iForest - Biogeosciences and Forestry


Tree aging does not affect the ranking for water use efficiency recorded from δ13C in three Populus deltoides × P. nigra genotypes

Fahad Rasheed (1-2)   , Erwin Dreyer (1-3), Didier Le Thiec (1-3), Zikria Zafar (2), Sylvain Delagrange (4)

iForest - Biogeosciences and Forestry, Volume 12, Issue 3, Pages 272-278 (2019)
doi: https://doi.org/10.3832/ifor2896-012
Published: May 21, 2019 - Copyright © 2019 SISEF

Research Articles

A large variability of water use efficiency (assessed from the carbon isotopic discrimination in leaves and leaf soluble sugars) has been detected among poplar genotypes. Checking whether such differences detected in young trees (1-2 years old) remain stable with tree age is a prerequisite to use this trait with confidence for breeding purposes. In this study, a synchronic approach was used to test the age-related stability of the genotypic ranking of carbon isotopic discrimination in wood (Δ13C) until tree maturity. We sampled 376 trees between 4 and 20 years from three Populus deltoides × P. nigra genotypes growing in 41 common-garden trials across France. Carbon and nitrogen percentages along with δ13C was measured in the bulk wood of the year 2009 and used to compute the Δ13C. Basal area increment between 2008 and 2009 was also measured. Results showed that Δ13C increased (i.e., water use efficiency decreased) between ages 4 to 6 and remained stable later on. Significant differences among genotypes were found but the ranking among genotypes remained stable with age during the assessed life span. Furthermore, basal area increment and Δ13C were positively correlated interannually. This large-scale survey shows that despite crossing over in the temporal trend, water use efficiency remained stable with age across 3 poplar genotypes. However, further studies with a large number of genotypes are required to confirm whether this trait can be used to maintain or even improve productivity of poplar plantations, while lowering water consumption.


Water Use Efficiency, Age, Wood, Tree Ring, Populus × euramericana, Basal Area Increment, Synchronic Approach

Authors’ address

Fahad Rasheed
Erwin Dreyer 0000-0003-4999-5072
Didier Le Thiec 0000-0002-4204-551X
INRA, UMR1137 Ecologie et Ecophysiologie Forestières, IFR 110 EFABA, F-54280 Champenoux (France)
Fahad Rasheed
Zikria Zafar 0000-0001-8881-7653
Department of Forestry & Range Management, University of Agriculture Faisalabad, P.O. Box 38000 (Pakistan)
Erwin Dreyer 0000-0003-4999-5072
Didier Le Thiec 0000-0002-4204-551X
Université de Lorraine, UMR1137 Ecologie et Ecophysiologie Forestières, IFR 110 EFABA, F-54500 Vandoeuvre-lès-Nancy (France)
Sylvain Delagrange 0000-0001-8669-4282
Department of Natural Sciences, Institute of Temperate Forest Sciences (ISFORT), University of Quebec in Outaouais (UQO), 58 Main St, Ripon, Quebec J0V 1V0 (Canada)

Corresponding author

Fahad Rasheed


Rasheed F, Dreyer E, Le Thiec D, Zafar Z, Delagrange S (2019). Tree aging does not affect the ranking for water use efficiency recorded from δ13C in three Populus deltoides × P. nigra genotypes. iForest 12: 272-278. - doi: 10.3832/ifor2896-012

Academic Editor

Rossella Guerrieri

Paper history

Received: Jun 15, 2018
Accepted: Mar 18, 2019

First online: May 21, 2019
Publication Date: Jun 30, 2019
Publication Time: 2.13 months

Breakdown by View Type

(Waiting for server response...)

Article Usage

Total Article Views: 40072
(from publication date up to now)

Breakdown by View Type
HTML Page Views: 31856
Abstract Page Views: 2170
PDF Downloads: 5556
Citation/Reference Downloads: 3
XML Downloads: 487

Web Metrics
Days since publication: 1825
Overall contacts: 40072
Avg. contacts per week: 153.70

Article Citations

Article citations are based on data periodically collected from the Clarivate Web of Science web site
(last update: Feb 2023)

Total number of cites (since 2019): 1
Average cites per year: 0.20


Publication Metrics

by Dimensions ©

Articles citing this article

List of the papers citing this article based on CrossRef Cited-by.

