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The state of knowledge of the alien marine Mollusca in Italy is reviewed and updated. Littorina saxatilis (Olivi, 1792), Polycera hedgpethi Er. Marcus, 1964 and Haminoea japonica Pilsbry, 1895are here considered as established on the basis of published and unpublished data, and recent records of the latter considerably expand its known Mediterranean range to the Tyrrhenian Sea. COI sequences obtained indicate that a comprehensive survey of additional European localities is needed to elucidate the dispersal pathways of Haminoea japonica.Recent records and interpretation of several molluscan taxa as alien are discussed both in light of new Mediterranean (published and unpublished) records and of four categories previously excluded from alien species lists. Within this framework, ten taxa are no longer considered as alien species, or their records from Italy are refuted. Furthermore, Trochocochlea castriotae Bellini, 1903 is considered a new synonym for Gibbula albida (Gmelin, 1791). Data provided here leave unchanged as 35 the number of alien molluscan taxa recorded from Italy as well as the percentage of the most plausible vectors of introduction, but raise to 22 the number of established species along the Italian shores during the 2005–2010 period, and backdate to 1792 the first introduction of an alien molluscan species (Littorina saxatilis) to the Italian shores.
Alien Mollusca, natural entries, translocations, state of knowledge, Italy
Although marine invasions have been well documented all over the world, they are particularly conspicuous in the Mediterranean Sea, mainly due to the high number of vectors of introduction (
The inclusion (or not) of the taxa listed as aliens in the Mediterranean is based on strict accordance to the definition of alien species by the International Union for Conservation of Nature:
‘[non-native, non-indigenous, foreign, exotic] means a species, subspecies, or lower taxon occurring outside of its natural range (past or present) and dispersal potential (i.e., outside the range it occupies naturally or could not occupy without direct or indirect introduction or care by humans) and includes any part, gametes or propagule of such species that might survive and subsequently reproduce.’
Four categories previously excluded (
A survey of published Mediterranean records of the taxa listed in the present paper was conducted and, where necessary, a full list of synonyms for Mediterranean records is provided. Unpublished records, when available, are listed under each species and come from the examination of preserved specimens, photographs and personal observations obtained from different research projects conducted in several sites along the Italian coasts. Updated taxonomy and nomenclature used follow WoRMS (World Register of Marine Species: last accessed 30 January 2013), unless clearly specified [see Gibbula albida (Gmelin, 1791) for the new synonymy proposed].
A total of 8 specimens of Haminoea japonica Pilsbry, 1895from two populations in Italy (Lago Fusaro and Lago di Sabaudia)were sequenced for the cytochrome c oxidase I (COI) mitochondrial gene, following methods used in
In order to verify the presence or absence of alien species, a continuous monitoring effort is necessary. Only field surveys may provide such evidence, and the new records of the two species reported below ensure that they fit wel into the category of established species.
Family LITTORINIDAE Children, 1834
Littorina saxatilis (Olivi, 1792)
Unpublished material examined. Italy - Veneto: Malamocco (45°20.35'N, 12°18.80'E), under and on rocks and in crevices at tidal level. Voucher specimens: 05/2009, approx. 50 sps., legit F. Crocetta and F. Favero; 06/2009, approx. 100 sps., legit F. Crocetta and F. Favero; 03/2010, approx. 20 sps., legit F. Crocetta.
Remarks. Littorina saxatilis (Olivi, 1792) was originally described from the Venice Lagoon (Italy); its disjunct distribution in the eastern and western Atlantic Ocean, Barents Sea, White Sea and Mediterranean (see
Family HAMINOEIDAE Pilsbry, 1895
Haminoea japonica Pilsbry, 1895
Published Mediterranean records
Haminaea callidegenita Gibson and Chia, 1989 (sic!) -
Haminoea callidegenita (Gibson & Chia, 1989) -
Haminoea cf. japonica -
Unpublished material examined. Italy - Latium: Lago diSabaudia (S2: 41°17.58'N, 13°1.06'E; S3: 41°17.58'N, 13°1.21'E; S4: 41°16.13'N, 13°2.23'E; S5: 41°15'N, 13°2.33'E), low depth on mud and amidst algae. Very common in the area during observations and samplings held from April 2007 to May 2012 (A. Macali, pers. obs) - Voucher specimens: 29/05/2007, approx. 30 sps. and egg masses, legit A. Macali; 05/02/2008, around 50 sps. and egg masses, legit A. Macali; 06/05/2008, approx. 50 sps. and egg masses, legit A. Macali; 24/11/2009, approx. 50 sps. and egg masses, legit A. Macali; 24/05/2010, approx. 100 sps. and egg masses, legit A. Macali; 21/04/2012, approx. 100 sps. and egg masses, legit A. Macali and C. Smriglio (4 sps. used for molecular analysis - JX679602-JX679605).
