An account of the taxonomy and distribution of Syllidae (Annelida, Polychaetes) in the eastern Mediterranean, with notes on the genus Prosphaerosyllis San Martín, 1984 in the Mediterranean

Abstract The syllid fauna of three locations in Crete and Israel (eastern Mediterranean Sea) was studied, yielding 82 syllid species, many of which were found for the first time in the respective areas: Seventeen species were recorded for the first time on the Israeli coasts and 20 in Greek waters. Perkinsyllis augeneri (Hartmann-Schröder, 1979) and Prosphaerosyllis chauseyensis Olivier et al., 2011 are new records for the Mediterranean Sea. Detailed information is given on the morphology, ecology and distribution of the species recorded for the first time in the studied areas. In addition, an update on the distribution of the genus Prosphaerosyllis San Martín, 1984 in the Mediterranean is given and an identification key to the Mediterranean species is provided.


Keywords
Polychaetes, Syllidae, eastern Mediterranean Sea, taxonomy, distribution, new records, alien species introduction The Syllidae are a highly diverse family of polychaetes with currently around 900 valid species belonging to over 80 genera (pers. obs.) and have recently received considerable taxonomic and phylogenetic research effort, including a high number of new taxon descriptions (e.g. , De Matos Nogueira et al. 2001, San Martín 2005, 2008, San Martín and Hutchings 2006). Syllids are (usually) small-sized polychaetes with a high diversity of morphological and ecological features and are found globally on all types of substrates from the intertidal to the abyss (San Martín 2003).
The present study contributes to the current knowledge of the syllid fauna of three different locations in the eastern Mediterranean Sea: two in Crete, one in Israel. The material has been collected in the framework of two different research programmes and from two different habitats (Fig. 1, Table 1): a) hard-bottom samples from Crete have been obtained within the NaGISA project (Natural Geography in Shore Areas, http://www.nagisa.coml.org), a field project of the Census of Marine Life (COML, http://www.coml.org); b) soft-sediment samples from the Israeli coast have been obtained in the framework of a project focusing on the soft bottom benthos of Haifa Bay. In all samples, Syllidae were highly abundant and yielded many species recorded for the first time in the respective area, as well as a species new to science (Faulwetter et al. 2011).
In the Mediterranean Sea, syllids have been studied by numerous authors in extensive taxonomic and biogeographic works (e.g. Ben-Eliahu 1977a, 1977b, Campoy 1982, Çinar 1999, San Martín 1984b, 2003, Musco and Giangrande 2005, however, most research on the taxon is being carried out in the western Mediterranean basin, whereas the syllid fauna of the eastern Mediterranean has only recently started to be investigated more intensely (e.g. Ben-Eliahu 1977a, 1977b, Çinar 1999, Çinar and Ergen 2002, 2003, Aguado and San Martín 2007, Abd-Elnaby and San Martín 2010. In Greece, polychaetes have been studied by various authors (e.g. Bellan 1964, Fassari 1982, Arvanitidis 1994, Simboura 1996, Simboura and Nicolaidou 2001, Antoniadou et al. 2004). However, the only studies in the Aegean Sea focussing specifically on Syllidae are those of Çinar (1999) and Çinar and Ergen (2002) from the Turkish Aegean coasts. Polychaetes of the Mediterranean coast of Israel have been studied by Monro (1937), Tebble (1959), Fauvel (1955Fauvel ( , 1957, Ben-Eliahu (1976a, 1976b, Ben-Eliahu and Golani (1990) and Ben-Eliahu and Fiege (1995) and syllids in particular by Harlock and Laubier (1966) and Ben-Eliahu (1977a, 1977b. This paper gives an account of the syllid species encountered in the three sampling locations and provides detailed information on the morphology, distribution and ecology of those species recorded for the first time in the respective area. Furthermore, during this study it became clear that the distribution range of the genus Prosphaerosyllis San Martín, 1984 in the Mediterranean is outdated or confused. In addition, since several new species have recently been described in this genus (Çinar et al. 2011(Çinar et al. , Olivier et al. 2011) and were also identified in the present material, an update on the distribution of the genus Prosphaerosyllis in the Mediterranean and an updated identification key are provided at the end of this paper.

