Tree age-related effects on sun acclimated leaves in a chronosequence of beech (Fagus sylvatica) stands
Juliette Louis A , Hélène Genet B C , Sylvie Meyer A D F , Kamel Soudani A , Pierre Montpied B C , Arnaud Legout E , Erwin Dreyer B C , Zoran G. Cerovic A and Eric Dufrêne A
+ Author Affiliations
- Author Affiliations
A Laboratoire Ecologie Systématique et Evolution, CNRS, UMR 8079 (CNRS, UPS, AgroParisTech), Université Paris-Sud, Bât 362, F-91405 Orsay, France.
B INRA, UMR 1137, Ecologie et Ecophysiologie Forestières, F-54280 Champenoux, France.
C Université de Lorraine, UMR 1137, Ecologie et Ecophysiologie Forestières, F-54500 Vandoeuvre les Nancy, France.
D Univ Paris Diderot, Sorbonne Paris Cité, F-75475, Paris, France.
E INRA, UR 1138, Biogéochimie des Ecosystèmes Forestiers, F-54280 Champenoux, France.
F Corresponding author. Email: sylvie.meyer@u-psud.fr
Functional Plant Biology 39(4) 323-331 https://doi.org/10.1071/FP11248
Submitted: 1 November 2011 Accepted: 1 March 2012 Published: 30 March 2012
Abstract
The assessment of the effect of tree age on leaves is usually limited by the difficulty of sampling sun leaves from tall ageing trees. In this study, we investigated tree age-related effects on sun leaves in a chronosequence of beech (Fagus sylvatica L.) stands. The effects of stand age on leaf mass to area ratio (LMA), chlorophyll (Chl), epidermal polyphenols (EPhen), nitrogen and carbon contents in sun leaves were investigated in 17 even-aged stands distributed into six age classes (14–175 years old). Chl and EPhen were assessed in vivo with SPAD and Dualex portable leaf-clips respectively. Leaves were sampled by shooting and sun leaves were identified based on criteria obtained from a vertical profile of the ratio abaxial vs adaxial EPhen across the canopy. Sun leaves were characterised by a high and similar adaxial and abaxial EPhen contents, high LMA value and low mass-based Chl content. These sun leaf characteristics, together with leaf nitrogen and carbon contents, were not significantly affected by stand age. Along the chronosequence, beech trees invested a stable fraction of leaf mass into nitrogen, carbon, Chl and EPhen with decreasing leaf size, i.e. dry mass and area.
Additional keywords: chlorophyll, Dualex, light gradient, nitrogen, flavonoids, SPAD.
References
Abrams MD (1994) Genotypic and phenotypic variation as stress adaptations in temperate tree species: a review of several case studies. Tree Physiology 14, 833–842.Baize D, Girard MC (1998) ‘A sound reference base for soils: the Référentiel Pédologique.’ (INRA: Paris)
Barnes JD, Balaguer L, Manrique E, Elvira S, Davison AW (1992) A reappraisal of the use of DMSO for the extraction and determination of chlorophylls a and b in lichens and higher plants. Environmental and Experimental Botany 32, 85–100.
| A reappraisal of the use of DMSO for the extraction and determination of chlorophylls a and b in lichens and higher plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38Xkt1aktL0%3D&md5=15d97168e3dfa5d1eeaec82def99f1beCAS |
Bate-Smith EC (1962) The phenolic constituents of plants and their taxonomic significance. Journal of the Linnean Society – Botany 58, 95–173.
| The phenolic constituents of plants and their taxonomic significance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaF3sXkslKluro%3D&md5=5d63820779521bed2780d80e56e58f7fCAS |
Bidel LPR, Meyer S, Goulas Y, Cadot Y, Cerovic ZG (2007) Responses of epidermal phenolic compounds to light acclimation: in vivo qualitative and quantitative assessment using chlorophyll fluorescence excitation spectra in leaves of three woody species. Journal of Photochemistry and Photobiology. B, Biology 88, 163–179.
