Mesoscale and sub-mesoscale variability in phytoplankton community composition in the Sargasso Sea

Abstract The Sargasso Sea is a dynamic physical environment in which strong seasonal variability combines with forcing by mesoscale (~100 km) eddies. These drivers determine nutrient, light, and temperature regimes and, ultimately, the composition and productivity of the phytoplankton community. On four cruises (2011 and 2012; one eddy per cruise), we investigated links between water column structure and phytoplankton community composition in the Sargasso at a range of time and space scales. On all cruises, cyanobacteria ( Prochlorococcus and Synechococcus ) dominated the phytoplankton numerically, while haptophytes were the dominant eukaryotes (up to 60% of total chl- a ). There were substantial effects of mesoscale and sub-mesoscale forcing on phytoplankton community composition in both spring and summer. Downwelling (in anticyclones) resulted in Prochlorococcus abundances that were 22−66% higher than at ‘outside’ stations. Upwelling (in cyclones) was associated with significantly higher abundances and POC biomass of nanoeukaryotes. In general, however, each eddy had its own unique characteristics. The center of anticyclone AC1 (spring 2011) had the lowest phytoplankton biomass (chl- a ) of any eddy we studied and had lower nitrate+nitrite (N+N −2 ) and eukaryote chl- a biomass as compared to its edge and to the Bermuda Atlantic Time-Series station (BATS). At the center of cyclone C1 (summer 2011), we observed uplift of the 26.5 kg m −3 isopycnal and high nutrient inventories (N+N=74±46 mmol m −2 ). We also observed significantly higher haptophyte chl- a (non-coccolithophores) and lower cyanobacterial chl- a at the center and edge of C1 as compared to outside the eddy at BATS. Cyclone C2 (spring 2012) exhibited a deep mixed layer, yet had relatively low nutrient concentrations. We observed a shift in the taxonomic composition of haptophytes between a coccolithophore-dominated community in C2 (98% of total haptophyte chl- a ) and a non-coccolithophore community at BATS. In summer 2012, downwelling associated with anticyclone AC2 occurred at the edge of the eddy (not at the center), where AC2 interacted with a nearby cyclone. At the edge, we found significantly lower Synechococcus abundances and higher eukaryote chl- a compared to the center of AC2 and BATS. These along-transect nuances demonstrate the significance of small-scale perturbations that substantially alter phytoplankton community structure. Therefore, while seasonality in the North Atlantic is the primary driver of broad-scale trends in phytoplankton community composition, the effects of transient events must be considered when studying planktonic food webs and biogeochemical cycling in the Sargasso Sea.

[1]  M. Lomas,et al.  Prochlorococcus contributes to new production in the Sargasso Sea deep chlorophyll maximum , 2007 .

[2]  Sallie W. Chisholm,et al.  Phytoplankton population dynamics at the Bermuda Atlantic Time-series station in the Sargasso Sea , 2001 .

[3]  M. Latasa Improving estimations of phytoplankton class abundances using CHEMTAX , 2007 .

[4]  Paul G. Falkowski,et al.  Photosynthetic community responses to upwelling in mesoscale eddies in the subtropical North Atlantic and Pacific Oceans , 2008 .

[5]  Louise Schlüter,et al.  Phytoplankton Pigments: Quantitative interpretation of chemotaxonomic pigment data , 2011 .

[6]  Patrice Klein,et al.  Upper Ocean Turbulence from High-Resolution 3D Simulations , 2008 .

[7]  H. Bouman,et al.  Water-column stratification governs the community structure of subtropical marine picophytoplankton. , 2011, Environmental microbiology reports.

[8]  H. Sverdrup,et al.  On Conditions for the Vernal Blooming of Phytoplankton , 1953 .

[9]  Anthony H. Knap,et al.  Overview of the U.S. JGOFS Bermuda Atlantic Time-series Study and the Hydrostation S program , 1996 .

[10]  M. Lomas,et al.  Assimilation of upwelled nitrate by small eukaryotes in the Sargasso Sea , 2011 .

[11]  G. Jackson,et al.  Small Phytoplankton and Carbon Export from the Surface Ocean , 2007, Science.

[12]  Paul G. Falkowski,et al.  Primary Productivity and Biogeochemical Cycles in the Sea , 1992 .

[13]  A. Worden,et al.  Assessing the dynamics and ecology of marine picophytoplankton: The importance of the eukaryotic component , 2004 .

[14]  R. Olson,et al.  Prochlorococcus marinus nov. gen. nov. sp.: an oxyphototrophic marine prokaryote containing divinyl chlorophyll a and b , 1992, Archives of Microbiology.

