First Records of Mnemiopsis Leidyi A. Agassiz 1865 Off the NW Mediterranean Coast of Spain

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Short communication

First records of Mnemiopsis leidyi A. Agassiz 1865 off the NW Mediterranean coast of Spain

Verónica L. Fuentes1*, Dacha Atienza1, Josep-Maria Gili1 and Jennifer E. Purcell2,3 1Institut de Ciencies del Mar, CSIC, P. Marítim de la Barceloneta, 37-49 08003 Barcelona, Spain 2Western Washington University, Shannon Point Marine Center, 1900 Shannon Point Rd, Anacortes, WA 98221 USA 3University College Cork, Coastal and Marine Resources Centre, Naval Base, Haulbowline Island, Cobh, Co. Cork, Ireland E-mail: [email protected] (FLF), [email protected] (DA), [email protected] (JMG), [email protected] (JT) *Corresponding author

Received 6 October 2009; accepted in revised form 29 October 2009; published online 5 November 2009

Abstract

The comb jelly Mnemiopsis leidyi was first reported in July 2009 along the Spanish coast of the NW Mediterranean Sea and occurred throughout the summer (last report 26 September 2009). Large numbers of the ctenophore were reported by many participants of the “Medusa Project”. The high concentrations of M. leidyi along the Spanish coast, together with its blooms earlier this year in Israel, suggests establishment in the Mediterranean Sea. This is of great concern because of the well-known effects of M. leidyi on marine ecosystems and the consequences for commercial fisheries.

Key words: Mnemiopsis leidyi, Ctenophora, invasive species, NW Mediterranean, Spain

The introduction of Mnemiopsis leidyi A. and Malej 2009) shows an increasing number of Agassiz 1865 is one of the best-documented of a observations in recent years. non-indigenous gelatinous species in the The “Medusa Project”, comprised of a Mediterranean and adjacent seas. The native network of organizations, has been monitoring range of M. leidyi is along the Atlantic coast of the presence of jellyfish along the entire Catalan the Americas (reviewed in Purcell et al. 2001). coast since 2007. The Catalan Water Agency The species favours shallow estuaries and bays (ACA), which underwrites the project, records (2 - 30 m) and coastal waters. It tolerates tempe- the presence of jellyfish daily at more than 300 ratures from 0°C in northern locations in the beaches covering the 69 Municipalities of winter to 32°C in the southern estuaries during Catalonia as part of their routine monitoring the summer, and salinities from ≤2 to 38. These program. Inspectors record presence of jellyfish environments also have high zooplankton at fixed locations on beaches, in near-shore biomasses, ranging from 11 to 200 mgCm−3, and water, and at a distance of 200 m offshore small copepods predominating the mesozoo- beyond the swimming zone. The project also plankton (Purcell et al. 2001). Following its involves Emergency Services from 26 of the 69 accidental introduction to the Black Sea in the Municipalities that report the presence of 1980’s, M. leidyi has spread to the Caspian, jellyfish daily (ACA 2009), and the Fisherman Baltic, and North seas (Mianzan 1999; Shiga- Associations of Catalonia. As part of the project nova et al. 2001a; Faasse and Bayha 2006; data on water temperature and salinity are Javidpour et al. 2006). The first occurrence in recorded. All the information is summarized on the Mediterranean Sea was reported in 1990 in the ACA web page and is available to the public the Gulfs of Saronikos and Elefasis in the (ACA 2009). western Aegean Sea (Shiganova et al. 2001b). In the summer of 2009, M. leidyi was recorded The chronology of M. leidyi presence in the along the entire length of the Catalan coast and Mediterranean Sea (Galil et al. 2009; Shiganova in some other locations along the Mediterranean

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coast of Spain (Figure 1). We report only the beach), 2 (many, < 1 medusa m-2), and 3 (a lot, > confirmed observations (Table 1). We were 1 medusa m-2) (Gili and Pagés 2005; Gili et al. unable to confirm many records from other 2007, 2008). The ACA beach observation locations along the Catalan coast, but believe program followed this classification scheme; M. leidyi may have been commonly distributed. most of the M. leidyi observations during Confirmed records of large swarms lasted from summer 2009 were in category 3. early July to the end of August along the entire coast from Cap de Creus to Alcanar. Mnemiopsis leidyi was recorded also in Denia (Valencia) and in Cabrera (Balearic Islands) (Table 1, Figure 2), where emergency services reported several instances of gelatinous organisms on the beaches during summer 2009. The presence of large numbers of M. leidyi at several locations off the Spanish Mediterranean coast suggests there may have been more than one point of origin. It is unclear whether M. leidyi was transported by currents or ships from other areas of the Mediterranean Sea. Semi-quantitative data have been compiled in the NW Mediterranean on large gelatinous plankton, predominantly the scyphomedusae Figure 1. The ctenophore Mnemiopsis leidyi collected in Pelagia noctiluca Forsskål, 1775, Rhizostoma Alcanar (NW Mediterranean) in August 2009. Photo: pulmo Macri 1778, and Cotylorhiza tuberculata Georgios Tsounis Macri 1778 since 2000. The abundance of stranded (beached) jellyfish was classified in three categories: 1 (few, < 10 animals per

