Hydrobiologia

, Volume 645, Issue 1, pp 81–96 | Cite as

Recurrence of bloom-forming scyphomedusae: wavelet analysis of a 200-year time series

  • Tjaša Kogovšek
  • Branko Bogunović
  • Alenka Malej
JELLYFISH BLOOMS

Abstract

Four meroplanktonic scyphomedusae, Aurelia aurita, Chrysaora hysoscella, Cotylorhiza tuberculata and Rhizostoma pulmo, and the holoplanktonic, non-resident Pelagia noctiluca have formed blooms in the northern Adriatic over the last 200 years. Published data about the historical occurrences of these five scyphomedusae, in combination with our data, were used to analyse their long-term fluctuations in this northernmost part of the Mediterranean Sea. Analysis of the most recent blooms was complemented with environmental descriptors (temperature, salinity, pH, chlorophyll a, zooplankton dry weight and major river discharges). Continuous wavelet transformation analysis of the historical time series of scyphomedusae occurrences and environmental parameters revealed that the five species have been present regularly in the northern Adriatic over the last 200 years, with two major periods of jellyfish proliferations. The first period in the years around 1910 was characterised by significant periodicity of 8–12 years for each species, while the second period from the 1960s onwards was characterised by a shortened significant periodicity of less than 8 years. Pelagia noctiluca fluctuations were analysed in greater detail for the last four decades, revealing significant periodicities of ~10 years, 2.5 years, 8–14 months, and 8 months. The significantly marked periodicity of about 10 years in the P. noctiluca spectrum indicates a pattern similar to that observed in the western Mediterranean. Wavelet analysis showed that the periodicity of occurrence of five jellyfish species has shortened in recent decades and the recurrence of blooms has increased, particularly for A. aurita and R. pulmo.

Keywords

Time series Fluctuations Wavelet analysis Mediterranean Sea Jellyfish 

Notes

Acknowledgements

This research was supported by the Slovenian Research Agency Program P1-0237, and European Commission 6th Framework Programme: SESAME project (Contract No GOCE-036949).

