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First records of Carybdea marsupialis proliferation(Cnidaria: Cubozoa) along the eastern Tunisian coast(Central Mediterranean)S. K. M. Guerouna, M. J. Acevedob, O. Kéfi-Daly Yahiac, A. Deidund, V. L. Fuentesb, S.Pirainoe & M. N. Daly Yahiaa

a Laboratory of Aquatic Systems Biodiversity and Functioning, Faculty of Sciences ofBizerte, University of Carthage, Bizerte, Tunisiab Institut de Ciències del Mar, CSIC, Barcelona, Catalonia, Spainc Laboratoire de planctonologie, Institut National Agronomique de Tunisie, Tunis, Tunisia(U.R. Biologie Marine – FST)d IOI – Malta Operational Centre, University of Malta, Msida, Maltae Evolutionary and Developmental Biology of Marine Invertebrates, Dipartimento Scienze eTecnologie Biologiche ed Ambientali (DISTEBA), University of Salento, Lecce, ItalyPublished online: 20 May 2015.

To cite this article: S. K. M. Gueroun, M. J. Acevedo, O. Kéfi-Daly Yahia, A. Deidun, V. L. Fuentes, S. Piraino & M. N. DalyYahia (2015): First records of Carybdea marsupialis proliferation (Cnidaria: Cubozoa) along the eastern Tunisian coast (CentralMediterranean), Italian Journal of Zoology, DOI: 10.1080/11250003.2015.1045945

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First records of Carybdea marsupialis proliferation (Cnidaria:Cubozoa) along the eastern Tunisian coast (Central Mediterranean)

S. K. M. GUEROUN1*, M. J. ACEVEDO2, O. KÉFI-DALY YAHIA3, A. DEIDUN4,V. L. FUENTES2, S. PIRAINO5, & M. N. DALY YAHIA1

1Laboratory of Aquatic Systems Biodiversity and Functioning, Faculty of Sciences of Bizerte, University of Carthage, Bizerte,Tunisia, 2Institut de Ciències del Mar, CSIC, Barcelona, Catalonia, Spain, 3Laboratoire de planctonologie, Institut NationalAgronomique de Tunisie, Tunis, Tunisia (U.R. Biologie Marine – FST), 4IOI – Malta Operational Centre, University ofMalta, Msida, Malta, and 5Evolutionary and Developmental Biology of Marine Invertebrates, Dipartimento Scienze eTecnologie Biologiche ed Ambientali (DISTEBA), University of Salento, Lecce, Italy

(Received 16 December 2014; accepted 21 April 2015)

AbstractThe cubozoan jellyfish Carybdea marsupialis Linnaeus, 1758 is recorded for the first time from the eastern Tunisian coast(Hammamet beach). A few specimens (three adult individuals) were first recorded in July 2005. In spite of several jellyfishmonitoring campaigns carried out along the Tunisian coasts in recent years, new records of C. marsupialis from the samelocation were only made years later, in July and August 2014, consisting of aggregations of adult jellyfish (mean density of1.1 ± 1.0 ind. m−3), which may pose a severe threat to bathers due to their painful stings. The mean morphometricparameter values from 55 C. marsupialis specimens sampled during the same period are reported here, and the possiblecauses for box jellyfish proliferation in the Hammamet coastal zone are also discussed.

Keywords: Box jellyfish, Medusozoa, outbreaks, marine stingers, Northern African coasts

Introduction

The cnidarian class Cubozoa includes 2 orders hav-ing some 50 species described worldwide andgrouped in 7 families (Bentlage & Lewis 2012).Within the Carybdeidae family, Carybdea Péron &Lesueur, 1809 is the sole genus recognized, with 7–8accepted species (Bentlage et al. 2010; Bentlage &Lewis 2012), including the oldest describedcubozoan taxon Carybdea marsupialis (Linneaus,1758), C. murrayana (Haeckel, 1880), C. rastonii(Haacke, 1887), C. brevipedalia (Kishinouye, 1891),C. arborifera (Mass, 1897), C. xaymacana (Conant,1897), C. branchi (Gershwin & Gibbons, 2009) and,more recently, C. morandinii (Straehler-Pohl &Jarms, 2005), whose validity has still to be con-firmed. Cubozoan jellyfish, including C. marsupialis,have a biphasic life cycle with a benthic polyp and afree-swimming medusa. The sessile polyp stage has arenowned prolific potential for asexual reproduction

