The genus Alvania (Gastropoda: Rissoidae) along the Turkish Aegean coast with the description of a new species

Summary : This study deals with the distribution of the species of the genus Alvania along the Turkish Aegean coast. The investigated material was collected from different habitats (soft and hard bottoms, and macrophyte beds) at a depth range of 0-875 m, at 39 stations along the Aegean coast of Turkey between 1995 and 2014. Among the analysed benthic material, 537 living specimens and 249 empty shells belonging to 20 species of the genus Alvania were obtained. Alvania marmarisensis is described as a new species. Alvania hispidula was recorded for the first time from the Turkish Aegean coast. Alvania mamil- lata was found to be the most widely distributed species in the study area, while Alvania colossophilus was the rarest one. Alvania cimicoides and Alvania testae were found in the deepest samples (between 93 and 875 m). Certain taxonomic and ecological characteristics of the identified species, along with photographs, are also provided.


INTRODUCTION
The Aegean Sea is an ecologically distinct part of the Mediterranean Sea due to its peculiar hydrographic characteristics. It is an area where the brackish waters of the Black Sea (17‰) merge with the saline waters of the eastern Mediterranean Sea (39‰) (Öztürk et al. 2006). According to Kocataş and Bilecik (1992), ecological features such as temperature, salinity and nutrients fluctuate significantly in the southern Aegean Sea due to the influence of the eastern Mediterranean Sea, and in the northern Aegean Sea due to the influence of the Black Sea. This ecological variation affects the biota in the area.
The genus Alvania Risso, 1826 belongs to the family Rissoidae, which is represented by a high number of genera and species in the northeast Atlantic and Mediterranean Sea (CLEMAM 2016). Alvania species are characterized by their typical clathrate sculpture on the teleoconch; ovate-conical shell with axial ribs, and spirals and nodules on their intersections varying according to the species. Alvania are differentiated from other rissoids by having either axial and spiral lines, or cords, on the surface of the teleoconch. The representatives of the genus have a worldwide distribution, with the exception of the Antarctic Ocean and sub-Antarctic regions (Ponder 1985), and most of the species (about 70%) inhabit the littoral depths, although some of them can be found in deeper areas (Avila et al. 2012). The Alvania species inhabiting shallow depths feed mostly on periphyton of macrophytes, whereas some bathyal species [e.g. Alvania testae (Aradas and Maggiore, 1844), Alvania jeffreysi (Waller, 1864) and Alvania cimicoides (Forbes, 1844)] feed on the detritus and foraminifers (Fretter andGraham 1978, Ponder 1985).
Comprehensive revisions of the Rissooidea based on morphological characters have been published by Coan (1964) and Ponder (1985). Recently, a phylogenetic analysis of this family testing the diagnostic utility of morphological traits was conducted by Criscione et al. (2016).
The genus Alvania has been the subject of several studies in the Mediterranean Sea (e.g. van Aartsen 1982a, b, c, Amati 2014, where 74 Alvania species are present according to Avila et al. (2012). However, few works include taxonomic or ecological information on the representatives of this genus in the eastern Mediterranean (van Aartsen et al. 1989, Cecalupo andQuadri 1996).
The aim of this study is to contribute to the knowledge of the Alvania species distributed in the Turkish Aegean Sea, including information on their taxonomy, bathymetric distribution, preferred habitats and patterns of distribution. Special attention has been paid to the protoconch due to its importance as a taxonomic character. It can be used to deduce the type of larval development, which has implications for the potential dispersal capacity of larvae in the distribution areas. A multispiral protoconch (typically with more than 2 whorls) suggests planktotrophic larval development, while a paucispiral protoconch (fewer than 2 whorls) is indicative of non-planktotrophic larval development.