References

  1. Avian, M. & L. Rottini Sandrini, 1994. History of Scyphomedusae in the Adriatic Sea. Bolletino della Societa Adriatica di Scienze 75: 5–12.Google Scholar
  2. Babić, K., 1913. Planktonički celenterati iz Jadranskog mora. Rad Jugoslavenske Akademije Znanosti i Umjetnosti 200: 186–202.Google Scholar
  3. Berline, L., F. Ibanez & P. Grosgean, 2009. Roadmap for Zooplankton Time Series Analysis. SESAME WP 1. Unpublished.Google Scholar
  4. Brodeur, R. D., C. E. Mills, J. E. Overland, G. E. Walters & J. D. Schumacher, 1999. Evidence for a substantial increase in gelatinous zooplankton in the Bering Sea, with possible links to climate change. Fisheries Oceanography 8: 296–306.CrossRefGoogle Scholar
  5. Celio, M., V. Malačič, A. Bussani, B. Čermelj, C. Comici & B. Petelin, 2006. The coastal scale observing system component of ADRICOSM: Gulf of Trieste network. Acta Adriatica 47(Suppl): 65–79.Google Scholar
  6. CIESM, 2001. Gelatinous Zooplankton Outbreaks: Theory and Practice. CIESM Workshop Series 14, Monaco: 112 pp.Google Scholar
  7. Comici, C. & A. Bussani, 2007. Analysis of the River Isonzo discharge (1998–2005). Bolletino di Oceanologia Teorica ed Applicata 8: 435–454.Google Scholar
  8. Cori, D. J. & A. Steuer, 1901. Beobachtungen über das Plankton des Triester Golfes in den Jahren 1899 und 1900. Zoologischer Anzeiger 24: 111–116.Google Scholar
  9. Cushman-Roisin, B., M. Gačić, P. M. Poulain & A. Artegiani, 2001. Physical Oceanography of the Adriatic Sea: Past, Present and Future. Kluwer Academic Publisher, Dordrecht.Google Scholar
  10. de Wit, M. & G. Bendoricchio, 2001. Nutrient fluxes in the Po basin. Science of the Total Environment 273: 147–161.CrossRefPubMedGoogle Scholar
  11. Del Negro, P., F. Kokelj, A. Tubaro & R. Della Loggia, 1992. Chrysaora hysoscella in the Gulf of Trieste: presence, evolution and cutaneous toxicity in man. Science of the Total Environment (Suppl): 427–430.Google Scholar
  12. Di Camillo, C. G., F. Betti, M. Bo, M. Martinelli, S. Puce & G. Bavestrello, 2010. Contribution to the understanding of seasonal cycle of Aurelia aurita (Cnidaria, Scyphozoa) scyphopolyps in the northern Adriatic Sea. Journal of the Marine Biological Association of the United Kingdom. doi:10.1017/S0025315409000848.Google Scholar
  13. Dulčić, J., B. Grbec, L. Lipej, G. Beg Paklar, N. Supić & T. Smirčić, 2004. The effect of the hemispheric climatic oscillations on the Adriatic ichthyofauna. Environmental Bulletin 13: 293–298.Google Scholar
  14. Gaggiotti, O. E. & I. Hanski, 2004. Mechanisms of population extinction. In Hanski, I. & O. E. Gaggiotti (eds), Ecology, Genetics, and Evolution of Metapopulations. Elsevier Academic Press, Amsterdam: 337–366.CrossRefGoogle Scholar
  15. Giorgi, R., M. Avian, L. Rottini Sandrini & A. Troian, 1985. Monitoraggio meduse e danni alla pesca: analisi a breve termine del Golfo di Trieste. Nova Thalassia 7: 55–62.Google Scholar
  16. Goy, J., P. Morand & M. Etienne, 1989. Long term fluctuations of Pelagia noctiluca (Cnidaria, Scyphomedusae) in the western Mediterranean Sea, Prediction by climatic variables. Deep-Sea Research 36: 269–279.CrossRefGoogle Scholar
  17. Graeffe, E., 1875. Seethierfauna des Golfes von Triest. III. Coelenteraten, Cnidaria. Arbeiten aus dem Zoologischen Institut der Universität Wien und der Zoologischen Station in Triest 5: 333–362.Google Scholar
  18. Graham, W. M., 2001. Numerical increases and distribution shifts of Chrysaora quinquecirrha (Desor) and Aurelia aurita (Linné) (Cnidaria: Scyphozoa) in the northern Gulf of Mexico. Hydrobiologia 451: 97–111.CrossRefGoogle Scholar
  19. Grbec, B., I. Vilibić, A. Bajić, M. Morović, G. Bec Paklar & V. Dadić, 2007. Response of the Adriatic Sea to the atmospheric anomaly in 2003. Annales Geophysicae 25: 835–846.CrossRefGoogle Scholar
  20. Grinsted, A., J. C. Moore & S. Jevrejeva, 2004. Application of the cross wavelet transform and wavelet coherence to geophysical time series. Nonlinear Processes in Geophysics 11: 561–566.Google Scholar
  21. Hays, G. C., A. J. Richardson & C. Robinson, 2005. Climate change and marine plankton. Trends in Ecology and Evolution 20: 337–344.CrossRefPubMedGoogle Scholar