(through budding), comparable to what can befound in other medusozoan taxa (Boero et al. 2002).In spite of records of C. marsupialis from the

tropical and subtropical regions of the AtlanticOcean, the Caribbean Sea (Bigelow 1938; Kramp1961; Studebaker 1972; Sánchez-Rodríguez et al.2006) and Californian waters (Larson & Arneson1990), in the light of recent morphologic andgenetic analyses results (Acevedo et al. in prepara-tion), C. marsupialis seems to be an endemic speciesfor the Mediterranean Sea, with its type localitybeing the Northern Adriatic (coastal waters inclose proximity to Rimini along the Italian coast-line) (Gershwin 2005).Besides frequent records from the Adriatic Sea

(Boero & Minelli 1986; Mizzan 1993; Bettoso2002; Di Camillo et al. 2006), C. marsupialis wasalso reported from the Aegean (Geldiay & Balik1977) and the western Mediterranean (Mayer

*Correspondence: S. K. M. Gueroun, Faculty of Sciences of Bizerte, Laboratory of Aquatic Systems Biodiversity and Functioning, 7021 Zarzouna, Bizerte,Tunisia. Tel: 216 72591906. Fax: 216 72590566. Email: sgueroun@yahoo.fr

Italian Journal of Zoology, 2015, 1–6http://dx.doi.org/10.1080/11250003.2015.1045945

© 2015 Unione Zoologica Italiana

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1910; Thiel 1928; Stiasny 1930; Rossi 1949; citedin Kramp 1961). Along the Spanish Mediterraneancoastline, C. marsupialis specimens are familiar toSCUBA divers but were rarely spotted until theoccurrence of a bloom during the summer of2008, which led to a high number of stings(Bordehore et al. 2011). Along the North AfricanMediterranean coasts, up to now only two cubome-dusan specimens were collected in Tunisian waters(Raouad) and one cubomedusan specimen was col-lected in Algiers in 1973 and 1974, respectively.They were deposited in the Smithsonian Institutein Washington DC (USA) (1973: USNM #54378,accession number 299591; 1974: USNM 56659,accession number 311278) and labelled asCarybdea marsupialis but they are under revision(Acevedo et al. in preparation) to check their iden-tity due to significant morphological differencescompared to the Adriatic specimens. We documenthere the first records and the subsequent occur-rence of large numbers of Carybdea marsupialisalong the eastern Tunisian coast, providing evi-dence of jellyfish proliferation at a popular touristhotspot of the Central Mediterranean Sea.

Materials and methods

Within the framework of the Tunisian NationalProgramme on Jellyfish monitoring launched bythe Laboratory of Aquatic Systems Biodiversityand Functioning in 2001 and the MED-JELLYRISK – ENPI CBCMED project (http://www.jellyrisk.eu), several coastal zones along theTunisian coastline were selected for monitoringthe incidence of jellyfish blooms and stranding.Among these, a study area represented by shallowwaters facing the sandy beach at Hammamet(Eastern Tunisian coast; 36°23ʹ54.82ʹʹN, 10°34ʹ42.04ʹʹE) was selected for the installation of ananti-jellyfish experimental net to protect bathersagainst large scyphomedusae. At this site, hun-dreds of specimens of cubozoan jellyfish wereobserved and photographed by SCUBA divers on17–18 July 2014, during the installation of theanti-jellyfish net.

In order to assess semi-quantitatively the size ofthe cubozoan jellyfish population within the samecoastal waters, dedicated sampling of C. marsupialisindividuals was subsequently carried out at thesame site on 14 August 2014. Horizontal hauls ofa WP2 net (200 µm mesh size) equipped with aflowmeter were performed to collect C. marsupialisand zooplankton by wading in shallow water in aparallel direction to the coast. The net was kept atapproximately 5–10 cm above the seabed and a

standardized distance of 100 m was covered ineach transect (Bordehore et al. 2011). Two paralleltransects were carried out, at depths of approxi-mately 1.3 and 2 m, with a SCUBA diver guidingthe net in the water to ensure it was being towed at aconstant height above the seabed. On the beach, allC. marsupialis specimens caught in the net fromeach transect (noticeable to the naked eye) wererapidly removed, preserved in 4% formalin, withthe bell height (BH) being measured in all ofthem. All preserved specimens were brought intothe laboratory for further analysis and careful taxo-nomic identification by microscope. The identifica-tion of the species was done according to thedescription by Claus (1878), which was based onan Adriatic specimen.

