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Title: Piegeage,´ preservation´ et debut´ de fossilisation de mollusques predateurs´ benthiques au sein d’un systeme` corallien d’eau profonde en mer mediterran´ ee´

Authors: Lorenzo Angeletti, Marco Taviani

PII: S0016-6995(11)00076-3 DOI: doi:10.1016/j.geobios.2011.02.004 Reference: GEOBIO 544

To appear in: Geobios

Received date: 1-9-2010 Revised date: 3-2-2011 Accepted date: 4-2-2011

Please cite this article as: Angeletti, L., Taviani, M., Piegeage,´ preservation´ et debut´ de fossilisation de mollusques predateurs´ benthiques au sein d’un systeme` corallien d’eau profonde en mer mediterran´ ee,´ Geobios (2010), doi:10.1016/j.geobios.2011.02.004

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Entrapment, preservation and incipient fossilization of benthic predatory molluscs within deep-water frames in the Mediterranean Sea 

Piégeage, préservation et début de fossilisation de mollusques prédateurs benthiques au sein d’un système corallien d’eau profonde en mer méditerranée

Lorenzo Angeletti *, Marco Taviani

ISMAR-CNR, UOS Bologna, Via Gobetti 101, Bologna, Italy

Received 1 September 2010; accepted 4 February 2011

 Corresponding editor: Davide Olivero E-mail address: [email protected] (L. Angeletti)

Abstract

Holocene Madrepora-Lophelia subfossil frames recovered at ca. 690 m from deep-water coral grounds south of Malta (Strait of Sicily, Central Mediterranean Sea) were found to entrap shells of cnidarian predatory gastropods such as sentix, “” squamosa (morphotype ruderatus) and architectonicids. This finding documents the capability of deep water coral reefs to serve as taphonomic traps eventually promoting the preservation of rare components of their original biota.

Keywords: Deep-water ; Taphonomy; Gastropods; -; Architectonicidae; Mediterranean Sea

Résumé

Nous montrons que des systèmes coralliens d‟eau profonde subfossiles (holocènes) à Madrepora-Lophelia découverts à environ 690 m de profondeur au sud de Malte (Détroit de Sicile, Mer Méditerranée centrale) ont capturé des coquilles de gastéropodes prédateurs de cnidaires, tels que Babelomurex sentix, “Coralliophila” squamosa (morphotype ruderatus) et des architectonicidés. Cette observation illustre la capacité des récifs coralliens d‟eau profonde à servir de piège taphonomique, favorisant éventuellement la préservation d‟éléments rares de leurs biotopes d‟origines.

Mots clés : Coraux d‟eau profonde ; Taphonomie ; Gastéropodes ; Muricidae-Coralliophilinae ; Architectonicidae ; Mer méditerranée

1. Introduction

Cold- (or deep-) water coral reefs (CWCs) are marine habitats characterized by high levels of biodiversity (Freiwald, 2002; Freiwald et al., 2004; Roberts et al., 2006; Hovland, 2008). They can contribute to making spectacular carbonate mounds, such as those along the NE European margin (e.g., Wheeler et al., 2007). CWCs occur almost world-wide, including the semi-enclosed Mediterranean basin which boasts a superb, albeit discontinuous, paleontological documentation from the Miocene onwards (Taviani et al., 2005, and references therein). In this basin most of the extant CWC-bearing assemblages are of the Pleistocene and either crop out in southern Italy and Rhodes (Di Geronimo et al., 2005; Titschack and Freiwald, 2005) or are still submerged (Taviani et al., 2005). Both living andAccepted dead coral structures can provide niches Manuscript to a variety of benthic organisms (Freiwald et al., 1997, 2004; Freiwald and Wilson, 1998). Biohermal frame growth and related biostromal production may optimise entrapment, and ultimately the preservation of vagile visitors or stable exploiter visitors of such coral habitats. The recurrent process of early submarine cementation is conducive to the lithification of the intracoral fine-grained matrix resulting in carbonate rocks (framestones) which encase both coral frames and skeletal remains of associated macrofauna, mainly molluscs, followed by brachiopods, echinoids and decapods. Collections of pre-Modern coral frames and coral hardgrounds obtained from various Mediterranean submerged locations show that this taphonomic process is common. Although the main coral entrappers are basically the same basin-wide (i.e., the colonial scleractinians Lophelia pertusa (Linnaeus, 1758) and Madrepora oculata Linnaeus, 1758, and more rarely the solitary Desmophyllum dianthus (Esper, 1794)), the entrapped organisms may differ from site to site (e.g., Remia and Taviani, 2005; Taviani et al., 2005, 2010). Benthic gastropod shells belonging to Emarginula, Putzeysia, Alvania and Amphissa as well as holoplanktonic