Specimen collection and processing
Specimens from Israel were collected on 31 May 2009 and 11 Oct 2009 in Haifa Bay, (Israel, eastern Mediterranean Sea) from soft sediments of mixed grain sizes in shallow waters (Table 1). Sediment samples were taken with a Van-Veen grab (KAHLSICO, model WA265/SS214) 32×35cm, volume 20 l, penetration 20 cm. The sediment was preserved in buffered formalin 10% for 3-7 days, then sieved through a 250 µm mesh sieve and subsequently stored in 70% ethanol. In this study, only a subset of the collected material is presented.
Specimens from Crete were collected in September 2007 and June 2008 from two sites in northern Crete characterized by a continuous hard bottom habitat with dense algal coverage and a moderate wave exposure (Table 1). At each site, two vertical transects with sampling depths at 1 m, 5 m, 10 m, 15 m and 20 m were defined and five replicates were taken from each transect and depth. Samples were collected by means of SCUBA diving according to the NaGISA protocol (Iken and Konar 2003). A plexiglas frame (25 × 25 cm) with a net of 0.5 mm mesh size attached to its top opening was placed onto the rock and the surface within the frame was scraped off. The sample was collected by a manually operated suction device, supplied by air from an extra scuba tank. Large particles (>2 cm) were collected manually after suction. The samples were subsequently washed through a 0.5 mm mesh sieve, fixed and preserved in 99% ethanol.
Specimens were examined under an Olympus SZx12 stereomicroscope and an Olympus BX50 microscope and identified by employing the most recent literature on Syllidae (e.g. Nygren 2004, San Martín 2003, San Martín and Hutchings 2006. Illustrations in pencil were made by means of a drawing tube, subsequently scanned, imported into a graphic program (GIMP), re-drawn and saved as a vector graphic. All specimens are deposited in the invertebrate collection of the Institute of Marine Biology and Genetics, Hellenic Centre for Marine Research. Comparative material has been loaned by the Zoologisches Museum and Institut, Universität Hamburg, Germany, Ege University, Izmir, Turkey and the Muséum National d'Histoire Naturelle, Paris, France.
Information on habitat and global distribution of species was adopted from San Martín (2003), unless indicated otherwise, and updated with findings from this study. Information on species distribution among Mediterranean regions was adopted from Musco and Giangrande (2005) and updated according to recent literature and to findings from this study. Abbreviations for biogeographic regions used in the text are: MED (Mediterranean), WB (Western Basin), EB (Eastern Basin), CB (Central Basin), AD (Adriatic Sea), AS (Aegean Sea), BS (Black Sea), LB (Levantine Basin), following Arvanitidis et al. 2002who modified Por's (1989 system.

Electronic publication
This manuscript was prepared in a Virtual Research Environment (Scratchpads) allowing for rapid and simultaneous publication of the results in print as well as electronically in a semantically enhanced form . This publication and all supplementary data (tables, figures, taxon information) are also available under a Creative Commons license on the Polychaete Scratchpads (http:// polychaetes.marbigen.org).
The underlying dataset of this study has been published under a Creative Commons license according to the Pensoft Data Publishing Policies and Guidelines for Biodiversity Data (Penev et al. 2011) and are available through the GBIF Integrated Publishing Toolkit hosted by Pensoft (http://ipt.pensoft.net/ipt/resource. do?r=easternmedsyllids). The data are furthermore available in Darwin Core Archive format, a simple and extensible schema for sharing biodiversity data which has been developed by the Global Biodiversity Information Facility (GBIF, http:// www.gbif.org/informatics/standards-and-tools/publishing-data/data-standards/ darwin-core-archives/) to allow easy and rapid mobilisation of species occurrence data through the internet. Darwin Core Archives are essentially a set of text files stored together with an XML descriptor file which describes the structure of the data files. Data are described through the Darwin Core schema, allowing for their usage within the semantic web. This new type of data publishing allows data to be indexed and discoverable through global biodiversity infrastructures such as GBIF or other data repositories, allows data to be integrated and compared with other datasets and ensures proper accreditation of the data provider (Penev et al. 2011). Additionally, the data have been deposited in the Dryad Data Repository (http:// www.datadryad.org) and can be accessed at doi: 10.5061/dryad.4b7k408g.

