The molluscan fauna of Chella Bank and surroundings (Western Mediterranean Sea)

INTRODUCTION

The Alboran Sea, located in the transition area between the Mediterranean Sea and the Atlantic Ocean, undergoes complex hydrodynamic processes caused by the mixing of water masses with different characteristics (Rodríguez 1982Rodríguez J. 1982. Oceanografía del Mar Mediterráneo. Pirámide, Madrid, 174 pp., Parrilla and Kinder 1987Parrilla G., Kinder T.H. 1987. Oceanografía física del mar de Alborán. Bol. Inst. Esp. Oceanogr. 4: 133-165., Vargas-Yáñez et al. 2019Vargas-Yáñez M., García-Martinez M.C., Moya F., et al. 2019. The Alboran Sea: From Cape Pino to Cape Gata. In: Vargas-Yáñez M., García-Martinez M.C., Moya F. et al. (eds), The present state of marine ecosystems in the Spanish Mediterranean in a climate change context. Tuimagina Editorial, Grupo Mediterráneo de Cambio Climático, Málaga, pp. 33-72.). Because of its unique hydrodynamics, partly conditioned by the coastal and seabed morphology, the Alboran Sea has nutrient-enriched upwellings on its margin and is considered one of the areas with the highest biological productivity within the Mediterranean Sea (Rodríguez 1982Rodríguez J. 1982. Oceanografía del Mar Mediterráneo. Pirámide, Madrid, 174 pp., 1995Rodríguez J. 1995. Las reservas marinas en el marco ecológico y oceanográfico del Mediterráneo Occidental. In: Guirado J. (eds): La gestión de los espacios marinos en el Mediterráneo Occidental, Instituto de Estudios Almerienses, Diputación de Almería, pp. 13-28., Sarhan et al. 2000Sarhan T., García Lafuente J., Vargas M., et al. 2000. Upwelling mechanisms in the northwestern Alboran Sea. J. Mar. Syst. 23: 317-331. https://doi.org/10.1016/S0924-7963(99)00068-8 ). In addition, the Alboran basin contains a wide variety of bottom types and physiographic features along the coastline (e.g. soft bottoms, rocky outcrops and cliffs), as well as in the circalittoral and bathyal zones (e.g. submarine canyons, banks, knolls, carbonated mounds and mud volcanoes) (Muñoz et al. 2008Muñoz A., Ballesteros M., Montoya I., et al. 2008. Alborán Basin, southern Spain - part I: geomorphology. Mar. Petrol. Geol. 25: 59-73. https://doi.org/10.1016/j.marpetgeo.2007.05.003 , Palomino et al. 2015Palomino D., Alonso B., Lo Iocano C., et al. 2015. Seamounts and seamount-like structures of the Alborán Sea. In: Würtz, M. and Rovere M. (eds), Atlas of the Mediterranean Seamounts and Seamount-like Structures. IUCN, Gland, Switzerland and Málaga, Spain, pp. 21-57.; Vázquez et al. 2021Vázquez J.T., Ercilla G., Catalán M., et al. 2021. A geological history for the Alboran Sea region. In: Báez J.C., Vázquez J.T, Camiñas J.A., Malouli M. (eds), Alboran Sea-Ecosystems and Marine Resources. Springer, Cham, pp. 111-155. https://doi.org/10.1007/978-3-030-65516-7_5 ). This also promotes a great heterogeneity of benthic habitats and communities that favour the presence of species with different ecological requirements, including some that are highly threatened and vulnerable (Templado 2011Templado J. 2011. La diversidad marina en España. In: Viejo J.L. (ed), Biodiversidad: aproximación a la diversidad botánica y zoológica en España. Mem. R. Soc. Esp. Hist. Nat. 9: 343-362., Templado et al. 2021Templado J., Luque Á. A., Moreno D., et al. 2021. Invertebrates: The Realm of Diversity. In: Báez J.C., Vázquez J.T, Camiñas J.A., Malouli M. (eds), Alboran Sea-Ecosystems and Marine Resources. Springer, Cham, pp. 359-430. https://doi.org/10.1007/978-3-030-65516-7_10 , Rueda et al. 2021Rueda J. L., Gofas S., Aguilar R., et al. 2021. Benthic fauna of littoral and deep-sea habitats of the Alboran Sea: a hotspot of biodiversity. In: Báez J.C., Vázquez J.T, Camiñas J.A., Malouli M. (eds), Alboran Sea-Ecosystems and Marine Resources. Springer, Cham, pp. 285-358. https://doi.org/10.1007/978-3-030-65516-7_9 ). Furthermore, three biogeographical regions converge close to the Alboran Sea, including the temperate Lusitanian region (from the English Channel to the Strait of Gibraltar), the warm Mauritanian region (from the Strait of Gibraltar to Cap Blanc) and the Mediterranean region itself (Ekman 1953Ekman S. 1953. Zoogeography of the sea. Sidgwick and Jackson, London, 417 pp., Caballero-Herrera et al. 2021Caballero‐Herrera J.A., Olivero J., von Cosel R., Gofas S. 2021. An analytically derived delineation of the West African Coastal Province based on bivalves. Divers. Distrib. 28 https://onlinelibrary.wiley.com/doi/10.1111/ddi.13454 ). This biogeographic confluence enables the coexistence of species from the North Atlantic or subtropical northwestern Africa with Mediterranean species, in addition to some endemic species (Gofas 1998Gofas S. 1998. Marine molluscs with a very restricted range in the Strait of Gibraltar. Divers Distrib. 4: 255-266., Rueda et al. 2010Rueda J.L., Urra J., Marina P., et al. 2010. Especies africanas en las costas de Andalucía: Un patrimonio natural único en Europa. Quercus 293: 24-31., Urra et al. 2017Urra J., Gofas S., Rueda J.L., Marina P., Mateo-Ramírez Á., Antit M., Salas C. 2017. Biodiversity and biogeographical patterns of molluscan assemblages in vegetated and unvegetated habitats in the northern Alboran Sea (W Mediterranean Sea). Mar. Biodiv. 47: 187-201. https://doi.org/10.1007/s12526-016-0468-3 , Sitjà et al. 2020Sitjà C., Maldonado M., Farias C., Rueda J. L. 2020. Export of bathyal benthos to the Atlantic through the Mediterranean outflow: Sponges from the mud volcanoes of the Gulf of Cadiz as a case study. Deep-Sea Res. Part I 163: 103326. https://doi.org/10.1016/j.dsr.2020.103326 ). Because of all these features, the Alboran Sea is considered one of the biodiversity hotspots within the Mediterranean basin and the European margin (García Raso et al. 2010García Raso J.E., Gofas S., Salas Casanova C., et al. 2010. El mar más rico de Europa: Biodiversidad del litoral occidental de Málaga entre Calaburras y Calahonda. Consejería de Medio Ambiente, Junta de Andalucía, Sevilla, 138 pp., Templado 2011Templado J. 2011. La diversidad marina en España. In: Viejo J.L. (ed), Biodiversidad: aproximación a la diversidad botánica y zoológica en España. Mem. R. Soc. Esp. Hist. Nat. 9: 343-362., Rueda et al. 2021Rueda J. L., Gofas S., Aguilar R., et al. 2021. Benthic fauna of littoral and deep-sea habitats of the Alboran Sea: a hotspot of biodiversity. In: Báez J.C., Vázquez J.T, Camiñas J.A., Malouli M. (eds), Alboran Sea-Ecosystems and Marine Resources. Springer, Cham, pp. 285-358. https://doi.org/10.1007/978-3-030-65516-7_9 ).

