Seasonality of soil moisture mediates responses of ecosystem phenology to elevated CO2 and warming in a semi‐arid grassland

Summary Vegetation greenness, detected using digital photography, is useful for monitoring phenology of plant growth, carbon uptake and water loss at the ecosystem level. Assessing ecosystem phenology by greenness is especially useful in spatially extensive, water-limited ecosystems such as the grasslands of the western United States, where productivity is moisture dependent and may become increasingly vulnerable to future climate change. We used repeat photography and a novel means of quantifying greenness in digital photographs to assess how the individual and combined effects of warming and elevated CO2 impact ecosystem phenology (greenness and plant cover) in a semi-arid grassland over an 8-year period. Climate variability within and among years was the proximate driver of ecosystem phenology. Individual and combined effects of warming and elevated CO2 were significant at times, but mediated by variation in both intra- and interannual precipitation. Specifically, warming generally enhanced plant cover and greenness early in the growing season but often had a negative effect during the middle of the summer, offsetting the early season positive effects. The individual effects of elevated CO2 on plant cover and greenness were generally neutral. Opposing seasonal variations in the effects of warming and less so elevated CO2 cancelled each other out over an entire growing season, leading to no net effect of treatments on annual accumulation of greenness. The main effect of elevated CO2 dampened quickly, but warming continued to affect plant cover and plot greenness throughout the experiment. The combination of warming and elevated CO2 had a generally positive effect on greenness, especially early in the growing season and in later years of the experiment, enhanced annual greenness accumulation. However, interannual precipitation variation had larger effect on greenness, with two to three times greater greenness in wet years than in dry years. Synthesis. Seasonal variation in timing and amount of precipitation governs grassland phenology, greenness and the potential for carbon uptake. Our results indicate that concurrent changes in precipitation regimes mediate vegetation responses to warming and elevated atmospheric CO2 in semi-arid grasslands. Even small changes in vegetation phenology and greenness in response to warming and rising atmospheric CO2 concentrations, such as those we report here, can have large consequences for the future of grasslands.

[1]  A. Knapp,et al.  Ecophysiological responses of two dominant grasses to altered temperature and precipitation regimes , 2009 .

[2]  I. C. Prentice,et al.  Climatic Control of the High-Latitude Vegetation Greening Trend and Pinatubo Effect , 2002, Science.

[3]  G. Marion,et al.  A meta-analysis of the response of soil respiration, net nitrogen mineralization, and aboveground plant growth to experimental ecosystem warming , 2001, Oecologia.

[4]  Yiqi Luo,et al.  Direct and indirect effects of experimental warming on ecosystem carbon processes in a tallgrass prairie , 2005 .

[5]  Michael A. Crimmins,et al.  Monitoring Plant Phenology Using Digital Repeat Photography , 2008, Environmental management.

[6]  S. Kurc,et al.  Digital image-derived greenness links deep soil moisture to carbon uptake in a creosotebush-dominated shrubland , 2010 .

[7]  Mark West,et al.  C4 grasses prosper as carbon dioxide eliminates desiccation in warmed semi-arid grassland , 2011, Nature.

[8]  W. Parton,et al.  Progressive Nitrogen Limitation of Ecosystem Responses to Rising Atmospheric Carbon Dioxide , 2004 .

[9]  G. Meehl,et al.  Climate extremes: observations, modeling, and impacts. , 2000, Science.

[10]  Daniel E. Schindler,et al.  CLIMATE CHANGE UNCOUPLES TROPHIC INTERACTIONS IN AN AQUATIC ECOSYSTEM , 2004 .

[11]  Alistair Rogers,et al.  A mechanistic evaluation of photosynthetic acclimation at elevated CO2 , 2000 .

[12]  G. Suter.  Species Interactions , 2004 .

[13]  Alan K. Knapp,et al.  Relative effects of precipitation variability and warming on tallgrass prairie ecosystem function , 2011 .

[14]  C. Field,et al.  Relationships Between NDVI, Canopy Structure, and Photosynthesis in Three Californian Vegetation Types , 1995 .

