Warming induces divergent stomatal dynamics in co-occurring boreal trees

Dusenge, Mirindi E.; Ward, Eric J.; Warren, Jeffrey M.; Stinziano, Joseph R.; Wullschleger, Stan D.; Hanson, Paul J.; Way, Danielle A.

doi:10.1111/gcb.15620

Warming induces divergent stomatal dynamics in co-occurring boreal trees

Journal Article · Fri Apr 23 00:00:00 EDT 2021 · Global Change Biology

DOI:https://doi.org/10.1111/gcb.15620· OSTI ID:1784475

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Univ. of Western Ontario, London, ON (Canada); Univ. of Gothenburg (Sweden)
US Geological Survey, Lafayette, VA (United States); Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
Univ. of Western Ontario, London, ON (Canada); Univ. of New Mexico, Albuquerque, NM (United States)
Univ. of Western Ontario, London, ON (Canada); Duke Univ., Durham, NC (United States); Australian National Univ., Canberra, ACT (Australia); Brookhaven National Lab. (BNL), Upton, NY (United States)

Abstract Climate warming will alter photosynthesis and respiration not only via direct temperature effects on leaf biochemistry but also by increasing atmospheric dryness, thereby reducing stomatal conductance and suppressing photosynthesis. Our knowledge on how climate warming affects these processes is mainly derived from seedlings grown under highly controlled conditions. However, little is known regarding temperature responses of trees growing under field settings. We exposed mature tamarack and black spruce trees growing in a peatland ecosystem to whole-ecosystem warming of up to +9°C above ambient air temperatures in an ongoing long-term experiment (SPRUCE: Spruce and Peatland Responses Under Changing Environments). Here, we report the responses of leaf gas exchange after the first two years of warming. We show that the two species exhibit divergent stomatal responses to warming and vapor pressure deficit. Warming of up to 9°C increased leaf N in both spruce and tamarack. However, higher leaf N in the warmer plots translate into higher photosynthesis in tamarack but not in spruce, with photosynthesis being more constrained by stomatal limitations in spruce than in tamarack under warm conditions. Surprisingly, dark respiration did not acclimate to warming in spruce, and thermal acclimation of respiration was only seen in tamarack once changes in leaf N were considered. Our results highlight how warming can lead to differing stomatal responses to warming in co-occurring species, with consequent effects on both vegetation carbon and water dynamics.

View Accepted Manuscript (DOE)

Research Organization:: Brookhaven National Laboratory (BNL), Upton, NY (United States); Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)

Sponsoring Organization:: USDOE; USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: AC05-00OR22725; SC0012704

OSTI ID:: 1784475

Alternate ID(s):: OSTI ID: 1780121
OSTI ID: 1798632

Report Number(s):: BNL--221449-2021-JAAM

Journal Information:: Global Change Biology, Journal Name: Global Change Biology Journal Issue: 13 Vol. 27; ISSN 1354-1013

Publisher:: WileyCopyright Statement

Country of Publication:: United States

Language:: English

References (88)

