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Article

New Deep-Sea Molluscan Records from Mallorca Channel Seamounts (North-Western Mediterranean)

1
Centre Oceanogràfic de les Balears, Instituto Español de Oceanografía (IEO–CSIC), 07015 Palma, Spain
2
Centro Oceanográfico de Cádiz, Instituto Español de Oceanografía (IEO–CSIC), 11006 Cádiz, Spain
3
Departament Recursos Vius, Institut de Ciències del Mar (ICM-CSIC), 08003 Barcelona, Spain
4
Laboratori de Genètica, Departament de Biologia, Universitat de les Illes Balears, 07122 Palma, Spain
5
Centro Oceanográfico de Málaga, Instituto Español de Oceanografía (IEO-CSIC), 29640 Fuengirola, Spain
*
Author to whom correspondence should be addressed.
Diversity 2022, 14(11), 928; https://doi.org/10.3390/d14110928
Submission received: 17 October 2022 / Revised: 27 October 2022 / Accepted: 27 October 2022 / Published: 29 October 2022
(This article belongs to the Special Issue Diversity and Ecology of Marine Benthic Communities)

Abstract

:
Seamounts are globally important and essential ecosystems for supporting and maintaining marine biodiversity. In the Mallorca Channel, three prominent seamounts are present: Ausias March, Ses Olives and Emile Baudot. Currently, this area is being evaluated for inclusion in the Natura 2000 network. For this objective three surveys were conducted in the seamounts of the Mallorca Channel during July 2018 and July 2020. Samples of macro-invertebrates obtained in the deep sea revealed a rich fauna of Mollusca (68 species belonging to 40 families). New Mollusca occurrences included: four species of Gastropoda: Colus jeffreysianus, Cantrainea peloritana, Fusiturris similis, Gymnobela abyssorum, and seven species of Bivalvia: Pododesmus squama, Allogramma formosa, Asperarca nodulosa, Cetomya neaeroides, Spondylus gussonii, Haliris granulata and Policordia gemma. Where possible, the identification of these species was confirmed using the DNA barcoding method (sequencing of the cytochrome c oxidase subunit I). This study contributes towards filling the gap in knowledge of deep-sea mollusc fauna of the north-western Mediterranean.

1. Introduction

In the Mediterranean, over 242 seamounts have been recorded [1,2]. Although seamounts are globally important and deemed essential ecosystems for supporting and maintaining marine biodiversity [3,4,5], much of these seamounts remain poorly studied or unexplored [6]. This gap needs to be filled in order to discover the potential contribution of these systems to deep Mediterranean biodiversity and/or to identify vulnerable marine ecosystems [7].
This is the case of the Mallorca Channel (Balearic Islands, western Mediterranean), where three prominent seamounts are present, of between 86 and 1005 m in depth: Ses Olives, Ausias March and Emile Baudot. This area is located in the Eastern and Balearic demarcation (LEBA) one of five Spanish marine demarcations of the Marine Strategy Framework Directive (MSFD), 2008/56/EC [8]. There are relatively few studies on these seamounts. Some studies have focused on specifics zoological groups, such as Porifera [9,10] or Cnidaria [11]. The first habitat/faunistic studies were carried out by OCEANA [12,13]. All these studies suggest their high ecological value, as biological hotspots, and for this reason the three seamounts have recently received scientific attention to preserve the deep-sea ecosystem of the Mediterranean.
Currently, these seamounts are being evaluated within the LIFE IP INTEMARES project (https://intemares.es/en/the-project/life-integrated; accessed on 11 September 2022) for their inclusion in the Natura 2000 Network (proposed Sites of Community Importance, pSCIs) (LIFE IP INTEMARES project). For that, it is necessary to improve the scientific knowledge on the presence of areas of ecological interest that host vulnerable and protected habitats and species. Recent studies have already highlighted the ecological importance of these seamounts, where up to 547 taxa and 29 categories of benthic habitats have been found [14]. Biodiversity studies on unexplored areas, such as seamounts, lead, in most cases, to the discovery of new species for science [15], to new species records [16] or to an increase in species distribution knowledge (geographical and/or bathymetric) [17].
Molluscans are an important component of the seamount macrobenthos, being a large part of the abundance and biomass in any marine assemblage [18,19]. Molluscs are one of the most species-rich phyla inhabiting the Mediterranean waters [20]. In fact, the Mediterranean malacofauna is considered the best known in the world [21], with 2113 species described up to 2010 [22]. Recent studies in Mediterranean seamounts have revealed that these ecosystems can host a high biodiversity of molluscs [14,17,23,24].
In 2017, Gofas et al. [18] published an update of the Spanish marine mollusc master list for compliance with the requirements of the MSFD [25,26]. These valuable and laborious biodiversity updates provide basic knowledge for effective marine conservation. Therefore, this type of work, like future contributions to the list, represents a link between biodiversity studies and conservation, highlighting the important task of understanding regional biodiversity patterns and its ecology, as O’Hara et al. [27] observed, “to conserve marine biodiversity, we must first understand the spatial distribution and status of at-risk biodiversity” and be able to conserve it through effective management programs, or/and award conservation status, such as SCI and Special Areas of Conservation (SAC), within the Natura 2000 Network. The checklist of Gofas et al. [18] highlights the gap in knowledge in the mollusc fauna of the Balearic Islands, as most of the records underlying the 1165 reported species in the LEBA demarcation of the MSFD (East coast of Spain and Balearic Islands) were from the mainland.
The aim of the present study was to improve knowledge of north-western Mediterranean mollusc diversity, by adding information on the Mallorca Channel (Balearic Islands) seamounts, where this Phylum has been poorly characterized. To do so, where possible, identification of species was performed through both morphological characterization and molecular analyses.

2. Materials and Methods

2.1. Study Area

The Mallorca Channel corresponds to a seaway between the Ibiza and Mallorca islands, at the central sector of the Balearic Promontory. This promontory, of structural origin, is located in the middle of the western Mediterranean (Figure 1). It is characterized by the presence of a variety of morphological features namely seamounts, scarps and depressions [28,29]. Three seamounts called Ses Olives, Ausias March and Emile Baudot, are located between 86 and 1005 m depth. They are 375, 264, 600 m high, respectively, 10 to 17 km long and up to 77° of slope. They have tabular summits and irregular basal geometry, remarkably elongated in NE-SW trends [30]. While Ses Olives and Ausias March are of continental origin, the Emile Baudot is of volcanic origin [31].

