DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Responses of two semiarid conifer tree species to reduced precipitation and warming reveal new perspectives for stomatal regulation

Abstract

Here, relatively anisohydric species are predicted to be more predisposed to hydraulic failure than relatively isohydric species, as they operate with narrower hydraulic safety margins. We subjected co-occurring anisohydric Juniperus monosperma and isohydric Pinus edulis trees to warming, reduced precipitation, or both, and measured their gas exchange and hydraulic responses. We found that reductions in stomatal conductance and assimilation by heat and drought were more frequent during relatively moist periods, but these effects were not exacerbated in the combined heat and drought treatment. Counter to expectations, both species exhibited similar gs temporal dynamics in response to drought. Further, whereas P. edulis exhibited chronic embolism, J. monosperma showed very little embolism due to its conservative stomatal regulation and maintenance of xylem water potential above the embolism entry point. This tight stomatal control and low levels of embolism experienced by juniper refuted the notion that very low water potentials during drought are associated with loose stomatal control and with the hypothesis that anisohydric species are more prone to hydraulic failure than isohydric species. Because direct association of stomatal behaviour with embolism resistance can be misleading, we advocate consideration of stomatal behaviour relative to embolism resistance for classifying species drought response strategies.

Authors:
ORCiD logo [1];  [2];  [2];  [2]; ORCiD logo [2];  [3];  [4];  [5];  [2];  [1];  [2]
  1. CREAF (Spain); Univ. Autonoma Barcelona (Spain)
  2. Los Alamos National Lab. (LANL), Los Alamos, NM (United States)
  3. Univ. of New Mexico, Albuquerque, NM (United States)
  4. Macquarie Univ., Sydney, NSW (Australia)
  5. Univ. of California, Santa Cruz, CA (United States)
Publication Date:
Research Org.:
Los Alamos National Laboratory (LANL), Los Alamos, NM (United States)
Sponsoring Org.:
USDOE
OSTI Identifier:
1257819
Report Number(s):
LA-UR-14-28231
Journal ID: ISSN 0140-7791
Grant/Contract Number:  
CGL2013-46808-R; CGL2010-16373; AC52-06NA25396
Resource Type:
Accepted Manuscript
Journal Name:
Plant, Cell and Environment
Additional Journal Information:
Journal Volume: 39; Journal Issue: 1; Journal ID: ISSN 0140-7791
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; 54 ENVIRONMENTAL SCIENCES; drought; increased temperature; global change; mortality; iso- vs. anisohydric behavior; stomatal conductance; hydraulic conductivity; hydraulic failure; carbon starvation

