2urn:lsid:arphahub.com:pub:45048D35-BB1D-5CE8-9668-537E44BD4C7Eurn:lsid:zoobank.org:pub:91BD42D4-90F1-4B45-9350-EEF175B1727AZooKeysZK1313-29891313-2970Pensoft Publishers10.3897/zookeys.563.68366836Research ArticleAscidiaceaBiological InvasionsEuropeTurkeyThe alien ascidian Styelaclava now invading the Sea of Marmara (Tunicata: Ascidiacea)ÇinarMelih Ertan1melih.cinar@ege.edu.trhttps://orcid.org/0000-0002-1802-2801Ege University, Faculty of Fisheries, Department of Hydrobiology, 35100, Bornova, İzmir, TurkeyEge UniversityİzmirTurkey
201615022016563110B346FFC3-D804-D95E-FF95-FFF6FF9FFFC49C2A27E2-3053-486A-BEDF-F81952D3A3AC5792901310201524112015Melih Ertan ÇinarThis is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.http://zoobank.org/9C2A27E2-3053-486A-BEDF-F81952D3A3AC
During the implementation of a large project aimed to investigate the benthic community structures of the Sea of Marmara, specimens of the invasive ascidian species Styelaclava were collected on natural substrata (rocks) at 10 m depth at one locality (Karamürsel) in İzmit Bay. The specimens were mature, containing gametes, indicating that the species had become established in the area. The Sea of Marmara seems to provide suitable conditions for this species to survive and form proliferating populations.
Invasive alien speciesStyelaclavaAscidiaceaTunicataSea of MarmaraCitation
Çinar ME (2016) The alien ascidian Styela clava now invading the Sea of Marmara (Tunicata: Ascidiacea). ZooKeys 563: 1–10. doi: 10.3897/zookeys.563.6836
Introduction
The Sea of Marmara is unique in having two stratified water layers separated by a halocline, generally developing at 20-25 m depths (Besiktepe et al. 1994). The upper layer is composed of brackish water originating from the Black Sea, while, the lower layer comprises marine water from the Aegean Sea. This sea has been under great anthropogenic pressures, mainly due to crowded cities situated along its coastlines (including İstanbul), and the presence of many industrialized regions, in particular, İzmit Bay. Pollution from different sources has caused hyper eutrophication (Aral 1992) and occasionally anoxia (Basturk et al. 1990) in some areas. Moreover, the establishment of some invasive alien species [e.g. the ctenophore Mnemiopsisleidyi Agassiz, 1865, the asteroid Asteriasrubens Linnaeus, 1758 and the gastropod Rapanavenosa (Valenciennes, 1846)] in the basin has made conditions worse (Çinar et al. 2011). The mussel and oyster beds in the sea have been largely destroyed by the aforementioned asteroid and gastropod.
The invasive alien species are known to have great impacts on native communities and often make complete changes to ecosystems that cannot be rectified (Ruiz et al. 1997). The eastern Mediterranean Sea is one of the known regions that hosts high numbers of alien species, due to its proximity to the Suez Canal and high rate of maritime traffic (Çinar et al. 2012). This region includes 75% of the total number of alien species reported for the whole of the Mediterranean Sea (Zenetos et al. 2012). Seventeen alien ascidian species were reported from the Mediterranean Sea (see Zenetos et al. 2012), some of which, such as Distapliabermudensis Van Name, 1902, Microcosmussquamiger Michaelsen, 1927 Botrylloidesviolaceus Oka, 1927 and Didemnumvexillum Kott, 2002, have become invasive in some areas, especially in the western Mediterranean and Adriatic Sea (Mastrototaro and Brunetti 2006; Occhipinti-Ambrogi 2000; Turon et al. 2007; Tagliapietra et al. 2012). The lessepsian invaders such as Symplegmabrakenhielmi (Michaelsen, 1904), Herdmaniamomus (Savigny, 1816), Microcosmusexasperatus Heller, 1878 and Phallusianigra Savigny, 1816 densely colonize both natural habitats and man-made structures in coastal regions of the eastern Mediterranean (in Levantine Sea), gradually extending their distributions to the north and west, including the Aegean Sea (Çinar et al. 2006; Kondilatos et al. 2010; Thessalou-Legaki 2012; Evans et al. 2013; Ramos-Esplá et al. 2013). Shenkar and Loya (2009) reported 7 alien species along the Mediterranean coast of Israel, including Microcosmusexasperatus Heller, 1878. A total of 4 alien ascidian species [P.nigra, H.momus, M.exasperatus and S.brakenhielmi] have been reported along the Levantine and Aegean coasts of Turkey up to date, but no alien ascidian species have been encountered in the Sea of Marmara and the Black Sea coasts of Turkey (Çinar 2014).