2.2. Sample Collection

Specimens of deep-sea molluscs were obtained during the sampling operations of the INTEMARES project. The project aimed to improve the scientific knowledge on habitats, species, and human activities to include these seamounts in the European network of marine Natura 2000 sites. For this objective, three INTEMARES surveys were conducted in the seamounts of the Mallorca Channel in July 2018, October 2019 and July 2020 on board the R/V Ángeles Alvariño. Sampling gears included a Jennings type beam trawl (BT) of 2 and 0.5 m horizontal and vertical openings, respectively, equipped with a 5 mm mesh size cod-end, and a rock dredge (DR) with 0.77 and 0.35 m horizontal and vertical openings with a 6 cm mesh size code-end. A total of 85 samples between 99 and 764 m depth, and 55 samples between 89 and 1191 m depth, were collected using BT and DR, respectively. Samples were taken during daytime and had 5–15 min duration at around 2 knots for BT and 1 knot for DR (Table 1) [14]. All samples were sorted and identified as species or to the lowest possible taxonomic category. Molluscs with uncertain identification on board were preserved in absolute ethanol for further analyses in the laboratory.

2.3. Sedimentological Analysis

Samples of surface sediments, collected using Shipek and Box–Corer grabs during the above-mentioned INTEMARES surveys, were also analyzed [14]. The sedimentological analysis for grain size distribution was carried out on 10–15 g of sediment pre-treated with 10% H2O2 to remove organic matter and sodium hexametaphosphate as a dispersing agent. Samples were wet sieved to separate the coarse fraction (gravel) using a 2 mm mesh size sieve. Particles < 2 mm (sand, silt, and clay) were determined by using a laser diffraction analyzer (Mastersizer 3000, Malvern® Panalytical, Centro Oceanográfico de Málaga, IEO-CSIC). The textural classification of the sediments was based on Folk [32] ternary diagrams and also the organic matter was obtained [33].

2.4. Morphological Identification

Only live-taken specimens are considered. Individuals were analyzed under a stereomicroscope Leica M165C equipped with a camera Leica MC170. Identification was done using specific taxonomic guides [34,35,36,37]. The taxonomic names of the species were checked in MolluscaBase database [38]. The specimens were deposited in the Biological Reference Collections (CBMR) at the Institut de Ciències del Mar (ICM-CSIC) under serial code shown in the description of the examined material.

2.5. Molecular Identification

Genomic DNA was extracted from a small piece of tissue using the DNeasy Blood and Tissue Extraction kit (Qiagen, West Sussex, UK). Polymerase chain reaction (PCR) was used to amplify the mitochondrial DNA barcoding fragment (cytochrome c oxidase subunit I, COI) with the universal primers LCO1490/HCO2198 proposed by Folmer et al. [39].
PCR was performed in 25 μL volume (17.2 μL ddH2O, 2.5 μL Mangobuffer (Bioline, Toronto, ON, Canada), 1 μL DNTPs, 1.75 MgCl2, 0.5 μL BSA, 0.5 μL each primer (each 10 pmol), 0.05 μL TAQ (Bioline) and 1 μL DNA). The PCR thermal profile was: initial stage of 96 °C for 5 min; then 35 cycles at 94 °C for 60 s, 50 °C for 60 s and 72 °C for 60 s, followed by a final extension at 72 °C for 10 min. PCR products were purified using the QIAquickR PCR Purification Kit (QIAGEN). Both heavy and light strands were sequenced on an ABI 3130 sequencer (Applied Biosystems).
Sequences were imported into BioEdit 7.0.5.2. [40] and checked for quality and accuracy with nucleotide base assignment. The DNA sequences obtained were deposited in the GenBank database (http://www.ncbi.nlm.nih.gov/genbank/; accessed on 2 February 2021).
Sequences were validated using the BLAST function from the GenBank database (https://blast.ncbi.nlm.nih.gov/Blast.cgi; accessed on 15 March 2021 [41]) as well as the IDENTIFICATION function from the Barcode of Life Data System BOLD system (https://www.boldsystems.org; accessed 21 March 2021 [42]).

3. Results

3.1. Mollusca Biodiversity

A total of 2509 individual molluscs were collected during the INTEMARES surveys in the seamounts of the Mallorca Channel. These individuals belonged to 68 species, of which 34 species were bivalves and 34 species were gastropods (Table 2). Up to 15 of these species were present in all three seamounts. In Ses Olives seamount, 27 species were identified, 46 species were identified in Ausias March seamount, and 43 species in the Emile Baudot seamount. Figure 2 shows photographs of some of the species that form part of the mollusc community of the seamounts of the Mallorca Channel.

3.2. New Occurrence from Mallorca Channel Seamount

Up to 11 species of Phylum Mollusca constitute new records that improve the scientific knowledge on Mallorca Channel seamounts in the western Mediterranean; 4 species belong to the Class Gastropoda and 7 species to the Class Bivalvia (Table 2; Figure 3).

