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On some Indo-Pacific boring endolithic Bivalvia species introduced intothe Mediterranean Sea with their host – spread of Sphenia rueppelli A. Adams, 1850

A. ZENETOS1, P. OVALIS2 and D. EVIKER 3

1 Hellenic Centre for Marine Research, Institute of Marine Biological Resources,P.O. Box 712, 19013 Anavissos, Hellas

2 Agisilaou 37-39, Kallithea, 17674 Athens, Hellas3 Balmumcu Itri sok. No 4, 34349, Besiktas, Istanbul, Turkey

Corresponding author: zenetos@ath.hcmr.gr

Received: 14 May 2010; Accepted: 21 May 2010; Published on line: 9 June 2010

Abstract

The study of the endolithic molluscs found on/in living alien Spondylus shells collected in theGulf of Iskenderun (Turkey) brought to light three more alien Bivalvia species, namely Petricolahemprichi, Gastrochaena cymbium and Sphenia rueppelli. The presence of Sphenia rueppelli deservesattention as it constitutes the first record of this species as living in the Mediterranean Sea. Thedefinitive establishment and spread of these bivalves in the basin seems to be also attested by care-ful analysis of specimens sampled in other southern Turkish localities and previously retained in localprivate collections. The present records raise some questions on the vector of arrival of the speciesin the Mediterranean Sea, which could be strictly connected with their hosts.

Keywords: Alien Bivalvia; S. Turkey; Sphenia rueppelli.

Short CommunicationMediterranean Marine ScienceIndexed in WoS (Web of Science, ISI Thomson)The journal is available on line at http://www.medit-mar-sc.net

Introduction

The Gulf of Iskenderun appears to bea hotspot area for alien marine species.ALBAYRAK (2010) has reported that 9 ofthe 63 Bivalvia species (14,3%) in soft sub-strata of the Gulf are alien. The majority areof Indo-Pacific origin and have arrived ei-ther as Lessepsian immigrants (progressivepenetration via the Suez Canal) or trans-ferred by ships. This is mainly due to the high

levels of shipping transport in the area. Isk-enderun is in fact not only one of Turkey'slargest ports on the Mediterranean Sea butserves also as an important naval trainingbase. Other ports located in the IskenderunGulf include Dörtyol, at the head of the Gulf,a port and oil terminus and Yumurtalik, ata distance of about 40 km from the centreof Adana, whose harbour is heavily visitedby recreational boats during the summer.

One of the most invasive species in

the Gulf of Iskenderun is Spondylus spinosusSchreibers, 1793 whose most probable vec-tor of introduction is assumed to be ship-ping via the Suez Canal. Spondylus spinosuswas first sighted in the Mediterranean Seain 1988, off Haifa, attached to rocky sea bedsat depths of 2-25m together with Chamapacifica Broderip, 1834 and other Spondyl-idae (MIENIS et al., 1993), and then rapid-ly spread to Lebanon, Syria, Turkey andCyprus (ENGL & EVIKER, 1999;ZIBROWIUS & BITAR, 2003; KATSA-NEVAKIS et al., 2009) soon becoming oneof the top invasive species in the Mediter-ranean (STREFTARIS & ZENETOS, 2006).Dense populations of up to 15 specimensper m2 (MIENIS et al., 1993) and stable-re-producing populations (MIENIS et al., 1993;ENGL & EVIKER, 1999) suggest a de-finitive establishment of the species in theMediterranean Sea. A congeneric species,Spondylus multisetosus Reeve, 1856 has beenreported as common in the Iskenderun areasince 1992. Even if it was sometimes sus-pected to be a variant of the establishedspecies Spondylus spinosus EVIKER, 2001),the two ‘morphotypes’ are here treated asdifferent species.

Methodology

During a diving expedition in August2009 in Dörtyol, Hatay (36Æ50’43”N

36Æ13’22”E) the shallow water rocky sub-strata were found to be dominated by Spondy-lus spp (S. spinosus, S. multisetosus) andChama pacifica. A number of Spondylusspinosus and S. multisetosus specimens weredetached and brought to the laboratory forfurther examination. In most of them, thethick upper shell (left valve) showed holesand signs of infestation by boring organ-isms. Endolithic bivalves were extractedfrom the shells of Spondylids and then iden-tified to species level, revealing to be threefurther alien species: Petricola hemprichi,Gastrochaena cymbium and Sphenia ruep-pelli. In addition, local amateur collectorswere asked for further material, resultingin the discovery of further additional spec-imens from Iztuzu, Dalyan, Mugla(36Æ50’03”N 28Æ38’33”E) SW Turkey and Yu-murtalik, Adana (36Æ 46' 0 N 35Æ 46' 60” E).Voucher specimens have been deposited inthe Hellenic Centre for Marine Research,mollusc collection.

