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DOI 10.1007/s10347-006-0094-9

ORIGINAL ARTICLE

Skeletal response of Lophelia pertusa (Scleractinia) to bioeroding sponge infestation visualised with micro-computed tomography

Lydia Beuck · Agostina Vertino · Elizaveta Stepina · Marek Karolczak · Olaf Pfannkuche

Received: 27 July 2006 / Accepted: 22 November 2006 / Published online: 16 March 2007© Springer-Verlag 2007

Abstract The skeleton morphology of the azooxanthel-late cold-water coral Lophelia pertusa can be stronglyinXuenced by invasive boring sponges that infest corallitesin the still living part of the colony. Atypically swollencorallites of live Lophelia pertusa from the GalwayMound (Belgica Carbonate Mound Province, PorcupineSeabight, NE Atlantic), heavily excavated by boringorganisms, have been examined with a wide range of non-destructive and destructive methods: micro-computedtomography, macro- and microscopic observations of theouter coral skeleton, longitudinal and transversal thin sec-tions and SEM analyses of coral skeleton casts. As a result,three excavating sponge species have been distinguishedwithin the coral skeleton: Alectona millari, Spiroxya het-eroclita and Aka infesta. Furthermore, four main coral/

sponge growth stages have been recognised: (1) cylindricaljuvenile corallite/no sponge cavities; (2) Xared juvenilecorallite/linear sponge cavities (if present); (3) slightlyswollen adult corallites/chambered oval sponge cavities;(4) very swollen adult corallites/widespread cavities. Theinferred correlation between corallite morphology and bor-ing sponge infestation has been detected in micro-com-puted tomography (micro-CT) images and conWrmed insponge trace casts and peculiar features of coral skeletonmicrostructure.

Keywords Bioerosion · Interaction · Ecotype · Lophelia · Boring sponges · Micro-computed tomography (micro-CT) · Porcupine Seabight

Introduction

Shallow-water scleractinian corals are notorious for thehigh level of skeletal intraspeciWc variability, generallyinterpreted as a result of varying environmental factors,like light, wave/current intensity and sedimentation rate(e.g. Wells 1957; Hubbard and Pocock 1984; Veron 2000).It is well known that deep-water corals also present highlyvariable morphologies, but the factors that trigger this highvariability are still poorly understood. In most commondeep-water, reef-building species of the NE Atlantic—Lophelia pertusa (Linnaeus, 1758), Madrepora oculataLinnaeus 1758 and Solenosmilia variabilis Duncan,1873—coenosteal development, packing of corallites,morphology of individual calices and their internal struc-tures frequently vary even within the same colony (e.g.Duncan 1877; Gravier 1920; Strømgren 1971; Cairns1979; Zibrowius 1980, 1984; Freiwald et al. 1997).Zibrowius (1980, 1984) points out that the size and stability

Electronic supplementary material The online version of this article (doi:10.1007/s10347-006-0094-9) contains supplementary material, which is available to authorised users.

L. Beuck (&) · A. VertinoInstitute of Palaeontology, Erlangen University, Loewenichstr. 28, 91054 Erlangen, Germanye-mail: beuck@pal.uni-erlangen.de

A. VertinoDepartment of Geological Science, Corso Italia 55, 95129 Catania, Italy

E. Stepina · M. KarolczakInstitute of Medical Physics, Erlangen University, Henkestr. 91, 91052 Erlangen, Germany

O. PfannkucheIFM-GEOMAR, Wischhofstr. 1–3, 24148 Kiel, Germany

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of the substrate, as well as the available space during thecoral growth, remarkably inXuence the attachment struc-tures and the shapes of both solitary and colonial deep-water scleractinian taxa. Freiwald et al. (1997) rule out thatthe distribution of the three Lophelia growth forms fromStjernsund Sill depends solely on hydrodynamics. Instead,they consider the competition for food and space with ses-sile organisms (such as octocorals, sponges and hydroids)as a potential cause of ecotypes in Lophelia. Furthermore,they underline the positive correlation between increasedcoenosteum thickness (inducing “introvert ecotype” for-mation) and the presence of the non-obligate symbioticpolychaete Eunice norvegica (Linnaeus, 1767); an obser-vation subsequently conWrmed by Freiwald and Wilson(1998) and widely developed in Roberts (2005). Accord-ing to these authors, the coral would overgrow and sup-press episkeletozoans (such as bryozoans, polychaetes,foraminiferans) that colonise the tissue-barren skeletonclose to the polyp edge.

The Wnding at 1,039 m depth on the western Xank ofthe Galway Mound (Porcupine Seabight) of remarkablyswollen corallites of living Lophelia pertusa, highlyaVected by bioerosion processes, has led us to investigatethe possible eVects of sponge infestation on skeletalaccretion. Boring sponges are the most eYcient bioero-ders of deep-water corals exposed to the seawater. Nor-mally, they infest the tissue-barren portions of coralskeleton. At the coral site oV Santa Maria di Leuca (IonianSea), it was observed that the Wrst juvenile sponge tracesappear 1.5 cm below the living zone in a Desmophyllumdianthus (Esper, 1794; =Desmophyllum cristagalli MilneEdwards and Haime, 1848; Beuck, personal observations,2006). In Lophelia pertusa colonies from the PropellerMound (Porcupine Seabight), the Wrst sponge traces aregenerally found 10 cm below the living zone. However,exceptional occurrences within the living zone are alsoreported (e.g. for Spiroxya heteroclita) and discussed as apotential indicator for environmental stress (Beuck andFreiwald 2005).

So far, the inXuence of endobionts on coral skeletalaccretion has not been investigated. In order to correlateabnormal Lophelia morphology observed at GalwayMound with the spatial distribution of boring spongesinfesting the coral, we carried out a combination of severalinvasive and non-invasive analyses: macro- and micro-photography, micro-computed tomography (micro-CT),thin sectioning and trace casting. Micro-CT has recentlybecome a well-known entity for medical applications deal-ing with tissue samples, biopsies and preserved or livingorganisms (Kalender 2005; Nickel et al. 2006a, b). Fur-thermore, the methodology has been applied to fossilbones, teeth, belemnites, algae and embryos for palaeobio-logical studies (e.g. Rossi et al. 2004; Siegel 2003;

Mietchen et al. 2005). Trace studies with the aid of com-puted tomography (CT) have already been carried out onRecent and fossil empty sponge borings, however, the res-olution of this methodology hampers a detailed trace anal-ysis (see Schönberg 2001; Beuck 2002). In this paper,micro-CT is used for the Wrst time to visualise the three-dimensional development of boring sponge cavities inscleractinian coral skeletons. Our results show that thismethod is also extremely useful in the understanding ofinterspeciWc interactions.

