrrhenian Seas. (ORSI RELINI, pers. comm.). The species was also The hypothesis that S. leucoptera, some dec- recorded in Sardinian waters by CUCCU et al. ades ago, naturally entered the western Mediter- (2010): one specimen, ML = 10.4 mm, caught ranean Sea from the Atlantic Ocean through the on June 2005 in the western Tyrrhenian Sea at Straits of Gibraltar is supported by several ele- 550 m depth; the other, ML = 14.5 mm, caught ments: many individuals of the species collected in February 2007 in the Gulf of Cagliari at the in the northwest basin only since the ’80s of the depth of 360 m. Both of them were ripe females, last century, its progressive range expansion to the larger one was mated; they were the first the west side of the Tyrrhenian Sea where it had females recorded in the Mediterranean. In addi- not been found before (CUCCU et al., 2010), and tion to the several specimens of S. leucoptera the small size coupled with a bentho-pelagic collected in Italian seas, i.e. the Ligurian and mode of life, i.e. the likelihood to be carried by Tyrrhenian Seas, SANCHEZ et al. (1998) reported currents over long distances. On this respect it one individual caught in the Catalan Sea on Feb- must be pointed out that some areas of the west- ruary 1996, at 357 m depth, and QUETGLAS et al. ern Mediterranean Sea had been extensively (2013) provided information on the catch of 25 surveyed for cephalopods in the last century (cf. specimens (ML range: 10-25 mm) in the west- MANGOLD & BOLETZKY, 1988), specifically for ern Mediterranean (Alboran Sea and Balearic Sepiolidae (NAEF, 1923). Islands) from 1994 to 2010, within the depth Nevertheless, the hypothesis that the Medi- range 324-612 m. According to QUETGLAS et al. terranean Stoloteuthis species is a cryptogenic (2013), biological information was available for entity cannot be discarded (FERNÁNDEZ-ÁLVA- only 13 individuals: nine immature females and four males (two mature and two maturing indi- REZ, pers. comm.). The latter hypothesis is sup- viduals) caught during May. Other individuals ported by both its diminutive size and the fact caught off the Balearic Islands were reported by that deep fishing grounds, where it lives, started FANELLI et al. (2012), who estimated the species to be regularly explored only in the last half of standardised total abundance, 0.25 individuals · a century. Moreover, the water column, where ha-1, and biomass, wet weight 0.5 g · ha-1, at the this heteroteuthine preferentially lives, has been depth of 800 m. In the same location, ZARAGOZA scantly investigated all over the western basin. et al. (2015) caught one specimen by bongo net at The only unquestionable piece of informa- 55 m depth. tion is that this species has an established self- In summary, all of the above-mentioned sustained population in the western Mediter- specimens of S. leucoptera were caught by ranean Sea, as shown by its many records that bottom trawling, with the exception of two include fully mature males and females. individuals caught by plankton nets in midwater (VOLPI et al., 1995; ZARAGOZA et al., 2015). There- Sepioteuthis lessoniana Férussac, 1830 fore, despite the members of the subfamily Het- (Decapodiformes: Myopsida: Loliginidae) eroteuthinae are generally deemed pelagic, S. § Geographical distribution outside the Medi- leucoptera is considered bentho-pelagic (REID terranean: a species-complex inhabiting the & JEREB, 2005). However, as shown by the rare tropical Indo-Pacific Ocean, from Hawaii to reported catches in epipelagic (ZARAGOZA et al., the Red Sea and the south-eastern African 2015) and mesopelagic waters (VOLPI et al., 1995), coast (nesis, 1987; jereb et al., 2010). this species may have a wider bathymetric dis- § First Mediterranean documented occur- tribution in the water column, which is possibly rence and literature record: 2002, Gulf of underestimated because of the paucity of studies İskenderun, Turkey (Levant Sea) (SALMAN & investigating midwaters. KATAĞAN, 2002). Bello et al: Non-indigenous species of cephalopods in the Mediterranean Sea: a review 119

§ Notes on the species: medium-sized benthic Montenegro, southern Adriatic Sea) in Decem- , males larger than females (maximm ber 2015; incidentally, this is its northernmost ML: 42 and 38 cm, respectively); weight to record (dragičević et al., 2019). about 2 kg; it occurs in coastal environments, As for the African specimens, RIAD (2008) from the surface to about 100 m depth (JEREB described the morphology of the female S. les- et al., 2010). The nominal species S. lessoniana soniana based on specimens obtained from the – locality: New Guinea (LESSON, 1830), artisanal fishery (trammel net) based in Alexan- traditionally reported to live in a wide geo- dria (Egypt, Levant Sea) and WAHEED & GAREB graphical range in the tropical Indopacific (2010) studied the morphology, digestive and Ocean (NESIS, 1987) – represents indeed