MATERIALS AND METHODS
The Alvania specimens investigated in this study were collected during various cruises or research projects conducted along the Aegean coast of Turkey between the years 1995 and 2014. The samples were taken from various substrates [sand, mud, mixture of sand and mud, coralligenous, algae (Padina pavonica, Cystoseira amentacea, C. crinita, C. foeniculacea f. schiffneri, C. spinosa, C. elegans, C. compressa, Halopteris scoparia, H. filicina, Ulva linza), phanerogams (Posidonia oceanica, Zostera noltei, Z. marina, Cymodocea nodosa), the sponge Aplysina aerophoba, the scleractinian coral Cladocora caespitosa, the fan shell Pinna nobilis and rocky bottoms] at depths ranging from 0 to 875 m at 39 stations ( Fig. 1, Table 1). Benthic samples (10-875 m) were taken by means of a dredge and van Veen Grap, while the shallower water materials (0-10 m) were collected by snorkelling and hand picking. The sampled material was sieved through 0.5 mm mesh and the retained material was fixed in 5% formalin solution. The Alvania specimens were separated from the other benthic materials using a stereomicroscope.
Some shell features of the investigated species, such as total height (H) with standard errors, mean diameter (D) with standard errors, mean height (h) of the last whorl with standard errors and minimum and maximum values for each species [.....] are presented in the following order: The protoconch whorls of the investigated species were counted according to Warén (1974) and Verduin (1984), while the relevant specimens have been deposited in the museum of the Faculty of Fisheries (ESFM), Ege University (Izmir-Turkey).

RESULTS
As a result of the study of the material collected along the Turkish Aegean coast, we identified 537 specimens and 249 shells belonging to 20 species of   Oliverio, 1986 (Fig. 2A, B) Alvania amatii Oliverio, 1986 Mean dimensions (1 specimen and 3 shells): 2.02 (±0. Remarks. Alvania amatii is characterized by its smaller shell dimensions and paucispiral protoconch having 5 spiral threads.

Remarks.
A. beanii has a multispiral protoconch. It differs from the similar A. hispidula in its greater number of spiral cords on the penultimate and last whorls of the teleoconch.
Remarks. The species can be confused with A. lanciae (Calcara, 1845) and with the juveniles of A. discors, but A. bozcaadensis has no microsculpture on the surface of its protoconch and teleoconch, whereas A. lanciae bears microsculpture on both its protoconch and teleoconch. It differs from A. discors because the protoconch of the later species has a multispiral proto-  Remarks. Alvania cancellata is one of the most common and characteristic species of the genus, be-cause of its typical shell structure, large nodule on the base of the columella and multispiral protoconch.
Distribution. Northeast Atlantic Ocean and Mediterranean Sea (Fretter andGraham 1978, Gofas 2007  Remarks. Alvania carinata can be easily distinguished by the strong spiral sculpture of its teleoconch and paucispiral protoconch.

Remarks.
A. cimex is quite similar to A. mamillata, but they differ in the number of whorls of their protoconchs. The protoconch of Alvania cimex consists of 2-2.3 whorls, compared with about 1.3 whorls in A. mamillata. However, the protoconch figure given by Gianuzzi-Savelli et al. (1997: 100, fig. 395a) for A. cimex does not seem to belong to this species.
It is stated that the number of protoconch whorls was used as a discriminating feature of the shells, but according to some studies (Oliver et al. 2015, Criscione et al. 2016) the protoconch features do not suffice for correct identification. Oliver et al. (2015) considered that A. cimex and A. mamillata may be the same species because they have the same distribution, habitats and colour patterns, except for the larval life span. Similarly, Criscione et al. (2016: Fig. 2) stated that the two species shared the same 16S and 28S sequences in the maximum-likelihood phylogram. In this study, we have considered the two species as different taxa, following the current WoRMS (2016) and CLEMAM (2016) databases. Future genetic studies on the larval development of these two species should clarify this aspect. (Barash and Danin 1992). Turkish coasts: Levantine Sea (Buzzurro andGreppi 1996, Bitlis Bakır et al. 2012), Aegean Sea (Kocataş 1978), Sea of Marmara (Oberling 1969(Oberling -1971 and Black Sea (Öztürk 1998). (Forbes, 1844) ( Remarks. This species is characterized by its dark brown-coloured and multispiral protoconch. It is distributed mostly at bathyal depths.

Remarks.
A. colossophilus may be confused with A. lineata, but the first species differs in the sculpture of its paucispiral protoconch and the stronger and larger size of the shell. Distribution. The species appears to be an eastern Mediterranean endemic (Bogi et al. 1989, Gianuzzi-Savelli et al. 1997. Turkish coasts: Levantine Sea (Buzzurro andGreppi 1996, Bitlis Bakır et al. 2012) and Aegean Sea (Okuş et al. 2006). Amati and Oliverio, 1987 ( Fig. 4G, H) Alvania datchaensis Amati and Oliverio, 1987 Mean dimensions ( Remarks. It can be distinguished from the other similar Alvania species by the sculpture of its paucispiral protoconch with zigzag spiral lines, and the outer lip without labial varix.