Study area

The Porcupine Seabight (PSB) is a roughly semicircularembayment in the continental margin southwest of Ire-land (Fig. 1a). It is bounded by the Porcupine Bank to thewest and north, the Irish and Celtic Sea shelves to thenorth and east and the Goban Spur to the south. It openson to the Porcupine Abyssal Plain through a relativelysmall entrance to the southwest. The eastern margindiVers markedly from the other parts of the PSB via theoccurrence of carbonate mounds and a system of smallchannels (Gollum channel system) which coalesce in thedeeper PSB and apparently constitute a major conduitsystem on the eastern slope (Masson and Miles 1986).Recent research cruises proved the existence of 64mounds in the eastern PSB, the Belgica Mound Province(BMP), of which about 20 are buried by sediment drifts(De Mol et al. 2002, 2005). Belgica Mound Province(BMP) mounds cluster in two ridges at 700 and 900 mdepth of a major N–S trending contourite channel (vanRooij et al. 2003). The top of the elongated, and N–S ori-ented Galway Mound (Fig. 1a) lies at 800 m water depthat about 51°27.083�N and 11°45.133�W and is denselycovered by living reef-forming scleractinians (Madre-pora oculata and secondarily Lophelia pertusa), oftenassociated with gorgonians and sponges—e.g. Aphrocall-istes beatrix Gray, 1858 (Fig. 1b). Towards the base ofthe mound, live coral colonies are sparse, whereas thesponge Aphrocallistes beatrix becomes more abundant(Fig. 1c). Hydrodynamic studies (Huthnance et al. 2001)indicate that the major transport in the area of the shelfbreak is generated by a northward slope current. Typicalvelocities are 5 cm/s. Tidal currents of about 20 cm/s onthe adjacent shelf can generate strong internal waves atthe shelfbreak. Wind-, tide- and wave-forced currents,typically reaching 100 cm/s, are the most important fac-tors for cross-slope exchanges. However, topographiceVects, e.g. by carbonate mounds, can generate signiW-cant hydrodynamic local changes. Reef-forming coralstake advantage of the high current regime, related nutri-ent Xux and the reduced sediment deposition of the deep

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NS orientated channel. Water masses in the BMP aremainly composed of Eastern North Atlantic Water(ENAW) which exhibits a linear, uniform distributiondown to a salinity minimum at around 700 m, where itoverlies Mediterranean outXow water (MOW), which isdepicted by a salinity increase to maximum values of35.5 at 900 m and a relatively low-dissolved oxygen con-tent of 4.3 ml/L (Pfannkuche and Utecht 2005). Belowthe MOW, the inXuence of Labrador Sea water is seen ina salinity minimum and oxygen maximum at about1,700 m depth at a temperature of 3.5°C.

Materials and methods

Lophelia pertusa specimens were taken with a box-core(station no. POS 316-525) at the southwestern Xank of theGalway Mound (51°26.878�N and 11°45.617�W) at1,039 m water depth (Fig. 1a) on RV Poseidon cruise P316in August 2004 (Pfannkuche and Utecht 2005). The sedimenttemperature measured was 9.3°C. The box-core had adimension of 50£50 cm and a maximum recovery of30 cm. The upper 3 cm of the sampled sediment werecomposed of coral rubble mixed with light brownish grey

Fig. 1 a–c Study area. a Over-view map (source NGDC; http://www.ngdc.noaa.gov/mgg/im-age/2minrelief.html) showing the Belgica Mound Province (BMP) and close-up of the elon-gated and N–S-oriented Galway Mound (generated from multi-beam data of Andreas Beyer, AWI-Bremerhaven, Germany). The box core POS316-525 was recovered on the southwestern Xank at 1,039 m water depth. b Mound top colonised by octoco-rals and scleractinians (© Ma-rum, Bremen, Germany, 2004); image width about 120 cm. c Mound base: sparsely distrib-uted living coral colonies associ-ated with the white sponge Aphrocallistes beatrix Gray, 1858 (© Marum, Bremen, Ger-many, 2004); image width about 120 cm. d–e Studied box-core sample (POS316-525). d Sur-face mainly composed of dead coral rubble, serving as a sub-strate for Aphrocallistes beatrix (white arrows), yellow sponges and other encrusting organisms (box-core surface dimension: 50£50 cm). e Close-up of d showing the dominance of dark-coated Lophelia pertusa (Linna-eus, 1758) branches; white ar-rows pointing at the living colonial fragments studied herein

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silty sand (Fig. 1d), whereas the lower part of the core con-sisted of homogeneous greyish-brown clay. The gradualtransition between the upper and lower parts was aVectedby bioturbation (see also Beuck 2005).

Nearly all coral specimens found on the surface of thesediment were dead (Fig. 1d, e): dark-coated branches upto 30 cm in height of Lophelia pertusa and Madreporaoculata and the solitary species (in order of abundance)Caryophyllia sarsiae (Zibrowius, 1974), Desmophyllumdianthus and Stenocyathus vermiformis (Pourtalès, 1868).Most of the dead colonial fragments had been heavilyeroded by boring sponges and encrusted by dead and/orlive epifauna such as hydrozoans, serpulids, bryozoans,sponges (e.g. Aphrocallistes beatrix), bivalves—e.g.Delectopecten vitreus (Gmelin, 1791)—actinians and sty-lasterids. Only two scleractinian species, Lophelia per-tusa and Caryophyllia sarsiae, were recovered alive.These were preserved in ethanol. When collected, the liveLophelia fragments were widely devoid of coenenchyme.Although the young corallites and the distalmost part ofthe adult ones still contained pale orange soft tissue, theywere strongly excavated and contained yellowish boringsponge tissue. The surface of the remaining tissue-barrenskeletal portions were coated with a faint brownish layerof Fe–Mn oxides (see Freiwald and Wilson 1998) andshowed several circular holes corresponding to spongeopenings (Figs. 2g and 3). Average diameters of the largerapertures ranged between 1 and 1.5 mm. The smallestdiameters measured are 0.1–0.3 mm. In some holes, yel-lowish sponge tissue could be seen.

The results presented herein are based on generalobservations of both the tissue-barren and tissue-bearingLophelia pertusa fragments collected from the surface ofthe box-core. Detailed morphological analyses were doneon the live branch portions (Figs. 2, 3, 4, 5, 6; Table 1). Inorder to reconstruct the spatial distribution of the tracegalleries within the live coral branches, a 3 cm long seg-ment including two and one half corallites (POS316-525-1, Fig. 5) and a 3.8-cm-long-one containing six corallites(POS316-525-2, Fig. 4) were selected for micro-CT anal-ysis. A high-resolution micro-CT scanner (Institute ofMedical Physics, Erlangen University, Germany) wasused (see also Kalender 2005, Fig. 7.9). The samples werescanned at a tube voltage of 80 kV and a nominal voxelsize of 30 �m, creating 720 projections and reconstructedin a 550£400£600 volume. The data were visualised insyngo CT.3D with two-dimensional and three-dimen-sional post-processing tools. The common view ofacquired slices on a monitor is from caudal, resulting inside-inverted images. Thus, the micro-CT scan analysisWgures of this study were taken by screenshots from themonitor and subsequently mirrored. Additionally, threetypes of movies were produced: (1) two-dimensional

movies using individual section images serially takenwith an interval of 0.1 mm (movies 2D1 and 2D2), (2)movies of rotating three-dimensional sample reconstruc-tions using 360 images, showing the object from all possi-ble angles in a deWned rotation axis (movies 3D2_1,3D2_2, 3D2_3, 3D2_4 and 3D2_5), (3) movies for ana-glyph glasses (movies rb2_1, rb2_2, rb2_3, rb2_4 andrb2_5), using the dataset of the latter by superimposingtwo movies with a six frame oVset (equal to 6°). The con-version from images to movies was done with the soft-ware VideoMach 3.1.7. The anaglyph technique for thethree-dimensional movies was carried out in Adobe Pre-miere 2.0 by colouring the individual movies (red/blue)and rendering the compound movie with a transparency of50% of the upper one. In total, 12 movies were created,which are stored in the online data repository of FACIESas electronic supplementary material.