[15]  Donald J. Wuebbles,et al.  Regional Climate Trends And Scenarios For The U.S. National Climate Assessment Part 3: Climate Of The Midwest U.S. , 2013 .

[16]  Mark A. Weltz,et al.  Near-Ground Remote Sensing of Green Area Index on the Shortgrass Prairie , 2006 .

[17]  M. Rummukainen,et al.  Evaluating the performance and utility of regional climate models: the PRUDENCE project , 2007 .

[18]  J. Y. King,et al.  Elevated atmospheric CO2 effects and soil water feedbacks on soil respiration components in a Colorado grassland , 2003 .

[19]  Ramakrishna R. Nemani,et al.  Real-time monitoring and short-term forecasting of land surface phenology , 2006 .

[20]  Marco Bindi,et al.  Free Air CO2 Enrichment of potato (Solanum tuberosum, L.): design and performance of the CO2‐fumigation system , 1997 .

[21]  A. Michelsen,et al.  Effects of elevated CO₂, warming and drought episodes on plant carbon uptake in a temperate heath ecosystem are controlled by soil water status. , 2011, Plant, cell & environment.

[22]  D. T. Booth,et al.  Frontiers inEcology and the Environment Image-based monitoring to measure ecological change in rangeland , 2007 .

[23]  Yiqi Luo,et al.  Divergence of reproductive phenology under climate warming , 2007, Proceedings of the National Academy of Sciences.

[24]  R. Nowak,et al.  No cumulative effect of 10 years of elevated [CO2] on perennial plant biomass components in the Mojave Desert , 2013, Global change biology.

[25]  Nicholas G Smith,et al.  Plant respiration and photosynthesis in global‐scale models: incorporating acclimation to temperature and CO2 , 2013, Global change biology.

[26]  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.

[27]  Osvaldo E. Sala,et al.  Long-term dynamics of water and carbon in semi-arid ecosystems: a gradient analysis in the Patagonian steppe , 2000, Plant Ecology.

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

[29]  M. Loik,et al.  A multi-scale perspective of water pulses in dryland ecosystems: climatology and ecohydrology of the western USA , 2004, Oecologia.

[30]  L. Barthès,et al.  Short-Term Uptake of 15N by a Grass and Soil Micro-Organisms after Long-Term Exposure to Elevated CO2 , 2006, Plant and Soil.

[31]  Nathaniel A. Brunsell,et al.  Timing of climate variability and grassland productivity , 2012, Proceedings of the National Academy of Sciences.

[32]  M. Edwards,et al.  Impact of climate change on marine pelagic phenology and trophic mismatch , 2004, Nature.

[33]  J. Zak,et al.  Assessing the Response of Terrestrial Ecosystems to Potential Changes in Precipitation , 2003 .

[34]  J. Xia,et al.  The Effects of Warming-Shifted Plant Phenology on Ecosystem Carbon Exchange Are Regulated by Precipitation in a Semi-Arid Grassland , 2012, PloS one.

[35]  H. Mooney,et al.  Shifting plant phenology in response to global change. , 2007, Trends in ecology & evolution.

[36]  P. Ciais,et al.  Effect of climate and CO2 changes on the greening of the Northern Hemisphere over the past two decades , 2006 .

[37]  Y. Carrillo,et al.  Warming Reduces Carbon Losses from Grassland Exposed to Elevated Atmospheric Carbon Dioxide , 2013, PloS one.

[38]  E. Pendall,et al.  Soil carbon storage under simulated climate change is mediated by plant functional type , 2011 .

[39]  J. Megonigal,et al.  Ecosystem response to elevated CO2 levels limited by nitrogen-induced plant species shift , 2010, Nature.

[40]  J. Bascompte,et al.  Global change and species interactions in terrestrial ecosystems. , 2008, Ecology letters.

[41]  Pavel Ya. Groisman,et al.  Prolonged Dry Episodes over the Conterminous United States: New Tendencies Emerging during the Last 40 Years , 2008 .

[42]  A. Heinemeyer,et al.  Biotic carbon feedbacks in a materially closed soil-vegetation-atmosphere system , 2012 .