Citation Formats

Garcia-Forner, Nuria, Adams, Henry D., Sevanto, Sanna, Collins, Adam D., Dickman, Lee T., Hudson, Patrick J., Zeppel, Melanie J. B., Jenkins, Michael W., Powers, Heath, Martinez-Vilalta, Jordi, and Mcdowell, Nate G. Responses of two semiarid conifer tree species to reduced precipitation and warming reveal new perspectives for stomatal regulation. United States: N. p., 2015. Web. doi:10.1111/pce.12588.
Garcia-Forner, Nuria, Adams, Henry D., Sevanto, Sanna, Collins, Adam D., Dickman, Lee T., Hudson, Patrick J., Zeppel, Melanie J. B., Jenkins, Michael W., Powers, Heath, Martinez-Vilalta, Jordi, & Mcdowell, Nate G. Responses of two semiarid conifer tree species to reduced precipitation and warming reveal new perspectives for stomatal regulation. United States. https://doi.org/10.1111/pce.12588
Garcia-Forner, Nuria, Adams, Henry D., Sevanto, Sanna, Collins, Adam D., Dickman, Lee T., Hudson, Patrick J., Zeppel, Melanie J. B., Jenkins, Michael W., Powers, Heath, Martinez-Vilalta, Jordi, and Mcdowell, Nate G. Sat . "Responses of two semiarid conifer tree species to reduced precipitation and warming reveal new perspectives for stomatal regulation". United States. https://doi.org/10.1111/pce.12588. https://www.osti.gov/servlets/purl/1257819.
@article{osti_1257819,
title = {Responses of two semiarid conifer tree species to reduced precipitation and warming reveal new perspectives for stomatal regulation},
author = {Garcia-Forner, Nuria and Adams, Henry D. and Sevanto, Sanna and Collins, Adam D. and Dickman, Lee T. and Hudson, Patrick J. and Zeppel, Melanie J. B. and Jenkins, Michael W. and Powers, Heath and Martinez-Vilalta, Jordi and Mcdowell, Nate G.},
abstractNote = {Here, relatively anisohydric species are predicted to be more predisposed to hydraulic failure than relatively isohydric species, as they operate with narrower hydraulic safety margins. We subjected co-occurring anisohydric Juniperus monosperma and isohydric Pinus edulis trees to warming, reduced precipitation, or both, and measured their gas exchange and hydraulic responses. We found that reductions in stomatal conductance and assimilation by heat and drought were more frequent during relatively moist periods, but these effects were not exacerbated in the combined heat and drought treatment. Counter to expectations, both species exhibited similar gs temporal dynamics in response to drought. Further, whereas P. edulis exhibited chronic embolism, J. monosperma showed very little embolism due to its conservative stomatal regulation and maintenance of xylem water potential above the embolism entry point. This tight stomatal control and low levels of embolism experienced by juniper refuted the notion that very low water potentials during drought are associated with loose stomatal control and with the hypothesis that anisohydric species are more prone to hydraulic failure than isohydric species. Because direct association of stomatal behaviour with embolism resistance can be misleading, we advocate consideration of stomatal behaviour relative to embolism resistance for classifying species drought response strategies.},
doi = {10.1111/pce.12588},
journal = {Plant, Cell and Environment},
number = 1,
volume = 39,
place = {United States},
year = {Sat Aug 08 00:00:00 EDT 2015},
month = {Sat Aug 08 00:00:00 EDT 2015}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record

Citation Metrics:
Cited by: 100 works
Citation information provided by
Web of Science

Save / Share:

Works referenced in this record:

Temperature sensitivity of drought-induced tree mortality portends increased regional die-off under global-change-type drought
journal, April 2009

  • Adams, Henry D.; Guardiola-Claramonte, Maite; Barron-Gafford, Greg A.
  • Proceedings of the National Academy of Sciences, Vol. 106, Issue 17
  • DOI: 10.1073/pnas.0901438106

Nonstructural leaf carbohydrate dynamics of Pinus edulis during drought-induced tree mortality reveal role for carbon metabolism in mortality mechanism
journal, January 2013

  • Adams, Henry D.; Germino, Matthew J.; Breshears, David D.
  • New Phytologist, Vol. 197, Issue 4
  • DOI: 10.1111/nph.12102

A global overview of drought and heat-induced tree mortality reveals emerging climate change risks for forests
journal, February 2010

  • Allen, Craig D.; Macalady, Alison K.; Chenchouni, Haroun
  • Forest Ecology and Management, Vol. 259, Issue 4
  • DOI: 10.1016/j.foreco.2009.09.001

Regional vegetation die-off in response to global-change-type drought
journal, October 2005

  • Breshears, D. D.; Cobb, N. S.; Rich, P. M.
  • Proceedings of the National Academy of Sciences, Vol. 102, Issue 42
  • DOI: 10.1073/pnas.0505734102

Tree die-off in response to global change-type drought: mortality insights from a decade of plant water potential measurements
journal, May 2009

  • Breshears, David D.; Myers, Orrin B.; Meyer, Clifton W.
  • Frontiers in Ecology and the Environment, Vol. 7, Issue 4
  • DOI: 10.1890/080016

Abscisic Acid Mediates a Divergence in the Drought Response of Two Conifers
journal, May 2013


Conifer species adapt to low-rainfall climates by following one of two divergent pathways
journal, September 2014

  • Brodribb, Timothy J.; McAdam, Scott A. M.; Jordan, Gregory J.
  • Proceedings of the National Academy of Sciences, Vol. 111, Issue 40
  • DOI: 10.1073/pnas.1407930111

Understanding plant responses to drought — from genes to the whole plant
journal, January 2003

  • Chaves, Manuela M.; Maroco, João P.; Pereira, João S.
  • Functional Plant Biology, Vol. 30, Issue 3
  • DOI: 10.1071/FP02076

