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Gonioinfradens paucidentatus (A. Milne Edwards, 1861) (Crustacea, Decapoda,Portunidae): a new alien crab in the Mediterranean Sea

M. CORSINI-FOKA1, M.-A. PANCUCCI-PAPADOPOULOU2, G. KONDILATOS1

and S. KALOGIROU1

1 Hellenic Centre for Marine Research, Hydrobiological Station of Rodos, Cos Street,85100 Rodos, Hellas

2 Hellenic Centre for Marine Research, Institute of Oceanography, P.O. Box 712,19013 Anavissos, Hellas

Corresponding author: mcorsini@ath.hcmr.gr

Received: 8 July 2010; Accepted: 18 October 2010; Published on line: 11 November 2010

Abstract

The first record for the Mediterranean Sea of the Red Sea/Indo-Pacific portunid Gonioinfradenspaucidentatus (red swimming crab) is documented. A detailed description of the specimens collect-ed at Rodos Island (southeastern Aegean Sea) is given, while possible introduction vectors of thespecies in the area are discussed

Keywords: Mediterranean Sea; SE Aegean Sea; Brachyura; Portunidae; Introduction; Alien.

Research ArticleMediterranean Marine ScienceIndexed in WoS (Web of Science, ISI Thomson)The journal is available on line at http://www.medit-mar-sc.net

Introduction

Southeastern Aegean coasts are con-sidered a crucial region for the arrival,establishment and spread of alien species,in particular warm-water species of Indo-Pacific origin (CORSINI-FOKA, 2010; cfrELNAIS 2010). The Dodecanese Islandsbelong to the biogeographic region of theMediterranean named by POR (1990) the‘Lessepsian Province’ and they are consid-ered to be a hot-spot area for the spread ofalien species to the European Mediter-ranean coasts. A huge increase in alienspecies’ introductions has been observed

during the last three decades. The lower-ing of the salinity in the Suez Canal seemsto play an important role in this ongoingprocess in the whole Eastern Mediter-ranean area (POR, 2010). Moreover, theremarkable increase in alien species in theSoutheastern Aegean Sea has also paral-leled the observed warming of the area,which is creating more favourable condi-tions for the establishment of exotic species(PANCUCCI-PAPADOPOULOU et al.,2009; PANCUCCI-PAPADOPOULOU& CORSINI-FOKA, 2010).

Gonioinfradens paucidentatus (A.Milne Edwards, 1861) is a portunid crab

with a wide Indo-Pacific distribution: theRed Sea (SPIRIDONOV & NEUMANN,2008), the Persian Gulf (Arabian and Iran-ian coasts, Gulf of Oman), the EastAfrican coast, Madagascar, Western Indi-an Ocean islands, Australia, New Caledo-nia, French Polynesia, Japan, Hawaii(POUPIN, 1994, 2007, 2008; APEL &SPIRIDONOV, 1998; DAVIE, 1998;APEL, 2001; NADERLOO & SARI,2007). It occurs mainly on hard substratefrom shallow subdital waters to 100 m ofdepth and reaches a carapace length of52.5 mm (POUPIN, 1994).

The aim of the present work is toreport the presence of Gonioinfradens pau-cidentatus from Rodos Island (Dodeca-nese, Southeastern Aegean Sea) as thefirst record of the species for the wholeMediterranean Sea and to discuss its pos-sible introduction vectors in the study area.

Material examined

Three males of Gonioinfradens pauci-dentatus were caught along the easterncoasts of Rodos Island (Fig. 1); the first twospecimens were observed during snorkel-

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Fig. 1: Sampling locations of Gonioinfradens paucidentatus at Rodos Island, Southeastern Aegean Sea(�: Kolimbia; � Agathi; � Haraki).

ing and collected by hand, while the thirdwas captured in fishing pot. The first sam-ple (specimen 1) was found on 1 May 2010in a crevice between sand and rock at 15 mof depth (seawater temperature 19Æ C),at Kolimbia; the second (specimen 2) wascollected on 28 May 2010 from sandy-rockybottom at 15 m of depth (seawater temper-ature 20Æ C), at Agathi; the third (speci-men 3) was caught on 27 June 2010 on bio-genic detritus at 200 m of depth, off Hara-ki (Fig. 1). Specimen 1 was damaged (itlacked the right cheliped, the first and sec-ond right walking legs and the left swim-ming leg) and it is now preserved in alcohol(Catalogue number HSR53). Specimens 2and 3 were delivered alive (specimen 2lacked the first left walking leg) and theyare now deep-frozen at -22Æ C (respectiveCatalogue numbers HSR54 and HSR58).

