Long-term variation of phytoplankton biomass and physiology in Taihu lake as observed via MODIS satellite.

Estimation of phytoplankton biomass (noted as phytoplankton carbon, Cphyto) and evaluation of phytoplankton physiology is central to the estimation of primary productivity and the carbon cycle. This issue has been widely considered in oceans but not in inland water. Here, we develop experiential and semi-analytical models, which validated by independent in situ measurement data, respectively, to derive Cphyto and phytoplankton absorption coefficient at 675 nm (aph(675)) from MODIS. The effects of nutrients and temperature on the seasonal variation of phytoplankton physiology were assessed through a novel proxy of Cphyto to aph(675) ratio (Cphyto/aph(675)) over the Lake Taihu, the third largest lake in China. Significant seasonal climatological cycles of Cphyto, aph(675) and Cphyto/aph(675) were observed in Lake Taihu, especially in Meiliang Bay and Zhushan Bay, where algal blooms occur frequently. The highest Cphyto and aph(675) values were observed in summer due to the growth of phytoplankton biomass and chlorophyll-a concentration. Lower values were observed in winter and spring, which are characterized by relatively high total nitrogen levels and low irradiance, owing to the low temperature astricts the algae growth. However, the Cphyto/aph(675) shows an opposite trend compared to Cphyto and aph(675), which have high values in winter and low values in summer. The analysis of Cphyto, aph(675) and Cphyto/aph(675) with total phosphorus (TP) levels and temperature indicates that TP are the main positive driver of the increase in Cphyto and aph(675) and negatively regulate Cphyto/aph(675). Warming promotes an increase in Cphyto and aph(675) and restricts Cphyto/aph(675) in summer. Biomass and nutrient levels are the primary drivers of the decrease of Cphyto/aph(675) in such a typical eutrophic lake. The results present some new findings compared to previous oceanic studies and expand our knowledge in the study of phytoplankton biomass and physiology in eutrophic lakes.

[1]  Mingli Zhang,et al.  Wind and rainfall regulation of the diffuse attenuation coefficient in large, shallow lakes from long‐term MODIS observations using a semianalytical model , 2017 .

[2]  Delu Pan,et al.  Absorption and scattering properties of water body in Taihu Lake, China: backscattering , 2009 .

[3]  Stanford B. Hooker,et al.  Photoacclimation and nutrient-based model of light-saturated photosynthesis for quantifying oceanic primary production , 2002 .

[4]  David A. Siegel,et al.  Annual cycles of ecological disturbance and recovery underlying the subarctic Atlantic spring plankton bloom , 2013 .

[5]  David A. Siegel,et al.  Carbon‐based primary productivity modeling with vertically resolved photoacclimation , 2008 .

[6]  S. Markager,et al.  Carbon‐to‐chlorophyll ratio for phytoplankton in temperate coastal waters: Seasonal patterns and relationship to nutrients , 2016 .

[7]  N. Huang,et al.  The empirical mode decomposition and the Hilbert spectrum for nonlinear and non-stationary time series analysis , 1998, Proceedings of the Royal Society of London. Series A: Mathematical, Physical and Engineering Sciences.

[8]  Adam J. Heathcote,et al.  Impacts of Eutrophication on Carbon Burial in Freshwater Lakes in an Intensively Agricultural Landscape , 2011, Ecosystems.

[9]  N. Anderson,et al.  Low organic carbon burial efficiency in arctic lake sediments , 2014 .

[10]  R. Hecky,et al.  Total nitrogen, total phosphorus, and nutrient limitation in lakes and oceans: Is there a common relationship? , 2000 .

[11]  B. Guenet,et al.  Priming effect: bridging the gap between terrestrial and aquatic ecology. , 2010, Ecology.

[12]  Q. Béchet,et al.  Modeling the effects of light and temperature on algae growth: state of the art and critical assessment for productivity prediction during outdoor cultivation. , 2013, Biotechnology advances.

[13]  Qian P. Li,et al.  Modeling phytoplankton growth rates and chlorophyll to carbon ratios in California coastal and pelagic ecosystems , 2010 .

[14]  Huiyu Liu,et al.  Climatic and human impacts on quasi-periodic and abrupt changes of sedimentation rate at multiple time scales in Lake Taihu, China , 2016 .

[15]  Val H. Smith,et al.  Responses of estuarine and coastal marine phytoplankton to nitrogen and phosphorus enrichment , 2006 .

[16]  A. Mangin,et al.  Estimation of light penetration, and horizontal and vertical visibility in oceanic and coastal waters from surface reflectance , 2007 .

[17]  Aaron I. Packman,et al.  Biophysical controls on organic carbon fluxes in fluvial networks , 2008 .

[18]  E. Boss,et al.  Resurrecting the ecological underpinnings of ocean plankton blooms. , 2014, Annual review of marine science.

[19]  Ronghua Ma,et al.  Moderate Resolution Imaging Spectroradiometer (MODIS) observations of cyanobacteria blooms in Taihu Lake, China , 2010 .