Increasing net ecosystem biomass production of Canada's boreal and temperate forests despite decline in dry climates: FOREST GROWTH ENHANCEMENT IN CANADA Hember, Robbie A.; Kurz, Werner A.; Coops, Nicholas C. Global Biogeochemical Cycles, Vol. 31, Issue 1 https://doi.org/10.1002/2016GB005459	journal	January 2017
Field-quantified responses of tropical rainforest aboveground productivity to increasing CO ₂ and climatic stress, 1997-2009 : TROPICAL RAINFOREST PRODUCTIVITY RESPONSES Clark, Deborah A.; Clark, David B.; Oberbauer, Steven F. Journal of Geophysical Research: Biogeosciences, Vol. 118, Issue 2 https://doi.org/10.1002/jgrg.20067	journal	May 2013
An Introduction to Environmental Biophysics Campbell, Gaylon S.; Norman, John M. Springer New York, NY https://doi.org/10.1007/978-1-4612-1626-1	book	January 1998
Different photosynthesis-nitrogen relations in deciduous hardwood and evergreen coniferous tree species Reich, P. B.; Walters, M. B.; Kloeppel, B. D. Oecologia, Vol. 104, Issue 1 https://doi.org/10.1007/BF00365558	journal	January 1995
Photosynthesis and nitrogen relationships in leaves of C3 plants Evans, John R. Oecologia, Vol. 78, Issue 1 https://doi.org/10.1007/BF00377192	journal	January 1989
The CLIMEX soil-heating experiment: soil response after 2 years of treatment Verburg, P. S. J.; Van Loon, W. K. P.; Lükewille, A. Biology and Fertility of Soils, Vol. 28, Issue 3 https://doi.org/10.1007/s003740050493	journal	January 1999
Soil nitrogen availability, plant luxury consumption, and herbivory by white-tailed deer Tripler, C.; Canham, C.; Inouye, R. Oecologia, Vol. 133, Issue 4 https://doi.org/10.1007/s00442-002-1046-x	journal	December 2002
General patterns of acclimation of leaf respiration to elevated temperatures across biomes and plant types Slot, Martijn; Kitajima, Kaoru Oecologia, Vol. 177, Issue 3 https://doi.org/10.1007/s00442-014-3159-4	journal	December 2014
Impacts of Elevated Carbon Dioxide and Temperature on a Boreal Forest Ecosystem (CLIMEX Project) Breemen, Nico van; Jenkins, Alan; Wright, Richard F. Ecosystems, Vol. 1, Issue 4 https://doi.org/10.1007/s100219900028	journal	July 1998
Fine-root growth in a forested bog is seasonally dynamic, but shallowly distributed in nutrient-poor peat Iversen, Colleen M.; Childs, Joanne; Norby, Richard J. Plant and Soil, Vol. 424, Issue 1-2, p. 123-143 https://doi.org/10.1007/s11104-017-3231-z	journal	March 2017
Thermal acclimation of photosynthesis: on the importance of adjusting our definitions and accounting for thermal acclimation of respiration Way, Danielle A.; Yamori, Wataru Photosynthesis Research, Vol. 119, Issue 1-2 https://doi.org/10.1007/s11120-013-9873-7	journal	June 2013
Thermal acclimation and the dynamic response of plant respiration to temperature Atkin, O. Trends in Plant Science, Vol. 8, Issue 7 https://doi.org/10.1016/S1360-1385(03)00136-5	journal	July 2003
Growth of European beech (Fagus sylvatica L.) saplings is limited by elevated atmospheric vapour pressure deficits Lendzion, Jasmin; Leuschner, Christoph Forest Ecology and Management, Vol. 256, Issue 4 https://doi.org/10.1016/j.foreco.2008.05.008	journal	August 2008
Tamm Review: On the nature of the nitrogen limitation to plant growth in Fennoscandian boreal forests Högberg, Peter; Näsholm, Torgny; Franklin, Oskar Forest Ecology and Management, Vol. 403 https://doi.org/10.1016/j.foreco.2017.04.045	journal	November 2017
Acclimation of ecosystem CO2 exchange in the Alaskan Arctic in response to decadal climate warming Oechel, Walter C.; Vourlitis, George L.; Hastings, Steven J. Nature, Vol. 406, Issue 6799 https://doi.org/10.1038/35023137	journal	August 2000
