Hydrobiologia

, Volume 645, Issue 1, pp 23–37 | Cite as

Blooms of the invasive ctenophore, Mnemiopsis leidyi, span the Mediterranean Sea in 2009

  • Verónica L. Fuentes
  • Dror L. Angel
  • Keith M. Bayha
  • Dacha Atienza
  • Dor Edelist
  • Cesar Bordehore
  • Josep-Maria Gili
  • Jennifer E. Purcell
JELLYFISH BLOOMS

Abstract

Blooms of the invasive ctenophore, Mnemiopsis leidyi, occurred in 2009 along the Mediterranean Sea coasts of Spain and Israel. This voracious zooplanktivore spread throughout the Black Sea basin after its introduction in the early 1980s, throughout northern European coastal waters, and now occurs throughout the Mediterranean Sea. M. leidyi occurred throughout the summer along the entire Catalan Spanish and Israeli coasts in 2009. Those locations had high temperatures (18–26°C) and salinities (37–38) during the blooms. The patterns of abundance of large jellyfish along the Catalan coast were unusual in 2009, with low numbers during July, August, and September when ctenophores were abundant. Small populations of those potential predators and food competitors of M. leidyi could have contributed to the ctenophore bloom. The identity of the ctenophores from Spain and Israel was confirmed as M. leidyi by molecular analysis based on DNA sequencing of the nuclear internal transcribed spacer (ITS) regions. This is the first molecular confirmation of M. leidyi in the Mediterranean Sea. Most ctenophores had an ITS genotype previously found in M. leidyi from other invaded regions (the Black, Azov, and Mediterranean seas), as well as native regions in the United States, suggesting common ancestry. Based on the circulation patterns of Mediterranean surface waters and shipping activities, we conclude that the spread of M. leidyi in the Mediterranean probably resulted from re-introductions by ballast water transport and subsequent distribution by currents. We also conclude that the near-simultaneous blooms in opposite ends of both the Mediterranean basins indicate that M. leidyi is resident around the Mediterranean. We discuss environmental conditions, food, and predators of M. leidyi in both regions that would influence the future effects of this voracious consumer on the pelagic food web of the Mediterranean Sea.

Keywords

Jellyfish Zooplankton Climate Israel Spain 

Notes

Acknowledgments

Thanks are due to the Catalan Water Agency for funding the Medusa Project. We are indebted to all institutions collaborating with the reporting network. We thank the Haifa University Maritime Workshop for their help in collecting M. leidyi at sea; G. Yahel and the School of Marine Sciences and Marine Environment, Ruppin Academic Center, Michmoret Israel for provision of zooplankton abundance data; N. Drimmer at CAMERI - Coastal and Marine Engineering Research Institute Ltd. for the Israel Ports Development & Assets Company Ltd. for the sea-surface temperature data, and A. Glazer at the Israel Electric Corporation for sea-surface temperature and salinity data. All molecular work was performed in the lab of Dr. Michael N Dawson at the University of California Merced.

