The holothurian Parastichopus tremulus, a species only know from the north-eastern Atlantic, is reported for the
first time from the Mediterranean Sea. Five individuals of the species were collected in the vicinity of the Seco de los Olivos
sea mount in May 2017 from a bottom trawl sample carried out during the MEDITS trawl survey. Scanning Electron
Microscope images of body wall ossicles are supplied to support species identification. Connectivity between Atlantic and
Mediterranean populations of P. tremulus is suggested due to the existence of a nearby Atlantic population in the Gulf of
Cádiz and the documented presence of abundant holothuroid larvae in the anticyclonic gyre which originates in the Atlantic
current entering the Mediterranean, near the Strait of GibraltarPremier signalement du concombre de mer Parastichopus tremulus (Gunnerus, 1767) (Echinodermata :
Aspidochirotida) en Méditerranée (Mer d’Alboran, Méditerranée occidentale). L’holothurie Parastichopus tremulus, une
espèce connue seulement du nord-est Atlantique, est signalée pour la première fois en Mer Méditerranée. Cinq individus
de l’espèce ont été récoltés près du mont sous-marin Seco de los Olivos en mai 2017 d’un échantillon de chalut de fond
effectué pendant la campagne de recherche avec chalut MEDITS. Des photographies au microscope électronique à balayage
d’osselets de la paroi du corps sont fournies pour valider l’identification de l’espèce. La connectivité entre les populations
atlantiques et méditerranéennes de P. tremulus est suggérée en raison de la proximité d’une population atlantique dans le
Golfe de Cádiz et de la présence documentée de larves d’holothurie abondantes dans le vortex anticyclonique originaire du
courant atlantique entrant en Méditerranée, près du Détroit de GibraltarVersión del edito

Farias, C. (Carlos)

Ferriol, Pere

García-Ruiz, C. (Cristina)

Moya-Ruiz, F. (Francisca)

Ordines, F. (Francesc)

Rueda, J.L. (José Luis)

English

The holothurian Parastichopus tremulus, a species only know from the north-eastern Atlantic, is reported for the first time from the Mediterranean Sea. Five individuals of the species were collected in the vicinity of the Seco de los Olivos sea mount in May 2017 from a bottom trawl sample carried out during the MEDITS trawl survey. Scanning Electron Microscope images of body wall ossicles are supplied to support species identification. Connectivity between Atlantic and Mediterranean populations of P. tremulus is suggested due to the existence of a nearby Atlantic population in the Gulf of Cádiz and the documented presence of abundant holothuroid larvae in the anticyclonic gyre which originates in the Atlantic current entering the Mediterranean, near the Strait of Gibraltar

Ferriol, P. (Pere)

Repositorio Institucional Digital del IEO

First record of the sea cucumber Parastichopus tremulus (Gunnerus, 1767) (Echinodermata: Holothuroidea: Aspidochirotida) in the Mediterranean Sea (Alboran Sea, western Mediterranean)

The holothurian Parastichopus tremulus, a species only know from the north-eastern Atlantic, is reported for the
first time from the Mediterranean Sea. Five individuals of the species were collected in the vicinity of the Seco de los Olivos
sea mount in May 2017 from a bottom trawl sample carried out during the MEDITS trawl survey. Scanning Electron
Microscope images of body wall ossicles are supplied to support species identification. Connectivity between Atlantic and
Mediterranean populations of P. tremulus is suggested due to the existence of a nearby Atlantic population in the Gulf of
Cádiz and the documented presence of abundant holothuroid larvae in the anticyclonic gyre which originates in the Atlantic
current entering the Mediterranean, near the Strait of GibraltarPremier signalement du concombre de mer Parastichopus tremulus (Gunnerus, 1767) (Echinodermata :
Aspidochirotida) en Méditerranée (Mer d’Alboran, Méditerranée occidentale). L’holothurie Parastichopus tremulus, une
espèce connue seulement du nord-est Atlantique, est signalée pour la première fois en Mer Méditerranée. Cinq individus
de l’espèce ont été récoltés près du mont sous-marin Seco de los Olivos en mai 2017 d’un échantillon de chalut de fond
effectué pendant la campagne de recherche avec chalut MEDITS. Des photographies au microscope électronique à balayage
d’osselets de la paroi du corps sont fournies pour valider l’identification de l’espèce. La connectivité entre les populations
atlantiques et méditerranéennes de P. tremulus est suggérée en raison de la proximité d’une population atlantique dans le
Golfe de Cádiz et de la présence documentée de larves d’holothurie abondantes dans le vortex anticyclonique originaire du
courant atlantique entrant en Méditerranée, près du Détroit de GibraltarEvaluación de Recursos Demersales por métodos directos en el Mar de AlboránDEMALBORANS