  22. Holm-Hansen, O., C. J. Lorenzen, R. W. Holmes & J. D. H. Strickland, 1965. Fluorometric determination of chlorophyll. Journal du Conseil permanent International pour l’ Exploration de la Mer 30: 3–15.Google Scholar
  23. Hsieh, C. H., S. M. Glaser, A. J. Lucas & G. Sugihara, 2005. Distinguishing random environmental fluctuations from ecological catastrophes for the North Pacific Ocean. Nature 435: 336–340.CrossRefPubMedGoogle Scholar
  24. Issel, R., 1922. Nuove indagini sul plankton nelle acque di Rovigno. Rapporti Comitato Talassografico Italiano, Memoria 102: 1–36.Google Scholar
  25. Kamburska, L. & S. Fonda Umani, 2006. Long-term copepod dynamics in the Gulf of Trieste (northern Adriatic Sea): recent changes and trends. Marine Ecology Progress Series 31: 195–203.Google Scholar
  26. Kohama, T., N. Shinya, N. Okuda, H. Miyasaka & H. Takeoka, 2006. Estimation of trophic level of Aurelia aurita using stable isotope ratios in Uwa Sea, Japan. In Proceedings of COE International Symposium 2006 (Ehime University, Matsuyama, Japan). Pioneering Studies of Young Scientists on Chemical Pollution and Environmental changes.Google Scholar
  27. Kuzmić, M. & M. Orlić, 2006. Modeling the northern Adriatic double-gyre response to intense bora wind: a revisit. Journal of Geophysical Research. doi:10.1029/2005JC003377.
  28. Lilley, M. K. S., J. D. R. Houghton & G. C. Hays, 2009. Distribution, extent of inter-annual variability and diet of the bloom-forming jellyfish Rhizostoma in European waters. Journal of the Marine Biological Association of the United Kingdom 89: 39–48.CrossRefGoogle Scholar
  29. Lynam, C. P., S. J. Hay & A. S. Brierley, 2004. Interannual variability in abundances of North Sea jellyfish and links to the North Atlantic Oscillation. Limnology and Oceanography 49: 637–643.Google Scholar
  30. Lyons, D. M., I. Janeković, R. Precali & N. Supić, 2006. Northern Adriatic Sea hydrographic conditions from October 2002–September 2003 including the climatic heating anomaly of summer 2003. Acta Adriatica 47(Suppl): 81–96.Google Scholar
  31. Malačič, V., 1991. Estimation of the vertical eddy diffusion coefficient of heat in the Gulf of Trieste (Northern Adriatic). Oceanologica Acta 14: 23–32.Google Scholar
  32. Malačič, V. & B. Petelin, 2009. Climatic circulation in the Gulf of Trieste (northern Adriatic). Journal of Geophysical Research 114. doi:10.1029/2008JC004904.
  33. Malačič, V., M. Celio, B. Čermelj, A. Bussani & C. Comici, 2006. Interannual evolution of seasonal thermohaline properties in the Gulf of Trieste (northern Adriatic) 1991–2003. Journal of Geophysical Research 111. doi:10.1029/2005JC003267.
  34. Malej, A., 1982. Unusual occurrence of Pelagia noctiluca in the Adriatic. Acta Adriatica 23(1/2): 97–102 (in Slovenian).Google Scholar
  35. Malej, A., 1989. Shifts in size-classes and structure of net zooplankton in the presence of the jellyfish Pelagia noctiluca (Scyphozoa). Biološki Vestnik 37: 35–46.Google Scholar
  36. Malej, A., 2001. Are irregular plankton phenomena getting more frequent in the northern Adriatic Sea? In Gelatinous Zooplankton Outbreaks: Theory and Practice. CIESM Workshop Series 14, Monaco: 16–18.Google Scholar
  37. Malej, A. & M. Malej, 1992. Population dynamics of the jellyfish Pelagia noctiluca (Forsskål, 1775). In Colombo, G., et al. (eds), Marine Eutrophication and Population Dynamics. Proceedings of the 25th EMBS. Olsen and Olsen, Fredensborg: 215–219.Google Scholar
  38. Malej, A. & A. Malej, 2004. Invasion of the jellyfish Pelagia noctiluca in the northern Adriatic: a non-success story. In Dumont, H., et al. (eds), Aquatic Invasions in the Black, Caspian, and Mediterranean Seas. NATO ASI Series 5, Vol. 35. Kluwer Academic Publisher, Dordrecht: 273–285.Google Scholar
  39. Malej, A., V. Turk, D. Lučić & A. Benović, 2007. Direct and indirect trophic interactions of Aurelia sp. (Scyphozoa) in a stratified marine environment (Mljet Lakes, Adriatic Sea). Marine Biology 151: 827–841.CrossRefGoogle Scholar
  40. Malej M., A. Malej & A. Malej, 2007. The use of modified Leslie matrix and genetic algorithms to model jellyfish population (Pelagia noctiluca, Scyphozoa). In Proceedings of 6th European Conference on Ecological Modelling, ECEM ’07: 326–327.Google Scholar
  41. Miloš, Č., 2009. Biometry and elemental analysis of scyphomedusae in the Gulf of Trieste with emphasis on Rhizostoma pulmo. M.Sc. thesis, University of Zagreb: 81 pp.Google Scholar
