A review of occurrence, distribution and alien status of Notodiaphana atlantica Ortea, Moro and Espinosa, 2013 and Liloa mongii (Audouin, 1826) (Mollusca: Heterobranchia) in the Mediterranean Sea

Notodiaphana atlantica and Liloa mongii are two cephalaspidean species described respectively from the Atlantic Ocean and the Red Sea, and considered widespread in their native ranges. Both species have also been recently recorded from the Mediterranean Sea, prompting some authors to consider them alien. Notwithstanding clear morphological differences in their shells, the two species have often been confused or misidentified in the literature, or specimens have been described with incorrect locality data. We hereby review the occurrence, distribution and status of both species in the Mediterranean Sea based on published data and examination of new material. Notodiaphana atlantica is considered a cryptogenic species with a range spanning from the western to eastern part of the basin. The presence of L. mongii in the Mediterranean is questioned until specimens that can be reliably assigned to this taxon or to any congeneric species are found in the area. Alien species inventories play an important role in regional policy and management decisions, thus requiring a high degree of confidence in the validity of species identification and their non-indigenous status. The present paper adds further evidence of the excess of “bibliographically introduced” alien records and reiterates the need for periodic re-evaluation of published data.

Acknowledgements

The following people offered assistance during the fieldwork, research on the material in public and private collections, bibliographic research, or provided useful advice: Franco Agamennone (Pescara, Italy), Cesare Bogi (Livorno, Italy), Alberto Cecalupo (Milano, Italy), Gian Paolo Franzoni (Tortoreto, Italy), Virginie Héros (Paris, France), Harry Lee (Jacksonville, FL, USA), Philippe Maestrati (Paris, France), Pasquale Micali (Fano, Italy), Constantine Mifsud (Rabat, Malta), Leopoldo Moro (Santa Cruz de Tenerife, Spain), Andrea Nappo (Pomezia, Italy), Jesús Ortea (Oviedo, Spain), Attilio Pagli (Empoli, Italy), Alessandro Raveggi (Firenze, Italy), Walter Renda (Amantea, Italy), Emilio Rolán (Vigo, Spain), Maria Scaperrotta (Firenze, Italy), and Franco Siragusa (Livorno, Italy); specifically Stefano Bartolini (Firenze, Italy) and Edoardo Perna (Napoli, Italy) allowed us to use their own photographs. We are grateful to all of them.

References

Adams, A. (1850). Monograph of the family Bullidae. In G.B. Sowerby II (Ed.), Thesaurus Conchyliorum, vol. 2 (pp. 553–608, pls 119–125). London, United Kingdom: Sowerby.
Audouin, V. (1826). Explication sommaire des planches de Mollusques de l'Egypte et de la Syrie, publiées par J.C. Savigny. Description de l’Égypte ou recueil des observations et des recherches qui ont été faites en Égypte pendant l'expédition de l'armée française, publié par les ordres de sa majesté l'empereur Napoléon le grand. Histoire Naturelle, Animaux invertébrés 1(4): 7–56. Paris, France: Imprimerie impériale.
Albano, P.G., Azzarone, M., Amati, B., Bogi, C., Sabelli, B. et al. (2020). Low diversity or poorly explored? Mesophotic mollusks highlight undersampling in the Eastern Mediterranean. Biodivers. Conserv. 29: 4059–4072. DOI: 10.1007/s10531-020-02063-w.
Alexander, J. & Valdés, Á. (2013). The ring doesn’t mean a thing: molecular data suggest a new taxonomy for two Pacific species of sea hares (Mollusca: Opisthobranchia, Aplysiidae). Pac. Sci. 67(2): 283–294. DOI: 10.2984/67.2.10.
Amati, B., Appolloni, M., Quaggiotto, E., Smriglio, C. & Oliverio, M. (2019). Notes on some taxa of the Alvania lineata-complex with the descriptions of three new species from the Mediterranean Sea (Gastropoda: Rissoidae). Iberus 37(1): 81–112.
Ávila, S.P., Azevedo, J.M.N., Gonçalves, J.M., Fontes, J. & Cardigos, F. (1998). Checklist of the shallow-water marine molluscs of the Azores: 1 – Pico, Faial, Flores and Corvo. Açoreana 8(4): 487–523.