Death from drought in tropical forests is triggered by hydraulics not carbon starvation Rowland, L.; da Costa, A. C. L.; Galbraith, D. R. Nature, Vol. 528, Issue 7580 https://doi.org/10.1038/nature15539	journal	November 2015
Boreal and temperate trees show strong acclimation of respiration to warming Reich, Peter B.; Sendall, Kerrie M.; Stefanski, Artur Nature, Vol. 531, Issue 7596 https://doi.org/10.1038/nature17142	journal	March 2016
A drought-induced pervasive increase in tree mortality across Canada's boreal forests Peng, Changhui; Ma, Zhihai; Lei, Xiangdong Nature Climate Change, Vol. 1, Issue 9 https://doi.org/10.1038/nclimate1293	journal	November 2011
Temperature as a potent driver of regional forest drought stress and tree mortality Park Williams, A.; Allen, Craig D.; Macalady, Alison K. Nature Climate Change, Vol. 3, Issue 3 https://doi.org/10.1038/nclimate1693	journal	September 2012
Geographic range predicts photosynthetic and growth response to warming in co-occurring tree species Reich, Peter B.; Sendall, Kerrie M.; Rice, Karen Nature Climate Change, Vol. 5, Issue 2 https://doi.org/10.1038/nclimate2497	journal	January 2015
The increasing importance of atmospheric demand for ecosystem water and carbon fluxes Novick, Kimberly A.; Ficklin, Darren L.; Stoy, Paul C. Nature Climate Change, Vol. 6, Issue 11 https://doi.org/10.1038/nclimate3114	journal	September 2016
Boreal forest biomass accumulation is not increased by two decades of soil warming Lim, Hyungwoo; Oren, Ram; Näsholm, Torgny Nature Climate Change, Vol. 9, Issue 1 https://doi.org/10.1038/s41558-018-0373-9	journal	December 2018
A multi-species synthesis of physiological mechanisms in drought-induced tree mortality Adams, Henry D.; Zeppel, Melanie J. B.; Anderegg, William R. L. Nature Ecology & Evolution, Vol. 1, Issue 9 https://doi.org/10.1038/s41559-017-0248-x	journal	August 2017
Plant functional trait change across a warming tundra biome Bjorkman, Anne D.; Myers-Smith, Isla H.; Elmendorf, Sarah C. Nature, Vol. 562, Issue 7725 https://doi.org/10.1038/s41586-018-0563-7	journal	September 2018
Limited evidence of declining growth among moisture-limited black and white spruce in interior Alaska Sullivan, Patrick F.; Pattison, Robert R.; Brownlee, Annalis H. Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/s41598-017-15644-7	journal	November 2017
Leaf-level resource use for evergreen and deciduous conifers along a resource availability gradient: Deciduous and evergreen conifer leaf gas exchange Kloeppel, B. D.; Gower, S. T.; Vogel, J. G. Functional Ecology, Vol. 14, Issue 3 https://doi.org/10.1046/j.1365-2435.2000.00439.x	journal	June 2000
Changes in leaf nitrogen and carbohydrates underlie temperature and CO ₂ acclimation of dark respiration in five boreal tree species Tjoelker, M. G.; Reich, P. B.; Oleksyn, J. Plant, Cell and Environment, Vol. 22, Issue 7 https://doi.org/10.1046/j.1365-3040.1999.00435.x	journal	July 1999
Survey and synthesis of intra- and interspecific variation in stomatal sensitivity to vapour pressure deficit: Intra- and interspecific variation in stomatal sensitivity to vapour pressure deficit Oren, R.; Sperry, J. S.; Katul, G. G. Plant, Cell & Environment, Vol. 22, Issue 12 https://doi.org/10.1046/j.1365-3040.1999.00513.x	journal	December 1999
Soil warming, carbon-nitrogen interactions, and forest carbon budgets Melillo, J. M.; Butler, S.; Johnson, J. Proceedings of the National Academy of Sciences, Vol. 108, Issue 23 https://doi.org/10.1073/pnas.1018189108	journal	May 2011
Half-century evidence from western Canada shows forest dynamics are primarily driven by competition followed by climate Zhang, Jian; Huang, Shongming; He, Fangliang Proceedings of the National Academy of Sciences, Vol. 112, Issue 13 https://doi.org/10.1073/pnas.1420844112	journal	March 2015