a reproductive systems of an unreported number species complex (SEGAWA et al., 1993; NOR- of male individuals caught off the rocky coast MAN, 2000; JEREB et al., 2010). Accordingly, the of Abu Qir (Egypt, Levant Sea). The specimen identity of the Mediterranean specimens to S. reported by HATTOUR (2011) came from commer- lessoniana should be validated; in fact, theo- cial trammel-net catches in central eastern coast retically, they might be found to belong to a of Tunisia, at 8-10 m depth. The one recorded species other than S. lessoniana in the future. by SHAKMAN et al. (2017) off Tripoli (Libya) was § NIS category and status: Lessepsian; estab- caught at about 10 m depth by an angler using lished. jigging technique and measured 170 mm ML. The specimen reported by SALMAN & Several recent additional records of S. lesso- KATAĞAN (2002), unsexed, 25.2 cm ML and niana have been reported in the eastern Mediter- 770 g weight, was found in littoral waters. In ranean Sea (CORSINI-FOKA et al., 2010; CROCETTA the following years, a few more individuals et al., 2014; AMMAR & MAAROOF, 2019; KATSANE- of this loliginid squid were collected in the VAKIS et al., 2020). AMMAR & MAAROOF (2019) Levant and Aegean Seas: an individual film- collected two specimens (15.5 and 17.9 cm ML) recorded in shallow waters off Achziv (Israel) off the Syrian coasts by bottom trawl fishery, in spring 2004 (MIENIS, 2004); two males caught whereas both CROCETTA et al. (2014) and KAT- in 2009, one 196 mm ML / 356 g by hook-and- SANEVAKIS et al. (2020) reported several speci- line, the other 244 mm ML / 522 g by trammel mens observed underwater, in the upper 6 m net respectively, from the waters of Rhodes depth. CROCETTA et al. (2014) referred the obser- (Greece) (LEFKADITOU et al., 2009); one or more vation of nine individuals along the Lebanese specimens, ML = 32 cm, fished in Cyprus in coast, and KATSANEVAKIS et al. (2020) recorded 2009 (TZOMOS et al., 2010). more than 100 individuals from Lebanon, 15 According to the published literature, S. les- from Greece and 15 from Cyprus. soniana appears to have initially spread all along This squid has established a stable popula- the eastern and northern coasts of the Levant tion in the Levant Sea in less than twenty years Sea, including Cyprus, and to have entered the since its first record by SALMAN & KATAĞAN Aegean Sea from its easternmost access, i.e. the (2002), to the extent that it is commercial- Rhodes Strait. LEFKADITOU et al. (2009) drew a ly exploited (CORSINI-FOKA et al., 2010). For map of the possible pathway followed by this instance, in Cyprus the ‘new’ squid is regularly squid to reach both the southern side of Rhodes found in fish markets (TZOMOS et al., 2010) and (Levant Sea) and its northern side (Aegean Sea) in Rhodes it was even given its own vernacular from its Mediterranean entrance site at Port term, i.e. soupiocalamaro (= cuttlefish-squid) Said. Later, this species has been recorded along by local fishermen (LEFKADITOU et al., 2009). the Mediterranean African coasts, in Egypt It is evident that S. lessoniana, which thrives (RIAD, 2008; WAHEED & GAREB, 2010), Tunisia in shallow warm waters throughout its range, (HATTOUR, 2011) and Libya (SHAKMAN et al., found a suitable environment in the Levant Sea 2017). Recently, it also reached the Adriatic Sea: thanks to its comparatively high temperatures, one specimen caught near Ploče beach (Budva, the highest in the Mediterranean. Furthermore, 120 ACTA ADRIATICA, 61 (2): 113 - 134, 2020 the hatchling size (mean total length > 5 mm) Algeciras (Andalusia) in 2012 (ANONYMOUS, and robustness, as well as its high grow rate (> 2020). The fourth specimen was a male trawled 12% body mass/day, in the first 100 days) make at 450 m off Gandia (Gulf of Valencia) in 2005 S. lessoniana early juveniles unique among (BUSTAMANTE et al., 2008), that is far away from teuthids, since they are independent from cur- the Strait of Gibraltar. To sum up, four giant rents, i.e. they leave the planktonic mode of life squids have been recorded in the Mediterranean within two weeks (LEE et al., 1994). Moreover, Sea. larger hatchlings benefit of reduced mortal- When the first specimen was found ity rates. All such features may slow down the (GONZÁLEZ et al., 2000), it was hypothesized to population range expansion; on the other hand, have entered the Mediterranean Sea through though, they favour the establishment of new the Gibraltar Strait carried by the surface cur- populations from a few specimens by reducing rents when already moribund (as for the over- to a great extent the early juveniles spreading all Mediterranean current pattern cf. MILLOT & over a too wide area. TAUPIER-LETAGE, 2005). Indeed, several A. dux This loliginid squid is utilized both in bio- specimens have been found in a bad condi- medical research (LEE et al., 1994) and for human tion, floating on the surface of all oceans (e.g. consumption; the latter use is being practiced in ANONYMOUS, 2020), which may be linked to its Greek islands (LEFKADITOU et al., 2009; TZOMOS aversion to comparatively warm surface waters et al., 2010). because of its respiratory physiology (BRIX, 1983). However, the capture of a healthy male Architeuthis dux Steenstrup, 1857 (Decapo- in the Gulf of Valencia compels to reconsider diformes: : Architeuthidae) the hypothesis that only dying individuals cross § Geographical distribution outside the Medi- the Strait of Gibraltar coming from the Atlantic terranean: worldwide oceanic in tropical and Ocean or, else, individuals that enter the Medi- temperate waters (ROPER & JEREB, 2010a). terranean become moribund (see also GUERRA & § First Mediterranean documented occurrence SEGONZAC, 2014). Since no giant squid was ever and literature record: 1997, Fuengirola, Spain found elsewhere in the Mediterranean, it may be (Alboran Sea) (GONZÁLEZ et al., 2000). These deemed that this species does not form a stable authors recorded the specimen as Architeu- population in this sea. this sp.; it was shown afterwards that all architeuthid squids belong to the only species Cranchia scabra Leach, 1817 (Decapodi- A. dux, which is distributed worldwide (WIN- formes: Oegopsida: Cranchiidae: ) KELMANN et al., 2013). § Geographical distribution outside the Medi- § Notes on the species: gigantic oceanic squid, terranean: circumglobal in tropical and sub- epipelagic to mesopelagic and bathyal tropical open oceanic waters (ROPER & JEREB, (ROPER & JEREB, 2010a). 2010c). § NIS category and status: vagrant, sporadi- § First Mediterranean documented occur- cally entering from the Atlantic Ocean. rence and literature record: 1998, in Balear- The giant squid recorded by GONZÁLEZ et al. ic waters, south-west of Mallorca (western (2000) was found stranded on the beach. It was a Mediterranean Sea) (QUETGLAS et al., 1999). female approaching sexual maturity, 149.5 cm § Notes on the species: small squid living in ML and 104 kg body mass (tentacles missing the water column, from the epipelagic to the and body damaged). Subsequently, the occur- bathypelagic zone (ROPER & JEREB, 2010c). rence of four additional specimens was docu- § NIS category and status: vagrant. mented in the western Mediterranean. Two of The first specimen recorded was collected by them were found in the Alboran Sea: a female bottom trawling between 506 and 769 m depth. trawled at 400 m off Malaga, 2001 (GUERRA et It measured 102 mm ML (sex undetermined al., 2006) and another female washed ashore near because of its bad condition); according to its Bello et al: Non-indigenous species of cephalopods in the Mediterranean Sea: a review 121 size, it was an adult or a subadult. A second (2010c), there are at least three species in record of C. scabra was reported by ZARAGOZA this : M. maxima Pfeffer, 1884 in the et al. (2015), a caught by bongo net in southern Atlantic and Indian oceans and NW the western Mediterranean Sea at 150 m depth. Pacific Ocean, M. oceanica (Voss,1960) in Both specimens may be considered stray speci- the North Atlantic Ocean, M. fisheri (Berry, mens that entered the Mediterranean from the 1909) in the central North Pacific Ocean. Atlantic Ocean. § First Mediterranean documented occurrence and literature record: 1993, off Gorgona Taonius pavo (Lesueur, 1821) (Decapodi- Island, Ligurian Sea (western Mediterranean formes: Oegopsida: Cranchiidae: ) Sea) (BELLO & BIAGI, 1999). § Geographical distribution outside the Medi- § Notes on the species: paralarvae and early terranean: in the Atlantic Ocean from about juveniles are epipelagic; juveniles and sub- 45° N to the Southern Subtropical Con- adults progressively descend to more than vergence and in the SW portion of the 2,000 m depth; adults are very large as the Indian Ocean (ROPER & JEREB, 2010c). OKU- generic name suggests. TANI (2015) reports it also in west Australian § NIS category and status: vagrant. waters and in the Pacific Ocean, E to Japan. The only specimen of this genus ever collect- § First Mediterranean documented occurrence ed in the Mediterranean was a large one (weight and literature record: 1998, Gulf of Lion = 86 kg; conservative estimated ML = 1.70 m), (western Mediterranean Sea) (QUETGLAS et most probably an adult. Only a photograph doc- al., 2013). umented its capture, according to whose exami- § Mode of life and habitat: medium-large squid nation it was tentatively ascribed to either Gali- living in the water column, from the epipe- teuthis sp. or, more probably, Megalocranchia lagic zone to 2,000 m and deeper (ROPER & sp. (BELLO & BIAGI, 1999). Afterwards, the late JEREB, 2010c). Kir Nesis assigned this specimen to the latter § NIS category and status: vagrant, sporadi- genus (NESIS, pers. comm. to GB). According to cally entering from the Atlantic Ocean. both its size and fin shape, the Mediterranean QUETGLAS et