Bazzicalupo, E., Crocetta, F., Estores-Pacheco, K., Golestani, H., Bazairi, H. et al. (2018). Population genetics of Bursatella leachii (De Blainville, 1817) and implications for the origin of the Mediterranean population. Helgol. Mar. Res. 72: 19. DOI: 10.1186/s10152-018-0521-7.
Bazzicalupo, E., Crocetta, F., Gosliner, T.M., Berteaux-Lecellier, V., Camacho-García, Y.E. et al. (2020). Molecular and morphological systematics of Bursatella leachii de Blainville, 1817 and Stylocheilus striatus Quoy and Gaimard, 1832 reveals cryptic diversity in pantropically distributed taxa (Mollusca, Gastropoda, Heterobranchia). Invertebr. Syst. 34: 535–568. DOI: 10.1071/IS19056.
Bouchet, P. & Danrigal, F. (1982). Napoleon’s Egyptian Campaign (1798-1801) and the Savigny collection of shells. The Nautilus 96(1): 9–24.
Buzzurro, G. & Greppi, E. (1997). The Lessepsian mollusca of Tasuçu (South East Turkey). La Conchiglia. Annuario 1996 (Supplement to n° 279): 3–22.
Cachia, C. (1999). Il-Molluski ta' Malta. Kullana kulturali. 5: 1–210.
Cachia, C., Mifsud, C. & Sammut, P.M. (1993). An annotated checklist of the marine Mollusca of the Maltese Islands. Rankweil, Austria: Erste Vorarlberger Malakologische Gesellschaft.
Cachia, C., Mifsud, C. & Sammut, P.M. (2001). The Marine Mollusca of the Maltese Islands. Part Three. Sub-class Prosobranchia to sub-class Pulmonata, Order Basommatophora. Leiden, The Netherlands: Backhuys.
Cachia, C., Mifsud, C. & Sammut, P.M. (2004). The Marine Mollusca of the Maltese Islands. Part four. The classes: Caudofoveata, Solenogastres, Bivalvia, Scaphopoda & Cephalopoda. Leiden, The Netherlands: Backhuys.
Cachia, C., Mifsud, C., Sammut, C.I. & Sammut, P. (2019). An annotated and bibliographical check-list of the marine Mollusca of the Maltese Islands. Żejtun, Malta: Sunland Printers Limited.
Canning-Clode, J. & Carlton, J.T. (2017). Refining and expanding global climate change scenarios in the sea: Poleward creep complexities, range termini, and setbacks and surges. Divers. Distrib. 23(5): 463–473. DOI: 10.1111/ddi.12551.
Cecalupo, A. & Quadri, P. (1996). Contributo alla conoscenza malacologia per il nord dell’isola di Cipro (Terza e ultima parte). Boll. Malacol. 31(5–8): 95–118.
Cecalupo, A., Buzzurro, G. & Mariani, M. (2008). Contributo alla conoscenza della malacofauna del Golfo di Gabès (Tunisia). Quad. Civica Staz. Idrobiol. Milano 31: 1–175.
Chaban, E.M. (2016). Heterobranch mollusks of the orders Acteonoidea and Cephalaspidea (Gastropoda: Heterobranchia) of Vietnam: annotated check-list with illustrations of some species. In A.V. Adrianov & K.A. Lutaenko (Eds.), Biodiversity of the western part of the South China Sea (pp. 415–448). Vladivostok, Russia: Dalnauka.
Convention on Biological Diversity (2000). Interim Guiding Principles. Conference of the Parties Decision V/8. Alien species that threaten ecosystems, habitats or species. http://www.cbd.int/decision/cop/default.shtml?id=7150.
Coppini, M. (2002). [Documenti del Gruppo Malacologico Livornese]. I generi Acteocina, Cylichna, Retusa, Cylichnina, Pyrunculus e Volvulella nel Mediterraneo. [available online at the web page: https://www.societaitalianadimalacologia.it/PDF/Coppini-2002.pdf]
Coppini, M. (2004). [Documenti del Gruppo Malacologico Livornese]. I generi Acteocina, Cylichna, Retusa, Cylichnina, Pyrunculus e Volvulella nel Mediterraneo. Notiziario S.I.M. 22(5–8): 13–24.
Corsini-Foka, M., Zenetos, A., Crocetta, F., Çinar, M.E., Koçak, F. et al. (2015). Inventory of alien and cryptogenic species of the Dodecanese (Aegean Sea, Greece): collaboration through COST Action training school. Manag. Biol. Invasions 6(4): 351–366. DOI: 10.3391/mbi.2015.6.4.04.