3.3. Systematic Account

Phyllum Mollusca Linnaeus, 1758
Class Gastropoda Cuvier, 1797
Family Colidae Gray, 1857
Colus jeffreysianus (P. Fischer, 1868)
Material examined: R/V Ángeles Alvariño; St. BT088, 38°45.480′ N 002°27.750′ E, Emile Baudot seamount, 574 m depth, A22B_0718, 1 specimen. Deposited under the serial code ICMCBR000393.
External morphology: Shell large with sculpture attenuated, consisting only of fine spiral grooves and protoconch of more than 2 whorls, with a small nucleus. Within the genus Colus, protoconch morphology, such as the number of whorls and the way they are whorled, may be regarded as being specific.
Distribution: Colus jeffreysianus lives in deep water from 400 to 2100 m from South Iceland and Norway, the Shetland Islands and the Faroes, the Kattegat and SW Skagerrak and off the British Isles. Further southwards it is found on the continental shelf of the Bay of Biscay, the Iberian Peninsula and the western Mediterranean Sea [43]. It is not common anywhere, but less common in the east English Channel and southern North Sea than elsewhere [44].
Remarks: Records have been reported in the north-western Mediterranean was probably based on fossil specimens according to Gofas et al. [18]. We provide a live specimen, in which the operculum was preserved (Figure 3A), collected on coarse slit in Emile Baudot seamount at 574 m depth. Identification has been based on another two specimens whose protoconch were preserved and had more than 2 whorls. The present record is the first record for the Balearic Islands.
Genetics: PCR amplification of C. jeffreysianus did not work.
Family Colloniidae Cossmann, 1917
Cantrainea peloritana (Cantraine, 1835)
(Figure 3B1,B2)
Material examined: R/V Ángeles Alvariño; St. BT088, 38°45.480′ N 002°27.750′ E, A22B_0718, Emile Baudot seamount, 574 m depth, 07/2018, 1 specimen. Deposited under the serial code ICMCBR000443.
External morphology: This species is remarkable for the uniform white colour, the concavity at the upper part of the whorls, the median angle or carination, and the two or three keels upon the last whorl. Mediterranean shape is smaller.
Distribution: C. peloritana species was collected in northern Spain and western Portugal, cited by Nobre [45] and Locard [46] at depths ranging from 135 to 512 m. In the Atlantic Ocean it has been documented in Canary Islands [47] at 470–485 depth, Azores at 454 m depth [48] and in the northern part of the Bay of Biscay, at 630–650 m depth [49]. In the Mediterranean, this species has been reported on deep-sea coral banks in Sardinia (Capo Carbonara) and Central Tyrrhenian Sea (coast of Latium), at 300-600 m depth [48]. The few specimens reported in the Mediterranean classify this species as rare in this area [38].
Remarks: Two individuals were collected at the Emile Baudot seamount at 574 and 508 m depth on fine sand and coarse silt. The presence of C. peloritana in the western Mediterranean is confirmed. The present record also represents the first record of the species in the north-western Mediterranean.
Genetics: PCR amplification of C. peloritana did not work.
Family Fusiturridae Abdelkrim, Aznar-Cormano, Fedosov, Kantor, Lozouet, Phuong, Zaharias & Puillandre, 2018
Fusiturris similis (Bivona Ant. in Bivona And., 1838)
Material examined: R/V Ángeles Alvariño; St. BT093, 38°48.400′ N 001°48.030′ E, Ausias March, 376 m depth, A22B_1019, 1 specimen; St. BT101, 38°48.700′ N 001°42.880′ E, Ausias March, 320 m depth, A22B_1019, 1 specimen; St. BT104, 38°45.620′ N 001°50.770′ E, Ausias March, 116 m depth, A22B_1019, 2 specimens. Deposited under the serial code ICMCBR000450.
External morphology: Shell elongated and fusiform shape, up to 50 mm. Very narrow and turriculate with numerous narrow axial ribs with three reddish-brown bands.
Distribution: F. similis can be found characterizing deep rubble on the Alborán shelf [24,50] as well as in bathyal muds and sediment-covered rocky bottoms of the Seco de los Olivos seamount [13]. Gofas and Zenetos [51] considered F. similis a tropical or subtropical species, distributed from the Ibero-maroccan Atlantic coasts, the Sahara and Morocco to the Alborán Sea, and Algeria and Tunisian coasts in the south-west Mediterranean. This species has been also collected in Amanay seamount in the Canary Islands (Atlantic Ocean) [52].
Remarks: Four specimens were collected at the Ausias March seamount between 120-370 m depth on sand or coarse silt. The present record extends the distribution of the species to the north-western Mediterranean.
Genetics: A fragment of 594 base pairs (bp) of the COI fragment was sequenced and deposited in GenBank under the accession number: OP329214. High similarity values (98.82%) were detected in both genetic databases, GenBank and BOLD system, from sequences of F. similis published by Cunha et al. [53]. Therefore, this result supported the morphological identification of F. similis.
Family Raphitomidae Bellardi, 1875
Gymnobela abyssorum (Locard, 1897)
(Figure 3D,D1)
Material examined: R/V Ángeles Alvariño; St. BT005, 38°58.620′ N 001°59.880′ E, Ses Olives seamount, 259 m depth, A22B_0718, 1 specimen; St. BT020, 38°56.100′ N 001°58.520′ E, Ses Olives seamount, 275 m depth, A22B_0718, 1 specimen; St. BT088, 38°45.480′ N 002°27.750′ E, Emile Baudot seamount, 574 m depth, A22B_0718, 1 specimen. Deposited under the serials code ICMCBR000385, ICMCBR000446, ICMCBR000453, respectively.
External morphology: Shell light brown-brownish white. The sculpture consists of short, low and broad axial ribs and a spiral sculpture of rather equal-sized spiral lines.
Distribution: This species inhabits circalittoral and bathyal muddy bottoms [34,54]. The upper bathyal in the northern part of the Bay of Biscay to the Ibero-Moroccan Gulf [55] and in the Alborán Sea (Mediterranean) [47]. Ortega and Gofas [47] gave the last new record for G. abyssorum in the Canary Islands.
Remarks: Three individuals were collected in Ses Olives and Emile Baudot seamounts on fine or coarse bottoms. The present record extends the distribution to the north-western Mediterranean.
Genetics: For this specimen a fragment of 540 bp was sequenced deposited in GenBank under the accession number: OP328907. Similarity values were different for genetic databases, for the BOLD system highest values with 94.6% and 92.92% were for sequences of Pagodibela meridionalis Hallan, Criscione, Fedosov & Puillandre, 2021 Pagodibela meridionals and Gymnobela sp. published by Criscione et al. [56] and Hallan et al. [57], respectively. While, for GenBank the highest values (from 94.6 to 91.7%) were for Pagodibela genus, and a high value (91.7%) was recorded for Gymnobela sp. published by Puillandre et al. [58]. Although molecular identification may be unclear for Gymnobela and Pagodibela genera, it is to know that Gymnobela is composed by a high number of species (around 94; http://www.marinespecies.org/; accessed on 1 September 2021) with an extended geographic distribution, while Pagodibela is a newly recognized genus from the tropical Indo-Pacific [56]. Considering this and the shell morphological characteristics, it is expected that the specimen studied corresponds to the Gymnobela genus.
Class Bivalvia
Family Anomiidae Rafinesque, 1815
Pododesmus squama (Gmelin, 1791)
(Figure 3E1,E2)
Material examined: R/V Ángeles Alvariño; St. BT022, 38°44.570′ N 001°46.250′ E, Ausias March seamount, 105 m depth, A22B_0718, 2 specimens; St. BT049, 38°43.330′ N 001°49.370′ E, Ausias March seamount, 124 m depth, A22B_1019, 1 specimen; St. BT055, 38°45.440′ N 001°47.560′ E, Ausias March seamount, 114 m depth, A22B_1019, 1 specimen. Deposited under the serials code ICMCBR000381, ICMCBR000386.
External morphology: It has radial striate but no riblets on the outside of the upper valve, attached muscle scars, thin and transparent mantle, and the tentacles are thin and narrowly rounded.
Distribution: This species inhabits 20-200 m depth of the continental shelf and it is distributed from Iceland, Norway and English Channel [36,59,60,61] to Morocco [62] and South Africa [63]. It is also distributed in the central [64] and eastern Mediterranean, cited in Marmara and Aegean Sea [65], and in the Alborán Sea off the coast of Morocco [37].
Remarks: The individuals collected in this study are the first records of the species in the north-western Mediterranean.
Genetics: A fragment of 432 bp was sequenced and deposited in GenBank under the accession number: OP347785. Similarity values observed in GenBank and BOLD system were similar (98.4%), and corresponded to an unpublished sequence of P. squama submitted by SweBol Marine invertebrates [59]. Thus, molecular results supported the morphological identification of P. squama.
Family Spondylidae Gray, 1826
Spondylus gussonii O. G. Costa, 1830
(Figure 3F1,F2)
Material examined: R/V Ángeles Alvariño; St. DR047, 38°43.840′ N 002°29.400′ E Emile Baudot seamount, 127 m depth, A22B_0720, 1 specimen. Deposited under the serial code ICMCBR000481.