[43]  R. Seager,et al.  Model Projections of an Imminent Transition to a More Arid Climate in Southwestern North America , 2007, Science.

[44]  M. Bradford,et al.  Contingency in ecosystem but not plant community response to multiple global change factors. , 2012, The New phytologist.

[45]  R. Monson,et al.  Longer growing seasons lead to less carbon sequestration by a subalpine forest , 2010 .

[46]  S. Solomon,et al.  Irreversible climate change due to carbon dioxide emissions , 2009, Proceedings of the National Academy of Sciences.

[47]  Rik Leemans,et al.  Faculty Opinions recommendation of European phenological response to climate change matches the warming pattern. , 2006 .

[48]  Alan K. Knapp,et al.  Altered Rainfall Patterns, Gas Exchange, and Growth in Grasses and Forbs , 2002, International Journal of Plant Sciences.

[49]  E. Pendall,et al.  Invasive forb benefits from water savings by native plants and carbon fertilization under elevated CO2 and warming. , 2013, The New phytologist.

[50]  Judea Pearl,et al.  Direct and Indirect Effects , 2001, UAI.

[51]  J. Merilä,et al.  Experimental support for the cost–benefit model of lizard thermoregulation: the effects of predation risk and food supply , 2008, Oecologia.

[52]  S. Collins,et al.  A framework for assessing ecosystem dynamics in response to chronic resource alterations induced by global change. , 2009, Ecology.

[53]  Yiqi Luo.  Terrestrial Carbon-Cycle Feedback to Climate Warming , 2007 .

[54]  A. Lüscher,et al.  Elevated CO2 increases carbon allocation to the roots of Lolium perenne under free‐air CO2 enrichment but not in a controlled environment , 2002 .

[55]  Tiina Markkanen,et al.  Air temperature triggers the recovery of evergreen boreal forest photosynthesis in spring , 2003 .

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

[57]  B. Drake,et al.  MORE EFFICIENT PLANTS: A Consequence of Rising Atmospheric CO2? , 1997, Annual review of plant physiology and plant molecular biology.

[58]  Daniel G. Milchunas,et al.  CO2 ENHANCES PRODUCTIVITY, ALTERS SPECIES COMPOSITION, AND REDUCES DIGESTIBILITY OF SHORTGRASS STEPPE VEGETATION , 2004 .

[59]  Markus Reichstein,et al.  Consequences of More Extreme Precipitation Regimes for Terrestrial Ecosystems , 2008 .

[60]  Robert D. Berryman,et al.  Point Sampling Digital Imagery with ‘Samplepoint’ , 2006, Environmental monitoring and assessment.

[61]  C. Field,et al.  The velocity of climate change , 2009, Nature.

[62]  K. Trenberth,et al.  Modern Global Climate Change , 2003, Science.

[63]  P. Reich,et al.  Nitrogen limitation constrains sustainability of ecosystem response to CO2 , 2006, Nature.

[64]  Pang-Ning Tan,et al.  Continental-scale comparisons of terrestrial carbon sinks estimated from satellite data and ecosystem modeling 1982–1998 , 2003 .

[65]  T. Sharkey,et al.  Acclimation of Photosynthesis to Elevated CO(2) in Five C(3) Species. , 1989, Plant physiology.

[66]  Christopher B. Field,et al.  Changing feedbacks in the climate–biosphere system , 2008 .

[67]  M. Power,et al.  Species Interactions Reverse Grassland Responses to Changing Climate , 2007, Science.

[68]  C. Gunderson,et al.  Thermal plasticity of photosynthesis: the role of acclimation in forest responses to a warming climate , 2009 .

[69]  E. Cook,et al.  A 1,200-year perspective of 21st century drought in southwestern North America , 2010, Proceedings of the National Academy of Sciences.

[70]  D. Jiang,et al.  Vegetation feedback under future global warming , 2011 .

[71]  Elena Aikawa,et al.  A Novel Quantitative Approach for Eliminating Sample-To-Sample Variation Using a Hue Saturation Value Analysis Program , 2014, PloS one.

