Estuaries and Coasts

, Volume 33, Issue 2, pp 342–361 | Cite as

Coastal Phytoplankton Do Not Rest in Winter

  • Adriana Zingone
  • Laurent Dubroca
  • Daniele Iudicone
  • Francesca Margiotta
  • Federico Corato
  • Maurizio Ribera d’Alcalà
  • Vincenzo Saggiomo
  • Diana Sarno


The climatology and interannual variability of winter phytoplankton was analyzed at the Long Term Ecological Research Station MareChiara (LTER-MC, Gulf of Naples, Mediterranean Sea) using data collected from 1985 to 2006. Background winter chlorophyll values (0.2–0.5 μg chl a dm−3) were associated with the dominance of flagellates, dinoflagellates, and coccolithophores. Winter biomass increases (<5.47 μg chl a dm−3) were often recorded until 2000, generally in association with low-salinity surface waters (37.3–37.9). These blooms were most often caused by colonial diatoms such as Chaetoceros spp., Thalassiosira spp., and Leptocylindrus danicus. In recent years, we observed more modest and sporadic winter biomass increases, mainly caused by small flagellates and small non-colonial diatoms. The resulting negative chl a trend over the time series was associated with positive surface salinity and negative nutrient trends. Physical and meteorological conditions apparently exert a strict control on winter blooms, hence significant changes in winter productivity can be foreseen under different climatic scenarios.


Phytoplankton Winter dynamics Sverdrup’s theory Mediterranean Sea Time series Climate 