al. (2013) mention three speci- mens (ML = 97, 106, 173 mm) netted by a com- specimen might belong to M. maxima (cf. ROPER mercial trawler in the Gulf of Lion, in 1998 few & JEREB, 2010C; OKUTANI, 2015); this is the largest days apart in the same place, and a fourth one Megalocranchia species and may reach 1.8 m (ML = 153 mm ML) collected off the Balearic ML (ROPER & JEREB, 2010c). Islands, at 380-609 m depth, in 2010. None of Most probably, this individual was a vagrant them was sexed. one that entered the Mediterranean Sea through As all cranchiids, T. pavo is also a fully the Strait of Gibraltar. It is impossible to decide pelagic cephalopod throughout its life, so that whether it entered as an adult that actively its early juvenile and juvenile stages may be crossed the strait or as a paralarva/juvenile pas- easily carried along by currents, which explains sively carried by the inflow of surface currents its wide distribution. The hypothesis that T. from the Atlantic Ocean. pavo entered the Mediterranean Sea through the Gibraltar Strait is well supported. No data are Teuthowenia megalops (Prosch, 1849) (Deca- available about the settlement of a stable popula- podiformes: Oegopsida: Cranchiidae: Taoniinae) tion in this basin. § Geographical distribution outside the Medi- terranean: subarctic and temperate Atlantic Megalocranchia sp. (cf. maxima Pfeffer, Ocean (ROPER & JEREB, 2010c). 1884) (Decapodiformes: Oegopsida: Cranchii- § First Mediterranean documented occur- dae: Taoniinae) rence and literature record: 1983, off Blanes, § Geographical distribution outside the Medi- Catalan Sea (western Mediterranean Sea) terranean: according to ROPER & JEREB (SÁNCHEZ, 1985). 122 ACTA ADRIATICA, 61 (2): 113 - 134, 2020

§ Notes on the species: medium-sized squid venti, because of its fully oceanic habits, might living in the water column, from 40 to 2,700 well be a cryptic inhabitant of the Mediterranean m depth; early stages inhabit the upper zones that had been overlooked until GUERRA’s (1992, and then descend to deeper waters (ROPER & pers. comm.) finding. This hypothesis is supported JEREB, 2010c). by the fact that the Mediterranean findings § NIS category and status: vagrant. occurred in a quite short lapse of time, widely The only specimen recorded in the Mediter- spread apart in the whole basin (ANDALORO, ranean was a paralarva, 7.4 mm ML, collected 2011). On the other hand, the facts that no other by bongo net in midwater (bottom depth = 190 specimen has ever been found in this sea, nei- m). ther before nor after those reported by GUERRA It was most probably a vagrant specimen (1992, pers. comm.), and that the only ones found that entered this basin from the Atlantic Ocean were juveniles evoke another possible scenario. through the Strait of Gibraltar, passively carried That is, planktonic juveniles recurrently enter by currents. the Mediterranean, either passively carried by currents through the Gibraltar Straits or through Joubin, 1919 (Decapo- the Suez Canal, yet they do not succeed in diformes: Oegopsida: Cycloteuthidae) growing to the adult stage, because of environ- mental constraints; hence their presence in the § Geographical distribution outside the Medi- Mediterranean makes just a pseudo-population terranean: tropical to temperate waters of (BOUCHET & TAVIANI, 1992). Whichever is the the Atlantic and Indo-West Pacific (JEREB right hypothesis, the safest conduct is to ascribe & ROPER, 2010); not reported in the Pacific C. sirventi to the cryptogenic species category Ocean by OKUTANI (2015). (CARLTON, 1996). § First Mediterranean documented occurrence and literature record: 1969, NW of the Asi- Taningia danae Joubin, 1931 (Decapodi- nara island (Sardinia), Italy (western Medi- formes: Oegopsida: Octopoteuthidae) terranean basin) (GUERRA, 1992). § Geographical distribution outside the Medi- § Notes on the species: medium-sized squid terranean: circumglobal in tropical to tem- found from the lower epipelagic to the mes- perate waters venturing in the boreal range opelagic, rarely in the bathybenthic zone (ROPER & JEREB, 2010b; OKUTANI, 2015). (JEREB & ROPER, 2010). § First Mediterranean documented occurrence § NIS category and status: cryptogenic. and literature record: 2003, off the Algerian The specimen recorded by GUERRA (1992) coast, Alboran Sea (QUETGLAS et al., 2006). was collected by IKMT net between 0 and § Notes on the species: large-sized pelagic 140 m depth, during the Woods Hole Oceano- squid (ML up to 1.6 m) that performs an graphic Institution cruise no. 49 (May-June ontogenetic descent from the epipelagic to 1969), onboard the R/V “Atlantis II”. In addi- deeper waters, down to the bathyal zone tion to the specimen reported by GUERRA (1992) (ROPER & VECCHIONE, 1993; ROPER & JEREB, (in this work only specimens pertaining to Ibe- 2010b). Despite its gelatinous body, it is a rian waters were described) the same scientist