Ordines, Francesc

Moya-Ruiz, Francisca

Farias, Carlos

Rueda, José Luis

García-Ruiz, Cristina

Digital.CSIC

First record of the sea cucumber Parastichopus tremulus Gunnerus, 1767 (Echinodermata: Holothuroidea: Aspidochirotida) in the Mediterranean Sea (Alboran Sea, western Mediterranean)

The holothurian Parastichopus tremulus, a species only know from the north-eastern Atlantic, is reported for the
first time from the Mediterranean Sea. Five individuals of the species were collected in the vicinity of the Seco de los Olivos
sea mount in May 2017 from a bottom trawl sample carried out during the MEDITS trawl survey. Scanning Electron
Microscope images of body wall ossicles are supplied to support species identification. Connectivity between Atlantic and
Mediterranean populations of P. tremulus is suggested due to the existence of a nearby Atlantic population in the Gulf of
Cádiz and the documented presence of abundant holothuroid larvae in the anticyclonic gyre which originates in the Atlantic
current entering the Mediterranean, near the Strait of GibraltarPremier signalement du concombre de mer Parastichopus tremulus (Gunnerus, 1767) (Echinodermata :
Aspidochirotida) en Méditerranée (Mer d’Alboran, Méditerranée occidentale). L’holothurie Parastichopus tremulus, une
espèce connue seulement du nord-est Atlantique, est signalée pour la première fois en Mer Méditerranée. Cinq individus
de l’espèce ont été récoltés près du mont sous-marin Seco de los Olivos en mai 2017 d’un échantillon de chalut de fond
effectué pendant la campagne de recherche avec chalut MEDITS. Des photographies au microscope électronique à balayage
d’osselets de la paroi du corps sont fournies pour valider l’identification de l’espèce. La connectivité entre les populations
atlantiques et méditerranéennes de P. tremulus est suggérée en raison de la proximité d’une population atlantique dans le
Golfe de Cádiz et de la présence documentée de larves d’holothurie abondantes dans le vortex anticyclonique originaire du
courant atlantique entrant en Méditerranée, près du Détroit de Gibralta