Results

Petricola hemprichi (Issel, 1869)

Petricola hemprichi (Fig. 1) is a speciesof Indo-Pacific origin that was reported fromthe Suez Canal and Port Said in the early1900s (TILLIER & BAVAY 1905). Thespecies was also stated to be common in

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Fig. 1: P. hemprichi (left); P. lithophaga (middle); P. lajonkairii (right).

Alexandria (FARAG et al. 1999), where itis eaten. As this statement was not confirmed,ZENETOS et al. (2004) did not include itin the Atlas. However, empty shells werefound in 2002 at Great Bitter Lake at 1 mdepth [HOFFMAN et al., 2006 as Choristodonhemprichii (Issel, 1869)] and further speci-mens were reported in the holes of shells ofSpondylus spinosus from a 7 m depth at Karatas,SE Turkey in August 1999 ( EVIKER &ALBAYRAK, 2006). The distinctive char-acteristics between Petricola hemprichi andtwo similar species of Petricola present in theRed Sea and Suez Canal are provided in

EVIKER & ALBAYRAK (2006). Petri-cola hemprichi has a distinct shape in com-parison to the Mediterranean native Petri-cola lithophaga (Philippson, 1788) and Pet-ricola lajonkairii (Payraudeau, 1826) (Fig.1). For full description see EVIKER &ALBAYRAK (2006).

Material examined:Two individuals and one loose valve were

collected in December 2006 in Iztuzu, Dalyan,Mugla, SW Turkey (colln D. eviker).

Four living specimens were present inholes in valves of Spondylus spp. (Fig. 2) col-lected in August 2009, at Dörtyol, Hatay(colln P. Ovalis). Findings of the presentwork confirm the establishment of Petrico-la hemprichi in the Iskenderun Gulf and SWTurkey.

Sphenia rueppelli A. Adams, 1850

Sphenia rueppelli (Fig. 3) originates inthe Indian Ocean. Despite its presence inthe Suez Canal (MOAZZO, 1939), the specieswas never previously collected alive fromthe Mediterranean Sea, where it was knownonly from a single valve collected in 1978 inNetanya (Israel) (BARASH & DANIN,

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Fig. 3: Sphenia rueppelli collected in Dörtyol (Photo: P. Ovalis).

Fig. 2·, b: Petricola hemprichi in Spondylus multisetosus shell (Photo: P. Ovalis).

1986). This led ZENETOS et al. (2004) toconsider the species as unlikely to be estab-lished in the Mediterranean. The distin-guishing characteristics with the Mediter-ranean native Sphenia binghami Turton, 1822are given in ZENETOS et al. (2004).

Material examined:Nine living specimens of S. rueppelli were

collected in October 1998 in Yumurtalik,Adana (colln D. eviker).

Five living specimens were found in Au-gust 2009 in Dörtyol Hatay (colln P. Ovalis)

Gastrochaena cymbium Spengler, 1783

Gastrochaena cymbium (Fig. 4) is of In-do-Pacific origin. By 1933 it had been record-ed in the Suez Canal (MOAZZO, 1939) andit is currently very common in the far east-ern Mediterranean (BARASH & DANIN,1973; MIENIS, 2002) attached to shells ofCardita and Glycymeris in Haifa Bay(BARASH & DANIN, 1977). Other recordsinclude S.Turkey: 1990 (NIEDERHÖFERet al., 1991); Lebanon (LAKKIS & NOVEL-LAKKIS 2005); and the Saronikos Gulf(TENEKIDES, 1989).

The flask shell (Gastrochaena) has beenencountered on 52 species of bivalves, 2species of scaphopods, 12 species of gas-tropods and on corals, a sharktooth, bones

and stones along the Mediterranean coastof Israel (MIENIS, 2002). Shell differencesamong the native Gastrochaena dubia (Pen-nant, 1777) and the alien Gastrochaena cym-bium were illustrated in DELONGUEVILLE& SCAILLET (2005) on the basis of spec-imens recorded on living Hexaplex pecchi-olanus (d'Ancona, 1871).

Material examined:More than 30 specimens were collect-

ed in October 1993 nested in several emptyshells and living mollusc specimens fromYumurtalik (colln D. eviker).

Seven living specimens were collectedin August 2009 in valves of Spondylus spin-osus and S. multisetosus from Dörtyol (collnP. Ovalis).