quite powerful swimmer (KUBODERA et al., observed three more specimens collected during 2007). the same cruise, by IKMT net in the same depth § NIS category and status: vagrant. range, in the Tyrrhenian Sea, in the Ionian Sea The only collected specimen of T. danae was and in the Levant Sea, respectively (GUERRA, a juvenile (ML = 5.6 cm) netted by bottom trawl pers. comm.). These specimens were juveniles. at 385-395 m depth (QUETGLAS et al., 2006). Cycloteuthis sirventi had never been col- The specimen recorded by QUETGLAS et al. lected before in any of the historical Mediterra- (2006) is regarded as a stray individual passively nean plankton cruises nor from any teuthivorous carried into the Mediterranean from the surface predator stomach contents. Nonetheless, C. sir- inflow of Atlantic waters. Bello et al: Non-indigenous species of cephalopods in the Mediterranean Sea: a review 123

Octopus cyanea Gray, 1849 (Octopodi- name Amphioctopus sp. is supposedly the first formes: Octopoda: Octopodidae) Lessepsian cephalopod. Although its presence in § Geographical distribution outside the Medi- the Mediterranean became officially document- terranean: an Indo-Pacific octopod that ed and recorded only towards the end of the past thrives in the Red Sea as well (NORMAN et al., millennium (SALMAN et al., 1999, 2005), MIENIS 2016). (2005) based on museum evidences showed that § First Mediterranean documented occurrence in fact this octopod had entered the Mediterrane- and literature record: 1997-98, off the Israel an as early as December 1934. Many specimens coast (Levant Sea, eastern Mediterranean have been collected and recorded since SALMAN Sea) (MIENIS, 2003a); GALIL (2007) gives the et al.’s (1999) record, throughout the eastern-most year 1997 as the collection date for the first part of the Mediterranean, so that this small recorded specimen). octopus can be now considered established in § Mode of life and habitat: a small octopus, this basin (e.g. ZENETOS et al., 2010). benthic in shallow waters (0 to at least 22 m As regards the nomenclature of this species, depth). it has been variously reported as either Octopus § NIS category and status: Lessepsian; estab- aegina Gray, 1849 or Octopus kagoshimensis lished? Ortmann, 1888 and generally ascribed to a MIENIS (2003a) reports the collection of two species complex (e.g. SALMAN et al., 1999, 2005). individuals of this species off the Israeli coast. Lately, it appeared that this species belongs The first one, from Haifa, is kept in the Biologi- indeed to the genus Amphioctopus and has been cal Collections of the Hebrew University, Jeru- usually ascribed to A. aegina (e.g. ÖZTÜRK et al., salem; the second one, caught off Mikhmoret 2014). In fact, Amphioctopus cf. aegina (Gray, in May 1998, was kept alive for a while in an 1849) / kagoshimensis (Ortmann, 1888) is an aquarium. unresolved alien species. There is no doubt that Therefore, it may be safely stated that the this octopus is a member of the genus Amphi- two individuals recorded by MIENIS (2003a) came octopus (cf. the genus description in NORMAN into the Mediterranean through the Suez Canal. et al., 2016). Anyway, because of both morpho- Amphioctopus sp. (Octopodiformes: Octopo- logical characters and geographical distribution da: Octopodidae) considerations, it does not belong neither to § Geographical distribution outside the Medi- aegina (distribution: coastal waters of the Indo- terranean: the genus Amphioctopus has a Pacific, from India to northern China, including circumglobal distribution; because of the Indonesia and the Philippines; NORMAN et al., undefined identity of the Mediterranean indi- 2016) nor to kagoshimensis (distribution: West viduals, no further information may be given Pacific Ocean, Taiwan and Japan; NORMAN et about the distribution of their species. al., 2016) (BELLO, 2017b). Hence, we do not assign § First Mediterranean documented occurrence: this alien cephalopod to any Amphioctopus spe- 1934, off Atlit, Israel, Levant Sea (eastern cies and stress the need to further investigate its Mediterranean) (MIENIS, 2005). taxonomic position. § First Mediterranean literature record: 1992, 13 specimens off the Turkish coast (Levant Tremoctopus gracilis (Eydoux & Souleyet, Sea, eastern Mediterranean Sea) (SALMAN et 1852) (Octopodiformes: Octopoda: Tremocto- al., 1999). podidae) § Notes on the genus: Amphioctopus includes § Geographical distribution outside the Medi- small/medium-sized octopuses, benthic to 40 terranean: Indian and Pacific Oceans (FINN, m depth or more (NORMAN et al., 2016). 2016). § NIS category and status: Lessepsian; estab- § First Mediterranean documented occurrence: lished. 1936, North Adriatic Sea (KRAMER, 1937; The species that we indicate here under the misidentified as Tremoctopus violaceus). 124 ACTA ADRIATICA, 61 (2): 113 - 134, 2020