Reçu le 1 août 2017 ; accepté après révision le 5 juillet 2018.Received 1 August 2017; accepted in revised form 5 July 2018.Cah. Biol. Mar. (2019) 60 : 111-115First record of the sea cucumber Parastichopus tremulus(Gunnerus, 1767) (Echinodermata: Holothuroidea:Aspidochirotida) in the Mediterranean Sea (Alboran Sea, western Mediterranean)Francesc ORDINES1, Pere FERRIOL2, Francina MOYA3, Carlos FARIAS4, José L. RUEDA3and Cristina GARCÍA-RUIZ3(1) Instituto Español de Oceanografía - Centre Oceanogràfic de les Balears, Palma, Spain(2) Interdisciplinary Ecology Group, Biology Department, Universitat de les Illes Balears, Palma, Spain (3) Instituto Español de Oceanografía - Centro Oceanográfico de Málaga, Málaga, Spain(4) Instituto Español de Oceanografía - Centro Oceanográfico de Cádiz, Cádiz, SpainCorresponding author: xisco.ordinas@ieo.esAbstract: The holothurian Parastichopus tremulus, a species only know from the north-eastern Atlantic, is reported for thefirst time from the Mediterranean Sea. Five individuals of the species were collected in the vicinity of the Seco de los Olivossea mount in May 2017 from a bottom trawl sample carried out during the MEDITS trawl survey. Scanning ElectronMicroscope images of body wall ossicles are supplied to support species identification. Connectivity between Atlantic andMediterranean populations of P. tremulus is suggested due to the existence of a nearby Atlantic population in the Gulf ofCádiz and the documented presence of abundant holothuroid larvae in the anticyclonic gyre which originates in the Atlanticcurrent entering the Mediterranean, near the Strait of Gibraltar. Résumé : Premier signalement du concombre de mer Parastichopus tremulus (Gunnerus, 1767) (Echinodermata :Aspidochirotida) en Méditerranée (Mer d’Alboran, Méditerranée occidentale). L’holothurie Parastichopus tremulus, uneespèce connue seulement du nord-est Atlantique, est signalée pour la première fois en Mer Méditerranée. Cinq individusde l’espèce ont été récoltés près du mont sous-marin Seco de los Olivos en mai 2017 d’un échantillon de chalut de fondeffectué pendant la campagne de recherche avec chalut MEDITS. Des photographies au microscope électronique à balayaged’osselets de la paroi du corps sont fournies pour valider l’identification de l’espèce. La connectivité entre les populationsatlantiques et méditerranéennes de P. tremulus est suggérée en raison de la proximité d’une population atlantique dans leGolfe de Cádiz et de la présence documentée de larves d’holothurie abondantes dans le vortex anticyclonique originaire ducourant atlantique entrant en Méditerranée, près du Détroit de Gibraltar.Keywords: Echinoderm l Stichopodidae l Atlantic inflow l Taxonomy l Morphological examinationDOI: 10.21411/CBM.A.137C121D112 MEDITERRANEAN RECORD OF PATASTICHOPUS TREMULUSIntroductionThe genus Parastichopus was established by Clark (1922)for the sea-cucumber Parastichopus tremulus. Nowadays,it includes only two species: P. tremulus (Gunnerus, 1767)and P. regalis (Cuvier, 1817). Both species are distributedin the north-eastern Atlantic Ocean. However, only P.regalis has been documented to occur in the MediterraneanSea, where it is widespread distributed in shelf and upperslope bottoms from 5 to 800 m depth, and even representsa resource of local commercial importance (Mortensen,1927; Tortonese, 1965; Smith et al., 2000; Massutí &Reñones, 2005; Tanti & Schembri, 2006; Abad et al., 2007;Aydin, 2008; Ramon et al., 2010). On the contrary, the distribution of P. tremulus is poorlyknown and is currently based on disjunctive records fromthe Scandinavian Peninsula, where it is also present in theFjords, to the Canary Islands, including Iceland, FaroeIslands, Ireland and Great Britain (Mortensen, 1927; Perez-Ruzafa et al., 1992; Samyn, 2013; Buhl-Mortensen & Buhl-Mortensen, 2014). This Parastichopus species has a widebathymetric range, from 20 to 1900 m depth, in which it hasshown preference for muddy or sandy-mud sediments(Mortensen, 1927; Buhl-Mortensen & Buhl-Mortensen,2014; Robert et al., 2016). It is a benthic deposit-feeder thatseems to feed selectively on faecal pellets from otherbenthic animals and on other sediment aggregates that arericher in organic matter than the surrounding sediments(Hauksson, 1979; Godbold et al., 2009).Increasing exploration and studies on the compositionand structure of benthic communities from coastal to deep-sea areas of the Mediterranean Sea has resulted in a betterknowledge on the distribution of specific benthic speciesthat were not expected to occur in this basin, e.g. theechinoderm Luidia atlantidea (Madsen, 1950) (Gallardo-Roldán et al., 2015). Regarding Parastichopus, OCEANA(2011) explored the Seco de Palos seamount (westernMediterranean) using a Remote Operated Vehicle (ROV)and reported the