Bert D, Leavitt SW, Dupouey JL (1997)
Variation of wood δ13C and water use efficiency of Abies alba during the last century. Ecology 78: 588-1596.
CrossRef | Gscholar
Billings SA, Boone AS, Stephen FM (2016)
Tree-ring δ13C and δ18O, leaf δ13C and wood and leaf N status demonstrate tree growth strategies and predict susceptibility to disturbance. Tree Physiology 36: 576-588.
CrossRef | Gscholar
Bonhomme L, Barbaroux C, Monclus R, Morabito D, Berthelot A, Villar M, Dreyer E, Brignolas F (2008)
Genetic variation in productivity, leaf traits and carbon isotope discrimination in hybrid poplars cultivated on contrasting sites. Annals of Forest Science 65: 503.
CrossRef | Gscholar
Brendel O, Le Thiec D, Scotti-Saintagne C, Bodénès C, Kremer A, Guehl J (2008)
Quantitative trait loci controlling water use efficiency and related traits in Quercus robur L. Tree Genetic and Genomes 4: 263-278.
CrossRef | Gscholar
Brendel O, Pot D, Plomion C, Rozenberg P, Guehl J (2002)
Genetic parameters and QTL analysis of δ13C and ring width in maritime pine. Plant, Cell and Environment 25: 945-953.
CrossRef | Gscholar
Brienen RJW, Gloor E, Clerici S, Newton R, Arppe L, Boom A, Bottrell S, Callaghan M, Heaton T, Helama S, Helle G, Leng MJ, Mielikäinen K, Oinonen M, Timonen M (2017)
Tree height strongly affects estimates of water-use efficiency responses to climate and CO2 using isotopes. Nature Communications 8: 288.
CrossRef | Gscholar
Cernusak LA, Winter K, Aranda J, Turner BL (2008)
Conifers. Angiosperm trees and lianas growth whole plant water and nitrogen use efficiency and stable isotope composition (δ13C and δ18O) of seedlings grown in a tropical environment. Plant Physiology 148: 642-659.
CrossRef | Gscholar
Ceulemans R, Impens I, Imler R (1987)
Stomatal conductance and stomatal behaviour in Populus clones and hybrids. Canadian Journal of Botany 66: 1404-1414.
CrossRef | Gscholar
Condon AG, Richards RA, Rebetzke GJ, Farquhar GD (2004)
Breeding for high water-use efficiency. Journal of Experimental Botany 55: 2447-2460.
CrossRef | Gscholar
Dillen S, Marron N, Koch B, Ceulemans R (2008)
Genetic variation of stomatal traits and carbon isotope discrimination in two hybrid poplar families (Populus deltoides “S9-2” × P. nigra “Ghoy” and P. deltoides “S9-2” × P. trichocarpa “V24”). Annals of Botany 102: 399-407.
CrossRef | Gscholar
Dupouey JL, Leavitt S, Choisnel E, Jourdain S (1993)
Modeling carbon isotope fractionation in tree rings based on effective evapotranspiration and soil water status. Plant, Cell and Environment 16: 939-947.
CrossRef | Gscholar
Duquesnay A, Bréda N, Stievenard M, Dupouey JL (1998)
Changes of tree-ring δ13C and water use efficiency of beech (Fagus sylvatica L.) in north-eastern France during the past century. Plant Cell and Environment 21: 565-572.
CrossRef | Gscholar
Ehleringer JR, Hall AE, Farquhar GD (1993)
Water use in relation to productivity. In: “Stable Isotopes and Plant Carbon-Water Relations” (Ehleringer JR, Hall AE, Farquhar GD eds). Academic Press, New York, USA, pp. 3-8.
Farquhar G, Richards R (1984)
Isotopic composition of plant carbon correlates with water use efficiency of wheat genotypes. Australian Journal of Plant Physiology 11: 539-552.
CrossRef | Gscholar
Farquhar G, Ehleringer J, Hubick K (1989)
Carbon isotope discrimination and photosynthesis. Annual Review of Plant Physiology and Plant Molecular Biology 40: 503-537.
CrossRef | Gscholar
Francey RJ, Farquhar GD (1982)
An explanation of 13C/12C variations in tree rings. Nature 297: 28-31.
CrossRef | Gscholar
Guerrieri R, Mencuccini M, Sheppard LJ, Saurer M, Perks MP, Levy P, Sutton MA, Borghetti M, Grace J (2011)
The legacy of enhanced N and S deposition as revealed by the combined analysis of δ13C, δ18O and δ15N in tree rings. Global Change Biology 17: 1946-1962.
