Serpulid species ( Polychaeta : Serpulidae ) from the Levantine coast of Turkey ( eastern Mediterranean ) , with special emphasis on alien species

The faunistic analysis of benthic samples taken from 0 to 200 m depths on the eastern Levantine coast of Turkey in September 2005 yielded the presence of 16 serpulid species, 9 of which are considered to be aliens: Hydroides brachyacanthus, H. diramphus, H. elegans, H. heterocerus, H. homoceros, H. minax, H. operculatus, Pomatoleios kraussii and Spirobranchus tetraceros. Ten species are new records for the Levantine coast of Turkey. Hydroides operculatus and P. kraussii formed dense populations on shallow-water artificial and natural hard substrates in the area. The population density and biomass (wet weight) of H. operculatus reached up to 384,000 individuals.m and 245.76 g.m in Mersin Bay and those of P. kraussii up to 52,000 individuals.m and 154.76 g.m in Iskenderun Harbour. The species with the highest frequency values at shallow water stations (0-5 m) were P. kraussii (50%), Pomatoceros lamarckii (50%), H. minax (42%), H. brachyacanthus (38%) and H. elegans (29%). Alien species were not found at depths deeper than 25 m. Alien species accounted for more than 85% of the serpulid specimens collected. Brief descriptions of the species, and their distributional, reproductive and ecological characteristics are given. In addition, population characteristics of the dominant species, H. operculatus and P. kraussii, are analyzed.


Introduction
Compared to other families of Polychaeta, the Serpulidae of the Levantine Sea have been relatively well studied: a total of 47 species belonging to 20 genera have been reported from the area (see Ben-Eliahu and Fiege 1996).In contrast, serpulids have only occasionally been reported from along and near the Turkish Levantine coast.Hitherto available data are due to Marenzeller (1895) from deep water off the Turkish coast (315-943 m), Ben-Eliahu and Fiege (1996) from the island of Kastellorizon (=Meis) and Ergen and Çinar (1997) from Antalya Bay.Up to now, 23 species of serpulids were thus known from or near the Turkish Levantine coast, this number including only one alien species (Hydroides elegans).This contrasts with 9 alien serpulid species reported from the coasts of Lebanon and Israel (Zibrowius andBitar 1981, Ben-Eliahu andten Hove 1992).Of these, Hydroides elegans and H. diramphus had come to the Mediterranean via shipping throughout the Strait of Gibraltar and are also known from the other parts of the Mediterranean (Zibrowius 1973a(Zibrowius , 1992)).Seven species were Erythrean aliens (=Lessepsian migrants) and have only colonized habitats of the Levantine Sea.However, Spirobranchus tetraceros had already expanded its distributional range as far as Rhodos by 1970(Ben-Eliahu 1991).
Serpulids, with their calcareous tubes, may become a nuisance in harbours or other disturbed environments, as they are able to form dense populations on fouling structures such as quay, mariculture equipment and ship hulls (Ben-Eliahu and ten Hove 1992, Relini 1993).They can also clog seawater intake pipes of industrial cooling systems.Various techniques to reduce or remove serpulid growth have been tried world-wide.However, in the nuisance context, one needs to identify the species in question and understand its bio-ecological requirements.Alien serpulids deserve special attention as they may be resistant to changing conditions.
The actual status of serpulids along the Lebanon and Israeli coasts appears to be adequately documented whereas only preliminary data were available for part of the marine fauna (including serpulids) along the much longer Turkish coastline that also comprises additional different habitats (e.g., Posidonia oceanica beds).To fill in the gap, a project funded by TUBITAK (The Scientific and Technological Research Council of Turkey, Project No: 104Y065) was carried out in fall 2005 along the Turkish Levantine coast to investigate the zoobenthic communities with particular attention to alien species.Note that a recent study by Çinar et al. (2006) had found nine previously unrecorded alien species from the area.
This paper presents some serpulid species of the eastern part of the Turkish Levantine coast, and focuses on aspects of their morphology, ecology and reproduction.As Hydroides operculatus and Pomatoleios kraussii formed dense populations in the area, some of population parameters are analyzed.

