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Non-Indigenous Cephalopods in the Mediterranean Sea: a Review

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Non-Indigenous Cephalopods in the Mediterranean Sea: a Review ISSN: 0001-5113 ACTA ADRIAT., REVIEW PAPER AADRAY 61 (2): 113 - 134, 2020 Non-indigenous cephalopods in the Mediterranean Sea: 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, Stoloteuthis leucoptera, Sepioteuthis lessoniana, Architeuthis dux, Cranchia scabra, Taonius pavo, Megalocranchia sp., Teuthowenia megalops, Cycloteuthis 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 Atlantic Ocean 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 squids, 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: Mollusca, 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 waters 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 cephalopod 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
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