Alvania datchaensis
Distribution. It is endemic to the eastern Mediterranean Sea (Cecalupo andQuadri 1996, Amati 2012). Turkish coasts: Levantine Sea (Buzzurro and Greppi 1996) and Aegean Sea Oliverio 1987, van Aartsen andKinzelbach 1990 Remarks. The species is characterized by its polymorphic shell with a variable number of axial ribs (11-12) and spiral cords (8-9) on the last whorl. The protoconch is multispiral, and its shell may be completely brownish or with white bands.

Alvania hispidula (Monterosato, 1884) (Fig. 3A-C)
Acinus hispidulus Monterosato, 1884 The shell is solid with 4 convex teleoconch whorls and deep suture. Protoconch is multispiral. On the last whorl, above the aperture, there are 10-14 axial ribs, and 3 spiral cords on the last and penultimate whorls. There is a noteworthy distance between the first spiral cords and the suture. Remarks. Alvania hispidula is similar to A. beanii but differs in the number of spiral and axial ribs on the last whorl. Alvania beanii has a smaller shell and 6-7 spiral cords on the last whorl above the aperture, instead of 3 spirals in A. hispidula (4 in the penultimate whorl). The protoconch of A. hispidula (Fig. 3C)

and
A. beanii (Fig. 3D) are similar, but the protoconch of A. beanii has micro papillae.

Distribution. Atlantic Ocean and Mediterranean
Sea (van Aartsen 1982a). Turkish coasts: Sea of Marmara (Ostroumoff 1896) and Aegean Sea (this study). (Michaud, 1832) ( Fig. 5A Remarks. A. lactea differs markedly from the other species of the genus in its shell sculpture and large aperture. The protoconch is paucispiral.

