Mediterranean Marine Science

Vol. 11, 2010

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

ZENETOS A. Hellenic Centre for Marine Research, Institute of Marine Biological Resources, Agios Kosmas, P.C. 16610, Elliniko, Athens OVALIS P. Agisilaou 37-39, Tzitzifies/Kallithea, 17674 Athens EVIKER D. Balmumcu Itri sok. No 4, 34349, Besiktas, Istanbul https://doi.org/10.12681/mms.104

Copyright © 2010

To cite this article:

ZENETOS, A., OVALIS, P., & EVIKER, D. (2010). On some Indo-Pacific boring endolithic Bivalvia species introduced into the Mediterranean Sea with their host – spread of Sphenia rueppelli A. Adams, 1850. Mediterranean Marine Science, 11(1), 201. doi:https://doi.org/10.12681/mms.104

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On some Indo-Pacific boring endolithic Bivalvia species introduced into the 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, Hellas 3 Balmumcu Itri sok. No 4, 34349, Besiktas, Istanbul, Turkey

Corresponding author: [email protected]

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 the Gulf of Iskenderun (Turkey) brought to light three more alien Bivalvia species, namely Petricola hemprichi, cymbium and Sphenia rueppelli. The presence of Sphenia rueppelli deserves attention as it constitutes the first record of this species as living in the Mediterranean Sea. The definitive 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 local private collections. The present records raise some questions on the vector of arrival of the species in the Mediterranean Sea, which could be strictly connected with their hosts.

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

Introduction levels of shipping transport in the area. Isk- enderun is in fact not only one of Turkey's The Gulf of Iskenderun appears to be largest ports on the Mediterranean Sea but a hotspot area for alien marine species. serves also as an important naval training ALBAYRAK (2010) has reported that 9 of base. Other ports located in the Iskenderun the 63 Bivalvia species (14,3%) in soft sub- Gulf include Dörtyol, at the head of the Gulf, strata of the Gulf are alien. The majority are a port and oil terminus and Yumurtalik, at of Indo-Pacific origin and have arrived ei- a distance of about 40 km from the centre ther as Lessepsian immigrants (progressive of Adana, whose harbour is heavily visited penetration via the Suez Canal) or trans- by recreational boats during the summer. ferred by ships. This is mainly due to the high One of the most invasive species in

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http://epublishing.ekt.gr | e-Publisher: EKT | Downloaded at 28/06/2020 22:55:56 | the Gulf of Iskenderun is Spondylus spinosus 36Æ13’22”E) the shallow water rocky sub- Schreibers, 1793 whose most probable vec- strata were found to be dominated by Spondy- tor of introduction is assumed to be ship- lus spp (S. spinosus, S. multisetosus) and ping via the Suez Canal. Spondylus spinosus Chama pacifica. A number of Spondylus was first sighted in the Mediterranean Sea spinosus and S. multisetosus specimens were in 1988, off Haifa, attached to rocky sea beds detached and brought to the laboratory for at depths of 2-25m together with Chama further examination. In most of them, the pacifica Broderip, 1834 and other Spondyl- thick upper shell (left valve) showed holes idae (MIENIS et al., 1993), and then rapid- and signs of infestation by boring organ- ly spread to Lebanon, Syria, Turkey and isms. Endolithic bivalves were extracted Cyprus (ENGL & EVIKER, 1999; from the shells of Spondylids and then iden- ZIBROWIUS & BITAR, 2003; KATSA- tified to species level, revealing to be three NEVAKIS et al., 2009) soon becoming one further alien species: Petricola hemprichi, of the top invasive species in the Mediter- Gastrochaena cymbium and Sphenia ruep- ranean (STREFTARIS & ZENETOS, 2006). pelli. In addition, local amateur collectors Dense populations of up to 15 specimens were asked for further material, resulting per m2 (MIENIS et al., 1993) and stable-re- in the discovery of further additional spec- producing populations (MIENIS et al., 1993; imens from Iztuzu, Dalyan, Mugla ENGL & EVIKER, 1999) suggest a de- (36Æ50’03”N 28Æ38’33”E) SW Turkey and Yu- finitive establishment of the species in the murtalik, Adana (36Æ 46' 0 N 35Æ 46' 60” E). Mediterranean Sea. A congeneric species, Voucher specimens have been deposited in Spondylus multisetosus Reeve, 1856 has been the Hellenic Centre for Marine Research, reported as common in the Iskenderun area mollusc collection. since 1992. Even if it was sometimes sus- pected to be a variant of the established Results species Spondylus spinosus EVIKER, 2001), the two ‘morphotypes’ are here treated as Petricola hemprichi (Issel, 1869) different species. Petricola hemprichi (Fig. 1) is a species Methodology of Indo-Pacific origin that was reported from the Suez Canal and Port Said in the early During a diving expedition in August 1900s (TILLIER & BAVAY 1905). The 2009 in Dörtyol, Hatay (36Æ50’43”N species was also stated to be common in