External morphology: White, oval to pyriform shell shape with coarse spiny processes in the attachment area and right valve more irregularly sculptured. expanded posterior side, radial rows of minute, short tubular spines; thin commarginal lamellae more clearly visible towards the ventral margin.
Distribution: Bathyal species that inhabits attached to deep water coral or cemented in hard substrata [66]. Pons-Moya and Pons [67] cited S. gussonii in the Balearic Islands from partial or subfossil shells. The species is typical of the Mediterranean, with records also from the Bay of Biscay, Portugal and the archipelago of the Azores [68]. It has been reported in three Spanish demarcations of the MSFD, North Atlantic, South Atlantic and Strait and Alborán Sea [18], between 70–850 m depth, being common around 600 m [36].
Remarks: A single specimen was collected at Emile Baudot seamount, fixed to rock on rhodolith beds at 127 m depth. The new record provided in this study confirms the presence of the species in the Balearic Islands (north-western Mediterranean).
Genetics: PCR amplification of S. gussonii did not work.
Family Lyonsiellidae Dall, 1895
Allogramma formosa (Jeffreys, 1882)
Material examined: R/V Ángeles Alvariño; St. BT036, 38°57.190′ N001°56.110′ E, Ses Olives seamount, 619 m depth, A22B_1019, 1 specimen; St. B0109, 38°53.670′ N 001°55.370′ E, Ses Olives seamount, 715 m depth, A22B_1019, 1 specimen; St. BT0123, 38°58.270′ N 001°55.85′ E, Ses Olives seamount, 675 m depth, A22B_1019, 1 specimen. Deposited under the serial code ICMCBR000396.
External morphology: Sub-rectangular shell and broad, obliquely triangular, resilient cavity; possesses posterior radial ridges gnarled plus some weaker ones in middle part of shell; anterior wrinkles wavy running dorsoventrally; sparse rows of minute pustules, raised in short spines on posterodorsal area.
Distribution: Rare and fragile species, characteristic of the hypobathial mud [69]. A. formosa is distributed in the north-western Atlantic, from the Caribbean basin to south-eastern Brazil, in the north-eastern Atlantic off Guinea-Bissau, Canary Islands, Azores and Bay of Biscay [36,37,70,71]. In the Mediterranean it is distributed in the Levantine basin, from lower slope to abyssal depths [36,68,69,72,73], and in the Aegean Sea [74].
Remarks: Four specimens were collected at the Ausias March seamount between 619 and 715 m depth, in medium to coarse silt sediment. The record provided in this study represents the first record of the species in the north-western Mediterranean.
Genetics: A fragment of 573 bp was sequenced and deposited in GenBank under the accession number: OP328904. Low similarity values (<85%) were recorded in GenBank and BOLD system. The closest taxon was the Euciroidae family, with 80.57% and 76.15% similarity, for BOLD system and GenBank, respectively. There are no COI sequences available for any member of the Lyonsiellidae family. In this case, the molecular result cannot support the morphological identification, but it will be useful for future comparisons.
Family Arcidae Lamarck, 1809
Asperarca nodulosa (O. F. Müller, 1776)
(Figure 3H1,H2)
Material examined: R/V Ángeles Alvariño; St. DR014, 38°58.970′ N001°59.970′ E, Ses Olives seamount, 479–278 m depth, A22B_0718, 3 specimens; St. DR018, 38°57.360′ N 002°01.090′ E, Ses Olives seamount, 263-235 m depth, A22B_0718, 20 specimens; St. DR086, 38°40.650′ N 002°25.730′ E, Emile Baudot seamount, 337-309 m depth, A22B_0718, 1 specimen; St. BT001, 38°56.80′N 001°58.540′ E, Ses Olives seamount, 290 m depth, A22B_0718, 3 specimens; St. BT005, 38°58.620′ N 001°59.880′ E, Ses Olives seamount, 260 m depth, A22B_0718, 3 specimens; St DR057, 38°41.720′ N 002°21.880′ E, Emile Baudot seamount, 665–488 m depth, A22B_0720, 1 specimen. Deposited under the serials code ICMCBR000397, ICMCBR000398.
External morphology: A. nodulosa is large with subrectangular shell, flat mantle without siphons, lobes are attached to shell valves along the pallian line, peripheral to which is the mantle edge, roundish D-shaped outline with convex profile.
Distribution: North-east Atlantic (from Norway to Moroco) and the Gulf of Cádiz [75]. Inhabits from the tidal zone to a depth of 730 m [76], being also found at 4134 m depth [77], and the western Mediterranean from depths of 450–550 m [78].
Remarks: It was the most abundant species in the rocky outcrops with medium sand of Ausias March seamount. The specimens of the present study confirm the presence of this species in the Mallorca Channel.
Genetics: A fragment of 561 bp was sequenced and deposited in GenBank under the accession number: OP328905. The highest similarity value was found in BOLD system with 99.46% from an unpublished sequence of A. nodulosa (NBMM506-18; NTNU University Museum). While in GenBank the closest taxon (89.05%) was found with a sequence of A. secreta published by Plazzi et al. [78]. Thus, molecular results supported the morphological identification of A. nodulosa.
Family Poromyidae Dall, 1886
Cetomya neaeroides (Seguenza, 1877)
Material examined: R/V Ángeles Alvariño; St. DR018, 38°57.360′ N 002°01.090′ E, Ses Olives seamount, 263–235 m depth, A22B_0718, 1 specimen; St. BT028, 38°56.750′ N 002°01.160′ E, Ses Olives seamount, 449 m depth, A22B_1019, 1 specimen. Deposited under the serial reference: ICMCBR000389.
External morphology: Shell thin, white, semitransparent, ovate, slightly inequivalve. Sculpture of faint growth lines and densely set minute granules in radial row.
Distribution: Western Atlantic, from Virginia to Gulf of Mexico [79]; Eastern Atlantic: Portugal and south of the Iberian Peninsula [37], Canary Islands [80]; Mediterranean basin: eastern of Sardinia [81] and Greek waters [74]. This species lives in deep habitats. In the Atlantic it is found up to 2980 m depth [79], while in the Mediterranean it is distributed shallower, between 320–350 m depth [81].
Remarks: Specimens were collected in Ausias March seamount on rock and medium sand bottom. It represents the first record of the species in the Balearic Islands.
Genetics: A fragment of 573 bp of the COI fragment was sequenced and deposited in GenBank under the accession number: OP328906. Low similarity values (<80%) were recorded in GenBank and BOLD system. In this last, the closest taxon was the Poromyidae family with 74.95%, whilst in GenBank there are not available COI sequences for members of this family. In this case, the molecular result cannot support the morphological identification, but it will be useful for future comparisons.
Family Verticordiidae Stoliczka, 1870
Haliris granulata (Seguenza, 1860)
(Figure 3J1,J2)
Material examined: R/V Ángeles Alvariño; St. DR086, 38°40.650′ N 002°25.730′ E, Emile Baudot seamount, 337–309 m depth, A22B_0718, 1 specimen. St. BT175, 38°46.070′ N 002°30.150′ E, Emile Baudot seamount, 412 m depth, A22B_1019, 1 specimen; BT026, 38°47.160′ N 001°50.760′ E, Ausias March seamount, 127 m depth, A22B_0720, 1 specimen. Deposited under the serials code ICMCBR000411, ICMCBR000419.
External morphology: Shell solid, semitransparent, inequivalve, right valve being more convex than the left one, inequilateral, the beaks situated close to the anterior margin, sculpture of about 20 strong radial ribs.
Distribution: H. granulata inhabits in the circumlittoral seafloor at 195-200 m depth. North Atlantic and northeastern Atlantic in archipelagos of Madeira and Canary Islands [18,82,83]; Mediterranean basin: eastern Mediterranean from the Levantine Coast of Turkey [74,84]. The species is found on muddy bottoms. Most of records cited as syn. Verticordia granulata [83,85].
Remarks: The specimens collected were found at Ausias March seamount between 150-300 m depth and at Emile Baudot seamount around 400 m depth. These new records extend the bathymetry and geographic distribution of the species, representing its first record in the western Mediterranean.
Genetics: PCR amplification of H. granulata did not work.
Family Lyonsiellidae Dall, 1895
Policordia gemma (A. E. Verrill, 1880)
(Figure 3K1,K2)
Material examined: R/V Ángeles Alvariño; St. BT049, 38°43.330′ N 001°49.370′ E, Ausias March seamount, 124 m depth, A22B_1019, 1 specimen. Deposited under the serial code ICMCBR000424.
External morphology: Shell fragile, white, small, inequivalve, inequilateral, little inflated, shell and ornamented externally with about 15–30 axial threads faintly concentric growth lines present.
Distribution: P. gemma has a wide range of distribution cited along the north, south, east and west Atlantic [37,79,83]. In the Mediterranean, it has been found only off Ceuta and along the Alborán Sea [37,71].
Remarks: Only one specimen was found in the Ausias March seamount on medium sand, at 124 m depth. It represents the first record of the species in the north-western Mediterranean.
Genetics: PCR amplification of P. gemma did not work.