In view of species identiWcation, tissue of the boringsponges was taken from individual cavities and maceratedwith H2O2 for spicule isolation. The sponge spicules wereanalysed with a CamScan scanning electron microscope(SEM). Voltage was set at 15–17 kV, and cathode emissionwas forced at 100–130 �A. After micro-CT analysis, thespecimens POS-316-525-1/-2, as well as Wve additionalcorallites, were embedded in resin according to the vacuumembedding technique described in Beuck and Freiwald(2005). Six corallites of the specimens POS316-525-1/-2(two and four, respectively) were treated for longitudinaland transverse thin sections (Figs. 4a, 5a, 6) and analysedwith a transmission light microscope for skeletal micro-structure analyses. The remaining pieces and the Wveembedded individual corallites were sectioned longitudi-nally and the carbonate was entirely dissolved with a solu-tion of 5% HCl. The exposed trace casts were analysedwith a microscope and documented on digital images(Fig. 7a).

Ichnometry was done with Adobe Photoshop CS soft-ware. The morphological reconstruction of the sponge cav-ity (Fig. 8) resulted from the combined analysis of micro-CT and an observation of trace resin casts. For comparison,specimens of Madrepora carolina (Pourtalès, 1871) fromthe Strait of Florida (24°29� N–80°53� W; 191 m water

Fig. 2 Coral morphological groups/growth stages 1–3. a–b Cylindri-cal corallite (growth stage 1). a Lateral view. b Calicular view; note re-mains of pale-orange polyp tissues within the large fossa. c–d DistallyXared corallite (growth stage 2). c Lateral view. d Calicular view; noteremains of pale-orange polyp tissues within the narrow fossa. e–f Sym-metrically slightly swollen corallite (growth stage 3a). e Lateral view.f Calicular view; note soft tissue remains between septa. g–h Asym-metrically slightly swollen corallite (growth stage 3b). g Lateral view.Note sponge aperture (sa). h Calicular view; note soft tissue remainsbetween septa

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depth), held at the Rosenstiel School Museum (Miami Uni-versity, Florida) were examined and illustrated.

Terminology

We have deWned the term white zone as the part of the skel-eton that has a “fresh-looking” aspect (e.g. Fig. 3c). Whenthis part of the colony is still alive, its skeleton is coveredby the soft tissue and, therefore, protected against erodingand fouling organisms. In adult corallites, the lower part ofthe white zone can be slightly infested due to episodicupward retractions of the soft tissues (polyp “edge zone”;Harmelin 1990; Stolarski 1996). The terms “endoskeletozo-ans”, “episkeletozoans” and “endozoans” are used in thetext according to the deWnition of Taylor and Wilson(2002). The abbreviations of the coral skeletal features usedin the text are explained in Table 1.

Results

Morphology and growth stages of swollen Lophelia pertusa and associated excavating sponges

Live Lophelia pertusa

The branches are massive and bear atypically swollen andirregularly arranged corallites. The soft tissues cover onlythe juvenile corallites or the distal part of the adult ones.The tissue-bearing skeleton, protected against epibionts,appears white and clean, whereas the tissue-barren skeletalparts (below the maximal extension of the coenenchyme)are covered with a faint brownish coating of Fe–Mnoxides and infested by excavating and encrusting organ-isms (note the sharp boundary in Fig. 3c). The shape andsize of the living corallites is extremely variable (Figs. 2and 3). Generally, with increasing size, their shapeevolves from tubular to globular and the living polyp zoneprogressively retreats. Both the longitudinal and transver-sal proWle of the most adult corallites can be very irregu-lar, resulting in aberrant morphologies (see detaileddescription). Considering the corallite skeletal featureslisted in Table 1, four main morphological groups havebeen recognised, each of them corresponding to a distinctcoral growth stage.

Group 1. Cylindrical corallites (juvenile stage; Fig. 2a,b): straight to slightly curved tubular shapes (Fig. 2a), up to15 mm in length. Diameter of the corallite (2–3 mm) moreor less constant along its extension, calice proWle generallycircular and calicular edge slightly jagged. Very narrow (upto 1 mm wide) and thin septa, ranging in number from 18 to24, encircling a relatively large and very deep fossa(Fig. 2b). Septa arranged in irregular systems: 2–4 primary

septa and correspondent very short costae just below thecalicular edge. Thickness of the uppermost theca rangesfrom 0.3 to 0.5 mm. Outer theca surface is smooth in thevicinity of the calicular edge and homogeneously granu-lated in the proximal area. Skeletal white zone widelydeveloped; when alive, the smallest corallites are entirelycovered with soft tissues.

Group 2. Distally Xared corallites (juvenile to adultstage; Fig. 2c, d; corallites four and Wve in Fig. 4): straightand cylindrical in the proximal part, slightly curved andXared in the upper part (Fig. 2c). Length up to 16 mm, butmost commonly around 12 mm. Calice circular to slightlyelliptical; greater calicular diameter rarely exceeding 8 mm,most commonly around 6 mm. Slightly jagged calicularedge and the total septal number is around 30. Primarysepta (S1) more exsert than the others (S2, S3) and varyingin number from 5 to 7. S2 externally thinner and slightlynarrower than S1; S3 often recessed in the corallite wall,very narrow and thin (Fig. 2d). Narrow and deep fossa(maximum diameter up to one third of the GCD: greatcalicular diameter), sometimes partitioned by thin tabulae(white arrows in Fig. 4b). Along the calicular edge, thesolid theca (ca. 1 mm thick) embeds the septa outer parts.S1 are embedded in it for one third to one half of theirwidth. Rarely, very short costae corresponding to the pri-mary septa are visible just below the calicular edge. Livingtissue covers the entire corallite or, most commonly, ismissing in the lower half part.

Group 3. Symmetrically or asymmetrically, slightlyswollen corallites (adult stage; Fig. 2e–h; corallite three inFig. 4a, d): several shapes, from (1) subcylindrical orslightly Xared (Fig. 2e) to (2) Xared in the proximal part,asymmetrically swollen and slightly curved in the mid-dis-tal part, and contracted in the uppermost part (Fig. 2g). Thetypical corallite length is around 14 mm and the GCD isaround 7 mm. Calice and fossa are slightly to heavily elliptical

Fig. 3 Coral morphological group/growth stage 4. a Overview of acolony fragment bearing corallites provided with soft tissues. b–cClose-up of a. b Corallite with retracted polyp; a characteristic featurefor growth stage 4 is that the greater diameter of the corallite is muchlarger than the calicular margin; note the gastropod Amphissa acute-costata (Philippi, 1844) adjacent to the coral tissue. c Lateral view ofb; note the sharp boundary between the fresh-looking uppermost partof the corallite (white zone) and the brownish and encrusted dead zone.d Lateral view of an irregularly humped corallite overcrusting a serpu-lid tube. e Irregular longitudinal proWle of a corallite showing excavat-ing sponge openings just below and on the white zone. f Calicular viewof a corallite overcrusting a serpulid tube; note the elliptical shape ofthe calice, the narrow and elongated fossa, the outer septal zones totallyembedded in the thick septotheca and the increasing theca thicknessjust below the calicular margin. g Calicular view of a corallite showinga “subangular” transversal proWle. The aberrant shape is probably dueto overcrusting of broken oVsprings. h Calicular view of a highly ellip-tical corallite bearing a broken oVspring (right side) and partly coveredwith soft tissues; note “5 septa” groups (1 S1, 1 S2, 1 S3, 2 S4)

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(Fig. 2h); the former has a maximum extension of 10 mm,the latter rarely exceeds 3 mm. Septa irregularly arrangedand exceptionally over 40 in number (normally less than35). S1 (7 to 9 in number) more exsert and slightly widerthan S2; S3 one half or two thirds narrower than S1. Septacontribute to the formation of the solid, ca. 1–1.5 mm thicktheca (traditional septotheca; see also Stolarski 1995).Along the calicular margin S1 are embedded in this struc-ture for ca. one half of their width. Very short costae, corre-sponding to the primary septa, are seldom present justbelow the calicular edge. Generally, the largest corallitediameter and corresponding largest theca thickness occurfew mm below the calicular margin (Figs. 2g, 4d). Thisgives the corallite a typically “contracted” shape. Noteworthy,in the distalmost part of the corallite, the theca thicknessand the corresponding number of aragonite layers abruptlydecrease downwards; in coral thin sections, local tapering(and interruption) of theca layers is clearly visible (Fig. 6d).The polyp edge zone extension is variable, less developedthan in the previous morphological groups and neverexceeding 40% of the corallite length.