During a TUBITAK project (number 111Y268), specimens of Styelaclava Herdman, 1881 were encountered and photographed in one locality, Karamürsel, located in Izmit Bay. This sessile and solitary ascidian species is native to the north-western Pacific but now occurs worldwide, due to anthropogenic transport (Carlisle 1954; Millar 1960; Holmes 1976; Christiansen and Thomsen 1981; Berman et al. 1992; Cohen et al. 1998; Lambert and Lambert 1998; Minchin et al. 2006; Davis and Davis 2007; Ross et al. 2007; Hayward and Morley 2009). It is mainly characterized by its tunic shape and long stalk. This species was first reported in the Mediterranean Sea in June 2005, in Bassin de Thau (France) and was thought to have been transferred to the area by shellfish transfer (Davis and Davis 2008). This species was also recorded in the Black Sea in a species list of the macro-zoobenthos associated with a mussel facies inside the Constanta Sud-Agigea Seaport situated on the coast of Romania (Micu and Micu 2004). The species generally colonizes areas of shallow water and is especially abundant 10-200 cm below the sea surface, occasionally inhabiting hard substrate at depths of 15-40 m (Lützen 1999). However, Kott (2008) found it at 100 m depth in Shark Bay (Western Australia).
The aim of this paper is to report this species in the Sea of Marmara and to give additional information regarding its morphological and ecological characteristics.
Material and methods
Specimens of Styelaclava were collected at one locality (Karamürsel, K15, İzmit Bay, 40°41'38"N-29°36'26"E) in the Sea of Marmara at 10 m depth on rocks via scuba-diving on 01 October 2012 (Figure 1). The animals were randomly sampled and fixed with 4% formaldehyde in the field. In the laboratory, specimens were rinsed with tap water and preserved in 70% ethanol. Specimens were deposited at the
https://binary.pensoft.net/fig/77854Results and discussionThe description of Styelaclava
Four specimens (registration code: ESFM-TUN/2012-1) were collected in the Sea of Marmara from station K15 at 10 m depth on rocks. Specimens are stalked and sessile. The body is more or less cylindrical, tapering to stalk. The body of the largest specimen is 5.5 cm long and 2 cm wide. The smallest specimen is 3.2 cm long and 1.8 mm wide. The specimen stalk reaches 3.5 cm long (Figure 2A–C). The siphons are short and placed anteriorly; the branchial siphon is more obvious than the atrial siphon. The external body surface is leathery, wrinkled, with irregular rounded conical warts (Figure 2B, C). The body color is white in fixed specimens (Figure 2C), but is chocolate-brown when alive (Figure 2A, B). Apertures have alternate longitudinal pale brown and dark brown stripes (Figure 2A).
Styelaclava, A Live animals densely covered with sediment and epibionts at K15 B Live animal almost bare at same station C Fixed specimens D Gonads. Scale bars: C = 1 cm, D = 2 mm.
https://binary.pensoft.net/fig/77855
The branchial tentacles are simple. There are four branchial folds curved inwards on each side of the posterior part of the body. The branchial sac has numerous rows of straight stigmata. The gut is placed on the left side of the branchial sac, like a simple vertical loop. Gonads are long, parallel to each other, consisting of a central ovarian tube with testis follicles on the body wall along the each side of the ovary (Figure 2D). In the largest specimen, gonads are placed on both sides (2 on the left side and 4 on the right side), consisting of a long ovary surrounded by male follicles (Figure 2D).