4. Discussion

At present, marine ecosystems face many threats, mainly due to anthropogenic pressures [86]. In addition to this, climate change is changing marine biodiversity on a global scale, and one of the problems is the loss of biodiversity [87] because marine species respond by shifting ranges poleward and/or into deeper depths [88,89].
Numerous scientific projects and studies are being carried out to monitoring biodiversity and guarantee the health and functioning of the oceans [27,90]. The INTEMARES project is part of this objective, aiming to ensure the long-term survival of the most endangered species and habitats in Europe (Natura 2000 Network), with the Mallorca Channel seamounts currently being studied for inclusion in the Natura 2000 Network [14].
The research presented is one of the results of the INTEMARES project and has focused on the study of the biodiversity of the Mollusca. The material collected during INTEMRES surveys brings interesting information on the very rich deep-water mollusc fauna occurring off the three seamounts of the Mallorca Channel. Obtaining a total of 68 species of the group (Figure 2; Table 2), of which 11 species have been collected for the first time in the north-western Mediterranean: seven bivalves and four gastropods (Figure 3; Table 2).
The most diverse mollusc groups were the bivalve superfamily belonging to Pectinoidea with 12 species (Figure 2). In agreement with Dijkstra and Gofas [91], seamounts have extensive areas of hard bottom (Table 1), which implies a predominance of epifauna, and under these conditions, Pectinoidea are one of the best represented bivalve families being one of the bivalve taxa, which is successful in deep-sea environments [91]. The next most diverse families were Cuspidariidae and Arcidae, with four and four species, respectively, and the remaining Mollusca families ranged from one to three species.
The number of new occurrences of molluscs was higher than those reported in previous studies conducted in same area, such as the OCEANA report [12,13]. This difference may be due to the sampling methodology (remote operated vehicle ROV transects) applied in the surveys. All records in the present study were based on beam-trawl and rock dredge samples, although non-invasive methodologies such as ROV and photogrammetric sled were also used in two of the surveys [14], (A22B_0820, not included in the present study). However, the mollusc group could not be identified with these methodologies. At the same time, thanks to the collected live specimens, molecular sequences could be obtained.
Of all the species studied, only six were successfully sequenced for the COI fragment, which highlights the need to test specific primers for molluscs. Integrative species-level identification, based on morphological and molecular features, was possible for three species: Fusiturris similis, Pododesmus squama and Asperarca nodulosa. On the other hand, the low percentage of similarity (<85%) detected for these specimens morphologically identified as Allogramma formosa and Policordia gemma suggest that public genetic databases such as GenBank and BOLD system are far from being complete in the Mediterranean, which makes the detection of these species impossible or leads to incorrect records of closely related species. Therefore, it is necessary to assemble a comprehensive barcode register for the mollusc fauna in the Mediterranean that will be useful for future comparisons in order to have an accurate record of the diversity of this widespread phylum. In addition, it will be useful for new monitoring techniques based on molecular approaches such as environmental DNA (DNA metabarcoding), which require complete genome libraries for a successful application.
The new occurrences of molluscs in the north-western Mediterranean are based on Spanish molluscs from the master list by Gofas et al. [18], the most updated list of molluscs in the area of the study. This list was published following compliance with the requirements of the Marine Strategy Framework Directive (MSFD) of the European Union [25], following descriptor 1 (Biodiversity) of the 11 descriptors in Annex I of the MSFD. Scientific work that provides new information on species distribution and habitats is of great scientific significance for further management and conservation studies of marine areas. The present study provides useful information on the biodiversity of seamounts and contributes towards filling the gap in knowledge in deep-sea mollusc fauna, which adds value to the proposal for their inclusion in the Natura 2000 network.