image and the frequent presence of anholothuroid which was listed as Parastichopus cf. tremulusindicating the possible species identity or resemblance.Nevertheless, the species identity could not be confirmedsince no anatomical nor molecular analyses were done.This study reports the first substantiated record of P.tremulus in the Mediterranean Sea, by studying themorphological treats, including scanning electronmicroscopy of ossicles of individuals collected during theMEDITS bottom trawl survey in the Alboran Sea.Material and methodsIn May 2017, during the MEDITS bottom trawl survey (seeBertrand et al. (2002) for specifications on samplingscheme and gear used), five specimens of a Parastichopusspecies were collected from an otter trawl haul carried outat a depth of 640 m in the vicinity of Seco de los Olivosseamount (also known as Chella Bank) located in theAlboran Sea (western Mediterranean) (Fig. 1). The external morphology (length, shape, color andpresence of feet) of all individuals was studied. Two ofthem were dissected and their feeding tentacles wereisolated and photographed using a stereomicroscope LeicaM165 C. Moreover, a small cube-shaped piece of dorsalbody wall was excised for isolation of ossicles. Followinga similar methodology to that described in Hickman (1998),the piece of body wall was placed in a tube with 10%concentrated bleach (NaCl) until the body wall wasdissolved. Then the tube was lightly centrifuged (3000 rpmduring 3-5 minutes) and the supernatant was pipetted offand discarded. Precipitated ossicles were resuspended indistilled water, lightly centrifuged whereupon thesupernatant was again discarded. In order to clean theFigure 1. Parastichopus tremulus. Map of the study area (Alboran Sea, western Mediterranean), indicating with a star symbol thesampling station were the individuals were caught. Isobaths correspond to 200, 600 and 1000 m depth.F. ORDINES, P. FERRIOL, F. MOYA, C. FARIAS, J.L. RUEDA, C. GARCÍA-RUIZ 113ossicles from any remaining tissue, a hydrogen peroxidedigestion step was included. One milliliter of a 30%solution of hydrogen peroxide was added to the precipitatedossicles and the tube was gently shaken on an orbital shakerfor several hours. After shaking, ossicles were let to settlefor 15 minutes, rinsed several times with distilled water andfinally preserved in absolute ethanol until they wereprepared for scanning electron microscopy (SEM). Twoaliquots of suspended ossicles were mounted onto copperconductive tape, air-dried, sputter-coated with gold andobserved with a SEM HITACHI S-3400N. Two of theremaining specimens have been permanently fixed andpreserved in 4% formalin, whereas the rest were preservedin 70% ethanol. All of them are kept in the Marine FaunaCollection (http://www.ma.ieo.es/cfm/) based at the CentroOceanográfico de Málaga, Instituto Español deOceanografía, where they are labelled correlatively asCFM-IEOMA-6405 to CFM-IEOMA-6409.ResultsThe size of the collected Parastichopus tremulus specimensranged between 19.3 to 20.5 cm in length. Their freshweight varied between 190 and 234 g. The collectedindividuals belong to the order Aspidochirotida due to thefollowing characters: presence of tube feet andcharacteristic shield-shaped feeding tentacles (Fig. 2), andthe absence of retractor muscles. They also belong to theStichopodidae family due to the presence of gonads on bothsides of the dorsal mesentery. We identified them as P.tremulus due to their cylindrical body shape with theventral side slightly flattened; dorsal side was reddish incolour whereas the ventral side was white (Fig. 2). Bodywall ossicles were very abundant with rods and tables as themost common ones, but also with star-shaped bodies(Fig. 3). C-shaped rods and buttons absent. Tablespresented disks with serrated edge, perforated by 14 to 21peripheral and 4 central larger holes; disk diameters rangedfrom 96.5 to 118.7 µm and averaged 105.6 µm (n = 21); thespire was composed by four pillars connected by twobeams and terminating with three levels of bifid spines.Rods were spinous, ranging from 107.9 to 307.4 µm andaveraging 179.5 µm in length (n = 30), with variable shapebut usually bearing two to three branches at the ends. Star-shaped bodies were highly ramified with thorn-like spinesin the branches; their maximum diameters ranged from98.3 to 140.9 µm and averaged 120.8 µm (n = 6). All thesemorphological traits are in total coincidence with the re-description of the species by Mortensen (1927).DiscussionThe present study represents the first confirmed record of P.tremulus in the Mediterranean Sea, specifically in the slopeclose to the seamount Seco de los Olivos, in the AlboranSea. The presence of this species had recently beensuggested from the Seco de Palos, another seamountlocated eastwards from our