Material and Methods
A cruise to the Turkish Levantine coast was undertaken in September 2005 to collect benthic samples from different depths and habitats.The present study deals with samples taken from the eastern part of the Turkish Levantine coast including Iskenderun and Mersin Bays (Figure 1).Scuba diving and snorkeling were used at shallow water stations (ca.0-5 m).In deeper stations, sampling gear such as anchor dredge, a commercial bottom-trawl and a Van Veen grab were used.On board the ship, benthic samples were washed through a 0.5 mm mesh sieve and fixed with a 5% formaldehyde solution.In shallow-water stations, various substrates (i.e., stones, sand, algae, phanerogames) were sampled, using a quadrant of 20x20 cm.At all stations, small samples of rocks were collected with hammer.In harbours where serpulids formed dense populations, a quadrant with 5x5 cm or 10x10 cm was also used.The dates, coordinates, depths and habitat structures of stations were indicated in Annex.In the laboratory, materials were sorted under a stereomicroscope and serpulid species were identified and counted.Biometrical measurements of the largest specimen of each species, such as the body length, thorax width, length of radioles, length of peduncle plus operculum and length of distal blade of bayonet chaeta, and the number of thoracic and abdominal chaetigers, were made.The wet-weight of specimens (excluding tubes) was estimated by using a balance of 0.0001 sensitivity.Terminology used for descriptions of the species follow Bastida-Zavala and ten Hove (2002).All measurements were done using an ocular micrometer.
To characterize population structures of Hydroides operculatus and Pomatoleios kraussii in the area, the regression and Pearson Product-Moment Correlation analyses were performed to assess the relationship among the biometrical measurements taken.
The photographs of the serpulids were taken by a digital camera (Olympus, Camedia, C-7070) attached to stereo and compound microscopes.
Two specimens of Hydroides brachyacanthus collected from Ecuador and deposited in Zoological Museum of Amsterdam (ZMA) were examined and compared to specimens collected from the Levantine coast of Turkey.
The specimens are deposited in the Museum of the Faculty of Fisheries, Ege University (ESFM).