| Responses of epidermal phenolic compounds to light acclimation: in vivo qualitative and quantitative assessment using chlorophyll fluorescence excitation spectra in leaves of three woody species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtVCmt7vO&md5=276606dd53cb3bb2f5a974bc9c2a34f1CAS |
Bilger W, Veit M, Schreiber L, Schreiber U (1997) Measurement of leaf epidermal transmittance of UV radiation by chlorophyll fluorescence. Physiologia Plantarum 101, 754–763.
| Measurement of leaf epidermal transmittance of UV radiation by chlorophyll fluorescence.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXivFartg%3D%3D&md5=c00c09ec5dccd920d78fb712a5c6c6b3CAS |
Bond B (2000) Age-related changes in photosynthesis of woody plants. Trends in Plant Science 5, 349–353.
| Age-related changes in photosynthesis of woody plants.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3cvhtFCktA%3D%3D&md5=c9a1d1edf2af35b40398a8a8b783fe5dCAS |
Brown DE, Rashotte AM, Murphy AS, Normanly J, Tague BW, Peer WA, Taiz L, Muday GK (2001) Flavonoids act as negative regulators of auxin transport in vivo in Arabidopsis. Plant Physiology 126, 524–535.
| Flavonoids act as negative regulators of auxin transport in vivo in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXks1Gnu7s%3D&md5=ae85529f4e491252c5005df09a9c7b69CAS |
Caldwell MM, Robberecht R, Flint SD (1983) Internal filters: prospects for UV-acclimation in higher plants. Physiologia Plantarum 58, 445–450.
| Internal filters: prospects for UV-acclimation in higher plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3sXks1KktL4%3D&md5=6a83431a4f7e992695353310c5ae88d7CAS |
Cartelat A, Cerovic ZG, Goulas Y, Meyer S, Lelarge C, Prioul JL, Barbottin B, Jeuffroy MH, Gate P, Agati G, Moya I (2005) Optically assessed contents of leaf polyphenolics and chlorophyll as indicators of nitrogen deficiency in wheat (Triticum aestivum L.). Field Crops Research 91, 35–49.
| Optically assessed contents of leaf polyphenolics and chlorophyll as indicators of nitrogen deficiency in wheat (Triticum aestivum L.).Crossref | GoogleScholarGoogle Scholar |
Cerovic ZG, Ounis A, Cartelat A, Latouche G, Goulas Y, Meyer S, Moya I (2002) The use of chlorophyll fluorescence excitation spectra for the non-destructive in situ assessment of UV-absorbing compounds in leaves. Plant, Cell & Environment 25, 1663–1676.
| The use of chlorophyll fluorescence excitation spectra for the non-destructive in situ assessment of UV-absorbing compounds in leaves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXislCjtw%3D%3D&md5=aa3b21b9278f5b86a1516145e080ce42CAS |
Delzon S, Satore M, Burlett R, Dewar R, Loustau D (2004) Hydraulic response to height growth in maritime pine trees. Plant, Cell & Environment 27, 1077–1087.
| Hydraulic response to height growth in maritime pine trees.Crossref | GoogleScholarGoogle Scholar |
Drake JE, Raetz LM, Davis SC, DeLucia EH (2010) Hydraulic limitation not declining nitrogen availability causes the age-related photosynthesis decline in loblolly pine (Pinus taeda L.). Plant, Cell & Environment 33, 1756–1766.
| Hydraulic limitation not declining nitrogen availability causes the age-related photosynthesis decline in loblolly pine (Pinus taeda L.).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtlemsbfP&md5=de245cc16bd669f98ed8e09ecd8fce98CAS |
Evans JR (1989) Photosynthesis and nitrogen relationships in leaves of C3 plants. Oecologia 78, 9–19.
| Photosynthesis and nitrogen relationships in leaves of C3 plants.Crossref | GoogleScholarGoogle Scholar |
Genet H (2009) Ageing and site fertility impacts on carbon allocation to growth, carbohydrates storage and reproduction in oak and beech. PhD thesis, University Paris-Sud, Orsay, France.