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

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http://epublishing.ekt.gr | e-Publisher: EKT | Downloaded at 28/06/2020 22:55:56 | Alexandria (FARAG et al. 1999), where it Material examined: is eaten. As this statement was not confirmed, Two individuals and one loose valve were ZENETOS et al. (2004) did not include it collected in December 2006 in Iztuzu, Dalyan, in the Atlas. However, empty shells were Mugla, SW Turkey (colln D. eviker). found in 2002 at Great Bitter Lake at 1 m Four living specimens were present in depth [HOFFMAN et al., 2006 as Choristodon holes in valves of Spondylus spp. (Fig. 2) col- hemprichii (Issel, 1869)] and further speci- lected in August 2009, at Dörtyol, Hatay mens were reported in the holes of shells of (colln P. Ovalis). Findings of the present Spondylus spinosus from a 7 m depth at Karatas, work confirm the establishment of Petrico- SE Turkey in August 1999 ( EVIKER & la hemprichi in the Iskenderun Gulf and SW ALBAYRAK, 2006). The distinctive char- Turkey. acteristics between Petricola hemprichi and two similar species of Petricola present in the Sphenia rueppelli A. Adams, 1850 Red Sea and Suez Canal are provided in EVIKER & ALBAYRAK (2006). Petri- Sphenia rueppelli (Fig. 3) originates in cola hemprichi has a distinct shape in com- the Indian Ocean. Despite its presence in parison to the Mediterranean native Petri- the Suez Canal (MOAZZO, 1939), the species cola lithophaga (Philippson, 1788) and Pet- was never previously collected alive from ricola lajonkairii (Payraudeau, 1826) (Fig. the Mediterranean Sea, where it was known 1). For full description see EVIKER & only from a single valve collected in 1978 in ALBAYRAK (2006). Netanya (Israel) (BARASH & DANIN,

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

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

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http://epublishing.ekt.gr | e-Publisher: EKT | Downloaded at 28/06/2020 22:55:56 | 1986). This led ZENETOS et al. (2004) to and stones along the Mediterranean coast consider the species as unlikely to be estab- of Israel (MIENIS, 2002). Shell differences lished in the Mediterranean. The distin- among the native Gastrochaena dubia (Pen- guishing characteristics with the Mediter- nant, 1777) and the alien Gastrochaena cym- ranean native Sphenia binghami Turton, 1822 bium were illustrated in DELONGUEVILLE are given in ZENETOS et al. (2004). & SCAILLET (2005) on the basis of spec- imens recorded on living Hexaplex pecchi- Material examined: olanus (d'Ancona, 1871). Nine living specimens of S. rueppelli were collected in October 1998 in Yumurtalik, Material examined: Adana (colln D. eviker). More than 30 specimens were collect- Five living specimens were found in Au- ed in October 1993 nested in several empty gust 2009 in Dörtyol Hatay (colln P. Ovalis) shells and living mollusc specimens from Yumurtalik (colln D. eviker). Gastrochaena cymbium Spengler, 1783 Seven living specimens were collected in August 2009 in valves of Spondylus spin- Gastrochaena cymbium (Fig. 4) is of In- osus and S. multisetosus from Dörtyol (colln do-Pacific origin. By 1933 it had been record- P. Ovalis). ed in the Suez Canal (MOAZZO, 1939) and it is currently very common in the far east- Discussion ern Mediterranean (BARASH & DANIN, 1973; MIENIS, 2002) attached to shells of A variety of marine bivalve molluscs are Cardita and Glycymeris in Haifa Bay endolithic, living inside rock, coral, (BARASH & DANIN, 1977). Other records shells, or in the pores between mineral grains include S.Turkey: 1990 (NIEDERHÖFER of a rock. The endolithic life habit has evolved et al., 1991); Lebanon (LAKKIS & NOVEL- several times in the Bivalvia, e.g., in the fam- LAKKIS 2005); and the Saronikos Gulf ilies Modiolopsidae, Arcidae, Mytilidae (sub- (TENEKIDES, 1989). family Lithophaginae), Tridacnidae, Petri- The flask shell (Gastrochaena) has been colidae, , Myidae, Phola- encountered on 52 species of bivalves, 2 didae and Teredinidae (CARTER & species of scaphopods, 12 species of gas- STANLEY, 2004). A substantial lateral asym- tropods and on corals, a sharktooth, bones metry of the shell is observed in boring en-