The epibionts of Styelaclava
The specimens of Styelaclava from the Sea of Marmara were generally covered by sediment and some epibionts, such as Diadumenecincta Stephenson, 1925, Spirobranchustriqueter (Linnaeus, 1758) and green algae. The former species is known also to be an alien species, probably transferred to the area by shipping from the north-east Atlantic (Çinar et al. 2014). Lützen (1999) reported various epibionts on S.clava in the North Sea, from tufts of red or green algae to ascidians including smaller specimens of the same species as well as Ascidiellaaspersa (Müller, 1776) and Botryllusschlosseri (Pallas, 1766).
The density of Styelaclava
During many scuba dives and snorkeling trips performed along the Sea of Marmara in September and October 2012 (30 stations), this species was only encountered at station K15 (İzmit Bay, Karamürsel) and only 10 specimens were observed at a depth of 10 m on natural habitats (on rocks). The density of the species was approximately 1 ind.m-2. The dominant macrozoobenthic species sharing the same habitat with S.clava were Mytilusgalloprovincialis Lamarck, 1819, S.triqueter, D.cincta, R.venosa and A.rubens. The latter three species are also invasive alien species in the Sea of Marmara. Styelaclava has been known to become extremely dominant in some areas, attaining a density of 1000 ind.m-2 in European waters (Lützen 1999; Minchin et al. 2006). Micu and Micu (2004) reported a density of 4 ind.m-2 and biomass (dry-weight) of 22.8 g.m-2 in the Agigea seaport in the Black Sea (Romanian coast).
The survival requirements of Styelaclava
This species has a club-shaped body that can reach a length of 200 mm and attaches to hard substrata by an expanded membranous plate (Minchin et al. 2006). It reaches maturity at a size of 5 to 7.5 cm after ten months of settlement (Davis and Davis 2007). It is a hermaphroditic species and has a pelagic lecithotrophic larva that rarely travels more than a few centimeters according to Davis et al. (2007), but probably travels much father due to currents. It is known to tolerate temperatures ranging from -2 to +23 °C and salinity from 20 to 32 psu (Davis and Davis 2007). At this particular station within the Sea of Marmara, the temperature was near the maximum known tolerance limit of the species (22.6 °C) and the salinity was 23 psu. Similar environmental conditions were also encountered at different sampling stations in the Sea of Marmara, but no animals of this species were found at those stations. These findings might suggest that the species was found at the area of first establishment. In the Sea of Marmara, the summer surface water temperatures and salinity at the sampling site (İzmit Bay) were reported to be 25 °C and 23 psu, respectively (Isinibilir et al. 2008). Winter surface water temperature of Izmit Bay is around 7 °C. This suggests that there are no physico-chemical barriers in the region to hinder the population spread of S.clava. The Sea of Marmara’s specimens had ripe gonads, indicating its successful reproductive capacity in the area. At this stage it could be concluded that this species is established and has formed a proliferating population in the area.
The vector for introduction of Styelaclava
This species has been introduced to different parts of the world’s oceans, including the east Atlantic coast (see Minchin et al. 2006), Australia (Hewitt et al. 1999), New Zealand (Davis and Davis 2006), both coasts of North America (Osman et al. 1989; Lambert and Lambert 1998; Lambert 2003; Wonham and Carlton 2005), Mediterranean Sea (Davis and Davis 2008) and the Black Sea (Micu and Micu 2004). As Davis and Davis (2008) summarized, there are two possible mechanisms of ascidian introduction; shellfish transportation (juvenile ascidians) or via ship’s hulls and sea chests (mature ascidians) (Coutts and Dodgshun 2007). As there is no shellfish farming in the Sea of Marmara, the only possible vector for the introduction of this species to the area was via shipping. The sampling station (K15, Karamursel) is located in İzmit Bay, which is one of the most industrialized areas in Turkey, with intense international ship traffic. The donor area for the Sea of Marmara’s population of this species is unknown at present. It might have been transferred from an area in the Black Sea or/the Mediterranean, or from outside the Mediterranean. Molecular analysis to be performed on the specimens might shed more light on from where this population was originated.
