Marine Biodiversity Records, page 1 of 5. # Marine Biological Association of the United Kingdom, 2015 doi:10.1017/S1755267214001420; Vol. 8; e3; 2015 Published online New records of punctata (: ) in the Mediterranean Sea from Italy, France and Greece paolo g. albano Universita¨t Wien, Institut fu¨r Pala¨ontologie, Althanstraße 14, A-1090 Wien, Austria

Echinolittorina punctata was historically distributed in the southern sectors of the Mediterranean Sea. However, in the last decades a progressive range extension has occurred. In this context, new populations in France (Colliure, Cap d’Agde) and in Italy (Monte Argentario, Tuscany) are reported here. The population in Cap d’Agde is the northernmost in the entire Mediterranean Sea, the population in Monte Argentario is the northernmost along the Italian Tyrrhenian coastline and along the direction of range extension described in the last few years. Details on population density and size frequency dis- tributions in Monte Argentario are provided, showing a decrease in density and an increase in minimum size from south to north. New records are also provided from Salamina Island and Rhodes Island in Greece. The latter likely dates back to 1836– 1837 and is the first record from the Mediterranean Sea. This record confirms that the was widely distributed in the Levantine Sea at the time, although records from Greece and Turkey are extremely rare in the literature and in museum collections.

Keywords: , Littorinidae, Mediterranean Sea, Italy, France, Greece, distribution records, new records

Submitted 24 October 2014; accepted 25 November 2014

INTRODUCTION shell collector communities in Europe. E. punctata has always been considered an interesting finding due to its southern dis- (Gmelin, 1791) is a prosobranch tribution; it is easily observable in the intertidal zone and also gastropod belonging to the family Littorinidae. Its taxonomic easily recognizable; it would not have escaped the attention of history and current status were reviewed by Reid (2011). the several collectors that have beachcombed Italian shores. E. punctata lives in the intertidal zone, on both natural and In this context, I wish to provide further new records in the man-made hard substrates. Its range spans from the Mediterranean Sea: (i) from southern Tuscany, the northern- Atlantic coast of South Africa to The Gambia, the Canary most locality in Italy; (ii) from southern France, the northern- Islands and the Mediterranean Sea, with the exception of its most locality in the Mediterranean Sea; and (iii) from Greece, northernmost sectors. It is in this latter basin that a remark- likely the first record in the Mediterranean Sea. Consequently, able range extension has been recorded in the last few the maps provided in Albano (2014, Figure 17.2) are updated. decades (see Albano, 2014 for a review). Until approximately 1950, the species was confined to the westernmost Mediterranean Sea (southern Spain and Algeria) and the MATERIALS AND METHODS south-eastern Levantine Sea. Since then, it has been reliably recorded from Tunisia, Turkey, Cyprus and Greece. Living individuals were searched for, by eye, on rocky shores. However, to what extent these records were related to newly Where found, coordinates were retrieved from Google Earth settled populations versus newly surveyed areas is not (datum WGS84) and input into a relational database. In known. On the contrary, the prodigious range extension Monte Argentario (Tuscany, Italy) on 27 May 2014, the along the Italian peninsula that brought the species from the density was estimated by counts in 1 m2 quadrats haphazardly southernmost tip of Sicily (Brugnone, 1850) to the Jonian selected on the shore. Sea in Puglia (Albano & Trono, 2008) and at the latitude of Specimens were then taken to the laboratory, where their Rome along the Tyrrhenian Sea (Albano, 2010) is quite cer- size was measured with a stereomicroscope equipped with a tainly not an artefact of poor detection. The Italian shores high precision measuring stage. Statistical tests and histo- have been surveyed for decades by one of the most numerous grams were performed using the statistical programming environment R, version 3.1.1 (R Development Core Team,

Corresponding author: 2009). Specimens were photographed with a Leica M420 P.G. Albano macroscope, shooting photos at different depths of field that Email: [email protected] were later stacked with the CombineZP software.