  1. Backhaus, J.O., E.N. Hegseth, H. Wehde, X. Irigoien, K. Hatten, and K. Logemann. 2003. Convection and primary production in winter. Marine Ecology Progress Series 251:1–14. doi:10.3354/meps251001.CrossRefGoogle Scholar
  2. Bakun, A., and K. Broad. 2003. Environmental loopholes and fish population dynamics: comparative pattern recognition with particular focus on El Niňo effects in the Pacific. Fisheries Oceanography 12:458–473. doi:10.1046/j.1365-2419.2003.00258.x.CrossRefGoogle Scholar
  3. Bernardi Aubry, F., A. Berton, M. Bastianini, G. Socal, and F. Acri. 2004. Phytoplankton succession in a coastal area of the NW Adriatic, over a 10-year sampling period (1990–1999). Continental Shelf Research 24:97–115. doi:10.1016/j.csr.2003.09.007.CrossRefGoogle Scholar
  4. Bloom, S.A. 1981. Similarity indices in community studies: potential pitfalls. Marine Ecology Progress Series 5:125–128. doi:10.3354/meps005125.CrossRefGoogle Scholar
  5. Byun, D.S., X.H. Wang, D.E. Hart, and Y.K. Cho. 2005. Modeling the effect of freshwater inflows on the development of spring blooms in an estuarine embayment. Estuarine Coastal and Shelf Science 65:351–360. doi:10.1016/j.ecss.2005.06.012.CrossRefGoogle Scholar
  6. Calbet, A., S. Garrido, E. Saiz, M. Alcaraz, and 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. doi:10.1093/plankt/23.3.319.CrossRefGoogle Scholar
  7. Caroppo, C., A. Fiocca, P. Sammarco, and G. Magazzù. 1999. Seasonal variations of nutrients and phytoplankton in the coastal SW Adriatic Sea (1995–1997). Botanica Marina 42:389–400. doi:10.1515/BOT.1999.045.CrossRefGoogle Scholar
  8. Carrada, G.C., T.S. Hopkins, G. Bonaduce, A. Ianora, D. Marino, M. Modigh, M. Ribera d’Alcalà, and B. Scotto Di Carlo. 1980. Variability in the hydrographic and biological features of the Gulf of Naples. P.S.Z.N. I: Marine Ecology 1:105–120. doi:10.1111/j.1439-0485.1980.tb00213.x.CrossRefGoogle Scholar
  9. Carrada, G.C., E. Fresi, D. Marino, M. Modigh, and M. Ribera d’Alcalà. 1981. Structural analysis of winter phytoplankton in the Gulf of Naples. Journal of Plankton Research 3:291–314. doi:10.1093/plankt/3.2.291.CrossRefGoogle Scholar
  10. Casotti, P., C. Brunet, B. Arnone, and M. Ribera d’Alcalà. 2000. Mesoscale features of phytoplankton and planktonic bacteria in a coastal area as induced by external water masses. Marine Ecology Progress Series 195:15–27. doi:10.3354/meps195015.CrossRefGoogle Scholar
  11. Cerino, F., L. Orsini, D. Sarno, C. Dell'Aversano, L. Tartaglione and A. Zingone. 2005. The alternation of different morphotypes in the seasonal cycle of the toxic diatom Pseudo-nitzschia galaxiae. Harmful Algae 4:33–48. doi:10.1016/j.hal.2003.10.005.CrossRefGoogle Scholar
  12. Cerino, F., and A. Zingone. 2006. A survey of cryptomonad diversity and seasonality at a coastal Mediterranean site. European Journal of Phycology 41:363–378. doi:10.1080/09670260600839450.CrossRefGoogle Scholar
  13. Clarke, K.R., P.J. Somerfield, and M.G. Chapman. 2006. On resemblance measures for ecological studies, including taxonomic dissimilarities and a zero-adjusted Bray-Curtis coefficient for denuded assemblages. Journal of Experimental Marine Biology and Ecology 330:55–80. doi:10.1016/j.jembe.2005.12.017.CrossRefGoogle Scholar
  14. Cloern, J.E. 1996. Phytoplankton bloom dynamics in coastal ecosystems: a review with some general lessons from sustained investigation of San Francisco Bay, California. Reviews of Geophysics 34:127–168. doi:10.1029/96RG00986.CrossRefGoogle Scholar
  15. Coma, R., M. Ribes, J.-M. Gili, and M. Zabala. 2000. Seasonality in coastal benthic ecosystems. Trends in Ecology & Evolution 15:448–453. doi:10.1016/S0169-5347(00) 01970-4.CrossRefGoogle Scholar