Author Contributions

Conceptualization, E.M.-H. and E.M.; Methodology on board, E.M.-H., S.R.-A., O.S.-G., F.O., C.L.-R., M.T.F., J.T.V. and E.M.; Species identification, M.R. and E.M.-H.; Molecular analyze, S.R.-A. Sediment analysis, C.L.-R. and O.S.-G.; Writing—original draft and editing, E.M.-H.; Writing—molecular section, S.R.-A.; Review, All authors; Supervision, E.M.-H. and S.R.-A.; Funding acquisition, E.M. All authors have read and agreed to the published version of the manuscript.

Funding

This research was performed in the scope of the LIFE IP INTEMARES project, coordinated by the Biodiversity Foundation of the Ministry for the Ecological Transition and the Demographic Challenge. It receives financial support from the European Union’s LIFE program (LIFE15 IPE ES 012). S.R.-A. is supported by postdoctoral contract, co-funded by the Regional Government of the Balearic Islands and the European Social Fund.

Institutional Review Board Statement

Not applicable.

Data Availability Statement

Data are stored in the database of the Instituto Español de Oceanografía (IEO-CSIC) for the INTEMARES project, some of which is available at the IEO marine geospatial information viewers and services: http://www.ieo.es/en/ideo.

Acknowledgments

We thank all participants who helped us at different stages of this work: the captains and the crews of the R/V Ángeles Alvariño during the surveys INTEMARES_A22B_0718, INTEMARES_A22B_1019 and INTEMARES_A22B_0720. Also grateful to Serge Gofas at University of Málaga, who helped us in the identification of some specimens. We also thank the ICM’s Biological Reference Collections Service. Thanks to the anonymous reviewers.

Conflicts of Interest

The authors declare no conflict of interest.