Cossignani, T. & Ardovini, R. (2011). Malacologia Mediterranea. Atlante delle conchiglie del Mediterraneo: 7500 foto a colori. Ancona, Italy: L’Informatore Piceno.
Crocetta, F. & Tringali, L.P. (2015). Mapping alien Mollusca distribution in the Mediterranean Sea: the Lessepsian immigrant Retusa desgenettii (Audouin, 1826) reaches Turkey. Quatern. Int. 390: 15–20. DOI: 10.1016/j.quaint.2015.03.009.
Crocetta, F., Macali, A., Furfaro, G., Cooke, S., Villani, G. et al. (2013). Alien molluscan species established along the Italian shores: an update, with discussions on some Mediterranean alien species categories. ZooKeys 277: 91–108. DOI: 10.3897/zookeys.277.4362.
Crocetta, F., Poursanidis, D., Tringali, L.P. (2015). Biodiversity of sea slugs and shelled relatives (Mollusca: Gastropoda) of the Cretan Archipelago (Greece), with taxonomic remarks on selected species. Quatern. Int. 390: 56–68. DOI: 10.1016/j.quaint.2015.02.061.
Crocetta, F., Gofas, S., Salas, C., Tringali, L.P. & Zenetos, A. (2017). Local ecological knowledge versus published literature: a review of non-indigenous Mollusca in Greek marine waters. Aquat. Invasions 12(4): 415–434. DOI: 10.3391/ai.2017.12.4.01.
Crocetta, F., Bitar, G., Zibrowius, H. & Oliverio, M. (2020). Increase in knowledge of the marine gastropod fauna of Lebanon since the 19th century. Bull. Mar. Sci. 96(1): 1–22. DOI: 10.5343/bms.2019.0012.
Delongueville, C. & Scaillet, R. (2007). Les espèces invasives de mollusques en Méditerranée. Novapex 8: 47–70.
Delongueville, C., Scaillet, R. & Swinnen, F. (2019). New records of marine littoral Gastropoda and Bivalvia in the Azores Archipelago (Northeast Atlantic Ocean). Novapex. 20(1–2): 35–43.
Forli, M. (2016). Il problema dei molluschi marini alloctoni, invasivi nel Mare Mediterraneo. Alleryana 34(2): 85–90.
Giacobbe, S. & Renda, W. (2018). Mollusc diversity in Capo d’Armi (Central Mediterranea Sea) subtidal cliff: a first, tardy, report. Biodivers. J. 9(1): 25–34.
Gofas, S. & Zenetos, A. (2003). Exotic molluscs in the Mediterranean basin: Current status and perspectives. Oceanogr. Mar. Biol. 41: 237–277.
Golestani, H., Crocetta, F., Padula, V., Camacho-García, Y., Langeneck, J. et al. (2019). The little Aplysia’s coming of age: From one species to a complex of species complexes in Aplysia parvula Mörch, 1863 (Mollusca, Gastropoda, Heterobranchia). Zool. J. Linnean Soc. 187(2): 279–330. DOI: 10.1093/zoolinnean/zlz028.
Higo, S., Callomon, P. & Goto, Y. (2001). Catalogue and Bibliography of the Marine Shell-Bearing Mollusca of Japan. Gastropoda Bivalvia Polyplacophora Scaphopoda. Type Figures. Yao, Japan: Elle Scientific Publications.
Lin, G. (1997). Fauna Sinica. Phylum Mollusca, Class Gastropoda, Subclass Opisthobranchia, Order Cephalaspidea. Beijing, China: Science Press.
Malaquias, M.A.E. (2001). Updated and annotated checklist of the opisthobranch molluscs (excluding Thecosomata and Gymnosomata), from the Azores archipelago (North Atlantic Ocean, Portugal). Iberus 19(1): 37–48.
Micali, P. (2014). On the presence of Notodiaphana atlantica Ortea, Moro et Espinosa, 2013 in the Mediterranen Sea, with notes on Retusa multiquadrata Oberling, 1970 and Cylichna mongii (Audouin, 1826) (Cephalaspidea Cylichnidae). Biodivers. J. 5(4): 499–504.
Micali, P., Bogi, C. & Galil, B.S. (2016). On the occurrence of Atys angustatus E. A. Smith, 1872 and Atys macandrewii E. A. Smith, 1872 (Cephalaspidea: Haminoeidae) in the Mediterranen Sea. Iberus 34(1): 49–53.
