Limitations to winter and spring photosynthesis of a Rocky Mountain subalpine forest

Abstract Temperate and boreal conifer forests are dormant for many months during the cold season. Climate change is altering the winter environment, with increased temperature, altered precipitation, and earlier snowmelt in many locations. If significant enough, these changes may alter patterns of dormancy and activity of evergreens. Here we studied the factors limiting photosynthetic activity of a high-elevation subalpine forest that has undergone substantial warming in recent decades. We tested the hypothesis that this warming has been significant enough to allow photosynthesis during sunny warm days in winter. Using thermal imagery, we found that foliage in winter was sometimes near the temperature optimum for photosynthesis, but no net carbon gain occurred for most of the cold season. Water transport was limited by blockage of sap transport by frozen boles, but not by frozen soils. Foliar carotenoid content was much higher during winter, driven largely by increases in the pool size of the photoprotective xanthophyll cycle. There was no seasonal change in chlorophyll or lutein content. Net carbon uptake began only as boles thawed, with no difference in timing among tree species, and the spring increase in canopy-level photosynthetic capacity occurred before sap transport was detected. The seasonality of gross primary productivity (GPP) was strongly linked to seasonality of xanthophyll cycle deepoxidation state in all species. Seasonality of GPP was detectable with two metrics of canopy color – the Green Chromatic Coordinate and Green-Red Vegetation Index (a proxy for the newly proposed MODIS-based chlorophyll/carotenoid index or CCI). Both indices were significantly correlated with GPP. Together these results indicate the potential for airborne or near-surface remote sensing of leaf color to serve as a metric of photosynthetic activity in evergreen forests, and to monitor physiological changes associated with the progression in and out of winter dormancy.

[1]  John A Gamon,et al.  Three causes of variation in the photochemical reflectance index (PRI) in evergreen conifers. , 2015, The New phytologist.

[2]  N. Huner,et al.  Photosynthesis of overwintering evergreen plants. , 2001, Annual review of plant biology.

[3]  Marcy E. Litvak,et al.  Differential responses of production and respiration to temperature and moisture drive the carbon balance across a climatic gradient in New Mexico , 2011 .

[4]  Damiano Gianelle,et al.  SpecNet revisited: bridging flux and remote sensing communities , 2010 .

[5]  P. Blanken,et al.  Estimating sublimation of intercepted and sub‐canopy snow using eddy covariance systems , 2007 .

[6]  John S. Sperry,et al.  Xylem Embolism in Ring‐Porous, Diffuse‐Porous, and Coniferous Trees of Northern Utah and Interior Alaska , 1994 .

[7]  Martyn P. Clark,et al.  Effects of Temperature and Precipitation Variability on Snowpack Trends in the Western United States , 2005 .

[8]  J. Belnap,et al.  Carbon, water, and energy fluxes in a semiarid cold desert grassland during and following multiyear drought , 2010 .

[9]  Richard B Primack,et al.  Leaf-out phenology of temperate woody plants: from trees to ecosystems. , 2011, The New phytologist.

[10]  A. Granier,et al.  Evaluation of transpiration in a Douglas-fir stand by means of sap flow measurements. , 1987, Tree physiology.

[11]  A. Porcar-Castell,et al.  A high-resolution portrait of the annual dynamics of photochemical and non-photochemical quenching in needles of Pinus sylvestris. , 2011, Physiologia plantarum.

[12]  J. Peñuelas,et al.  Remote estimation of carbon dioxide uptake by a Mediterranean forest , 2008 .

[13]  Stefan Jansson,et al.  Intermittent low temperatures constrain spring recovery of photosynthesis in boreal Scots pine forests , 2004 .

[14]  A. Deslauriers,et al.  The timing of spring rehydration and its relation with the onset of wood formation in black spruce , 2009 .

[15]  D. Hollinger,et al.  Statistical modeling of ecosystem respiration using eddy covariance data: Maximum likelihood parameter estimation, and Monte Carlo simulation of model and parameter uncertainty, applied to three simple models , 2005 .

[16]  John A Gamon,et al.  The photochemical reflectance index provides an optical indicator of spring photosynthetic activation in evergreen conifers. , 2015, The New phytologist.

[17]  M. Araújo,et al.  Exposure of global mountain systems to climate warming during the 21st Century , 2007 .