Molluscs account for 25% of the marine fauna and are one of the most diverse faunal groups in benthic communities (Appeltans et al. 2012Appeltans W., Ahyong S.T., Anderson G., Angel M., Artois T., Bailly N., et al. 2012. The magnitude of global marine species diversity. Curr. Biol. 22: 2189-2202. https://doi.org/10.1016/j.cub.2012.09.036 ). The Iberian margin, favoured by its geographical location and its great variety of benthic habitats from the supralittoral zone to the deep-sea bottoms, hosts more than half of the mollusc species registered within the European Register of Marine Species (http://www.marbef.org/data/erms.php) and therefore the richest molluscan biodiversity for the European margin (Gofas et al. 2017Gofas S., Luque Á.A., Templado J., Salas C. 2017. A national check list of marine Mollusca in Spanish waters. Sci. Mar. 81: 241-254. https://doi.org/10.3989/scimar.04543.21A ). Molluscs are an appropriate group for the evaluation of the local biodiversity of a specific area, since they are a very well-known faunal group, and several studies allow comparisons with neighbouring areas (Bedulli et al. 2002Bedulli D., Bassignani F., Bruschi A. 2002. Use of biodiversity hotspots for conservation of marine Molluscs: a regional approach. Mediterr. Mar. Sci. 3: 113-121. https://doi.org/10.12681/mms.250 , Gladstone 2002Gladstone W. 2002. The potential value of indicator groups in the selection of marine reserves. Biol. Conserv. 104: 211-220. https://doi.org/10.1016/S0006-3207(01)00167-7 , Smith 2005Smith S.D. 2005. Rapid assessment of invertebrate biodiversity on rocky shores: where there’s a whelk there’s a way. Biodivers. Conserv. 14: 3565-3576. https://doi.org/10.1007/s10531-004-0828-3 ). Additionally, they are an important component of benthic communities, playing a key trophic role due to their different feeding strategies and, in some cases, providing an ecosystem service because they can improve water and sediment quality (e.g. filter feeders and deposit feeders) (Gosling 2003Gosling E. 2003. Bivalve molluscs: Biology, ecology and culture. Wiley Blackwell, Oxford, UK, pp 456. https://doi.org/10.1002/9780470995532 ). Molluscs also form a fundamental link to upper trophic levels, including humans, who have exploited some mollusc species for centuries (Edgar and Shaw 1995Edgar G.J., Shaw C. 1995. The production and trophic ecology of shallow-water fish assemblages in southern Australia III. General relationships between sediments, seagrasses, invertebrates and fishes. J. Exp. Mar. Biol. Ecol. 194(1): 107-131. https://doi.org/10.1016/0022-0981(95)00085-2 , Pasquaud et al. 2010Pasquaud S., Pillet M., David V., Sautour B., Elie P. 2010. Determination of fish trophic levels in an estuarine ecosystem. Est. Coast. Shelf Sci. 86(2): 237-246. https://doi.org/10.1016/j.ecss.2009.11.019 ). Most previous studies on molluscs have focused on those of the infralittoral habitats from the northern Alboran Sea (Salas and Hergueta 1986Salas C., Hergueta E. 1986. The molluscan fauna of calcareous concretions of Mesophyllum lichenoides (Ellis) Lemoine. Study of annual cycle diversity. Iberus 6: 57-65., Rueda et al. 2009Rueda J.L., Gofas S., Urra J., Salas C. 2009. A highly diverse molluscan assemblage associated with eelgrass beds (Zostera marina L.) in the Alboran Sea: Micro-habitat preference, feeding guilds and biogeographical distribution. Sci. Mar. 73: 679-700. https://doi.org/10.3989/scimar.2009.73n4679 , Urra et al. 2011Urra J., Gofas S., Rueda JL., Marina P. 2011. Molluscan assemblages in littoral soft bottoms of the Alboran Sea (Western Mediterranean Sea). Mar. Biol. Res. 7: 27-42. https://doi.org/10.1080/17451001003660301 , 2017Urra J., Gofas S., Rueda J.L., Marina P., Mateo-Ramírez Á., Antit M., Salas C. 2017. Biodiversity and biogeographical patterns of molluscan assemblages in vegetated and unvegetated habitats in the northern Alboran Sea (W Mediterranean Sea). Mar. Biodiv. 47: 187-201. https://doi.org/10.1007/s12526-016-0468-3 , 2018Urra J., Rueda J.L., Marina P., Antit M., Salas C. 2018. Populations of commercial molluscs within a highly biodiverse Marine Protected Area of the Northern Alboran Sea (W Mediterranean): preferential habitats, seasonal dynamics and importance for artisanal fisheries. Thalassas 34: 349-359. https://doi.org/10.1007/s41208-018-0070-5 ). However, the molluscan assemblages associated with insular and/or deep zones have been poorly studied in the Alboran Sea, with few studies focused on surrounding areas of the Strait of Gibraltar (Salas 1996Salas C. 1996. Marine Bivalves from off the Southern Iberian Peninsula collected by the Balgim and Fauna 1 expeditions. Haliotis 25: 33-100.), the Alboran Island platform (Templado 1993Templado J. 1993. Fauna marina circalitoral del sur de la Península Ibérica: resultados de la campaña oceanográfica “Fauna I”. CSIC, Madrid, 135 pp., Peñas et al. 2006Peñas A., Rolán E., Luque A.A., et al.2006. Moluscos marinos de la isla de Alborán. Iberus 24(1): 23-151.), the Djibouti Bank (Gofas et al. 2014Gofas S., Salas C., Rueda J.L., et al. 2014. Mollusca from a species-rich deep-water Leptometra community in the Alboran Sea. Sci. Mar. 78(4): 537-553. https://doi.org/10.3989/scimar.04097.27A ) and the trawlable grounds of the shelf and slope (Ciércoles et al. 2018Ciércoles C., García-Ruiz C., González-Aguilar M., et al. 2018. Molluscs collected with otter trawl in the northern Alboran Sea: main assemblages, spatial distribution and environmental linkage. Mediterr. Mar. Sci. 19: 209-222. https://doi.org/10.12681/mms.2124 ).

The present study was carried out on a submarine knoll of the northeastern Alboran Sea, known as Chella Bank (also known in Spanish as Seco de los Olivos) and its adjacent bottoms. This submarine knoll has been recently integrated into the European Union (EU) Natura 2000 network as a site of community importance (SCI) (ESZZ16003 “Sur de Almería - Seco de los Olivos”). Previous studies in the area have focused on the presence of different habitats and their associated megabenthic species (de la Torriente et al., 2014de la Torriente A., Aguilar R., Serrano A., et al. 2014. Sur de Almería - Seco de los Olivos. Proyecto LIFE+ INDEMARES. Fundación Biodiversidad del Ministerio de Agricultura, Alimentación y Medio Ambiente, Madrid, pp 102., 2018de la Torriente A., Serrano A., Fernández-Salas L.M., et al. 2018. Identifying epibenthic habitats on the Seco de los Olivos Seamount: Species assemblages and environmental characteristics. Deep-Sea Res. Pt I. 135: 9-22. https://doi.org/10.1016/j.dsr.2018.03.015 , 2019de la Torriente A., González‐Irusta J.M., Aguilar R., et al. 2019. Benthic habitat modelling and mapping as a conservation tool for marine protected areas: A seamount in the western Mediterranean. Aquat. Conserv. 29: 732-750. https://doi.org/10.1002/aqc.3075 ) or specific benthic groups (e.g. brachiopods, bryozoans) (Llompart 1988Llompart C. 1988. Braquiópodos del Banco de Chella (Mar de Alborán, Mediterráneo Occidental). Acta Geol. Hisp. 23: 311-319.; Ramalho et al. 2020Ramalho L.V., Caballero-Herrera J.A., Urra J., Rueda J.L. 2020. Bryozoans from Chella Bank (Seco de los Olivos), with the description of a new species and some new records for the Mediterranean Sea. Mar. Biodiv. 50: 106. https://doi.org/10.1007/s12526-020-01119-y ). However, information on other benthic macro- and micro-fauna, including molluscs, is very scarce and restricted to the presence of a few macrofaunal species (e.g. for molluscs Episcomitra zonata (Marryat, 1818), Ranella olearium (Linnaeus, 1758), Octopus vulgaris Cuvier, 1797 and Sepia officinalis Linnaeus, 1758) (Abad et al. 2007Abad E., Preciado I., Serrano A., Baro J. 2007. Demersal and epibenthic assemblages of trawlable grounds in the northern Alboran Sea (western Mediterranean). Sci. Mar. 71: 513-524. https://doi.org/10.3989/scimar.2007.71n3513 , de la Torriente et al. 2014de la Torriente A., Aguilar R., Serrano A., et al. 2014. Sur de Almería - Seco de los Olivos. Proyecto LIFE+ INDEMARES. Fundación Biodiversidad del Ministerio de Agricultura, Alimentación y Medio Ambiente, Madrid, pp 102.). Formally speaking, Chella Bank does not qualify as a seamount because it is close to the mainland and its elevation above the sea bottom is far less than 1000 m, as defined by Staudigel et al. (2010)Staudigel H., Koppers A.A., Lavelle J.W., et al. 2010. Defining the word “Seamount”. Oceanography 23: 20-21. https://doi.org/10.5670/oceanog.2010.85 . However, it retains some seamount characteristics (Von Rad 1974Von Rad U. 1974. Great Meteor and Josephine seamounts (eastern North Atlantic): composition and origin of bioclastic sands, carbonate and pyroclastic rocks. Meteor Forschungsergeb. C 19: 1-61.), among which the most important may be the absence of sedimentary input to the upper platform from the mainland, separated by a channel about 350 m deep (Fig. 1).