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Further records were communicated by colleagues on the and Le Cannelle were different (Kolmogorov–Smirnov test, basis of their field observations (A. Benocci, D. Grech, D ¼ 0.5171, P ≪ 0.05). R. Huet and P. Ovalis). Identification was checked in person or with photos sent by colleagues and further material was retrieved from museum collections (namely, Museum fu¨r DISCUSSION Naturkunde, Berlin). New records from Italy RESULTS The first record of Echinolittorina punctata in Italy dates back to 1850, when G. Brugnone described siculus, later recognized as a junior synonym of E. punctata, as an abundant New records species on the rocks of Pozzallo at the south-easternmost tip of New populations and records are reported from Italy, France Sicily. The species seemed confined to this area for all of the and Greece (Table 1). Echinolittorina punctata was found 19th century. It was then reported from Catania, on the in Italy in Ansedonia, the southernmost part of Tuscany eastern coast of Sicily, by Patane´ (1946), from the neighbour- (A. Benocci, personal communication), and all around ing coast of Palermo in the 1970s (D’Anna, 1986), from Monte Argentario, Tuscany (Figure 1A, B), on upper inter- Calabria in the 1980s (Micali & Giovine, 1983), in tidal rocks, 5–20 cm above the water-line. In France, indivi- Campania (D’Anna, 2001), Lazio (Soppelsa et al., 2004; duals were found in Colliure (D. Grech, personal Albano, 2010) and Puglia (Albano & Trono, 2008) in the communication) (Figure 2C, D), close to the border with 2000s. The populations that are described here from Spain, and Cap d’Agde (R. Huet, personal communication), Tuscany represent a further step northward along the Italian approximately 80 km to the north-east. In Greece, the Tyrrhenian coast; an advancement of approximately 100 km species was found on Salamina Island, near Athens (P. from the latest records in Lazio, north of Rome, from 2010, Ovalis, personal communication). Moreover, a lot from which is the northernmost record in Italy (Figure 3B). There Rhodes is reported from the Museum fu¨r Naturkunde, is no record in the literature of E. punctata populating Berlin. It was probably collected in 1836–1837. Tuscany. Looking at the personal observations carried out in Monte Argentario from 2001 to 2007, where the species was not previously recorded, it is likely that this population is of Details on the populations at Monte very recent settlement. Argentario, Tuscany It is not clear why all the collected individuals were adults and above 3.2 mm in height. One simple explanation could be In Monte Argentario, species density had a clear south to that smaller (younger) individuals were overlooked due to north trend: the southernmost locality, Feniglia, had a mean their small size. However, Monte Argentario hosts another density of 25.3 specimen m22, Le Cannelle had a mean periwinkle, neritoides (Linnaeus, 1758), which is density of 4.5 specimen m22 and Bagni di Domiziano had a widespread species in the Mediterranean basin. M. neritoides only 0.5 specimen m22. The localities were situated 10 km was collected in the same quadrats, it is usually smaller than from each other. Moreover, no specimen had a height meas- E. punctata, and indeed very young specimens of 1–2 mm uring less than 3.2 mm (Feniglia) (Figure 2) and the in size were collected along with E. punctata. minimum size increased from south to north, being 5.0 mm A further explanation might be that juveniles live lower on at Le Cannelle and 5.2 mm at Bagni di Domiziano. The the shore, maybe even below the water-line. Palant & height distributions at Feniglia and Le Cannelle were Fishelson (1968) observed that small individuals (less than normal (Shapiro-Wilk test, W ¼ 0.9746 and W ¼ 0.9797 5 mm) of E. punctata lived lower on the shore in Israel, in respectively, P ≫ 0.05), while at Bagni di Domiziano they the regularly wetted zone among Chthamalus, an observation could not be computed because only two specimens confirmed at a different locality by Lipkin & Safriel (1971). were found. Moreover, the height distributions at Feniglia Indeed, this appears to be a general trend in several littorinids,

Table 1. New populations and records of Echinolittorina punctata in the Mediterranean Sea.

Locality No. specimens Latitude Longitude Date Source

Italy, Monte Argentario, Feniglia Beach 76 42824′20′′N11812′36′′E April and May 2014 P.G. Albano under Poggio Pertuso Italy, Monte Argentario, L’Acqua Dolce A few 42822′33′′N11811′22′′E April and May 2014 P.G. Albano Italy, Monte Argentario, Le Cannelle 27 42822′38′′N11808′20′′E April and May 2014 P.G. Albano Italy, Monte Argentario, Porto Santo Stefano A few 42826′22′′N11807′04′′E April 2014 P.G. Albano Italy, Monte Argentario, Bagni di Domiziano 2 42826′07′′N11809′12′′E April and May 2014 P.G. Albano Italy, Promontorio di Ansedonia, Several 42824′N11817′E 16th May 2014 A. Benocci Spacco della Regina France, Colliure A few 42831′27′′N3805′08′′E 10th April 2012 D. Grech France, Cap d’Agde A few 43816′N3830′E 2008 R. Huet Greece, Salamina Island Several 37855′N23830′E 20th May 2012 P. Ovalis Greece, Rhodos 4 36826′N28813′E 1836–1837 Museum fu¨r Naturkunde, Berlin (no. 117971) new records of echinolittorina punctata 3