Identification of specimens was per-formed following APEL & SPIRIDO-NOV (1998). LEENE (1938), CROSNIER(1962), POUPIN (1994, 1996, 2007) andSAKAI (2004) were also consulted.

Description

Carapace hexagonal, length 1.27-1.37times in carapace width, front 2.68-2.75 incarapace width and 2.01-2.12 in carapacelength (Table 1). Front with six teeth, themedian and submedian ones truncate, thelateral ones triangular with rounded tipsand separated from the previous by adeeper groove. Four large acute antero-lateral teeth, the first more rounded, thelast spiniform; there are also two accesso-ry denticles, positioned respectively at thebase of the external border of the first and

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Table 1Measurements (mm) of Gonioinfradens paucidentatus male specimens

caught at Rodos Island in May and June 2010.

Measurements Specimen Specimen Specimen

1 2 3

Carapace length 29.2 30.1 31.9

Carapace width 37.0 39.2 43.8

Frontal margin (=Front) 13.8 14.4 15.9

Fronto-orbital width* 28.5 30.0 31.5

Orbital cavity diameter 5.9 6.2 6.8

Posterior margin of carapace 12.2 12.5 13.2

Left chela length 26.9 28.1 30.0

Left chela height 10.7 11.5 11.8

Right chela length - 27.1 31.0

Right chela height - 10.0 14.4

Left cheliped length** 53.8 54.4 60.3

Right cheliped length** - 52.8 60.2

* distance between external orbital angles** maximum opening

second teeth, the second denticle verysmall, better distinguishable in specimens 3,more reduced in specimens 1 and 2 (Fig.2A); furthermore, an inconspicuous tuber-cule between the third and fourth antero-lateral teeth in specimen 3. Carapacesmooth, granular lines on frontal, protogas-tric and mesogastric regions, epibranchialline interrupted at the cervical groove andacross midline. Postero-lateral junctionsrounded. Antennal flagellum excludedfrom orbit. Basal antennal article with astrong spine. Chelipeds: merus with 3strong spines on the anterior border, car-pus with a strong interior spine and three

smaller spines on the outer face; chela bear-ing two large spines on the superior surfaceand two other marginal and smooth spinesnear the movable finger (Fig. 2A), a singlespine at carpus articulation, lower surfacesmooth. Swimming leg: merus with a sub-distal posterior spine, propodus with a rowof 7 spinules on posterior border followedby 1-2 small tubercule-like protuberances inspecimens 1 and 2, a single row of 8 spinulesin specimen 3. Distal part of first male pleo-pod tubular, with short bristles proximally,on the lateral external surface.

Colour in life (specimen 2): Carapacereddish-brown dorsally with sparse darker

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Fig. 2: Gonioinfradens paucidentatus (specimen 2, male, color in life, carapace length 30.1 mm) col-lected at Haraki, Rodos (A: dorsal view, B: ventral view).

shades, apart from a longitudinal whitishshade from the front to the mesogastricregion, yellow-orange ventrally (Fig. 2A,B); chelipeds reddish externally, yellow-orange internally, fingers dark brown;walking legs reddish with yellow bands.Tips of anterolateral teeth, spines of che-lipeds and merus of 5th pereiopod darkbrown, preceded by a whitish band.

Discussion

APEL & SPIRIDONOV (1998) rec-ognized full generic status in Gonioin-fradens Leene, 1938, and separated it fromCharybdis De Haan, 1833, followed in thisby all subsequent authors (NG et al., 2008).Gonioinfradens includes only one species,G. paucidentatus. The presence of onlyfour large anterolateral teeth allowsGonioinfradens to be easily distinguishedfrom all the other subgenera retained inCharybdis (CROSNIER, 1962; APEL &SPIRIDONOV, 1998), namely Charybdis,Goniohellenus, Gonioneptunus and Gonio-supradens.