[15]  R. Bidigare,et al.  Temporal variability of phytoplankton community structure based on pigment analysis , 1993 .

[16]  J. Cullen,et al.  Subsurface chlorophyll maximum layers: enduring enigma or mystery solved? , 2015, Annual review of marine science.

[17]  Glen A. Tarran,et al.  High bacterivory by the smallest phytoplankton in the North Atlantic Ocean , 2008, Nature.

[18]  P. Masqué,et al.  Particle fluxes associated with mesoscale eddies in the Sargasso Sea , 2008 .

[19]  Philip L. Richardson,et al.  A census of eddies observed in North Atlantic SOFAR float data , 1993 .

[20]  P. Falkowski,et al.  Role of eddy pumping in enhancing primary production in the ocean , 1991, Nature.

[21]  Scott C. Doney,et al.  Impact of eddy–wind interaction on eddy demographics and phytoplankton community structure in a model of the North Atlantic Ocean , 2011 .

[22]  F. Rassoulzadegan,et al.  Growth and grazing on Prochlorococcus and Synechococcus by two marine ciliates , 1999 .

[23]  C. Carlson,et al.  Microbial dynamics in cyclonic and anticyclonic mode-water eddies in the northwestern Sargasso Sea , 2008 .

[24]  William K. W. Li Primary production of prochlorophytes, cyanobacteria, and eucaryotic ultraphytoplankton: Measurements from flow cytometric sorting , 1994 .

[25]  Patrice Klein,et al.  The oceanic vertical pump induced by mesoscale and submesoscale turbulence. , 2009, Annual review of marine science.

[26]  H. Claustre,et al.  Prochlorococcus and Synechococcus: A comparative study of their optical properties in relation to their size and pigmentation , 1993 .

[27]  S. Chisholm,et al.  Nutrient gradients in the western North Atlantic Ocean: Relationship to microbial community structure and comparison to patterns in the Pacific Ocean , 2001 .

[28]  Lisa R. Moore,et al.  Photophysiology of the marine cyanobacterium Prochlorococcus: Ecotypic differences among cultured isolates , 1999 .

[29]  A. Knap,et al.  Mesoscale Variations of Biogeochemical Properties in the Sargasso Sea , 1999 .

[30]  T. D. Dickey,et al.  Influence of mesoscale eddies on new production in the Sargasso Sea , 1998, Nature.

[31]  M. Sieracki,et al.  Plankton community response to sequential silicate and nitrate depletion during the 1989 North Atlantic spring bloom , 1993 .

[32]  D. Karl,et al.  MAGIC : a sensitive and precise method for measuring dissolved phosphorus in aquatic environments , 1992 .

[33]  W. J. Jenkins,et al.  The subtropical nutrient spiral , 2003 .

[34]  H. Claustre,et al.  Extreme diversity in noncalcifying haptophytes explains a major pigment paradox in open oceans , 2009, Proceedings of the National Academy of Sciences.

[35]  David Archer,et al.  Association of sinking organic matter with various types of mineral ballast in the deep sea: Implications for the rain ratio , 2002 .

[36]  Sallie W. Chisholm,et al.  Comparative physiology of Synechococcus and Prochlorococcus: influence of light and temperature on growth, pigments, fluorescence and absorptive properties , 1995 .

[37]  L. Dubroca,et al.  Response of the deep chlorophyll maximum to fluctuations in vertical mixing intensity , 2013 .

[38]  Michael W. Lomas,et al.  Sargasso Sea phosphorus biogeochemistry: an important role for dissolved organic phosphorus (DOP) , 2009 .

[39]  Eddy-driven pulses of respiration in the Sargasso Sea , 2009 .

[40]  R. Bidigare,et al.  Light driven seasonal patterns of chlorophyll and nitrate in the lower euphotic zone of the North Pacific Subtropical Gyre , 2004 .

[41]  A. Robinson,et al.  Eddy-induced nutrient supply and new production in the Sargasso Sea , 1997 .

[42]  M. Lomas,et al.  Evidence for aggregation and export of cyanobacteria and nano-eukaryotes from the Sargasso Sea euphotic zone , 2010 .

[43]  D. M. Nelson,et al.  Biogeochemical responses to late-winter storms in the Sargasso Sea. IV. Rapid succession of major phytoplankton groups , 2009 .

[44]  S. Tringe,et al.  Targeted metagenomics and ecology of globally important uncultured eukaryotic phytoplankton , 2010, Proceedings of the National Academy of Sciences.

