Marine Biodiversity Records, page 1 of 4. # Marine Biological Association of the United Kingdom, 2015 doi:10.1017/S1755267215000032; Vol. 8; e26; 2015 Published online Northernmost record of quadricolor (: Nudibranchia) in the SCI “Fondali Noli – Bergeggi” (Ligurian Sea) federico betti1, riccardo cattaneo-vietti2 and simone bava1 1Comune di Bergeggi, AMP Isola di Bergeggi, Via De Mari, 28/D, 17028, Bergeggi, SV, Italy, 2DiSVA, Universita` Politecnica delle Marche, Via Brecce Bianche, 60131, Ancona, Italy

The northernmost record of the alien Godiva quadricolor is reported here, about 400 km farther north than the previously published one and the farthest to be recorded from the equator. It is also the second published record of this along the Italian coasts and the first record from the Ligurian Sea. A single specimen was reported during a scuba dive, crawl- ing on small stones inside the Site of Community Importance ‘Fondali Noli – Bergeggi SCI’, at a depth of 3.5 m. The species, described in 1927 in South Africa, is considered to be rapidly expanding its original areal distribution thanks to maritime traffic. A review of the known actual distribution is also reported here.

Keywords: Godiva quadricolor, alien species, Mediterranean Sea, Ligurian Sea, first record, northernmost record

Submitted 23 September 2014; accepted 08 January 2015

INTRODUCTION 2011, about 20 specimens were found in Pialassa della Baiona, a lagoon directly connected with the North Adriatic The nudibranch Godiva quadricolor (Barnard, 1927) Sea and Ravenna Harbour, but researchers successively (Nudibranchia: ) is characterized by a pale failed in finding any other specimens, suggesting that the slender body, with a long tapering tail and numerous blue, 2011 findings were an occasional bloom (A. Rinaldi, personal yellow and orange . The head is orange, the communication); it was however hypothesized that the species wrinkled and the oral tentacles are long, with a white stripe on could have also been present in other Italian lagoons them. It feeds on sea anemones and other nudibranchs (Crocetta, 2012). In 1987, Godiva quadricolor was recorded (Barnard, 1927; Gosliner, 1987). in Fremantle and Cockburn Sound, Western Australia This species represents a curious case in terms of geograph- (Willan, 1987), and in 2004 it reached the coasts of South ic distribution; first collected in 1912 in False Bay, South Queensland; at both sites, this species is now considered estab- Africa, it was described in 1927 (Barnard, 1927) and nowadays lished (Willan, 2004). In 2010, the species was found in the it is considered to be common in shallow waters along the north-east Atlantic Ocean, in particular in Morocco, and in whole east coast of South Africa (Macnae, 1954; Gosliner, the Strait of Gibraltar (Algeciras Bay); moreover, one speci- 1987; Fraser, 2001). In 1954, it was recorded in Inhaca, men was found in an aquaculture tank in Salobren˜a, close to Mozambique (Macnae, 1954), and three years later the same Granada (Cervera et al., 2010). author found the species in the estuarine complex of the So far, Godiva quadricolor has been found in both tropical Zwartkops River (Port Elizabeth, South Africa) (Macnae, and temperate waters, mainly in the intertidal area of brackish 1957); at these sites, Godiva quadricolor was always found in lagoons; as pointed out by Cervera et al. (2010) and Willan intertidal areas, on and under stones or in Zostera meadows. (2004), it is usually found in areas subjected to important The subsequent synonymy with Godiva rachelae Rudman, maritime traffic and high anthropization, suggesting that the 1980 extended the distribution range of Godiva quadricolor species, endemic to South Africa, was most likely introduced up to Dar es Salaam, Tanzania (Willan, 2004). In 1977, the to other regions through ballast waters. A review of the species was recorded in the Atlantic Ocean for the first time, actual distribution is shown in Figure 1A. in a boat hull in Ghana (Edmunds, 1977). In 1985, it was In the last decades, the Mediterranean Sea has been sub- reported stable and very abundant in Fusaro Lake, a brackish jected to an increasing ingression of alien species, mainly lagoon with a narrow connection to the sea, located in the Gulf due to the warming of shallow waters, which promotes the of Naples (Mediterranean Sea) (Villani & Martinez, 1993), but entrance and the establishment of tropical species from was erroneously reported as Facelina coronata because of a Gibraltar and the Suez Channel, and to marine traffic and misidentified picture in Cattaneo-Vietti et al., 1990; the aquaculture (Galil, 2009; Zenetos et al., 2012). Molluscs are mistake was pointed out by Cervera in 2002. In October the dominant taxa of the alien species in the Mediterranean Sea, with more than 200 recorded species (Zenetos et al.,

Corresponding author: 2012). In Italy, 35 mollusc alien taxa are known, of which F. Betti 18 are gastropods and 12 are Opisthobranchia (Crocetta, Email: [email protected] 2012). Due to its low winter water temperatures, it appears

Downloaded from https://www.cambridge.org/core. University of Athens, on 27 Sep 2021 at 03:37:17, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms1 . https://doi.org/10.1017/S1755267215000032 2 federico betti et al.