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Page 1 of 9 thecosomatous pteropods and heteropods are almost ubiquitous. Last glacial Desmophyllum-bearing micritic hardgrounds dredged at depths > 2000 m from the Malta-Siracusa escarpment encase articulated Delectopecten vitreus (Gmelin, 1791) shells, a bathyal pectinid, inside the coral calices (Taviani and Colantoni, 1979). Buried latest Pleistocene Madrepora mounds at ca. 350-400 m in the NE Tyrrhenian sea have been documented by Remia and Taviani (2005) to enclose in their weakly-cemented frames articulate brachiopods (Gryphus, Megerlia) and vagile gastropods (Emarginula, Coralliophila). By and large, most of the „fossilized‟ shells are not uniquely related to deep-water corals. Cnidarian predatory-gastropods (such as Muricidae-Coralliophilinae, Ovulidae, Epitoniidae, Architectonicidae; Robertson, 1967, 1970; Sabelli and Taviani, 1984; Bieler, 1993; Oliverio et al., 1997; Gittenberger, 2006; Kokshoorn et al., 2007; Reijnen et al., 2010) occur much more rarely in fossil taphonomic coral traps. A spectacular case in point is discussed here, related to Madrepora-Lophelia subfossil frames from deep- water coral grounds south of Malta (Strait of Sicily) entrapping shells of the extremely rare cnidarian-predatory gastropods. The area is the CWC province recently described by Schembri et al. (2007) and Freiwald et al. (2009). Location and main topographic characteristics of the study area are presented in Fig. 1.

2. Material and methods

The study material is sourced from CNR cruise MEDCOR with RV Urania (December 2009), more precisely from MEDCOR Station 25 (35° 30.796′ Lat N-14° 11.076′ Long E, Depth -690 m). Swath bathymetry data were acquired using a RESON 8160 multibeam echo-sounder with nominal sonar frequency of 30 kHz and angular coverage sector of 135 beams per ping at 1°. Sub-bottom Chirpsonar profiles were obtained using a hull- mounted 16-transducer source with a sweep modulated 2-7 kHz outgoing signal equivalent to a 3.5 kHz profiler. Sampling was achieved using various equipment (corers, grabs, epibenthic hauls), depending upon the nature of the sea bottom. Samples were washed on-board in freshwater, dried and examined with the aid of magnifying lenses and optical microscopes. One Babelomurex sentix (Bayer, 1971) shell and one Lophelia pertusa coral were 14C-AMS dated at the Poznan Radiometric Laboratory, Poland. Radiocarbon results (Table 1) are reported as raw 14C-ages given in 14C-yrs BP, and as calendar year estimates (cal. years BP) after calibration; BP refers to 1950 AD.