Increasing knowledge on the biodiversity of different habitats of this SCI will improve our understanding of the role of this submarine elevation for the Alboran Sea and western Mediterranean Sea biodiversity. Moreover, accurate information on the circalittoral and bathyal communities of the Alboran Sea is needed to implement suitable conservation and management measures within the framework of current European Directives (e.g. the Marine Strategy Framework Directive) and the ecosystem approach to fisheries management (Borja et al. 2010Borja A., Elliott M., Carstensen J., Heiskanen A.-S., Bund W. 2010. Marine management-Towards an integrated implementation of the European Marine Strategy Framework and the Water Framework Directives. Mar. Pollut. Bull. 60: 2175-2186. https://doi.org/10.1016/j.marpolbul.2010.09.026 , Jennings et al. 2014Jennings S., Smith A.D., Fulton E.A., Smith D.C. 2014. The ecosystem approach to fisheries: management at the dynamic interface between biodiversity conservation and sustainable use. Ann. N. Y. Acad. Sci. 1322: 48-60. https://doi.org/10.1111/nyas.12489 ). Technological progress, mainly in the fisheries sector, is promoting the human exploitation of fish resources into deeper areas that are increasingly distant from the coast, causing severe impacts on the habitats and their associated biodiversity (Clark et al. 2007Clark M.R., Koslow J.A. 2007. Impacts of fisheries on seamounts. In: Pitcher T.J., Morato T., Hart P.J.B., et al. (eds), Seamounts: Ecology, fisheries, and conservation. Blackwell, Oxford, pp. 413-441. https://doi.org/10.1002/9780470691953.ch19 ). Therefore, to achieve a sustainable extraction of resources, it is necessary to study and characterize the deep sea to improve its management and conservation, especially when it harbours vulnerable marine ecosystems (VMEs) such as those occurring on submarine elevations. The main aim of the present study was to improve knowledge of the biodiversity of this SCI and in particular (1) to characterize the molluscan taxocenoses and thanatocenoses and (2) to analyse the affinities of the molluscan fauna with its biogeographical context. This information will also be beneficial for the development of the management plans of this SCI to become a special conservation area in the near future.

MATERIALS AND METHODS

RESULTS

Rare species

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Anatoma micalii and Granigyra granulifera are recorded for the first time in Spanish waters and Anekes paucistriata for the first time in the Alboran Sea (Fig. 2). Other species are not new, but are seldom recorded: e.g. the eulimid Curveulima beneitoi (Fig. 2) (so far only known from its type locality in the Alboran platform), the columbellid Mitrella templadoi (Fig. 3) (recently described by Gofas et al. 2019Gofas S., Luque Á., Urra J. 2019. Planktotrophic Columbellidae (Gastropoda) in the northeast Atlantic and the Mediterranean Sea, with description of a new species in the genus Mitrella. Bull Mar Sci. 96. https://doi.org/10.5343/bms.2019.0015 from the Strait of Gibraltar and the Meteor group seamounts of the northeastern Atlantic), the pyramidellid Parthenina palazzii, and three species of the genus Mathilda (Fig. 3). Episcomitra angelesae (Fig. 2) was described very recently, partly using the present material (Caballero-Herrera et al. 2022Caballero-Herrera J.A., Gofas S., Rueda J.L. 2022. Episcomitra angelesae (Mollusca: Gastropoda: Mitridae), a new species from an exceptional deep habitat in the Alboran Sea. Mediterr. Mar. Sci. 23: 14-24. https://doi.org/10.12681/mms.27880 ).

Fig. 2.  - Rare or unusual monoplacophorans (A, B) and gastropods (C-R) found on Chella Bank (Seco de los Olivos) and its adjacent bottoms (measurements refer to largest dimension). A, B: Veleropilina euglypta (Medwaves VV37; 1.8 mm). C, D: Anatoma micalii, new record for Spanish waters (MEDWAVES VV40; 1.9 mm). E: Anekes paucistriata (MEDWAVES VV44, 0.9 mm). F: Granigyra granulifera, new record for Spanish waters (MEDWAVES VV34; 2.1 mm). G, H: Tricolia deschampsi, exclusively found in the thanatocoenosis (MONCARAL VV10; 1.6 mm). I, J: Talassia dagueneti (MEDWAVES VV36; 2.4 mm). K, L: Opalia abbotti and its protoconch (MEDWAVES VV38; 3.6 mm). M: Ionthoglossa pseudocanarica (MEDWAVES VV38; 5.1 mm). N: Retilaskeya horrida (MEDWAVES VV38; 9.0 mm). O, P: Onchodia valeriae (MEDWAVES VV39; 4.2 mm). Q, R: Curveulima beneitoi (MEDWAVES VV40; 1.4 mm).

Fig. 3.  - Rare or unusual gastropods found on Chella Bank (Seco de los Olivos) and its adjacent bottoms. A: Episcomitra angelesae, MEDWAVES VV39; 22 mm). B, C: Leufroyia erronea (MEDWAVES VV40; 10.9 mm). D: Mitrella templadoi (MEDWAVES VV38; 9.1 mm). E: Mitrolumna wilhelminae (MONCARAL VV12; 7.2 mm). F, G: Mathilda coronata (MEDWAVES VV38; 5.4 mm). H, I: Mathilda cochleaeformis (MEDWAVES VV39; 8.4 mm). J, K: Mathilda retusa (MEDWAVES VV39; 8.9 mm). L, M: Parthenina palazzii (MEDWAVES VV43; 1.8 mm). N: Parthenina flexuosa (MEDWAVES VV43; 1.6 mm). O, P: Rhinodiaphana ventricosa (MEDWAVES VV35; 2.8 mm). Q, R: Colpodaspis pusilla (MEDWAVES VV38; 1.4 mm).

Affinity between samples

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Four main groups of samples (similarity >0.2) were detected in multivariate analyses of live-taken molluscs (Fig. 4), one of them corresponding to the samples collected on buried carbonate mounds located close to the shelf break northwards of Chella Bank, and the other three to samples collected on Chella Bank. Two samples (VV12 and VV13) displayed no similarity to any group and were not considered further. The four groups were supported by the SIMPROF test (π = 2.68, p < 0.005). The typifying taxa (according to SIMPER) within each groups of samples are displayed in Table S1 (Supplementary material).

Fig. 4.  - Cluster based on Bray-Curtis similarity index and abundance data of live-taken molluscs species (fourth root transformed) collected on Chella Bank (Seco de los Olivos) and its adjacent bottoms. Continuous lines indicate significant differences between samples or group of samples in SIMPROF test (p < 0.005).

Group I (VV09, VV10, VV11) (Upper bathyal muddy bottoms with buried rhodoliths)

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This group of samples was collected on buried carbonate mounds located close to the mainland shelf break northwest of Chella Bank at 178-210 m depth. The sediment was composed predominantly of mud (>60%), except in sample VV11, which contained a greater percentage of coarse and medium sand (>30%, respectively). These samples showed an intermediate percentage of organic matter (%OM) (4.3±0.2%, mean±standard error) and one of the highest carbonate contents (%CO₃, 22.9±6.9%) in comparison with other groups of samples. They were characterized by the presence of remains of dead rhodoliths within the sediment, and the abundance of dead shells of Tricolia deschampsi (Fig. 2) (a species always found living among rhodoliths but not detected alive in any of the samples) was noteworthy. A total of 16 live-taken molluscan species were found, with the bivalves Kelliella miliaris, Saccella commutata and Parvicardium minimum as the top dominant taxa (Fig. 5, Table S2).

