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J. Mar. Biol. Ass. U.K. (2004), 84, 593^598 Printed in the United Kingdom

Rare (Porifera: Demospongiae) species from the Mediterranean Sea

P O Eleni Voultsiadou* and Dimitris Va¢dis O *Department of Zoology, School of Biology, Aristotle University of Thessaloniki, GR-54124, Thessaloniki, Greece. Fisheries Research P Institute, NAGREF, N. Peramos 64007, Kavala, Greece. Corresponding author, e-mail: [email protected]

Fourteen rare or poorly known sponge species have been found in the Aegean Sea. The species Pachastrissa pathologica, Calthropella stelligera, Weberella verrucosa, Aaptos papillatus, Timea geministellata, Spiroxya heteroclita, translata, Hymedesmia simillima, Mycale serrulata, Myrmekioderma spelaea, Callyspongia septimaniensis and Ircinia pipetta are new records for the eastern Mediterranean while the species Geodia barretti and Petrosia vansoesti are reported for the ¢rst time from the Mediterranean Sea. Information on their morphology, geographical and bathymetrical distribution is given and discussed.

INTRODUCTION SYSTEMATICS Although the sponge fauna of the western basin of the Twenty-¢ve sponge specimens belonging to 14 demos- Mediterranean is widely considered among the best ponge species classi¢ed in 13 families and 6 orders were known in the world (Uriz & Maldonado, 1993), the knowl- examined. edge of the eastern basin is poor compared with that of the other parts of the Mediterranean (Voultsiadou- Koukoura & van Soest, 1993). Moreover, the sponge Order ASTROPHORIDA diversity of the Aegean Sea is far from being adequately Family CALTHROPELIDAE Lendenfeld, 1907 studied, as has been pointed out by various authors Pachastrissa pathologica (Schmidt, 1868) (Voultsiadou-Koukoura & Koukouras, 1993; Pansini et al., Stelletta pathologica Schmidt, 1868. 2000) and new species are continuously being described Calthropella pathologica, Vacelet, 1969. (e.g. Voultsiadou-Koukoura & van Soest, 1991a,b; Voultsiadou-Koukoura et al., 1991). Our knowledge of the Material examined Porifera of these regions is included in a restricted number One specimen from Station 17, on calcareous algae, at a of publications which have been to some extent reviewed depth of 70 m. by Voultsiadou-Koukoura & Koukouras (1993) and Pansini et al. (2000). Description Accordingly, it is not surprising that sampling in various Massive specimen, having a size of 3.7Â2.5Â2 cm (cortex sites of the Aegean revealed the presence of sponges not width 0.8 mm), with choanosomal canals 2.5 mm in previously recorded from this area. These sponges can be diameter. Skeleton made of calthrops (50^495Â3.6^50 mm), characterized as rare species since they have been oxeas greater than 2000 mm all broken with a maximum recorded with a small number of specimens, from very width of 15 mm, and oxyshaeresters (7.2^17.6 mm). few geographical areas or from speci¢c ecological habitats. The main goal of this paper is to contribute to our Distribution and habitat knowledge of diversity in the Aegean Sea Sciaphilic species found in submarine caves and bathyal and the eastern Mediterranean, as well as to give informa- coral communities, recorded to date only from the western tion on the morphology and distribution of some poorly Mediterranean. Bathymetrical range: 13^250 m. known sponge species. Calthropella stelligera (Schmidt, 1868) MATERIALS AND METHODS Corticium stelligerum Schmidt, 1868. Sponge specimens were collected from 17 stations Corticella stelligera, Lendenfeld, 1894. scattered over the Aegean Sea, excluding the Turkish Corticellopsis stelligera, Diaz & van Soest, 1994. coasts (Figure 1). Sampling was made by free or SCUBA diving, dredges, and grabs down to 90 m. InTable 1 a list of Material examined sampling stations is presented. Sponge specimens and One specimen from Station 7, found as an encrustation spicule preparations have been deposited in the Museum on a mass of calcareous algae, rodophycae and corals, at a of the Department of Zoology. depth of 20 m. The classi¢cation followed in this work was based on a large number of publications and is in agreement with that Description proposed by Hooper & van Soest (2002) in Systema Porifera, The sponge has the form of a thin encrustation. Skeleton and by van Soest (2001). is made of calthrops with rays 120^240 mm long, having a

Journal of the Marine Biological Association of the United Kingdom (2004) 594 E. Voultsiadou and D.Va¢dis Rare sponges from the Mediterranean

Remarks Topsent (1895), as well, reports the presence of oxeas in his description of the type specimen found by Schmidt in the Adriatic. Although large (580^670Â8 mm) and abun- dant, Topsent considers that oxeas are probably foreign material incorporated by C. stelligera.