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

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http://epublishing.ekt.gr | e-Publisher: EKT | Downloaded at 28/06/2020 22:55:56 | dolithic bivalves like members of the Pet- this work were found in holes and crevices ricolidae that bore in rock or mineralised of Spondylus spp. occurring in areas where biogenic substrata (SAVAZZI, 2005). there was some disturbance of the bottom Petricola (Petricolidae) are nonspecial- deposits and water transparency was low due ized borers in peat, firm mud, and soft rock to high percentage of Particulate Organic (ANSELL, 1970). They resemble burrow- Matter. The establishment and spread of ing forms in the importance of the hydro- Spondylus spinosus is well documented in dynamic role of the body fluids (ANSELL the Levantine Sea, Iskenderun Bay includ- & NAIR, 1969). Findings of the present work ed (ZENETOS et al, 2004). The occurrence confirm the establishment of Petricola of Petricola and Gastrochaena in the wider hemprichi in the Iskenderun Gulf and Iskenderun Gulf is documented in this work S.Turkey. Indeed, in May 2005 one valve of along with the spread of Sphenia rueppelli. Sphenia rueppelli associated with Spondylus However, to date, the vector of introduction was found at Yumurtalik (R. Scaillet and C. of the three aforementioned species has been Delongeville pers. Comm). assumed to be Lessepsian migration. The Sphenia (Myidae) are small bivalves that present findings of the three species so close- live, attached by byssus threads, on substra- ly related in life habit with the alien Spondy- ta that provide shelter and protection against lus spp raises new questions on the means direct wave action. Sphenia live within of arrival of these species in the Mediter- madreporic rocks, shells on beaches, under ranean basin. It is herein suggested that the stones and are subject to numerous defor- three endolithic species were most likely in- mities. Sphenia antillensis Dall & Simpson, troduced attached to the shells of other in- 1901 lives where there is some disturbance droduced Indo-Pacific such as the of the bottom deposits and the water con- bivalve Chama pacifica. Their spread and tains a small amount of suspended materi- establishment was further facilitated in the al (NARCHI & DOMANESCHI, 1993). 1990s following the invasion of Spondylus The present findings of Sphenia rueppelli spp., the shells of which form excellent sub- confirm not only its northward expansion strates not only for some Lessepsian immi- but most likely its establishment in S. Turkey. grants but also for quite a number of local Gastrochaena (Gastrochaenidae) are Mediterranean species. Nineteen species of specialized for boring by having a closed molluscs of Mediterranean origin and six- mantle cavity, a large pedal gape, and a trun- teen Lessepsian invasive molluscs (Gas- cate foot, allowing them to press the foot trochaena cymbium included) are reported and shell against the burrow wall (ANSELL on about 20 Spondylus shells coming from & NAIR, 1969). When it bores into shells the Gulf of Iskenderun (DELONGUEVILLE the species forms a sectioned calcareous case & SCAILLET, 2006a). Another alien bi- to protect itself (OLIVER, 1992). In litera- valve in the Mediterranean whose presence ture they are recorded as boring in lime- is directly related to that of Spondylus spin- stone, in encrusting coralines, and on old osus is Afrocardium richardi (Audouin, 1826) oyster shells, maerl and shell gravel. ALBANO (DELONGUEVILLE & SCAILLET, 2006b). (2003) suggests that the species should be Other documented cases of Indo-Pa- named as Cucurbitula cymbium (Spengler, cific species introduced with hosts include 1793). the parasitic barnacle Heterosaccus dollfusi All three mollusc species reported in Boschma, 1960, introduced with its host, the