  16. De Boyer Montégut, C., G. Madec, A.S. Fisher, A. Lazar, and D. Iudicone. 2004. Mixed layer depth over the global ocean: An examination of profile data and a profile-based climatology. Journal of Geophysical Research 109:1–20. doi:10.1029/2004JC002378.Google Scholar
  17. Duarte, C.M., S. Agustí, H. Kennedy, and D. Vaqué. 1999. The Mediterranean climate as a template for Mediterranean marine ecosystems: the example of the northeast Spanish littoral. Progress in Oceanography 44:245–270. doi:10.1016/S0079-6611(99) 00028-2.CrossRefGoogle Scholar
  18. Efron, B., and R. Tibshirani 1994. An introduction to the bootstrap: Chapman & Hall/CRC.Google Scholar
  19. Eilertsen, H.C.H.R. 1993. Spring blooms and stratification. Nature 363:24. doi:10.1038/363024a0.CrossRefGoogle Scholar
  20. Eilertsen, H.C.H.R., S. Sandberg, and H. Tollefsen. 1995. Photoperiodic control of diatom spore growth: a theory to explain the onset of phytoplankton blooms. Marine Ecology Progress Series 116:303–307. doi:10.3354/meps116303.CrossRefGoogle Scholar
  21. Estrada, M., F. Vives, and M. Alcaraz. 1985. Life and the productivity of the open sea. In Western Mediterranean, ed. R. Margalef, 148–197. Oxford: Pergamon Press.Google Scholar
  22. Estrada, M., R.A. Varela, J. Salat, A. Cruzado, and E. Arias. 1999. Spatio-temporal variability of the winter phytoplankton distribution across the Catalan and North Balearic fronts (NW Mediterranean). Journal of Plankton Research 21:1–20. doi:10.1093/plankt/21.1.1.CrossRefGoogle Scholar
  23. Feldman, G. C., C. R. McClain, Ocean Color Web, SeaWIFS Reprocessing L3m Daily. NASA Goddard Space Flight Center, eds. N. Kuring and S. W. Bailey, Accessed in September 2008,
  24. Glé, C., Y. Del Amo, B. Bec, B. Sautour, J.-M. Froidefond, F. Gohin, D. Maurer, M. Plus, P. Laborde, and P. Chardy. 2007. Typology of environmental conditions at the onset of winter phytoplankton blooms in a shallow macrotidal coastal ecosystem, Arcachon Bay (France). Journal of Plankton Research 29:999–1014. doi:10.1093/plankt/fbm074.CrossRefGoogle Scholar
  25. Goffart, A., J.H. Hecq, and L. Legendre. 2002. Changes in the development of the winter-spring phytoplankton bloom in the Bay of Calvi (NW Mediterranean) over the last two decades: a response to changing climate? Marine Ecology-Progress Series 236:45–60. doi:10.3354/meps236045.CrossRefGoogle Scholar
  26. Gran, H.H. 1931. On the conditions for the production of plankton in the sea. Rapports et Procés-verbaux des Reunions, Conseil International pour L’Exploration de la Mer 75:37–46.Google Scholar
  27. Hansen, H.P., and K. Grasshoff. 1983. Automated chemical analysis. In Methods of seawater analysis, ed. K. Grasshoff, M. Ehrhardt, and K. Kremlin. Weinheim: Verlag Chemie.Google Scholar
  28. Holm-Hansen, O., C.J. Lorenzen, R.W. Holmes, and J.D.H. Strickland. 1965. Fluorimetric determination of chlorophyll. Journal du Conseil International pour l’Exploration de la Mer 30:3–15.Google Scholar
  29. Huisman, J., P. van Oostveen, and F.J. Weissing. 1999. Critical depth and critical turbulence: Two different mechanisms for the development of phytoplankton blooms. Limnology and Oceanography 44:1781–1787.Google Scholar
  30. Irigoien, X., K.J. Flynn, and R.P. Harris. 2005. Phytoplankton blooms: a ’loophole’ in microzooplankton grazing impact? Journal of Plankton Research 27:313–321. doi:10.1093/plankt/fbi011.CrossRefGoogle Scholar
  31. Ji, R., C.S. Davis, C. Chen, D.W. Townsend, D.G. Mountain, and R.C. Beardsley. 2007. Influence of ocean freshening on shelf phytoplankton dynamics. Geophysical Research Letters 34:L24607. doi:10.1029/2007 GL032010.CrossRefGoogle Scholar
  32. Ji, R., C.S. Davis, C. Chen, and R. Beardsley. 2008. Influence of local and external processes on the annual nitrogen cycle and primary productivity on Georges Bank: A 3-D biological-physical modeling study. Journal of Marine Systems 73:31–47. doi:10.1016/j.jmarsys.2007.08.002.CrossRefGoogle Scholar