Family GEODIDAE Gray, 1867 Geodia barretti Bowerbank, 1858 Geodia barretti, Arndt, 1935; Boury-Esnault et al., 1994.

Material examined Five specimens from Station 14, on a vertical rock, at 4 to 6 m. One of the specimens was attached on a polychaete tube.

Description Massive form, one of the specimens spherical, with a diameter of 1cm. Cortex built of a dense layer of sterrasters, 66.5^72 mm and strongyllasters, 2.5^5.8 mm. Choanosomal skeleton includes: dichotriaenes with a rhabdome of 837^1449Â13.5^31.5 mm, protoclads of Figure 1. Map of the Aegean Sea showing the sampling 45^58.5Â11.7 ^31.5 mm and deuteroclads of 27^153Â stations. 6.3^28.8 mm; anatriaenes with clads of 36^55Â3.2 mm and rhabdome length greater than 2000 mm (all were found broken); protriaenes with clads of 36^60Â1.5 mm width of about 20 mm at their base. Microscleres are (their rhabdome length similar to that of the anatriaenes); euasters of two distinct types: chiasters with 8^12 rays, oxysphaerasters, 18^38.8 mm and oxyasters, 7.2^21.6 mm. each 5^8 mm long and oxyasters with six rays measuring 20^28 mm. A considerable number of oxeas, measuring 100^350 mm, exist. Distribution and habitat This is the ¢rst record of this species in the Distribution and habitat Mediterranean Sea. Eurybathic species found on The species has been reported up to date only from the infralittoral, circalittoral and bathyal bottoms. Known coasts of Algery, the Adriatic and the Canary Islands, from the Arctic Seas, the eastern Atlantic coasts and among coral polyps and in the intertidal zone. Bathyme- the Spanish^Moroccan Gulf. Bathymetrical range: trical range: 0^20 m. 4^1747 m .

Table 1. List of sampling stations.

Station Locality Coordinates

1 Thermaikos Gulf 40812’00’’N22852’55’’E 2 Thermaikos Gulf 39849’50’’N23813’20’’E 3 Agia Paraskevi 39855’15’’N23842’20’’E 4 Strymonikos Gulf 40835’10’’N23858’45’’E 5 GulfofKavala 40851’20’’N24828’00’’E 6 North-east of Lemnos Island 40800’00’’N25821’25’’E 7 North-west of Agios Eustratios Island 39833’30’’N25803’60’’E 8 North-east of Youra Island 39827’20’’N24815’50’’E 9 Youra Island 39825’20’’N24808’10’’E 10 South-west of Lesvos Island 39804’20’’N25855’20’’E 11 West of Chios Island 38826’30’’N25847’40’’E 12 Linaria, Skyros Island 38849’00’’N24831’40’’E 13 Agios Georgios, Evoia Island 38849’20’’N22856’70’’E 14 Skorponeria, Voiotia 38834’00’’N23821’20’’E 15 Sarakiniko, Evoia Island 38846’20’’N23842’20’’E 16 Mesochoria, Evoia Island 38821’30’’N24814’20’’E 17 Lindos, Rhodes Island 36808’40’’N28805’20’’E

Journal of the Marine Biological Association of the United Kingdom (2004) Rare sponges from the Mediterranean E. Voultsiadou and D.Va¢dis 595