Results
Examination of a total of 111 samples yielded 82 syllid species (Table 2), of which 49 were found in Alykes (Crete), 62 in Elounda (Crete) and 23 in Haifa Bay (Israel). Species of all subfamilies have been found in the stations in Crete, with the majority (80%) of species belonging to Syllinae and Exogoninae, whereas the samples from Israel did not contain any specimens of Anoplosyllinae or Autolytinae, and 73% of the examined species belong to the small-sized Exogoninae (Fig. 2). The material yielded a number of species reported for the first time in the studied areas: Twenty species are reported for the first time in Greek waters, of these, six are new additions to the Aegean fauna. Seventeen species are newly reported for the Israeli coast, of these, 4 are also new records for the Levantine Basin. The studied material yielded also 4 species which are new additions to the eastern Mediterranean and 2 to the Mediterranean fauna (Table 2, Fig. 3). Information on morphology, distribution and ecology of the newly recorded species are given below.
Distribution. East and west Atlantic (European and African coasts, Cuba), northeast Pacific, Red Sea (San Martin 1994, Nygren 2004). Mediterranean Sea: WB, CB, AD, AS, LB. New record for the Greek coast.
Remarks. The subfamilial affiliation of Perkinsyllis augeneri has not yet been fully resolved. In recent molecular phylogenies the species groups either within Exogoninae or as a sister group, and forms a sister clade of Eusyllinae in all analyses Bleidorn 2010, Aguado et al. 2007).
The morphological characters of the Mediterranean individuals agree well with the description of San Martín and Hutchings (2006) from Australia. Therefore, a detailed description of the specimens is unnecessary here. The Mediterranean specimens show slight differences from the description of the Australian ones in the length of the pharynx (6-7 chaetigers in Australian specimens vs 5 in Mediterranean ones), and the number of falcigers per bundle in anterior chaetigers (ca. 15 in Australian specimens vs ca. 10 in Mediterranean ones). These differences might however be attributed to fixation and / or individual variation.
Until now, the species had been known only from north-west Australia and New Zealand, while the record from the Carribean Sea (Hartmann-Schröder 1980a) is assumed to be a different species ). The present findings thus extend the distribution range of the species to the eastern Mediterranean Sea. Since there are no intermediate records of the species from the Indian Ocean or Red Sea, this disjunct distribution suggests a potential human-induced introduction of the species to the Mediterranean Sea by vectors such as ballast water or fouling fauna on the hulls of ships. However, since the polychaete fauna of the Indian Ocean, Red Sea and eastern Mediterranean Sea is understudied, the species might have a truly circumtropical distribution. This is the second record of an Australian syllid species for the Mediterranean Sea (after Prosphaerosyllis longipapillata (Hartmann-Schröder, 1979), recorded for the first time in 2003 in Cyprus (Çinar et al. 2003)).
Remarks. The specimens agree well with the description of San Martín (2003), except for having longer dorsal papillae (15 µm), especially posteriorly. Remarks. The specimens from Israel agree well with the specimens from Normandy, however, the Mediterranean specimens differ from the Holotype in: a) Papillation pattern: each segment with one papilla between dorsal cirri and four papillae, situated dorso-laterally and ventro-laterally on each side of parapodium, most developed in posterior chaetigers, from mid-body additional papillae arranged in two very irregular lines along middle of dorsum, increasing in length towards posterior end (ca. 20 µm posteriorly). Ventrally 2 smaller (about half the size of dorsal papillae) papillae in middle of ventrum at posterior end of each segment. Specimens from Normandy have an irregular papillation pattern, but papillation is more distinct laterally, as in specimens from Israel; b) Length of anal cirri: about 125 µm, ca. 2.5-3 times length of posterior dorsal cirri (Fig. 4) (the anal cirri are broken in the holotype and the large lateral anal papillae might have been erroneously regarded as anal cirri in the original description). Specimens from both locations have anterior dorsal cirri with two papillae (dorsal and ventral) and posterior dorsal cirri only with dorsal papilla (Fig. 5, not reported by Olivier et al. 2011).