Group 4. Strongly swollen corallites (adult stage; Fig. 3;corallites 1 and 2 in Fig. 4a–c, e; Fig. 5; Fig. 6a–c and e–h)with extremely irregular shapes: generally, subcylindricalor slightly Xared in the proximal part, strongly swollen inthe mid-distal part and contracted in the distalmost part(Fig. 3c–e); circular (Fig. 3b) to heavily elliptical (Fig. 3f,h) calicular edge; circular to “subangular” (Fig. 3g) trans-versal proWle in correspondence with the highest diameter.Typical corallite length is around 16 mm, rarely exceeding20 mm. Calicular edge and fossa slightly to strongly ellipti-cal (Figs. 3f and h), seldom circular (Fig. 3b). Typically,the greater calicular diameter (GCD) is around 10 mm(maximum extension 12 mm); very narrow fossa, rarelyexceeding 3.5 mm. Radial elements irregularly arranged orforming 8–9 regular groups of Wve septa (1 S1, 1 S2, 1 S3, 2S4; Fig. 3h), never exceeding 48 in number. S1 and S2 are ofcomparable width and exsertness; S3 and S4 are progres-sively smaller both in longitudinal and transversal exten-sion. Septa contribute to the formation of the solid, ca. 2-mm-thick theca (septotheca). Along the calicular margin,S1 are embedded in this structure for more than one half totwo thirds of their width. Further down, additional extrathecal deposits (tectura sensu Stolarski 1995) occur(Fig. 6a–c, e–g). In the most irregular forms, the greatercorallite diameter, corresponding to the highest theca thick-ness (over 4 mm), is located in correspondence with over-grown episkeletozoans. Examples of serpulid tubesovercrusted by coral skeleton are shown in Figs. 3f, 4e, 5d,e and 6g, h. The layered structure of the theca deposits ismarkedly disturbed at the outer end of some of the boringsponge cavities (Fig. 6b). Furthermore, the theca layerscurve, taper and interrupt at the boundary of active boring

sponge papillae, serpulid openings (Fig. 6e, g, respectively)or when in contact with other living organisms, such asbivalve anomiids (see section of anomiid trace Centrichnuseccentricus Bromley and Martinell 1991 in Fig. 6f). Thetheca outer surface bears coarse and packed granules thatincrease in size and density toward the proximal part of thecorallite. The living polyp is restricted to the distalmost partof the corallite, the white zone rarely exceeds 15% of thecorallite length.

Dead and black-coated Lophelia pertusa

All fragments show the typical skeletal features of the spe-cies Lophelia pertusa. The largest pieces, up to 30 cm inheight and 20 cm in width, are often fused with deadbranches of Madrepora oculata. The distal branch frag-ments are generally slender (ranging from 4 to 9 mm indiameter) and characterised by typical alternately arrangedcorallites. The more massive basal branches and those over-crusting parchment-like tubes of the symbiotic polychaeteEunice norvegica bear stout and recessed corallites, locallyimmersed in a relatively thick coenosteum. The calice ofthese corallites can reach 15 mm in diameter but theirheight rarely exceeds 10 mm. Generally, both slender andstout corallites show regular Xared morphologies. How-ever, some corallites of the distal branches are subcylindri-cal for two thirds of their length, irregularly Xared in theupper third part and abruptly “contracted” in the uppermostzone of the corallite. The moderately jagged calicular mar-gin is circular to slightly elliptical. Short primary costae arenormally visible just below the calicular edge. The fossa isvery deep although shortened in some corallites by thintabulae. The septa, rarely exceeding 48, are irregularly

Fig. 4 Three-dimensional visualisation of corallite surfaces and innercavities from a micro-computed tomography scan. Sample POS 316-525-2. a Overview of the sample; the numbers 1–5 identify the individ-ual corallites (collected alive) scanned by micro-CT; the red dashedlines on corallites 2 and 3 correspond to the thin sections shown inFig. 6d–f, respectively; the white arrow points at the anomiid traceCentrichnus eccentricus Bromley and Martinell 1991; scale bar 1 cm.b–e The corallites scanned contain all four boring growth stages of Akainfesta (Johnson, 1899); b virtual reconstruction showing corallites 2,4, 5. Corallite 2 (coral growth stage 3, 4) contains in its upper part ovalsponge chambers connected by intercameral canals (blue) that arefused towards the base of the corallite, forming a lobate chamber; Wrstsearch threads invade corallite 4 (coral growth stage 2, 3); no spongeinfestation in corallite 5 (coral growth stage 2); scale bar 2 mm. Whitearrows pointing at skeletal tabulae. c Oval sponge chambers located di-rectly below the polyp living zone and connected with each other byintercameral canals (blue); scale bar 2 mm. d Corallite 3 is character-ised by unilateral sponge infestation (blue) within the skeleton, repre-senting coral growth stage 3b. The isolated spherical chambers directlybelow the skeleton surface (see white arrow) are initial trace stages ofAka infesta (Johnson, 1899); scale bar 2 mm. e Corallite 1 (coralgrowth stage 4) containing excavating sponge growth stage D (blue)and overcrusting a serpulid tube (inner void in pink); scale bar 2 mm

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arranged; typically seven to nine primary septa (moreexsert and larger than the others) are recognisable. Thetheca thickness is variable along the longitudinal extensionof a single corallite as well as between diVerent corallites.Generally, it increases proportionally to the corallite sizeand within a single corallite it decreases toward the distalpart. Along the calicular edge of adult corallites (10–15 mmin diameter) the wall thickness is around 1 mm. The outertheca surface is characterised by rounded and uniform gran-ules (increasing in size and density toward the base) and,rarely, by shallow longitudinal striae. It is generally maskedby dark Fe–Mn oxide coatings and locally shows variousscratch traces of grazers.

Excavating sponges

Three sponge species have been identiWed by spicule analy-sis, namely Alectona millari Carter, 1879, Spiroxya het-eroclita Topsent, 1896 and Aka infesta (Johnson, 1899).The micro-CT analysis of the sample POS316-525-1reveals a prevailing infestation by Aka infesta (Fig. 5c–f).However, it is not possible to attribute individual cavities totheir producers because of interwoven sponge-cavity net-works within corallites (movie 2D1). In contrast, the spic-ule analysis of the sample POS316-525-2 indicates that theentire colony is exclusively infested by Aka infesta (Fig. 4;boring sponge cavities coloured in blue). Distinct tracemorphology and spatial distribution of Spiroxya heteroclitaand Alectona millari have not been observed within thesamples studied (see movies 2D2, 3D2_5 and rb2_5). Thus,exclusively for Aka infesta, a detailed description is givenin the following, based on the combined study of spiculeanalysis, micro-CT analysis and a microscopic examinationof POS316-525-2 as well as of its trace casts. Furthermore,its trace morphology has been illustrated (Fig. 7) and isclassiWed into four growth phases (a–d) according to Brom-ley and D’Alessandro (1984).