References

  1. Altschul, S. F., T. L. Madden, A. A. Schäffer, J. Zhang, Z. Zhang, W. Miller & D. J. Lipman, 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Research 25: 3389–3402.CrossRefPubMedGoogle Scholar
  2. Arnheim, N., M. Krystal, R. Schmickel, G. Wilson, O. Ryder & E. Zimmer, 1980. Molecular evidence for genetic exchanges among ribosomal genes on nonhomolohous chromosomes in man and apes. Proceedings of the National Academy of Sciences, USA 77: 7323–7327.CrossRefGoogle Scholar
  3. Bas, C., F. Maynou, F. Sardà & J. Leonard, 2003. Variacions demogràfiques a les poblacions d’espècies demersals explotades: es darrers quaranta anys a Blanes i Barcelona. Institut d’Estudis Catalans. Secció de Ciències Biològiques Vol. 135: 202 pp.Google Scholar
  4. Bayha, K. M., 2005. The molecular systematics and population genetics of four coastal ctenophores and scyphozoan jellyfish of the U.S. Atlantic and Gulf of Mexico. Ph.D. Dissertation, The University of Delaware, Newark.Google Scholar
  5. Bayha, K. M., G. R. Harbison, J. H. McDonald & P. M. Gaffney, 2004. Preliminary investigation on the molecular systematics of the invasive ctenophore Beroe ovata. In Dumont, H., T. A. Shiganova & U. Niermann (eds), Aquatic Invasions in the Black, Caspian and Mediterranean Seas. Kluwer Academic Publishers, Dordrecht: 167–175.CrossRefGoogle Scholar
  6. Boero, F., M. Putti, E. Trainito, E. Prontera, S. Piraino & T. Shiganova, 2009. Recent changes in Western Mediterranean Sea biodiversity: the establishment of Mnemiopsis leidyi (Ctenophora) and the arrival of Phyllorhiza punctata (Cnidaria). Aquatic Invasions 4: 675–680.CrossRefGoogle Scholar
  7. Calbet, A., S. Garrido, E. Saiz, M. Alcaraz & C. M. Duarte, 2001. Annual zooplankton succession in coastal NW Mediterranean waters: the importance of the smaller size fractions. Journal of Plankton Research 23: 319–331.CrossRefGoogle Scholar
  8. CAMERI (Coastal and Marine Engineering Institute of the Technion), 2008. Annual report for the Israel Ports Development & Assets Company Ltd, http://eng.israports.co.il/.
  9. Coll, M., I. Palomera, S. Tudela & F. Sardà, 2006. Trophic flows, ecosystem structure and fishing impacts in the South Catalan Sea, Northwestern Mediterranean. Journal of Marine Systems 59: 63–96.CrossRefGoogle Scholar
  10. Costello, J. H., B. K. Sullivan & D. J. Gifford, 2006a. A physical–biological interaction underlying variable phonological responses to climate change by coastal zooplankton. Journal of Plankton Research 28: 1099–1105.CrossRefGoogle Scholar
  11. Costello, J. H., B. K. Sullivan, D. Van Keuren & D. J. Gifford, 2006b. Seasonal refugia, shoreward thermal amplification, and metapopulation dynamics of the ctenophore Mnemiopsis leidyi in Narragansett Bay, Rhode Island. Limnology and Oceanography 51: 1819–1831.CrossRefGoogle Scholar
  12. Cushing, D. H., 1989. A difference in structure between ecosystems in strongly stratified waters and in those that are only weakly stratified. Journal of Plankton Research 11: 1–13.CrossRefGoogle Scholar
  13. Dawson, M. N., K. A. Raskoff & D. K. Jacobs, 1998. Preservation of marine invertebrate tissues for DNA analyses. Molecular Marine Biology and Biotechnology 7: 145–152.PubMedGoogle Scholar
  14. Estrada, M., 1996. Primary production in the northwestern Mediterranean. Scientia Marina 60(Suppl. 2): 55–64.Google Scholar