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http://epublishing.ekt.gr | e-Publisher: EKT | Downloaded at 28/06/2020 22:55:56 | swimming crab, Charybdis longicollis Leene, additions to the knowledge of Indo-Pa- 1938 (INNOCENTI & GALIL, 2007) and cific mollusca in the Mediterranean Sea. three parasitic copepods on immigrant and Spixiana, 9 (2): 117-141. native clupeid fish caught in Egyptian coastal CARTER, J.G. & STANLEY, J.R. G.D., waters off Alexandria (EL-RASHIDY & 2004. Late Triassic Gastrochaenid and BOXSHALL, 2010) Lithophaginid borings (Mollusca: Bi- valvia) from Nevada (USA) and Austria. Acknowledgements Journal of Paleontology, 78 (1): 230-234. EVIKER, D., 2001. Recent immigrant The authors wish to thank Fabio Cro- bivalves in the Northeastern Mediter- cetta (Italy), Henk Mienis (Israel), Chris- ranean off Iskenderun. La Conchiglia, tiane Delongueville (Belgium) and Serhat 298: 39-46. Albayrak (Turkey) for constructive criticism EVIKER, D. & ALBAYRAK, S., 2006. of the draft ms. Three alien molluscs from Iskenderun Bay (SE Turkey). Aquatic Invasions, 1 References (2): 76-79. DELONGUEVILLE, C. & SCAILLET, R., ALBANO, P.J., 2003. Mediterranean Gas- 2005. Illustration de Gastrochaena cym- trochaenidae (Mollusca: Bivalvia). Bol- bium Spengler, 1783 en Méditerranée lettino Malacologico, Roma, 38 (9-12): orientale sur Hexaplex pecchiolianus 135-138. (d’Ancona, 1871). Novapex / Société, 6 ALBAYRAK, S., 2010. Distribution of alien (4), 10 décembre 2005: 129-131. bivalve species in the soft bottom of Isk- DELONGUEVILLE, C. & SCAILLET, R., enderun Bay (Turkey, NE Levantine Sea). 2006a. Mollusques associés à Spondylus Cahiers de Biologie Marine, 51: 45-53. spinosus Schreibers, 1793 dans le golfe ANSELL, A.D., 1970. Boring and burrow- d’Iskenderun (Turquie). Novapex So- ing mechanisms in Petricola pholadi- ciété 7 (2-3), 10 juin 2006 : 29-33. formis Lamarck. Journal of Experimen- DELONGUEVILLE, C. & SCAILLET, R., tal Marine Biology and Ecology, 4 (3): 2006b. Afrocardium richardi (Audouin, 211-220. 1826) alive on Spondylus spinosus ANSELL, A.D. & NAIR, N.B, 1969. A com- Schreibers, 1793 in the Gulf of Iskenderun parative study of bivalves which bore (Eastern Mediterranean Sea). Neptunea, mainly by mechanical means. American 5 (1): 12-14. Zoologist, 9 (3): 857-868. EL-RASHIDY, H. & BOXSHALL, G.A., BARASH, A. & DANIN, Z., 1973. The In- 2010. Parasitic copepods on immigrant do-Pacific species of mollusca in the and native clupeid fishes caught in Egypt- Mediterranean and notes on a collec- ian coastal waters off Alexandria. Sys- tion from the Suez Canal. Israel Journal tematic Parasitology , 76 (1): 19-38. of Zoology, 21 (3-4): 301-374. ENGL, W. & EVIKER, D., 1999. New BARASH, A. & DANIN, Z., 1977. Addi- migrant species from southeast Turkey tions to the knowledge of Indo-Pacific Psammotreta praerupta (Salisbury, 1934) Mollusca in the Mediterranean. and Antigona lamellaris Schumacher, Conchiglie, 13 (5-6): 85-116. 1817. La Conchiglia, 290: 17-20. BARASH, A. & DANIN, Z., 1986. Further FARAG, E.A., DEKINESH, S.I. & EL-