Costa, 1778) close to the limit of the species distribution in the north of Scotland were dominated by the larger, older individuals. Subsequently, Kendall (1987) observed that all populations of the trochid Osilinus lineatus (da Costa, 1778) recently settled in the northern part of the range had low dens- ities, missing year classes and were dominated by older indi- viduals. Two decades later, Mieszkowska et al. (2007) observed that O. lineatus showed a larger proportion of juve- niles as a result of an increased recruitment success that occurred in recent years. Indeed, the increasing minimum size and the decreasing density of E. punctata from south to north in Monte Argentario may fit a similar pattern of edge- distribution populations. Density might be also influenced by substrate suitability, although E. punctata is known to occur on a wide variety of artificial and natural substrates (Albano & Trono, 2008; Albano, 2010; Reid, 2011).

New records from France Echinolittorina punctata was recorded in Southern France by Locard (1886) who reported it from Cannes, Nice and the Maritime Alps, and from the Roussillon, on the basis of Michaud’s material and then again in 1891, describing it as ‘rare’. However, these records were not confirmed by other contemporary authors: Risso (1826) (Nice and Alpes Maritimes), Roux (1862) (Alpes Maritimes), Dautzenberg (1881, 1886) (Cannes), Bucquoy et al. (1882–1898) (Roussillon) and Claudon (1902) (Saint-Raphae¨l) did not Fig. 1. Echinolittorina punctata (Gmelin, 1791) from Monte Argentario, report E. punctata. However, they all recorded Melarhaphe Tuscany, Italy (A, B: height 6.2 mm) and Colliure, France (C, D: height neritoides (Linnaeus, 1758), evidence that intertidal rocks 7.3 mm). were inspected in their studies. In more modern times, Buzzurro et al. (1999) did not report the species from Agay, related to the increasing physical rigor of the environment considering the records in southern France from previous (temperature, desiccation, salinity) in an upshore direction authors as very questionable. In November 2012, the species (Vermeij, 1972). Small individuals are more susceptible to was not recorded from Menton, the easternmost part of the death from extreme physical conditions than large ones of French Mediterranean coast (personal observation). the same species, particularly area-dependent effects such as Hence, the records provided here are the first unquestion- desiccation. able ones in modern times from the French coast. They all However, the reason for this pattern could be related to the pertain to the south-westernmost part of southern France, dynamics of colonization. Kendall & Lewis (1986) observed possibly as a range extension from the nearby Spanish coast. that populations of the trochid Gibbula umbilicalis (da The population in Cap d’Agde is currently the northernmost in the whole of the Mediterranean Sea (Figure 3B).

New records from Greece Notwithstanding the coastal extension of Greece and its pos- ition between the Central and the Eastern Mediterranean, its malacofauna has been poorly studied, especially in past research. Echinolittorina punctata is not cited by Forbes (1844) from the Aegean Sea. In the collection of the Academy of Natural Sciences of Philadelphia, two lots are present; one collected in ‘Greece’ by M. Conemenos, a 19th century collector, and another from Rhodes, probably dating back to the early 20th century (P. Callomon, personal commu- nication). In modern times, the species was reported by Nicolay & Angioy (1988) from Keratea, south-east of Athens and from Loutro, southern Crete (Reid, 2011), although Koutsoubas et al. (1992) cite only Melarhaphe neri- toides in their review of the malacofauna of Crete. The lot of four specimens reported here from Rhodes and Fig. 2. Histogram of the height frequency distribution (N ¼ 105) of preserved in the Museum fu¨r Naturkunde (no. 117971), Echinolittorina punctata (Gmelin, 1791) from Monte Argentario, Tuscany, Berlin, is likely to be the oldest record from Greece. It Italy. No individuals below 3 mm were found. belongs to the collection of W. Dunker (1809–1885), but 4 paolo g. albano

Fig. 3. Distribution of Echinolittorina punctata in 1900 (A) and today (B), updating figure 17.2 in Albano (2014). Sky blue areas represent distributions reconstructed from the literature and collection data. Grey areas represent expected distributions, unconfirmed by the bibliography and collections, probably due to the lack of sampling in the area. Blue points represent single records of interest, most likely due to poor sampling efforts or because they are the first record of successive range extensions. ‘NO’ means the species was not recorded by regional works in the area at the time. Question marks, ‘?’, indicate areas where doubtful records were reported. Text highlights the localities reported in the present paper for the first time.