  15. Faasse, M. A. & K. M. Bayha, 2006. The ctenophore Mnemiopsis leidyi A. Agassiz 1865 in coastal waters of the Netherlands: an unrecognized invasion? Aquatic Invasions 1: 270–277.CrossRefGoogle Scholar
  16. Faris, S., 2009. A gelatinous invasion. Time 174: 47–48.Google Scholar
  17. Fernández de Puelles, M. L., F. Alemany & J. Jansá, 2007. Zooplankton time-series in the Balearic Sea (Western Mediterranean): variability during the decade 1994–2003. Progress in Oceanography 74: 329–354.CrossRefGoogle Scholar
  18. Font, J., J. Salat & J. Tintoré, 1988. Permanent features of the circulation in the Catalan Sea. Oceanologica Acta 1988: 51–57.Google Scholar
  19. Foshtomi, M. Y., B. Abtahi, A. E. Sari & M. Taheri, 2007. Ion composition and osmolarity of Caspian Sea ctenophore, Mnemiopsis leidyi, in different salinities. Journal of Experimental Marine Biology and Ecology 352: 28–34.CrossRefGoogle Scholar
  20. Fuentes, V. L., D. Atienza, J.-M. Gili & J. E. Purcell, 2009. First records of Mnemiopsis leidyi A. Agassiz 1865 off the NW Mediterranean coast of Spain. Aquatic Invasions 4: 671–674.CrossRefGoogle Scholar
  21. Galil, B. S., 2007. Seeing red: alien species along the Mediterranean coast of Israel. Aquatic Invasions 2: 281–312.CrossRefGoogle Scholar
  22. Galil, B. S., E. Spanier & W. W. Ferguson, 1990. The scyphomedusae of the Mediterranean coast of Israel, including two Lessepsian migrants new to the Mediterranean. Zoologische Mededelingen 64: 95–105.Google Scholar
  23. Galil, B. S., N. Kress & T. A. Shiganova, 2009. First record of Mnemiopsis leidyi A. Agassiz, 1865 (Ctenophora Lobata Mnemiidae) off the Mediterranean coast of Israel. Aquatic Invasions 4: 356–362.Google Scholar
  24. García, E., J. Tintoré, J. Pinot, J. Font & M. Manríquez, 1994. Surface circulation and dynamics of the Balearic Sea. Coastal and Estuarine Studies 46: 73–91.Google Scholar
  25. GESAMP (IMO/FAO/UNESCO-IOC/WMO/WHO/IAEA/UN/UNEP Joint Group of Experts on the Scientific Aspects of Marine Environmental Protection), 1997. Opportunistic settlers and the problem of the ctenophore Mnemiopsis leidyi invasion in the Black Sea. Report and Studies GESAMP 58: 84 pp.Google Scholar
  26. Gili, J. M. & F. Pagés, 2005. Les proliferacions de meduses. Bolletí de la Societat d’Història Natural de les Balears 48: 9–22.Google Scholar
  27. Gili, J. M., V. Fuentes & D. Atienza, 2007. Medusa project: data year 2007. Technical report No. 1: 98 pp.Google Scholar
  28. Gili, J. M., V. Fuentes & D. Atienza, 2008. Medusa project: data year 2008. Technical report No. 2: 198 pp.Google Scholar
  29. Gorokhova, E., M. Lehtiniemi, S. Viitasalo-Frosen & S. H. D. Haddock, 2009. Molecular evidence for the occurrence of ctenophore Mertensia ovum in the northern Baltic Sea and implications for the status of the Mnemiopsis leidyi invasion. Limnology and Oceanography 54: 2025–2033.Google Scholar
  30. Hamad, N., C. Millot & I. Taupier-Letage, 2005. A new hypothesis about the surface circulation in the eastern basin of the Mediterranean Sea. Progress in Oceanography 66: 287–298.CrossRefGoogle Scholar
  31. Herut, B., E. Shefer & Y. Cohen, 2005. Environmental quality of Israel’s Mediterranean coastal waters in 2004. IOLR Report H34/2005.Google Scholar
  32. Herut, B., Y. Cohen, E. Shefer, N. Gordon, B. Galil, G. Tibor & M. Tom, 2006. Environmental quality of Israel’s Mediterranean coastal waters in 2005. IOLR Report H25/2006.Google Scholar