[20]  H. Bouman,et al.  Carbon-to-chlorophyll ratio and growth rate of phytoplankton in the sea , 2009 .

[21]  M. Perry,et al.  Estimating primary production at depth from remote sensing. , 1996, Applied optics.

[22]  Deyong Sun,et al.  Detection of algal bloom and factors influencing its formation in Taihu Lake from 2000 to 2011 by MODIS , 2014, Environmental Earth Sciences.

[23]  V. Garçon,et al.  Long‐term variability of phytoplankton carbon biomass in the Sargasso Sea , 2014 .

[24]  Michael J. Behrenfeld,et al.  The CAFE model: A net production model for global ocean phytoplankton , 2016 .

[25]  T. Dittmar,et al.  Uncoupled organic matter burial and quality in boreal lake sediments over the Holocene , 2015 .

[26]  E. Laws,et al.  Nutrient‐ and light‐limited growth of Thalassiosira fluviatilis in continuous culture, with implications for phytoplankton growth in the ocean , 1980 .

[27]  Jianhua Xu,et al.  Multiscale evolution of surface air temperature in the arid region of Northwest China and its linkages to ocean oscillations , 2017, Theoretical and Applied Climatology.

[28]  John M. Melack,et al.  Lakes and reservoirs as regulators of carbon cycling and climate , 2009 .

[29]  E. Boss,et al.  Regulation of phytoplankton carbon to chlorophyll ratio by light, nutrients and temperature in the Equatorial Pacific Ocean: a basin-scale model , 2008 .

[30]  S. Lohrenz,et al.  Photophysiological and light absorption properties of phytoplankton communities in the river‐dominated margin of the northern Gulf of Mexico , 2017, Journal of geophysical research. Oceans.

[31]  Mridul K. Thomas,et al.  Temperature–nutrient interactions exacerbate sensitivity to warming in phytoplankton , 2017, Global change biology.

[32]  Norden E. Huang,et al.  Ensemble Empirical Mode Decomposition: a Noise-Assisted Data Analysis Method , 2009, Adv. Data Sci. Adapt. Anal..

[33]  Changchun Huang,et al.  Assessment of NIR-red algorithms for observation of chlorophyll-a in highly turbid inland waters in China , 2014 .

[34]  K. M. Reifel,et al.  Photoacclimation of natural phytoplankton communities , 2016 .

[35]  L. Tranvik,et al.  Preferential sequestration of terrestrial organic matter in boreal lake sediments , 2017 .

[36]  Ronghua Ma,et al.  Two-decade reconstruction of algal blooms in China's Lake Taihu. , 2009, Environmental science & technology.

[37]  T. Platt,et al.  An Exact Solution For Modeling Photoacclimation of the Carbon-to-Chlorophyll Ratio in Phytoplankton , 2017, Front. Mar. Sci..

[38]  Thomas S. Bianchi,et al.  The role of terrestrially derived organic carbon in the coastal ocean: A changing paradigm and the priming effect , 2011, Proceedings of the National Academy of Sciences.

[39]  David A. Siegel,et al.  Carbon‐based ocean productivity and phytoplankton physiology from space , 2005 .

[40]  Chen Lin,et al.  Carbon and nitrogen burial in a plateau lake during eutrophication and phytoplankton blooms. , 2018, The Science of the total environment.

[41]  E. Laws Evaluation of in situ phytoplankton growth rates: a synthesis of data from varied approaches. , 2013, Annual review of marine science.

[42]  Yunmei Li,et al.  An Improved Land Target-Based Atmospheric Correction Method for Lake Taihu , 2016, IEEE Journal of Selected Topics in Applied Earth Observations and Remote Sensing.

[43]  R. Arnone,et al.  Penetration of UV-visible solar radiation in the global oceans: Insights from ocean color remote sensing , 2013 .

[44]  Deyong Sun,et al.  Satellite observation of hourly dynamic characteristics of algae with Geostationary Ocean Color Imager (GOCI) data in Lake Taihu , 2015 .

[45]  Adam J. Heathcote,et al.  Large increases in carbon burial in northern lakes during the Anthropocene , 2015, Nature Communications.

[46]  Y. Kuzyakov,et al.  Sources and mechanisms of priming effect induced in two grassland soils amended with slurry and sugar , 2006 .

[47]  Kenta Watanabe,et al.  How organic carbon derived from multiple sources contributes to carbon sequestration processes in a shallow coastal system? , 2015, Global change biology.

[48]  David A. Siegel,et al.  Annual cycles of phytoplankton biomass in the subarctic Atlantic and Pacific Ocean , 2016 .

[49]  Val H. Smith,et al.  The nitrogen and phosphorus dependence of algal biomass in lakes: An empirical and theoretical analysis1 , 1982 .