Global convergence in the vulnerability of forests to drought
journal, November 2012

  • Choat, Brendan; Jansen, Steven; Brodribb, Tim J.
  • Nature, Vol. 491, Issue 7426
  • DOI: 10.1038/nature11688

Use of Positive Pressures to Establish Vulnerability Curves: Further Support for the Air-Seeding Hypothesis and Implications for Pressure-Volume Analysis
journal, September 1992

  • Cochard, Hervé; Cruiziat, Pierre; Tyree, Melvin T.
  • Plant Physiology, Vol. 100, Issue 1
  • DOI: 10.1104/pp.100.1.205

Cavitation and water storage capacity in bole xylem segments of mature and young Douglas-fir trees
journal, April 2001


Carbon dynamics of eucalypt seedlings exposed to progressive drought in elevated [CO2] and elevated temperature
journal, August 2013


Carbon reserves and canopy defoliation determine the recovery of Scots pine 4 yr after a drought episode
journal, January 2011


Stomatal control of photosynthesis and transpiration
journal, March 1998


Regulation and acclimation of leaf gas exchange in a piñon-juniper woodland exposed to three different precipitation regimes: Rainfall manipulation in piñon-juniper woodland
journal, March 2013

  • Limousin, Jean-Marc; Bickford, Christopher P.; Dickman, Lee T.
  • Plant, Cell & Environment, Vol. 36, Issue 10
  • DOI: 10.1111/pce.12089

Limits to water transport in Juniperus osteosperma and Pinus edulis: implications for drought tolerance and regulation of transpiration
journal, December 1998


Mechanisms Linking Drought, Hydraulics, Carbon Metabolism, and Vegetation Mortality
journal, January 2011


Mechanisms of plant survival and mortality during drought: why do some plants survive while others succumb to drought?
journal, June 2008


Evaluating theories of drought-induced vegetation mortality using a multimodel-experiment framework
journal, September 2013

  • McDowell, Nate G.; Fisher, Rosie A.; Xu, Chonggang
  • New Phytologist, Vol. 200, Issue 2
  • DOI: 10.1111/nph.12465

A new look at water transport regulation in plants
journal, July 2014

  • Martínez-Vilalta, Jordi; Poyatos, Rafael; Aguadé, David
  • New Phytologist, Vol. 204, Issue 1
  • DOI: 10.1111/nph.12912

Stay wet or else: three ways in which plants can adjust hydraulically to their environment
journal, November 2006

  • Maseda, P. H.; Fernandez, R. J.
  • Journal of Experimental Botany, Vol. 57, Issue 15
  • DOI: 10.1093/jxb/erl127

Xylem hydraulic safety margins in woody plants: coordination of stomatal control of xylem tension with hydraulic capacitance
journal, October 2009


Dynamics of leaf water relations components in co-occurring iso- and anisohydric conifer species: Dynamics of leaf water relations components
journal, April 2014

  • Meinzer, Frederick C.; Woodruff, David R.; Marias, Danielle E.
  • Plant, Cell & Environment, Vol. 37, Issue 11
  • DOI: 10.1111/pce.12327

Co-ordination of growth, gas exchange and hydraulics define the carbon safety margin in tree species with contrasting drought strategies
journal, March 2014


Genotypic Variability in Vulnerability of Leaf Xylem to Cavitation in Water-Stressed and Well-Irrigated Sugarcane
journal, October 1992

  • Neufeld, Howard S.; Grantz, David A.; Meinzer, Frederick C.
  • Plant Physiology, Vol. 100, Issue 2
  • DOI: 10.1104/pp.100.2.1020

Assimilate transport in phloem sets conditions for leaf gas exchange: Transport stoma
journal, October 2012

  • Nikinmaa, Eero; HÖLttÄ, Teemu; Hari, Pertti
  • Plant, Cell & Environment, Vol. 36, Issue 3
  • DOI: 10.1111/pce.12004

Hydraulic limits preceding mortality in a piñon-juniper woodland under experimental drought: Hydraulic limits in a piñon-juniper woodland
journal, April 2012


Reduced transpiration response to precipitation pulses precedes mortality in a piñon-juniper woodland subject to prolonged drought
journal, July 2013

