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North America’s oldest boreal trees are more efficient water users due to increased [CO2], but do not grow faster
Edited by Donald R. Ort, University of Illinois, Urbana, IL, and approved December 20, 2018 (received for review September 27, 2018)

Significance
The metabolism of North America’s oldest boreal trees (Thuja occidentalis L.) is strongly affected by rising anthropogenic
Abstract
Due to anthropogenic emissions and changes in land use, trees are now exposed to atmospheric levels of [
Plants are an integral component of both water and carbon cycles on Earth. This is because stomata (i.e., microscopic apertures on plant leaves) allow plants to adjust their metabolism to changing environmental conditions by controlling the tradeoff between
One of the most striking consequences of elevated
Evolution of
Moreover, it is still unclear how these shifts in stomatal behavior impact forest productivity, i.e., whether changes in the rate of increase in
To remedy this uncertainty, we report on the acclimation of a population of long-lived white cedars (Thuja occidentalis L.) growing in xeric conditions that offers a unique, long-term perspective on
Results and Discussion
Acclimation to Rising c a .
Our results indicate a remarkable and unprecedented (59%)
Tree-ring
The observed rate of
A shift in the acclimation strategy to rising
Ultimately, our study provides in situ evidence of a shift in stomatal behavior: Old-growth white cedars maximized carbon gains at low
Contributions of c a and Climate to i W U E Variability.
Commonality analysis revealed that both
(A and B) Commonality analysis showing beta weights (A) and the proportion of variance (B) in
While most of the variance in
The unprecedented increase in
As trees have been acclimating to rising
No Unprecedented Growth Despite Increasing i W U E .
Given the significant increase in
Several studies have reported
Four mechanisms can explain the lack of growth stimulation in a context of increasing
Our study has important implications for the modeling of vegetation response to atmospheric variability. Most ecophysiological and dynamic global vegetation models (DGVMs) predict an increase in plant biomass due to a stimulation of photosynthesis by
Conclusions
North America’s oldest boreal trees (T. occidentalis L.) exhibited an unprecedented 59% increase in
SI Appendix.
SI Appendix provides complementary information on methods and results: the regional curve used for regional curve standardization (RCS), quality statistics for the RCS chronology, cohorts selected for
Materials and Methods
Study Site and Sampling Strategy.
Lake Duparquet is located at the southern limit of the boreal forest (48,
Stable Isotope Chronologies.
Eleven trees were selected for carbon and oxygen stable isotope ratio analysis to cover the maximum time period with the smallest number of possible cohort changes (SI Appendix, Fig. S4). This avoids loss of a reliable mean as we go back in time, considering the systematic offsets typically encountered in the stable isotope analyses of different trees (25, 48, 49). Isotope chronologies have been shown to require few replicates (as little as four) to obtain a strong common signal (expressed population signal ≥0.85) (25). Two cohorts of six (cohort 1: 1620–2014) and five trees (cohort 2: 1295–1645) were selected, with an overlap of 25 y (SI Appendix, Fig. S4). The trees selected for stable isotope analysis had different ages that were well spread through time. This avoids incorporating noise due to nonclimatic age effects (SI Appendix, Fig. S4). The first 50 y of each sample were excluded to avoid any nonclimatic age-related trends (49, 50) (SI Appendix).
δ 13 C -Derived Physiological Parameters.
Records of
Based on plant physiology theory and models, physiological parameters can be derived from tree-ring
For each of the three theoretical scenarios of leaf–gas strategy (7), the
Dendroclimatic Analyses.
Daily weather data (1901–2014 maximum and minimum temperatures) and precipitation (1901–2014 sum) and VPD (1953–2014) were retrieved from BioSIM v.10, which interpolates site-specific estimates from historical weather observations (56) as described in ref. 57. The quantity of available soil moisture was estimated for each month using the quadratic + linear (QL) formulation procedure described in ref. 58, which accounts for water loss through evapotranspiration (simplified Penman–Monteith potential evapotranspiration) and gain from precipitation. Parameter values for maximum and critical available soil water were set at 300 mm and 400 mm, respectively; the number of weather stations for interpolation was set to eight. We used values of annual mean
Commonality analysis (61) was used to explore the climate effects of
Acknowledgments
We acknowledge the contribution of many people who helped with field and laboratory work: A. Barbe, G. Proulx, P. Leclerc, M. Gratton, and A. Adamowicz-Walczak. We thank the Natural Sciences and Engineering Research Council (NSERC) and Her Majesty The Queen in due right of Canada. C.G.-C. acknowledges financial support from both NSERC and Fonds de Recherche Québécois Nature et Technologies for her master’s thesis.
Footnotes
↵1C.G.-C. and É.B. contributed equally to this work.
- ↵2To whom correspondence should be addressed. Email: boucher.etienne{at}uqam.ca.
Author contributions: C.G.-C., É.B., Y.B., I.D., and M.G. designed research; C.G.-C., É.B., and M.P.G. performed research; C.G.-C., É.B., M.P.G., and J.-F.H. contributed new reagents/analytic tools; C.G.-C., É.B., Y.B., M.P.G., I.D., L.C.R.S., and J.-F.H. analyzed data; C.G.-C., É.B., Y.B., M.P.G., I.D., L.C.R.S., and J.-F.H. wrote the paper; and É.B. provided funding.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission.
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1816686116/-/DCSupplemental.
- Copyright © 2019 the Author(s). Published by PNAS.
This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND).
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