Prosphaerosyllis chauseyensis
Individuals identified by Ben-Eliahu (1977a) as Sphaerosyllis tetralix Eliason, 1920, from the Gulf of Elat and the Mediterranean Sea might in fact belong to P. chauseyensis. The description and illustrations agree with many characteristics of P. chauseyensis, including the characteristic papilla on the dorsal cirri. However, Ben-Eliahu reports the species to have palps widely separated anteriorly (fused in P. chauseyensis), dor-sum with four longitudinal rows of papillae (irregular rows in P. chauseyensis) and the proventriculum stretching through 4 chaetigers (5 in P. chauseyensis). The material of the species described by Ben-Eliahu could not be examined during this study, therefore it can only tentatively be assigned to P. chauseyensis.
Habitat. Until 17 m depth, in muddy sand (Çinar et al. 2011), in coarse and mixed sand (this study).
Remarks. The specimens from Israel agree with the material of Çinar et al. (2011), except for the absence of eyespots (might be de-colourised due to fixation). The recently described P. laubieri Olivier et al. 2011 is very similar to P. marmarae. Both species have eyespots, strongly papillated palps, short, retractile antennae and dorsal cirri, pharynx and proventriculum each through 4 segments and short (8-10 µm) blades of falcigers. These two species differ however in the following characteristics: a) P. laubieri has small, scattered papillae all over the dorsum, in P. marmarae they are restricted to the lateral margins, near the dorsal cirri; b) cirrostyles of antennae and dorsal cirri of P. marmarae are much shorter (1/4 of total length) than those of P. laubieri (1/3 of total length) and appear as small, retracted caps; c) dorsal cirri of P. laubieri possess a small papilla at distal end of cirrophore (not reported by Olivier et al. 2011); d) falcigerous blades of P. marmarae are stouter than those of P. laubieri and serrated only at their bases (serrated all along cutting edge in P. laubieri). P. riseri Perkins, 1981 from Florida shares with P. marmarae the shape of the dorsal cirri and antennae (short and strongly retracted), however, its palps are less densely papillated. Prosphaerosyllis sp. A (San Martín 1991b) from Cuba has strongly papillated palps, but no cirri on chaetiger 2 and longer dorsal cirri.
Specimens from the Red Sea described by Ben-Eliahu (1977a) as Sphaerosyllis brevicirra Hartmann-Schröder, 1960 do not belong to this species (see Discussion section), but might in fact belong to P. marmarae. The morphological characteristics of her specimens agree very well wth those of P. marmarae (papillated palps, presence of eyespots, minute (19.5 µm), retractile cirri, falcigerous blades short (7.8 µm), proventriculum longer than proboscis (through 4 segments), no discernible dorsal papillation). Differences can be found in the cutting edge of the falcigerous blades which are smooth in the Red Sea specimens, whereas those of P. marmarae are serrated. However, due to the size of the blades (8 µm) this is a feature difficult to observe under an optical microscope and might have been overlooked. The material of the species described by Ben-Eliahu was not examined during this study, therefore it can only tentatively proposed to be assigned to P. marmarae.

Remarks.
Pionosyllis subterranea was synonymized with P. neapolitana and transferred to Grubeosyllis by Jiménez et al. (1994). San Martín (2003) subsequently replaced the name Grubeosyllis with Salvatoria, which has priority over the former. Habitat. Until 20 m depth, in sandy substrates, on rocks among algae.

Sphaerosyllis glandulata
Remarks. The specimens from Israel differ from San Martín's (2003) description in having papillated palps and a longer proventriculum (3-4 chaetigers vs 2 chaetigers in the Iberian material). Other characteristics, especially chaetal ones, agree well with former descriptions of S. glandulata. Habitat. Shallow subtidal depths, in medium to coarse sands, among algae.
Remarks. The examined specimens agree well with the description of San Martín (2003), especially in the chaeteal structures, but in the Israeli specimens the dorsal cirri are as long as parapodial lobes in posterior and midbody chaetigers and only slightly shorter than parapodial lobe in anterior chaetigers (dorsal cirri shorter than parapodial lobe in San Martín's (2003) description).
Distribution. Mediterranean Sea: WB, CB, AD, AS, LB. New record for the Aegean Sea.

Syllis pulvinata
Type locality. Canary Islands (Atlantic Ocean). Distribution. North-east Atlantic (Cantabrian Sea to Canary Islands), Red Sea, Mediterranean: WB, CB, AD, AS, LB. New record for the Aegean Sea.
Remarks. Specimens from Greece have a faint or no visible trepan. Individuals without trepan but otherwise identical to T. coeliaca have in the past been identified as Pseudosyllis brevipennis Grube, 1863, but according to San Martín (2003) the absence of the trepan can be attributed to a number of reasons, including loss, and P. brevipennis is regarded as a synonym of T. coeliaca.