  • Plaut, Jennifer A.; Wadsworth, W. Duncan; Pangle, Robert
  • New Phytologist, Vol. 200, Issue 2
  • DOI: 10.1111/nph.12392

Water-use strategies of six co-existing Mediterranean woody species during a summer drought
journal, February 2011


Stomatal response of an anisohydric grapevine cultivar to evaporative demand, available soil moisture and abscisic acid
journal, December 2011


Carbon dynamics in trees: feast or famine?
journal, February 2012


How do trees die? A test of the hydraulic failure and carbon starvation hypotheses: How do trees die?
journal, June 2013

  • Sevanto, Sanna; Mcdowell, Nate G.; Dickman, L. Turin
  • Plant, Cell & Environment, Vol. 37, Issue 1
  • DOI: 10.1111/pce.12141

Water deficits and hydraulic limits to leaf water supply
journal, February 2002


Differential summer water use by Pinus edulis and Juniperus osteosperma reflects contrasting hydraulic characteristics
journal, December 2007


Temperature as a potent driver of regional forest drought stress and tree mortality
journal, September 2012

  • Park Williams, A.; Allen, Craig D.; Macalady, Alison K.
  • Nature Climate Change, Vol. 3, Issue 3
  • DOI: 10.1038/nclimate1693

Hydraulic traits are influenced by phylogenetic history in the drought-resistant, invasive genus Juniperus (Cupressaceae)
journal, March 2008

  • Willson, Cynthia J.; Manos, Paul S.; Jackson, Robert B.
  • American Journal of Botany, Vol. 95, Issue 3
  • DOI: 10.3732/ajb.95.3.299

High temperature causes negative whole-plant carbon balance under mild drought
journal, July 2013

  • Zhao, Junbin; Hartmann, Henrik; Trumbore, Susan
  • New Phytologist, Vol. 200, Issue 2
  • DOI: 10.1111/nph.12400

Physiological Plant Ecology
journal, June 1981


Physiological plant ecology
journal, January 1981


Stomatal control of photosynthesis and transpiration
journal, March 1998


Temperature as a potent driver of regional forest drought stress and tree mortality
text, January 2012

  • Williams, A. Park; Allen, Craig D.; Macalady, Alison K.
  • Columbia University
  • DOI: 10.7916/d8-b9ec-8z87

Physiological plant ecology
journal, January 1976


Works referencing / citing this record:

Interannual variations in needle and sapwood traits of Pinus edulis branches under an experimental drought
journal, January 2018

  • Guérin, Marceau; Martin-Benito, Dario; von Arx, Georg
  • Ecology and Evolution, Vol. 8, Issue 3
  • DOI: 10.1002/ece3.3743

Tree species and size drive water consumption of beech/spruce forests - a simulation study highlighting growth under water limitation
journal, June 2017


A multi-species synthesis of physiological mechanisms in drought-induced tree mortality
journal, August 2017

  • Adams, Henry D.; Zeppel, Melanie J. B.; Anderegg, William R. L.
  • Nature Ecology & Evolution, Vol. 1, Issue 9
  • DOI: 10.1038/s41559-017-0248-x

Unsaturation of vapour pressure inside leaves of two conifer species
journal, May 2018


Temperature response surfaces for mortality risk of tree species with future drought
journal, November 2017

  • Adams, Henry D.; Barron-Gafford, Greg A.; Minor, Rebecca L.
  • Environmental Research Letters, Vol. 12, Issue 11
  • DOI: 10.1088/1748-9326/aa93be

Gas exchange at whole plant level shows that a less conservative water use is linked to a higher performance in three ecologically distinct pine species
journal, March 2018

  • Salazar-Tortosa, D.; Castro, J.; Rubio de Casas, R.
  • Environmental Research Letters, Vol. 13, Issue 4
  • DOI: 10.1088/1748-9326/aab18f

Mechanisms of a coniferous woodland persistence under drought and heat
journal, April 2019

  • McDowell, Nate G.; Grossiord, Charlotte; Adams, Henry D.
  • Environmental Research Letters, Vol. 14, Issue 4
  • DOI: 10.1088/1748-9326/ab0921