  33. Labry, C., A. Herbland, D. Delmas, P. Laborde, P. Lazure, J.M. Froidefond, A.M. Jegou, and B. Sautour. 2001. Initiation of winter phytoplankton blooms within the Gironde plume waters in the Bay of Biscay. Marine Ecology Progress Series 212:117–130. doi:10.3354/meps212117.CrossRefGoogle Scholar
  34. Lance, G.N., and W.T. Williams. 1967. A general theory of classificatory sorting strategies. 1. Hierarchical systems. Computer Journal 9:373–380.Google Scholar
  35. Legendre, L., and F. Rassoulzadegan. 1996. Food-web mediated export of biogenic carbon in oceans: hydrodynamic control. Marine Ecology Progress Series 145:179–193. doi:10.3354/meps145179.CrossRefGoogle Scholar
  36. Longhurst, A.R. 2006. Ecological geography of the sea, 2nd ed. New York: Academic Press.Google Scholar
  37. López, S., X. Turón, E. Montero, C. Palacín, C.M. Duarte, and I. Tarjuelo. 1998. Larval abundance, recruitment and early mortality in Paracentrotus lividus (Echinoidea). Interannual variability and plankton-benthos coupling. Marine Ecology Progress Series 172:239–251. doi:10.3354/meps172239.CrossRefGoogle Scholar
  38. Margalef, R. 1978. Life-forms of phytoplankton as survival alternatives in an unstable environment. Oceanologica Acta 1:493–509.Google Scholar
  39. Marino, D., M. Modigh, and A. Zingone. 1984. General features of phytoplankton communities and primary production in the Gulf of Naples and adjacent waters. In Marine phytoplankton and productivity, ed. O. Holm-Hansen, L. Bolis, and R. Gilles, 89–100. Berlin: Springer-Verlag.Google Scholar
  40. Marshall, H.G., and M.S. Cohn. 1987. Phytoplankton distribution along the eastern coast of the U.S.A. Part VI. Shelf waters between Cape Charles and Cape May. Journal of Plankton Research 9: 139–149. doi:10.1093/plankt/9.1.139.CrossRefGoogle Scholar
  41. Marty, J.C., J. Chiaverini, M.D. Pizay, and B. Avril. 2002. Seasonal and interannual dynamics of nutrients and phytoplankton pigments in the western Mediterranean Sea at the DYFAMED time-series station (1991–1999). Deep-Sea Research Part II-Topical Studies in Oceanography 49:1965–1985. doi:10.1016/S0967-0645(02) 00022-X.CrossRefGoogle Scholar
  42. McDonald, S.M., D. Sarno, D.J. Scanlan, and A. Zingone. 2007. Genetic diversity of eukaryotic ultraphytoplankton in the Gulf of Naples during an annual cycle. Aquatic Microbial Ecology 50:75–89. doi:10.3354/ame01148.CrossRefGoogle Scholar
  43. Menden-Deuer, S., and E.J. Lessard. 2000. Carbon to volume relationships for dinoflagellates, diatoms, and other protist plankton. Limnology and Oceanography 45:569–579.Google Scholar
  44. Menna, M., A. Mercatini, M. Uttieri, B. Buonocore, and E. Zambianchi. 2007. Wintertime transport processes in the Gulf of Naples investigated by HF radar measurements of surface currents. Il Nuovo Cimento 30:605–622.Google Scholar
  45. Miquel, J.C., S.W. Fowler, J.L. Rosa, and P. Buat-Menard. 1994. Dynamics of the downward flux of particles and carbon in the open northwestern Mediterranean Sea. Deep-Sea Research 41:243–261. doi:10.1016/0967-0637(94) 90002-7.CrossRefGoogle Scholar
  46. Moran, X.A.G., and M. Estrada. 2005. Winter pelagic photosynthesis in the NW Mediterranean. Deep Sea Research Part I: Oceanographic Research Papers 52:1806–1822. doi:10.1016/j.dsr.2005.05.009.CrossRefGoogle Scholar
  47. Mura, M.P., S. Agustí, J. Cebrián, and M.P. Satta. 1996. Seasonal variability of phytoplankton biomass and community composition in Blanes Bay (1992–1994). Publicaciones Especiales Instituto Espanol de Oceanografia 22:23–29.Google Scholar
  48. Neveux, J., and M. Panouse. 1987. Spectrofluorometric determination of chlorophylls and pheophytins. Archiv für Hydrobiologie 109:567–581.Google Scholar