[72]  Osvaldo E. Sala,et al.  A non-destructive and rapid method to estimate biomass and aboveground net primary production in arid environments , 2007 .

[73]  D. Hollinger,et al.  Use of digital webcam images to track spring green-up in a deciduous broadleaf forest , 2007, Oecologia.

[74]  D. Ellsworth,et al.  Functional responses of plants to elevated atmospheric CO2– do photosynthetic and productivity data from FACE experiments support early predictions? , 2004 .

[75]  Gregory S. McMaster,et al.  Elevated CO2 further lengthens growing season under warming conditions , 2014, Nature.

[76]  P. Newton,et al.  Seasonal not annual rainfall determines grassland biomass response to carbon dioxide , 2014, Nature.

[77]  E. Pendall,et al.  Long-term exposure to elevated CO2 enhances plant community stability by suppressing dominant plant species in a mixed-grass prairie , 2014, Proceedings of the National Academy of Sciences.

[78]  Christopher B. Field,et al.  Diverse responses of phenology to global changes in a grassland ecosystem , 2006, Proceedings of the National Academy of Sciences.

[79]  M. S. Moran,et al.  Ecosystem resilience despite large-scale altered hydroclimatic conditions , 2013, Nature.

[80]  M. Loik,et al.  Photosynthetic responses of Mojave Desert shrubs to free air CO2 enrichment are greatest during wet years , 2003 .

[81]  N. Pettorelli,et al.  Using the satellite-derived NDVI to assess ecological responses to environmental change. , 2005, Trends in ecology & evolution.

[82]  Douglas E. Johnson,et al.  Technical Note: Lightweight Camera Stand for Close-to-Earth Remote Sensing , 2004 .

[83]  Mark West,et al.  Carbon dioxide enrichment alters plant community structure and accelerates shrub growth in the shortgrass steppe , 2007, Proceedings of the National Academy of Sciences.

[84]  F. Dijkstra,et al.  Simple additive effects are rare: a quantitative review of plant biomass and soil process responses to combined manipulations of CO2 and temperature , 2012, Global change biology.

[85]  Maosheng Zhao,et al.  Drought-Induced Reduction in Global Terrestrial Net Primary Production from 2000 Through 2009 , 2010, Science.

[86]  Ranga B. Myneni,et al.  Relation between interannual variations in satellite measures of northern forest greenness and climate between 1982 and 1999 , 2003 .

[87]  Connie A. Woodhouse,et al.  A 431-Yr Reconstruction of Western Colorado Snowpack from Tree Rings , 2003 .

[88]  A. Kinzig,et al.  Global Warming and Soil Microclimate: Results from a Meadow‐Warming Experiment , 1995 .

[89]  Bruce E. Gorham,et al.  Using digital photographs and object-based image analysis to estimate percent ground cover in vegetation plots , 2006 .

[90]  Corinne Le Quéré,et al.  Contributions to accelerating atmospheric CO2 growth from economic activity, carbon intensity, and efficiency of natural sinks , 2007, Proceedings of the National Academy of Sciences.

[91]  Y. Xue,et al.  Terrestrial biosphere models need better representation of vegetation phenology: results from the North American Carbon Program Site Synthesis , 2012 .

[92]  W. Shen,et al.  Effects of changing precipitation regimes on dryland soil respiration and C pool dynamics at rainfall event, seasonal and interannual scales , 2008 .

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

[94]  E. Leger,et al.  Strong natural selection during plant restoration favors an unexpected suite of plant traits , 2013, Evolutionary applications.

[95]  J. Paruelo,et al.  ANPP ESTIMATES FROM NDVI FOR THE CENTRAL GRASSLAND REGION OF THE UNITED STATES , 1997 .

[96]  K. Price,et al.  Temporal responses of NDVI to precipitation and temperature in the central Great Plains, USA , 2003 .

[97]  Andrew D Richardson,et al.  Near-surface remote sensing of spatial and temporal variation in canopy phenology. , 2009, Ecological applications : a publication of the Ecological Society of America.