[18]  D. Hollinger,et al.  Influence of spring phenology on seasonal and annual carbon balance in two contrasting New England forests. , 2009, Tree physiology.

[19]  D. Bowling,et al.  Seasonal snowpack characteristics influence soil temperature and water content at multiple scales in interior western U.S. mountain ecosystems , 2014 .

[20]  Courtenay Strong,et al.  Climate change impact on the roles of temperature and precipitation in western U.S. snowpack variability , 2016 .

[21]  Martyn P. Clark,et al.  DECLINING MOUNTAIN SNOWPACK IN WESTERN NORTH AMERICA , 2005 .

[22]  David Medvigy,et al.  Diversity in plant hydraulic traits explains seasonal and inter-annual variations of vegetation dynamics in seasonally dry tropical forests. , 2016, The New phytologist.

[23]  A. Edwards,et al.  Freezing and Its Effect on Chemical and Biological Properties of Soil , 1992 .

[24]  N. McDowell,et al.  Pragmatic hydraulic theory predicts stomatal responses to climatic water deficits. , 2016, The New phytologist.

[25]  H. Mooney,et al.  Wintertime Photosynthesis of Bristlecone Pine (Pinus Aristata) In the White Mountains of California , 1967 .

[26]  Albert Porcar-Castell,et al.  Field and controlled environment measurements show strong seasonal acclimation in photosynthesis and respiration potential in boreal Scots pine , 2014, Front. Plant Sci..

[27]  L. Guanter,et al.  Satellite chlorophyll fluorescence measurements reveal large‐scale decoupling of photosynthesis and greenness dynamics in boreal evergreen forests , 2016, Global change biology.

[28]  E. DeLucia Effect of low root temperature on net photosynthesis, stomatal conductance and carbohydrate concentration in Engelmann spruce (Picea engelmannii Parry ex Engelm.) seedlings. , 1986, Tree physiology.

[29]  S. Running,et al.  Soil Temperature Influences on Root Resistance of Pinus contorta Seedlings. , 1980, Plant physiology.

[30]  Stefan Mayr,et al.  Xylem temperatures during winter in conifers at the alpine timberline , 2006 .

[31]  P. Templer,et al.  Carbon and Nitrogen Cycling in Snow‐Covered Environments , 2011 .

[32]  M. Friedl,et al.  Tracking forest phenology and seasonal physiology using digital repeat photography: a critical assessment. , 2014, Ecological applications : a publication of the Ecological Society of America.

[33]  W. W. Adams,et al.  Photoprotective Strategies of Overwintering Evergreens , 2004 .

[34]  R. Monson,et al.  Temperature as a control over ecosystem CO2 fluxes in a high-elevation, subalpine forest , 2003, Oecologia.

[35]  J. Berry,et al.  A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species , 1980, Planta.

[36]  Ingo Ensminger,et al.  Soil temperature and intermittent frost modulate the rate of recovery of photosynthesis in Scots pine under simulated spring conditions. , 2007, The New phytologist.

[37]  D. Bowling,et al.  Assessing the thermal dissipation sap flux density method for monitoring cold season water transport in seasonally snow-covered forests , 2017, Tree physiology.

[38]  Gaylon S. Campbell,et al.  Water content, hydraulic conductivity, and ice formation in winter stems of Pinus contorta: a TDR case study , 2001, Oecologia.

[39]  J. Marshall,et al.  Seasonal variation in photosynthetic capacity of montane conifers , 2004 .

[40]  A. Verhoeven Sustained energy dissipation in winter evergreens , 2014 .

[41]  A. Holzwarth,et al.  The role of the xanthophyll cycle and of lutein in photoprotection of photosystem II. , 2012, Biochimica et biophysica acta.

[42]  Bolei Zhou,et al.  Learning Deep Features for Scene Recognition using Places Database , 2014, NIPS.

[43]  John C. Lin,et al.  An observational constraint on stomatal function in forests: evaluating coupled carbon and water vapor exchange with carbon isotopes in the Community Land Model (CLM4.5) , 2016 .

[44]  E. Nikinmaa,et al.  Interpreting canopy development and physiology using a European phenology camera network at flux sites , 2015 .

[45]  Mark A. Friedl,et al.  Digital repeat photography for phenological research in forest ecosystems , 2012 .

[46]  Trevor Darrell,et al.  Caffe: Convolutional Architecture for Fast Feature Embedding , 2014, ACM Multimedia.