Italy - Campania: Casina Vanvitelliana, Lago Fusaro (FuI: 40°49.16'N, 14°3.53'E), low depth on mud and amidst algae. Voucher specimens: 27/01/2012, approx. 100 sps. and egg masses, legit F. Crocetta; 17/02/2012, 12 sps. and egg masses, legit F. Crocetta and G. Villani (Fig. 1A); 25/02/2012, approx. 200 sps. and egg masses, legit F. Crocetta (4 sps. used for molecular analysis - JX679598-JX679601); 29/03/2012, approx. 50 sps. and egg masses, legit F. Toscano.
Remarks. According to
However, the recently discovered populations from Lago di Sabaudia (Latium, Tyrrhenian Sea) since 2007 and from Lago Fusaro during 2012 (Figure 1A) considerably expand its known Mediterranean distribution to the Tyrrhenian Sea, and suggest that non-native genotypes can become established in areas warmer than previously thought. Sequence data obtained from Italian specimens are similar to those obtained for other specimens found in the non-native range of Haminoea japonica: two distinct haplotypes for COI were detected in Italy, H20 and H25 (according to the haplotype nomenclature by
Discussions on previously excluded categories
Species recorded on the basis of empty shells only
The durable composition of molluscan shells, primarily made of calcium carbonate, often allow the study of local assemblages without sacrificing living animals, offering reliable data on taxa distributions and the ability to study populations qualitatively. Data obtained from the study of empty shells, however, should always be complemented by a very critical approach, and the three taxa cited below are a good example of this. They have been recorded on the basis of worn empty shells only, found in bioclastic sediments trawled at depths of 400-500 m off Latium in 2007 (
Family SCALIOLIDAE Jousseaume, 1912
Finella pupoides A. Adams, 1860
Remarks. Finella pupoides Adams, 1860 is an Indo-Pacific taxon well established along the eastern Mediterranean shores up to Turkey (
Family CERITHIIDAE Fleming, 1822
Clathrofenella ferruginea (A. Adams, 1860) sensu
Remarks. Four empty shells of a taxon belonging to Cerithiidae have been recently recorded for the first time from Italy (off Latium) as Clathrofenella ferruginea (A. Adams, 1860) (
Family VENERIDAE Rafinesque, 1815
Timoclea roemeriana (Issel, 1869) sensu
Remarks. Two loose valves of a bivalve belonging the genus Timoclea have been recently recorded for the first time from Italy (off Latium) as Timoclea roemeriana (Issel, 1869) (
A. Haminoea japonica Pilsbry, 1895 from Lago Fusaro, 17/02/2012, approx. 15 mm. Photo: Guido Villani. B. Anteaeolidiella foulisi (Angas, 1864) from Lago di Sabaudia, April 2009, 13 mm. Photo: Paolo Mariottini.
After the complete re-establishment of the Atlanto-Mediterranean connection, dating approximately 5.33 million years ago, no evidence of further closing of the Strait of Gibraltar exists (
Family CIMIDAE Warén, 1993
Cima apicisbelli Rolán, 2003
Remarks. Cima apicisbelli Rolán, 2003 has been recently described from Dakar (Senegal, Atlantic Ocean) on the basis of differences in shell and protoconch sculpture with the closely related Cima cylindrica (Jeffreys, 1856) (see
Family SEPIOLIDAE Leach, 1817
Stoloteuthis leucoptera (A.E. Verrill, 1878)
and
Family CYCLOTEUTHIDAE Naef, 1923
Cycloteuthis sirventi Joubin, 1919
Remarks. The deep water sepiolid Stoloteuthis leucoptera (A.E. Verrill, 1878), described from the Gulf of Maine and then recorded from the eastern Atlantic Ocean and the Mediterranean Sea (
Species with a complex/unclear taxonomy
Family AEOLIDIIDAE Gray, 1827
Anteaeolidiella foulisi (Angas, 1864)
Published Mediterranean records
Aeolidiella takanosimensis Baba, 1949 (sic!) -
Aeolidiella orientalis takanosimensis Bergh, 1888 (sic!) -
Aeolidiella indica Bergh, 1888 -
Unpublished material examined. Italy - Latium: Canale Romano, Lago di Sabaudia (S6: 41°15.03'N, 13°2.35'E; S7: 41°14.9'N, 13°2.35'E), 2.5 m depth under stones. Very common in the area during samplings conducted from April 2009 to September 2011 (Fig. 1B) (A. Macali, pers. obs). Voucher specimens: April 2011: 3 sps. and egg masses, legit A. Macali; 16/11/2011: 5 sps. and egg masses, legit A. Macali.
