Changes in timing of seasonal peak photosynthetic activity in northern ecosystems

Seasonality in photosynthetic activity is a critical component of seasonal carbon, water, and energy cycles in the Earth system. This characteristic is a consequence of plant's adaptive evolutionary processes to a given set of environmental conditions. Changing climate in northern lands (>30°N) alters the state of climatic constraints on plant growth, and therefore, changes in the seasonality and carbon accumulation are anticipated. However, how photosynthetic seasonality evolved to its current state, and what role climatic constraints and their variability played in this process and ultimately in carbon cycle is still poorly understood due to its complexity. Here, we take the “laws of minimum” as a basis and introduce a new framework where the timing (day of year) of peak photosynthetic activity (DOYPmax) acts as a proxy for plant's adaptive state to climatic constraints on its growth. Our analyses confirm that spatial variations in DOYPmax reflect spatial gradients in climatic constraints as well as seasonal maximum and total productivity. We find a widespread warming‐induced advance in DOYPmax (−1.66 ± 0.30 days/decade, p < 0.001) across northern lands, indicating a spatiotemporal dynamism of climatic constraints to plant growth. We show that the observed changes in DOYPmax are associated with an increase in total gross primary productivity through enhanced carbon assimilation early in the growing season, which leads to an earlier phase shift in land‐atmosphere carbon fluxes and an increase in their amplitude. Such changes are expected to continue in the future based on our analysis of earth system model projections. Our study provides a simplified, yet realistic framework based on first principles for the complex mechanisms by which various climatic factors constrain plant growth in northern ecosystems.

[1]  Atul K. Jain,et al.  Widespread seasonal compensation effects of spring warming on northern plant productivity , 2018, Nature.

[2]  P. Reich,et al.  Effects of climate warming on photosynthesis in boreal tree species depend on soil moisture , 2018, Nature.

[3]  Y. Bergeron,et al.  Beneficial effects of climate warming on boreal tree growth may be transitory , 2018, Nature Communications.

[4]  T. F. Keenan,et al.  Greening of the land surface in the world’s cold regions consistent with recent warming , 2018, Nature Climate Change.

[5]  Alemu Gonsamo,et al.  Peak season plant activity shift towards spring is reflected by increasing carbon uptake by extratropical ecosystems , 2018, Global change biology.

[6]  Michael E. Schaepman,et al.  Shifting relative importance of climatic constraints on land surface phenology , 2018 .

[7]  A. Mäkelä,et al.  Early snowmelt significantly enhances boreal springtime carbon uptake , 2017, Proceedings of the National Academy of Sciences.

[8]  Jonathan R. Thompson,et al.  Climate change imposes phenological trade‐offs on forest net primary productivity , 2017 .

[9]  Bin Zhao,et al.  The Modern-Era Retrospective Analysis for Research and Applications, Version 2 (MERRA-2). , 2017, Journal of climate.

[10]  Scot M. Miller,et al.  Carbon dioxide sources from Alaska driven by increasing early winter respiration from Arctic tundra , 2017, Proceedings of the National Academy of Sciences.

[11]  Ranga B. Myneni,et al.  Weakening temperature control on the interannual variations of spring carbon uptake across northern lands , 2017 .

[12]  D. Baldocchi,et al.  A New Data Set to Keep a Sharper Eye on Land-Air Exchanges , 2017 .

[13]  Philippe Ciais,et al.  Dominant role of plant physiology in trend and variability of gross primary productivity in North America , 2017, Scientific Reports.

[14]  Stephen Sitch,et al.  A roadmap for improving the representation of photosynthesis in Earth system models. , 2017, The New phytologist.

[15]  L. Guanter,et al.  New methods for the retrieval of chlorophyll red fluorescence from hyperspectral satellite instruments: simulations andapplication to GOME-2 and SCIAMACHY , 2016 .

[16]  Ranga B. Myneni,et al.  Changes in growing season duration and productivity of northern vegetation inferred from long-term remote sensing data , 2016 .

[17]  Prabir K. Patra,et al.  Increasing summer net CO 2 uptake in high northern ecosystems inferredfrom atmospheric inversions and comparisons to remote-sensing NDVI , 2016 .

[18]  Atul K. Jain,et al.  Decadal trends in the seasonal-cycle amplitude of terrestrial CO2 exchange resulting from the ensemble of terrestrial biosphere models , 2016 .

[19]  S. Malyshev,et al.  Foliar temperature acclimation reduces simulated carbon sensitivity to climate , 2016 .

[20]  Nuno Carvalhais,et al.  Enhanced seasonal CO2 exchange caused by amplified plant productivity in northern ecosystems , 2016, Science.

[21]  Philippe Ciais,et al.  Declining global warming effects on the phenology of spring leaf unfolding , 2015, Nature.

[22]  Niels Martin Schmidt,et al.  Climate sensitivity of shrub growth across the tundra biome , 2015 .

[23]  Rick Mueller,et al.  Mapping global cropland and field size , 2015, Global change biology.

[24]  S. Higgins,et al.  Three decades of multi-dimensional change in global leaf phenology , 2015 .

[25]  P. Blanken,et al.  Joint control of terrestrial gross primary productivity by plant phenology and physiology , 2015, Proceedings of the National Academy of Sciences.

[26]  A. Huete,et al.  Estimation of vegetation photosynthetic capacity from space‐based measurements of chlorophyll fluorescence for terrestrial biosphere models , 2014, Global change biology.

[27]  N. Zeng,et al.  Continued increase in atmospheric CO 2 seasonal amplitude in the 21st century projected by the CMIP5 Earth system models , 2014 .