Aka infesta

The sponge tissue preserved in alcohol is yellowish. Mostof the apertures contain papillae, which have a pore sievetexture at their apex and are inhalant in contrast to thosethat are open apically and presumably are exhalant, if thepore sieve structure has not been damaged mechanically(see also van Soest et al. 2000). The spicules are curvedoxeas of 73–106£8–11 �m having a smooth surface(Fig. 7b). In the terminal 7.5–11 �m, the apices of the spic-ules are tapered oV in an angle of about 45°. The initial pen-etration of the substrate by the juvenile sponge producessmall spherical cavities (see arrow in Fig. 4d). The youngestzone of mature sponge borings is of bifurcating, “antler”-like exploratory canals (pioneer Wlaments) of variable

length and dominated by a linear growth. Adjacent to thelinear growth zone, the diameter of the boring is increasedby lateral growth, resulting in the Wrst local swellings at thebranching points, which appear to form chambers. Thesegrowth stages correspond to excavating sponge (Entobia)growth phases A and B after Bromley and D’Alessandro(1984). Growth phase C is represented by oval shapedchambers that measure about 5 mm across and are alwaysconnected by distinct intercameral canals of cylindricalshape and with average sizes of 1.8£0.6 mm. The individ-ual chambers are connected with the exterior via aperturalcanals (papillar canals) that are between 0.8–1.7 mm inlength and show circular cross-sectional areas. They can bedistinguished in two distinct size groups by their diameter.Diameters of the bigger apertural canals are between 0.2and 0.5 mm in contrast to the smaller sized, which arebetween 30 and 70 �m (movies 3D2_4 and rb2_4). Growthphase D is characterised by lobate chambers of 5 mm ormore across, which result from fusion of chambers (movies3D2_1 and rb2_1). Diameters of intercameral canals aswell as of apertural canals are circular and can be up to1 mm. In all phases, the apophyses are long and numerous,usually unbranched but, rarely, can also be bifurcated.

Relationships between Lophelia corallite growth stages and boring sponge spatial distribution

Combining observations on corallite outer morphology,corallite skeletal accretion pattern and boring spongegrowth phases, a clear relationship between coral shape andsponge infestation has been noted. Furthermore, the aber-rant growth forms of adult Lophelia corallites also seem tobe inXuenced by the overgrowth of encrusting organisms inthe vicinity of the calicular edge (movies 3D2_1 andrb2_1). Presence and spatial distribution of endo- and epi-skeletozoans for each corallite growth stage is brieXydescribed below and schematised in Fig. 9 and Table 1.

Fig. 5 Two- and three-dimensional visualisation of corallites from amicro-computed tomography scan. Sample POS316-525-1. a Over-view of the sample; the numbers 1, 2 identify the individual corallitesscanned by micro-CT; the red dashed line corresponds to the thin sec-tion shown in Fig. 6g, h; scale bar 1 cm. b Overview of the sample(back of a); numbers 1–3 correspond to the corallites scanned by mi-cro-CT; the red dashed lines on corallites 2 and 3 correspond to the thinsections shown in Fig. 6g, h and a–c, respectively; scale bar 1 cm. cThree-dimensional visualisation of corallite surfaces and inner cavi-ties; scale bar 0.5 cm. d Calicular view of corallite 2 showing a wormtube, whose skeleton is partly removed by excavating sponges (com-pare Fig. 6h); scale bar 0.5 cm. e–f Virtual longitudinal two-dimen-sional sections through the coral skeleton. The fragment scannedshows a very high porosity, due to the presence of large sponge cham-bers and encrusted worm tubes of Eunice norvegica (Linnaeus, 1767;ET); scale bars 0.5 cm

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Coral growth stage 1. Juvenile subcylindrical corallitesentirely covered with soft tissue, not infested by endo- andepiskeletozoans.

Coral growth stage 2. Distally Xared corallites areentirely or partially covered with soft tissues, potentiallyinfested by boring sponge search threads (sponge growthphases A, B, Fig. 8) and episkeletozoans in the tissue-bar-ren basal part. There is no evidence of relationship betweencorallite morphology and infesting organisms (movies3D2_4 and rb2_4).

Coral growth stage 3. Symmetrically or asymmetricallyslightly swollen corallites. Large sponge cavities (growthstage C, D, Fig. 8) in the tissue-barren parts of the coral skel-eton; sponge search threads (stage A, B, Fig. 8) and juvenilesponge cavities potentially present in the corallite white zone(Fig. 3e). Evidence of direct relationship between corallitemorphology and excavating sponge spatial distribution: (1)symmetrically-shaped corallites show homogeneously-dis-tributed sponge cavities within the skeleton (stage 3a inFig. 9); (2) asymmetrically humped corallites (Fig. 2g, h)show unilaterally-distributed sponge cavities within the skel-eton (Fig. 7a; stage 3b in Fig. 9; movies 3D2_2, rb2_2,3D2_3 and rb2_3). Episkeletozoans infest the wide tissue-barren skeleton, but are preferentially located in the proximalpart of the corallite. There is no evidence of direct relationbetween corallite morphology and epibionts.

Coral growth stage 4. Very “swollen” corallites highlyvariable in shape. Large sponge cavities (stage a–d) infest-ing the entire corallite skeleton with exception of theperipheral zone (Figs. 4b, c, e and 5). Sponge apertures andbiofouling exist in the white zone, even in the vicinity ofthe calicular margin. In several corallites, coral over-growths of carbonate serpulid tubes are close to the calicu-lar edge. There is evidence of a direct relationship betweencorallite morphology and endo-epibiontic infestation.

Discussion

Freiwald et al. (1997) and Kaszemeik and Freiwald (2002),focusing on samples and video observations from Norwayand the Porcupine Seabight (SW Ireland), described an“introvert or stereome-thickened ecotype” of Lophelia per-tusa. This ecotype is generally characterised by (1) anexceptionally thick wall, (2) introvert septa (sunken withinthe theca), (3) a high dissepiment density strongly reducingthe calice volume and (4) a contracted distalmost part(calicular edge diameter is less than the highest corallitediameter). Similar coenosteum-thickened Lophelia coral-lites are also known from the deep-water Pleistocenedeposits of southern Italy. They were originally describedby Seguenza (1864) as Lophohelia stoppaniana, but Recenttaxonomic studies led to designate this species as a syno-

nym of Lophelia pertusa (see Vertino 2003). The factorstriggering the development of Recent and fossil coenost-eum-thickened ecotype are not yet well known. Today, theintrovert ecotypes can dominate wide Lophelia coral reefframeworks (e.g. Propeller Mound, SW Ireland, and Stj-ernsund Ridge, northern Norway: see Freiwald et al. 1997,Kaszemeik and Freiwald 2002), but can also occur in smallreef “subhabitats” hosting several sessile invertebrates (e.g.sponges, ascidians and gorgonians) aggressively competingfor space and food (e.g. Sula Ridge Reef, Kaszemeik andFreiwald 2002).

The “swollen” Lophelia described herein shares with thetypical coenosteum-thickened ecotype the general corallitemorphology, the thick wall and the theca-embedded septa.In particular, there are strong similarities between thegrowth stage 3a illustrated in Fig. 9 and the above-men-tioned Recent and fossil introvert corallites. Nevertheless,the living swollen corallites from Galway Mound do notcharacterise healthy and well-developed colonies, butrather the distal part of sparse, dying colonies (Fig. 1c)abnormally infested by boring and encrusting organisms.