Convergence in the temperature response of leaf respiration across biomes and plant functional types Heskel, Mary A.; O’Sullivan, Odhran S.; Reich, Peter B. Proceedings of the National Academy of Sciences, Vol. 113, Issue 14 https://doi.org/10.1073/pnas.1520282113	journal	March 2016
Nonlinear, interacting responses to climate limit grassland production under global change Zhu, Kai; Chiariello, Nona R.; Tobeck, Todd Proceedings of the National Academy of Sciences, Vol. 113, Issue 38 https://doi.org/10.1073/pnas.1606734113	journal	September 2016
No growth stimulation of Canada’s boreal forest under half-century of combined warming and CO ₂ fertilization Girardin, Martin P.; Bouriaud, Olivier; Hogg, Edward H. Proceedings of the National Academy of Sciences, Vol. 113, Issue 52 https://doi.org/10.1073/pnas.1610156113	journal	December 2016
Global change effects on plant communities are magnified by time and the number of global change factors imposed Komatsu, Kimberly J.; Avolio, Meghan L.; Lemoine, Nathan P. Proceedings of the National Academy of Sciences, Vol. 116, Issue 36 https://doi.org/10.1073/pnas.1819027116	journal	August 2019
Untangling methodological and scale considerations in growth and productivity trend estimates of Canada’s forests Marchand, William; Girardin, Martin P.; Gauthier, Sylvie Environmental Research Letters, Vol. 13, Issue 9 https://doi.org/10.1088/1748-9326/aad82a	journal	August 2018
Response of ecosystem intrinsic water use efficiency and gross primary productivity to rising vapor pressure deficit Zhang, Quan; Ficklin, Darren L.; Manzoni, Stefano Environmental Research Letters, Vol. 14, Issue 7 https://doi.org/10.1088/1748-9326/ab2603	journal	July 2019
Thermal acclimation of photosynthesis and respiration of southern and northern white spruce seed sources tested along a regional climatic gradient indicates limited potential to cope with temperature warming Benomar, Lahcen; Lamhamedi, Mohammed S.; Pepin, Steeve Annals of Botany, Vol. 121, Issue 3 https://doi.org/10.1093/aob/mcx174	journal	December 2017
Photosynthetic responses to needle water potentials in Scots pine after a four-year exposure to elevated CO2 and temperature Kellomaki, S.; Wang, K. -Y. Tree Physiology, Vol. 16, Issue 9 https://doi.org/10.1093/treephys/16.9.765	journal	September 1996
Seedlings of five boreal tree species differ in acclimation of net photosynthesis to elevated CO2 and temperature Tjoelker, M. G.; Oleksyn, J.; Reich, P. B. Tree Physiology, Vol. 18, Issue 11 https://doi.org/10.1093/treephys/18.11.715	journal	November 1998
Ecosystem warming does not affect photosynthesis or aboveground autotrophic respiration for boreal black spruce Bronson, D. R.; Gower, S. T. Tree Physiology, Vol. 30, Issue 4 https://doi.org/10.1093/treephys/tpq001	journal	February 2010
Differential responses to changes in growth temperature between trees from different functional groups and biomes: a review and synthesis of data Way, D. A.; Oren, R. Tree Physiology, Vol. 30, Issue 6 https://doi.org/10.1093/treephys/tpq015	journal	April 2010
Growth of mature boreal Norway spruce was not affected by elevated [CO2] and/or air temperature unless nutrient availability was improved Sigurdsson, B. D.; Medhurst, J. L.; Wallin, G. Tree Physiology, Vol. 33, Issue 11 https://doi.org/10.1093/treephys/tpt043	journal	July 2013
Acclimation of light and dark respiration to experimental and seasonal warming are mediated by changes in leaf nitrogen in Eucalyptus globulus Crous, K. Y.; Wallin, G.; Atkin, O. K. Tree Physiology, Vol. 37, Issue 8 https://doi.org/10.1093/treephys/tpx052	journal	May 2017
Boreal tree hydrodynamics: asynchronous, diverging, yet complementary Pappas, Christoforos; Matheny, Ashley M.; Baltzer, Jennifer L. Tree Physiology, Vol. 38, Issue 7 https://doi.org/10.1093/treephys/tpy043	journal	May 2018