Discussion

A variety of marine bivalve molluscs areendolithic, living inside rock, coral, animalshells, or in the pores between mineral grainsof a rock. The endolithic life habit has evolvedseveral times in the Bivalvia, e.g., in the fam-ilies Modiolopsidae, Arcidae, Mytilidae (sub-family Lithophaginae), Tridacnidae, Petri-colidae, Gastrochaenidae, Myidae, Phola-didae and Teredinidae (CARTER &STANLEY, 2004). A substantial lateral asym-metry of the shell is observed in boring en-

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Fig. 4: Gastrochaena cymbium Dörtyol (Photo: P. Ovalis).

dolithic bivalves like members of the Pet-ricolidae that bore in rock or mineralisedbiogenic substrata (SAVAZZI, 2005).

Petricola (Petricolidae) are nonspecial-ized borers in peat, firm mud, and soft rock(ANSELL, 1970). They resemble burrow-ing forms in the importance of the hydro-dynamic role of the body fluids (ANSELL& NAIR, 1969). Findings of the present workconfirm the establishment of Petricolahemprichi in the Iskenderun Gulf andS.Turkey. Indeed, in May 2005 one valve ofSphenia rueppelli associated with Spondyluswas found at Yumurtalik (R. Scaillet and C.Delongeville pers. Comm).

Sphenia (Myidae) are small bivalves thatlive, attached by byssus threads, on substra-ta that provide shelter and protection againstdirect wave action. Sphenia live withinmadreporic rocks, shells on beaches, understones and are subject to numerous defor-mities. Sphenia antillensis Dall & Simpson,1901 lives where there is some disturbanceof the bottom deposits and the water con-tains a small amount of suspended materi-al (NARCHI & DOMANESCHI, 1993).The present findings of Sphenia rueppelliconfirm not only its northward expansionbut most likely its establishment in S. Turkey.

Gastrochaena (Gastrochaenidae) arespecialized for boring by having a closedmantle cavity, a large pedal gape, and a trun-cate foot, allowing them to press the footand shell against the burrow wall (ANSELL& NAIR, 1969). When it bores into shellsthe species forms a sectioned calcareous caseto protect itself (OLIVER, 1992). In litera-ture they are recorded as boring in lime-stone, in encrusting coralines, and on oldoyster shells, maerl and shell gravel. ALBANO(2003) suggests that the species should benamed as Cucurbitula cymbium (Spengler,1793).

All three mollusc species reported in

this work were found in holes and crevicesof Spondylus spp. occurring in areas wherethere was some disturbance of the bottomdeposits and water transparency was low dueto high percentage of Particulate OrganicMatter. The establishment and spread ofSpondylus spinosus is well documented inthe Levantine Sea, Iskenderun Bay includ-ed (ZENETOS et al, 2004). The occurrenceof Petricola and Gastrochaena in the widerIskenderun Gulf is documented in this workalong with the spread of Sphenia rueppelli.However, to date, the vector of introductionof the three aforementioned species has beenassumed to be Lessepsian migration. Thepresent findings of the three species so close-ly related in life habit with the alien Spondy-lus spp raises new questions on the meansof arrival of these species in the Mediter-ranean basin. It is herein suggested that thethree endolithic species were most likely in-troduced attached to the shells of other in-droduced Indo-Pacific mollusca such as thebivalve Chama pacifica. Their spread andestablishment was further facilitated in the1990s following the invasion of Spondylusspp., the shells of which form excellent sub-strates not only for some Lessepsian immi-grants but also for quite a number of localMediterranean species. Nineteen species ofmolluscs of Mediterranean origin and six-teen Lessepsian invasive molluscs (Gas-trochaena cymbium included) are reportedon about 20 Spondylus shells coming fromthe Gulf of Iskenderun (DELONGUEVILLE& SCAILLET, 2006a). Another alien bi-valve in the Mediterranean whose presenceis directly related to that of Spondylus spin-osus is Afrocardium richardi (Audouin, 1826)(DELONGUEVILLE & SCAILLET, 2006b).

Other documented cases of Indo-Pa-cific species introduced with hosts includethe parasitic barnacle Heterosaccus dollfusiBoschma, 1960, introduced with its host, the

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swimming crab, Charybdis longicollis Leene,1938 (INNOCENTI & GALIL, 2007) andthree parasitic copepods on immigrant andnative clupeid fish caught in Egyptian coastalwaters off Alexandria (EL-RASHIDY &BOXSHALL, 2010)

Acknowledgements

The authors wish to thank Fabio Cro-cetta (Italy), Henk Mienis (Israel), Chris-tiane Delongueville (Belgium) and SerhatAlbayrak (Turkey) for constructive criticismof the draft ms.

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