  42. Molinero, J. C., M. Casini & E. Buecher, 2008. The influence of the Atlantic and regional climate variability on the long-term changes in gelatinous carnivore populations in the northwestern Mediterranean. Limnology and Oceanography 53: 1456–1467.Google Scholar
  43. Mozetič, P., C. Solidoro, G. Cossarini, G. Socal, R. Precali, J. France, F. Bianchi, C. De Vittor, N. Smodlaka & S. Fonda Umani, 2009. Recent trends towards oligotrophication of the northern Adriatic: evidence from chlorophyll a time series. Estuaries and Coast. doi:10.1007/s1223-009-9191-7.
  44. Percival, D. B. & A. T. Walden, 2000. Wavelet Methods for Time Series Analysis. Cambridge University Press, Cambridge, UK.Google Scholar
  45. Piccinetti, C. & G. Piccinetti Manfrin, 1991. Considerations sur la distribution de Pelagia noctiluca (Forskǻl) dans l’Adriatique de 1976 a 1987. 2nd Workshop on Jellyfish in the Mediterranean, Trieste, 1987. MAP Technical Reports Series 47: 133–140 (in French).Google Scholar
  46. Piccinetti Manfrin, G. & C. Piccinetti, 1986. Distribuzione di Pelagia noctiluca in Adriatico dal 1983 e 1984. Nova Thalassia 8(Suppl): 103–106.Google Scholar
  47. Purcell, J. E., 2005. Climate effects on formation of jellyfish and ctenophore blooms: a review. Journal of Marine Biology Association of United Kingdom 85: 461–476.CrossRefGoogle Scholar
  48. Purcell, J. E., 2009. Extension of methods for jellyfish and ctenophore trophic ecology to large-scale research. Hydrobiologia 616: 23–50.CrossRefGoogle Scholar
  49. Purcell, J. E., S.-I. Uye & W.-T. Lo, 2007. Anthropogenic causes of jellyfish blooms and direct consequences for humans: a review. Marine Ecology Progress Series 350: 153–174.CrossRefGoogle Scholar
  50. Rottini Sandrini, L. & M. Avian, 1991. Reproduction of Pelagia noctiluca in the central and northern Adriatic. Hydrobiologia 216(217): 197–202.CrossRefGoogle Scholar
  51. Sournia, A., 1973. La production primaire planctonique en Méditerranée. Essai de mise a jour. Bulletin Etude en commun de la Méditerranée 5: 1–128.Google Scholar
  52. Steuer, A., 1902. Beobachtungen über das Plankton des Triester Golfes im Jahre 1901. Zoologischer Anzeiger 25: 371–372.Google Scholar
  53. Steuer, A., 1904. Beobachtungen über das Plankton des Triester Golfes im Jahre 1902. Zoologischer Anzeiger 27: 145–148.Google Scholar
  54. Stiasny, G., 1909. Beobachtungen über die marine Fauna des Triester Golfes im Jahre 1908. Zoologischer Anzeiger 34: 289–294.Google Scholar
  55. Stiasny, G., 1910. Beobachtungen über die marine Fauna des Triester Golfes im Jahre 1909. Zoologischer Anzeiger 35: 583–587.Google Scholar
  56. Stiasny, G., 1911. Beobachtungen über die marine Fauna des Triester Golfes während des Jahres 1910. Zoologischer Anzeiger 37: 517–522.Google Scholar
  57. Stiasny, G., 1912. Beobachtungen über die marine Fauna des Triester Golfes im Jahre 1911. Zoologischer Anzeiger 39: 604–608.Google Scholar
  58. Stiasny, G., 1914. Zwei neue Pelagien aus der Adria. Zoologischer Anzeiger 44: 529–533.Google Scholar
  59. Stiasny, G., 1919. Die Scyphomedusen-Sammlung des Naturhistoricshen Reichmuseum in Leiden. Stauromedusae, Coronatae, Semaeostomae. Zoologische Mededelingen 5: 66–99.Google Scholar
  60. Szüts, A., 1915. Biologische Beobachtungen wahrend der ersten und zweiten terminfahrt des Ungarischen Adriavereins an S.M.S. “Najade” im Oktober 1913 und im April–Mai 1914. Zoologischer Anzeiger 45: 432–442.Google Scholar
  61. Stopar, K., A. Ramšak, P. Trontelj & A. Malej, submitted. Molecular evidence for panmixia in mauve stinger, Pelagia noctiluca, in European seas.Google Scholar
  62. Torrence, C. & G. P. Compo, 1998. A practical guide to wavelet analysis. Bulletin of the American Meteorological Society 79: 61–78.CrossRefGoogle Scholar
  63. Zanchettin, D., P. Traverso & M. Tomasino, 2008. Po River discharges: a preliminary analysis of a 200-year time series. Climatic Change 89: 411–433.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  • Tjaša Kogovšek
    • 1
  • Branko Bogunović
    • 1
  • Alenka Malej
    • 1
  1. 1.Marine Biology Station, National Institute of BiologyPiranSlovenia

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