  33. Herut, B., E. Shefer, N. Gordon, B. Galil, G. Tibor & M. Tom, 2008. Environmental quality of Israel’s Mediterranean coastal waters in 2007. IOLR Report H52/2008.Google Scholar
  34. IEC (Israel Electric Corporation), 2009. Environmental report 2009 (in preparation).Google Scholar
  35. Isinibilir, M. & A. N. Tarkan, 2002. Distribution of the invasive ctenophore Mnemiopsis leidyi in the north-eastern Aegean Sea in August 1998. Turkish Journal of Fisheries and Aquatic Sciences 2: 129–132.Google Scholar
  36. Ivanov, V. P., A. M. Kamakin, V. B. Ushivtsev, T. A. Shiganova, O. P. Zhukova, N. Aladin, S. I. Wilson, G. R. Harbison & H. J. Dumont, 2000. Invasion of the Caspian Sea by the comb jellyfish Mnemiopsis leidyi (Ctenophora). Biological Invasions 2: 255–258.CrossRefGoogle Scholar
  37. Javidpour, J., U. Sommer & T. A. Shiganova, 2006. First record of Mnemiopsis leidyi A. Agassiz 1865 in the Baltic Sea. Aquatic Invasions 1: 299–302.CrossRefGoogle Scholar
  38. Javidpour, J., J. Molinero & J. Peschutter, 2008. Seasonal changes and population dynamics of the ctenophore Mnemiopsis leidyi after its first year of invasion in the Kiel Fjord, Western Baltic sea. Biological Invasions. doi:10.1007/s10530-008-9300-8.
  39. Kamburska, L. & S. Fonda-Umani, 2009. From seasonal to decadal inter-annual variability of mesozooplankton biomass in the Northern Adriatic Sea (Gulf of Trieste). Journal of Marine Systems 78: 490–504.CrossRefGoogle Scholar
  40. Kideys, A. E. & U. Niermann, 1993. Intrusion of Mnemiopsis mccradyi (Ctenophora; Lobata) into the Mediterranean Sea. Senckenbergiana Maritima 23: 43–47.Google Scholar
  41. Kideys, A. E. & U. Niermann, 1994. Occurrence of Mnemiopsis along the Turkish coasts (from northeastern Mediterranean to Istanbul). ICES Journal of Marine Science 51: 423–427.CrossRefGoogle Scholar
  42. Kremer, P., 1994. Patterns of abundance for Mnemiopsis in US coastal waters: a comparative overview. ICES Journal of Marine Science 51: 347–354.CrossRefGoogle Scholar
  43. Kube, S., L. Postel, C. Honnef & C. B. Augustin, 2007. Mnemiopsis leidyi in the Baltic Sea – distribution and overwintering between autumn 2006 and spring 2007. Aquaic Invasions 2: 137–145.CrossRefGoogle Scholar
  44. Lehtiniemi, M., J. P. Pääkkönen, J. Flinkman, T. Katajisto, E. Gorokhova, M. Karajalanein, S. Viitasalo & H. Björk, 2007. Distribution and abundance of the American comb jelly (Mnemiopsis leidyi) – a rapid invasion to the northern Baltic Sea during 2007. Aquatic Invasions 2: 445–449.CrossRefGoogle Scholar
  45. Leonard, J. & F. Maynou, 2003. Fish stocks assessment in the Mediterranean: state of the art. In Ulltang, O. & G. Blom (eds), Fish Stocks Assessments and Predictions: Integrating Relevant Knowledge. Scientia Marina 67 (Suppl. 1): 37–49.Google Scholar
  46. Lotan, A., R. Ben-Hillel & Y. Loya, 1992. Life cycle of Rhopilema nomadica: a new immigrant scyphomedusan in the Mediterranean. Marine Biology 112: 237–242.CrossRefGoogle Scholar
  47. Monserrat, S., J. L. López-Jurado & M. Marcos, 2008. A mesoscale index to describe the regional circulation around the Balearic Islands. Journal of Marine Systems 71: 413–420.CrossRefGoogle Scholar
  48. OCEANA, 2008. Illes Balears: propuesta para la gestión de habitat amenazados y la pezca, http://oceana.org/fileadmin/oceana/uploads/europe/reports/Illes_Balears_OCEANA.pdf.
  49. Oguz, T., 2005. Long-term impacts of anthropogenic forcing on the Black Sea ecosystem. Oceanography 18: 112–121.Google Scholar
