Phosphorus limitation during a phytoplankton spring bloom in the western Dutch Wadden Sea

Abstract Like many aquatic ecosystems, the western Dutch Wadden Sea has undergone eutrophication. Due to changes in management policy, nutrient loads, especially phosphorus decreased after the mid-80s. It is still under debate, however, whether nutrients or light is limiting phytoplankton production in the western Wadden Sea, as studies using monitoring data delivered sometimes opposite conclusions and outcomes were related to years, seasons and approaches used. Clearly, the monitoring data alone were not sufficient. We therefore examined the limiting factors for the phytoplankton spring bloom using different experimental approaches. During the spring bloom in April 2010, we investigated several nutrient regimes on natural phytoplankton assemblages at a long term monitoring site, the NIOZ-Jetty sampling (Marsdiep, The Netherlands). Four bioassays, lasting 6 days each, were performed in controlled conditions. From changes in phytoplankton biomass, chlorophyll- a (Chl a ), we could conclude that the phytoplankton in general was mainly P-limited during this period, whereas a Si–P-co-limitation was likely for the diatom populations, when present. These results were confirmed by changes in the photosynthetic efficiency (F v /F m ), in the expression of alkaline phosphatase activity (APA) measured with the fluorescent probe ELF-97, and in the 13 C stable isotope incorporation in particulate organic carbon (POC). During our bioassay experiments, we observed a highly dynamic phytoplankton community with regard to species composition and growth rates. The considerable differences in net population growth rates, occurring under more or less similar environmental incubation conditions, suggest that phytoplankton species composition and grazing activity by small grazers were important structuring factors for net growth during this period.

[1]  Robert W. Howarth,et al.  Nitrogen as the limiting nutrient for eutrophication in coastal marine ecosystems: Evolving views over three decades , 2006 .

[2]  R. Hecky,et al.  Nutrient limitation of phytoplankton in freshwater and marine environments: A review of recent evidence on the effects of enrichment1 , 1988 .

[3]  M. Loebl,et al.  Seasonality of microzooplankton grazing in the northern Wadden Sea , 2008 .

[4]  P. Herman,et al.  Impacts of Nutrient Reduction on Coastal Communities , 2007, Ecosystems.

[5]  W. Admiraal,et al.  Phosphate Utilization in Phaeocystis pouchetii (Haptophyceae) , 1991 .

[6]  Michael T. Brett,et al.  The role of highly unsaturated fatty acids in aquatic foodweb processes , 1997 .

[7]  J. Waterbury,et al.  Phosphonate utilization by the globally important marine diazotroph Trichodesmium , 2006, Nature.

[8]  J. Cullen,et al.  FLUORESCENCE‐BASED MAXIMAL QUANTUM YIELD FOR PSII AS A DIAGNOSTIC OF NUTRIENT STRESS , 2001 .

[9]  Adriaan D. Rijnsdorp,et al.  Signals from the shallows: in search of common patterns in long-term trends in Dutch estuarine and coastal fish , 2008 .

[10]  C. Benitez‐Nelson,et al.  Cell-Specific Alkaline Phosphatase Expression by Phytoplankton from Winyah Bay, South Carolina, USA , 2009 .

[11]  G. Cadée,et al.  Phytoplankton in the Marsdiep at the end of the 20th century; 30 years monitoring biomass, primary production, and Phaeocystis blooms , 2002 .

[12]  D. L. Aksnes,et al.  Silicate as regulating nutrient in phytoplankton competition , 1992 .

[13]  D. Schindler A personal history of the Experimental Lakes ProjectThis paper is part of the series “Forty Years of Aquatic Research at the Experimental Lakes Area”. , 2009 .

[14]  C. Lancelot,et al.  Hydroclimatic modulation of diatom/Phaeocystis blooms in nutrient‐enriched Belgian coastal waters (North Sea) , 2006 .

[15]  J. Beardall,et al.  Approaches for determining phytoplankton nutrient limitation , 2001, Aquatic Sciences.

[16]  P. Herman,et al.  A new trend in the development of the phytoplankton in the Oosterschelde (SW Netherlands) during and after the construction of a storm-surge barrier , 1994, Hydrobiologia.

[17]  J. Daly The maturation and breeding biology of Harmothoë imbricata (Polychaeta: Polynoidae) , 1972, Marine Biology.

[18]  J. Kromkamp,et al.  Light dependence of quantum yields for PSII charge separation and oxygen evolution in eucaryotic algae , 1998 .

[19]  K. Flynn,et al.  Chlorophyll content and fluorescence responses cannot be used to gauge reliably phytoplankton biomass, nutrient status or growth rate. , 2006, The New phytologist.

[20]  J. Nieuwenhuize,et al.  A rapid microwave dissolution method for the determination of trace and minor elements in lyophilized plant material , 1989 .

[21]  Zoe V. Finkel,et al.  Phytoplankton in a changing world: cell size and elemental stoichiometry , 2010 .

[22]  J. Cloern The relative importance of light and nutrient limitation of phytoplankton growth: a simple index of coastal ecosystem sensitivity to nutrient enrichment , 1999, Aquatic Ecology.

[23]  J. Valderrama,et al.  The simultaneous analysis of total nitrogen and total phosphorus in natural waters , 1981 .

[24]  Y. Monbet,et al.  Control of phytoplankton biomass in estuaries: A comparative analysis of microtidal and macrotidal estuaries , 1992 .