Figure 2. Recorded locations of Mnemiopsis leidyi along the Spanish NW Mediterranean coast during summer 2009

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Mnemiopsis reaches Spanish Mediterranean coast

Table 1. Records of Mnemiopsis leidyi along the Spanish NW Mediterranean coast during summer 2009. ACA is the Catalan Water Agency

Geographic coordinates Survey date in 2009 Location Source Latitude, N Longitude, E and number of reports Catalonia Cap de Creus 42º19'05.78" 3º19'31.40" July (2 reports) ACA, Fisherman Mataro port 41º 32'01.70" 2º27'01.62" August (1 report) ACA Salou, La Pineda beach 41º03'12.28" 1º10'08.52" August (reported daily for 1 week) ACA – Red Cross Cambrils 41º03'46.60" 1º10'20.63" August (reported daily for 1 week) ACA – Red Cross Les Cases d’Alcanar beach 40º33'02.22" 0º31'49.37" July-September (several reports) ACA July to September (several Alcanar, Del Marjal beach 40º33'15.13" 0º32'04.41" ACA reports) Mediterranean coast of Spain, outside Catalonia Cabrera port (Balearic Islands) 39º08'43.13" 2º55'49.70" August (1 report) Red Cross Denia (Alicante), Big port 38º50'57.18" 0º06'34.25" July-August (observed frequently) Red Cross

Although large numbers of M. leidyi were of nutrients, resulting in increased prokaryotic reported off the Spanish Mediterranean coast in picoplankton that predominate the biomass of July 2009, the ctenophores may have been primary producers (Cushing 1989). The areas present earlier but unnoticed until the popula- where M. leidyi was reported were along the tions increased. Earlier occurrences of M. leidyi coast and were not estuarine. All of these may be established by examination of formalin- conditions in the Catalan Sea are suitable for preserved plankton samples, as in Purcell (1988). M. leidyi, as was predicted by Siapsis et al. The observations of M. leidyi along the (2008), who modelled the potential habitat of the Spanish coast during summer 2009 coincided species. with the presence of large swarms of this species The success of introduced M. leidyi has been along the entire Mediterranean coast of Israel attributed mainly to reduced competition due to (Galil et al. 2009; Dror Angel pers. com.) and over-fished populations of zooplanktivorous fish Italy (Boero et al. 2009). Although there are no and the lack of predators (Oguz et al. 2008; data that conclusively show that M. leidyi has Siapsis et al. 2008). In the NW Mediterranean established permanent populations in Medi- Sea, overfishing is believed to be one reason that terranean waters, the fact that large numbers of gelatinous zooplankton seem to be increasing in M. leidyi occurred along the Mediterranean abundance in recent decades (Gili and Pages coastlines of both Israel, Italy and Spain during 2005). In its native range, M. leidyi is eaten by summer 2009 suggests an established population. other ctenophores (Beroe spp.) and scypho- The coastal waters of the Catalan Sea (NW medusae (Chrysaora sp.; reviewed in Purcell et Mediterranean) during the summer months of al. 2001). In the Western Mediterranean Sea, the 2009 (from May to September) were characte- ctenophores Beroe cucumis and Beroe forskalii rized by salinities between 34 and 38.2 and are abundant (Shiganova and Malej 2009) and temperatures between 22 and 25ºC. In general, can be potential predators of M. leidyi; however, the Catalan Sea is characterized by the presence Beroe spp. normally are abundant only in spring of a permanent shelfbreak density front defined and early summer along the Catalan coast (Pagés by salinity differences between oceanic waters pers. com.), suggesting that these species were and shelf waters. The shelf has high spatial not abundant in the area when M. leidyi occurred variability due to freshwater inputs from in high numbers (July and August 2009). continental runoff that interact with topography Nevertheless, at the beginning of July 2009, both and local conditions (Salat et al. 2002). During M. leidyi and Pelagia noctiluca were present in summer, a clear vertical stratification exists that the coastal waters and P. noctiluca ate M. leidyi increases stability of the water column. This in the laboratory (Fuentes pers. obs.). In late July situation has important effects on the distribution 2009, P. noctiluca almost disappeared from the

