Hydraulic theory predicts stomatal responses to climatic water deficits

Pragmatic hydraulic theory predicts stomatal responses to climatic water deficits

by Sperry J. S., Wang Y., Wolfe B. T., Mackay D. S., Anderegg W. R. L., McDowell N. G., Pockman W. T. (2016)

John Sperry, Yujie Wang, Brett Wolfe, D. Scott Mackay, William R L Anderegg, Nate McDowell, William Pockman,

Sperry JS1Wang Y2Wolfe BT3Mackay DS4Anderegg WR2McDowell NG5Pockman WT6.

1 Department of Biology, University of Utah, Salt Lake City, UT, 84112, USA.

2 Department of Biology, University of Utah, Salt Lake City, UT, 84112, USA.

3 Smithsonian Tropical Research Institute, PO Box 0843-03092, Balboa, Panama.

4 Department of Geography, State University of New York, Buffalo, NY, 14260, USA.

5 Earth and Environmental Sciences Division, Los Alamos National Lab, Los Alamos, NM, 87545, USA.

6 Biology Department, University of New Mexico, Albuquerque, NM, 87131, USA.

===

In New Phytol. 212: 577–589 – DOI: 10.1111/nph.14059

https://www.ncbi.nlm.nih.gov/pubmed/27329266

Abstract

Ecosystem models have difficulty predicting plant drought responses, partially from uncertainty in the stomatal response to water deficits in soil and atmosphere.

We evaluate a ‘supply-demand’ theory for water-limited stomatal behavior that avoids the typical scaffold of empirical response functions. The premise is that canopy water demand is regulated in proportion to threat to supply posed by xylem cavitation and soil drying.

The theory was implemented in a trait-based soil-plant-atmosphere model. The model predicted canopy transpiration (E), canopy diffusive conductance (G), and canopy xylem pressure (Pcanopy ) from soil water potential (Psoil ) and vapor pressure deficit (D). Modeled responses to D and Psoil were consistent with empirical response functions, but controlling parameters were hydraulic traits rather than coefficients.

Maximum hydraulic and diffusive conductances and vulnerability to loss in hydraulic conductance dictated stomatal sensitivity and hence the iso- to anisohydric spectrum of regulation. The model matched wide fluctuations in G and Pcanopy across nine data sets from seasonally dry tropical forest and piñon-juniper woodland with < 26% mean error.

Promising initial performance suggests the theory could be useful in improving ecosystem models. Better understanding of the variation in hydraulic properties along the root-stem-leaf continuum will simplify parameterization

Advertisements

Plant water potential improves prediction of empirical stomatal models

Plant water potential improves prediction of empirical stomatal models

by Anderegg W. R. L., Wolf A., Arango-Velez A., Choat B., Chmura D. J., Jansen S., Kolb T., Li S., Meinzer F., Pita P., Resco de Dios V., Sperry J. S., Wolfe B. T., Pacala S. W. (2017)

===

In PLOS one 12(10): e0185481 – https://doi.org/10.1371/journal.pone.0185481

https://journals.plos.org/plosone/article?id=10.1371/journal.pone.0185481

Abstract

Climate change is expected to lead to increases in drought frequency and severity, with deleterious effects on many ecosystems.

Stomatal responses to changing environmental conditions form the backbone of all ecosystem models, but are based on empirical relationships and are not well-tested during drought conditions.

Here, we use a dataset of 34 woody plant species spanning global forest biomes to examine the effect of leaf water potential on stomatal conductance and test the predictive accuracy of three major stomatal models and a recently proposed model.

We find that current leaf-level empirical models have consistent biases of over-prediction of stomatal conductance during dry conditions, particularly at low soil water potentials. Furthermore, the recently proposed stomatal conductance model yields increases in predictive capability compared to current models, and with particular improvement during drought conditions.