[25]  Helmut Hillebrand,et al.  Global analysis of nitrogen and phosphorus limitation of primary producers in freshwater, marine and terrestrial ecosystems. , 2007, Ecology letters.

[26]  F. Colijn,et al.  Development of the diatom-Phaeocystis spring bloom in the Dutch coastal zone of the North Sea: the silicon depletion versus the daily irradiance threshold hypothesis , 1998 .

[27]  Christiane Lancelot,et al.  Phaeocystis blooms in the global ocean and their controlling mechanisms: a review , 2005 .

[28]  J. Cloern Our evolving conceptual model of the coastal eutrophication problem , 2001 .

[29]  R. Scharek,et al.  Responses of Southern Ocean phytoplankton to the addition of trace metals , 1997 .

[30]  P. Burkill,et al.  Microzooplankton grazing in Phaeocystis and diatom-dominated waters in the southern North Sea in spring , 2004 .

[31]  F. Colijn,et al.  Direct impact of silicate on the photosynthetic performance of the diatom Thalassiosira weissflogii assessed by on- and off-line PAM fluorescence measurements , 1999 .

[32]  J. G. Baretta-Bekker,et al.  Recent patterns in potential phytoplankton limitation along the Northwest European continental coast , 2009 .

[33]  M. Lomas,et al.  Taxonomic variability of phosphorus stress in Sargasso Sea phytoplankton , 2004 .

[34]  Mark Hildebrand,et al.  SILICON METABOLISM IN DIATOMS: IMPLICATIONS FOR GROWTH  , 2000 .

[35]  C. Heip,et al.  Production and consumption of biological particles in temperate tidal estuaries , 1995 .

[36]  R. Howarth,et al.  � 2006, by the American Society of Limnology and Oceanography, Inc. Eutrophication of freshwater and marine ecosystems , 2022 .

[37]  F. Colijn,et al.  Is phytoplankton growth in the Wadden Sea light or nitrogen limited , 2003 .

[38]  H. Ridderinkhof Tidal and residual flows in the western Dutch Wadden Sea II: An analytical model to study the constant flow between connected tidal basins☆ , 1988 .

[39]  M. Boersma,et al.  Nutrient limitation of primary producers affects planktivorous fish condition , 2007 .

[40]  Jason G. Bragg,et al.  Allometry and stoichiometry of unicellular, colonial and multicellular phytoplankton. , 2009, The New phytologist.

[41]  E. Epping,et al.  The Wadden Sea: A Coastal Ecosystem under Continuous Change , 2010 .

[42]  Suzanne J.M.H. Hulscher,et al.  Understanding coastal morphodynamics using stability methods , 2003 .

[43]  F. Jochem Probing the physiological state of phytoplankton at the single-cell level , 2000 .

[44]  A new trend in the development of the phytoplankton in the Oosterschelde (SW Netherlands) during and after the construction of a storm-surge barrier , 1994 .

[45]  D. Anderson,et al.  Detection and quantification of alkaline phosphatase in single cells of phosphorus-starved marine phytoplankton , 1998 .

[46]  P. Falkowski,et al.  Effects of Growth Irradiance and Nitrogen Limitation on Photosynthetic Energy Conversion in Photosystem II. , 1988, Plant physiology.

[47]  Alain F. Zuur,et al.  Four decades of variability in turbidity in the western Wadden Sea as derived from corrected Secchi disk readings , 2013 .

[48]  David M. Karl,et al.  Alkaline phosphatase activity and regulation in the North Pacific Subtropical Gyre , 2010 .

[49]  G. Bertru,et al.  Phytoplankton community growth in enrichment bioassays : possible role of the nutrient intracellular pools , 1997 .

[50]  S. Dyhrman,et al.  A SINGLE‐CELL IMMUNOASSAY FOR PHOSPHATE STRESS IN THE DINOFLAGELLATE PROROCENTRUM MINIMUM (DINOPHYCEAE) , 2001 .

[51]  B. L. Howes,et al.  Experimental investigation of taxon‐specific response of alkaline phosphatase activity in natural freshwater phytoplankton , 2003 .

[52]  D. Campbell,et al.  Chlorophyll Fluorescence Analysis of Cyanobacterial Photosynthesis and Acclimation , 1998, Microbiology and Molecular Biology Reviews.

[53]  V. Martin‐Jézéquel,et al.  UNCOUPLING OF SILICON COMPARED WITH CARBON AND NITROGEN METABOLISMS AND THE ROLE OF THE CELL CYCLE IN CONTINUOUS CULTURES OF THALASSIOSIRA PSEUDONANA (BACILLARIOPHYCEAE) UNDER LIGHT, NITROGEN, AND PHOSPHORUS CONTROL1 , 2002 .

[54]  Sonya T. Dyhrman,et al.  Microbes and the marine phosphorus cycle , 2007 .

[55]  A. Leynaert,et al.  Diatom succession, silicification and silicic acid availability in Belgian coastal waters (Southern North Sea) , 2002 .

[56]  C. Philippart,et al.  Long‐term phytoplankton‐nutrient interactions in a shallow coastal sea: Algal community structure, nutrient budgets, and denitrification potential , 2000 .

[57]  C. Heip,et al.  The fate of intertidal microphytobenthos carbon: An in situ 13C‐labeling study , 2000 .

[58]  Urban Tillmann,et al.  Planktonic primary production in the German Wadden Sea , 2000 .