Results and Discussion
Benthos samples taken from 0 to 200 m depth in the eastern Levantine coast of Turkey comprised 16 serpulid species, 9 of which are considered to be aliens:   2D).Colouration (preserved specimens): Body pale yellow; operculum, area on thoracic and abdomen uncini dark brown; a pale brown band on constriction of peduncle (Figure 2A).
Colouration (preserved specimens): Body pale yellow; base of spines, area on thoracic uncini dark brownish; tips of radii and spines pale brown (Figure 3A); collor chaetae amber coloured.Distribution: Hydroides diramphus is a circumtropical species (Bastida-Zavala and ten Hove 2002) and considered to be an alien species for the Mediterranean Sea that was transferred via shipping from the tropical American Atlantic (Zibrowius 1992).This species has been previously recorded both from the western and eastern Mediterranean (Zibrowius 1971, Bianchi 1981, Zibrowius and Bitar 1981, Ben-Eliahu 1991).
Distribution: Hydroides elegans seems to be a circumtropical species, extending into the warmtemperate zone, and is considered to be an alien species for the Mediterranean Sea that travelled on ship hulls (Zibrowius 1992).This species is generally abundant in harbour environments in the Mediterranean Sea (Bianchi 1981, Koçak et al. 1999).
Hydroides heterocerus (Grube, 1868) (  with 26 radii, T-shaped with a pair of lateral points; verticil with 7 spines, curved inwards; dorsal spine larger than others, without lateral spinules; others with a pair of lateral spinules directed downward; spines with one short basal internal spinule (Figure 4A, B).Collar chaetae including 5 amber-coloured bayonet chaetae, 5 capillary chaetae; bayonet chaetae with two pointed-elongate teeth, distal blade 370 µm long (Figure 4C).Tube whitish, with three longitudinal ridges.Juveniles of Brachidontes pharaonis and filamentous algae were found attached to the operculum of a large individual.Colouration (preserved specimens): Body pale yellow; operculum and peduncle brownish (Figure 4A); base of radioles with a dark brown band.
Distribution: This species was previously found in the Indian Ocean (Wesenberg-Lund 1949), Red Sea, Suez Canal and Mediterranean Sea, and is an Erythrean alien (Ben-Eliahu and ten Hove 1989, Ben-Eliahu 1991).
Distribution: This species has been recorded from the Pacific Ocean, Indian Ocean, Red Sea and Mediterranean Sea, and is considered to be an Erythrean alien (Imajima 1976, Zibrowius andBitar 1981).
Distribution: Hydroides operculatus was previously reported from the Indian Ocean (type locality: coast of Somalia, Gulf of Aden) (Treadwell 1929) and the Mediterranean Sea (Zibrowius andBitar 1981, Ben-Eliahu 1991, Ben-Eliahu and ten Hove, 1992).This species was first reported as Hydroides cf.dianthus (Verrill, 1871) by Ben-Eliahu (1976) in the Mediterranean Sea (see Ben-Eliahu 1995).As it has not been reported in the Red Sea and Suez Canal, its presence in the Mediterranean Sea could not be simply explained by the migration through the Suez Canal, though Ben-Eliahu and ten Hove (1992)  Notes: Specimen incomplete, with anterior fragment.Thorax 6.2 mm long, 0.8 mm wide, with 6 chaetigers.Collar without chaetae, with two lateral belts composed of amber-coloured granules (Figure 7C).Branchial crown 4.8 mm long, with 28 radioles.Peduncle plus operculum 5 mm long; operculum cup-shaped, with an enlarged part and horny concave plaque distally (Figure 7B).Colouration (preserved specimens): Body pale yellow; operculum dark brown distally (Figure 7B).
Distribution: This species occurs in the Atlantic (type locality: coast of Norway), Mediterranean Sea and Japan (Imajima 1978).
Distribution: This species has been previously reported from the eastern Atlantic and Mediterranean Sea (Bianchi 1981).
Distribution: This species was previously found in the Atlantic Ocean and Mediterranean Sea (Bianchi 1981).
Distribution: Although Bianchi (1981) assumes a cosmopolitan distribution for this species, ten-Hove and Jansen-Jacobs (1984) regard the taxon to be a complex of species, each with more restricted distributions.
Distribution: This species was known from the Caribbean Sea, tropical Pacific coast of America, Malaysian Archipel, Indian Ocean, Red Sea, Japan and Mediterranean Sea [ten Hove 1970;Laubier 1966(as Spirobranchus giganteus coutierei Gravier, 1908)], and is considered to be an Erythrean alien (Ben-Eliahu and ten Hove 1992).infundibulum to the Mediterranean/Atlantic taxon, not Indo-Pacific.
Distribution: This species occurs in the northeast Atlantic Ocean and Mediterranean Sea (Bianchi 1981).

Population structure of Hydroides operculatus and Pomatoleios kraussii
Five parameters (total length, thorax width, peduncle plus operculum length, number of radioles and individual wet weight) taken on 45 undamaged specimens of Hydroides operculatus at station K14 were analyzed by using regression and correlation analyses (Figure 10).The lengthweight relationship was exponential.The growth seems to be allometric (i.e., phenomenon whereby parts of the same organism grow at different rates) for H. operculatus as the parameter b (1.62) is lower than 3.A linear relationship was found between total length and other parameters measured.The correlation coefficients between parameters were positive and significant (p<0.05).The total length of the specimens of H. operculatus ranged from 2.9 mm to 13.3 mm and the wet weight from 0.1 mg to 1.9 mg.The highest length frequency value (20%) was estimated between 9 and 10 mm, and the highest weight frequency value (20%) was between 0.2 and 0.4 mg, and 0.4 and 0.6 mg.The relationships between the biometrical measurements of Pomatoleios kraussii were presented in Figure 11.The length-weight relationship was exponential and the growth seems to be allometric for P. kraussii; the parameter b is 2.48.A linear relationship was found between the total length and the other parameters measured.The correlation coefficients between parameters were positive and significant (p<0.05).The total length of specimens of P. kraussii ranged from 1.8 mm to 10.2 mm and the wet weight of specimens from 0.6 mg to 16.5 mg.In the population examined (at station K15), specimens with 5-6 mm total length (15%) and 2-4 mg wet weight (20%) were dominant.

