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Plant function and evolutionary biology
RESEARCH ARTICLE

Spatial and age-dependent modifications of photosynthetic capacity in four Mediterranean oak species

Ülo Niinemets A B , John D. Tenhunen C and Wolfram Beyschlag D
+ Author Affiliations
- Author Affiliations

A Department of Plant Physiology, University of Tartu, Riia 23, Tartu 51 010, Estonia.

B Centro di Ecologia Alpina, I-38 040 Viote del Monte Bondone (TN), Italy. Corresponding author. Email: ulo.niinemets@ut.ee

C Department of Plant Ecology, University of Bayreuth, D-95 440, Bayreuth, Germany.

D Department of Experimental and Systems Ecology, University of Bielefeld, Universitätsstraße 25, 33 615 Bielefeld, Germany.

Functional Plant Biology 31(12) 1179-1193 https://doi.org/10.1071/FP04128
Submitted: 15 July 2004  Accepted: 21 September 2004   Published: 8 December 2004

Abstract

Drought is one of the most important limitations of photosynthesis in Mediterranean climates. However, Mediterranean sclerophyllous species with long-lived leaves also support extensive and dynamic canopies, with potentially large spatial and age-dependent gradients. We studied within-canopy and temporal patterns in foliage structure, chemistry and photosynthesis in the evergreen species Quercus coccifera L., Q. ilex L. subsp. ballota (Desf.) Samp. in Bol. and Q. suber L. and in the semi-deciduous marcescent species Q. faginea Lam. to determine the role of within-canopy shading and leaf age on foliage functioning. There was a 2.5-fold within-canopy gradient in leaf dry mass per unit area (MA) that was accompanied by a 3-fold range in area-based leaf nitrogen (N) content, the capacity for photosynthetic electron transport (Jmax) and maximum Rubisco carboxylase activity (Vcmax), while the fractional investments of leaf nitrogen in electron transport (FB) and in Rubisco (FR) were relatively constant within the canopy. Leaf aging led to increased MA, larger or constant mass-based N content, larger phosphorous (P) and structural carbon contents, but decreased movable cation contents. Age-dependent increases in MA and N per dry mass meant that Jmax and Vcmax per area were weakly related to leaf age, with a trend of decreasing values in older leaves. However, Jmax and Vcmax per unit dry mass decreased 4-fold across the range of leaf age, primarily owing to decreases in apparent N investments in photosynthetic machinery. This decrease in apparent N investments in photosynthetic machinery was possibly the result of a larger fraction of N bound to cell walls, or of an enhanced CO2 diffusion resistance from the outer surface of cell walls to the chloroplasts in older leaves with thicker and more lignified cell walls. The age-dependent variation in apparent fractional investments of N in photosynthetic machinery reduced the generality of leaf nitrogen v. photosynthesis relationships. Photosynthetic characteristics qualitatively fitted the same patterns with leaf age in all species, but at a common leaf age, area-based leaf photosynthetic potentials depended on species-specific values of MA. These data collectively demonstrate important canopy and age-dependent controls on leaf structure, chemistry and photosynthetic potentials that should be included in larger-scale photosynthesis simulations in Mediterranean climates.

Keywords: age effects, leaf structure, nitrogen v. photosynthesis relationship, nutrient content, sclerophyll species.


Acknowledgments

We thank Annette Suske for the help with chemical analyses. Financial support was provided by the Estonian Science Foundation (grant 5702), the Estonian Ministry of Education and Science (grant 0182468As03) and the Deutsche Bundesministerium für Bildung, Wissenschaft, Forschung und Technologie (Grant PT BEO 51 0339476B).