Fig. 5.  - Some characteristic species (bivalves, A-K, P-Q; gastropod, M-N; caudofoveate, L; scaphopod, O) of the four groups of samples identified on Chella Bank (Seco de los Olivos) and its adjacent bottoms. A, B: Saccella commutata (MONCARAL VV09; 5.5 and 5.1 mm). C, D: Kelliella miliaris (MONCARAL VV10; 1.6 and 1.7 mm). E: Mendicula ferruginosa, live-taken specimen with thick oxide crust (MEDITS VV25; 1.3 mm). F: M. ferruginosa from thanatocoenosis, without the crust (MEDWAVES VV34; 2.4 mm). G: Dacrydium hyalinum, byssally attached to a sediment particle (MEDWAVES VV38; 2.0 mm). H: Limopsis angusta, byssally attached to a coarse particle (MEDWAVES VV40; 2.7 mm). I, J: Thyasira obsoleta (MEDWAVES VV34; 1.5 mm). K: Axinulus croulinensis (MEDWAVES VV34; 1.6 mm). L: Class Caudofoveata, Prochaetoderma sp. (MEDWAVES VV32; 1.4 mm). M, N: Class Gastropoda, Gibberula turgidula (MEDWAVES VV42; 2.1 mm). O: Class Scaphopoda, Cadulus jeffreysi (MEDWAVES VV35; 3.2 mm). P, Q: Yoldiella philippiana (MEDWAVES VV36; 3.6 and 2.9 mm).

Group II (VV38, VV39, VV40) (Upper bathyal muddy bottoms with exposed coral rubble on the flanks of Chella Bank)

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This group corresponded to samples collected on the NE flank of the main elevation of Chella Bank between the pinnacles (ca. 250 m depth). The seabed was characterized by the presence of abundant exposed coral rubble corresponding mostly to the cold-water coral M. oculata, together with a wide variety of invertebrates inhabiting the coral rubble matrix, including crinoids, ophiurids (e.g. Ophiothrix sp.) and solitary corals such us Caryophyllia sp. The main sediment component was mud (>75%), with an intermediate %OM (4.9±0.17) and the lowest %CO₃ (5.6±0.4) (Kruskal-Wallis for %CO₃ comparisons: χ2=9.7, p<0.05). There were 31 live-taken species, with the bivalves Dacrydium hyalinum, Mendicula ferruginosa, Heteranomia squamula and Limopsis angusta and the gastropod Vitreolina curva as the top dominant species (Fig. 5, Table S2).

Group III (VV24, VV25, VV26 VV31, VV32, VV34, VV41, VV44) (Upper and middle bathyal muddy hemipelagic bottoms on the flanks of Chella Bank and adjacent bottoms).

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This group was composed of eight samples located on bathyal muddy bottoms on the periphery of the main elevation of Chella Bank along a wide bathymetrical range (334-729 m depth). The seabed was mainly characterized by muddy hemipelagic sediments (>90%) with the presence of planktonic pteropod and foraminifera shells and showed the highest %OM (5.7±0.8%) (Kruskal-Wallis for OM comparisons: χ²= 12.2, p<0.05) and intermediate %CO₃ (7.2±2.1). A total of 23 live-taken molluscs species were found, with the bivalves Thyasira obsoleta, Axinulus croulinensis, Mendicula ferruginosa and Kelliella miliaris as the top dominant species (Fig. 5, Table S2).

Group IV (VV35, VV36, VV37, VV42, VV43) (Upper Bathyal sandy bottoms on the flanks of Chella Bank)

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This group was detected northeast of Chella Bank at 280-320 m depth. The seabed was generally characterized by sandy sediment (>50%) and the presence of buried bioclasts, including some coral rubble. The sediment displayed the lowest %OM (2.9±0.2%) (Kruskal-Wallis for OM comparisons: χ²= 12.2, p<0.05) and intermediate %CO₃ (12.5±1.1%). There were 26 live-taken species, with the gastropod Gibberula turgidula, the bivalves Yoldiella philippiana and Bathyarca pectunculoides and the scaphopod Cadulus jeffreysi as the top dominant species (Fig. 5, Table S2).

Ungrouped samples (VV12, VV13)

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These two samples were taken at the summit of Chella Bank at 95 and 140 m depth, respectively, at the shallowest sampling stations of the study area. Sample VV12 was composed predominantly of coarse sand (51.44%) with very abundant bioclasts and live rhodoliths. It contained 4.4% OM and showed the highest %CO₃ (51.7%) of all samples (Kruskal-Wallis for %CO₃ comparissons: χ²= 9.7, p<0.05). The live-taken molluscan fauna was represented by the bivalves Goodallia triangularis, Modiolula phaseolina and Striarca lactea, and the gastropods Anatoma aspera and Talassia dagueneti (Table S2, supplementary material). On the other hand, sample VV13 was composed predominantly of gravel (70.7%) with very abundant exposed bioclasts but dead rhodoliths with a size ranging between 7 and 10 cm. Four live-taken gastropod species dominated, including Curveulima beneitoi, Chauvetia recondita, Sticteulima jeffreysiana and Orania fusulus (Table S2, Supplementary material).

Regarding ecological parameters, the highest values of species richness (S) and Shannon-Wiener diversity H’(log₂) index were detected in Group II (S=17±2.1 spp.; H’(log₂)=3.4±0.2) (Kruskal-Wallis S, χ²=8.84, p<0.05); H’(log2), χ²=8.57, p<0.05), whereas the highest abundance (N) value was detected in Group I (1310±603.7 ind.) (Kruskal-Wallis N, χ²=12.179, p<0.05). On the other hand, the lowest S and N values were observed in Group III (S=6.9±1.1 spp.; N=136±27.1 ind.), although this group displayed the highest evenness index value (J’=0.95 ±0.02) (Kruskal-Wallis J’, χ²=10.24, p<0.05). The lowest H’(log₂) and J’ values were observed in the group I (H’(log₂)=1.8±0.6; J’= 0.6±0.2).

Affinities with the biogeographical context

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Most of the mollusc species from Chella Bank and its adjacent bottoms considered in the analyses display a wide distributional range in the Atlantic Ocean and are also present in the Mediterranean Sea. Three major chorotypes and another group of species with a gradual distribution pattern were identified (Fig. 6, Table 3).

Fig. 6.  - Cluster of live-taken molluscs species collected on Chella Bank (Seco de los Olivos) and its adjacent bottoms from different geographic areas using presence/absence data and the Baroni-Urbani and Buser (1976)Baroni-Urbani C., Buser M.W. 1976. Similarity of binary data. Syst. Zool. 25: 251-259. https://doi.org/10.2307/2412493 similarity index. (ALB, Alboran Sea; CN, Canary Islands, Madeira and Lusitanian seamounts; IB, Ibero-Moroccan Gulf; ME, Mediterranean; NE, North Europe; WA, West Africa; WE, West Europe; ALL, all geographic areas; +, presence; -, absence). Black point indicates chorotypes 1, 2 and 3, respectively, and white point corresponds to a group of species with a gradual pattern distribution.

Table 3.  Parameters for chorotypes and gradual patterns in Figure 6. IH is the internal homogeneity index. IH >0 and a significant G (independence G-test, with p-value) indicate that the cluster can be considered a chorotype. Otherwise, the cluster is a group of species with a gradual distribution pattern.

	IH	G	P
Chorotype 1	0.55	392.602	0
Chorotype 2	0.439	53.282	0
Chorotype 3	0.558	130.036	0
Gradual pattern	0.223	2.023	0.155

Chorotype 1 (C1) shares 40 species widely distributed along the Atlantic Ocean and Mediterranean Sea: 14 of them are present in all the localities (e.g. Heteranomia squamula, Myrtea spinifera, Anatoma aspera), 8 are widely distributed and absent in Northern Europe (e.g. Gregariella semingranata, Striarca lactea, Epitonium algerianum), 13 are absent in West Africa (e.g. Asperarca nodulosa, Bathyarca philippiana, Alvania cimicoides) and 4 are also widely distributed but not present in West Africa and Northern Europe (Thyasira succisa, Drilliola lopestriana, Vitreolina curva and Talassia dagueneti).