Italy - Campania: Canale Est di Maremorto di Miseno (40°47.55'N, 14°4.68'E), low depth under stones, 30/09/2011: 5 sps. and egg masses, legit G. Villani; 04/10/2011: 29 sps. and egg masses, legit G. Villani; 01/01/2012: 6 sps., legit G. Villani.
Remarks. Anteaeolidiella foulisi (Angas, 1864) -senior synonym of Anteaeolidiella indica (Bergh, 1888), following
Records from Maremorto di Miseno (Campania, Tyrrhenian Sea) confirm the presence of this species at the same sampling site after approximately 40 years after the last records from Italy, while those from Lago di Sabaudia (Latium, Tyrrhenian Sea) constitute the first record from the area and the only other known Italian site where the species has been reported. Unpublished Italian records reported here, as well as recent records from the Atlantic Ocean (
Family CRANCHIIDAE Prosch, 1849
Megalocranchia sp.
Remarks. The genus Megalocranchia includes several species widespread all over the world (
Translocations of native Mediterranean species to an area where they previously did not occur
Mediterranean translocations (species introduced from elsewhere within the Mediterranean) have been recently listed as alien species when the introduction event was unmistakable (
Family TROCHIDAE Rafinesque, 1815
Gibbula albida (Gmelin, 1791)
( = Trochocochlea castriotae Bellini, 1903, new synonym)
Remarks. Gibbula albida (Gmelin, 1791) has been considered a native species to the Adriatic Sea, but an alien in the western Mediterranean Sea due to recent introductions into the Ebro Delta (Spain) and the French Mediterranean lagoons (see
This taxon, however, was originally described with no type locality (Gmelin 1791), and has been known for centuries to occur commonly in the Adriatic Sea (e.g.
Although a translocation into the western Mediterranean from the Adriatic is possible, but may have happened earlier than the recent records from France and Spain cited by
A. Haplotype network of non-native haplotypes of Haminoea japonica Pilsbry, 1895 (haplotype IDs from
The rate of reporting (as number of species per decade) of alien molluscan species from the Italian territorial seawaters.
The last decades have seen an ever-increasing worldwide scientific emphasis on biological pollution. Marine alien species feature among the qualitative descriptors of good environmental status in the EU’s Marine Strategy Framework Directive. In this view, alien species inventories play important roles in informing regional policy and management decisions, as well as in identifying resource priorities. The scientific community is called upon to pay particular attention to their accuracy and veracity (
Alien Mollusca established from the territorial seawaters of Italy during the 2005-2010 period - data after
Taxa |
Cerithium scabridum Philippi, 1848 |
Littorina saxatilis (Olivi, 1792) |
Rapana venosa (Valenciennes, 1846) |
Haminoea cyanomarginata Heller & Thompson, 1983 |
Haminoea japonica Pilsbry, 1895 |
Aplysia dactylomela Rang, 1828 |
Syphonota geographica (Adams & Reeve, 1850) |
Bursatella leachii Blainville, 1817 |
Polycera hedgpethi Er. Marcus, 1964 |
Melibe viridis (Kelaart, 1858) |
Godiva quadricolor (Barnard, 1927) |
Anadara transversa (Say, 1822) |
Anadara kagoshimensis (Tokunaga, 1906) |
Brachidontes pharaonis (P. Fischer, 1870) |
Arcuatula senhousia (Benson in Cantor, 1842) |
Limnoperna securis (Lamarck, 1819) |
Pinctada imbricata radiata (Leach, 1814) |
Crassostrea gigas (Thunberg, 1793) |
Fulvia fragilis (Forsskål, 1775) |
Theora lubrica Gould, 1861 |
Venerupis philippinarum (Adams & Reeve, 1850) |
Mya arenaria Linnaeus, 1758 |
Flavio Favero (Ferrara, Italy), Manuel Malaquias (Bergen, Norway), Paolo Mariottini (Rome, Italy), Francesco Toscano (Naples, Italy) and John van Aartsen (Leiden, The Netherlands) shared with us their own data or helped with sampling. Andrea Travaglini (Naples, Italy) and Nicola Maio (Naples, Italy) provided information regarding museum collections. Paolo Crovato (Naples, Italy), Serge Gofas (Malaga, Spain) and Ermanno Quaggiotto (Longare, Italy) provided requested papers. We are grateful to all of them.