  50. Oguz, T., B. Fach & B. Salihoglu, 2008. Invasion dynamics of the alien ctenophore Mnemiopsis leidyi and its impact on anchovy collapse in the Black Sea. Journal of Plankton Research 30: 1385–1397.CrossRefGoogle Scholar
  51. Pisanty, S. & E. Grofit, 1991. Limiting effort in the Israeli trawl fishery. Fisheries and Fishbreeding in Israel 24: 100–133. (in Hebrew with English abstract).Google Scholar
  52. Podar, M., S. H. D. Haddock, M. L. Sogin & G. R. Harbison, 2001. A molecular genetic framework for the phylum Ctenophora using 18s rRNA genes. Molecular Phylogenetics and Evolution 21: 218–230.CrossRefPubMedGoogle Scholar
  53. Purcell, J. E., 1988. Quantification of Mnemiopsis leidyi (Ctenophora, Lobata) from formalin-preserved plankton samples. Marine Ecology Progress Series 45: 197–200.CrossRefGoogle Scholar
  54. Purcell, J. E., 1991. Predation by Aequorea victoria on other species of potentially competing pelagic hydrozoans. Marine Ecology Progress Series 72: 255–260.CrossRefGoogle Scholar
  55. Purcell, J. E. & M. B. Decker, 2005. Effects of climate on relative predation by scyphomedusae and ctenophores on copepods in Chesapeake Bay during 1987–2000. Limnology and Oceanography 50: 376–387. http://aslo.org/lo/toc/vol_50/issue_1/0376.pdf.
  56. Purcell, J. E., T. A. Shiganova, M. B. Decker & E. D. Houde, 2001. The ctenophore Mnemiopsis in native and exotic habitats: U.S. estuaries versus the Black Sea basin. Hydrobiologia 451: 145–176.CrossRefGoogle Scholar
  57. Rapoza, R., D. Novak & J. H. Costello, 2005. Life-stage dependent, in situ dietary patterns of the lobate ctenophore Mnemiopsis leidyi Agassiz 1865. Journal of Plankton Research 27: 951–956.CrossRefGoogle Scholar
  58. REMPEC (Regional Marine Pollution Emergency Response Centre for the Mediterranean Sea), 2008. Study of maritime traffic flows in the Mediterranean Sea. Final report, Unrestricted Version, EU-Funded MEDA Regional Project MED 2005/109-573.Google Scholar
  59. Riisgård, H. U., L. Bøttiger, C. V. Madsen & J. E. Purcell, 2007. Invasive ctenophore Mnemiopsis leidyi in Limfjorden (Denmark) in late summer 2007 – assessment of abundance and predation effects. Aquatic Invasions 2: 395–401.CrossRefGoogle Scholar
  60. Rosentraub, Z. & S. Brenner, 2007. Circulation over the southeastern continental shelf and slope of the Mediterranean Sea: direct current measurements, winds, and numerical model simulations. Journal of Geophysical Research: Oceans 112(C11001): 1–21.Google Scholar
  61. Sabatés, A., M. P. Olivar, J. Salat, I. Palomera & F. Alemany, 2007. Physical and biological processes controlling the distribution of fish larvae in the NW Mediterranean. Progress in Oceanography 74: 355–376.CrossRefGoogle Scholar
  62. Sabatés, A., F. Pagès, D. Atienza, V. Fuentes, J. E. Purcell & J.-M. Gili, this volume. Planktonic cnidarian distribution and feeding of Pelagia noctiluca from near shore to open sea in the NW Mediterranean. Hydrobiologia. doi:10.1007/s10750-010-0221-z.
  63. Saiz, E., A. Calbet, D. Atienza & M. Alcaraz, 2007. Feeding and production of zooplankton in the Catalan Sea (NW Mediterranean). Progress in Oceanography 74: 313–328.CrossRefGoogle Scholar
  64. Salat, J., 1995. The circulation between the Catalan and Balearic currents in the southern Catalan Sea. Oceanologica Acta 18: 227–234.Google Scholar