3. Deep water coral taphonomic traps

The south Malta CWC province is a site where live scleractinians (Lophelia, Madrepora, Desmophyllum, Dendrophyllia, Javania, Caryophyllia) and other sessile invertebrates such as octocorals (including Corallium), antipatharians (Leiopathes), barnacles (Pachylasma) and hexactinellid sponges contribute to make an important and diverse hotspot settling a deep-water escarpment (Freiwald et al., 2009; Taviani et al., 2010). Although lush live coral communities are well documented here, dead subfossil corals and coral hardgrounds are equally common. During cruise MEDCOR we sampled various examples of framestones and wackestones mostly consisting of the colonial scleractinians Madrepora oculata and, subordinately, Lophelia pertusa, showing various degrees of patination by Fe-Mn oxides, bioerosion and cementation. MEDCOR Station 25 was particularly prolific in providing samples of such carbonates. The screening of framestones and hardgrounds produced various examples of benthic organisms entombed in these degraded coral frames often affected by early diagenetic processes. Although some of the coral frames are only weakly cemented and retain no intracoral matrix, others show more advanced lithification also at the expense of the muddy matrix (Fig. 2(A)). This process likely started during the latter hundreds or thousands of years in the Holocene and is still continuing. These potential fossils can be conveniently categorized as occasional visitors or more rarely ecologically-consistent associates, i.e., basically „freezing‟ in situ part of the original ecosystem. The first group includes taxa such as the gastropod Amphissa acutecostata (Philippi, 1844) and decapod calcified remains (Fig. 2(B)). The second group includes examples of vagile organisms inhabiting the coral reef itself. In the specific case-studyAccepted treated here we document the inclusion Manuscript in coral frames and hardgrounds of some rare predatory gastropods (Fig. 3(A‒ J)). Coral frames can often trap pelagic tests (Fig. 3(K)). Blackened shells of the elusive Muricidae-Coralliophilinae neogastropods Babelomurex sentix and “Coralliophila” squamosa (the deep-sea morphotype ruderatus Sturany, 1896, of the common subtidal- circalittoral nominal taxon “Coralliophila” squamosa (Bivona Ant. in Bivona And., 1838): see Taviani et al. 2009) were observed cemented inside Madrepora-dominated framestones and subordinated Lophelia (Fig. 3(C, F‒ J)). Both taxa, unknown as fossils, are seldom recorded in the literature (e.g., Oliverio, 1989; Giannuzzi- Savelli et al., 2003; Oliverio and Gofas, 2006) and have been recently recorded alive from these same CWC grounds by Taviani et al. (2009). It is likely that they feed upon some cnidarians associated with the CWC reefs but the precise host(s) is unknown at present. One shell of B. sentix from MEDCOR 25 provided a 14C-AMS age of 732 ± 73 years BP while one Lophelia branch from the same station held an age of 628 ± 68 years BP (Table 1). Therefore, the present finding documents that these rare gastropods consistently inhabit the South

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Page 2 of 9 Malta CWC province at least since the latest Holocene, co-occurring with another member of the subfamily Coralliophilinae, „Coralliophila‟ richardi (P. Fisher, 1882) (predatory on Madrepora and Lophelia: Taviani et al. 2009) of which some dead shells were also found at MEDCOR 25 but not entrapped in coral framestones or hardgrounds. Some of the shells served as a substrate for coral settlement. Besides Coralliophilinae, other predators of cnidarians have been detected in our samples. Shells belonging to at least two different species in the family Architectonicidae (, ) were detected welded to lithified matrix in coral framestones and hardgrounds (Fig. 3(A, B, D‒ E)). One such shell is poorly preserved and its base is embedded in the lithified matrix not allowing one to ascertain with confidence its , but possibly referable to Discotectonica discus (Philippi, 1844). As for some of the Coralliophilinae discussed above, the shell was also functional to later coral settlement. Two shells belonging to Heliacus alleryi (Seguenza, 1876) were also detected in the coral hardgrounds (Figs. 2(C) and 3(D‒ E)). Loose shells of these uncommon Mediterranean Architectonicidae (Melone and Taviani, 1984) were relatively common in MEDCOR 25, but their precise cnidarian preys are unknown at present.

4. Conclusion

Deep water coral reefs may serve as efficient taphonomic traps which may help the post-mortem preservation of skeletonized organisms, potentially ensuring their fossilization. A remarkable example of such is offered by the finding of pre-modern Lophelia-Madrepora coral frames and hardgrounds at the recently discovered South Malta CWC province. These carbonates were found entrapping shells of exceedingly rare deep-water Coralliophilinae (Babelomurex sentix, “Coralliophila” squamosa - morphotype ruderatus) and Architectonicidae (cf. Discotectonica discus, Heliacus alleryi). This record is a rare case documenting the incipient fossilization of ecologically consistent CWC predator-host assemblages.