Lack of acclimation of leaf area:sapwood area ratios in piñon pine and juniper in response to precipitation reduction and warming
journal, September 2018

  • McBranch, Natalie A.; Grossiord, Charlotte; Adams, Henry
  • Tree Physiology, Vol. 39, Issue 1
  • DOI: 10.1093/treephys/tpy066

Phenotypic interactions between tree hosts and invasive forest pathogens in the light of globalization and climate change
journal, December 2016

  • Stenlid, Jan; Oliva, Jonàs
  • Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 371, Issue 1709
  • DOI: 10.1098/rstb.2015.0455

Contrasting plant water-use responses to groundwater depth in coastal dune ecosystems
journal, April 2018

  • Antunes, Cristina; Díaz Barradas, Mari Cruz; Zunzunegui, Maria
  • Functional Ecology, Vol. 32, Issue 8
  • DOI: 10.1111/1365-2435.13110

More than iso/anisohydry: Hydroscapes integrate plant water use and drought tolerance traits in 10 eucalypt species from contrasting climates
journal, April 2019

  • Li, Ximeng; Blackman, Chris J.; Peters, Jennifer M. R.
  • Functional Ecology, Vol. 33, Issue 6
  • DOI: 10.1111/1365-2435.13320

Precipitation, not air temperature, drives functional responses of trees in semi-arid ecosystems
journal, October 2016

  • Grossiord, Charlotte; Sevanto, Sanna; Adams, Henry D.
  • Journal of Ecology, Vol. 105, Issue 1
  • DOI: 10.1111/1365-2745.12662

Poor plant performance under simulated climate change is linked to mycorrhizal responses in a semi-arid shrubland
journal, November 2017

  • León-Sánchez, Lupe; Nicolás, Emilio; Goberna, Marta
  • Journal of Ecology, Vol. 106, Issue 3
  • DOI: 10.1111/1365-2745.12888

Mapping ‘hydroscapes’ along the iso- to anisohydric continuum of stomatal regulation of plant water status
journal, September 2016

  • Meinzer, Frederick C.; Woodruff, David R.; Marias, Danielle E.
  • Ecology Letters, Vol. 19, Issue 11
  • DOI: 10.1111/ele.12670

A dynamic leaf gas-exchange strategy is conserved in woody plants under changing ambient CO 2 : evidence from carbon isotope discrimination in paleo and CO 2 enrichment studies
journal, January 2016

  • Voelker, Steven L.; Brooks, J. Renée; Meinzer, Frederick C.
  • Global Change Biology, Vol. 22, Issue 2
  • DOI: 10.1111/gcb.13102

Global variations in ecosystem-scale isohydricity
journal, July 2016

  • Konings, Alexandra G.; Gentine, Pierre
  • Global Change Biology, Vol. 23, Issue 2
  • DOI: 10.1111/gcb.13389

Groundwater drawdown drives ecophysiological adjustments of woody vegetation in a semi-arid coastal ecosystem
journal, August 2018

  • Antunes, Cristina; Chozas, Sergio; West, Jason
  • Global Change Biology, Vol. 24, Issue 10
  • DOI: 10.1111/gcb.14403

Impacts of droughts on the growth resilience of Northern Hemisphere forests: Forest growth resilience to drought
journal, September 2016

  • Gazol, A.; Camarero, J. J.; Anderegg, W. R. L.
  • Global Ecology and Biogeography, Vol. 26, Issue 2
  • DOI: 10.1111/geb.12526

Warming combined with more extreme precipitation regimes modifies the water sources used by trees
journal, September 2016

  • Grossiord, Charlotte; Sevanto, Sanna; Dawson, Todd E.
  • New Phytologist, Vol. 213, Issue 2
  • DOI: 10.1111/nph.14192

Antecedent soil water content and vapor pressure deficit interactively control water potential in Larrea tridentata
journal, August 2018

  • Guo, Jessica S.; Ogle, Kiona
  • New Phytologist, Vol. 221, Issue 1
  • DOI: 10.1111/nph.15374

Greater focus on water pools may improve our ability to understand and anticipate drought‐induced mortality in plants
journal, January 2019

  • Martinez‐Vilalta, Jordi; Anderegg, William R. L.; Sapes, Gerard
  • New Phytologist, Vol. 223, Issue 1
  • DOI: 10.1111/nph.15644