Mikkelsen, P.M. (1995). Cephalaspid opisthobranchs of the Azores. In: A.M.F. Martins (Ed.), The marine fauna and flora of the Azores. Proceedings of the Second International Workshop of Malacology and Marine Biology, Vila Franca do Campo, São Miguel, Azores. Açoreana. Supplement 4: 193–215.
MolluscaBase. (2020). MolluscaBase. Accessed at http://www.molluscabase.org on 2020-11-12.
Nordsieck, F. (1972). Die Europäischen Meeresschnecken. Stuttgart, Germany: Gustav Fischer Verlag.
Ojaveer, H., Galil, B.S., Minchin, D., Olenin, S., Amorim, A. et al. (2014). Ten recommendations for advancing the assessment and management of non-indigenous species in marine ecosystems. Mar. Policy. 44: 160–165. DOI: 10.1016/j.marpol.2013.08.019.
Okutani, T. (Ed.) (2017). Marine Mollusks in Japan, second edition. 2 vols. Tokyo, Japan: Tokai University Press.
Oliver, J.D., Calvo, M., Guallart, J., Sánchez-Tocino, L. & Templado, J. (2015). Gasterópodos marinos de las islas Chafarinas (Mediterráneo suroccidental). Iberus 33(1): 97–150.
Ortea, J., Moro, L. & Espinosa, J. (2013). Nueva especie de Notodiaphana Thiele, 1931 del Océano Atlántico y nueva ubicación genérica para Atys alayoi Espinosa & Ortea, 2004 (Gastropoda: Opisthobranchia: Cephalaspidea). Rev. Acad. Canar. Cienc. 25: 15–24.
Ortea, J. & Moro, L. (2018). Nuevas citas y nuevos datos sobre las lesmas do mar (Mollusca: Gastropoda) de las islas de Cabo Verde (II). Avicennia. 22: 49–58.
Oskars, T.R., Bouchet, P. & Malaquias, M.A.E. (2015). A new phylogeny of the Cephalaspidea (Gastropoda: Heterobranchia) based on expanded taxon sampling and gene markers. Mol. Phylogenetics Evol. 89: 130–150. DOI: 10.1016/j.ympev.2015.04.011.
Oskars, T.R., Too, C.C., Rees, D., Mikkelsen, P.M., Willassen, E. et al. (2019). A molecular phylogeny of the gastropod family Haminoeidae sensu lato (Heterobranchia: Cephalaspidea): a generic revision. Invertebr. Syst. 33(2): 426–472. DOI: 10.1071/IS18051.
Perna, E. (2013). La collezione Perna Atlanto-Mediterranea – Gastropoda. I Quaderni di Malachia. 7: 1–271.
Pola, M., Paz-Sedano, S., Macali, A., Minchin, D., Marchini, A. et al. (2019). What is really out there? Review of the genus Okenia Menke, 1830 (Nudibranchia: Goniodorididae) in the Mediterranean Sea with description of two new species. PLoS ONE 14(5): e0215037. DOI: 10.1371/journal.pone.0215037.
Poppe, G.T. (Ed.) (2008). Philippine Marine Mollusks. Volume 3 (Gastropoda – Part III). Hackenheim, Germany: Conchbooks.
Redfern, C. (2001). Bahamian seashells. A thousand species from Abaco, Bahamas. Boca Raton, Florida: Bahamianseashells.com, Inc.
Redfern, C. (2013). Bahamian seashells. 1161 species from Abaco, Bahamas. Boca Raton, Florida: Bahamianseashells.com, Inc.
Repetto, G., Orlando F. & Arduino, G. (2005). Conchiglie del Mediterraneo. Alba, Italy: Amici del Museo “Federico Eusebio”.
Rushmore-Villaume, M.R. (2008). Seashells of the Egyptian Red Sea. The Illustrated Handbook. Cairo, Egypt: The American University in Cairo Press.
Sabelli, B. & Taviani, M. (2014). The making of the Mediterranean molluscan biodiversity. In S. Goffredo & Z. Dubinsky (Eds.), The Mediterranean Sea: its history and present challenges (pp. 285–306). Dordrecht, The Netherlands: Springer.
Sammut, C.R. & Perrone, A.S. (1998). A preliminary check-list of Opisthobranchia (Mollusca, Gastropoda) from the Maltese Islands. Basteria 62: 221–240.