Genet H, Breda N, Dufrêne E (2010) Age-related variation in carbon allocation at tree and stand scales in beech (Fagus sylvatica L.) and sessile oak (Quercus petraea (Matt.) Liebl.) from a chronosequence approach. Tree Physiology 30, 177–192.
| Age-related variation in carbon allocation at tree and stand scales in beech (Fagus sylvatica L.) and sessile oak (Quercus petraea (Matt.) Liebl.) from a chronosequence approach.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3c%2FltFKiug%3D%3D&md5=62cbc16679594d368ec4cb2ac7b9f2a9CAS |
Goulas Y, Cerovic ZG, Cartelat A, Moya I (2004) Dualex: a new instrument for field measurements of epidermal ultraviolet absorbance by chlorophyll fluorescence. Applied Optics 43, 4488–4496.
| Dualex: a new instrument for field measurements of epidermal ultraviolet absorbance by chlorophyll fluorescence.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXnsFCkurk%3D&md5=1d4d3fb8a7e4e2f2baa6e9f87413421dCAS |
Gower ST, Ross E, McMurtrie RE, Murty D (1996) Aboveground net primary production decline with stand age: potential causes. Trees 11, 378–382.
Grammatikopoulos G, Petropoulou Y, Manetas Y (1999) Site-dependent differences in transmittance and UV-B-absorbing capacity of isolated leaf epidermes and mesophyll in Urginea maritima (L.) Baker. Journal of Experimental Botany 50, 517–521.
| Site-dependent differences in transmittance and UV-B-absorbing capacity of isolated leaf epidermes and mesophyll in Urginea maritima (L.) Baker.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXit1eqtb0%3D&md5=53be4c90a358dca95ee40dfda8fe639dCAS |
Granier A, Tardieu F (2009) Multi-scale phenotyping of leaf expansion in response to environmental changes: the whole is more than the sum of parts. Plant, Cell & Environment 32, 1175–1184.
| Multi-scale phenotyping of leaf expansion in response to environmental changes: the whole is more than the sum of parts.Crossref | GoogleScholarGoogle Scholar |
Granier A, Pilegard K, Jensen NO (2002) Similar net ecosystem exchange of beech stands located in France and Denmark. Agricultural and Forest Meteorology 114, 75–82.
| Similar net ecosystem exchange of beech stands located in France and Denmark.Crossref | GoogleScholarGoogle Scholar |
Gross HL (1972) Crown deterioration and reduced growth associated with excessive seed production by birch. Canadian Journal of Botany 50, 2431–2437.
| Crown deterioration and reduced growth associated with excessive seed production by birch.Crossref | GoogleScholarGoogle Scholar |
Hallik L, Niinemets U, Wright IJ (2009) Are species shade and drought tolerance reflected in leaf-level structural and functional differentiation in Northern Hemisphere temperate woody flora? New Phytologist 184, 257–274.
| Are species shade and drought tolerance reflected in leaf-level structural and functional differentiation in Northern Hemisphere temperate woody flora?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXht1Kitb%2FN&md5=f24e44aca98883ecfc336a6100edacfdCAS |
Han Q, Kabeya D, Iio A, Kakubari Y (2008) Masting in Fagus crenata and its influence on the nitrogen content and dry mass of winter buds. Tree Physiology 28, 1269–1276.
| Masting in Fagus crenata and its influence on the nitrogen content and dry mass of winter buds.Crossref | GoogleScholarGoogle Scholar |
Hikosaka K, Terashima I (1995) A model of the acclimation of photosynthesis in the leaves of C3 plants to sun and shade with respect to nitrogen use. Plant, Cell & Environment 18, 605–618.
| A model of the acclimation of photosynthesis in the leaves of C3 plants to sun and shade with respect to nitrogen use.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXmvFKks78%3D&md5=d77da3ce3d87660a159fd1ccd22e9715CAS |
Hollósy F (2002) Effects of ultraviolet radiation on plant cells. Micron 33, 179–197.
| Effects of ultraviolet radiation on plant cells.Crossref | GoogleScholarGoogle Scholar |
Innes JL (1994) The occurrence of flowering and fruiting on individual trees over 3 years and their effects on subsequent crown conditions. Trees – Structure and Function 8, 139–150.