Results

Our first observation of C. marsupialis withinTunisian waters dates back to 29 July 2005, whenthree specimens (one specimen of 20 mm and twospecimens of 10 mm BH) were recorded along thecoast at Hammamet (coordinates: 36°26ʹ20.01ʹʹN,10°43ʹ56.09ʹʹN) (Daly Yahia, unpublished data).On 17–18 July 2014, hundreds of C. marsupialisspecimens were initially observed, photographedbut not collected during the MED-JELLYRISKexperimental installation of an anti-jellyfish net atthe Hammamet beach, at water depths of 1–3 m.The horizontal plankton net hauls along the 2shore-parallel transects in August 2014 yielded 55individuals (Figures 1a–b).All specimens present a thickened and domed

upper exumbrella having a slight horizontal con-striction at the gastric phacellae level (Figure 1c).The gastric phacellae, one in each of the fourcorners, were brush-like bundles on single trunks,with numerous short gastric filaments (Figure 1d).The rhopalia niche opening was heart-shaped, withone triangular upper covering scale (Figure 1e).The velarial canals, 3 per octant, were observedto be unforked when situated next to the frenulum,biforked in the middle canal and triforked or withmore branches in the canals flanking the pedalia(Figure 1f).The density of C. marsupialis along the two sam-

pling transects averaged 1.1 ± 1.0 ind. m−3, with amaximum value of 1.8 ind. m−3 in the deepest trans-ect (−2 m), with a dominance of mid-class sizes (14–16 mm BH). The smallest individual did not exceed1 mm and the largest specimens measured 28 mmBH (Figure 2). Among the 55 sampled specimens,78% reached sexual maturity.

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Discussion

Values for the morphometric parameters of Carybdeamarsupialis as recorded at Hammamet beachapproached those measured in Spain (Bordehoreet al. 2011), although, generally, smaller specimens(1–2 mm bell height) were recorded at the Tunisiansite. This difference could be due to differences inthe net mesh size used during sampling in bothstudies (5 mm in Spain area sampling versus0.2 mm in the present study) as well as differencesin the sampling period. In fact, samples in Spainwere collected between September and November,while in Hammamet area the sampling was con-ducted in August, when smaller medusae of this

Figure 1. Carybdea marsupialis caught at Hammamet beach on 14 August 2014 (A,B); bell apex (C); gastric phacellae (D); rhopalia niche(E); velarial canals (F).

Figure 2. Size distribution (bell height in mm) of Carybdea marsu-pialis caught in Hammamet beach on 14 August 2014.

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species may be collected. Additional sampling per-formed in Spanish waters between July 2010 and July2011, using a 200 µm net mesh size, showed the pre-sence of newly detached medusae from mid-spring tolate summer months (Canepa 2014). The simulta-neous occurrence of newly detached medusae andsexually mature individuals among the HammametC. marsupialis population indicates at least two meta-morphosis events (one in late spring–early summermonths and the second in late summer months). Thissuggests that the HammametC. marsupialis populationdynamic may be close to that observed in Spain.However, further prolonged monitoring surveys areneeded to expound on the population dynamics, lifecycle and proliferation potential of C. marsupialis alongthe Tunisian coast.

Prior to this study,C. marsupialis was never detectedin such high abundances along the Tunisian coast andit seems to have increased, especially at Hammametbeach. However, the density of C. marsupialis recordedwithin Tunisian waters remains quite low with respectto values recorded on some beaches near Denia(Spain), where box jellyfish densities may reach muchhigher values; for example, density values of near 91.6ind. m−3 for small medusae (diagonal bell width <5 mm), and 5.2 ind. m−3 for large medusae (diagonalbell width > 15 mm) (Canepa 2014) were recorded atthe Spanish sites.

The recent increase in the density of specimens ofC. marsupialis in Tunisian waters may be due to oneor many interacting factors, such as climate change,food availability and overfishing (Purcell et al. 2007).The alteration of the coastal habitat by human con-structions, such as marinas, docks and breakwaters,provides further substrates for planula settlementand asexual reproduction of the sessile polyp stage(Holst & Jarms 2007; Purcell et al. 2007; Duarteet al. 2013). Moreover, the polyp stage of C. marsu-pialis, besides performing budding, may also retainafter metamorphosis a small basal portion of regen-erative tissue attached to the substrate, from where anew polyp can arise (Straehler-Pohl & Jarms 2005).We noticed that near Hammamet beach, two har-bours, located at a distance of 4 km (YasmineHammamet) and 21 km (Beni Khiar) on either sideof the sampling area, are present. The artificial sub-strates present within these harbours may have sup-ported the settlement of the benthic polyp stage ofthis species, fuelling the observed box jellyfish pro-liferation. Coincidentally, the largest and newest ofthese two marinas (Yasmine Hammamet) has beenbuilt within the last 10 years.