Our results reveal that including stomatal sensitivity to declining water potential and consequent impairment of plant water transport will improve predictions during drought conditions and show that many biomes contain a diversity of plant stomatal strategies that range from risky to conservative stomatal regulation during water stress.

Such improvements in stomatal simulation are greatly needed to help unravel and predict the response of ecosystems to future climate extremes.

Seasonal and diurnal variation of stomatal behavior

Seasonal estimates of the stomatal cost function slope parameter in the wet (blue) and dry (red) periods for Juniperus monosperma (JUMO; N=576), Pinus edulis(PIED; N=511), Quercus douglasii (QUDO; N=166), Alphitonia excelsa (ALEX; N=173) and Brachychiton australis (BRAU; N=100). Black line is the median; boxes the interquartile range, and error bars show the highest and lowest value of the data excluding outliers. Stars indicate statistical significance (i.e. 95% confidence intervals do not overlap)

Quantifying seasonal and diurnal variation of stomatal behavior in a hydraulic-based stomatal optimization model

by Anderegg W. R. L. (2018)

William R. L. Anderegg,

In Joiurn. Pla nt HydraulicsDOI: 10.20870/jph.2018.e001 –

https://www.researchgate.net/publication/330653531_Quantifying_seasonal_and_diurnal_variation_of_stomatal_behavior_in_a_hydraulic-based_stomatal_optimization_model

Abstract

Plant responses to drought occur across many time-scales, with stomatal closure typically considered to be a critical short-term response.

Recent theories of optimal stomatal conductance linked to plant hydraulic transport have shown promise, but it is not known if stomata update their hydraulic “shadow price” of water use (marginal increase in carbon cost with a marginal drop in water potential) over days, seasons, or in response to recent drought.

Here, I estimate the hydraulic shadow price in five species – two semi-arid gymnosperms, one temperate and two tropical angiosperms – at daily timescales and in wet and dry periods.

I tested whether the shadow prices varies predictably as a function of current and/or lagged drought conditions. Diurnal estimates of the hydraulic shadow price estimated from observed stomatal conductance, while variable, did not vary predictably with environmental variables.

Seasonal variation in shadow price was observed in the gymnosperm species, but not the angiosperm species, and did not meaningfully influence prediction accuracy of stomatal conductance.

The lack of systematic variation in shadow price and high predictive ability of stomatal conductance when using a single set of parameters further emphasizes the potential of hydraulic-based stomatal optimization theories.

Optimal control of stomata to manage hydraulic risk is likely to have significant consequences for ecosystem fluxes during drought

Woody plants optimise stomatal behaviour relative to hydraulic risk

Anderegg W. R. L., Wolf A., Arango-Velez A., Choat B., Chmura D. J., Jansen S., Kolb T., Li S., Meinzer F., Pita P., Resco de Dios V., Sperry J. S., Wolfe B. T., Pacala S. W. (2018)

William R. L. Anderegg,1
Adam Wolf,2
Adriana Arango-Velez,3
Brendan Choat,4
Daniel J. Chmura,5

Steven Jansen,6
Thomas Kolb,7

Shan Li,6,8
Frederick C. Meinzer,9

Pilar Pita,10
Vıctor Resco de Dios,11
John S. Sperry,1

Brett T. Wolfe,12
Stephen Pacala,13

1 Department of Biology, University of Utah, Salt Lake City, UT 84112, USA
2 Arable Labs, Princeton, NJ 08544, USA
3 Connecticut Agricultural Experiment Station, New Haven, CT 06504, USA
4 Hawkesbury Institute for the Environment, Western Sydney University,
Penrith, 2751, NSW, Australia
5 Institute of Dendrology, Polish Academy of Sciences, ul. Parkowa 5, 62-035,
Kornik, Poland
6 Institute of Systematic Botany and Ecology, Ulm University, Albert-EinsteinAllee 11, 89081 Ulm, Germany
7 School of Forestry, Northern Arizona University, Flagstaff, AZ 86011,
USA
8 Department of Wood Anatomy and Utilization, Research Institute of Wood
Industry, Chinese Academy of Forestry, Beijing 100091, China
9 USDA Forest Service, Pacific Northwest Research Station, Corvallis, OR 97331, USA
10 Technical University of Madrid, Madrid, Spain
11 Department of Crop and Forest Sciences and Agrotecnio Center, Universitat
de Lleida, Lleida 25198, Spain
12 Smithsonian Tropical Research Institute, Balboa, Panama
13 Department of Ecology and Evolutionary Biology, Princeton University,
Princeton, NJ 08544, USA