  49. Nicholls, N. 2001. Commentary and analysis: The insignificance of significance testing. Bulletin of the American Meteorological Society 82:981–986. doi:10.1175/1520-0477(2001)082<0981:CAATIO>2.3.CO;2.CrossRefGoogle Scholar
  50. Platt, T., J.D. Woods, S. Sathyendranath, and W. Barkmann. 1994. Net primary production and stratification in the ocean. In The Polar Oceans and their role in shaping the global environment, ed. D.M. Johannesen, R.D. Muench, and D.E. Overland, 247–254. Washington: American Geophysical Union.Google Scholar
  51. R Development Core Team 2007. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Accessed 30 September 2008.
  52. Reynolds, C.S. 1998. What factors influence the species composition of phytoplankton in lakes of different trophic status? Hydrobiologia 369/370:11–26. doi:10.1023/A:1017062213207.CrossRefGoogle Scholar
  53. Ribera d’Alcalà, M., F. Conversano, F. Corato, P. Licandro, O. Mangoni, D. Marino, M.G. Mazzocchi, M. Modigh, M. Montresor, M. Nardella, V. Saggiomo, D. Sarno, and A. Zingone. 2004. Seasonal patterns in plankton communities in a pluriannual time series at a coastal Mediterranean site (Gulf of Naples): an attempt to discern recurrences and trends. Scientia Marina 68(Suppl. 1):65–83.Google Scholar
  54. Rochford, P.A., A.B. Kara, A.J. Wallcraft, and R.A. Arnone. 2001. Importance of solar subsurface heating in ocean general circulation models. Journal of Geophysical Research 106:30923–30938. doi:10.1029/2000JC000355.CrossRefGoogle Scholar
  55. Santer, B.D., T.M.L. Wigley, J.S. Boyle, D.J. Gaffen, J.J. Hnilo, D. Nychka, D.E. Parker, and K.E. Taylor. 2000. Statistical significance of trends and trend differences in layer-average atmospheric temperature time series. Journal of Geophysical Research 105:7337–7356. doi:10.1029/1999JD901105.CrossRefGoogle Scholar
  56. Saporta, G. 1990. Probabilités, analyses de données et statistiques. Paris: Editions Technip.Google Scholar
  57. Scotto Di Carlo, B., C.R. Tomas, A. Ianora, D. Marino, M.G. Mazzocchi, M. Modigh, M. Montresor, L. Petrillo, M. Ribera d’Alcalà, V. Saggiomo, and A. Zingone. 1985. Uno studio integrato dell’ecosistema pelagico costiero del Golfo di Napoli. Nova Thalassia 126:99–128.Google Scholar
  58. Siano, R. 2008. The phytoplankton of the Campania coasts: an ecological and taxonomic study. PhD thesis. University of Messina, Italy.Google Scholar
  59. Siegel, D.A., S.C. Doney, and J.A. Yoder. 2002. The North Atlantic spring phytoplankton bloom and Sverdrup’s critical depth hypothesis. Science 296:730–733. doi:10.1126/science.1069174.CrossRefGoogle Scholar
  60. Smayda, T.J. 1997. What is a bloom? A commentary. Limnology and Oceanography 42:1132–1136.Google Scholar
  61. Smayda, T.J., and C.S. Reynolds. 2001. Community assembly in marine phytoplankton: application of recent models to harmful dinoflagellate blooms. Journal of Plankton Research 23:447–461. doi:10.1093/plankt/23.5.447.CrossRefGoogle Scholar
  62. Smetacek, V., and U. Passow. 1990. Spring bloom initiation and Sverdrup’s critical-depth model. Limnology and Oceanography 35:228–234.CrossRefGoogle Scholar
  63. Socal, G., A. Boldrin, F. Bianchi, G. Civitarese, A.D. Lazzari, S. Rabitti, C. Totti, and M.M. Turchetto. 1999. Nutrient, particulate matter and phytoplankton variability in the photic layer of the Otranto strait. Journal of Marine Systems 20:381–398. doi:10.1016/S0924-7963(98) 00075-X.CrossRefGoogle Scholar
  64. Socal, G., A. Pugnetti, L. Alberighi, and F. Acri. 2002. Observations on phytoplankton productivity in relation to hydrography in the northern Adriatic. Chemistry and Ecology 18:61–73. doi:10.1080/02757540212686.CrossRefGoogle Scholar