[47]  Zong-Liang Yang,et al.  Technical description of version 4.5 of the Community Land Model (CLM) , 2013 .

[48]  Rebecca N. Handcock,et al.  Ground-Based Optical Measurements at European Flux Sites: A Review of Methods, Instruments and Current Controversies , 2011, Sensors.

[49]  Roger C. Bales,et al.  Evapotranspiration along an elevation gradient in California's Sierra Nevada , 2012 .

[50]  P. Blanken,et al.  Contrasting long-term alpine and subalpine precipitation trends in a mid-latitude North American mountain system, Colorado Front Range, USA , 2015 .

[51]  Eero Nikinmaa,et al.  Wintertime photosynthesis and water uptake in a boreal forest. , 2006, Tree physiology.

[52]  P. Ciais,et al.  Changes in satellite‐derived vegetation growth trend in temperate and boreal Eurasia from 1982 to 2006 , 2011 .

[53]  N. Holbrook,et al.  Confronting Maxwell's demon: biophysics of xylem embolism repair. , 2009, Trends in plant science.

[54]  Michael D. Dettinger,et al.  Trends in Snowfall versus Rainfall in the Western United States , 2006 .

[55]  S. Mayr,et al.  Winter at the Alpine Timberline. Why Does Embolism Occur in Norway Spruce But Not in Stone Pine?1 , 2003, Plant Physiology.

[56]  W. Smith,et al.  SAP FLUX OF CO-OCCURRING SPECIES IN A WESTERN SUBALPINE FOREST DURING SEASONAL SOIL DROUGHT , 2000 .

[57]  Juergen Kreyling,et al.  Winter climate change: a critical factor for temperate vegetation performance. , 2010, Ecology.

[58]  S. Mayr,et al.  Uptake of Water via Branches Helps Timberline Conifers Refill Embolized Xylem in Late Winter1[C][W][OPEN] , 2014, Plant Physiology.

[59]  Charles T. Driscoll,et al.  Colder soils in a warmer world: A snow manipulation study in a northern hardwood forest ecosystem , 2001 .

[60]  David Galbraith,et al.  Linking hydraulic traits to tropical forest function in a size-structured and trait-driven model (TFS v.1-Hydro) , 2016 .

[61]  K. Steppe,et al.  Sap-flux density measurement methods: working principles and applicability. , 2013, Functional plant biology : FPB.

[62]  P. Schaberg,et al.  Photosynthetic capacity of red spruce during winter. , 1998, Tree physiology.

[63]  Chris Landry,et al.  Biological consequences of earlier snowmelt from desert dust deposition in alpine landscapes , 2009, Proceedings of the National Academy of Sciences.

[64]  P. Blanken,et al.  The influence of warm-season precipitation on the diel cycle of the surface energy balance and carbon dioxide at a Colorado subalpine forest site , 2015 .

[65]  T. Vesala,et al.  On the separation of net ecosystem exchange into assimilation and ecosystem respiration: review and improved algorithm , 2005 .

[66]  Albert Porcar-Castell,et al.  Physiology of the seasonal relationship between the photochemical reflectance index and photosynthetic light use efficiency , 2012, Oecologia.

[67]  R. Guralnick,et al.  Elevation-Dependent Temperature Trends in the Rocky Mountain Front Range: Changes over a 56- and 20-Year Record , 2012, PloS one.

[68]  S. Mayr,et al.  Winter at the alpine timberline causes complex within-tree patterns of water potential and embolism in Picea abies. , 2007, Physiologia plantarum.

[69]  W. W. Adams,et al.  Operation of the xanthophyll cycle in higher plants in response to diurnal changes in incident sunlight , 1992, Planta.

[70]  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.

[71]  C. Frankenberg,et al.  Linking chlorophyll a fluorescence to photosynthesis for remote sensing applications: mechanisms and challenges. , 2014, Journal of experimental botany.

[72]  M. Kaufmann,et al.  Leaf water stress in engelmann spruce: influence of the root and shoot environments. , 1975, Plant physiology.

[73]  A. Hall,et al.  Causes of recent changes in western North American snowpack , 2012, Climate Dynamics.

[74]  A. Granier Une nouvelle méthode pour la mesure du flux de sève brute dans le tronc des arbres , 1985 .

[75]  R. Monson,et al.  Modeling whole-tree carbon assimilation rate using observed transpiration rates and needle sugar carbon isotope ratios. , 2010, The New phytologist.