Chorotype 2 (C2) is formed by 14 species distributed along the Mediterranean Sea and showing different combinations of distribution patterns along the Atlantic location. They are particularly absent in the Canary Islands (e.g. Nucula sulcata, Mendicula ferruginosa and Thyasira biplicata), absent in the Canary Islands and West Africa (e.g. Kelliella miliaris, Kurtiella bidentata and Thyasira granulosa) or absent in the Canary Islands, West Africa and Northern Europe (e.g. Chauvetia recondita, Krachia cylindrata and Alvania tomentosa).

Chorotype 3 (C3) is represented by 14 species with a more restricted distribution close to the Alboran Sea. Of these, there are only two strictly Mediterranean species, the bivalves Kelliopsis jozinae and Nucula perminima; six of them are reported in the Mediterranean and also in the Ibero-Moroccan Gulf but not in the rest of the Atlantic Ocean (e.g. Dacrydium hyalinum, Ennucula aegeensis and Anatoma micalii); two are present in the Ibero-Moroccan Gulf and the Canary Islands but not in the Mediterranean (Limopsis angusta and Onchodia valeriae); and three species are present along the Canary Islands, the Ibero-Moroccan Gulf and the Mediterranean Sea (Emarginula adriatica, Retilaskeya horrida and Pleurotomella demosia).

Another five species were clustered together showing occasional occurrence at different Atlantic locations and the Alboran Sea but not in the rest of the Mediterranean (Ennucula decipiens, Mitrella templadoi and Strobiligera brychia); were endemic to the Alboran Sea (the gastropod Curveulima beneitoi); or were restricted to the Alboran basin and West Europe (the gastropod Adeuomphalus ammoniformis).

The most predominant type of larval development was short planktonic (70% of the total of the live-taken species), followed by planktotrophic development (22%) and direct development (8%). This ratio was not found to differ significantly between the chorotypes.

DISCUSSION

This study has considerably increased the knowledge on molluscs for the recently declared SCI “Sur de Almería - Seco de los Olivos”, adding more than 95% to the previously reported species. The absence of cephalopods could be linked to the sampling method used here (van Veen grab), which is not appropriate for collecting those highly mobile organisms, whereas other studies using bottom otter trawling added appropriate data of this group for the northern Alboran Sea (Abad et al. 2007Abad E., Preciado I., Serrano A., Baro J. 2007. Demersal and epibenthic assemblages of trawlable grounds in the northern Alboran Sea (western Mediterranean). Sci. Mar. 71: 513-524. https://doi.org/10.3989/scimar.2007.71n3513 ; Ciércoles et al. 2018Ciércoles C., García-Ruiz C., González-Aguilar M., et al. 2018. Molluscs collected with otter trawl in the northern Alboran Sea: main assemblages, spatial distribution and environmental linkage. Mediterr. Mar. Sci. 19: 209-222. https://doi.org/10.12681/mms.2124 ). Previous studies listed 13 species on Chella Bank (de la Torriente et al. 2014de la Torriente A., Aguilar R., Serrano A., et al. 2014. Sur de Almería - Seco de los Olivos. Proyecto LIFE+ INDEMARES. Fundación Biodiversidad del Ministerio de Agricultura, Alimentación y Medio Ambiente, Madrid, pp 102.), including seven cephalopod species and the giant deep-sea oyster Neopycnodonte zibrowii, which forms small concretions in deep vertical rocky walls (Abad et al. 2007Abad E., Preciado I., Serrano A., Baro J. 2007. Demersal and epibenthic assemblages of trawlable grounds in the northern Alboran Sea (western Mediterranean). Sci. Mar. 71: 513-524. https://doi.org/10.3989/scimar.2007.71n3513 , de la Torriente et al. 2014de la Torriente A., Aguilar R., Serrano A., et al. 2014. Sur de Almería - Seco de los Olivos. Proyecto LIFE+ INDEMARES. Fundación Biodiversidad del Ministerio de Agricultura, Alimentación y Medio Ambiente, Madrid, pp 102.). Moreover, gastropods included in the Berna and/or Barcelona Convention and catalogued as vulnerable species in the Libro Rojo de los Invertebrados de Andalucía (Red Book of the Invertebrates of Andalusia) were reported by de la Torriente et al. (2014)de la Torriente A., Aguilar R., Serrano A., et al. 2014. Sur de Almería - Seco de los Olivos. Proyecto LIFE+ INDEMARES. Fundación Biodiversidad del Ministerio de Agricultura, Alimentación y Medio Ambiente, Madrid, pp 102., including Charonia lampas (Linnaeus, 1758), Episcomitra zonata, Ranella olearium and Zonaria pyrum (Gmelin, 1791). The richness of mollusc species found on Chella Bank and its adjacent bottoms confirms the importance of this marine protected area (MPA) as a biodiversity hotspot within the context of the Alboran Sea and the western Mediterranean Sea, which is a priority area for the conservation of the marine biodiversity integrated in the EU Natura 2000 network (de la Torriente et al. 2014de la Torriente A., Aguilar R., Serrano A., et al. 2014. Sur de Almería - Seco de los Olivos. Proyecto LIFE+ INDEMARES. Fundación Biodiversidad del Ministerio de Agricultura, Alimentación y Medio Ambiente, Madrid, pp 102., Mateo Ramírez et al. 2021Mateo-Ramírez, Á., Marina P., Moreno D., et al. 2021. Marine Protected Areas and Key Biodiversity Areas of the Alboran Sea and Adjacent Areas. In: Báez, J.C., Vázquez, JT., Camiñas, J.A., Malouli Idrissi, M. (eds) Alboran Sea - Ecosystems and Marine Resources. Springer, Cham, pp. 819-923. https://doi.org/10.1007/978-3-030-65516-7_25 ).

The high diversity of molluscs reported on Chella Bank and its adjacent bottoms is in agreement with the extraordinary biodiversity of other faunal groups that occur on this bank, such as gorgonians, corals, sponges, echinoderms and bryozoans (de la Torriente et al. 2014de la Torriente A., Aguilar R., Serrano A., et al. 2014. Sur de Almería - Seco de los Olivos. Proyecto LIFE+ INDEMARES. Fundación Biodiversidad del Ministerio de Agricultura, Alimentación y Medio Ambiente, Madrid, pp 102., 2018de la Torriente A., Serrano A., Fernández-Salas L.M., et al. 2018. Identifying epibenthic habitats on the Seco de los Olivos Seamount: Species assemblages and environmental characteristics. Deep-Sea Res. Pt I. 135: 9-22. https://doi.org/10.1016/j.dsr.2018.03.015 ; Ramalho et al. 2020Ramalho L.V., Caballero-Herrera J.A., Urra J., Rueda J.L. 2020. Bryozoans from Chella Bank (Seco de los Olivos), with the description of a new species and some new records for the Mediterranean Sea. Mar. Biodiv. 50: 106. https://doi.org/10.1007/s12526-020-01119-y ). Many of these benthic organisms have three-dimensional structures which provide architectural complexity and refuge for several species, including molluscs such as Epitoniidae, Muricidae (Coralliophilla spp.) and Solenogastres, where they find shelter, food and/or spawning areas (Gofas et al. 2011Gofas S., Moreno D., Salas C. 2011. Moluscos marinos de Andalucía. Servicio de Publicaciones e Intercambio Científico, Universidad de Málaga. Vol. I, pp 1-342; Vol. II, pp 343-798., Rossi et al. 2017Rossi S, Bramanti L, Gori A, Orejas C. 2017. An overview of the animal forests of the world. In: Rossi S., Bramanti L., Gori A., Orejas C. (eds) Marine animal forests. Springer, Cham, pp. 1-28. https://doi.org/10.1007/978-3-319-17001-5_1-1 ). Molluscs are considered key indicators (surrogates) of the biodiversity of other taxa (Reyers et al. 2000Reyers B., van Jaarsveld A.S., Krüger M. 2000. Complementarity as a biodiversity indicator strategy. Proc. Roy. Soc. B. Biol. Sci. 267: 505-513. https://doi.org/10.1098/rspb.2000.1029 ) and are therefore a suitable group for evaluating the biodiversity of a particular marine area (Reyers et al. 2000Reyers B., van Jaarsveld A.S., Krüger M. 2000. Complementarity as a biodiversity indicator strategy. Proc. Roy. Soc. B. Biol. Sci. 267: 505-513. https://doi.org/10.1098/rspb.2000.1029 , Mellin et al. 2011Mellin C., Delean S., Caley J., et al. 2011. Effectiveness of biological surrogates for predicting patterns of marine biodiversity: a global meta-analysis. PloS ONE. 6: e20141. https://doi.org/10.1371/journal.pone.0020141 ).