the label reports the name of Roth, likely Johannes Rudolf Albano P.G. (2014) Recent changes in the distribution of autochthonous Roth (Germany 1814–Lebanon 1858). J.R. Roth was a marine molluscs in the Mediterranean Sea. In Goffredo S. and German naturalist who travelled to Palestine in 1836–1837, Dubinsky Z. (eds) The Mediterranean Sea: its history and present chal- visiting several Greek islands along the way to and from the lenges. Dordrecht: Springer, pp. 307–318. Middle East (Hantzsch, 1907). He certainly visited Rhodes Albano P.G. and Trono D. (2008) On the occurrence of Echinolittorina too, because several records of land snails from this island punctata (Gmelin, 1791) (Gastropoda: Littorinidae) in Puglia, are reported in his doctoral dissertation (Roth, 1839). South-Eastern Italy. Bollettino Malacologico 44, 123–126. Moreover, this is the oldest record of E. punctata in the Brugnone G. (1850) Un nuovo Turbo siciliano. L’Armonia 1. Mediterranean Sea retrieved so far. It confirms that the species was present in the early 19th century in the whole of Bucquoy E., Dollfus G.-F. and Dautzenberg P. (1882–1898) Les mollus- ques marins du Roussillon. Paris: J.-B. Bailliere and Fils. the Levantine Sea and not only on the Middle East coasts (Figure 3A). Indeed, the species was reported from Syria in Buzzurro G., Hoarau A., Greppi E. and Pelorce J. (1999) Contributo alla 1847 by Philippi (as Litorina syriaca), but the first record to conoscenza dei molluschi marini della Rada d’Agay (Francia sudorien- be retrieved so far from Turkey dates back to 1988 (A. tale). La Conchiglia 31, 36–43 and 61–62. Lugli, private collection). The lot from Rhodes demonstrates Claudon E. (1902) Faunule malacologique marine de Saint-Raphae¨l. that the lack of records along the Turkish coast is likely to Feuille des Jeunes Naturalistes 32, 184–199. be due to the lack of monitoring rather than to true D’Anna G. (1986) Studio sulla distribuzione di punctata absence. The modern lot from Salamina Island is significant (Gmelin) e Littorina neritoides (L.) nel Golfo di Castellammare within the context of the poor knowledge of Greek (Sicilia Nord-Occidentale). Lavori della Societa` Italiana di malacofauna. Malacologia 22, 39–50. D’Anna G. (2001) Presenza di punctata (Gmelin, 1791) sulle coste del basso Salentino. La Conchiglia 33, 53–54. ACKNOWLEDGEMENTS Dautzenberg P. (1881) Liste de coquilles recueillies a Cannes par MM. E. & Ad. Dollfus. Feuille des Jeunes Naturalistes 11, 117–121. Several collectors and researchers continuously contribute to my database with their observations. In particular, Andrea Dautzenberg P. (1886) Nouvelle liste de coquilles de Cannes. Feuille des Benocci, Daniele Grech, Raymond Huet and Panayotis Jeunes Naturalistes 16, 127–130. Ovalis have provided samples and observations that have Forbes E. (1844) Report on the Mollusca and Radiata of the Aegean Sea, proved useful for this short article. Gloria Malavolta measured and on their distribution, considered as bearing on Geology. In: Report the specimens from Monte Argentario, Tuscany. The visit to 13th Meeting, British Association for the Advancement of Science. the Museum fu¨r Naturkunde was supported by a Synthesys London: John Murray, pp. 130–193. grant (DE-TAF-3510). Matthias Glaubrecht and Christine Gmelin J.F. (1791) Caroli a Linnaei Systema Naturae per Regna Tria Zorn helped greatly during their stay at the Museum. Data Naturae, Editio Decima Tertia, Aucta Reformata. Tome 1, Pars 6 and useful information was provided by Paul Callomon, (Vermes). Leipzig: G.E. Deer. Academy of Natural Sciences of Philadelphia. Hantzsch V. (1907) Roth, John. In: General German Biography, pp. 530– 533 [online version]. Available at: http://www.deutsche-biographie.de/ pnd116638028.html?anchor=adb (accessed 22 October 2014). REFERENCES Kendall M.A. (1987) The age and size structure of some northern popula- tions of the trochid gastropod Monodonta lineata. Journal of Albano P.G. (2010) Further northward extension of the distribution of Molluscan Studies 53, 213–222. Echinolittorina punctata (Mollusca: Gastropoda) along the Italian Tyrrhenian coastline: new stations in Lazio. Cahie´rs de Biologie Kendall M.A. & Lewis J.R. (1986) Temporal and spatial patterns in the Marine 51, 201–204. recruitment of Gibbula umbilicalis. Hydrobiologia 142, 15–22. new records of echinolittorina punctata 5

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