  65. Sommer, U., and K. Lengfellner. 2008. Climate change and the timing, magnitude and composition of the phytoplankton spring bloom. Global Change Biology 14:1199–1208. doi:10.1111/j.1365-2486.2008.01571.x.CrossRefGoogle Scholar
  66. Stemmann, L., G. Gorsky, J.C. Marty, M. Picheral, and J.C. Miquel. 2002. Four-year study of large-particle vertical distribution (0–1000 m) in the NW Mediterranean in relation to hydrology, phytoplankton, and vertical flux. Deep-Sea Research Part II 49:2143–2162. doi:10.1016/S0967-0645(02) 00032-2.CrossRefGoogle Scholar
  67. Strickland, J.D.H., and T.R. Parsons 1972. A practical handbook of sea-water analysis Ottawa: Journal of Fishery Research Board of Canada.Google Scholar
  68. Sverdrup, H.U. 1953. On conditions for the vernal blooming of phytoplankton. Journal du Conseil International pour l’Exploration de la Mer 18:287–295.Google Scholar
  69. Throndsen, J., and A. Zingone. 1994. Micronomads of the Mediterranean sea. Giornale Botanico Italiano 128:1031–1044.Google Scholar
  70. Tibshirani, R., G. Walther, and T. Hastie. 2001. Estimating the number of clusters in a data set via the gap statistic. Journal of the Royal Statistical Society: Series B (Statistical Methodology) 63:411–423. doi:10.1111/1467-9868.00293.CrossRefGoogle Scholar
  71. Townsend, D.W., D.W. Keller, M.D. Sieracki, and S.G. Ackleson. 1992. Spring phytoplankton blooms in the absence of vertical water column stratification. Nature 360:59–62. doi:10.1038/360059a0.CrossRefGoogle Scholar
  72. Townsend, D.W., L.M. Cammen, P.M. Holligan, D.E. Campbell, and N.R. Pettigrew. 1994. Causes and consequences of variability in the timing of spring phytoplankton blooms. Deep-Sea Research 41:747–765. doi:10.1016/0967-0637(94) 90075-2.CrossRefGoogle Scholar
  73. Travers, M. 1974. Le microplancton du Golfe de Marseille. Schema du cycle annuel, répartitions horizontale et verticale. Tethys 6:713–726.Google Scholar
  74. Tukey, J.W. 1977. Exploratory data analysis. Reading, MA: Addison-Wesley.Google Scholar
  75. Utermöhl, H. 1958. Zur Vervollkommnung der quantitativen Phytoplankton-Methodik. Mitteilungen der internationale Vereinigung für theoretische und angewandte Limnologie 9:1–38.Google Scholar
  76. Ward, J.H. 1963. Hierarchical grouping to optimize an objective function. Journal of American Statistical Association 58:236–244. doi:10.2307/2282967.CrossRefGoogle Scholar
  77. Zingone, A., M. Montresor, and D. Marino. 1990. Summer phytoplankton physiognomy in coastal water of the Gulf of Naples. P.S.Z.N.I: Marine Ecology 11:157–172. doi:10.1111/j.1439-0485.1990.tb00236.x.CrossRefGoogle Scholar
  78. Zingone, A., D. Sarno, and G. Forlani. 1999. Seasonal dynamics of Micromonas pusilla (Prasinophyceae) and its viruses in the Gulf of Naples (Mediterranean Sea). Journal of Plankton Research 21:2143–2159. doi:10.1093/plankt/21.11.2143.CrossRefGoogle Scholar
  79. Ziveri, P., A. Rutten, G.J. de Lange, J. Thomson, and C. Corselli. 2000. Present-day coccolith fluxes recorded in central eastern Mediterranean sediment traps and surface sediments. Palaeogeography, Palaeoclimatology, Palaeoecology 158:175–195. doi:10.1016/S0031-0182(00) 00049-3.CrossRefGoogle Scholar
  80. Zupo, V., and M.G. Mazzocchi. 1998. New perspectives in the investigation of food webs in benthic and planktonic coastal ecosystems. Biologia Marina Mediterranea 5:12–26.Google Scholar

Copyright information

© Coastal and Estuarine Research Federation 2009

Authors and Affiliations

  • Adriana Zingone
    • 1
  • Laurent Dubroca
    • 1
  • Daniele Iudicone
    • 1
  • Francesca Margiotta
    • 1
  • Federico Corato
    • 1
  • Maurizio Ribera d’Alcalà
    • 1
  • Vincenzo Saggiomo
    • 1
  • Diana Sarno
    • 1
  1. 1.Stazione Zoologica Anton DohrnNaplesItaly

Personalised recommendations