References


Acherar M, Rambal S (1992) Comparative water relations of four Mediterranean oak species. Vegetatio 99–100, 177–184.
Crossref |
open url image1

Asner GP, Wessman CA, Archer S (1998) Scale dependence of absorption of photosynthetically active radiation in terrestrial ecosystems. Ecological Applications 8, 1003–1021. open url image1

Baldocchi DD, Harley PC (1995) Scaling carbon dioxide and water vapour exchange from leaf to canopy in a deciduous forest. II. Model testing and application. Plant, Cell and Environment 18, 1157–1173. open url image1

Bernier PY, Raulier F, Stenberg P, Ung C-H (2001) Importance of needle age and shoot structure on canopy net photosynthesis of balsam fir (Abies balsamea): a spatially inexplicit modeling analysis. Tree Physiology 21, 815–830.
PubMed |
open url image1

Beyschlag W, Lange OL, Tenhunen JD (1986) Photosynthese und Wasserhaushalt der immergrünen mediterranen Hartlaubpflanze Arbutus unedo L. im Jahreslauf am Freilandstandort in Portugal. I. Tagesläufe von CO2-Gaswechsel und Transpiration unter natülichen Bedingungen. Flora 178, 409–444. open url image1

Beyschlag W, Phibbs A, Pfanz H (1990) The role of temperature and humidity in controlling the diurnal stomatal behaviour of Arbutus unedo L. during the dry season. Biochemie und Physiologie der Pflanzen 186, 265–271. open url image1

Beyschlag W, Pfanz H, Ryel RJ (1992) Stomatal patchiness in Mediterranean evergreen sclerophylls. Phenomenology and consequences for the interpretation of the midday depression in photosynthesis and transpiration. Planta 187, 546–553.
Crossref | GoogleScholarGoogle Scholar | open url image1

Caldwell MM, Meister H-P, Tenhunen JD, Lange OL (1986) Canopy structure, light microclimate and leaf gas exchange of Quercus coccifera L. in a Portugese macchia: measurements in different canopy layers and simulations with a canopy model. Trees: Structure and Function 1, 25–41. open url image1

Castell C, Terradas J, Tenhunen JD (1994) Water relations, gas exchange and growth of resprouts and mature plant shoots of Arbutus unedo L. and Quercus ilex L. Oecologia 98, 201–211. open url image1

Castro-Díez P, Villar-Salvador P, Pérez-Rontomé C, Maestro-Martínez M, Montserrat-Martí G (1997) Leaf morphology and leaf chemical composition in three Quercus (Fagaceae) species along a rainfall gradient in NE Spain. Trees: Structure and Function 11, 127–134. open url image1

Catarino FM, Correia OCA, Correia AIVD (1982) Structure and dynamics of Serra da Arrábida Mediterranean vegetation. Ecologia Mediterranea 8, 203–222. open url image1

Cescatti, A ,  and  Niinemets, Ü (2005). Light harvesting: from leaf to landscape. In ‘Evaluating photosynthetic adaptation from the chloroplast to the landscape. Ecological studies, 178’. In press. (Springer-Verlag: Berlin)

Cherbuy B, Joffre R, Gillon D, Rambal S (2001) Internal remobilization of carbohydrates, lipids, nitrogen and phosphorus in the Mediterranean evergreen oak Quercus ilex. Tree Physiology 21, 9–17.
PubMed |
open url image1

Damesin C, Rambal S, Joffre R (1998) Seasonal and annual changes in leaf δ13C in two co-occurring Mediterranean oaks: relations to leaf growth and drought progression. Functional Ecology 12, 778–785.
Crossref | GoogleScholarGoogle Scholar | open url image1

de Lillis M, Fontanella A (1992) Comparative phenology and growth in different species of the Mediterranean maquis of central Italy. Vegetatio 99–100, 83–96.
Crossref |
open url image1

Demmig-Adams B, Adams WW, Winter K, Meyer A, Schreiber U, Pereira JS, Krüger A, Czygan F-C, Lange OL (1989) Photochemical efficiency of photosystem II, photon yield of O2 evolution, photosynthetic capacity and carotenoid composition during the midday depression of net CO2 uptake in Arbutus unedo growing in Portugal. Planta 177, 377–387.
Crossref |
open url image1

Diamantoglou S, Kull U (1988) Der Stickstoffhaushalt immergrüner mediterraner Hartlaubblätter. Flora 180, 377–390. open url image1

Drossopoulos JB, Niavis CA (1988) Seasonal changes of the metabolites in the leaves, bark and xylem tissues of olive tree (Olea europaea L.). II. Carbohydrates. Annals of Botany 62, 321–327. open url image1