Innes JL, Boswell RC (1991) Monitoring of forest condition in Great Britain, 1990. Forestry Commission Bulletin 98. (HMSO: London)
Jansen MAK, van der Noort RE, Tan MYA, Prinsen E, Lagrimini LM, Thorneley RNF (2001) Phenol-oxidizing peroxydases contribute to the protection of plants from ultraviolet radiation stress. Plant Physiology 126, 1012–1023.
| Phenol-oxidizing peroxydases contribute to the protection of plants from ultraviolet radiation stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXlsVartbk%3D&md5=08896fd559dd2fd572a7cd2fb7202897CAS |
Jones CG, Hartley SE (1999) A protein competition model of phenolic allocation. Oikos 86, 27–44.
| A protein competition model of phenolic allocation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXkslOgu7c%3D&md5=b306bdd9a25c3931c291b9a9bb15b733CAS |
Larcher W (2003) ‘Physiological plant ecology, ecophysiology and stress physiology of functional groups.’ 4th edn. (Springer: Berlin)
Leal DB, Thomas SC (2003) Vertical gradients and tree-to-tree variation in shoot morphology and foliar nitrogen in an old-growth Pinus strobus stand. Canadian Journal of Forest Research 33, 1304–1314.
| Vertical gradients and tree-to-tree variation in shoot morphology and foliar nitrogen in an old-growth Pinus strobus stand.Crossref | GoogleScholarGoogle Scholar |
Legout AC, Walter C, Nys C (2008) Spatial variability of nutrient stocks in the humus and soils of a forest massif (Fougères, France). Annals of Forest Science 65, 108
| Spatial variability of nutrient stocks in the humus and soils of a forest massif (Fougères, France).Crossref | GoogleScholarGoogle Scholar |
Louis J, Meyer S, Maunoury-Danger F, Fresneau C, Meudec E, Cerovic ZG (2009) Seasonally changes in optically assessed epidermal phenolic compounds and chlorophyll contents in leaves of sessile oak (Quercus petraea): towards signatures of phenological stage. Functional Plant Biology 36, 732–741.
| Seasonally changes in optically assessed epidermal phenolic compounds and chlorophyll contents in leaves of sessile oak (Quercus petraea): towards signatures of phenological stage.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXovVert7g%3D&md5=76f30e0142602202ca91025d465b2fbbCAS |
Martínez-Vilalta J, Vanderklein D, Mencuccini M (2007) Tree height and age-related decline in growth in Scots pine (Pinus sylvestris L.) Oecologia 150, 529–544.
| Tree height and age-related decline in growth in Scots pine (Pinus sylvestris L.)Crossref | GoogleScholarGoogle Scholar |
Meyer S, Cerovic ZG, Goulas Y, Montpied P, Demotes-Mainard S, Bidel LPR, Moya I, Dreyer E (2006) Relationships between optically assessed polyphenols and chlorophyll contents, and leaf mass per area ratio in woody plants: a signature of the carbon-nitrogen balance within leaves? Plant, Cell & Environment 29, 1338–1348.
| Relationships between optically assessed polyphenols and chlorophyll contents, and leaf mass per area ratio in woody plants: a signature of the carbon-nitrogen balance within leaves?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XnsVGjsrg%3D&md5=b39e8542bfa44eaf2f2733e464bbe250CAS |
Meyer S, Louis J, Moise N, Piolot T, Baudin X, Cerovic ZG (2009) Developmental changes in spatial distribution of in vivo fluorescence and epidermal UV absorbance over Quercus petraea leaves. Annals of Botany 104, 621–633.