Fig. 1. Godiva quadricolor distribution: (A) map of the actual distribution (in yellow, the new record); (B) map of the coast, with Vado Ligure Harbour and the SCI “Fondali Noli – Bergeggi” (in purple); (C) map of the area of the record (black spot) with the border of the first sub-site of the SCI (in purple) and the biocenosis (in green, Posidonia oceanica meadows; in greenish-brown, dead matte of Posidonia oceanica; in grey, sand; in orange, mud). Map B and C obtained through MACISTE software (http://www.remare.org/cartografia-amp-maciste).

to be difficult for the Ligurian Sea to be colonized by alien Noli – Bergeggi’, which covers different habitats, such as sub- species (Astraldi et al., 1995; Brasseur et al., 1996). merged sandbanks, Posidonia oceanica beds, rocky reefs and caves (Figure 1B, C). Several investigations, by means of snor- kelling activities and scuba diving, are regularly carried out MATERIAL AND METHODS during the year by the authors, monitoring the environment and the species living in the whole area; Godiva quadricolor The coast between the town of Bergeggi and the Noli Cape was observed during a scuba dive on 21 October 2014, is partially protected by the MPA ‘Isola di Bergeggi’ and the inside the borders of the first of the four sub-sites of the Site of Community Importance (SCI) IT1323271 ‘Fondali SCI, between the town of Noli and the homonymous cape,

Downloaded from https://www.cambridge.org/core. University of Athens, on 27 Sep 2021 at 03:37:17, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S1755267215000032 northernmost record of godiva quadricolor 3

Table 1. Summary of Godiva quadricolor records in the Mediterranean Sea.

Year Locality Coordinates Paper

1985 Fusaro Lake, Gulf of Naples 40849′21′′N14803′20′′E Villani, personal communication; Villani & Martinez (1993) 2010 Algeciras Bay, Strait of Gibraltar 36809′28′′N05824′15′′W Cervera et al. (2010) 2010 Salobrena, Spain 36844′16′′N03835′43′′W Cervera et al. (2010) 2011 Pialassa della Baiona, North Adriatic Sea 44830′22′′N12815′00′′E Present paper 2014 Noli, Ligurian Sea 44812′07′′N08825′12′′E Present paper

at the WGS 84 coordinates 44812′07′′N08825′12′′E. Harbour, about 7 km north, may also suggest in this case, as Underwater pictures of the were taken using a reported in literature, an introduction of the species via Nikon D7000 in Isotta housing, equipped with a Nikon shipping transportation. The same introduction pattern is Nikkor 60 mm micro lens and two Sea & Sea external strobes. plausible for the Moroccan specimens found by Cervera A review of the existing literature regarding the distribu- et al. (2010) in Aghroud and Anza, both in the proximity of tion of G. quadricolor was performed to better describe the the important harbour of Agadir, and for the Pialassa novelty of information provided by this new record. della Baiona specimens, close and directly connected to Ravenna Harbour. Further observations are required to know if the presence of this alien species is occasional and RESULTS restricted to the Noli coast, or if it is more widespread along the Ligurian Sea. One specimen of Godiva quadricolor was found in the study area (Table 1). The record is based on the in vivo examination of the specimen and identification was confirmed by the ACKNOWLEDGEMENTS underwater pictures (Figure 2). It was easy to spot, crawling on the surface of small stones, at a depth of 3.5 m, about The authors would like to thank Dr Attilio Rinaldi 10 m away from the shore, on a plateau; the water temperature (Fondazione Centro Ricerche Marine Cesenatico, Italy) for was 208C. The total length, measured underwater, was 4 cm. the important data regarding the presence of Godiva quadri- The main features of the species, such as the colour pattern color in the Adriatic Sea. and the wrinkled rhinophores, perfectly match the original description (Barnard, 1927) and in particular the detailed ana- lysis performed by Willan (2004). REFERENCES