Order HADROMERIDA subterminal head. Spicule dimensions: astrose micro- Family POLYMASTIIDAE Gray, 1867 scleres, 6.75^20 mm, tylostyles 190^750 mm. Weberella verrucosa Va c e l e t , 19 6 0 Distribution and habitat Webe re ll a v e r r u cos a Vacelet, 1960. Known hitherto only from its type locality (Bay of Naples) where it was found on a Posidonia rhizome. Bathy- Material examined metrical range: 10^35 m. One specimen from Station 3, on calcareous algae, at 70 m. Family ALECTONIDAE Rossel, 1996 Description Spiroxya heteroclita Topsent, 1896 Massive globular specimen with a restricted base, Spiroxya heteroclitaTopsent, 1896. minutely hispid on the surface. Ectosome, not detachable, made of tylostyles measuring 95^15 0Â2 mm. Choano- Material examined somal skeleton made of spicule tracts forming an irregular One specimen from Station 8, on a rocky plateau, in reticulation. The dimensions of the choanosomal tylostyles crevices possibly made by boring sponges at 20 m. are 250^500Â4^8 mm. Description Distribution and habitat A small encrustation entirely used for spicule prepara- The species has been hitherto reported only from the tions. Skeleton: oxeas strongly curved in their middle north-western Mediterranean coast and the Spanish^ (82.8^774Â1.9^23.4 mm) and microstrongyles curved, with Moroccan Gulf, on rocky, detritic and coralligenous spines around them (68.4^86.4Â3.6^5.4 mm). bottoms. Bathymetrical range: 64^16 0 m. Distribution and habitat Family SUBERITIDAE Schmidt, 1870 Reported only from the western Mediterranean, in rock Aaptos papillatus (Keller, 1880) crevices, sub-horizontal rocks and coralligenous bottoms. Bathymetrical range: 12^35 m. Aaptos papillatus,Lopes,1989.

Material examined Order One specimen from Station 2, on a detritic bottom, at Family Carter, 1875 about 40 m. Clathria translata (Pulitzer-Finali, 1978) translata Pulitzer-Finali, 1978. Description translata, Hooper, 1996. Massive, spherical specimen, 6 cm in diameter, with a narrow base of attachment. Numerous papillae on the Material examined surface, 3^6 mm in diameter, 1^4 mm apart. Skeleton Two specimens from Stations 5 and 11 on detritic made of strongyloxeas (1800^2790Â31.5^63 mm) and bottoms at about 50 m. tylostyles or styles (270^630Â4.5^13.5 mm). Description Distribution and habitat Lobate form with ¢nely hispid surface. Skeleton structure Amphi-atlantic species, known so far in the and form of spicules ¢ts well to the description given by Mediterranean only from the north-western Italian coast, Pulitzer-Finali (1978). Styles measuring 90^333Â5^15 mm, collected on rocky and detritic bottoms. Bathymetrical the smaller showing a remarkable centrotylotism. Subtylo- range: 15^100 m. styles 320^380Â4^5 mm.

Distribution and habitat Family TIMEIDAE To p s e n t , 1 9 2 8 This is the second record of this species. It was known Timea geministellata Pulitzer-Finali, 1978 only from its type locality (Bay of Naples) where it was Timea geministellata Pulitzer-Finali, 1978. found on a gastropod shell. Bathymetrical range: 40^50 m.

Material examined Four specimens from Stations 1 and 4 on the sponge Family HYMEDESMIDAE Topsent, 1928 Hymedesmia simillima Fasciospongia cavernosa at 10 and 35 m and Stations 12 and Lundbeck, 1910 15 on rocks at 4^6m. Hymedesmia simillima Lundbeck, 1910.

Description Material examined All specimens are thin encrustations. Ectosomal One specimen from Station 5, attached on calcareous skeleton made of densely packed euasters of variable algae, at 80 m. form: chiasters (both strongylasters and oxyasters) and the characteristic asters described by Pulitzer-Finali Description (1978). Choanosomal skeleton made of erect, straight or Encrusting specimen, with soft surface, bearing small slightly curved tylostyles, with trilobate and sometimes spherical papillae. Ektosomal skeleton is made of tornotes

Journal of the Marine Biological Association of the United Kingdom (2004) 596 E. Voultsiadou and D.Va¢dis Rare sponges from the Mediterranean changing to oxeas, measuring 198^297 mm. Choanosomal Order HAPLOSCLERIDA skeleton made of erect on the substrate acanthostyles, of Family CALLYSPONGIIDAE de Laubenfels, 1936 two size categories: large, 270^424.8 mm, decorated with Callyspongia septimaniensis Griessinger, 1971 spines near their base, and small, 79.2^15 8.4 mm, almost Callyspongia septimaniensis Griessinger, 1971. totally covered with spines. Microscleres are arcuate Callyspongia simplex, de Weerdt & van Soest, 1986. isochelae, 16.2^32.4 mm. Material examined Distribution and habitat One specimen from Station 6, on a rock, at 4 m. Eurybathic species reported to date only from the Atlantic and the Adriatic Sea, living on shells, stones, poly- Description chaete tubes and detritic bottoms. Bathymetrical range: The specimen ¢ts well to the description given by 50^1264 m. Griessinger (1971).