Biomass and density of Hydroides operculatus and Pomatoleios kraussii
Two quantitative samples were taken to determine the density and biomass of Hydroides operculatus on the Turkish Levantine coast; on a tire at station K13 and on a stone at station K14.At station K14 (Karaduvar harbour), the surface of the tire submerged into the sea was completely covered with tubes of Hydroides operculatus, reaching up to 54,800 individuals.m - and 103.36 g.m -2 (Figure 12D).The surface of a stone found on the sandy bottom at station K13 (Kazanli beach) was completely covered with specimens of H. operculatus.The population density and biomass values were 384,000 individuals.m - and 245.76 g.m -2 , respectively (Figure 12D and F).This species was previously found on various mollusc species, coralligenous concretions, rocks and artificial substrates between 0 and 6 m depth on the Israeli coast (Ben-Eliahu and ten Hove 1992).However, a high population density of H. operculatus such as found in this study has not been encountered before; in maximum 15 specimens were found on an artificial substrate on the coast of Israel (Ben-Eliahu and ten Hove 1992).
Three quantitative samples were taken to determine the population density and biomass of Pomatoleios kraussii; on a tire at station K13, and on rocks in Iskenderun Harbour and at station K15.The density and biomass values of P. kraussii were 25,600 individuals.m - and 79.20 g.m -2 at K13, 52,000 individuals.m - and 154.76 g.m -2 in Iskenderun Harbour, and 31,375 individuals.m - and 80.25 g.m -2 at K15, respectively.Imajima (1976) reported that it formed a densely populated belt on coral reefs in shallow water sheltered areas of the southwest Japan.Ben-Eliahu and ten Hove (1992) first reported it from the Mediterranean Sea, based on few specimens collected in 1958 on molluscs, under rocks and artificial fouling panels in 0-6 m depth along the Israeli coast.However, such a dense population as presented in this study has not been described from the Mediterranean before.Miura and Kajihara (1984) pointed out that P. kraussii preferred natural substrate (rocks) whereas artificial substrates were particularly dominated by Hydroides ezoensis Okuda, 1934 and H. elegans.In this study, this species occurred on both artificial and natural substrates, and much preferred polluted areas such as harbours.

Reproduction features of the species found
In the present study, undertaken in September 2005, some species were found to be within their reproductive period.The posterior-dorsal surface of the abdomen of the largest specimen of Spirobranchus tetraceros at station D5 had a clump of eggs; maximum-minimum diameter= 52-90 µm, mean=75.5µm±1.81SE,n=20 (Figure 9E), which is distinctly larger than those mentioned by Kupriyanova et al. (2001) (60 µm) and Selim et al. (2005) (78 µm).Only one specimen of Pomatoleios kraussii had eggs in its coelomic cavity; minimum-maximum diameter= 40-60 µm, mean= 51.2 µm±1.4SE.Miura and Kajihara (1984) determined the reproductive period of P. kraussii between May and August on the Japan coasts and stated that the mature worms decreased in number in September and October.
Only one specimen was found with eggs among the material examined.However, a number of juveniles in populations of P. kraussii in the area may indicate that the reproductive period of this species takes place in summer on the Levantine coast.One specimen of Serpula concharum had eggs in its coelomic cavity; minimum-maximum diameter= 70-100 µm, mean= 84.7 µm ±1.98 SE).Eggs were found on the anterior end of the thorax and bases of radioles of a specimen of Pomatoceros triqueter: minimum-maximum diameter= 50-62µm, mean=57.3µm±0.93SE,n=20.The specimen of Placostegus tridentatus at station D32 possessed eggs in its coelomic cavity (minimum-maximum diameter = 70-120µm, mean=108.5µm± 3.5SE, n=15).No reproductive products were reported on specimens of the other species found in this study.