§ First Mediterranean literature record: ORSI and literature record: 2003, Israeli coast RELINI et al. (2004). (Levant Sea) (MIENIS, 2003b). § Mode of life and habitat: dimorphic pelagic § Notes on the species: a benthic, medium- octopodid: females large (ML = 32 cm, total sized cuttlefish that inhabits the bottom of length > 1 m), males dwarfed (ML = 1.5 the continental shelf down to 130 m of depth. cm); it lives in the epipelagic zone; females The nominal species S. pharaonis represents observed in surface waters at night (FINN, a species complex (REID et al., 2005). 2016). § NIS category and status: Lessepsian; pres- § NIS category and status: recurring human- ence to be confirmed. mediated transfer?; established? MIENIS (2003b) observed large numbers of The story of its occurrence in the Mediterra- washed ashore cuttlebones of this cephalopod, nean Sea is nicely told by ORSI RELINI et al. (2004) together with cuttlebones of the three autoch- (see also further iconographic documentation in thonous Mediterranean Sepia species – namely ORSI RELINI, 2009). After an adult female of this S. officinalis Linnaeus, 1758, S. orbignyana species was photographed in the Tyrrhenian Sea Férussac, 1826 and S. elegans Blainville, 1826 in August 2002 (BELLUSCIO et al., 2003), ORSI – along the Israeli coast, from the 20 to the 24 RELINI et al. (2004) became aware of the 1936 April 2003. The fact that S. pharaonis cuttle- swarm of blanket octopuses in the northern bones were spread over long beach stretches Adriatic Sea reported by KRAMER (1937). The (overall extending for some 36 km) and that they latter author erroneously ascribed them to Trem- seemingly had not floated around for a long time octopus violaceus Delle Chiaje, 1830, since (no epibionts, in particular goose-barnacles, that was the only member of the genus known were attached on them) made MIENIS (2003b: to live in the Mediterranean. ORSI RELINI et al. 127) state that this cephalopod “has most prob- (2004) showed that the species described by ably managed to get a foothold in the Eastern both KRAMER (1937) and BELLUSCIO et al. (2003) Mediterranean. However, this assumption has to belonged indeed to T. gracilis and emended be confirmed by the finds of living specimens.” KRAMER’s (1937) report. Several cuttlebones were collected and placed in Afterward, this eye-catching octopod has the collections of Tel Aviv University (MIENIS, been further recorded in Tunisian waters (RIFI & 2003b). BEN SOUISSI, 2014). The Mediterranean records of T. gracilis Sepia pharaonis is known to have gradually refer to female specimens only. moved northwards into the Suez Canal. At first To explain the occurrence of this pelagic a single cuttlebone was recorded in the Bitter octopod in the northern Adriatic Sea in 1936 Lakes, along the Suez Canal, by BARASH & DANIN (1972) (KRAMER, 1937) and in the Tyrrhenian Sea in . Afterwards, it colonized the Suez 2002 (BELLUSCIO et al., 2003), ORSI RELINI et al. Canal and establish there a stable population (2004) suggested transport by ships; given the that is commercially harvested (GABR et al., 1998). fragile nature of the individuals of this species Therefore, notwithstanding the need to confirm some doubts may be cast on this hypothesis. its presence in the Mediterranean Sea, it is rea- sonable that this cuttlefish may have progressed Questionable record into the Mediterranean basin. To the best of our knowledge, no additional report of its presence Sepia pharaonis Ehrenberg, 1831 (Decapodi- in the Mediterranean Sea has been published formes: Sepiida: Sepiidae) since. Indeed, in addition to the above MIENIS’ § Geographical distribution outside the Medi- (2003b) supposition, another one is conceivable, terranean: widely distributed from the west- that is the many washed ashore cuttlebones ern Pacific Ocean to the Red Sea (REID et al., were discards of products harvested elsewhere 2005). (cf, BELLO, 2006); accordingly, S. pharaonis may § First Mediterranean documented occurrence have not entered yet the Mediterranean Sea. Bello et al: Non-indigenous species of cephalopods in the Mediterranean Sea: a review 125

The nominal species S. pharaonis represents Shortly after, MIENIS (2008) specified that the a species complex. NORMAN (2000) described finding consisted in a partly damaged cuttlebone three different ‘forms’ of this species; the typi- washed ashore on the beach of Ashdod (Israel). cal one is found from the Red Sea to at least the In support of the S. gibba presence in the Medi- western Indian Ocean in accordance with the terranean, MIENIS (2008: 6) stated that “No epibi- type locality, viz. the Gulf of Suez (SWEENEY, onts were found on the cuticle [= cuttlebone], 2001). Later on, ANDERSON et al. (2011), based on a sign that most probably it did not float for a genetic analyses, found that the name pharaonis long time.” Indeed, cuttlebones can float for a encompasses a complex of at least five sub- very long time and over long distances (VOSS, clades, one of which was termed ‘western Indian 1974). Moreover, the occurrence of exotic cut- subclade’ to include specimens from the Red tlebones may have an unnatural origin, that is Sea, the Gulf of Aden and the Gulf of Oman. they may be the discard of dressing processes of Whatever future research will decide about the frozen products coming from all over the world taxonomic status of such a species complex, (BELLO, 2006). the Red Sea population, hence the individuals In summary, S. gibba is to be excluded from that may have entered or will enter the Mediter- the list of Mediterranean allochthonous cepha- ranean through the Suez Canal, belong to Sepia lopods. pharaonis Ehrenberg, 1831 sensu stricto. DISCUSSION Excluded records According to our analyses, the present Medi- Two more cephalopods have been recorded terranean teuthofauna includes 13 non-indige- in recent times in the Mediterranean basin, nous species (NIS) sensu lato. Until thirty years namely Spirula spirula (Linnaeus, 1758) (Deca- ago, it was not believed that there were exotic podiformes: Spirulida: Spirulidae) and Sepia cephalopods in this basin (MANGOLD & BOLETZ- gibba Ehrenberg, 1831 (Decapodiformes: Sepi- KY, 1988), although at least two octopods, namely ida: Sepiidae). Indeed, no documented Medi- Amphioctopus sp. and Tremoctopus gracilis, had terranean record of living individual of either been collected half a century earlier but had not species is available in the literature. All records been correctly identified (see Results). are in fact based on findings of skeletal remains The sources for NIS cephalopods are the (see further). same as for most other taxa: i) from the Atlantic Spirula spirula, a circumtropical microneck- Ocean via the natural entrance, i.e. the Strait tonic species provided with a calcareous cham- of Gibraltar; ii) from the Red Sea through the bered shell, has been reported in the western artificial Suez Canal; iii) from any ocean by Mediterranean since the XIX century thanks anthropo-phoresy (supposedly in ballast water). to the recurrent occurrence of stranded dead The cephalopod NIS that have crossed the specimens, “not only the plain shell, but also Strait of Gibraltar are mainly vagrant speci- the shell with fleshy remains” (BELLO, 2003: 215) mens either passively carried or assisted by the coming from the Atlantic Ocean. Anyway, no entrance current, either during their early stages truly documented record exists of the entrance or as adults/subadults: Cranchia scabra, Taonius of alive specimens into the Mediterranean. pavo, Megalocranchia sp., Teuthoweina mega- As for Sepia gibba, GALIL (2007: 309) reports lops, Taningia danae and, possibly, Cycloteuthis it in the annex Aquatic alien species reported sirventi; the latter, a cryptic species, might be a from the coastal waters of Israel, thus: “2001, very rarely collected inhabitant of the Mediterra- Ashdod; single record; [native range] Red Sea; nean Sea. All of them are fully oceanic oegopsid [pathway] Suez Canal; Mienis, unpublished.” squids. In particular, it cannot be excluded that In fact, this record was not substantiated by any one or more small-sized cranchiid species, all documented occurrence of living individuals. of which we labelled ‘vagrant’, might indeed 126 ACTA ADRIATICA, 61 (2): 113 - 134, 2020 have established stable populations in the West played and is still playing a dramatic role as for Mediterranean Sea. The remaining Atlantic spe- the Red Sea NIS migration and survival. cies, that is Stoloteuthis leucoptera, is a bentho- In percentual terms, the cephalopod NIS rep- pelagic heteroteuthine that indeed might be a resents the 18.7% of the overall Mediterranean Mediterranean native; anyway, it would be the teuthofauna (13 NIS vs. 57 autochthonous spe- only Atlantic cephalopod to have established a cies), a percentage surprisingly similar to that stable population in the Mediterranean basin. of the fish NIS (Osteichthyes + Chondrichthyes As for the Lessepsian migrants, i.e. the ceph- + Agnatha), that is 18.8% (update 2010; PSO- alopods that crossed the Suez Canal, namely MADAKIS et al., 2012). The comparison between Sepia dollfusi, Sepioteuthis lessoniana, Octopus cephalopods and fishes is pertinent since sup- cyanea and Amphioctopus sp., they are ben- ported by their many similarities driven by con- thic , partly decabrachians other than vergent evolution (PACKARD, 1972). oegopsid squids and partly octopods. Lastly, In Results we also disentangled the situa- Tremoctopus gracilis, an Indo-Pacific pelagic tion of three species whose occurrence in the octopod, whose occurrence in the Mediterranean Mediterranean is not warranted, namely Sepia has been recorded a few times, was supposed to pharaonis, Sepia gibba and Spirula spirula. In have been repeatedly carried in ballast waters this respect, the case of S. gibba is paradigmatic (ORSI RELINI et al., 2004); anyway, the