The present first report of the speciesin the Mediterranean comes with a seriesof question marks. The origin of theRodos specimens has to be clarified.Indeed, POUPIN (1994) asserts: «Lesspécimens polynésiens se distinguent dumatériel de la côte d'Arabie par la quasi dis-parition de la troisième plus petite épineantérolatérale, qui n'est repérable, dans lemeilleur des cas, que par un tubercule, et parla hauteur plus faible de la paume». In thespecimens from Rodos, the third smalldenticle between third and fourth antero-lateral teeth is absent or reduced to atubercule. Consequently, the origin of theRodos specimens (Red Sea and/or Indo-Pacific area) should be ascertainedthrough further comparisons with samples

from different areas of the native range ofthe species, including genetic analyses.

The second point to be mentioned isits depth distribution. Erythrean alieninvertebrates establish successfully in thelittoral and infralittoral zones of the east-ern Mediterranean to a depth of approxi-mately 50 m, and are hardly ever found indeeper waters, according to GALIL &ZENETOS (2002); to date, this was truealso for the majority of the brachyurans ofIndo-Pacific origin recorded in the marineregion of Rodos, although a few species,like Charybdis (Goniohellenus) longicollisLeene, 1938, could occur in deeper watersup to 80 m (KEVREKIDIS & GALIL,2003; ELNAIS 2010). In our case, thethird specimen of G. paucidentatus wasfound at 200 m. The species is consideredto inhabit coastal waters, even though ithas been reported from Polynesia at up to100 m (POUPIN, 1994). Its being found ata depth even higher than that known in itsnative range (100 m), could open new hori-zons concerning our knowledge about theability of certain alien species to colonizethe Mediterranean coasts, also wideningtheir possible distribution range to deepwaters.

Considering the present record, alienbrachyurans in the Mediterranean todayaccount for 46 species, as at least threemore species must be added to the CIESMAtlas list (GALIL et al., 2002 updated on2008), namely Sirpus monodi Gordon, 1953(PANCUCCI-PAPADOPOULOU & NA-LETAKI, 2007), Charybdis lucifera (Fabri-cius, 1798) (MIZZAN & VIANELLO, (2008)2009) and Eurycarcinus integrifrons(ÖZCAN et al., 2010).

Among the alien brachyurans, repre-sented in the Mediterranean Sea by 21families, 11 are of Atlantic origin (24%)and 35 of Indo-Pacific origin (76%). The

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most successful families in colonization ofthe Mediterranean coasts are Portunidae(12 species), Pilumnidae and Epialtidae (5and 4 species respectively), Leucosiidaeand Calappidae (3 species each one), inagreement with BROCKERHOFF &MCLAY (2008).

Concerning Hellenic waters andincluding the present record, exoticbrachyurans account today for 15 species:11 of Indo-Pacific origin and 4 of Atlanticorigin (ZENETOS et al., 2009;PANCUCCI-PAPADOPOULOU et al.,2010; CORSINI-FOKA & PANCUCCI-PAPADOPOULOU, 2010). Most of themoccur off Rodos (two of Atlantic originand all the 11 species of Indo-Pacific ori-gin) where 77% of them were first record-ed, mainly during the last decade. Portu-nids predominate with 7 species (6 Indo-Pacific, 1 Atlantic), followed by leucosiids(3 species), and finally by plagusiids, xan-thids and macrophthalmids, each with onespecies. All these alien crabs are actuallyestablished along the coast of the island,including the latest one recorded, Atergatisroseus (Rüppell, 1830) (CORSINI-FOKA& PANCUCCI-PAPADOPOULOU, 2010),as two more adult males (carapace length58-61 mm) were caught in May 2010(Authors pers. comm.).

The 10 crab species of Indo-Pacificorigin previously recorded from Rodoswere introduced via the Suez Canal,according to GALIL et al. (2002 updatedon 2008) and ZENETOS et al. (2009),while the vector of introduction of G. pau-cidentatus is an unclear point.