  65. Shiganova, T. A. & A. Malej, 2009. Native and non-native ctenophores in the Gulf of Trieste, Northern Adriatic Sea. Journal of Plankton Research 31: 61–71.CrossRefGoogle Scholar
  66. Shiganova, T. A., Z. A. Mirzoyan, E. A. Studenikina, S. P. Volovik, I. Siokou-Frangou, S. Zervoudaki, E. D. Christou, A. Y. Skirta & H. J. Dumont, 2001. Population development of the invader ctenophore Mnemiopsis leidyi in the Black Sea and other seas of the Mediterranean basin. Marine Biology 139: 431–445.CrossRefGoogle Scholar
  67. Shiganova, T. A., E. D. Christou, J. V. Bulgakova, I. Siokou-Frangou, S. Zervoudaki & A. Siapatis, 2004. Study on the distribution and biology of the invader M. leidyi in the northern Aegean Sea, comparison with indigenous species Bolinopsis vitrea. In Dumont, H., T. A. Shiganova & U. Niermann (eds), The Ctenophore Mnemiopsis leidyi in the Black, Caspian and Mediterranean Seas and Other Aquatic Invasions. NATO Science Series: IV. Earth and Environmental Sciences, Vol. 35. Kluwer Academic Publishers, Dordrecht: 113–135.Google Scholar
  68. Siapatis, A., M. Giannoulaki, V. D. Valavanis, A. Palialexis, E. Schismenou, A. Machias & S. Somarakis, 2008. Modelling potential habitat of the invasive ctenophore Mnemiopsis leidyi in Aegean Sea. Hydrobiologia 612: 281–295.CrossRefGoogle Scholar
  69. Spanier, E., & B. S. Galil, 1991. Lessepsian migration: a continuous biogeographical process. Endeavour 15: 102–106.CrossRefGoogle Scholar
  70. Sullivan, L. J., & D. J. Gifford, 2004. Diet of the larval ctenophore Mnemiopsis leidyi A. Agassiz (Ctenophora, Lobata). Journal of Plankton Research 26: 417–431.CrossRefGoogle Scholar
  71. Sullivan, B. K., D. Van Keuren & M. Claucy, 2001. Timing and size of blooms of the ctenophore Mnemiopsis leidyi in relation to temperature in Narragansett Bay, RI. Hydrobiologia 451: 113–120.CrossRefGoogle Scholar
  72. Vinogradov, M. E. & E. A. Shushkina, 1992. Temporal changes in community structure in the open Black Sea. Oceanology 32: 485–491.Google Scholar
  73. Vinogradov, M. E., E. A. Shushkina, E. I. Musayeva & P. Y. Sorokin, 1989. A newly acclimated species in the Black Sea: the ctenophore Mnemiopsis leidyi (Ctenophora: Lobata). Oceanology 29: 220–224.Google Scholar
  74. Vollmer, S. V. & S. R. Palumbi, 2004. Testing the utility of internal transcribed spacer sequences in coral phylogenetics. Molecular Ecology 13: 2763–2772.CrossRefPubMedGoogle Scholar
  75. Zviely, D., E. Kit & M. Klein, 2007. Longshore sand transport estimates along the Mediterranean coast of Israel in the Holocene. Marine Geology 238: 61–73.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  • Verónica L. Fuentes
    • 1
  • Dror L. Angel
    • 2
  • Keith M. Bayha
    • 3
    • 4
  • Dacha Atienza
    • 1
  • Dor Edelist
    • 2
  • Cesar Bordehore
    • 5
  • Josep-Maria Gili
    • 1
  • Jennifer E. Purcell
    • 6
    • 7
  1. 1.Institut de Ciencies del Mar, CSICBarcelonaSpain
  2. 2.Department of Maritime Civilizations, Leon Recanati Institute of Maritime StudiesUniversity of HaifaHaifaIsrael
  3. 3.University of California Merced, School of Natural SciencesMercedUSA
  4. 4.Dauphin Island Sea LabDauphin IslandUSA
  5. 5.Departamento de EcologíaUniversidad de AlicanteAlicanteSpain
  6. 6.Western Washington University, Shannon Point Marine CenterAnacortesUSA
  7. 7.Coastal and Marine Resources Centre, University College CorkCobhIreland

Personalised recommendations