Simulated projections of boreal forest peatland ecosystem productivity are sensitive to observed seasonality in leaf physiology† Jensen, Anna M.; Warren, Jeffrey M.; King, Anthony W. Tree Physiology, Vol. 39, Issue 4 https://doi.org/10.1093/treephys/tpy140	journal	January 2019
The variability of stomatal sensitivity to leaf water potential across tree species indicates a continuum between isohydric and anisohydric behaviours Klein, Tamir Functional Ecology, Vol. 28, Issue 6 https://doi.org/10.1111/1365-2435.12289	journal	May 2014
Water use by Swedish boreal forests in a changing climate Hasper, Thomas B.; Wallin, Göran; Lamba, Shubhangi Functional Ecology, Vol. 30, Issue 5 https://doi.org/10.1111/1365-2435.12546	journal	September 2015
Unusual forest growth decline in boreal North America covaries with the retreat of Arctic sea ice Girardin, Martin P.; Guo, Xiao Jing; De Jong, Rogier Global Change Biology, Vol. 20, Issue 3 https://doi.org/10.1111/gcb.12400	journal	December 2013
Acclimation of photosynthetic temperature optima of temperate and boreal tree species in response to experimental forest warming Sendall, Kerrie M.; Reich, Peter B.; Zhao, Changming Global Change Biology, Vol. 21, Issue 3 https://doi.org/10.1111/gcb.12781	journal	December 2014
Negative impacts of high temperatures on growth of black spruce forests intensify with the anticipated climate warming Girardin, Martin P.; Hogg, Edward H.; Bernier, Pierre Y. Global Change Biology, Vol. 22, Issue 2 https://doi.org/10.1111/gcb.13072	journal	October 2015
Carbon fluxes acclimate more strongly to elevated growth temperatures than to elevated CO ₂ concentrations in a northern conifer Kroner, Yulia; Way, Danielle A. Global Change Biology, Vol. 22, Issue 8 https://doi.org/10.1111/gcb.13215	journal	March 2016
Strong thermal acclimation of photosynthesis in tropical and temperate wet-forest tree species: the importance of altered Rubisco content Scafaro, Andrew P.; Xiang, Shuang; Long, Benedict M. Global Change Biology, Vol. 23, Issue 7 https://doi.org/10.1111/gcb.13566	journal	January 2017
Short-term acclimation to warmer temperatures accelerates leaf carbon exchange processes across plant types Smith, Nicholas G.; Dukes, Jeffrey S. Global Change Biology, Vol. 23, Issue 11 https://doi.org/10.1111/gcb.13735	journal	May 2017
Photosynthetic capacity and leaf nitrogen decline along a controlled climate gradient in provenances of two widely distributed Eucalyptus species Crous, Kristine Y.; Drake, John E.; Aspinwall, Michael J. Global Change Biology, Vol. 24, Issue 10 https://doi.org/10.1111/gcb.14330	journal	June 2018
Taxonomy, together with ontogeny and growing conditions, drives needleleaf species' sensitivity to climate in boreal North America Marchand, William; Girardin, Martin P.; Hartmann, Henrik Global Change Biology, Vol. 25, Issue 8 https://doi.org/10.1111/gcb.14665	journal	May 2019
Surprising lack of sensitivity of biochemical limitation of photosynthesis of nine tree species to open‐air experimental warming and reduced rainfall in a southern boreal forest Stefanski, Artur; Bermudez, Raimundo; Sendall, Kerrie M. Global Change Biology, Vol. 26, Issue 2 https://doi.org/10.1111/gcb.14805	journal	September 2019
Acclimation of leaf respiration consistent with optimal photosynthetic capacity Wang, Han; Atkin, Owen K.; Keenan, Trevor F. Global Change Biology, Vol. 26, Issue 4 https://doi.org/10.1111/gcb.14980	journal	February 2020
Contrasting acclimation responses to elevated CO ₂ and warming between an evergreen and a deciduous boreal conifer Dusenge, Mirindi E.; Madhavji, Sasha; Way, Danielle A. Global Change Biology, Vol. 26, Issue 6 https://doi.org/10.1111/gcb.15084	journal	April 2020