Having the right neighbors: how tree species diversity modulates drought impacts on forests
journal, January 2019


Anisohydric behavior linked to persistent hydraulic damage and delayed drought recovery across seven North American tree species
journal, February 2019

  • Kannenberg, Steven A.; Novick, Kimberly A.; Phillips, Richard P.
  • New Phytologist, Vol. 222, Issue 4
  • DOI: 10.1111/nph.15699

Conifers depend on established roots during drought: results from a coupled model of carbon allocation and hydraulics
journal, August 2019

  • Mackay, D. Scott; Savoy, Philip R.; Grossiord, Charlotte
  • New Phytologist
  • DOI: 10.1111/nph.16043

Temporal shifts in iso/anisohydry revealed from daily observations of plant water potential in a dominant desert shrub
journal, October 2019

  • Guo, Jessica S.; Hultine, Kevin R.; Koch, George W.
  • New Phytologist, Vol. 225, Issue 2
  • DOI: 10.1111/nph.16196

Conflicting demands on angiosperm xylem: Tradeoffs among storage, transport and biomechanics: Tradeoffs in xylem function
journal, December 2016

  • Pratt, R. Brandon; Jacobsen, Anna L.
  • Plant, Cell & Environment, Vol. 40, Issue 6
  • DOI: 10.1111/pce.12862

Stomatal kinetics and photosynthetic gas exchange along a continuum of isohydric to anisohydric regulation of plant water status: Leaf gas exchange and anisohydry
journal, May 2017

  • Meinzer, Frederick C.; Smith, Duncan D.; Woodruff, David R.
  • Plant, Cell & Environment, Vol. 40, Issue 8
  • DOI: 10.1111/pce.12970

Tree water dynamics in a drying and warming world: Future tree water dynamics
journal, June 2017

  • Grossiord, Charlotte; Sevanto, Sanna; Borrego, Isaac
  • Plant, Cell & Environment, Vol. 40, Issue 9
  • DOI: 10.1111/pce.12991

Co-occurring woody species have diverse hydraulic strategies and mortality rates during an extreme drought: Belowground hydraulic failure during drought
journal, January 2018

  • Johnson, Daniel M.; Domec, Jean-Christophe; Carter Berry, Z.
  • Plant, Cell & Environment, Vol. 41, Issue 3
  • DOI: 10.1111/pce.13121

Is desiccation tolerance and avoidance reflected in xylem and phloem anatomy of two coexisting arid-zone coniferous trees?: Xylem and Phloem Anatomy
journal, May 2018

  • Sevanto, Sanna; Ryan, Max; Dickman, L. Turin
  • Plant, Cell & Environment, Vol. 41, Issue 7
  • DOI: 10.1111/pce.13198

Stem radial growth and water storage responses to heat and drought vary between conifers with differing hydraulic strategies: Semiarid conifers responses to drought and heat
journal, June 2018

  • Manrique-Alba, Àngela; Sevanto, Sanna; Adams, Henry D.
  • Plant, Cell & Environment, Vol. 41, Issue 8
  • DOI: 10.1111/pce.13340

Reductions in tree performance during hotter droughts are mitigated by shifts in nitrogen cycling: Mitigation of hotter droughts
journal, August 2018

  • Grossiord, Charlotte; Gessler, Arthur; Reed, Sasha C.
  • Plant, Cell & Environment, Vol. 41, Issue 11
  • DOI: 10.1111/pce.13389

Growth and physiological responses to successional water deficit and recovery in four warm‐temperate woody species
journal, January 2019

  • Li, Qiang; Wang, Ning; Liu, Xiao
  • Physiologia Plantarum, Vol. 167, Issue 4
  • DOI: 10.1111/ppl.12922

Are Northeastern U.S. forests vulnerable to extreme drought?
journal, September 2017

  • Coble, Adam P.; Vadeboncoeur, Matthew A.; Berry, Z. Carter
  • Ecological Processes, Vol. 6, Issue 1
  • DOI: 10.1186/s13717-017-0100-x

Interannual variations in needle and sapwood traits of Pinus edulis branches under an experimental drought
text, January 2018