[28]  I. Wing,et al.  Net carbon uptake has increased through warming-induced changes in temperate forest phenology , 2014 .

[29]  Ranga B. Myneni,et al.  Temperature and Snow-Mediated Moisture Controls of Summer Photosynthetic Activity in Northern Terrestrial Ecosystems between 1982 and 2011 , 2014, Remote. Sens..

[30]  K. Hikosaka,et al.  Temperature response of photosynthesis in C3, C4, and CAM plants: temperature acclimation and temperature adaptation , 2013, Photosynthesis Research.

[31]  E. A. Kort,et al.  Enhanced Seasonal Exchange of CO2 by Northern Ecosystems Since 1960 , 2013, Science.

[32]  Ranga B. Myneni,et al.  Temperature and vegetation seasonality diminishment over northern lands , 2013 .

[33]  O. Sonnentag,et al.  Climate change, phenology, and phenological control of vegetation feedbacks to the climate system , 2013 .

[34]  Thomas M. Melvin,et al.  Thermal growing season and timing of biospheric carbon uptake across the Northern Hemisphere , 2012 .

[35]  Forrest M Hoffman,et al.  Photoperiodic regulation of the seasonal pattern of photosynthetic capacity and the implications for carbon cycling , 2012, Proceedings of the National Academy of Sciences.

[36]  Karl E. Taylor,et al.  An overview of CMIP5 and the experiment design , 2012 .

[37]  Susan M. Natali,et al.  Increased plant productivity in Alaskan tundra as a result of experimental warming of soil and permafrost , 2012 .

[38]  C. Peng,et al.  A drought-induced pervasive increase in tree mortality across Canada's boreal forests , 2011 .

[39]  J. Edmonds,et al.  RCP4.5: a pathway for stabilization of radiative forcing by 2100 , 2011 .

[40]  Fabienne Maignan,et al.  CO2 surface fluxes at grid point scale estimated from a global 21 year reanalysis of atmospheric measurements , 2010 .

[41]  P. Ciais,et al.  Influence of spring and autumn phenological transitions on forest ecosystem productivity , 2010, Philosophical Transactions of the Royal Society B: Biological Sciences.

[42]  G. Walther Community and ecosystem responses to recent climate change , 2010, Philosophical Transactions of the Royal Society B: Biological Sciences.

[43]  N. McDowell,et al.  A global overview of drought and heat-induced tree mortality reveals emerging climate change risks for forests , 2010 .

[44]  Dan Yakir,et al.  Contribution of Semi-Arid Forests to the Climate System , 2010, Science.

[45]  Damien Sulla-Menashe,et al.  MODIS Collection 5 global land cover: Algorithm refinements and characterization of new datasets , 2010 .

[46]  A. Arneth,et al.  Separation of net ecosystem exchange into assimilation and respiration using a light response curve approach: critical issues and global evaluation , 2010 .

[47]  P. Ciais,et al.  Net carbon dioxide losses of northern ecosystems in response to autumn warming , 2008, Nature.

[48]  Ramakrishna R. Nemani,et al.  Evaluation of remote sensing based terrestrial productivity from MODIS using regional tower eddy flux network observations , 2006, IEEE Transactions on Geoscience and Remote Sensing.

[49]  Tommaso Anfodillo,et al.  Conifers in cold environments synchronize maximum growth rate of tree-ring formation with day length. , 2006, The New phytologist.

[50]  C J Tucker,et al.  Drier summers cancel out the CO2 uptake enhancement induced by warmer springs. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[51]  Maosheng Zhao,et al.  Improvements of the MODIS terrestrial gross and net primary production global data set , 2005 .

[52]  Ramakrishna R. Nemani,et al.  A generalized, bioclimatic index to predict foliar phenology in response to climate , 2004 .

[53]  Jeffrey P. Walker,et al.  THE GLOBAL LAND DATA ASSIMILATION SYSTEM , 2004 .

[54]  Sander Houweling,et al.  CO 2 flux history 1982–2001 inferred from atmospheric data using a global inversion of atmospheric transport , 2003 .

[55]  J. Jacobs Ecohydrology: Darwinian Expression of Vegetation Form and Function , 2003 .

[56]  C. Tucker,et al.  Climate-Driven Increases in Global Terrestrial Net Primary Production from 1982 to 1999 , 2003, Science.

[57]  G. Yohe,et al.  A globally coherent fingerprint of climate change impacts across natural systems , 2003, Nature.

[58]  G. Powell,et al.  Terrestrial Ecoregions of the World: A New Map of Life on Earth , 2001 .

[59]  Isabelle Chuine,et al.  Phenology is a major determinant of tree species range , 2001 .

[60]  W. Oechel,et al.  FLUXNET: A New Tool to Study the Temporal and Spatial Variability of Ecosystem-Scale Carbon Dioxide, Water Vapor, and Energy Flux Densities , 2001 .

[61]  Christopher B. Field,et al.  Increases in early season ecosystem uptake explain recent changes in the seasonal cycle of atmospheric CO2 at high northern latitudes , 1999 .

[62]  R. Vautard,et al.  Singular-spectrum analysis: a toolkit for short, noisy chaotic signals , 1992 .

[63]  W. Cramer,et al.  A global biome model based on plant physiology and dominance, soil properties and climate , 1992 .

[64]  P. Tans,et al.  Atmospheric carbon dioxide at Mauna Loa Observatory: 2. Analysis of the NOAA GMCC data, 1974–1985 , 1989 .

[65]  F. F. Blackman Optima and Limiting Factors , 1905 .

[66]  J. Liebig,et al.  Organic Chemistry in Its Applications to Agriculture and Physiology , 1843, The Medico-chirurgical review.