Family MYCALIDAE Lundbeck, 1905 Distribution and habitat Mycale serrulata Sara & Siribelli, 1960 This is the second report of this species. It has been previously reported only from its type locality (Gulf of Mycale serrulata Sara & Siribelli, 1960. Lyon), on coastal detritic bottoms. Bathymetrical range: 4^35 m. Material examined Two specimens from Station10, on the sponge Fasciospongia cavernosa,atadepthof90m. Family PETROSIDAE van Soest, 1980 Petrosia vansoesti Boury-Esnault, Pansini & Uriz, 1994 Description (Figures 2 & 3) Small encrustation. Skeleton made of subtylostyles (270^ Petrosia vansoesti Boury-Esnault et al., 1994. 342Â3^11 mm), anisocheles of two size categories (small, 14^18 mm and large, 24^35 mm) and sigmata, characteris- Material examined tically indented on the outer surface of their big curving, One specimen from Station 9, on a cave wall, at 20 m. or rarely of both curvings (64^98 mm). Description Distribution and habitat The sponge has a stony texture and an almost globular Records of this species exist only from the Bay of shape with a diameter of 3.5Â3.5 cm, getting narrower Naples and Alboran Island. It has been found on coastal towards the base of attachment. It bears an oscule, detritic bottoms and Posidonia meadows. Bathymetrical having a diameter of 0.5 cm, in the middle of a depression, range: 15^90 m. on its upper surface. Small ostia are arranged in groups around the body. Ectosomal skeleton is made of a reticula- Order HALICHONDRIDA tion of spicules, while choanosomal skeleton of thick tracts, Family DESMOXYIDAE Hallmann, 1917 having a mean width of 200 mm, forming meshes with a Myrmekioderma spelaea (Pulitzer-Finali, 1983) mean diameter of 500 mm, obscured by irregular masses of spicules in some places. Spicules are oxeas to strongyles Rhaphisia spelaea Pulitzer-Finali, 1983. of very variable length and width, having a size range of 40^320Â2^32 mm. Styles of equally variable size are also Material examined present although not equally abundant. Size categories Three specimens from Station 9 at the entrance of a cannot be easily distinguished. However, in the ectosomal submarine cave at 10 m, and Station 16 on rocks at 2 m. skeleton, a dominance of oxeas measuring 50^200Â 3^8 mm is observed, while in the choanosome, most abun- Description dant seem to be large oxeas, strongyles and styles having a The largest of the specimens examined (that from Station 9) is an irregularly massive sponge measuring 4Â2.5Â2 cm. The other two specimens are only small pieces. The choanosomal skeleton consists of spicular tracts forming meshes of 150^300 mm. The ectosome is formed of a thick layer of spicules, not in any special arrangement. Spicules are: (a) oxeas (sometimes modi¢ed to styles) of two categories, small 100^300Â5^10 mm, and large 400^950Â10^25 mm; (b) trichodragmata measuring up to 300 mm, very abundant in all specimens.

Distribution and habitat This species is known only from the Adriatic and the Balearic Islands, living in submarine caves and rock cavities. Van Soest et al. (1990) took into account this Figure 2. Petrosia vansoesti Boury-Esnault, Pansini & Uriz, Aegean specimen in their review of Halichondrid 1994, whole specimen (natural size): (A) lateral view; (B) top classi¢cation. Bathymetrical range: 0.6^12 m. view.

Journal of the Marine Biological Association of the United Kingdom (2004) Rare sponges from the Mediterranean E. Voultsiadou and D.Va¢dis 597

Figure 3. Petrosia vansoesti Boury-Esnault, Pansini & Uriz, 1994, skeleton: (A) cross-section near the surface; (B) and (C) spicules. size of 200^320Â20^32 mm and small strongyles Specially Protected Areas and Biological Diversity in the measuring 50^100Â12^28 mm. Spicules very often bear Mediterranean adopted in the Barcelona Convention small rounded projections on their surface. (1996), revised in the Bern Convention (1998).