Impacts of alien serpulid species
Pomatoleios kraussii formed a calcareous belt together with an alien bivalve species, Brachidontes pharaonis, on a rock at station K15 (Figure 12B and C).The thickness of the belt was approximately 3-5 cm.Rocks in 0-1 m depths in Iskenderun Harbour were largely covered with this species (Figure 12A).In Mersin Bay, the population density of Hydroides operculatus was very high, covering almost all available surfaces of a stone found in 2 m at station K14 and a tire at Karaduvar Harbour (K13).These two species were also observed on hulls of fishing boats in harbours, indicating that they have a potential to cause economic trouble to ship owners and others using sea-water intake pipes.
The dominant serpulid species (Hydroides dianthus and H. elegans) of hard bottom communities of harbour environments in other parts of the Mediterranean (Zibrowius 1992;Koçak et al. 1999) were absent (H.dianthus) or represented by a few specimens only (H.elegans) in the present study.Hydroides dianthus has not also been reported from the Levantine coasts of Israel and Turkey (Ben-Eliahu and Ten Hove 1992, Ben-Eliahu and Payiatas 1999, Çinar 2005).This species was known to be introduced to the Mediterranean from the northern American Atlantic by shipping (Zibrowius 1992).The absence of this species in harbours of the Levantine Sea could be due to the fact that it cannot survive in high temperature and salinity conditions of the Levantine Sea or that it had been out-competed from the area by other alien serpulid species.However, Ghobashy and Ghobashy (2005) reported H. dianthus on panels submerged in Alexandria Harbor (Egypt) and also found it in the Suez Canal.In contrast, Pomatoleios kraussii and Hydroides operculatus, which were dominant components of benthic communities in Iskenderun and Karaduvar harbours, have not yet been reported from outside of the Levantine Sea, indicating the biotic difference between the Levantine Sea and other parts of the Mediterranean.
Individuals of Pomatoleious kraussii in Iskenderun Harbour were attached to rocks by their whole tube length, whereas individuals of P. kraussii at station K15 were erect in form, attached to rocks only by posterior parts of their tubes (Figure 12).At station K15, erect tubes of P. kraussii provide them more free spaces among specimens of Brachidontes pharaonis.The potential competitors of P. kraussii in Iskenderun Bay for space might be the barnacle Balanus amphitrite (Darwin, 1854) and limpets Patella spp.

Alien serpulid species in the Levantine Sea
All alien serpulid species previously known from the Levantine Sea were also found in this study; Hydroides brachyacanthus, H. elegans, H. diramphus, H. homoceros, H. heterocerus, H. minax, H. operculatus, Spirobranchus tetraceros and Pomatoleios kraussii (see Ben-Eliahu and Fiege 1996).Among these species, only H. elegans and H. diramphus are considered to be ship-borne invasive species (Zibrowius 1992), the others as Erythrean aliens (Ben-Eliahu and ten Hove 1992).However, as discussed previously, H. operculatus might have been introduced to the Mediterranean by shipping as it has not been reported from the Red Sea yet.It forms very dense populations only near Mersin Harbour (Turkey).In addition, H. brachyacanthus could be also a ship-borne species as it is absent-as far as known yet-in the Red Sea.However, Zibrowius (1979) found all alien species mentioned above on ship's hulls.

Alien species vs. native species
A total of 9 species, out of 16, were found to be alien species.The percentage of alien species in total serpulid species found in this study was 56%.The value is very high when compared to the percentage of alien polychaetes in the total number of polychaetes found in the Levantine Sea (9%) (Ben-Eliahu, 1995) and on Levantine coast of Turkey (4.6%) (Çinar et al. 2005).The alien serpulid species dominated rocks, molluscs (Brachidontes pharaonis, Thais rugosa and Spondylus gaederopus) and artificial substrates (i.e.dock's pilings, ropes and tires), comprising more than 95% of the specimens found in these habitats (Figure 13).On the algae such as Ulva sp. and Cystoseira sp.sampled in this study, alien species accounted for more than 85% of the specimens (Figure 13).