Alvania mamillata
There are uncertainties about the synonyms of A. scabra. According to the Checklist of European Marine Mollusca (CLEMAM 2016), A. oranica was regarded as a synonym of A. scabra. van Aartsen (1982c) examined this idea and remarked that the mean difference between A. scabra and A. oranica consisted in having a fourth spiral (always) in the subsutural area of A. oranica, which is rarely found in A. scabra. In addi-tion, Tringali (2001) indicated that the original description and figure of A. oranica given by Pallary (1900: 322, pl. 7, Fig. 4) was inadequate and still unclear and, due to this fact, A. oranica might be a synonym of A. sculptilis but not of A. scabra. Tringali (2001) also underlined that the figure of A. oranica provided by Gofas (1990: 130, Fig. 58) did not belong to A. oranica. He also stated that the figure of A. scabra in the study by van Aartsen et al. (1984) belongs to A. sculptilis (Monterosato, 1877) instead of A. scabra. In this study, we agree with Tringali's opinion about the original description of A. oranica, which is insufficient and requires improvement. Distribution. Mediterranean Sea (van Aartsen 1982c, Gofas et al. 2011). Turkish coasts: Levantine Sea (Buzzurro and Greppi 1996) and Aegean Sea (van Aartsen and Kinzelbach 1990). Remarks. Alvania testae is characterized by its shell shape. The shell is narrow and conical with 5-6 convex teleoconch whorls. Its protoconch is paucispiral. Aperture is roundish and outer lip opisthocline.
Description. Shell (holotype): Conical in shape, not very solid, with 4.5 less convex teleoconch whorls. Protoconch (holotype) is paucispiral (~1.25 whorls) and its nucleus diameter is about 0.150 mm. It has irregular spiral lines with rounded micro papillae in the interspaces.
Teleoconch (holotype) has four spirals on the penultimate whorl, 15 axial ribs in the last whorl, 4 spiral cords above the aperture, and 5 spirals on the base. The suture is deep, with a slope between the first and second spiral cords in the penultimate and last whorls. It has small granules at the intersections of the axial ribs, with spiral cords on the teleoconch whorls. There are also fine growth lines on the teleoconch. The aperture is large and ovate. The outer lip is thickened, with 7 internal denticles. It is light-brown coloured, while the apex is often darker. The soft parts and operculum were not examined.
Remarks. Among the species distributed along the Turkish Aegean coast, A. marmarisensis has some similarities with A. beanii, A. geryonia and A. mamillata (Fig.  7). However, it differs from A. beanii and A. geryonia in the number of protoconch whorls and rounded irregular micro papillae. The teleoconch whorls of A. beanii are more convex and have a greater number of axial ribs (24-26) and spiral cords (6-7). Alvania geryonia has a differently shaped teleoconch, with nearly flat whorls, and 5 spirals on the penultimate whorl. The protoconch of A. marmarisensis is also similar to that of A. mamillata (Verduin 1986: 28, Fig. 3;Oliver et al. 2015: 114, Figs 9, 10, 12, 13), but differs from A. mamillata in being more rounded and having large micro papillae on the protoconch whorls. On the other hand, A. mamillata has a more solid shell and a higher number of axial ribs on the last teleoconch whorl (14-20), and coarser granules at the intersections of the axial ribs with the spirals.
A. marmarisensis differs from A. hallgassi in having fewer axial ribs on the last whorl (13-17 against 15-40) and no coloured stripes on the whorls. Apart from the differences in the teleoconch, A. marmarisensis has a lower number of protoconch whorls (1.15-1.25 against 1.5 in A. hallgassi) bearing micro papillae in the interspaces between the spirals, which are smooth in A. hallgassi (Amati and Oliverio 1985: 34, Figs 1, 2).
The protoconch of A. marmarisensis is similar to that of A. dianiensis, except for the protoconch whorls (1.5) (Oliverio 1988: 120, Figs 2-7). Alvania marmarisensis is also larger (h=2.3-3.5 mm) and has a higher number of teleoconch whorls (4-4.5) than A. dianiensis (h=2-2.4 mm and 3.2 whorls). Alvania marmarisensis also bears a higher number of spiral cords on the last whorl (8-9 against 6-7), and 4 spirals against 3 spirals above the aperture. There are four spirals on the penultimate whorl in A. marmarisensis against 3 spirals in A. dianiensis. The other difference between the aforementioned two species regards the microsculpture of the teleoconchs; A. marmarisensis has only fine growth lines contrary to fine spiral striae in A. dianiensis (Oliverio 1988, Romani 2014).
There are also differences in the distribution areas and bathymetric ranges among A. marmarisensis and similar species (Table 3). With the exception of A. marmarisensis and A. dalmatica, all of the mentioned species were collected from infralittoral depths. Alvania marmarisensis was found at a depth of 99 m along the Aegean Sea coast (Marmaris) and Alvania dalmatica was recorded from the coasts of Croatia, Greece and the Adriatic Sea at depths ranging from 40 to 90 m (Buzzurro andPrkic 2007, Romani 2014). As regards the species that are similar to A. marmarisensis, A. dianiensis was reported from the Tyrrhenian, Ligurian and Adriatic Seas, from algal beds at depths ranging from 18 to 48 m (Oliverio 1988, Romani 2014, whereas Alvania hallgassi was described from infralittoral depths of the Ionian Sea (down to 20 m) (Amati and Oliverio 1985). This last species was also reported from Sicily, the Adriatic Sea, the Tyrrhenian Sea and the coasts of Cyprus , Cecalupo and Quadri 1996, Romani 2014. Alvania oliverioi was found along the Cypriot coastline at a depth of 4 m (Buzzurro 2003).

DISCUSSION
Among the analysed benthic material, we sorted 537 living specimens and 249 empty shells belonging to 20 species of the genus Alvania. Of the identified species, Alvania marmarisensis is described as a new species. The new species was only recorded near Marmaris at station 39.1 in muddy material sampled at 99 m depth.
A. mamillata was the commonest species, found at 18 stations in the Aegean Sea, followed by A. discors, found at 15 stations, whereas A. colossophilus was the rarest species with only one specimen found at station 27 (Table 2).
Alvania discors was the most abundant species, with 218 specimens and 82 shells, followed by A. datchaensis (52 specimens and 17 shells). However, A. bozcaadensis, A. carinata and A. colossophilus were only represented by a few specimens or shells (Table 2).
Bitlis Bakır and Öztürk (2016) investigated Rissooidea species distributed along the Turkish Levantine coast and reported 15 Alvania species, which have also been examined within the context of this study. A. beanii (60-1302 m) and A. testae (100-200 m), which were sampled at circalittoral and bathyal depths in the mentioned study, were encountered in our study at depths between 23 and 100 m and 93 and 875 m, respectively.