CrossRef | Gscholar
Guy RD, Holowachuk DL (2001)
Population differences in stable carbon isotope ratio of Pinus contorta Dougl. ex Loud.: relationship to environment, climate of origin, and growth potential. Canadian Journal of Botany 79: 274-283.
CrossRef | Gscholar
Hothorn T, Bretz F, Westfall P (2008)
Simultaneous inference in general parametric models. Biometrical journal 50: 346-363.
CrossRef | Gscholar
IPCC (2013)
Climate change 2013: the physical science basis. In “Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change” (Stocker TF, Qin D, Plattner G-K, Tignor M, Allen SK, Boschung J, Nauels A, Xia Y, Bex V, Midgley PM eds). Cambridge University Press, Cambridge, United Kingdom and New York, NY, USA, pp. 1535.
Johnsen KH, Flanagan LB, Huber DA, Major JE (1999)
Genetic variation in growth carbon isotope discrimination and foliar N concentration in Picea mariana: analyses from a half diallel mating design using field grown trees. Canadian Journal of Forestry Research 29: 1727-1735.
CrossRef | Gscholar
Lauteri M, Scartazza A, Guido MC, Brugnoli E (1997)
Genetic variation in photosynthetic capacity, carbon isotope discrimination and mesophyll conductance in provenances of Castanea sativa adapted to different environments. Functional Ecology 11: 675-683.
CrossRef | Gscholar
Leavitt SW (2010)
Tree-ring C-H-O isotope variability and sampling. Science of Total Environment 408: 5244-5253.
CrossRef | Gscholar
Loader NJ, Roberston I, McCarroll D (2003)
Comparison of stable carbon isotope ratios in the whole wood, cellulose and lignin of oak tree-rings. Palaeogeography, Palaeoclimatology, Palaeoecology 196: 395-407.
CrossRef | Gscholar
Lamlom SH, Savidge RA (2003)
A reassessment of carbon contents in wood: variation within and between 41 North American species. Biomass and Bioenergy 25: 381-388.
CrossRef | Gscholar
Marron N, Villar M, Dreyer E, Delay D, Boudouresque E, Petit J-M, Delmotte FM, Guehl JM, Brignolas F (2005)
Diversity of leaf traits related to productivity in 31 Populus deltoides × Populus nigra clones. Tree Physiology 25: 425-435.
CrossRef | Gscholar
McCarroll D, Loader NJ (2004)
Stable isotopes in tree rings. Quaternary Science Reviews 23: 771-801.
CrossRef | Gscholar
McCarroll D, Pawellek F (2001)
Stable carbon isotope ratios of Pinus sylvestris from northern Finland and the potential for extracting a climate signal from long Fennoscandian chronologies. The Holocene 11: 517-526.
CrossRef | Gscholar
Monclus R, Dreyer E, Delmotte FM, Villar M, Delay D, Boudouresque E, Petit JM, Marron N, Bréchet N, Brignolas F (2005)
Productivity leaf traits and carbon isotope discrimination in 29 Populus deltoides × P. nigra clones. New Phytologist 167: 53-62.
CrossRef | Gscholar
Monclus R, Dreyer E, Villar M, Delmotte FM, Delay D, Petit JM, Barbaroux C, Le Thiec D, Bréchet C, Brignolas F (2006)
Impact of drought on productivity and water- use efficiency in 29 genotypes of Populus deltoides × Populus nigra. New Phytologist 169: 765-777.
CrossRef | Gscholar
Monserud RA, Marshall JD (2001)
Time-series analysis of δ13C from tree rings time trends and autocorrelation. Tree Physiology 21: 1087-1102.
CrossRef | Gscholar
Nguyen-Queyrens A, Ferhi A, Loustau D, Guehl JM (1998)
Within-ring δ13C spatial variability and interannual variations in wood cellulose of two contrasting provenances of Pinus pinaster. Canadian Journal of Forestry Research 28: 766-773.
CrossRef | Gscholar
Osorio J, Pereira JS (1994)
Genotypic differences in water use efficiency and 13C discrimination in Eucalyptus globulus. Tree Physiology 14: 871-882.
CrossRef | Gscholar
Penuelas J, Hunt JM, Ogaya R, Jump A (2008)
Twentieth century changes of tree-ring δ13C at the southern range-edge of Fagus sylvatica: increasing water-use efficiency does not avoid the growth decline induced by warming at low altitudes. Global Change Biology 14: 1076-1088.