record, at a depth of around 550m (OCEANA, 2011; Fig. 1). This coincidence in habitatcharacteristics, and the lack of similar records in othersampled areas of the Alboran Sea, may indicate the speciesdistribution in the Mediterranean could be restricted toslope bottoms in the seamounts or their vicinity. Thisspecies, together with P. regalis, has generally beencollected in sedimentary habitats from the nearby Gulf ofCádiz in the annual bottom trawl surveys ARSA (Campañade evaluación demersales ARrastre SurAtlántica) carriedout in that area for the assessment of the exploitation stateof the bottom trawl fishery (Sobrino & Burgos, 2016).According to these surveys, in the Gulf of Cádiz, P.Figure 2. Parastichopus tremulus. Photographs of the individuals caught. A.Ventral and dorsal views (squares are 1x1 cm). B. Typicalshield-shaped tentacle of the Holothuroidea, order Aspidochirotida.tremulus is among the most important echinoderm species,in terms of both biomass and abundance, in the bathymetricstratum from 500 to 800 m depth, where the species showedaverage yields of around 1500 g × h-1 of trawling (Sobrino& Burgos, 2016).The Alboran Sea is an area highly influenced by Atlanticwaters that flow through the Strait of Gibraltar into theMediterranean in a layer from the surface to around 180 mdepth, below which the Mediterranean water outflows in acountercurrent (Bryden & Stommel, 1982; Jia et al., 2007).In the last years, several species of different phyla withAtlantic affinity (either boreal or from subtropical westAfrica) have been detected in different habitat types of theAlboran Sea (e.g. the crustacean Pagurus mbizi (Forest,1955), the echinoderm Luidia atlantidea and the fishDipturus nidarosiensis (Storm, 1881), recorded in GarcíaRaso et al. (2010), Gallardo-Roldán et al. (2015) andRamírez-Amaro et al. (2017), respectively), showing thesingularity of this area, located at the crossroads betweenthe Mediterranean Sea and the Atlantic Ocean, thatprobably supports the highest biodiversity in Europeanwaters (Coll et al., 2010; García Raso et al., 2010;Templado, 2011). The presence of these Atlantic specieshas been related to the hydrodynamics of this basin(Bouchet & Taviani, 1992; Cebrian & Ballesteros, 2004).This could also be the case for the occurrence of P. tremulusin the Mediterranean Sea, a population that could beconnected to nearby Atlantic populations through larvaldispersal mediated by Atlantic superficial waters enteringthe Mediterranean Sea. Pedrotti & Fenaux (1996) remarkedthat echinoderm larvae and postlarvae in the part of theAlboran Sea more influenced by Mediterranean waterswere scarce in comparison with the area more influencedby Atlantic waters, where the abundance and speciesrichness was higher. These authors detected holothuroidlarvae in the eastern Alboran Sea mainly from 75 to 600 mdepth in association with the anticyclonic gyre whichoriginates in the Atlantic current near the Strait of Gibraltar.Hence, the population of P. tremulus in the Alboran Seacould exchange individuals with, or be sustained by,Atlantic populations that could act as a source of larvae,such as those from the Gulf of Cádiz, which could betransported inside the Mediterranean within the Atlanticsuperficial currents.AcknowledgmentsThe authors wish to thank all the participants in theMEDITS surveys, as well as the crew of the R/V MiguelOliver. This work was supported by the projectDEMALBORAN, funded by the European Commissionand the Instituto Español de Oceanografía through the DataCollection Framework. The authors would like toacknowledge Dr. Ferran Hierro from the Scientific andTechnical Facilities Service of the UIB for taking scanningelectron microscope images.114 MEDITERRANEAN RECORD OF PATASTICHOPUS TREMULUSFigure 3. Parastichopus tremulus. Scanning electron microscope photographs of body wall ossicles. A. A wide field with mostimportant ossicles, rods, star-shaped bodies, and tables, represented. B. Detailed photograph of a star-shaped body. C-F. Differentperspectives of the characteristic tables.ReferencesAbad E., Preciado I., Serrano A. & Baro J. 2007. Demersal andepibenthic assemblages of trawlable grounds in the northernAlboran Sea (western Mediterranean) Scientia Marina, 71:513-524. Doi: 10.3989/scimar.2007.71n3513Aydin M. 2008. The commercial sea cucumber fishery in Turkey.SPC Bêche-de-Mer Information Bulletin, 28: 40-41.Bertrand J.A., Gil de Sola L., Papaconstantinou C., Relini G.& Souplet A. 2002. The general specifications of the Meditssurveys. 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First record of the sea cucumber Parastichopus tremulus Gunnerus, 1767 (Echinodermata: Holothuroidea: Aspidochirotida) in the Mediterranean Sea (Alboran Sea, western Mediterranean)

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