The observation within the same coastal waters oflarge adult box jellyfish medusae since July 2014 sug-gests that polyp metamorphosis may occur in the late

spring–early summer period, driven by the rapidwarming of the surface waters. The transition fromone life stage to another – in cnidarians as in manyother invertebrate benthic groups – is strongly relatedto the chemico-physical factors of the water, such astemperature or salinity (Canepa et al. 2014; Olive1995). Stangl et al. (2002) showed that the metamor-phosis of Carybdea polyps is induced by a water tem-perature rise. Recent studies demonstrated thatsalinity affects Carybdea sp. asexual reproduction byinducing the metamorphosis at low (32 ppm) salinityvalues and enhancing the budding rate and the polyppopulation size at high (38 ppm) salinity values(Canepa et al. 2014). In Hammamet Gulf, seawatertemperature and salinity vary considerably throughoutthe year, ranging between 10.3°C and 29.7°C and37.1 and 38.8 ppm, respectively, and as such mayprovide suitable conditions for C. marsupialis prolif-eration (Chouba et al. 1996). Little is known aboutCarybdea spp. behaviour and ecology (Canepa et al.2014; Nogueira & Haddad 2008; Acevedo et al. 2013;Kingsford & Mooney 2014), while the effects of itstoxin have been studied to a greater degree. Bathersstung by C. marsupialis are reported to have sufferedfrom severe local pain, cutaneous reactions, charac-terized by erythematous–vascular linear wheals, andan intense burning sensation (Kokelj et al. 1992;Rottini et al. 1995; Peca et al. 1997; Sánchez-Rodríguez et al. 2006; Bordehore et al. 2014).Public health problems triggered by C. marsupialisstings represent a threat for tourism activities andother local coastal socio-economic activities, in viewof the high abundance of the same species duringblooming events. For instance, during the summerof 2008, 3330 jellyfish stings were recorded by theRed Cross in beaches located near Denia in Spain,where a C. marsupialis bloom was underway(Bordehore et al. 2011). Within the Hammamet sam-pling area and at adjacent beaches, swimmers com-plained of painful stings.Until now, along the eastern Tunisian coastline,

Carybdea marsupialis had only been observed in thewaters off Hammamet. However, the species mighthave a wider but as yet undocumented distributionwithin Tunisian and North African waters by virtueof the highly adaptive life strategies characteristic ofmedusozoans. For instance, within the life cycle ofother cubomedusae, such as C. morandinii, the polypcan encyst into a resting stage to overcome unfavour-able environmental situations; the cyst can thendetach and float giving rise to new polyps after itsreattachment in a different habitat (Straehler-Pohl &Jarms 2011).The occurrence of C. marsupialis along the

Tunisian coast, at popular touristic hotspots,

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combined with the summer co-occurrence of sev-eral additional scyphozoan and hydrozoan stingingjellyfish, such as Pelagia noctiluca, Rhopilema noma-dica (Daly Yahia et al. 2003, 2013), Phyllorhizapunctata (Gueroun et al. 2014), Rhizostoma pulmoand Olindias phosphorica (Touzri et al. 2004) cancause a serious threat for local socio-economicactivities along the affected coastline: bathers arestung and fishing and aquaculture activities(Marcos-López et al. 2014) may be hampered.

The causes of the documented aggregation of C.marsupialis along stretches of the eastern Tunisiancoastline remain unclear, and further studies arecurrently being postulated in order to understandits behaviour and underlying causative factors, aswell as to further characterize the ecological andeconomic impacts of such aggregations.

Acknowledgements

We would like to thank the reviewers for their con-structive suggestions that significantly improved thismanuscript.

Funding

The research leading to these results has receivedfunding from the European project MED-JELLYRISK (ENPI – CBCMED/ref: I-A/1.3/098;www.jellyrisk.eu). This publication has been devel-oped in collaboration with LIFE CUBOMED pro-ject (LIFE08 NAT ES64; www.lifecubomed.eu).

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