Distribution and habitat This is the ¢rst record of this species in the DISCUSSION Mediterranean Sea and the second worldwide. It has The exact number of the Aegean sponge species is not been found in the Spanish^Moroccan Gulf, in bathyal known, although a rough estimation of 170 species is given rock communities. Bathymetrical range: 20^362 m. by Koukouras et al. (2001), and the construction of a check-list has been considered necessary. The 14 sponge species presented in this paper are Order DICTYOCERATIDA reported for the ¢rst time in the Aegean Sea and generally Family IRCINIIDAE Gray, 1867 in the area of the eastern Mediterranean. Eight of the Ircinia pipetta (Schmidt, 1868) species found in the Aegean (Pachastrissa pathologica, Timea Hircinia pipetta Schmidt, 1868. geministellata, Spiroxya heteroclita, Clathria translata, Mycale serrulata, Myrmekioderma spelaea, Callyspongia septimaniensis Material examined and Ircinia pipetta) should be considered Mediterranean One specimen from Station 13, on rocks, at 30 m. endemics. The number of the zoobenthic Mediterranean endemic species occurring in the Aegean Sea, which was Description estimated to be lower than that of other Mediterranean The specimen ¢ts well with the description given by areas (Koukouras et al., 2001), is thus increasing. Seven Uriz & Maldonado (1993). of the above endemic species, namely P. pathologica, T. geministellata, S. heteroclita, Clathria translata, Mycale Distribution and habitat serrulata, Callyspongia septimaniensis and I. pipetta have been The species has been hitherto reported only from the found so far only in the western Mediterranean, while western Mediterranean, found on rocky and coralligenous Myrmekioderma spelaea has a wider distribution in the substrates. It is considered endemic to the south-western Mediterranean including the Adriatic Sea. Moreover, the Mediterranean area. Bathymetrical range: 11^120 m. species Calthropella stelligera, Webe re ll a v e r r u cos a , Aaptos papillatus,andHymedesmia simillima have an Atlanto^ Remarks Mediterranean distribution. It is included among the endangered Mediterranean Most of the above species were generally collected within species and is protected according to the Protocol of their known bathymetric limits. Five species show an