[45]  L. A. Anderson,et al.  Nutrient flux into an intense deep chlorophyll layer in a mode-water eddy , 2008 .

[46]  Cindy Lee,et al.  Regional and temporal variability of sinking organic matter in the subtropical northeast Atlantic Ocean: a biomarker diagnosis. , 2009 .

[47]  S. Wright,et al.  CHEMTAX - a program for estimating class abundances from chemical markers: application to HPLC measurements of phytoplankton , 1996 .

[48]  D. Scanlan,et al.  Significant CO2 fixation by small prymnesiophytes in the subtropical and tropical northeast Atlantic Ocean , 2010, The ISME Journal.

[49]  J. C. Goldman Potential role of large oceanic diatoms in new primary production , 1993 .

[50]  Michael W. Lomas,et al.  Impact of ocean phytoplankton diversity on phosphate uptake , 2014, Proceedings of the National Academy of Sciences.

[51]  M. Lomas,et al.  DNA-based molecular fingerprinting of eukaryotic protists and cyanobacteria contributing to sinking particle flux at the Bermuda Atlantic time-series study , 2013 .

[52]  T. Moutin,et al.  Re-examination of the MAGIC method to determine low orthophosphate concentration in seawater , 2005 .

[53]  H. Ducklow,et al.  Stocks and dynamics of bacterioplankton in the northwestern Sargasso Sea , 1996 .

[54]  D. Siegel,et al.  Mesoscale Eddies, Satellite Altimetry, and New Production in the Sargasso Sea , 1999 .

[55]  J. Smith,et al.  A Small Volume, Short-Incubation-Time Method for Measurement of Photosynthesis as a Function of Incident Irradiance , 1983 .

[56]  R. Burton,et al.  Phytoplankton distribution patterns in the northwestern Sargasso Sea revealed by small subunit rRNA genes from plastids , 2011, The ISME Journal.

[57]  David M. Karl,et al.  Freezing as a method of sample preservation for the analysis of dissolved inorganic nutrients in seawater , 1996 .

[58]  Beatriz Mouriño-Carballido,et al.  Mesoscale variability in the metabolic balance of the Sargasso Sea , 2006 .

[59]  E. Mason,et al.  Carbon Dynamics within Cyclonic Eddies: Insights from a Biomarker Study , 2013, PloS one.

[60]  Nicholas R. Bates,et al.  Eddy/Wind Interactions Stimulate Extraordinary Mid-Ocean Plankton Blooms , 2007, Science.

[61]  Nicholas R. Bates,et al.  Overview of the US JGOFS Bermuda Atlantic Time-series Study (BATS): a decade-scale look at ocean biology and biogeochemistry , 2001 .

[62]  Ken O. Buesseler,et al.  Biogeochemical impacts due to mesoscale eddy activity in the Sargasso Sea as measured at the Bermuda Atlantic Time-series Study (BATS) , 2003 .

[63]  D. M. Nelson,et al.  Biogeochemical responses to late-winter storms in the Sargasso Sea, II: Increased rates of biogenic silica production and export , 2009 .

[64]  Patrice Klein,et al.  Impact of sub-mesoscale physics on production and subduction of phytoplankton in an oligotrophic regime , 2001 .

[65]  M. Lomas,et al.  Two decades and counting: 24-years of sustained open ocean biogeochemical measurements in the Sargasso Sea , 2013 .

[66]  K. Baker,et al.  Evidence for phytoplankton succession and chromatic adaptation in the Sargasso Sea during spring 1985 , 1990 .

[67]  V. Lance,et al.  Resolving the ocean's euphotic zone , 2014 .

[68]  Alberto Orfao,et al.  Combined Patterns of IGHV Repertoire and Cytogenetic/Molecular Alterations in Monoclonal B Lymphocytosis versus Chronic Lymphocytic Leukemia , 2013, PloS one.

[69]  H. Paerl,et al.  Flow scintillation counting of 14 C-labeled microalgal photosynthetic pigments , 1996 .

[70]  M. Lomas,et al.  Changes in partitioning of carbon amongst photosynthetic pico- and nano-plankton groups in the Sargasso Sea in response to changes in the North Atlantic Oscillation , 2013 .

[71]  Eric D. Barton,et al.  The influence of island-generated eddies on chlorophyll distribution : a study of mesoscale variation around Gran Canaria , 1997 .

[72]  J. C. Goldman,et al.  Effect of large marine diatoms growing at low light on episodic new production , 2003 .