Strong overestimation of water‐use efficiency responses to rising CO ₂ in tree‐ring studies Marchand, William; Girardin, Martin P.; Hartmann, Henrik Global Change Biology, Vol. 26, Issue 8 https://doi.org/10.1111/gcb.15166	journal	June 2020
Divergent species‐specific impacts of whole ecosystem warming and elevated CO ₂ on vegetation water relations in an ombrotrophic peatland Warren, Jeffrey M.; Jensen, Anna M.; Ward, Eric J. Global Change Biology, Vol. 27, Issue 9 https://doi.org/10.1111/gcb.15543	journal	February 2021
Impacts of climate change on natural forest productivity - evidence since the middle of the 20th century Boisvenue, Celine; Running, Steven W. Global Change Biology, Vol. 12, Issue 5 https://doi.org/10.1111/j.1365-2486.2006.01134.x	journal	May 2006
Elevated growth temperatures reduce the carbon gain of black spruce [Picea mariana (Mill.) B.S.P.] Way, Danielle A.; Sage, Rowan F. Global Change Biology, Vol. 14, Issue 3 https://doi.org/10.1111/j.1365-2486.2007.01513.x	journal	March 2008
Reconciling plant strategy theories of Grime and Tilman Craine, Joseph M. Journal of Ecology, Vol. 93, Issue 6 https://doi.org/10.1111/j.1365-2745.2005.01043.x	journal	July 2005
Thermal acclimation of photosynthesis in black spruce [ Picea mariana (Mill.) B.S.P.] Way, Danielle A.; Sage, Rowan F. Plant, Cell & Environment, Vol. 31, Issue 9 https://doi.org/10.1111/j.1365-3040.2008.01842.x	journal	September 2008
Global assessment of experimental climate warming on tundra vegetation: heterogeneity over space and time: Warming effects on tundra vegetation Elmendorf, Sarah C.; Henry, Gregory H. R.; Hollister, Robert D. Ecology Letters, Vol. 15, Issue 2 https://doi.org/10.1111/j.1461-0248.2011.01716.x	journal	December 2011
Mechanisms of plant survival and mortality during drought: why do some plants survive while others succumb to drought? McDowell, Nate; Pockman, William T.; Allen, Craig D. New Phytologist, Vol. 178, Issue 4 https://doi.org/10.1111/j.1469-8137.2008.02436.x	journal	June 2008
Rubisco: still the most abundant protein of Earth? Raven, John A. New Phytologist, Vol. 198, Issue 1 https://doi.org/10.1111/nph.12197	journal	February 2013
Drivers and mechanisms of tree mortality in moist tropical forests McDowell, Nate; Allen, Craig D.; Anderson-Teixeira, Kristina New Phytologist, Vol. 219, Issue 3 https://doi.org/10.1111/nph.15027	journal	February 2018
Plant carbon metabolism and climate change: elevated CO ₂ and temperature impacts on photosynthesis, photorespiration and respiration Dusenge, Mirindi Eric; Duarte, André Galvao; Way, Danielle A. New Phytologist, Vol. 221, Issue 1 https://doi.org/10.1111/nph.15283	journal	July 2018
Core principles which explain variation in respiration across biological scales O'Leary, Brendan M.; Asao, Shinichi; Millar, A. Harvey New Phytologist, Vol. 222, Issue 2 https://doi.org/10.1111/nph.15576	journal	December 2018
Plant responses to rising vapor pressure deficit Grossiord, Charlotte; Buckley, Thomas N.; Cernusak, Lucas A. New Phytologist, Vol. 226, Issue 6 https://doi.org/10.1111/nph.16485	journal	March 2020
Diel‐ and temperature‐driven variation of leaf dark respiration rates and metabolite levels in rice Rashid, Fatimah Azzahra Ahmad; Scafaro, Andrew P.; Asao, Shinichi New Phytologist, Vol. 228, Issue 1 https://doi.org/10.1111/nph.16661	journal	June 2020
Acclimation of leaf respiration temperature responses across thermally contrasting biomes Zhu, Lingling; Bloomfield, Keith J.; Asao, Shinichi New Phytologist, Vol. 229, Issue 3 https://doi.org/10.1111/nph.16929	journal	October 2020
Complete or overcompensatory thermal acclimation of leaf dark respiration in African tropical trees Mujawamariya, Myriam; Wittemann, Maria; Manishimwe, Aloysie New Phytologist, Vol. 229, Issue 5 https://doi.org/10.1111/nph.17038	journal	December 2020