Impacts of Styelaclava
The effects of Styelaclava on soft bottom sediment assemblages in Port Philip Bay were reported to be negligible (Ross et al. 2007). However, Bourque et al. (2007) reported that it caused a decline in mussel production in Canada, as it densely covered mussel lines. It was reported to be an aggressive invader, affecting native fauna by replacing the native competitive dominants in the benthic community (Clarke and Therriault 2007). The economic impact of this species on shellfish production in Canada alone was estimated at between $34–88,000 million (Canadian) per year (Colautti et al. 2006). Experiments made by Osman et al. (1989) indicated that S.clava is capable of greatly reducing the local settlement rate of oysters by preying on their planktonic larvae. The introduction and dense establishment of S.clava in England occurred simultaneously to a sharp decline in the population of the local ascidian, Cionaintestinalis (Linnaeus, 1767) (Lützen 1999). Styelaclava has effectively replaced the indigenous Pyurahaustor (Stimpson, 1864) and Ascidiaceratodes (Huntsman, 1912), which were the dominant ascidian species in southern California (Lambert and Lambert 1998). However, in the Mediterranean Sea, the population level of this species has not increased in the Bassin de Thau in the three years since its discovery in the area and has not affected the shellfish industry greatly. It is thought that summer water temperatures (max. 29.1 °C) and salinity (max. 40.4 psu) in the area might kill off large proportions of the population (Davis and Davis 2009).
Conclusions
As the Sea of Marmara’s hydrographical conditions conform with the survival requirements of Styelaclava, it has a great potential to invade the coastal habitats of the Sea of Marmara. In order to stop, or at least mitigate the effects of this invasion, an eradication program should be urgently planned and implemented while the population is still confined to a very small area.
Acknowledgments
The author is indebted to the Benthos team of the Faculty of Fisheries, Ege University for their help during the field and laboratory work, and to Dr. Kate Mortimer (National Museum Wales, UK) for correcting the English of the text. This study was financially supported by the TUBITAK Project (Number: 111Y268).
ReferencesAralN (1992) Hydrological budget and the role of Lake Nicea to the pollution of the Gemlik Bay (now called “Lake Iznik). In: VollenweiderRAMarchettiRVivianiR (Eds) Marine coastal eutrophication., 21–24 March, 1990, Elsevier, Suppl., 719–726.BasturkOYilmazASaydamC (1990) An observation on the occurrence of near-anoxia conditions in the Sea of Marmara.33: 46.BermanJHarrisLLambertWButtrickMDufresneM (1992) Recent invasions of the Gulf of Maine: three contrasting ecological histories.6: 435–441. doi: 10.1046/j.1523-1739.1992.06030435.xBesiktepeSTSurHIÖzsoyELatifMAOguzTÜnlüataA (1994) The circulation and hydrography of the Marmara Sea.34: 285–334. doi: 10.1016/0079-6611(94)90018-3BourqueDDavidsonJMacNairNGArsenaultGLeBlancARLandryTMironG (2007) Reproduction and early life history of an invasive ascidian Styelaclava Herdman in Prince Edward Island, Canada.342: 78–84. doi: 10.1016/j.jembe.2006.10.017CarlisleDB (1954) Styelamammiculata n. sp., a new species of ascidian from the Plymouth area.33: 329–334. doi: 10.1017/S0025315400008365ChristiansenJThomsenJC (1981) Styelaclava Herdman, 1882, a species new to the Danish fauna (TunicataAscidiacea).7: 15–24.