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Catalan coast; their absence coincided with high Gili JM, Pagés F (2005) Les proliferacions de meduses. abundances of M. leidyi. The importance of Bolletí de la Societat d’Història Natural de les Balears 48: 9-22 P. noctiluca and other species as predators and Gili JM, Fuentes V, Atienza D (2007) Medusa Project: Data competitors of M. leidyi in Mediterranean waters year 2007. Technical report Nº 1, 98 pp remains to be investigated. Gili JM, Fuentes V, Atienza D (2008) Medusa Project: Data The success of M. leidyi and the conse- year 2008. Technical report Nº 2, 198 pp Javidpour J, Sommer U, Shiganova TA (2006) First record of quences for the environment have not been Mnemiopsis leidyi A. Agassiz 1865 in the Baltic Sea. studied yet in Mediterranean waters. The Aquatic Invasions 1: 299-302, doi:10.3391/ai.2006.1.4.17 presence and possible establishment of M. leidyi Mianzan H (1999) Ctenophora. In: Boltovskoy D (ed), South populations could have serious consequences for Atlantic Zooplankton. BACKHUYS Publishers, Leiden (The Netherlands), pp 561-573 the Mediterranean ecosystem and fisheries as in Oguz T, Fach B, Salihoglu B (2008) Invasion dynamic of the other previously-invaded regions (e.g., Purcell et alien ctenophore Mnemiopsis leidyi and its impact on al. 2001; Shiganova et al. 2001a). anchovy collapse in the Black Sea. Journal of Plankton Research 30: 1385-1397, doi:10.1093/plankt/fbn094 Purcell JE (1988) Quantification of Mnemiopsis leidyi Acknowledgements (Ctenophora, Lobata) from formalin-preserved plankton samples. Marine Ecology Progress Series 45:197-200, doi:10.3354/meps045197 Thanks are due to the Catalan Water Agency for Purcell JE, Shiganova TA, Decker MB, Houde ED (2001) The funding the Medusa Project. We are indebted to ctenophore Mnemiopsis in native and exotic habitats: all institutions collaborating with the reporting U.S. estuaries versus the Black Sea basin. Hydrobiologia network. We are grateful to the anonymous 451: 145-176, doi:10.1023/A:1011826618539 Salat J, Garcia MA, Cruzado A, Palanques A, Arín L, Gomis reviewers and to Tamara Shiganova for the D, Guillén J, de León A, Puigdefèbregas J, Sospedra J, contributions to the manuscript. Velásquez ZR (2002) Seasonal changes of water mass structure and shelf slope exchanges at the Ebro shelf (NW Mediterranean). Continental Shelf Research References 22:327-346, doi:10.1016/S0278-4343(01)00031-0 Siapatis A, Giannoulaki M, Valavanis VD, PalialexisA, ACA (2009) Catalan Water Agency “Medusa Project”. Schismenou E, Machias A, Somarakis S (2008) http://aca-web.gencat.cat/aca/appmanager/aca/aca?_nfpb=true Modelling potential habitat of the invasive ctenophore &_pageLabel=B10200267951250775762574&_nfls=false Mnemiopsis leidyi in Aegean Sea. Hydrobiologia 612: (Accessed on October 2009) 281-295, doi:10.1007/s10750-008-9497-7 Boero F, Putti M, Trainito E, Prontera E, Piraino S, Shiganova Shiganova T, Malej A (2009) Native and non-native T (2009) Recent changes in Western Mediterranean Sea ctenophores in the Gulf of Trieste, Northern Adriatic biodiversity: the establishment of Mnemiopsis leidyi Sea. Journal of Plankton Research 31:61-71, doi:10.1093/ (Ctenophora) and the arrival of Phyllorhiza punctata plankt/fbn102 (Cnidaria). Aquatic Invasions 4: 675-680, doi:10.3391/ Shiganova TA, Kamakin A, Zhukova DP, Ushivtzhev VB, ai.2009.4.4.13 Dulimov AB, Musaeva E (2001a) New invader in the Cushing DH (1989) A difference in structure between Caspian Sea - ctenophore Mnemiopsis and its initial ecosystems in strongly stratified waters and in those that effect on the pelagic ecosystem. Oceanology 41: 542- are only weakly stratified. Journal of Plankton Research 549 11: 1-13, doi:10.1093/plankt/11.1.1 Shiganova TA, Mirzoyan ZA, Studenikina EA, Volovik SP, Faasse MA, Bayha KM (2006) The ctenophore Mnemiopsis Siokou-Frangou I, Zervoudaki S, Christou ED, Skirta leidyi A. Agassiz 1865 in coastal waters of the AY, Dumont HJ (2001b) Population development of the Netherlands: an unrecognized invasion? Aquatic invader ctenophore Mnemiopsis leidyi in the Black Sea Invasions 1: 270-277, doi:10.3391/ai.2006.1.4.9 and other seas of the Mediterranean basin. Marine Galil BS, Kress N, Shiganova TA (2009) First record of Biology 139: 431-445, doi:10.1007/s002270100554 Mnemiopsis leidyi A. Agassiz, 1865 (Ctenophora; Shiganova T, Malej A (2009) Native and non-native Lobata; Mnemiidae) off the Mediterranean coast of ctenophores in the Gulf of Trieste, Northern Adriatic Israel. Aquatic Invasions 4: 356-362, doi:10.3391/ Sea. Journal of Plankton Research 31: 61-71, ai.2009.4.2.8 doi:10.1093/plankt/fbn102

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