Astraldi M., Bianchi C.N., Gasparini G.P. and Morri C. (1995) Climatic DISCUSSION fluctuations, current variability and marine species distribution: a case study in the Ligurian Sea (north-west Mediterranean). Oceanologica This report represents the northernmost record of this species, Acta 18, 139–149. about 400 km farther north than the previous record from Fusaro Lake and the farthest to be recorded from the Barnard K.H. (1927) South African nudibranch , with descrip- tions of new species, and a note on some specimens from Tristan equator. It is also the second record of Godiva quadricolor d’Acunha. Annals of the South African Museum 25, 171–215, pls. to be made along the Italian coasts and the first for the 19–20. whole Ligurian Sea. Moreover, while the species is typically found in brackish waters and lagoons, the Ligurian specimen Brasseur P., Beckers J.M., Brankart J.M. and Schoenauen R. (1996) was found in an open shore area; its proximity to Vado Ligure Seasonal temperature and salinity fields in the Mediterranean Sea: cli- matological analyses of a historical data set. Deep-Sea Research 43, 159–192. Cattaneo-Vietti R., Chemello R. and Giannuzzi-Savelli R. (1990) Atlas of Mediterranean nudibranchs. Rome: La Conchiglia. Cervera J.L. (2002) Godiva quadricolor from Mediterranean. Available at: http://www.seaslugforum.net Cervera J.L., Tamsouri N., Moukrim A. and Villani G. (2010) New records of two alien opisthobranch molluscs from the north-eastern Atlantic: Polycera hedgpethi and Godiva quadricolor. Marine Biodiversity Records 3, e51, 1–4. Crocetta F. (2012) Marine alien Mollusca in Italy: a critical review and state of the knowledge. Journal of the Marine Biological Association of the United Kingdom 92, 1357–1365. Edmunds M. (1977) Larval development, oceanic currents, and origins of the opisthobranch fauna of Ghana. Journal of Molluscan Studies 43, 301–308.

Fig. 2. Underwater picture of the specimens of Godiva quadricolor reported in Fraser V. (2001) Godiva quadricolor from South Africa. Available at: the present paper. http://www.seaslugforum.net

Downloaded from https://www.cambridge.org/core. University of Athens, on 27 Sep 2021 at 03:37:17, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S1755267215000032 4 federico betti et al.

Galil B.S. (2009) Taking stock: inventory of alien species in the and Mediterranean Sea. Biological Invasions 11, 359–372. Gosliner T.M. (1987) Nudibranchs of Southern Africa. A guide to opistho- branch molluscs of Southern Africa. Monterey, CA: Sea Challengers Zenetos A., Gofas S., Morri C., Rosso A., Violanti D., Garcia Raso J.E., and Jeff Hamman Publications. Cinar M.E., Almogi-Labin A., Ates A.S., Azzurro E., Ballesteros E., Bianchi C.N., Bilecenoglu M., Gambi M.C., Giangrande A., Gravili Macnae W. (1954) On some eolidacean nudibranchiate molluscs from C., Hyams-Kaphzan O., Karachle P.K., Katsanevakis S., Lipej L., South Africa. Annals of the Natal Museum 13, 1–50. Mastrototaro F., Mineur F., Pancucci-Papadopoulou M.A., Ramos Macnae W. (1957) The ecology of plants and in the intertidal Espla` A., Salas C., San Martin G., Sfriso A., Streftaris N. and regions of the Zwartkops estuary, near Port Elizabeth, South Africa. Verlaque M. (2012) Alien species in the Mediterranean Sea by 2012. The Journal of Ecology 45, 361–387. A contribution to the application of European Union’s Marine Strategy Framework Directive (MSFD). Part 2. Introduction trends Villani G. and Martinez E. (1993) Some observations on the opistho- and pathways. Mediterranean Marine Science 13, 328–352. branch fauna from the Fusaro Lake, a brackish-water lagoon near Naples. Bollettino Malacologico 29, 201–09. Willan R.C. (1987) Phylogenetic systematics and zoogeography of Australian nudibranchs: 1. Presence of the aeolid Godiva quadricolor Correspondence should be addressed to: (Barnard) in Western Australia. Journal of the Malacological Society F. Betti of Australia 8, 71–85. Comune di Bergeggi, AMP Isola di Bergeggi Willan R.C. (2004) Godiva quadricolor (Barnard, 1927) (Nudibranchia: Via De Mari Facelinidae) spreads into southern Queensland. Beagle: Records of 28/D, 17028 Bergeggi, SV, Italy the Museums and Art Galleries of the Northern Territory 20, 31. email: [email protected]

Downloaded from https://www.cambridge.org/core. University of Athens, on 27 Sep 2021 at 03:37:17, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S1755267215000032