| Developmental changes in spatial distribution of in vivo fluorescence and epidermal UV absorbance over Quercus petraea leaves.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1MrmslGktQ%3D%3D&md5=3eedc3df50ff6b811db30f89d1d834a9CAS |
Montpied P, Granier A, Dreyer E (2009) Seasonal time-course of gradients of photosynthetic capacity and mesophyll conductance to CO2 across a beech (Fagus sylvatica L.) canopy. Journal of Experimental Botany 60, 2407–2418.
| Seasonal time-course of gradients of photosynthetic capacity and mesophyll conductance to CO2 across a beech (Fagus sylvatica L.) canopy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXmtlyitbc%3D&md5=010853639629eb2a08ab3beb8c72bb0dCAS |
Morales LO, Tegelberg R, Brosché M, Keinänen M, Lindfors A, Aphalo PJ (2010) Effects of solar UV-A and UV-B radiation on gene expression and phenolic accumulation in Betula pendula leaves. Tree Physiology 30, 923–934.
| Effects of solar UV-A and UV-B radiation on gene expression and phenolic accumulation in Betula pendula leaves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXpvVels7s%3D&md5=1274d15c6316b8e336cb71a491a1690dCAS |
Nicolini E (1997) Approche morphologique du développement du hêtre. PhD thesis, University Montpelleier II, Montpellier, France.
Nicolini E, Chanson B (2000) La pousse courte, un indicateur du degré de maturation chez le hêtre (Fagus sylvatica L.) Canadian Journal of Botany 77, 1539–1550.
| La pousse courte, un indicateur du degré de maturation chez le hêtre (Fagus sylvatica L.)Crossref | GoogleScholarGoogle Scholar |
Niinemets U (1995) Distribution of foliar carbon and nitrogen across the canopy of Fagus sylvatica: adaptation to a vertical light gradient. Acta Oecologica 16, 525–541.
Niinemets U (2006) The controversy over traits conferring shade-tolerance in trees: ontogenic changes revisited. Journal of Ecology 94, 464–470.
| The controversy over traits conferring shade-tolerance in trees: ontogenic changes revisited.Crossref | GoogleScholarGoogle Scholar |
Niinemets U, Kull O (1998) Stochiometry of foliar carbon constituents varies along light gradients in temperate woody canopies: implications for foliage morphological plasticity. Tree Physiology 18, 467–479.
Niinemets U, Tenhunen JD (1997) A model separating leaf structural and physiological effects on carbon gain along light gradients for shade-tolerant species Acer saccharum. Plant, Cell & Environment 20, 845–866.
| A model separating leaf structural and physiological effects on carbon gain along light gradients for shade-tolerant species Acer saccharum.Crossref | GoogleScholarGoogle Scholar |
Niinemets U, Kull O, Tenhunen JD (2004) Within-canopy variation in the rate of development of photosynthetic capacity is proportional to integrated quantum flux density in temperate deciduous trees. Plant, Cell & Environment 27, 293–313.
| Within-canopy variation in the rate of development of photosynthetic capacity is proportional to integrated quantum flux density in temperate deciduous trees.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXisF2gtr4%3D&md5=c8627be354c793a6faf74f57b54145a4CAS |
Niinemets U, Sparrow A, Cescatti A (2005) Light capture efficiency decreases with increasing tree age and size in the southern hemisphere gymnosperm Agathis australis. Trees 19, 177–190.
| Light capture efficiency decreases with increasing tree age and size in the southern hemisphere gymnosperm Agathis australis.Crossref | GoogleScholarGoogle Scholar |
Nock CA, Caspersen JP, Thomas SC (2008) Large ontogenetic declines in intra-crown leaf area index in two temperate deciduous tree species. Ecology 89, 744–753.