Scaperrotta, M., Bartolini, S. & Bogi, C. (2016). Accrescimenti: stadi di accrescimento dei molluschi marini del Mediterraneo. Vol. VIII. Ancona, Italy: L’Informatore Piceno.
Segers, W., Swinnen, F. & De Prins, R. (2009). Marine Molluscs of Madeira. Heule, Belgium: Snoeck Publishers.
Severns, M. (2011). Shells of the Hawaiian Islands. The sea shells. Hackenheim, Germany: ConchBooks.
Too, C.C., Carlson, C., Hoff, P.J. & Malaquias, M.A.E. (2014). Diversity and systematics of Haminoeidae gastropods (Heterobranchia: Cephalaspidea) in the tropical West Pacific Ocean: new data on the genera Aliculastrum, Atys, Diniatys and Liloa. Zootaxa. 3794(3): 355–392. DOI: 10.11646/zootaxa.3794.3.3.
Tunnell, J.W.Jr., Andrews, J., Barrera, N.C. & Moretzsohn, F. (2010). Encyclopedia of Texas Seashells. Identification, Ecology, Distribution & History. College Station, Texas: Texas A&M University Press.
Tunnell, J.W.Jr., Barrera, N.C. & Moretzsohn, F. (2014). Texas Seashells. A Field Guide. Harte Research Institute for Gulf of Mexico Studies Series. College Station, Texas: Texas A&M University Press.
Valdés, Á. & Héros, V. (1998). The types of Recent and certain fossil opisthobranch molluscs in the Muséum national d'Histoire naturelle, Paris. Zoosystema. 20(4): 695–742.
Valdés, Á., Hamann, J., Behrens, D.W. & DuPont, A. (2006). Caribbean Sea Slugs. A field guide to the opisthobranch mollusks from the tropical Northwestern Atlantic. Washington, District of Columbia. Sea Challengers Natural History Books.
Valdés, Á., Alexander, J., Crocetta, F., Yokeş, M.B., Giacobbe, S. et al. (2013). The origin and dispersal pathway of the spotted sea hare Aplysia dactylomela (Mollusca: Opisthobranchia) in the Mediterranean Sea. Aquat. Invasions 8(4): 427–436. DOI: 10.3391/ai.2013.8.4.06.
Vazzana, A. (2010). La malacofauna del Circalitorale di Scilla (Stretto di Messina). Boll. Malacol. 46: 65–74.
Vazzana, A. (2011). Biodiversità marina lungo le coste della provincial di Reggio Calabria. Villa San Giovanni, Italy: Laruffa Editore.
Zhang, D.Y. (2012). Antiguan shallow-water seashells. A collection with 18 years study and research of shoreline shells from Antigua and West Indies. Wellington, Florida: MDM Publishing.
Zenetos, A., Gofas, S., Russo, G. & Templado, J. (2004). CIESM Atlas of Exotic Species in the Mediterranean. Vol. 3 – Molluscs. Monaco: CIESM Publishers.
Zenetos, A., Gofas, S., Verlaque, M., Çinar, M.E., García Raso, J.E. et al. (2010). Alien species in the Mediterranean Sea by 2010. A contribution to the application of European Union’s Marine Strategy Framework Directive (MSFD). Part I. Spatial distribution. Medit. Mar. Sci. 11(2): 381–493. DOI: 10.12681/mms.87.
Zenetos, A., Gofas, S., Morri, C., Rosso, A., Violanti, D. et al. (2012). Alien species in the Mediterranean Sea by 2012. A contribution to the application of European Union’s Marine Strategy Framework Directive (MSFD). Part 2. Introduction trends and pathways. Medit. Mar. Sci. 13(2): 328–352. DOI: 10.12681/mms.327.
Zenetos, A., Çinar, M.E., Crocetta, F., Golani, D., Rosso, A. et al. (2017). Uncertainties and validation of alien species catalogues: the Mediterranean as an example. Estuar. Coast. Shelf Sci. 191: 171–187. DOI: 10.1016/j.ecss.2017.03.031.
Zenetos, A., Mačić, V., Jaklin, A., Lipej, L., Poursanidis, D. et al. (2016). Adriatic ‘opisthobranchs’ (Gastropoda, Heterobranchia): shedding light on biodiversity issues. Mar. Ecol. – Evol. Persp. 37(6): 1239–1255. DOI: 10.1111/maec.12306.