===

In Ecology Letters 21: 968-977 – doi: 10.1111/ele.12962 –

http://sperry.biology.utah.edu/publications/Anderegg_et_al_2018.pdf

Abstract

Stomatal response to environmental conditions forms the backbone of all ecosystem and carbon cycle models, but is largely based on empirical relationships.

Evolutionary theories of stomatal behaviour are critical for guarding against prediction errors of empirical models under future climates. Longstanding theory holds that stomata maximise fitness by acting to maintain constant marginal water use efficiency over a given time horizon, but a recent evolutionary theory proposes that stomata instead maximise carbon gain minus carbon costs/risk of hydraulic damage.

Using data from 34 species that span global forest biomes, we find that the recent carbon-maximisation optimisation theory is widely supported, revealing that the evolution of stomatal regulation has not been primarily driven by attainment of constant marginal water use efficiency.

Optimal control of stomata to manage hydraulic risk is likely to have significant consequences for ecosystem fluxes during drought, which is critical given projected intensification of the global hydrological ,cycle.

A stomatal control model

 

 

A stomatal control model based on optimization of carbon gain versus hydraulic risk predicts aspen sapling responses to drought

by Venturas M. D., Sperry J. S., Love D.M., Frehner E. H., Allred M. G., Wang Y. Anderegg W. R. L. ( 2018)

 

====

in New Phytol. – Online Version of Record  –

https://nph.onlinelibrary.wiley.com/doi/abs/10.1111/nph.15333?af=R

Summary

  • Empirical models of plant drought responses rely on parameters that are difficult to specify a priori. We test a trait‐ and process‐based model to predict environmental responses from an optimization of carbon gain vs hydraulic risk.
  • We applied four drought treatments to aspen (Populus tremuloides) saplings in a research garden. First we tested the optimization algorithm by using predawn xylem pressure as an input. We then tested the full model which calculates root‐zone water budget and xylem pressure hourly throughout the growing season.
  • The optimization algorithm performed well when run from measured predawn pressures. The per cent mean absolute error (MAE) averaged 27.7% for midday xylem pressure, transpiration, net assimilation, leaf temperature, sapflow, diffusive conductance and soil‐canopy hydraulic conductance. Average MAE was 31.2% for the same observations when the full model was run from irrigation and rain data. Saplings that died were projected to exceed 85% loss in soil‐canopy hydraulic conductance, whereas surviving plants never reached this threshold.
  • The model fit was equivalent to that of an empirical model, but with the advantage that all inputs are specific traits. Prediction is empowered because knowing these traits allows knowing the response to climatic stress.

Optimal stomatal behavior

 

Optimal stomatal behavior with competition for water and risk of hydraulic impairment

by Wolf A., Anderegg W. R. L.Pacala S. W. (2016) 

aaeaaqaaaaaaaagyaaaajdeyotm4mdmzlwuymtktngy3ny04yzqwltuym2rhzdrmyta4nq
Adam Wolf, Arable Labs, Inc., Princeton, NJ

image
William R. L. Anderegg, University of Utah, Salt Lake City, UT

et92lek1yg75t6z6gfb7aeeqcn7numq
Stephen W. Pacala, Princeton University, Princeton, NJ