The corallites studied show a positive correlationbetween (1) upward polyp retraction, (2) abnormal lateralexpansion of upper corallite skeleton and (3) upwardspreading of boring sponge cavities, which lead to the inter-pretation of their swollen shape as resulting from GalwayMound as resulting from a coral defensive mechanismagainst infesting bioeroding organisms. The episodicallyand irregular downward and outward expansions of the

Fig. 6 a–c Transverse thin-section of corallite 3 (coral growth stage4); sample POS316-525-1 (see Fig. 5a, b). a Overview of boringsponge cavities infesting a large part of the corallite skeleton. b Detailof a; note curved growth lines at the outer end of a boring sponge cavity(white arrow), probably corresponding to the opening of an explor-atory thread (see Fig. 8); yellow arrow indicates an old outer surface ofthe corallite infested by boring fungi, most probably Dodgella priscusZebrowski 1936 (dark spots). c Detail of a; note the transversal sectionof an externally prominent primary septum (ps), subsequently coveredby thick tectura deposits. The yellow arrow points at the same old outersurface shown in b. d Longitudinal-oblique section of corallite 3 (sam-ple POS316-525-2; compare with Fig. 4a, d); note the large spongecavity in the lower axial part of the corallite and the trace of an explor-atory thread (yellow arrow) in the distal part, close to the calicularedge. The white arrows point to tapering and interrupting extra thecallayers. e–f Transversal sections of the corallite 2 shown in Fig. 4a–c;sample POS316-525-2. e Distal transversal section (upper red dashedline on corallite 2, Fig. 4a) showing tapering thecal layers at the open-ing of a boring sponge (arrow). f Proximal transversal section (lowerred dashed line on corallite 2, Fig. 4a) showing overlapping, taperingand interruption of extra thecal (tectura) layers (arrow) in correspon-dence to a living (?) epizoic organism (anomiid); compare with whitearrow in Fig. 4a. g–h Transversal section of the distal part of the cor-allite 2 (coral growth stage 4) shown in Fig. 5a, b; sample POS316-525-1. g Longitudinal section of a dark serpulid tube encrusting thecoral surface and overcrusted by subsequent coral aragonite layers. hDetail of g cavity of a boring sponge (sc) infesting both coral and ser-pulid tube (st)

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Table 1 List of features characterising the swollen Lophelia pertusa (Linnaeus, 1758) growth stages described in the text

The corallite skeletal features are expressed in mm (see schematic drawing on the left; from the top: calicular and lateral view of an ideal corallite).The values exposed in this table represent the average ones measured in 117 corallites (87 alive, 30 dead). The sponge infestation growth stagesare named with letters (A–D) according to Bromley and D’Alessandro (1984), see also Fig. 8

Fig. 7 Aka infesta (Johnson, 1899). a Resin cast of the corallite pic-tured in Fig. 2g (growth form 3b in Fig. 9), exposing unilateral spongeinfestation within the corallite. b SEM image of resin cast showing the

fracture zone of an intercameral canal, which contains numerouscurved oxeas of Aka infesta

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retracted polyp tissues, as proven by discontinuous extrathecal layers deposited on the upper part of the corallites(Fig. 6), could be explained as attempts of the coral polypsto strengthen the excavated and weakened skeleton.

The results exposed herein imply that secretion of extrathecal deposits in the upper part of the corallites can befostered or simply inXuenced by interacting living endo-skeletozoans: (1) boring sponge accretion within the cor-allite seems to induce the polyp to secrete additionalaragonite to strengthen the excavated skeleton; however,it seems also clear that, since the growth stage 3, the polyptries to “escape” from the boring sponge aggression byretracting upwards (Fig. 9) and, sometimes, even chang-ing growth direction (Fig. 7a; stage 3b in Fig. 9; movies3D2_2, rb2_2, 3D2_3 and rb2_3); (2) coral growth lines,which are immediately adjacent to the outer margin ofsome sponge cavities, tend to fold, forming microscopic“chimney-like” projections (Fig. 6b); (3) tectura layerstaper and close in the vicinity (or contact) of boringsponge openings (Fig. 6e). The sponge growth seems tobe undisturbed by the calciWcation defence mechanism ofthe coral. Via specialised archaeocytes (etching cells),bioeroding sponges can locally invade the substrate byremoving skeleton portions (sponge chips) of their host(e.g. Rützler and Rieger 1973; Pomponi 1979). Thus,extra calciWcation by the polyp is not a real barrier forexcavating sponges, unless their growth rate is muchlower than the coral one (see Fig. 10a). The potential ofcalciWcation as a protection mechanism against bioerod-

ing organisms is already known for bivalves. For instance,Acesta excavata (Fabricius, 1779) forms characteristicprotuberances on the inner side of the shell as a reactionto the infesting parasitic foraminifer Hyrrokkin sarcoph-aga Cedhagen, 1994 (Cedhagen 1994; Freiwald andSchönfeld 1996; López Correa et al. 2005).

The hypothesis that the swollen Lophelia from Gal-way Mound interacts with bioeroding organisms and thatsuch interaction can heavily control the abnormal coralskeleton accretion is supported by the Wnding of swollencorallites of the NW Atlantic species Madrepora caro-lina (Pourtalès, 1871), which is highly infested by boringsponges (Fig. 11). Like Lophelia pertusa, the typical dis-tal branches of Madrepora carolina show sympodialarrangement of slightly Xared corallites (Fig. 11a, b).Like Lophelia from Galway Mound, the irregular-shapedcorallites of Madrepora carolina are highly infested withboring sponges (Fig. 11c–e). On the contrary, the skele-ton of the “normal” corallites, located in the upper part ofthe branch, show a perfectly preserved skeleton, withoutany trace of boring organisms. Although belonging todiVerent taxa, Lophelia pertusa and Madrepora carolinaoccupy the same ecological niche; they are both cold-water reef-building species. As a consequence, it is likelythat they show similar reactions to similar disturbingfactors.

The high number of serpulid tubes partly or entirelyovercrusted by aragonite coral layers in the vicinity ofthe calicular edge of the examined corallites supports thehypothesis that the discontinuous expansions of the Lop-helia polyps from Galway Mound and the consequentirregular tectura secretion represent defensive mecha-nisms of the coral against upward spreading episkeleto-zoans (Fig. 10b; movies 3D2_1 and rb2_1). Theinteractions between Lophelia polyps and associated epi-skeletozoans are also proven by tapering and interrup-tions of coral extra thecal layers in the vicinity of livingepiskeletozoans (e.g. anomiids; Fig. 6f). Freiwald andWilson (1998) have already described this phenomenonfor Norwegian coenosteum-thickened Lophelia coloniesovercrusting episkeletozoans located just below thepolyp edge zone. The calciWcation process of Lopheliapertusa seems to be more eVective as a defence mecha-nism against encrusting serpulids than against boringsponges. This is probably due to the incapability of ser-pulids to etch carbonate substrates. The high number ofepiskeletozoans, however, is seen to be an indicator foran already weakened polyp.

It is worth noting that almost all the dead Lopheliabranches showed “normal” morphologies (Fig. 1d, e) andthat the swollen corallites were restricted to the distal part ofthe colonies (Fig. 1e). If it is true that the abnormal shape ofthe living corallites is controlled by the development and spa-

Fig. 8 Trace morphology of Aka infesta (Johnson, 1899) within theskeleton of Lophelia pertusa (Linnaeus, 1758). The classiWcation ofgrowth stages (A–D) and morphological terminology refers to Bromleyand D’Alessandro (1984)

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tial distribution of coral-associated endo- and epizoans, it isplausible to presume that the infestation rate of Lopheliaincreased through time, even within the life span of a singlecolony. However, it is also plausible to think that, at constantinfestation rate, the defensive potential of Lophelia againstendo- and epibiontic infestation decreased through time.