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Figure 1. Maps showing: (A) western Mediterranean, with the two Mediterranean Spanish demarcations of the MSFD: Straits and Alborán demarcation (ESAL) and Eastern and Balearic demarcation (LEBA), separated with dashed line; (B) general view of the total area of study, Mallorca Channel (Balearic Islands); (C) Ses Olives; (D) Ausias March; and (E) Emile Baudot seamounts. Maps CE show the codes of the sampling stations with new occurrences of molluscans, developed during the INTEMARES surveys. The serial reference is shown above the track: (BT) beam trawl and (DR) rock dredge.
Figure 1. Maps showing: (A) western Mediterranean, with the two Mediterranean Spanish demarcations of the MSFD: Straits and Alborán demarcation (ESAL) and Eastern and Balearic demarcation (LEBA), separated with dashed line; (B) general view of the total area of study, Mallorca Channel (Balearic Islands); (C) Ses Olives; (D) Ausias March; and (E) Emile Baudot seamounts. Maps CE show the codes of the sampling stations with new occurrences of molluscans, developed during the INTEMARES surveys. The serial reference is shown above the track: (BT) beam trawl and (DR) rock dredge.
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Figure 2. Some molluscans species collected from Ses Olives, Ausias March and Emile Baudot seamounts in the Mallorca Channel (Balearic Islands): (A) Fusinus pulchellus; (B) Epitonium celesti; (C) Pagodula echinata; (D) Capulus ungaricus; (E) Orania fusulus; (F) Trophonopsis muricata; (G) Murexul aradasii; (H) Japonacteon pusillus; (I) Tetrarca tetragona; (J) Bathyarca philippiana; (K) Tropydomia abbreviata; (L) Cuspidaria cuspidata; (M) Cardiomya costellata; (N) Cuspidaria rostrata; (O) Ledella messanensis; (P1,P2) Similipecten similis; (Q1,Q2) Palliolum incomparabile; (R) Gari costellata; (S1,S2) Tolochlamys multistriata; (T1,T2) Manupecten pesfelis; (U1,U2) Karnekampia sulcata; and (W1,W2) Pseudamussium clavatum. Images not to scale.
Figure 2. Some molluscans species collected from Ses Olives, Ausias March and Emile Baudot seamounts in the Mallorca Channel (Balearic Islands): (A) Fusinus pulchellus; (B) Epitonium celesti; (C) Pagodula echinata; (D) Capulus ungaricus; (E) Orania fusulus; (F) Trophonopsis muricata; (G) Murexul aradasii; (H) Japonacteon pusillus; (I) Tetrarca tetragona; (J) Bathyarca philippiana; (K) Tropydomia abbreviata; (L) Cuspidaria cuspidata; (M) Cardiomya costellata; (N) Cuspidaria rostrata; (O) Ledella messanensis; (P1,P2) Similipecten similis; (Q1,Q2) Palliolum incomparabile; (R) Gari costellata; (S1,S2) Tolochlamys multistriata; (T1,T2) Manupecten pesfelis; (U1,U2) Karnekampia sulcata; and (W1,W2) Pseudamussium clavatum. Images not to scale.
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Figure 3. New deep-see molluscans records from Ses Olives, Ausias March and Emile Baudot seamounts in the Mallorca Channel (Balearic Islands): (A) Colus jeffreysianus; (B1,B2) Cantrainea peloritana; (C) Fusiturris similis; (D,D1) Gymnobela abyssorum; (E1,E2) Pododesmus squama; (F1,F2) Spondylus gussonii; (G) Allogramma formosa; (H1,H2) Asperarca nodulosa; (I) Cetomya neaeroides; (J1,J2) Haliris granulata; and (K1,K2) Policordia gemma. Images not to scale.
Figure 3. New deep-see molluscans records from Ses Olives, Ausias March and Emile Baudot seamounts in the Mallorca Channel (Balearic Islands): (A) Colus jeffreysianus; (B1,B2) Cantrainea peloritana; (C) Fusiturris similis; (D,D1) Gymnobela abyssorum; (E1,E2) Pododesmus squama; (F1,F2) Spondylus gussonii; (G) Allogramma formosa; (H1,H2) Asperarca nodulosa; (I) Cetomya neaeroides; (J1,J2) Haliris granulata; and (K1,K2) Policordia gemma. Images not to scale.
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Table 1. Information on the stations where new records of Mollusca were found in the seamounts of the Mallorca Channel (Balearic Islands, western Mediterranean): Ses Olives (SO), Ausias March (AM) and Emile Baudot (EB). Samples were collected with beam-trawl (BT), rock dredge (DR) during the INTEMARES surveys developed between 2018 and 2020. Depth range and mean depth for DR and BT stations, respectively are also shown.
Table 1. Information on the stations where new records of Mollusca were found in the seamounts of the Mallorca Channel (Balearic Islands, western Mediterranean): Ses Olives (SO), Ausias March (AM) and Emile Baudot (EB). Samples were collected with beam-trawl (BT), rock dredge (DR) during the INTEMARES surveys developed between 2018 and 2020. Depth range and mean depth for DR and BT stations, respectively are also shown.
SettingHauling
SurveySampling MethodSample CodeLatitude (N)Longitude (E)Latitude (N)Longitude (E)Depth (m)AreaHabitat
A22B_0718BTBT00138°56.800′001°58.540′38°57.380′38°57.3800′290SOFine sand
BT00538°58.620′001°59.880′38°58.120′001°59.240′259SOFine sand
BT02038°56.100′001°58.520′38°56.100′001°57.730′275SOFine sand
BT02238°44.570′001°46.250′38°44.420′001°45.890′105AMCoarse sand
BT08838°45.480′002°27.750′38°44.740′002°27.440′574EBCoarse silt
DRDR01438°58.970′001°59.970′38°58.740′001°59.980′479–278SOFine sand
DR01838°57.360′002°01.090′38°57.410′002°00.830′263–235SORocky outcrops with medium sand
A22B_1019BTBT01038°56.790′001°57.710′38°56.670′001°57.650′288SOFine sand
BT02838°56.750′002°01.160′38°57.290′002°01.320′449SOCoarse sand
BT03638°57.190′001°56.110′38°57.990′001°56.670′619SOMedium silt
BT04938°43.330′001°49.370′38°43.330′001°49.370′124AMMedium sand
BT05538°45.440′ 001°47.560′38°45.560′001°47.780′114AMMedium sand
BT09338°48.400′001°48.030′38°48.890′001°50.450′376AMVery fine sand
BT10138°48.700′001°42.880′38°47.830′001°42.400′320AMCoarse silt
BT10438°45.620′001°50.770′38°46.090′ 001°51.140′116AMCoarse sand
BT10938°53.670′001°55.370′38°55.120′001°56.120′715SOCoarse silt
BT12338°58.270′001°55.850′38°59.970′001°56.560′675SOMedium silt
BT17538°46.070′ 002°30.150′38°46.053′002°31.100′412EBFine sand
A22B_0720BTBT01838°45.050′001°46.550′38°45.270′001°46.900′113SOCoarse sand
BT02638°47.160′001°50.760′38°47.100′001°51.440′127AMVery fine silt
BT02938°46.240′001°47.570′38°46.030′001°46.520′195AMFine sand
BT03338°46.730′001°47.670′38°46.730′001°47.670′225AMCoarse sand
BT03538°44.420′001°43.790′38°43.800′001°42.750′352AMFine to medium sand