For the time being, we do not know ifcollected specimens represent only a localpopulation or if the species is presentalong other coasts of the Levantine basin,but not yet detected. Due to the significantdistance of the sampling location (Rodos

Island) from the Suez Canal, it is hard tohypothesize that the introduction into theMediterranean of this new alien is theresult of Lessepsian migration. Moreover,although it is a widespread species in itsnative range, no bibliographic referencecould be found for its occurrence in theSuez Canal. Nevertheless, even though notyet detected in other sites, the counter-clockwise circulation in the Levantinebasin could have favoured the propagationof the planktonic stages of the species(BEN RAIS LASRAM et al., 2008) up toRodos, as already discussed for Tyleriusspinosissimus (Regan, 1908), an Indo-Pacific tetraodontid, unknown in the RedSea, which to date occurs only in the spe-cific study area (GOLANI et al., 2006 on-line; CORSINI-FOKA et al., 2010).

Shipping is considered to be one of themost important introduction vectors ofexotic species in the Mediterranean, andthe second most important in Greekwaters (ZENETOS et al., 2009;PANCUCCI-PAPADOPOULOU &CORSINI-FOKA, 2010). According toABELL & HISPANO (2006) the mostprobable vector of the introduction intothe Western Mediterranean of anotherIndo-Pacific portunid, Charybdis feriata(Linnaeus, 1758), is shipping, probably dueto ‘an accidental escape from holdingtanks of live specimens’. It has however tobe noted that Charybdis feriata is a speciesof high commercial value and the uniquespecimen observed in the wild was foundin the vicinity of Barcelona, one of themost important international ports in theMediterranean. Transport in ballast is sup-posed the most likely vector of introduc-tion into the eastern Mediterranean of thealien Eurycarcinus integrifrons De Man,1879, a pilumnid native to the Red Sea-Indian Ocean and recently first recorded

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in an area subjected to intense industrialshipping traffic, Iskenderun Bay, Turkey(ÖZCAN et al., 2010). Rodos, on the otherhand, is a tourist area, and internationalmaritime traffic in its relatively small har-bour is mainly represented by cruise ships.However, large commercial ships (tankersand cargos) travel along trade routes in theopen sea, offshore of the island. Ballastwaters could offer suitable conditions forthe survival of the eggs and/or larvae of thered swimming crab, while young individu-als could survive in ballast sediments. Thishas been ascertained for other aliens,including some crabs, introduced into var-ious marine ecosystems all over the world(GALIL et al., 2008; MINCHIN et al.,2009), as it has been assumed for theabove-mentioned recent introduction of E.integrifrons into the Eastern Mediter-ranean. Also the sea-chests of ships couldbe taken into consideration as a possiblemeans of introduction of the species, asthoroughly discussed in SCHEMBRI et al.(2010) in relation to the finding of theexotic fish Oplegnathus fasciatus (Tem-minck & Schlegel, 1844) in Malta.

Concerning aquaculture, only nativefish are currently cultured in cages, while aland-based farm operated up to 2008 in thesouth of Rodos, both activities being car-ried out under the supervision and controlof the Ministry of Agriculture and strictlyfollowing the rigid EU and national proce-dures and legislations. Therefore, acciden-tal introduction of Gonioinfradens pauci-dentatus, a medium sized species withoutcommercial value, or of its eggs and/or lar-vae, through transport by ship for aquacul-ture purposes seems very improbable.

Data on local pet-shops and homeaquaria are not available, but import ofexotic organisms is also subjected to rigor-ous international law, and the red swim-

ming crab is not listed among the speciestraded for tropical aquaria purposes.

Even if all the above vectors appearsomewhat biased to explain the first occur-rence of G. paucidentatus in Rodos, thecollecting of three adult specimens in avery short time and from different sitesand depths suggests the already establish-ment of this new alien crab. Its presence inthe area could have been overlooked, bothbecause underwater identification at 15 mdepth on hard substrate is difficult andalso because, being not commerciallyexploited, it is probably discarded in fish-ery. Consequently, it is difficult to evaluatethe exact time of its introduction into thewater off Rodos and the Mediterranean asa whole.

Acknowledgements

The authors are grateful to Dr A.Sioulas for his substantial support andHaris Hatzialexiou, who provided thespecimens reported in this work. Theauthors wish to acknowledge furthermoretwo anonymous reviewers who offeredconstructive and valuable suggestions forimproving the final manuscript.

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