CrossRef | Gscholar
Pinheiro J, Bates B, DebRoy S, Sarkar D, the R Development Core Team (2012)
nlme: Linear and nonlinear mixed effects models. R package version 3.1-103.
Online | Gscholar
Pita P, Soria F, Canas I, Toval G, Pardos JA (2001)
Carbon isotope discrimination and its relationship to drought under field conditions in genotypes of Eucalyptus globulus Labill. Forest Ecology and Management 141: 211-221.
CrossRef | Gscholar
R Core Team (2012)
R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.
Online | Gscholar
Rasheed F, Richard B, Le Thiec D, Montpied P, Paillassa E, Brignolas F, Dreyer E (2011)
Time course of δ13C in poplar wood: genotype ranking remains stable over the life cycle in plantations despite some differences between cellulose and bulk wood. Tree Physiology 31: 1183-1193.
CrossRef | Gscholar
Rasheed F, Dreyer E, Richard B, Brignolas F, Montpied P, Le Thiec D (2013)
Genotype differences in 13C discrimination between atmosphere and leaf matter match differences in transpiration efficiency at leaf and whole-plant level in hybrid Populus deltoides × nigra. Plant, Cell and Environment 36: 87-102.
CrossRef | Gscholar
Rasheed F, Dreyer E, Richard B, Brignolas F, Brendel O, Le Thiec D (2015)
Vapour pressure deficit during growth has little impact on genotypic differences of transpiration efficiency at leaf and whole-plant level: an example from Populus nigra L. Plant, Cell Environment 38: 670-684.
CrossRef | Gscholar
Richards RA, Rebetzke GJ, Watt M, Condon AG, Spielmeyer W, Dolferus R (2010)
Breeding for improved water productivity in temperate cereals: phenotyping, quantitative trait loci, markers and the selection environment. Functional Plant Biology 37: 85-97.
CrossRef | Gscholar
Richards RA, Rebetzke GJ, Watt M, Condon AG, Rasheed F, Dreyer E, Richard B, Brignolas F, Brendel O, Le Thiec D (2015)
Vapour pressure deficit during growth has little impact on genotypic differences of transpiration efficiency at leaf and whole-plant level: an example from Populus nigra L. Plant, Cell Environment 38: 670-684.
CrossRef | Gscholar
Ripullone F, Lauteri M, Grassi G, Amato M, Borghetti M (2004)
Variation in nitrogen supply changes water-use efficiency of Pseudotsuga menziesii and Populus × euramericana; a comparison of three approaches to determine water-use efficiency. Tree Physiology 24: 671-679.
CrossRef | Gscholar
Rowell DM, Ades PK, Tausz M, Arndt SK, Adams MA (2008)
Lack of genetic variation in tree ring δ13C suggests a uniform stomatally-driven response to drought stress across Pinus radiata genotypes. Tree Physiology 29: 191-198.
CrossRef | Gscholar
Schleser GH, Jayasekera R (1985)
δ13C variations in leaves of a forest as an indication of reassimilated CO2 from the soil. Oecologia 65: 536-542.
CrossRef | Gscholar
Vadez V, Kholova J, Medina S, Kakkera A, Anderberg H (2014)
Transpiration efficiency: new insights into an old story. Journal of Experimental Botany 65: 6141-53.
CrossRef | Gscholar
Wilson AT, Grinsted MJ (1977)
12C/13C in cellulose and lignin as palaeothermometers. Nature 265: 133-135.
CrossRef | Gscholar
Xu ZH, Saffigna PG, Farquhar GD, Simpson JA, Haines RJ, Walker S, Osborne DO, Guinto D (2000)
Carbon isotope discrimination and oxygen isotope composition in clones of the F1 hybrid between slash pine and Caribbean pine in relation to tree growth water use efficiency and foliar nutrient concentration. Tree Physiology 20: 1209-1217.
CrossRef | Gscholar
Zhang JW, Fins L, Marshall JD (1994)
Stable carbon isotope discrimination photosynthetic gas exchange and growth differences among western larch families. Tree Physiology 14: 531-539.
CrossRef | Gscholar

This website uses cookies to ensure you get the best experience on our website. More info