Acknowledgements

We are grateful to Captain, Crew and Colleagues onboard RV Urania during MEDCOR mission. We thank A. Beu and an anonymous referee for their constructive criticism. English kindly revised by Derek Jones. Funding was partially provided by CNR and HERMIONE project (contract n° 226354) within the 7th Framework Program of the EU. This is ISMAR-Bologna scientific contribution n° 1679.

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Page 3 of 9 McCormac, G., Manning, S., Ramsey, C.B., Reimer, P.J., Reimer, R.W., Remmele, S., Southon, J.R., Stuiver, M., Talamo, S., Taylor, F.W., van der Plifcht, J., Weyhenmeyer, C.E., 2004. Marine04 marine radiocarbon age calibration, 0–26 cal kyr BP. Radiocarbon 46, 1059–1086. Kokshoorn, B., Goud, J., Gittenberger, E., Gittenberger, A., 2007. Epitoniid parasites (Gastropoda, , Epitoniidae) and their host sea anemones (Cnidaria, Actinaria, Ceriantharia) in the Spermonde archipelago, Sulawesi, Indonesia. Basteria 71, 33–56. Melone, G., Taviani, M., 1984. Revisione delle Architectonicidae del Mediterraneo. In: Sabelli, B (Ed.), Sistematica dei Prosobranchi del Mediterraneo. Lavori della Societa Italiana di Malacologia, Milano, pp.149– 192. Oliverio, M., 1989. Famiglia Coralliophilidae Chenu, 1869 in Mediterraneo. La Conchiglia 246/249, 48–55. Oliverio, M., Taviani, M., Chemello, R., 1997. A coral-associated epitoniid, new to the red sea (Prosobranchia, Ptenoglossa). Argonauta 9/10-12, 3–10. Oliverio, M., Gofas, S. 2006. Coralliophiline diversity at Mid-Atlantic Seamounts (, Muricidae, Coralliophilinae). Bulletin of Marine Science 79, 205–230. Reijnen, B.T., Hoeksema, B.W., Gittenberger, E., 2010. Host specificity and phylogenetic relationships among Atlantic Ovulidae (Mollusca: Gastropoda). Contribution to Zoology 79, 69–78. Remia, A., Taviani, M., 2005. Shallow-buried Pleistocene Madrepora-dominated coral mounds on a muddy continental slope, Tuscan Archipelago, NE Tyrrhenian Sea. Facies 50, 419–425. Roberts, J.M., Wheeler, A.J., Freiwald, A., 2006. Reefs of the deep: the biology and geology of cold-water coral ecosystems. Science 312, 543–547. Robertson, R., 1967. Heliacus (Gastropoda: Architectonicidae) symbiotic with Zoanthinaria (Coelenterata). Science 156, 246–248. Robertson, R., 1970. Review of the predators and parasites of stony corals, with special reference to symbiotic prosobranch gastropods. Pacific Science 24, 43–54. Sabelli, B., Taviani, M., 1984. Red sea record of a Fungia-associated Epitoniid. Bolletino Malacologico 20, 91– 94. Schembri, P.J., Dimech, M., Camilleri, M., Page, R., 2007. Living deep-water Lophelia and Madrepora corals in Maltese waters (Strait of Sicily, Mediterranean Sea). Cahiers de Biologie Marine 48, 77–83. Taviani, M., Angeletti, L., Dimech, M., Mifsud, C., Freiwald, A., Harasewych, M.G., Oliverio, M., 2009. Coralliophilinae (Mollusca: Gastropoda) associated with deep-water coral banks in the Mediterranean. The Nautilus 123, 106–112. Taviani, M., Colantoni, P., 1979. Thanatocoenoses wurmiennes associées aux coraux blancs. Rapports de la Commission internationale Mer Méditerranée 25/26, 141–142. Taviani, M., Freiwald, A., Zibrowius, H., 2005. Deep coral growth in the Mediterranean Sea: An overview. In: Freiwald, A., Roberts, J.M. (Eds.), Deep-Water Corals and Ecosystems. Springer-Verlag, Berlin-Heidelberg, pp. 137–156. Taviani, M., Vertino, A., López Correa, M., Savini, A., De Mol, B., Remia, A., Montagna, P., Angeletti, L., Zibrowius, H., Alves, T., Salomidi, M., Ritt, B., Henry, P., 2010. Pleistocene to Recent scleractinian deep-water corals and coral facies in the Eastern Mediterranean. Facies, doi:10.1007/s10347-010-0247-8. Titschack, J., Freiwald,Accepted A., 2005. Growth, deposition and facies Manuscript of Pleistocene bathyal coral communities from Rhodes, Greece. In: Freiwald, A., Roberts, J.M. (Eds.), Deep-Water Corals and Ecosystems. Springer-Verlag, Berlin-Heidelberg, pp. 41–59. Wheeler, A.J., Beyer, A., Freiwald, A., de Haas, H., Huvenne, V.A.I., Kozachencko, M., Olu-Le Roy, K., Opderbecke, J., 2007. Morphology and environment of cold-water coral carbonate mounds on the NW European margin. International Journal of Earth Sciences 96, 37–56.