BT05538°39.980′002°28.990′38°40.240′002°27.810′473EBVolcanic rock with fine sand
BT06238°43.250′002°27.820′38°44.000′002°27.680′508EBFine sand
DR00338°56.670′001°59.940′38°56.740′001°59.770′455–288SORocky outcrops with fine sand
DR00738°58.760′001°59.010′38°58.560′001°59.140′384–255SORocky outcrops with coarse silt
DR00838°58.165′002°00.670′38°58.200′002°00.430′355–295SORocky outcrops
DRDR01438°55.510′001°58.130′38°55.910′001°57.880′395–270SORocky outcrops with fine sand
DR03038°47.310′001°47.010′38°46.970′001°47.130′276–204AMRocky outcrops
DR04638°42.310′002°30.750′38°42.520′002°30.710′367–235EBVolcanic rocky outcrops
DR04738°43.840′002°29.400′38°43.940′002°29.280′127EBRhodoliths
DR05738°41.720′002°21.880′38°41.560′002°22.100′665–488EBFine sand
DR05838°40.700′002°35.370′38°40.940′002°35.270′1191–1066EBVolcanic rocky outcrops
Table 2. List of live collected molluscs specimens in the Mallorca Channel (Balearic Islands, western Mediterranean) seamounts: Ses Olives (SO), Ausias March (AM) and Emile Baudot (EB). Information on the presence (x) and no presence (0) of the species by seamount is also provided. New records shown in bold.
Table 2. List of live collected molluscs specimens in the Mallorca Channel (Balearic Islands, western Mediterranean) seamounts: Ses Olives (SO), Ausias March (AM) and Emile Baudot (EB). Information on the presence (x) and no presence (0) of the species by seamount is also provided. New records shown in bold.
ClassSubclassOrderFamilySpeciesSOAMEBDepht (m)
GASTROPODACaenogastropoda Littorinimorpha AporrhaidaeAporrhais serresiana (Michaud, 1828)xxx319–640
CapulidaeCapulus ungaricus (Linnaeus, 1758)0xx127–150
Cymatiidae Monolex corrugatus (Lamarck, 1816)00x116
NaticidaeEuspira fusca (Blainville, 1825)xxx281–474
Tectonatica rizzae (Philippi, 1844)xx0105–445
RanellidaeRanella olearium (Linnaeus, 1758)00x137–410
XenophoridaeXenophora crispa (König, 1825)0xx122–297
NeogastropodaClathurellidae Comarmondia gracilis (Montagu, 1803)00x127
ColidaeColus jeffreysianus (P. Fischer, 1868)00x503–574
ColumbellidaeMitrella gervillii (Payraudeau, 1826)00x665–488
FasciolariidaeAptyxis syracusana (Linnaeus, 1758)0x0118
Fusinus pulchellus (Philippi, 1840)0xx105–395
Gracilipurpura rostrata (Olivi, 1792)0xx127–483
FusiturridaeFusiturris similis (Bivona And., 1838)0x0116–376
MuricidaeMurexsul aradasii (Monterosato, 1883)00x123–126
Orania fusulus (Brocchi, 1814)00x123–131
Ocenebra erinaceus (Linnaeus, 1758)0x0225
Pagodula echinata (Kiener, 1839)xxx259–680
Trophonopsis muricata (Montagu, 1803)0x0319
RaphitomidaeGymnobela abyssorum (Locard, 1897)xxx259–574
-EpitoniidaeEpitonium celesti (Aradas, 1854)00x147–410
HeterobranchiaCephalaspidea PhilinidaePhiline monterosati Monterosato, 1874xxx98–410
Philine sp.xxx111–740
GastropteridaeGastropteron rubrum (Rafinesque, 1814)0x0105–242
Pteropoda CymbuliidaeCymbulia peronii Blainville, 1818xxx111–680
ActeonidaeJaponactaeon pusillus (Forbes, 1844)x00482–586
VetigastropodaLepetellida Addisoniidae Addisonia excentrica (Tiberi, 1855)0x0118
SeguenziidaChilodontaidae Danilia tinei (Calcara, 1839)0xx127–150
TrochidaCalliostomatidaeCalliostoma conulus (Linnaeus, 1758)00x302
Calliostoma granulatum (Born, 1778)xxx118–405
Calliostoma zizyphinum (Linnaeus, 1758)0xx225–483
ColloniidaeCantrainea peloritana (Cantraine, 1835)00x503–574
Trochidae Callumbonella suturalis (Philippi, 1836)0xx169–365
Clelamdella miliaris (Brocchi, 1814)xx0135–474
BIVALVIAAutobranchia ArcidaArcidae Anadara corbuloides (Monterosato, 1881)0x0111–112
Asperarca nodulosa (O. F. Müller, 1776)x0x260–665
Bathyarca philippiana (Nyst, 1848)xxx152–759
Tetrarca tetragona (Poli, 1795)0x099
CardiidaTellinidaeArcopella balaustina (Linnaeus, 1758)0x0122–195
SemelidaeAbra longicallus (Scacchi, 1835)xxx195–740
LimidaLimidaeLima lima (Linnaeus, 1758)0x0105
Limaria tuberculata (Olivi, 1792)0x0267
PectinidaAnomiidaeAnomia ephippium Linnaeus, 175800x274
PectinidaePododesmus patelliformis (Linnaeus, 1761)0x0105–122
Pododesmus squama (Gmelin, 1791)0x0105–124
Delectopecten vitreus (Gmelin, 1791)x0x640–674
Karnekampia sulcata (O. F. Müller, 1776)0xx122–348
Mimachlamys varia (Linnaeus, 1758)x00255–384
Palliolum incomparabile (Risso, 1826)xxx169–503
Parvamussium fenestratum (Forbes, 1844)xxx127–674
Pseudamussium clavatum (Poli, 1795)0xx105–352
Similipecten similis (Laskey, 1811)xxx105–298
Aequipecten commutatus (Monterosato, 1875)00x410
SpondylidaeSpondylus gussonii O. G. Costa, 183000x127
VeneridaMactridae Spisula subtruncata (da Costa, 1778)x00259
VeneridaeTimoclea ovata (Pennant, 1777)00x127
-CuspidariidaeCardiomya costellata (Deshayes, 1835)xx0118–607
- Cuspidaria cuspidata (Olivi, 1792)xxx127–474
- Cuspidaria rostrata (Spengler, 1793)xxx122–759
- Tropidomya abbreviata (Forbes, 1843)xxx122–523
-LyonsiidaeAllogramma formosa (Jeffreys, 1882)x00619–675
Policordia gemma (A. E. Verrill, 1880)0x0124
-PoromyidaePoromya granulata (Nyst & Westendorp, 1839)0xx122–352
Cetomya neaeroides (Seguenza, 1877)x00235–449
-VerticordiidaeHaliris granulata (Seguenza, 1860)0xx127–412
ProtobranchiaNuculanidaNuculanidaeLedella messanensis (Jeffreys, 1870)x00523–715
Nuculida Nuculidae Nucula nitidosa Winckworth, 19300x0320–365
Nucula sulcata Bronn, 18310x0376
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Marco-Herrero, E.; Ramón, M.; Ramírez-Amaro, S.; Sánchez-Guillamón, O.; Ordines, F.; López-Rodríguez, C.; Farriols, M.T.; Vázquez, J.T.; Massutí, E. New Deep-Sea Molluscan Records from Mallorca Channel Seamounts (North-Western Mediterranean). Diversity 2022, 14, 928. https://doi.org/10.3390/d14110928

AMA Style

Marco-Herrero E, Ramón M, Ramírez-Amaro S, Sánchez-Guillamón O, Ordines F, López-Rodríguez C, Farriols MT, Vázquez JT, Massutí E. New Deep-Sea Molluscan Records from Mallorca Channel Seamounts (North-Western Mediterranean). Diversity. 2022; 14(11):928. https://doi.org/10.3390/d14110928

Chicago/Turabian Style

Marco-Herrero, Elena, Montserrat Ramón, Sergio Ramírez-Amaro, Olga Sánchez-Guillamón, Francesc Ordines, Carmina López-Rodríguez, María Teresa Farriols, Juan Tomás Vázquez, and Enric Massutí. 2022. "New Deep-Sea Molluscan Records from Mallorca Channel Seamounts (North-Western Mediterranean)" Diversity 14, no. 11: 928. https://doi.org/10.3390/d14110928

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