Understanding the interactions between Lophelia per-tusa and its associated organisms is important for both eco-logical and palaeoecological studies of deep-waterenvironments. In fact, abnormal morphologies of fossilcoral skeletons can provide information on non-fossilisableassociated organisms.

The data discussed herein result from an innovativecombined methodology. The non-invasive micro-CT analy-sis of the Lophelia branches proved to be extremely impor-

tant in understanding the macroscopic accretion of the coralskeleton and fundamental in visualising the spatial distribu-tion of the boring sponge cavities within the biogenicsubstrate. Further combined application of micro-CT analy-ses with traditional destructive methodologies such asskeleton thin sections and casts, will provide bettercalibration of the micro-CT potential in taxonomic and eco-logical studies of Recent and fossil corals and associatedorganisms.

Conclusions

– The living corallites of the “swollen” Lophelia pertusafrom Galway Mound can be divided into four main

Fig. 9 Schematic drawing of growth stage succession of “swollen” Lophelia pertusa (Linnaeus, 1758). From the top: calicular view, lateral viewand longitudinal section of representative corallites for each morphological group/growth stages described in the text

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morphological groups, corresponding to four maingrowth stages: (1) cylindrical (juvenile); (2) Xared (juve-nile to adult); (3) slightly swollen (adult); (4) stronglyswollen (adult).

– The corallites of the adult stages host three excavatingsponge species: Alectona millari, Spiroxya heteroclitaand Aka infesta. The latter is characterised by three maingrowth phases: juvenile (A, B), intermediate (C) andadult (D).

– There is a positive correlation between the four“swollen” Lophelia growth stages and the boringsponge growth phases: (1) cylindrical juvenile coral-lite/no sponge cavities; (2) Xared juvenile corallite/linear sponge cavities (if present); (3) slightly swollenadult corallites/chambered oval-shaped sponge cavi-ties; (4) strongly swollen adult corallites/widespreadcavities.

– In particular, there is a positive correlation betweencorallite theca thickness and boring infestation. Thisleads to the interpretation of the abnormal secretion ofcorallite extra thecal deposits as a defensive mecha-nism of Lophelia pertusa against infesting bioerodingorganisms.

– The overcrusted serpulid tubes in the vicinity of the cor-allite calicular edges imply that the upward episkeleto-zoan spreading can be considered as an additionaldisturbing factor triggering the abnormal skeleton secre-tion of the coral.

– The non-invasive micro-CT analysis and especially theinnovative application of the stereoscopic technique onachieved micro-CT movies will likely be very importantfor (1) the study of colonial coral skeletal accretion andfundamental for (2) the visualisation of boring cavityspatial distribution within a carbonate biogenic substrate.

Fig. 10 Three-dimensional visualisations of corallite surfaces and in-ner cavities from a micro-CT scan focusing on spatial distribution ofepi- and endoliths. Sample POS 316-525-2. Shown are virtual seg-ments of the reconstructed specimen. a Aka infesta (Johnson, 1899;blue) infesting its host from basal dead skeleton and growing into thelive zone of Lophelia pertusa (Linnaeus, 1758). CalciWcation as poten-tial defence mechanism against sponge infestation is ineVective; scalebar 0.5 cm. b Sporadic basal expansion of the polyp’s soft tissue al-

lowed to overcrust epizoic organisms entirely. An encrusting serpulidtube (lumen in pink) grew towards the distal part of the corallite, assuggested by the increasing diameter of its tube towards the coral ca-lice. Afterwards, it was overcrusted by the coral tissue and obliquelytruncated by a boring sponge. The black dashed line indicates the inter-section between the distal end of the serpulid lumen and the spongecavity; scale bar 0.5 cm. c Detail of b

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Fig. 11 a–e Madrepora carolina (Pourtalès 1871) fragments col-lected alive from the Strait of Florida (24°29�N–80°53�W, 191 m wa-ter depth); sample 8-232 identiWed by Stephen Cairns and kept at theMuseum of the Rosenstiel School (Miami University). a Lateral viewof distal branches showing a sympodial arrangement of the corallite,typical of the species (see Cairns 1979). b Detail of a, “normal” coral-lites, Xared at their distal ends. c Colony fragment bearing atypical“swollen” corallites in the proximal part; note the dense and large cav-

ities of excavating sponges in a broken branch (white arrow). d Detailof c; back side of three swollen corallites shown in c; note the numer-ous holes on the coral surface (some very close to the calicular edge)corresponding to boring sponge oscula (white arrows). e Detail of c;calicular view of atypically swollen corallites; note that the greater cor-allite diameter is much larger than the calicular edge diameter as ob-served in the swollen Lophelia pertusa (Linnaeus, 1758) from theGalway Mound

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Acknowledgements We are indebted to André Freiwald (Erlangen,Germany), Jarek Stolarski (Warsaw, Poland), Antonietta Rosso (Cata-nia, Italy) and Rossana SanWlippo (Catania, Italy) for valuable discus-sions. We thank Richard G. Bromley (Copenhagen, Denmark), HelmutZibrowius (Marseille, France) and an unknown reviewer for their con-structive comments on this paper. Furthermore, we are beholden toBirgit Leipner-Mata for the preparation of thin sections, to ChristianSchulbert (Erlangen, Germany) for conWguring the colour balance inour Wgures, to the Marum Company (Bremen, Germany), especiallyVolker Ratmeyer, for providing us with ROV-Quest images from thestudy area (Meteor cruise 61/3) and Tim Beck for microscopic imagesof the living polyps and for the gastropod identiWcation. We expressour gratitude to the captain and crew of RV Poseidon and to the Ro-senstiel Museum (Miami, Florida). The study was funded by the HER-MES Project GOCE-CT-2005-511234 (Hotspot Ecosystem Researchon the Margins of European Seas) and the EURODOM Project HPRN-CT-2002-00212 (European Deep Ocean Margins: a new training-through-research frontier).

References

Beuck L (2002) Biodegradation und Ichnodiversität postmortaler Sta-dien der Tiefwasserkoralle Lophelia pertusa am Propeller Mound(Porcupine Seabight). MSc Thesis, Eberhard-Karls-Universität,Tübingen, Germany, 77 pp

Beuck L (2005) Sediment sampling and processing. In: Pfannkuche O,Utecht C (eds) Cruise report Poseidon 316: carbonate mounds andaphotic corals in the NE-Atlantic. Reykjavik-Lissabon 03.08-17.08. 2004. IFM-GEOMAR Report 3:17–59

Beuck L, Freiwald A (2005) Bioerosion patterns in a deep-water Lop-helia pertusa (Scleractinia) thicket (Propeller Mound, northernPorcupine Seabight). In: Freiwald A, Roberts JM (eds) Cold-wa-ter corals and ecosystems. Springer, Heidelberg, pp 915–936

Bromley RG, Martinell J (1991) Centrichnus, new ichnogenus for cen-trally patterned attachment scars on skeletal substrates. Bull GeolSoc Den 38:243–252

Bromley RG, D’Alessandro A (1984) The ichnogenus Entobia fromthe Miocene, Pliocene and Pleistocene of southern Italy. Riv ItalPaleont Stratigr 90:227–296

Cairns SD (1979) The deep-water Scleractinia of the Caribbean Seaand adjacent waters. Stud Fauna Curaçao Caribb Isl 57:1–341