[76]  Laura Verena Junker,et al.  Zeaxanthin-independent energy quenching and alternative electron sinks cause a decoupling of the relationship between the photochemical reflectance index (PRI) and photosynthesis in an evergreen conifer during spring , 2015, Journal of experimental botany.

[77]  Philip W. Mote,et al.  The Response of Northern Hemisphere Snow Cover to a Changing Climate , 2008 .

[78]  D. Clow,et al.  Changes in the timing of snowmelt and streamflow in Colorado: a response to recent warming , 2010 .

[79]  R. Monson,et al.  Estimating transpiration and the sensitivity of carbon uptake to water availability in a subalpine forest using a simple ecosystem process model informed by measured net CO2 and H2O fluxes , 2008 .

[80]  R. Monson,et al.  Earlier snowmelt reduces atmospheric carbon uptake in midlatitude subalpine forests , 2016 .

[81]  C. Frankenberg,et al.  Application of satellite solar-induced chlorophyll fluorescence to understanding large-scale variations in vegetation phenology and function over northern high latitude forests , 2017 .

[82]  D. Hodáňová An introduction to environmental biophysics , 1979, Biologia Plantarum.

[83]  J. Lundquist,et al.  Observed compression of in situ tree stems during freezing , 2017 .

[84]  C. Tucker Red and photographic infrared linear combinations for monitoring vegetation , 1979 .

[85]  Dar A. Roberts,et al.  Continuous, long-term, high-frequency thermal imaging of vegetation: Uncertainties and recommended best practices , 2016 .

[86]  G. McCabe,et al.  Regional patterns and proximal causes of the recent snowpack decline in the Rocky Mountains, U.S. , 2013 .

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

[88]  Philippe Ciais,et al.  Large‐scale variations in the vegetation growing season and annual cycle of atmospheric CO2 at high northern latitudes from 1950 to 2011 , 2013, Global change biology.

[89]  T. Luo,et al.  Seasonal Shift in Climatic Limiting Factors on Tree Transpiration: Evidence from Sap Flow Observations at Alpine Treelines in Southeast Tibet , 2016, Front. Plant Sci..

[90]  C. Körner,et al.  Tree species diversity affects canopy leaf temperatures in a mature temperate forest , 2007 .

[91]  R. Monson,et al.  Carbon sequestration in a high‐elevation, subalpine forest , 2001 .

[92]  K. Oleson,et al.  Modeling stomatal conductance in the earth system: linking leaf water-use efficiency and water transport along the soil–plant–atmosphere continuum , 2014 .

[93]  G. Bohrer,et al.  Trait-based representation of hydrological functional properties of plants in weather and ecosystem models , 2016, Plant diversity.

[94]  M. G. Ryan Sapwood volume for three subalpine conifers: predictive equations and ecological implications , 1989 .

[95]  E. DeLucia,et al.  Influence of cold soil and snowcover on photosynthesis and leaf conductance in two Rocky Mountain conifers , 1989, Oecologia.

[96]  Scott Ferrenberg,et al.  Mountain Pine Beetle Develops an Unprecedented Summer Generation in Response to Climate Warming , 2012, The American Naturalist.

[97]  J. Hadley Effect of Daily Minimum Temperature on Photosynthesis in Eastern Hemlock (Tsuga canadensis L.) in Autumn and Winter , 2000 .

[98]  Takeshi Motohka,et al.  Applicability of Green-Red Vegetation Index for Remote Sensing of Vegetation Phenology , 2010, Remote. Sens..

[99]  Christopher J. Still,et al.  Canopy skin temperature variations in relation to climate, soil temperature, and carbon flux at a ponderosa pine forest in central Oregon , 2016 .

[100]  Todd N. Rosenstiel,et al.  Climatic influences on net ecosystem CO2 exchange during the transition from wintertime carbon source to springtime carbon sink in a high-elevation, subalpine forest , 2005, Oecologia.

[101]  Josep Peñuelas,et al.  A remotely sensed pigment index reveals photosynthetic phenology in evergreen conifers , 2016, Proceedings of the National Academy of Sciences.

[102]  Michael D. Dettinger,et al.  Changes toward Earlier Streamflow Timing across Western North America , 2005 .

[103]  R. Armstrong,et al.  Application of Satellite Remote Sensing Techniques to Frozen Ground Studies , 2004 .