The samples analysed here were collected with a traditional sampling technique, the van Veen grab, which is a sediment sampler with a very small sampling area (ca. 0.1 m²) that has a low impact on the seabed, a factor which is crucial for studying biodiversity in VMEs. Despite the limited sampled area and the fact that samples were mostly collected in the bathyal zone, a high number of species was found. The combination of different sampling techniques, whenever it is possible, is the most appropriate methodology for studying benthic communities, because then the species of different ecosystem compartments (i.e. epibenthic and infaunal) can be collected. For instance, Utrilla et. al (2020)Utrilla O., Gofas S., Urra J., et al. 2020. Molluscs from benthic habitats of the Gazul mud volcano (Gulf of Cádiz). Sci. Mar. 84: 273-295. https://doi.org/10.3989/scimar.05027.17A used a combination of sampling methods (e.g. box-corer dredge, shipek grab, benthic dredge and beam-trawl) to study deep molluscan assemblages at Gazul mud volcano and adjacent areas in the northeastern Gulf of Cádiz, where they reported a total of 232 species. In the infralittoral zone of the northern Alboran Sea, Rueda et al. (2009)Rueda J.L., Gofas S., Urra J., Salas C. 2009. A highly diverse molluscan assemblage associated with eelgrass beds (Zostera marina L.) in the Alboran Sea: Micro-habitat preference, feeding guilds and biogeographical distribution. Sci. Mar. 73: 679-700. https://doi.org/10.3989/scimar.2009.73n4679 studied the fauna of molluscs associated with Zostera marina beds (12-16 m) by combining a small Agassiz trawl and quadrates taken with scuba-diving techniques, and reported a total of 162 species. The present study documents a significant number of mollusc species (299 taxa) for this SCI using a single sampling method, but the number is certainly underestimated and, for instance, the large species reported from video footages by de la Torriente et al. (2014)de la Torriente A., Aguilar R., Serrano A., et al. 2014. Sur de Almería - Seco de los Olivos. Proyecto LIFE+ INDEMARES. Fundación Biodiversidad del Ministerio de Agricultura, Alimentación y Medio Ambiente, Madrid, pp 102. are missing. Moreover, the small total area sampled (1.84 m²) represents a very small fraction of the studied bottoms and of the fauna that inhabit them, so any conclusion on the relationships of the studied fauna with environmental characteristics may be venturesome. Therefore, further sampling using low-impact sampling techniques may improve knowledge on the total faunistic list of molluscs of the SCI, the different assemblages that they form and the role of environmental variables on the spatial distribution of these species and assemblages. Nevertheless, the present work still provides a baseline of benthic molluscs associated with certain types of bottoms that are still poorly studied in bathyal areas of some parts of the Mediterranean Sea, in this case the Alboran Sea.

The study of the thanatocoenosis was given special consideration in this study, and this considerably increased the faunal list with the rare species that occur at low density and/or are difficult to collect (Kidwell 2001Kidwell S.M. 2001. Ecological fidelity of molluscan death assemblages. In: Aller J.Y., Woodin S.A.., Aller R.C. (eds), Organism-sediment Interactions. University of South Carolina Press, Columbia, pp. 199-221., Albano and Sabelli 2011Albano P.G., Sabelli B. 2011. Comparison between death and living molluscs assemblages in a Mediterranean infralittoral off-shore reef. Palaeogeogr. Palaeoclimatol. Palaeoecol. 310: 206-215. https://doi.org/10.1016/j.palaeo.2011.07.012 ). Examples of this fauna include species inhabiting stone cracks (e.g. Coralliophaga lithophagella) and rocky bottoms (e.g. Arca tetragona and Neopycnodonte cochlear), those living on vertical walls (e.g. N. zibrowii) that were not sampled in this study but observed in ROV images recorded during the MEDWAVES expedition, and epibionts such as species of the family Eulimidae, some of them parasites of echinoderms. Species only found in low numbers in the thanatocoenosis, such as Pisinna glabrata and Cardita calyculata (both inhabiting the infralittoral zone) are very probably extinct on Chella Bank. However, the presence of other shells may represent indicators of the actual existence in the area of species (e.g. Aporrhais serresiana and N. cochlear) that are common and abundant in similar environments of the Alboran Sea (Gofas et al. 2011Gofas S., Moreno D., Salas C. 2011. Moluscos marinos de Andalucía. Servicio de Publicaciones e Intercambio Científico, Universidad de Málaga. Vol. I, pp 1-342; Vol. II, pp 343-798., Ciércoles et al. 2018Ciércoles C., García-Ruiz C., González-Aguilar M., et al. 2018. Molluscs collected with otter trawl in the northern Alboran Sea: main assemblages, spatial distribution and environmental linkage. Mediterr. Mar. Sci. 19: 209-222. https://doi.org/10.12681/mms.2124 ). The same probably applies to the Mathilda species, which are epibiotic on Zoantharians and usually occur at low densities, so they are very difficult to capture alive with a small dredge sampler (Gofas et al. 2011Gofas S., Moreno D., Salas C. 2011. Moluscos marinos de Andalucía. Servicio de Publicaciones e Intercambio Científico, Universidad de Málaga. Vol. I, pp 1-342; Vol. II, pp 343-798.).

In addition, the thanatocoenosis provides information on species that lived in the past (Kidwell 2001Kidwell S.M. 2001. Ecological fidelity of molluscan death assemblages. In: Aller J.Y., Woodin S.A.., Aller R.C. (eds), Organism-sediment Interactions. University of South Carolina Press, Columbia, pp. 199-221.), such as the pteropod Limacina retroversa, which has been reported as a Mediterranean “cold host” during glacial periods and interpreted as an element of a thanatocoenosis that is now extinct in the Mediterranean Sea (Malatesta and Zarlenga 1986Malatesta A., Zarlenga F. 1986. Northern guests in the Pleistocene Mediterranean Sea. Geol. Romana 25: 91-154.). Another example is the gastropod Tricolia deschampsi (Fig. 2), which is a characteristic species of bottoms with calcareous algae (Gofas et al. 2011Gofas S., Moreno D., Salas C. 2011. Moluscos marinos de Andalucía. Servicio de Publicaciones e Intercambio Científico, Universidad de Málaga. Vol. I, pp 1-342; Vol. II, pp 343-798.), being mostly represented in the thanatocoenosis from samples collected on buried carbonate mounds close to the shelf break, where muddy bottoms with buried rhodoliths occur (Sánchez-Guillamón et al. 2022Sánchez-Guillamón O., Rueda J.L., et al. 2022. Morphosedimentary, Structural and Benthic Characterization of Carbonate Mound Fields on the Upper Continental Slope of the Northern Alboran Sea (Western Mediterranean). Geosciences 12: 111. https://doi.org/10.3390/geosciences12030111 ). This corresponds to an ancient occurrence on carbonate mounds of maërl-rhodolith bottoms from the glacial Pleistocene, when the sea level was lower than nowadays (Sánchez-Guillamón et al. 2022Sánchez-Guillamón O., Rueda J.L., et al. 2022. Morphosedimentary, Structural and Benthic Characterization of Carbonate Mound Fields on the Upper Continental Slope of the Northern Alboran Sea (Western Mediterranean). Geosciences 12: 111. https://doi.org/10.3390/geosciences12030111 ). However, T. deschampsi could still occur on Chella Bank since well-preserved shells were also found at the top of the bank (95 m depth), where live rhodoliths beds occur but could not be sufficiently sampled in this study.