High-resolution temperature responses of leaf respiration in snow gum ( Eucalyptus pauciflora ) reveal high-temperature limits to respiratory function : Temperature dependence of leaf respiration O'Sullivan, Odhran S.; Weerasinghe, K. W. Lasantha K.; Evans, John R. Plant, Cell & Environment, Vol. 36, Issue 7 https://doi.org/10.1111/pce.12057	journal	January 2013
Autumn photosynthetic decline and growth cessation in seedlings of white spruce are decoupled under warming and photoperiod manipulations: Day length and warming alter carbon and growth Stinziano, Joseph R.; Way, Danielle A. Plant, Cell & Environment, Vol. 40, Issue 8 https://doi.org/10.1111/pce.12917	journal	March 2017
Physiological acclimation dampens initial effects of elevated temperature and atmospheric CO ₂ concentration in mature boreal Norway spruce Lamba, Shubhangi; Hall, Marianne; Räntfors, Mats Plant, Cell & Environment, Vol. 41, Issue 2 https://doi.org/10.1111/pce.13079	journal	December 2017
Contrasting acclimation abilities of two dominant boreal conifers to elevated CO ₂ and temperature: CO ₂ and warming effects on spruce and pine Kurepin, Leonid V.; Stangl, Zsofia R.; Ivanov, Alexander G. Plant, Cell & Environment, Vol. 41, Issue 6 https://doi.org/10.1111/pce.13158	journal	March 2018
Climate-Driven Increases in Global Terrestrial Net Primary Production from 1982 to 1999 Nemani, R. R. Science, Vol. 300, Issue 5625 https://doi.org/10.1126/science.1082750	journal	June 2003
A Large and Persistent Carbon Sink in the World's Forests Pan, Y.; Birdsey, R. A.; Fang, J. Science, Vol. 333, Issue 6045 https://doi.org/10.1126/science.1201609	journal	July 2011
Enhanced Seasonal Exchange of CO2 by Northern Ecosystems Since 1960 Graven, H. D.; Keeling, R. F.; Piper, S. C. Science, Vol. 341, Issue 6150 https://doi.org/10.1126/science.1239207	journal	August 2013
Carbon in Canada’s boreal forest — A synthesis Kurz, W. A.; Shaw, C. H.; Boisvenue, C. Environmental Reviews, Vol. 21, Issue 4 https://doi.org/10.1139/er-2013-0041	journal	December 2013
Optimizing nitrogen loading of Picea mariana seedlings during nursery culture Salifu, K. F.; Timmer, V. R. Canadian Journal of Forest Research, Vol. 33, Issue 7 https://doi.org/10.1139/x03-057	journal	July 2003
Higher Thermal Acclimation Potential of Respiration but Not Photosynthesis in Two Alpine Picea Taxa in Contrast to Two Lowland Congeners Zhang, Xiao Wei; Wang, Jing Ru; Ji, Ming Fei PLOS ONE, Vol. 10, Issue 4 https://doi.org/10.1371/journal.pone.0123248	journal	April 2015
The Split-Apply-Combine Strategy for Data Analysis Wickham, Hadley Journal of Statistical Software, Vol. 40, Issue 1 https://doi.org/10.18637/jss.v040.i01	journal	January 2011
RESPONSES OF N-LIMITED ECOSYSTEMS TO INCREASED CO ₂ : A BALANCED-NUTRITION, COUPLED-ELEMENT-CYCLES MODEL Rastetter, Edward B.; Ågren, Göran I.; Shaver, Gaius R. Ecological Applications, Vol. 7, Issue 2 https://doi.org/10.1890/1051-0761(1997)007[0444:RONLET]2.0.CO;2	journal	May 1997
Larches: Deciduous Conifers in an Evergreen World Gower, Stith T.; Richards, James H. BioScience, Vol. 40, Issue 11 https://doi.org/10.2307/1311484	journal	December 1990
Attaining whole-ecosystem warming using air and deep-soil heating methods with an elevated CO ₂ atmosphere Hanson, Paul J.; Riggs, Jeffery S.; Nettles, W. Robert Biogeosciences, Vol. 14, Issue 4 https://doi.org/10.5194/bg-14-861-2017	journal	January 2017

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54 ENVIRONMENTAL SCIENCES
boreal conifers
leaf habit
photosynthesis
respiration
stomatal conductance
thermal acclimation
whole-ecosystem warming

Warming induces divergent stomatal dynamics in co-occurring boreal trees

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