Cedhagen T (1994) Taxonomy and biology of Hyrrokkin sarcophaga gen.et sp. n.: a parasitic foraminiferan (Rosalinidae). Sarsia 79:65–82

De Mol B, van Rensbergen P, Pillen S, Van Herreweghe K, Van RooijD, McDonnell A, Huvenne V, Ivanov M, Swennen R, Henriet JP(2002) Large deep-water coral banks in the Porcupine Basin,southwest of Ireland. Mar Geol 188:193–231

De Mol B, Henriet J-P, Canals M (2005) Development of coral banksin Porcupine Seabight: Do they have Mediterranean ancestors?In: Freiwald A, Roberts JM (eds) Cold-water corals and ecosys-tems. Springer, Heidelberg, pp 515–533

Duncan PM (1877) On the rapidity of growth and variability of someMadreporaria on an Atlantic cable, with remarks upon the rate ofaccumulation of foraminiferal deposits. Ann Mag Nat Hist20:361–365

Freiwald A, Schönfeld J (1996) Substrate pitting and boring patternof Hyrrokkin sarcophaga Cedhagen, 1994 (Foraminifera) in amodern deep-water coral reef mound. Mar Micropaleont28:199–207

Freiwald A, Henrich R, Pätzold J (1997) Anatomy of a deepwater coralreef mound from Stjernsund, West-Finnmark, northern Norway.SEPM Spec Publ 56:41–161

Freiwald A, Wilson JB (1998) Taphonomy of modern deep, cold-tem-perate water coral reefs. Hist Biol 13:37–52

Gravier C (1920) Madreporaires provenant des campagnes des yachtsPrincesse-Alice et Hirondelle II (1893-913). Resultats des cam-pagnes scientiWques accomplies sur son yacht par Albert Ier PrinceSouverain de Monaco 55:1–123

Harmelin JG (1990) Deep-water crisiids (Bryozoa: Cyclostomata)from the northeast Atlantic Ocean. J Nat Hist 24:1597–1616

Hubbard JAEB, Pocock YP (1984) Scleractinian functional morphol-ogy: a key to paleoecological reconstruction. Palaeont Am54:523–530

Huthnance J, Coelho H, GriYth CR, Knight PJ, Rees AP, Sinha B,Vangriesheim A, White M, Chatwin PG (2001) Physical struc-tures, advection and mixing in the region of Goban Spur. Deep-Sea Res Part II 48:2979–3021

Kalender WA (2005) Computed tomography. Fundamentals, systemtechnology, image quality, applications. Publicis, Erlangen, Ger-many, 306 pp

Kaszemeik K, Freiwald A (2002) Lophelia pertusa (Scleractinia)—from skeletal structures to growth patterns and morphotypes. In:A Freiwald (ed) ACES Atlantic coral ecosystem study. FifthManagement Report. Institute for Geosciences, Tübingen Univer-sity, Germany, pp 1–26

López Correa M, Freiwald A, Hall-Spencer J, Taviani M (2005) Dis-tribution and habitats of Acesta excavata (Bivalvia: Limidae),with new data on its shell ultrastructure. In: Freiwald A, RobertsJM (eds) Cold-water corals and ecosystems. Springer, Heidel-berg, pp 173–205

Masson DG, Miles PR (1986) Structure and development of PorcupineSeabight sedimentary basin, oVshore southwest Ireland. AAPGBull 70:536–548

Mietchen D, Keupp H, Manz B, Volke F (2005) Non-invasive diagnos-tics in pathological fossils by magnetic resonance imaging. Bio-geosci Discuss 2:239–260

Nickel M, Donath T, Schweikert M (2006a) Functional morphology ofTethya species (Porifera): 1. Quantitative 3D-analysis of Tethyawilhelma by synchrotron radiation based X-ray microtomogra-phy. Zoomorphology. doi:10.1007/s00435-006-0021-1

Nickel M, Bullinger E, Beckmann F (2006b) Functional morphologyof Tethya species (Porifera): 2. Three-dimensional morphomet-rics on spicules and skeleton superstructures of T. minuta. Zoo-morphology. doi:10.1007/s00435-006-0022-0

Pfannkuche O, Utecht C (2005) Cruise report Poseidon 316: carbonatemounds and aphotic corals in the NE-Atlantic. Reykjavik-Lissa-bon 03.08-17.08, 2004. IFM-GEOMAR Rep 3:1–61

Pomponi SA (1979) Ultrastructure of cells associated with excavationof calcium carbonate substrates by boring sponges. J Mar Biol As-soc UK 59:777–784

Roberts JM (2005) Reef-aggregating behaviour by eunicid polychaetesymbionts of cold-water corals: Do worms assemble reefs? J MarBiol Assoc UK 85:813–819

Rossi M, Casali F, Romani D, Bondioli L, Macchiarelli R, Rook L(2004) MicroCT scan in paleobiology: application to the study ofdental tissues. Nucl Instrum Methods 213:747–750

Rützler K, Rieger G (1973) Sponge burrowing: Wne structure of Clionalampa penetrating calcareous substrata. Mar Biol 21:144–162

Schönberg CHL (2001) Estimating the extent of endolithic tissue of aGreat Barrier Reef clionid sponge. Senckenb Marit 31:29–39

Seguenza G (1864) Disquisizioni paleontologiche intorno ai Corallariifossili delle rocce terziarie del distretto di Messina. Mem Real Ac-cad Sci Torino (ser 2) 21:399–560

Siegel LJ (2003) Preemies from the Precambrian. Astrobiology Maga-zine. http://www.astrobio.net. Cited 14 February 2007

Stolarski J (1995) Ontogenetic development of the thecal structuresin caryophylliine scleractinian corals. Acta Palaeontol Pol40:19–44

Stolarski J (1996) Gardineria: a scleractinian living fossil. Acta Pala-eont Pol 41:339–367

123

176 Facies (2007) 53:157–176

Strømgren T (1971) Vertical and horizontal distribution of Lopheliapertusa (Linné) in Trondheimsfjorden on the west coast of Nor-way. Det Kongelige Norske Videnskabers Selskabs Skrifter 6:1–9

Taylor PD, Wilson MA (2002) A new terminology for marine organ-isms inhabiting hard substrates. Palaios 17:522–525

Van Rooij D, De Mol B, Huvenne V, Ivanov M, Henriet JP (2003)Seismic evidence of current-controlled sedimentation in the Belg-ica Mound Province, upper Porcupine slope, southwest of Ireland.Mar Geol 195:31–53

Van Soest RWM, Picton B, Morrow C (2000) Sponges of the NorthEast Atlantic. Biodiversity Center of ETI, Multimedia InteractiveSoftware. UNESCO, Paris

Veron JEN (2000) Corals of the world, vols 1–3. In: StaVord-Smith M(ed), Australian Institute of Marine Science, Townsville, Austra-lia, 463 pp

Vertino A (2003) Sclerattiniari Plio-Pleistocenici ed attuali del Medi-terraneo (Sistematica, Biostratinomia e Paleoecologia). PhD The-sis, University of Messina, 306 pp

Wells JW (1957) Coral Reefs. In: Hedgepeth JW(ed), Treatise on Ma-rine Ecology and Paleoecology. Mem Geol Soc Am 67:609–631

Zibrowius H (1980) Les Scléractiniaires de la Méditerranée et de l’Atl-antique nord-oriental. Mém Instit Océanogr Monaco 11:284

Zibrowius H (1984) Taxonomy in ahermatypic scleractinian corals.Paleont Am 54:80–85

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