The importance of sorting the collected material into different size fractions, with special care for the fine fractions (0.5-1 mm and 1-2 mm) considering molluscs, is a key factor behind the large number of species found in this study. Gofas et al. (2014)Gofas S., Salas C., Rueda J.L., et al. 2014. Mollusca from a species-rich deep-water Leptometra community in the Alboran Sea. Sci. Mar. 78(4): 537-553. https://doi.org/10.3989/scimar.04097.27A documented the retention of over 90% of 156 species of molluscs in the fine fraction of a sample of sediment from Djibouti Bank (Alboran Sea) sieved on a 0.5 mm mesh, and this observation is similar to that from Streftaris and Zenetos (2007)Streftaris N., Zenetos A. 2007. Molluscan diversity in the N. East Aegean - Greece. Rapp. Comm. Int. Mer Médit. 38: 607.. When the benthos (mostly soft bottoms) is sampled with samplers that do not retain the fine fraction, the number of mollusc species drops dramatically, as in the case documented by Ciércoles et al. (2018)Ciércoles C., García-Ruiz C., González-Aguilar M., et al. 2018. Molluscs collected with otter trawl in the northern Alboran Sea: main assemblages, spatial distribution and environmental linkage. Mediterr. Mar. Sci. 19: 209-222. https://doi.org/10.12681/mms.2124 , who obtained 190 samples with a bottom otter trawl in circalittoral and bathyal soft bottoms of the northern Alboran Sea and reported only 101 molluscs species, mainly macrobenthic and demersal molluscs. Therefore, the methodology of this study is essential for obtaining a more complete assessment of species diversity, as micro-molluscs usually represent a large proportion of the total molluscan diversity (Albano et al. 2011Albano P.G., Sabelli B., Bouchet P. 2011. The challenge of small and rare species in marine biodiversity surveys: microgastropod diversity in a complex tropical coastal environment. Biodivers. Conserv. 20: 3223-3237. https://doi.org/10.1007/s10531-011-0117-x , Gofas et al. 2014Gofas S., Salas C., Rueda J.L., et al. 2014. Mollusca from a species-rich deep-water Leptometra community in the Alboran Sea. Sci. Mar. 78(4): 537-553. https://doi.org/10.3989/scimar.04097.27A ). Furthermore, the fine fractions can collect juvenile stages of species that are more difficult to collect when they reach adult sizes (e.g. species belonging to the superfamilies Nuculoidea and Tellinoidea live buried in the sediment).

The high biodiversity reported for Chella Bank and its adjacent bottoms contrasts with the old idea that bathyal areas in the deep Mediterranean Sea are poor from a biodiversity perspective (Bouchet and Taviani 1992Bouchet P., Taviani M. 1992. The Mediterranean deep-sea fauna: pseudopopulations of Atlantic species?. Deep-Sea Res. Pt A. 39: 169-184. https://doi.org/10.1016/0198-0149(92)90103-Z ). The studies carried out in the last two decades have shown that bathyal areas are not as poor as previously considered (Koutsoubas et al. 2000Koutsoubas D., Tselepides A., Eleftheriou A. 2000. Deep sea molluscan fauna of the Cretan Sea (Eastern Mediterranean): faunal, ecological and zoogeographical remarks. Senckenb. Marit. 30: 85-98. https://doi.org/10.1007/BF03042958 , Danovaro et al. 2010Danovaro R., Corinaldesi C., D’Onghia G., et al. 2010. Deep-sea biodiversity in the Mediterranean Sea: the known, the unknown, and the unknowable. PloS ONE. 5(8): e11832. https://doi.org/10.1371/journal.pone.0011832 ). The high richness found on Chella Bank, taking into account the small total area sampled with the van Veen grab (1.84 m²), is comparable to that found in other areas of the Alboran Sea: 156 mollusc species were collected from a single sampling station with a beam-trawl (over 889 m² sampled area) on Djibouti Bank (Gofas et al. 2014Gofas S., Salas C., Rueda J.L., et al. 2014. Mollusca from a species-rich deep-water Leptometra community in the Alboran Sea. Sci. Mar. 78(4): 537-553. https://doi.org/10.3989/scimar.04097.27A ), and 655 mollusc species were reported around the Alboran Island platform (Peñas et al. 2006Peñas A., Rolán E., Luque A.A., et al.2006. Moluscos marinos de la isla de Alborán. Iberus 24(1): 23-151.) from the supralittoral level down to 450 m depth using different sampling techniques. These are some examples of the extraordinary diversity of molluscs present in deep areas of the Alboran Sea when compared with other deep areas of the Mediterranean basin. For instance, Negri and Corselli (2016)Negri M.P, Corselli C. 2016. Bathyal Mollusca from the cold-water coral biotope of Santa Maria di Leuca (Apulian margin, southern Italy). Zootaxa 4186: 1-97. https://doi.org/10.11646/zootaxa.4186.1.1 reported only 97 species of molluscs in the thanatocoenosis of 18 samples retrieved with a box-corer at Santa Maria di Leuca (SE Italy). This high biodiversity of the Alboran Sea is probably due to several factors: (i) its location between the Lusitanian and Mauritanian biogeographical regions and the Mediterranean Sea (Ekman 1953Ekman S. 1953. Zoogeography of the sea. Sidgwick and Jackson, London, 417 pp., Caballero-Herrera et al. 2021Caballero‐Herrera J.A., Olivero J., von Cosel R., Gofas S. 2021. An analytically derived delineation of the West African Coastal Province based on bivalves. Divers. Distrib. 28 https://onlinelibrary.wiley.com/doi/10.1111/ddi.13454 ); (ii) its hydrological characteristics, which facilitate the transport of larvae from the Atlantic and the presence of persistent populations of species from the NE Atlantic that do not occur in other parts of the Mediterranean Sea (Gofas et al. 2011Gofas S., Moreno D., Salas C. 2011. Moluscos marinos de Andalucía. Servicio de Publicaciones e Intercambio Científico, Universidad de Málaga. Vol. I, pp 1-342; Vol. II, pp 343-798., Gallardo-Roldán et al. 2015Gallardo-Roldán H., Urra J., García T. et al. 2015. First record of the starfish Luidia atlantidea Madsen, 1950 in the Mediterranean Sea, with evidence of persistent populations. Cah. Biol. Mar. 56: 263-270., Rueda et al. 2021Rueda J. L., Gofas S., Aguilar R., et al. 2021. Benthic fauna of littoral and deep-sea habitats of the Alboran Sea: a hotspot of biodiversity. In: Báez J.C., Vázquez J.T, Camiñas J.A., Malouli M. (eds), Alboran Sea-Ecosystems and Marine Resources. Springer, Cham, pp. 285-358. https://doi.org/10.1007/978-3-030-65516-7_9 ); and (iii) the topographical heterogeneity of the bottom, which favours a wide diversity of habitats and, together with the particular hydrological features of the basin, promotes almost constant upwellings of nutrient-enriched deep waters, thereby enhancing nutrient supply to the ocean upper layers (Sarhan et al. 2000Sarhan T., García Lafuente J., Vargas M., et al. 2000. Upwelling mechanisms in the northwestern Alboran Sea. J. Mar. Syst. 23: 317-331. https://doi.org/10.1016/S0924-7963(99)00068-8 , Rueda et al. 2021Rueda J. L., Gofas S., Aguilar R., et al. 2021. Benthic fauna of littoral and deep-sea habitats of the Alboran Sea: a hotspot of biodiversity. In: Báez J.C., Vázquez J.T, Camiñas J.A., Malouli M. (eds), Alboran Sea-Ecosystems and Marine Resources. Springer, Cham, pp. 285-358. https://doi.org/10.1007/978-3-030-65516-7_9 , Vázquez et al. 2021Vázquez J.T., Ercilla G., Catalán M., et al. 2021. A geological history for the Alboran Sea region. In: Báez J.C., Vázquez J.T, Camiñas J.A., Malouli M. (eds), Alboran Sea-Ecosystems and Marine Resources. Springer, Cham, pp. 111-155. https://doi.org/10.1007/978-3-030-65516-7_5 ).