Discussion
The present study yielded a number of species reported for the first time in the respective areas, and a high number of the new additions belong to the subfamily Exogoninae (Fig. 3). This could be explained by the fact that the small-sized individuals of this subfamily might have been overlooked in earlier works on the syllid fauna of the area which report only very few or no Exogoninae species at all (e.g. Fauvel 1957, Tebble 1959, Bellan 1964, Ergen 1976). The Exogoninae genus Prosphaerosyllis, which has recently been raised from subgeneric to generic level by San Martín (2005), has a difficult and confused taxonomy and several species have recently been described or transferred to the genus (Olivier et al. 2011(Olivier et al. , Çinar et al. 2011. Currently, 31 species of the genus are considered valid (including an unnamed one, see San Martín 2003), of which 11 have so far been reported to occur in the Mediterranean Sea (Table 3). However, several of the reported species in the area do in fact belong to other species, the identity of which can only be determined through thorough examination of the material in question. The presence of the Red Sea species P. brevicirra (Hartmann-Schröder, 1960) in the Mediterranean belongs to these doubtful records. Records of Sphaerosyllis brevicirra from the western Mediterranean Sea by Alós (1989) and from the Aegean Sea (Simboura 1996(Simboura , Çinar 1999 belong to an undescribed Prosphaerosyllis species (San Martín 2003). These differ from P. brevicirra by the absence of dorsal cirri on chaetiger 2 (reported as present in Alós' (1989) description but in fact absent (San Martín 2003)), the absence of the conspicious papilla on the dorsal cirrus and by thicker aciculae. Hartmann-Schröder (1960) does not mention the papilla on the dorsal cirrus in her description of the species (only visible in the illustrations, but confirmed through examination of type material); instead she focuses on the reduced length of the dorsal cirri as a character to distinguish the species from its congeners. This fact might have lead to confusion of P. brevicirra with other species possessing short dorsal cirri. Two other reports of the species from adjacent areas (Red Sea, Atlantic) likewise do probably not belong to P. brevicirra: Ben-Eliahu's (1977a) redescription of the species based on material from the Gulf of Elat (Red Sea) differs in several aspects from Hartmann-Schröder's (1960) descrip-  4= Gambi et al. 1995, 5= Alós 1989, 6= Somaschini et al. 1994, 7= Lanera et al. 1990, 8= Zenetos et al. 1997, 9= Simboura 1996, 10= Çinar 1999, 11= San Martín et al. 1982, 12= Çinar and Ergen 2002, 13= Çinar et al. 2003, 14= Somaschini and San Martín 1994, 15= Çinar et al. 2011, 16= Katzmann, 1983, 17= Ben-Eliahu 1977a. Literature-based works (e.g. Musco andGiangrande 2005, Simboura andNicolaidou 2001) are not included to avoid repetition of records.  (Eliason, 1920) Öresund, Sweden 3 16 8 17 § P. xarifae (Hartmann-Schröder, 1960) Sarso, Egypt, Red Sea 3 12 tion and from the type material. In particular, Ben-Eliahu does not mention or illustrate the papilla on the dorsal cirrus, her specimens have four eyes and one anterior pair of eyespots (eyespots, a character considered as invariable within species (Riser 1991), are absent in P. brevicirra) and the proventriculum occupies 4 chaetigers (3 in P. brevicirra). According to the description and illustrations, the species might in fact belong to P. marmarae (see remarks for this species above). The record of Sphaerosyllis brevicirra from the Spanish Atlantic coast (Parapar et al. 1994), though described as similar to Alós' (1989) specimens, differs in fact from these by the presence of dorsal cirri on chaetiger 2 and much longer dorsal cirri. It also differs from P. brevicirra in having falcigers with serrated blades in anterior chaetigers, no papilla on the dorsal cirrus and much longer dorsal cirri anteriorly (140 µm vs ca. 20 µm in P. brevicirra). The species P. brandhorsti (Hartmann-Schröder, 1965) has been recorded in Italy by Gambi et al. (1995). However, the only other records of the species apart from its type locality (Isla Mocha, Chile) are from the northern Pacific (Banse 1972) and belong possibly to possibly P. ranunculus (Kudenov and Harris, 1995). The presence of P. brandhorsti in the Mediterranean Sea has thus to be considered as doubtful. An identification key to the currently valid Mediterranean species of Prosphaerosyllis can be found below.