Journal of the Marine Biological Association of the United Kingdom (2004) 598 E. Voultsiadou and D.Va¢dis Rare sponges from the Mediterranean extension of these limits:T.geministellata which was found at Lopes, M.T., 1989. On Aaptos papillata (Keller, 1880) 30 m shows an extension of its distribution to 10 and 35 m; (Hadromerida,Tethyidae). Arquivosdo Museu Bocage,1,233^240. Clathria translata found in 40 m, extends its distribution Lundbeck, W., 1910. Porifera. III. Desmacidonidae. The Danish down to 50 m; Mycale serrulata extends its lower limit from Ingolf Expedition,no.6,124pp. 50 m to 90 m; Callyspongia septimaniensis found at 35 m shows Pansini, M., Morri, C. & Bianchi, C.N., 2000.The sponge commu- nity of a subtidal area with hydrothermal vents: Milos Island, an extension of its distribution up to a depth of 4 m; for Aegean Sea. Estuarine, Coastal and Shelf Science, 51,627^635. Calthropella stelligera found in the present study at 20 m, Pulitzer-Finali, G., 1978. Report on a collection of sponges from there is only one depth record, at the intertidal zone. the Bay of Naples. III. Hadromerida, Axinellida, The species Geodia barretti, a boreal-Atlantic species, and Poecilosclerida, Halichondrida, Haplosclerida. Bolletino del Petrosia vansoesti, a species reported only from the Spanish^ Museo del Istintuto Biologico, Universita di Genova, 45,7^89. Moroccan Gulf, are new records for the Mediterranean Pulitzer-Finali, G., 1983. A collection of Mediterranean Sea. The ¢nding of these two Atlantic species in the Demospongiae (Porifera) with, in appendix, a list of the Aegean Sea is remarkable, since they have not been found Demospongiae hitherto recorded from the Mediterranean in the western part of the Mediterranean. However, Sea. Annali del Museo Civico di Storia Naturale di Genova, 84, according to Koukouras et al. (2001), the Aegean Sea, 445^621. although distant from the Strait of Gibraltar (the main Sara, M. & Siribelli, L., 1960. La fauna di Poriferi delle ß secche del Golfo di Napoli. Annuario dell’ Istituto e Museo di pathway for enrichment for the Mediterranean fauna) Zoologia della Universita di Napoli, 7,1^93. is dominated by Atlanto^Mediterranean species. The Schmidt, O., 1868. Die spongien der Ku«ste von Algier. Mit nachtregen zu present work extends the known upper limits of the bathy- den spongien des Adriatischen Meeres (drittes Supplement). Leipzig: metrical distribution of these two species. Petrosia vansoesti Engelman. was found in a submarine cave, at 20 m, while in its type Soest, R.W.M. van, 2001. Porifera. In European register of marine locality it was collected at 285^362 m (Boury-Esnault et species. A check-list of the marine species in Europe and a bibliography al., 1994); this di¡erence is acceptable since the cave envir- of guides to their identi¢cation (ed. M.J. Costello et al.), pp. 85^103. onment can be considered as an enclave of circalittoral Paris: Publications Scienti¢ques du Muse¤ um National conditions in the subtidal zone. Geodia barretti, reported to d’Histoire Naturelle. date from depths of 15^1747 m (Arndt, 1935; Boury- Soest, R.W.M. van, Diaz, M.C. & Pomponi, S., 1990. Phylogenetic classi¢cation of the Halichondrids (Porifera, Esnault et al., 1994), was collected at a depth of 4^6m. Demospongiae). Beaufortia, 40,15^62. All the sponge species studied have been rarely reported Topsent, E., 1895. Etude monographique des spongiaires de in the literature. The recently described species France. II. Carnosa. Archives de Zoologie Experimentale et T. geministellata, Clathria translata, Callyspongia septimaniensis Ge¤ne¤rale, 3,493^590. and P. vansoesti have been reported only once from their Topsent, E., 1896. Mate¤ riaux pour servir a l’e¤ tude de la faune des type locality and their ¢nding in the Aegean con¢rms spongiaires de France. 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Contribution to Boury-Esnault, N., Pansini, M. & Uriz, M.J., 1994. Spongiaires the knowledge of keratose sponges (Dyctioceratida, Dendro- bathyaux de la mer d’ Alboran et du golfe ibero-marocain. ceratida, Verongida: Demospongiae, Porifera) of the Aegean Me¤moires du Muse¤um National d’Histoire Naturelle, 160,1^174. Sea. Mittheilungen aus des Zoologischen Museum zu Berlin, 69,57^72. Diaz, M.C. & Soest, R.W.M. van, 1994. The Plakinidae: a Voultsiadou-Koukoura, E. & Soest, R.W.M. van, 1991a. systematic review. In Sponges in time and space (ed. R.W.M. van Hemiasterella aristoteliana n. sp. (Porifera, Hadromerida) from Soest et al.), pp. 93^109. Rotterdam: A.A. Balkema. the Aegean Sea with a discussion of the family Griessinger, J.-M., 1971. Etude des Re¤ nie¤ rides de Mediterranee¤ e Hemiasterellidae. Bijtragen tot der Dierkunde, 61,43^49. ( Haploscle¤ rides). Bulletin du Muse¤um National Voultsiadou-Koukoura, E. & Soest, R.W.M. van, 1991b. 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Macrobenthic fauna diversity in the Aegean Sea, a⁄- with comments on Coscinoderma confragosum (Porifera, nities with other Mediterranean regions and the Black Sea. Dictyoceratida). Zoologica Scripta, 20,195^199. Bios (Macedonia, Greece), 6,61^76. Weerdt, W.H. de & Soest, R.W.M. van, 1986. Marine shallow- Lendenfeld, R., 1894. Tetractinelliden der Adria (mit einen water Haplosclerida (Porifera) from the south-eastern part of anhang u« ber die Lithistiden). Denkschriften der Akademie der the North Atlantic Ocean. ZoologischeVerhandelingen, 225,1^49. Wissenschaften, 61,91^204. Submitted 25 September 2003. Accepted 10 March 2004.

Journal of the Marine Biological Association of the United Kingdom (2004)