| Large ontogenetic declines in intra-crown leaf area index in two temperate deciduous tree species.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1c3pvVSrsQ%3D%3D&md5=fa29d65e732fde9d7e2230db97b2550bCAS |
Planchais I, Sinoquet H (1998) Foliage determinants of light interception in sunny and shaded branches of Fagus sylvatica (L.). Agricultural and Forest Meteorology 89, 241–253.
| Foliage determinants of light interception in sunny and shaded branches of Fagus sylvatica (L.).Crossref | GoogleScholarGoogle Scholar |
Poorter H (1994) Construction costs and payback time of biomass: a whole plant perspective. In ‘A whole-plant perspectives: C-N interactions’. (Eds J Roy, E Garnier) pp. 111–127. (SPB Academic Publishing: The Hague, The Netherlands)
Poorter H, Villar R (1997) The fate of acquired carbon in plants: chemical composition and construction costs. In ‘Plant resource allocation’. (Eds A Bazzaz, J Grace) pp. 39–72. (Academic Press: San Diego)
Poorter H, Niinemets U, Poorter L, Wright IJ, Villar R (2009) Causes and consequence of variation in leaf mass per area (LMA): a meta-analysis. New Phytologist 182, 565–588.
| Causes and consequence of variation in leaf mass per area (LMA): a meta-analysis.Crossref | GoogleScholarGoogle Scholar |
Ryan MG, Binkley D, Fownes JH (1997) Age-related decline in forest productivity. Pattern and process. Advances in Ecological Research 27, 213–262.
| Age-related decline in forest productivity. Pattern and process.Crossref | GoogleScholarGoogle Scholar |
Ryan MG, Binkley D, Fownes JH, Giardina CP, Seacck RS (2004) An experimental test of the causes of forest growth decline with stand age. Ecological Monographs 74, 393–414.
| An experimental test of the causes of forest growth decline with stand age.Crossref | GoogleScholarGoogle Scholar |
Ryan MG, Phillips N, Bond BJ (2006) The hydraulic limitation hypothesis revisited. Plant, Cell & Environment 29, 367–381.
| The hydraulic limitation hypothesis revisited.Crossref | GoogleScholarGoogle Scholar |
Searles PS, Flint SD, Caldwell MM (2001) A meta-analysis of plant field studies simulating stratospheric ozone depletion. Oecologia 127, 1–10.
| A meta-analysis of plant field studies simulating stratospheric ozone depletion.Crossref | GoogleScholarGoogle Scholar |
Tattini M, Guidi L, Marassi-Bonzi P, Remorini D, Degl’Innocenti E, Giordano C, Massai R, Agati G (2005) On the role of flavonoids in the integrated mechanisms of response of Ligustrum vulgare and Phylliera latifolia to high solar radiation. New Phytologist 167, 457–470.
| On the role of flavonoids in the integrated mechanisms of response of Ligustrum vulgare and Phylliera latifolia to high solar radiation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXpt1ersb8%3D&md5=2f1f93581c8ab4db55e7239bf9df83b1CAS |
Thomas SC (1996) Reproductive allometry in Malaysian rain forest trees: biomechanics versus optimal allocation. Evolutionary Ecology 10, 517–530.
| Reproductive allometry in Malaysian rain forest trees: biomechanics versus optimal allocation.Crossref | GoogleScholarGoogle Scholar |
Thomas SC, Winner WE (2002) Photosynthetic differences between saplings and adult trees: an integration of field results by meta-analysis. Tree Physiology 22, 117–127.
| Photosynthetic differences between saplings and adult trees: an integration of field results by meta-analysis.Crossref | GoogleScholarGoogle Scholar |
Yamasaki M, Kikuzawa K (2003) Temporal and spatial variations in leaf herbivory within a canopy of Fagus crenata. Oecologia 137, 226–232.
| Temporal and spatial variations in leaf herbivory within a canopy of Fagus crenata.Crossref | GoogleScholarGoogle Scholar |