[50]  Wei Shi,et al.  Deriving Total Suspended Matter Concentration from the Near-Infrared-Based Inherent Optical Properties over Turbid Waters: A Case Study in Lake Taihu , 2018, Remote. Sens..

[51]  Richard J. Geider,et al.  LIGHT AND TEMPERATURE DEPENDENCE OF THE CARBON TO CHLOROPHYLL a RATIO IN MICROALGAE AND CYANOBACTERIA: IMPLICATIONS FOR PHYSIOLOGY AND GROWTH OF PHYTOPLANKTON , 1987 .

[52]  Scott A. Freeman,et al.  An assessment of optical properties and primary production derived from remote sensing in the Southern Ocean (SO GasEx) , 2011 .

[53]  A. Weidemann,et al.  Quantifying absorption by aquatic particles: A multiple scattering correction for glass-fiber filters , 1993 .

[54]  F. Roland,et al.  High Primary Production Contrasts with Intense Carbon Emission in a Eutrophic Tropical Reservoir , 2016, Front. Microbiol..

[55]  Michael J. Behrenfeld,et al.  Analytical phytoplankton carbon measurements spanning diverse ecosystems , 2015 .

[56]  B. Peucker‐Ehrenbrink,et al.  Global carbon export from the terrestrial biosphere controlled by erosion , 2015, Nature.

[57]  C. Verpoorter,et al.  A global inventory of lakes based on high‐resolution satellite imagery , 2014 .

[58]  G. Dall’Olmo,et al.  Intercomparison of Ocean Color Algorithms for Picophytoplankton Carbon in the Ocean , 2017, Front. Mar. Sci..

[59]  T. Kana,et al.  Dynamic model of phytoplankton growth and acclimation: responses of the balanced growth rate and the chlorophyll a:carbon ratio to light, nutrient-limitation and temperature , 1997 .

[60]  Xiaohan Liu,et al.  Long-Term Satellite Observations of Microcystin Concentrations in Lake Taihu during Cyanobacterial Bloom Periods. , 2015, Environmental science & technology.

[61]  H. Bennion,et al.  Lake eutrophication and its implications for organic carbon sequestration in Europe , 2014, Global change biology.

[62]  Luis Guanter,et al.  Atmospheric correction of ENVISAT/MERIS data over inland waters: Validation for European lakes , 2010 .

[63]  C. Chenu,et al.  Evidence that stable C is as vulnerable to priming effect as is more labile C in soil. , 2012 .

[64]  M. Perry,et al.  Estimating oceanic primary productivity from ocean color remote sensing: A strategic assessment , 2015 .

[65]  K. Halsey,et al.  Phytoplankton strategies for photosynthetic energy allocation. , 2015, Annual review of marine science.

[66]  David A. Siegel,et al.  Revaluating ocean warming impacts on global phytoplankton , 2016 .

[67]  Gianluca Volpe,et al.  Influence of photoacclimation on the phytoplankton seasonal cycle in the Mediterranean Sea as seen by satellite , 2016 .

[68]  M. Pace,et al.  Terrestrial dominance of organic matter in north temperate lakes , 2012 .

[69]  M. Behrenfeld Climate-mediated dance of the plankton , 2014 .

[70]  Philippe Ciais,et al.  Anthropogenic perturbation of the carbon fluxes from land to ocean , 2013 .

[71]  Xiaojuan Xu,et al.  Spatial heterogeneity of the relationship between vegetation dynamics and climate change and their driving forces at multiple time scales in Southwest China , 2018, Agricultural and Forest Meteorology.

[72]  B. Fu,et al.  Increasing global vegetation browning hidden in overall vegetation greening: Insights from time-varying trends , 2018, Remote Sensing of Environment.

[73]  L. Tranvik,et al.  Constrained microbial processing of allochthonous organic carbon in boreal lake sediments , 2012 .

[74]  K. Ruddick,et al.  Comparison of three SeaWiFS atmospheric correction algorithms for turbid waters using AERONET-OC measurements , 2011 .

[75]  C. Mobley,et al.  Hyperspectral remote sensing for shallow waters. 2. Deriving bottom depths and water properties by optimization. , 1999, Applied optics.

[76]  Timothy R. Parsons,et al.  A manual of chemical and biological methods for seawater analysis , 1984 .

[77]  Marcello Vichi,et al.  Using Optical Sensors on Gliders to Estimate Phytoplankton Carbon Concentrations and Chlorophyll-to-Carbon Ratios in the Southern Ocean , 2017, Front. Mar. Sci..

[78]  L. Yao,et al.  Variation pattern of particulate organic carbon and nitrogen in oceans and inland waters , 2017 .

[79]  Francisco P. Chavez,et al.  Basin-wide distributions of living carbon components and the inverted trophic pyramid of the central gyre of the North Atlantic Ocean, summer 1993 , 1996 .

[80]  Menghua Wang,et al.  Retrieval of diffuse attenuation coefficient in the Chesapeake Bay and turbid ocean regions for satellite ocean color applications , 2009 .