206 Medit. Mar. Sci., 11/1 2010, 201-207

http://epublishing.ekt.gr | e-Publisher: EKT | Downloaded at 28/06/2020 22:55:56 | ODESSY, H.M., 1999. Taxonomical Zoology in the Middle East, 9: 83-91. studies o the edible bivalve molluscs in- MOAZZO, P.G., 1939. Mollusques testacés habiting the coastal zones of Alexan- marins du Canal de Suez. Mémoirs de dria, Egypt. Pakistan Journal of Biolog- l’Institut d’Egypte, 38: 1-283. ical Sciences, 2 (4): 1341-1349. NARCHI, W. & DOMANESCHI, O., 1993. FOULQUIÉ, M. & DUPUY DE LA The Functional anatomy of Sphenia an- GRANDRIVE, R., 2003. First assign- tillensis Dall & Simpson, 1901 (Bivalvia: ment concerning the development of Myidae). Journal of Molluscan Studies, Marine Protected Areas on the Syrian 59: 195-210. coast, from 8-15 November 2002. NIEDERHÖFER, H., ENZENROSS, L. RAC/SPA. & ENZENROSS, R., 1991. Neue Erken- HOFFMAN, L., VAN HEUGTEN, B. & ntnisse über die Ausbreitung von "Lessep- DEKKER, H., 2006. Marine mollusca s’schen Einwanderern" (Mollusca) an collected during a journey to the Great der türkischen Mittelmeerküste. Club Bitter Lake (Suez Canal) and Nile Delta, Conchilia Information, 23 (3-4): 94- Egypt. Gloria Maris, 45 (1-2): 184-200. 108. INNOCENTI, G.∑. & GALIL, B.S., 2007. OLIVER, P.G., 1992. Bivalved seashells of Modus vivendi: invasive host/parasite the Red Sea. Wiesbaden: Verlag Christa relations-Charybdis longicollis Leene, Hemmen, 330 pp. 1938 (Brachyura: Portunidae) and SAVAZZI, E., 2005. The function and evo- Heterosaccus dollfusi Boschma, 1960 lution of lateral asymmetry in boring en- (Rhizocephala: Sacculinidae). Hydrobi- dolithic bivalves. Paleontological Re- ologia, 590 (1): 95-101. search, 9 (2): 169-187. KATSANEVAKIS, S., TSIAMIS, K., STREFTARIS, N. & ZENETOS, A., 2006. IOANNOU, G., MICHAILIDIS, N. & Alien marine species in the Mediter- ZENETOS, A., 2009. Inventory of alien ranean - the 100 ‘Worst Invasives’ and marine species of Cyprus. Mediterranean their impact. Mediterranean Marine Marine Science, 10 (2): 109-133. Science, 7 (1): 87-118. LAKKIS, S. & NOVEL-LAKKIS W., 2005. TENEKIDES, N.S., 1989. On a collection of Benthic populations diversity of soft sub- shells from the Greek Seas. Athens: Pro- stratum along the Lebanese coast ( Le- topapa Press, 187 pp. (in Greek). vantine basin, Eastern Mediterranean). TILLIER, L. & BAVAY, A., 1905. Les mol- MEDCORE International Conference, lusques testacés du Canal de Suez. Bul- Firenze 10-14 Nov. 2005. letin de la Société Zoologique de France, MIENIS, H.K., 2002. Marine molluscs from 30: 170-181. the Eastern Mediterranean: 10. Objects ZENETOS, A., GOFAS, S., RUSSO, G. & used by Cucurbitula cymbium as a sub- TEMPLADO, J., 2004. CIESM atlas of strate. Spirula, 327: 75-76. exotic species in the Mediterranean. Vol. MIENIS, H.K., GALILI, E. & RAPOPORT, 3. Molluscs. Monaco: CIESM Publish- J., 1993. The spiny oyster, Spondylus spin- ers, 376 pp. osus, a well established Indo-Pacific bi- ZIBROWIUS, H. & BITAR, G., 2003. In- valve in the eastern Mediterranean off vertébrés marins exotiques sur la côte du Israel (Mollusca, Bivalvia, Spondylidae). Liban. Lebanese Science Journal, 4: 67-74.

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