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Page 4 of 9 Fig. 1. Study area. A. Map showing the location of RV Urania MEDCOR 25 station in the Strait of Sicily. B. 3D reconstruction of the escarpment based on swath bathymetry data marking the South Malta CWC province from which the material examined in this article was obtained (white dot marks station MEDCOR 25).

Fig. 2. Coral framestone/hardground from MEDCOR 25. A. Large slab of coral framestone/hardground largely made up by Madrepora oculata and Lophelia pertusa branches (and subordinate Stenocyathus vermiformis and Corallium rubrum) displaying different degrees of sediment infilling and lithification from absent to advanced; note the patination by Fe-Mn oxides; scale bar = 5 cm. B. Detail of the same slab showing a blackened shell of Amphissa acutecostata (white arrow) almost completely embedded within the lithified matrix); scale bar = 1 cm. C. Same slab showing a coarser fabric with encased shells of Heliacus alleryi (black arrow) and of blackened “Coralliophila” squamosa (morphotype ruderatus: white arrow); scale bar = 1 cm.

Fig. 3. Examples of shells encased in coral framestones and hardgrounds, all from MEDCOR 25. A, B. Architectonicid shell (cf. Discotectonica discus) cemented to coral (Lophelia pertusa) framestone, black arrow points to the broken base of an unidentified scleractinian growing over the gastropod shell, white arrow points to the broken base of Corallium rubrum. C, F, G. Shell of Babelomurex sentix (Muricidae-Coralliophilinae) welded to a Lophelia branch; note degradation, fouling and blackening of the shell. D, E. Architectonicid shell (Heliacus alleryi) associated with a lithified matrix hosting pelagic molluscs and foraminifers. H. Loose Babelomurex sentix shell. I, J. Shell of “Coralliophila” squamosa (morphotype ruderatus) intensely fouled by various Lophelia corallites. K. Degraded and blackened ootheca of the epipelagic cephalopod Argonauta argo, infilled by lithified sediment. Scale bars = 5 mm.

Table 1. Radiocarbon Lab-code “Poz” refers to the Poznan Radiocarbon Laboratory in Poznan, Poland. Radiocarbon years (14C-yrs) correspond to the true half-life. Calibrated age ranges reflect the 95% probability window (2σ-error) and were calculated with Calib5.10, using the surface marine calibration curve MARINE 04 by Hughen et al. (2004).

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Page 5 of 9 Table 1

Sample Species Lab-code Radiocarbon Age [14C-yrs BP] Calibrated age range (2σ) [yrs cal BP] MEDCOR25 Babelomurex sentix Poz-37811 732 ± 73 659 - 804 MEDCOR25 Lophelia pertusa Poz-37812 628 ± 68 560 - 696

Table 1

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