option that of how utterly unsupported records of alloch- T. gracilis is a Lessepsian migrant cannot be thonous species (GALIL, 2007) become afterwards a priori excluded; also the possibility that this endorsed in a comprehensive list that refers to species has been misidentified as Tremoctopus previous sources (e.g. ZENETOS et al., 2010). Out violaceus some other times in the past (in addi- of those three cephalopods, only S. pharaonis tion to the misidentification by KRAMER (1937)) might reasonably have crossed or may cross the cannot be a priori excluded. Suez Canal, since it established a stable popula- To sum up, a quite sharp dichotomy is evi- tion there (GABR et al., 1998); nevertheless, sound dent in the mode of life of Mediterranean cepha- records of live or freshly dead specimens in lopod NIS: the Atlantic species are pelagic, the Mediterranean waters are necessary to label it a Red Sea ones are benthic. For the first group, a NIS for this basin. dominant role is played by the inflow of super- Lastly, the present paper contributes to fill a ficial Atlantic waters entering the Mediterranean gap in the knowledge of the Mediterranean non- indigenous cephalopods. We take advantage of Sea (anti-estuarine circulation; cf. MILLOT & the present paper to suggest the inclusion of TAUPIER-LETAGE, 2005) that carries organisms these cephalopods in lists of ‘exotic’ molluscs living in the water column. This explains why (e.g. the CIESM Atlas of Exotic Molluscs in the most of them are stray-animals, somewhat forc- Mediterranean by ZENETOS et al., 2004). edly transported through the Strait of Gibraltar, that are not capable of establishing a stable pop- ACKNOWLEDGEMENTS ulation in the Mediterranean basin (cf. BOUCHET & TAVIANI, 1992); the only possible exception is We thank the late Kir Nesis for the identifi- S. leucoptera. The latter group of NIS includes cation of Megalocranchia and Fernando Ángel benthic and nektobenthic species that appear to Fernández-Álvarez for the fruitful discussion on have crossed the Suez Canal at a comparatively Stoloteuthis leucoptera. We also acknowledge slow pace (e.g. Sepia dollfusi; see Results), the help by Lidia Orsi Relini, Angel Guerra whose crossing and subsequent establishment and Alessandro Voliani, who kindly provided in Mediterranean waters have been fostered by unpublished information about cephalopod NIS. favourable environmental conditions, mainly We also express our thanks to two anonymous suitable temperatures. In this respect the ‘tropi- reviewers for their helpful suggestions. calization’ of the Mediterranean basin (ANDAL- ORO & RINALDI, 1998; THIÉBAULT et al., 2016) has Bello et al: Non-indigenous species of cephalopods in the Mediterranean Sea: a review 127

Note: While the present paper was in press, we learned that the Mediterranean population of Stoloteuthis belongs indeed to a newly described species, different from S. leucoptera (Fernández- Álvarez F.Á., P. Sánchez and R. Villanueva, submitted. Morphological and molecular assessments of bobtail squids (Cephalopoda: Sepiolidae) reveal a hidden history of biodiversity. Frontiers in Marine Science)."

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Received: 28 September 2020 Accepted: 13 October 2020

134 ACTA ADRIATICA, 61 (2): 113 - 134, 2020

Alohtone vrste glavonožaca u Sredozemnom moru: pregled

Giambattista BELLO, Franco ANDALORO i Pietro BATTAGLIA

*Kontakt, e-pošta:[email protected] [email protected]

SAŽETAK

U ovom radu autori kritički procjenjuju nalaze glavonožaca koji su ušli u Sredozemno more u posljednjih nekoliko desetljeća, što uključuje 13 vrsta, a to su: Sepia dollfusi, Stoloteuthis leucopte- ra, Sepioteuthis lessoniana, Architeuthis dux, Cranchia scabra, Taonius pavo, Megalocranchia sp., Teuthowenia megalops, Cycloteuthis sirventi, Taningia danae, Octopus cyanea, Amphioctopus sp. i Tremoctopus gracilis. Prisutnost vrste Sepia pharaonis treba biti potvrđena, dok je prisutnost Sepia gibba i Spirula spirula isključena. Dolasci vrsta iz Atlantskog oceana kroz Gibraltarski tjesnac povezani su s ulaznom površinskom strujom koja je nosila pasivno planktonske paralarve ili je na neki drugi način favorizirala ulaz subadultnih i odraslih zalutalih primjeraka. Zapravo su svi atlantski glavonošci pelagične lignje, s izuzetkom nekto-bentoskog sepiolida S. leucoptera. Čini se da nijedna vrsta od navedenih tamo nije uspostavila stabilnu populaciju, osim potonje navednih vrsta. Naprotiv, glavonošci koji ulaze u Sredozemno more iz Crvenog mora kroz Sueski kanal (lesepsijski migranti) vode bentoski način života. Ipak, dvije vrste S. lessoniana i Amphioctopus sp., uspostavile su stabilne populacije u istoč- nom dijelu. Konačno, pojave pelagične hobotnice T. gracilis pripisuju se, u literaturi, prijenosu posredovanim antropogenim utjecajem.

Ključne riječi: mekušci, glavonošci, egzotične vrste, lesepsijski migranti, kriptične vrste