The highest values of mollusc diversity (i.e. species richness, Shannon-Wiener diversity) were observed in the group of samples from coral rubble (coral framework) bottoms (Group II), whereas the lowest values were found in those collected from the bathyal sedimentary bottoms around Chella Bank (Groups I and III). This type of complex bottoms, in which unusual species like Episcomitra angelesae and Mitrella templadoi (Fig. 3) were collected, provides a wide variety of ecological niches for species with different ecological requirements and biological interactions (e.g. substrate for attachment, feeding or parasitism and shelter) (Buhl-Mortensen et al. 2010Buhl-Mortensen L., Vanreusel A., Gooday AJ., et al. 2010. Biological structures as a source of habitat heterogeneity and biodiversity on the deep ocean margins. Mar. Ecol. 31: 21-50. https://doi.org/10.1111/j.1439-0485.2010.00359.x ). The results presented in this study confirm and support the importance of bottoms dominated with coral rubble as VMEs and the need for their conservation as they maintain a healthy ecosystem that is less susceptible to environmental changes and species loss, and allow degraded ecosystems to recover (de la Torriente et al. 2020de la Torriente A., Aguilar R., González-Irusta J.M., et al. 2020. Habitat forming species explain taxonomic and functional diversities in a Mediterranean seamount. Ecol. Indic. 118: 106747. https://doi.org/10.1016/j.ecolind.2020.106747 ).

From a biogeographical perspective, the malacofauna analysed here is dominated by species with a wide distributional range along the Atlantic Ocean and the Mediterranean Sea. The location of the Alboran Sea between these two basins and the proximity of the African and European biotic regions (Caballero-Herrera et al. 2021Caballero‐Herrera J.A., Olivero J., von Cosel R., Gofas S. 2021. An analytically derived delineation of the West African Coastal Province based on bivalves. Divers. Distrib. 28 https://onlinelibrary.wiley.com/doi/10.1111/ddi.13454 ) allow the confluence of species with different distribution patterns (Ekman 1953Ekman S. 1953. Zoogeography of the sea. Sidgwick and Jackson, London, 417 pp.). Almost 10% of the species are distributed in the Atlantic and also present in the Alboran Sea but absent in the rest of the Mediterranean, whereas ca. 8% are present in the Mediterranean and Ibero-Moroccan Gulf, and only ca. 4% are strictly Mediterranean. This biogeographical pattern is similar to that observed for molluscs from other coastal and circalittoral environments in the Alboran Sea (Rueda et al. 2009Rueda J.L., Gofas S., Urra J., Salas C. 2009. A highly diverse molluscan assemblage associated with eelgrass beds (Zostera marina L.) in the Alboran Sea: Micro-habitat preference, feeding guilds and biogeographical distribution. Sci. Mar. 73: 679-700. https://doi.org/10.3989/scimar.2009.73n4679 , Marina et al. 2012Marina P., Urra J., Rueda J.L., Salas C. 2012. Composition and structure of the molluscan assemblage associated with a Cymodocea nodosa bed in south-eastern Spain: seasonal and diel variation. Helgol. Mar. Res. 66: 1-15. https://doi.org/10.1007/s10152-012-0294-3 , Gofas et al. 2014Gofas S., Salas C., Rueda J.L., et al. 2014. Mollusca from a species-rich deep-water Leptometra community in the Alboran Sea. Sci. Mar. 78(4): 537-553. https://doi.org/10.3989/scimar.04097.27A ). According to these results, the Levantine Intermediate Water, considered to be the second “barrier” (after the sill of Gibraltar) for the incoming deep fauna in the Mediterranean (Bouchet and Taviani 1992Bouchet P., Taviani M. 1992. The Mediterranean deep-sea fauna: pseudopopulations of Atlantic species?. Deep-Sea Res. Pt A. 39: 169-184. https://doi.org/10.1016/0198-0149(92)90103-Z ), does not seem to be a permanent barrier to the dispersion of some Atlantic bathyal fauna larvae. The most striking feature of the molluscan fauna, however, is the occurrence of a few species with planktotrophic larval development for which Chella Bank is their sole recorded locality in the Mediterranean (Episcomitra angelesae, Mitrella templadoi) or which are extremely rare elsewhere (Mathilda spp.) (Fig. 3).

The in-depth knowledge on the composition of the fauna is important in an area designated as an MPA, especially in deep and poorly explored areas of the Alboran Sea, which has been identified as a biodiversity hotspot for European waters (Templado 2011Templado J. 2011. La diversidad marina en España. In: Viejo J.L. (ed), Biodiversidad: aproximación a la diversidad botánica y zoológica en España. Mem. R. Soc. Esp. Hist. Nat. 9: 343-362., Rueda et al. 2021Rueda J. L., Gofas S., Aguilar R., et al. 2021. Benthic fauna of littoral and deep-sea habitats of the Alboran Sea: a hotspot of biodiversity. In: Báez J.C., Vázquez J.T, Camiñas J.A., Malouli M. (eds), Alboran Sea-Ecosystems and Marine Resources. Springer, Cham, pp. 285-358. https://doi.org/10.1007/978-3-030-65516-7_9 , Mateo Ramírez et al. 2021Mateo-Ramírez, Á., Marina P., Moreno D., et al. 2021. Marine Protected Areas and Key Biodiversity Areas of the Alboran Sea and Adjacent Areas. In: Báez, J.C., Vázquez, JT., Camiñas, J.A., Malouli Idrissi, M. (eds) Alboran Sea - Ecosystems and Marine Resources. Springer, Cham, pp. 819-923. https://doi.org/10.1007/978-3-030-65516-7_25 ). Although the present study has contributed significantly to the knowledge of molluscs from Chella Bank and its adjacent bottoms, it probably does not yet provide a suitable representation of the malacofauna of some areas of this SCI, and it is expected that the number of species is still higher than is reported here. A high sampling effort in the shallower areas of the bank, where coralligenous formations and maërl beds occur, is suggested for future expeditions in order to improve the knowledge of this still poorly studied habitat in the Alboran Sea.

The high environmental heterogeneity and habitat diversity present in the SCI “Sur de Almería - Seco de los Olivos” (de la Torriente 2014de la Torriente A., Aguilar R., Serrano A., et al. 2014. Sur de Almería - Seco de los Olivos. Proyecto LIFE+ INDEMARES. Fundación Biodiversidad del Ministerio de Agricultura, Alimentación y Medio Ambiente, Madrid, pp 102., 2018de la Torriente A., Serrano A., Fernández-Salas L.M., et al. 2018. Identifying epibenthic habitats on the Seco de los Olivos Seamount: Species assemblages and environmental characteristics. Deep-Sea Res. Pt I. 135: 9-22. https://doi.org/10.1016/j.dsr.2018.03.015 ) explains the extraordinary list of molluscans reported, showing a good representation of the bathyal molluscans from the Alboran Sea. This list provides additional information, especially for the microbenthic fauna, which significantly increases the ecological importance of conservation in this MPA. It is important to highlight the presence of species which are hard to find in mollusc studies because of their low-density occurrence in marine ecosystems. This could be closely related to the existence of VMEs (de la Torriente 2018de la Torriente A., Serrano A., Fernández-Salas L.M., et al. 2018. Identifying epibenthic habitats on the Seco de los Olivos Seamount: Species assemblages and environmental characteristics. Deep-Sea Res. Pt I. 135: 9-22. https://doi.org/10.1016/j.dsr.2018.03.015 , 2020de la Torriente A., Aguilar R., González-Irusta J.M., et al. 2020. Habitat forming species explain taxonomic and functional diversities in a Mediterranean seamount. Ecol. Indic. 118: 106747. https://doi.org/10.1016/j.ecolind.2020.106747 ), some of them within the Habitats List of the Barcelona Convention in the framework of the Mediterranean Action Plan of the United Nations Environment Programme (UNEP/IUCN) (Mateo Ramírez et al. 2021Mateo-Ramírez, Á., Marina P., Moreno D., et al. 2021. Marine Protected Areas and Key Biodiversity Areas of the Alboran Sea and Adjacent Areas. In: Báez, J.C., Vázquez, JT., Camiñas, J.A., Malouli Idrissi, M. (eds) Alboran Sea - Ecosystems and Marine Resources. Springer, Cham, pp. 819-923. https://doi.org/10.1007/978-3-030-65516-7_25 ). The present study will also increase knowledge of the deep-sea fauna of the Alboran Sea, providing some baseline data for further environmental evaluation and conservation of habitats under the EU Marine Strategy Framework Directive (Directive 2008/56/EC) and the Directive on Establishing a Framework for Maritime Spatial Planning (2014/89/EU).