PNAS October 31, 2016 – 

http://www.pnas.org/content/early/2016/10/27/1615144113.short

Significance

Plants lose water and take up carbon through stomata, whose behavior has major influences on global carbon and water fluxes. Yet both competition for water and the potential fitness costs of hydraulic damage during water stress could alter how stomata behave. Here, we add variable xylem conductivity to water and carbon costs of low-xylem water potentials to the classic stomatal optimization and a pure carbon-maximization optimization. We show that both optimizations can reproduce known stomatal responses to environmental conditions but that the pure carbon-maximization optimization is also consistent with competition for water. We describe a new measure—the marginal xylem tension efficiency—that can be used to test stomatal optimizations.

Abstract

For over 40 y the dominant theory of stomatal behavior has been that plants should open stomates until the carbon gained by an infinitesimal additional opening balances the additional water lost times a water price that is constant at least over short periods. This theory has persisted because of its remarkable success in explaining strongly supported simple empirical models of stomatal conductance, even though we have also known for over 40 y that the theory is not consistent with competition among plants for water.

We develop an alternative theory in which plants maximize carbon gain without pricing water loss and also add two features to both this and the classical theory, which are strongly supported by empirical evidence:

(i) water flow through xylem that is progressively impaired as xylem water potential drops and

(ii) fitness or carbon costs associated with low water potentials caused by a variety of mechanisms, including xylem damage repair.

We show that our alternative carbon-maximization optimization is consistent with plant competition because it yields an evolutionary stable strategy (ESS)—species with the ESS stomatal behavior that will outcompete all others.

We further show that, like the classical theory, the alternative theory also explains the functional forms of empirical stomatal models.

We derive ways to test between the alternative optimization criteria by introducing a metric—the marginal xylem tension efficiency, which quantifies the amount of photosynthesis a plant will forego from opening stomatal an infinitesimal amount more to avoid a drop in water potential.

A ‘supply-demand’ theory for water-limited stomatal behavior

 

Pragmatic hydraulic theory predicts stomatal responses to climatic water deficits

Sperry J. S., Wang Y., Wolfe B. T., Mackay D. S., Anderegg W. R. L., McDowell N. G., Pockman W. T. (2016)

University of Utahjohn_sperry

University of Utah, Salt Lake City, yujie_wang9

University of Utah, Salt Lake City, brett_wolfe2

University Buffalo, State University New Yorkd_mackay

University of Utah, Salt Lake City, william_anderegg

Nate G. McDowell,

University of New Mexicowilliam_pockman

 

–  – New Phytologist 2016 – DOI: 10.1111/nph.14059 –

https://www.researchgate.net/publication/304330127_Pragmatic_hydraulic_theory_predicts_stomatal_responses_to_climatic_water_deficits

Abstract
Ecosystem models have difficulty predicting plant drought responses, partially from uncertainty in the stomatal response to water deficits in soil and atmosphere.
We evaluate a ‘supply-demand’ theory for water-limited stomatal behavior that avoids the typical scaffold of empirical response functions. The premise is that canopy water demand is regulated in proportion to threat to supply posed by xylem cavitation and soil drying.
The theory was implemented in a trait-based soil-plant-atmosphere model. The model predicted canopy transpiration (E), canopy diffusive conductance (G), and canopy xylem pressure (Pcanopy ) from soil water potential (Psoil ) and vapor pressure deficit (D).
Modeled responses to D and Psoil were consistent with empirical response functions, but controlling parameters were hydraulic traits rather than coefficients. Maximum hydraulic and diffusive conductances and vulnerability to loss in hydraulic conductance dictated stomatal sensitivity and hence the iso- to anisohydric spectrum of regulation.
The model matched wide fluctuations in G and Pcanopy across nine data sets from seasonally dry tropical forest and piñon-juniper woodland with < 26% mean error.
Promising initial performance suggests the theory could be useful in improving ecosystem models. Better understanding of the variation in hydraulic properties along the root-stem-leaf continuum will simplify parameterization.