ÇinarME (2014) Checklist of the phyla Platyhelminthes, Xenacoelomorpha, Nematoda, Acanthocephala, Myxozoa, Tardigrada, Cephalorhyncha, Nemertea, Echiura, Brachiopoda, Phoronida, Chaetognatha and Chordata (Tunicata, Cephalochordata and Hemichordata) from the coasts of Turkey.38: 698–722. doi: 10.3906/zoo-1405-70ÇinarMEBilecenogluMÖztürkBCanA (2006) New records of alien species on the Levantine coast of Turkey.1: 84–90. doi: 10.3391/ai.2006.1.2.6ÇinarMEYokeşMBAçikSBakirAK (2014) Checklist of Cnidaria and Ctenophora from the coasts of Turkey.38: 677–697. doi: 10.3906/zoo-1405-68ÇinarMEBilecenoğluMÖztürkBKatağanTYokeşMBAyselVDağlıEAçıkSÖzcanTErdoğanH (2011) An updated review of alien species on the coasts of Turkey.12: 257–315. doi: 10.12681/mms.34ÇinarMEKataganTÖztürkBDagliEAçikSBitlisBBakirKDoganA (2012) Spatio-temporal distributions of zoobenthos in Mersin Bay (Levantine Sea, eastern Mediterranean) and the importance of alien species in benthic communities.8: 954–968. doi: 10.1080/17451000.2012.706305ClarkeCLTherriaultTW (2007) Biological synopsis of the invasive tunicate Styelaclava (Herdman 1881).2807: 1–23.CohenAMillsCBerryHWonhamMBinghamBBookheimBCarltonJChapmanJCordellJHarrisLKlingerTKohnALambertCLambertGLiKSecordDToftJ (1998) Washington State Department of Natural Resources, Olympia, WA, 37 pp.ColauttiRIBaileySAvan OverdijkCDAAmundsenKMacIsaacHJ (2006) Characterized and projected costs of non-indigenous species in Canada.8: 45–59. doi: 10.1007/s10530-005-0236-yCouttsADMDodgshunTJ (2007) The nature and extent of organisms in vessel sea-chests: A protected mechanism for marine bioinvasions.54: 875–886. doi: 10.1016/j.marpolbul.2007.03.011DavisMHDavisME (2006) Styelaclava (Tunicata: Ascidiacea) a new edition to the fauna of New Zealand.20: 23–28.DavisMHDavisME (2007) The distribution of Styelaclava (Tunicata, Ascidiacea) in European waters.342: 182–184. doi: 10.1016/j.jembe.2006.10.039DavisMHDavisME (2008) First record of Styelaclava (Tunicata, Ascidiacea) in the Mediterranean region.3: 125–132. doi: 10.3391/ai.2008.3.2.2DavisMHDavisME (2009) Styelaclava (Tunicata, Ascidiacea)-a new threat to the Mediterranean shellfish industry?4: 283–289. doi: 10.3391/ai.2009.4.1.29DavisMHLützenJDavisME (2007) The spread of Styelaclava Herdman, 1882 (Tunicata, Ascidiacea) in European waters.2: 378–390. doi: 10.3391/ai.2007.2.4.6EvansJBorgJASchembriPJ (2013) First record of Herdmaniamomus (Ascidiacea: Pyuridae) from the central Mediterranean Sea.6(e134): 1–4. doi: 10.1017/s1755267213001127HaywardBWMorleyMS (2009) Introduction to New Zealand of two sea squirts (Tunicata, Ascidiacea) and their subsequent dispersal.46: 5–14.HewittCCampbellMLThresherREMartinRB (1999) Marine biological invasions of Port Phillip Bay, Victoria.No. 20, 344 pp.HolmesN (1976) Occurrence of the ascidian Styelaclava Herdman in Hobsons Bay, Victoria: a new record for the southern hemisphere.88: 115–116.IsinibilirMKideysAETarkanANNoyan YilmazI (2008) Annual cycle of zooplankton abundance and species composition in Izmit Bay (the northeastern Marmara Sea).78: 739–747. doi: 10.1016/j.ecss.2008.02.013KondilatosGCorsini-FokaMPancucci-PapadopoulouMA (2010) Occurrence of the first non-indigenous ascidian Phallusianigra Savigny, 1816 (Tunicata: Ascidiacea) in Greek waters.5: 181–184. doi: 10.3391/ai.2010.5.2.08KottP (2008) Ascidiacea (Tunicata) from deep waters of the continental shelf of western Australia.42: 1103–1217. doi: 10.1080/00222930801935958LambertG (2003) New records of ascidians from the NE Pacific: a new species of Trididemnum, range extension and redescription of Aplidiopsispannosum (Ritter, 1899) including its larva, and several non-indigenous species.25: 665–679.LambertCCLambertG (1998) Non-indigenous ascidians in southern California harbors and marinas.130: 675–688. doi: 10.1007/s002270050289LützenJ (1999) Styelaclava Herdman (Urochordata, Ascidiacea) a successful immigrant to North West Europe: ecology, propagation and chronology of spread.52: 383–391. doi: 10.1007/BF02908912MicuDMicuS (2004) A new type of macrozoobenthic community from the rocky bottoms of the Black Sea.International Workshop on Black Sea Benthos, 18–23 April 2004, İstanbul, Turkey, 70–83.MillarH (1960) The identity of the ascidians Styelamammiculata Carlisle and Styelaclava Herdman.39: 509–511. doi: 10.1017/S0025315400013503MinchinDDavisMHDavisME (2006) Spread of the Asian tunicate Styelaclava Herdman, 1882 to the east and south-west coasts of Ireland.1: 91–96. doi: 10.3391/ai.2006.1.2.7MastrototaroFBrunettiR (2006) The non-indigenous ascidian Distapliabermudensis in the Mediterranean: comparison with the native species Distapliamagnilarva and Distaplialucillae sp. nov.86: 181–185. doi: 10.1017/S0025315406013014Occhipinti-AmbrogiA (2000) Biotic invasions in a Mediterranean lagoon.2: 165–176. doi: 10.1023/A:1010004926405OsmanRWWhitlatchRBZajacRN (1989) Effects of resident species on recruitment into a community: larval settlement versus post-settlement mortality in the oyster Crassostreavirginica.54: 61–73. doi: 10.3354/meps054061Ramos-EspláAAIzquierdoAÇinarME (2013) Microcosmusexasperatus (Ascidiacea: Pyuridae), current distribution in the Mediterranean Sea.6(e89): 1–5. doi: 10.1017/s1755267213000663RossDJKeoughMJLongmoreARKnottNA (2007) Impacts of two introduced suspension feeders in Port Phillip Bay, Australia.340: 41–53. doi: 10.3354/meps340041RuizGMCarltonJTGrosholzEDHinesAH (1997) Global invasions of marine and estuarine habitats by nonindigenous species: mechanisms, extent, and consequences.37: 621–632. doi: 10.1093/icb/37.6.621ShenkarNLoyaY (2009) Non-indigenous ascidians (Chordata: Tunicata) along the Mediterranean coast of Israel.2(e166): 1–7. doi: 10.1017/s1755267209990753TagliapietraDKeppelESigoviniMLambertG (2012) First record of the colonial ascidian Didemnumvexillum Kott, 2002 in the Mediterranean: Lagoon of Venice (Italy).1: 247–254. doi: 10.3391/bir.2012.1.4.02Thessalou-LegakiMAydoğanÖBekasPBilgeGBoyacıYÖBrunelliECircostaVCrocettaFDurucanFErdemMErgolavouAKonstantinouGKoutsogiannopoulosDLamonSMacicVMazzetteRMeloniDMuredduAPaschosIPerdikarisCPirasFPoursanidisDRamos-EsplaAARossoASordinoPSperoneESteriotiATaşkınEToscanaFTripepiSTsiakkirosLZenetosA (2012) New Mediterranean Biodiversity Records (December 2012).13: 312–327. doi: 10.12681/mms.313TuronXNishikawaTRiusM (2007) Spread of Microcosmussquamiger (Ascidiacea: Pyuridae) in the Mediterranean Sea and adjacent waters.342: 185–188. doi: 10.1016/j.jembe.2006.10.040WonhamMJCarltonJT (2005) Trends in marine biological invasions at local and regional scales: the Northeast Pacific Ocean as a model system.7: 369–392. doi: 10.1007/s10530-004-2581-7ZenetosAGofasSMorriCRossoAViolantiDGarcia RasoJEÇinarMEAlmogi-LabinAAtesASAzzurroEBallesterosEBianchiCNBilecenogluMGambiMCGiangrandeAGraviliCHyams-KampzanOKarachlePKKatsanevakisSLipejLMastrototaroFMineurFPancucci-PapadopoulouMARamos EsplaASalasCSan MartinGSfrisoAStreftarisNVerlaqueM (2012) Alien species in the Mediterranean Sea by 2012. A contribution to the application of European Union’s Marine Strategy Directive (MSFD). Part 2. Introduction trends and pathways.13: 328–352. doi: 10.12681/mms.327