Habitat and depth preferences of alien species
Figure 14 shows the percentages of abundance and presence of the alien species in habitats.Pomatoleios kraussii was found in all shallow water habitats examined, whereas Hydroides heterocerus, H. homocera and Spirobranchus tetraceros occurred only on rocks or stones.Of the nine alien species, six were collected on artificial substrates in or outside harbours.However, Hydroides elegans and H. diramphus particularly dominated artificial substrates in harbours.Ben-Eliahu and ten Hove (1992) reported the occurrence of the alien species such as P. kraussii, H. homoceros, H. brachyacanthus and H. operculatus on mollusk substrates.
The majority of the alien species were found in shallow waters (0-5 m) and only Spirobranchus tetraceros was collected at depths ranging from 0 to 25 m.No alien species was found at depths deeper than 25 m.The alien serpulid species in the Levantine Sea were generally reported from 0 to 45 m depths (Ben-Eliahu and Fiege 1996), except for H. heteroceros, which was reported from 830 m off the Israeli coast on the surface of the sponge Sarcotragus cf.muscarum Schmidt, 1864 (Ilan et al. 1994).A total of 5 species were found to live in depths deeper than 25 m: Placostegus tridentatus, Pomatoceros triqueter, Serpula vermicularis, Vermiliopsis infundibulum and V. striaticeps.Of these, S. vermicularis was solely collected at 60 m and P. tridentatus at 200 m.identification of Hydroides operculatus and his valuable comments on some species, and to two anonymous referees for their constructive comments on the manuscript.This work has been financially supported by TUBITAK (Project Number: 104Y065).

Figure 1 .
Figure 1.Map of the studied area with sampling stations

Figure 6 .
Figure 6.Hydroides operculatus (ESFM-POL/05-149). A. Entire body.B. Operculum.C. Operculum (ESFM-POL/05-154).D. Apical view of operculum showing basal internal spinules.E. Collar chaetae.F. Operculum with two dorsal spines.Scale line A 0.70 mm, B 0.25 mm, C 0.35 mm, D 0.20 mm, E 50 µm, F 0.20 mm.Photographed by Melih Ertan Çinar considered it as an Erythrean alien.However, the mode of introduction of this species can be via shipping.The findings of this study support this hypothesis.Only two specimens were found in Iskenderun Bay (absent among material collected in Iskenderun Harbour) and it extensively invaded artifical substrates in Karaduvar Harbour (54800 individuals.m - ) and a stone on Kazanli beach (384000 individuals.m - ), which are very close to one of the biggest harbours in Turkey, Mersin Harbour.Such high densities of this species have not been reported from other parts of the Levantine Sea; Ben-Eliahu and ten Hove (1992) reported only 33 specimens of this species on various substrata along the Israeli coast.Hydroides operculatus might have first arrived to the area near Mersin Harbour via shipping and then expanded its distributional range in the Levantine Sea.Placostegus tridentatus (Fabricius, 1779) (Figure 7B, C) Placostegus tridentatus; Imajima 1978: 67-69, figure 9; Bianchi 1981: 116-118, figure 44.Material examined: ESFM-POL/05-89, 23.9.2005,Anamur, D32, 200 m, on a stone, 1 specimen.

Figure 8 .
Figure 8. Pomatoleios kraussii (ESFM-POL/05-137). A. Entire body, ventral view, B. Entire body, dorsal view, C. Operculum, D. Tubes.Scale line A and B 1.9 mm, C 0.80 mm, D 1.8 mm.Photographed by Melih Ertan Çinar gregarious; outer surface of tube white, inner surface blue or violet; with a flattened dorsal ridge projecting forward over opening of tube (Figure 8D).Colouration (preserved specimens): Body dark blue, dorsal surface of thorax sometimes dark violet, base of radioles with a large blue band, distal part of radioles with 4-5 small blue bands; peduncle blue or dark violet (Figure 8A, B).Distribution: This species was previously reported from the tropical Indo-Pacific region(Imajima 1979) and Mediterranean Sea, and is considered to be an Erythrean alien (Ben-Eliahu 1991, Ben-Eliahu and ten Hove 1992).

Figure 10 .
Figure 10.Length and weight frequencies and relationships between biometrical features of specimens of Hydroides operculatus collected at station K14

Figure 11 .
Figure 11.Length and weight frequencies, and relationships between biometrical features of specimens of Pomatoleios kraussii collected at station K15

Figure 12 .
Figure 12.General views of dense populations of Pomatoleios kraussii at station K7a (0.1 m depth, on a rock), Iskenderun Harbour (A) and at station K15 (0.1-0.05 m depth, on a rock), Davultepe (B and C), and those of H. operculatus at station K13 (0.1 m, on a tire), Karaduvar Harbour (D) and at station K14 (2 m depth, on a stone taken on shore) Kazanli beach (E and F).Photographed by Melih Ertan Çinar

Figure 13 .
Figure 13.Relative dominances of alien and native species in habitats