Dyckmans J, Flessa H, Brinkmann K, Mai C, Polle A (2002) Carbon and nitrogen dynamics in acid detergent fibre lignins of beech (Fagus sylvatica L.) during the growth phase. Plant, Cell and Environment 25, 469–478.
Crossref | GoogleScholarGoogle Scholar | open url image1

Escudero A, del Arco JM, Sanz IC, Ayala J (1992) Effects of leaf longevity and retranslocation efficiency on the retention time of nutrients in the leaf biomass of different woody species. Oecologia 90, 80–87.
Crossref |
open url image1

Evans, JR ,  and  Loreto, F (2000). Acquisition and diffusion of CO2 in higher plant leaves. In ‘Photosynthesis: physiology and metabolism’. pp. 321–351. (Kluwer Academic Publishers: Dordrecht)

Evans, JR ,  and  Seemann, JR (1989). The allocation of protein nitrogen in the photosynthetic apparatus: costs, consequences and control. In ‘Plant biology’. pp. 183–205. (AR Liss Inc.: New York)

Faria T, García-Plazaola JI, Abadía , Cerasoli S, Pereira JS, Chaves MM (1996) Diurnal changes in photoprotective mechanisms in leaves of cork oak (Quercus suber) during summer. Tree Physiology 16, 115–123.
PubMed |
open url image1

Farquhar, GD ,  and  von Caemmerer, S (1982). Modeling of photosynthetic response to environmental conditions. In ‘Physiological plant ecology’. pp. 549–588. (Springer-Verlag: Berlin)

Fleck I, Diaz C, Pascual M, Iñiguez FJ (1995) Ecophysiological differences between first-year resprouts after wildfire and unburned vegetation of Arbutus unedo and Coriaria myrtifolia. Acta Oecologica 16, 55–69. open url image1

Fleck S, Niinemets Ü, Cescatti A, Tenhunen JD (2003) Three-dimensional lamina architecture alters light harvesting efficiency in Fagus: a leaf-scale analysis. Tree Physiology 23, 577–589.
PubMed |
open url image1

Flexas J, Gulías J, Jonasson S, Medrano H, Mus M (2001) Seasonal patterns and control of gas exchange in local populations of the Mediterranean evergreen shrub Pistacia lentiscus L. Acta Oecologica 22, 33–43.
Crossref | GoogleScholarGoogle Scholar | open url image1

Gracia CA (1984) Response of the evergreen oak to the incident radiation at the Montseny (Barcelona, Spain). Bulletin de la Société Botanique de France. Actualités botaniques 131, 595–597. open url image1

Gratani L (1996) Leaf and shoot growth dynamics of Quercus ilex L. Acta Oecologica 17, 17–27. open url image1

Gratani L, Moriconi M (1983) Seasonal changes in nutrient concentration in Quercus ilex. Annals of Botany 41, 185–195. open url image1

Gratani L, Marzi P, Crescente MF (1992) Morphological adaptions of Quercus ilex leaves in the Castelporziano forest. Vegetatio 100, 155–161.
Crossref |
open url image1

Harley PC, Thomas RB, Reynolds JF, Strain BR (1992) Modelling photosynthesis of cotton grown in elevated CO2. Plant, Cell and Environment 15, 271–282. open url image1

Infante JM, Damesin C, Rambal S, Fernández-Alés R (1999) Modelling leaf gas exchange in holm-oak trees in southern Spain. Agricultural and Forest Meteorology 95, 203–223.
Crossref | GoogleScholarGoogle Scholar | open url image1

Insley H, Boswell RC, Gardiner JBH (1981) Foliar macronutrients (N, P, K, Ca and Mg) in lime (Tilia spp.). II. Seasonal variation. Plant and Soil 61, 391–401. open url image1

Jonasson S, Medrano H, Flexas J (1997) Variation in leaf longevity of Pistacia lentiscus and its relationship to sex and drought stress inferred from leaf δ13C. Functional Ecology 11, 282–289.
Crossref | GoogleScholarGoogle Scholar | open url image1

Jordan DB, Ogren WL (1984) The CO2 / O2 specificity of ribulose 1,5-bisphosphate carboxylase / oxygenase. Dependence on ribulose bisphosphate concentration, pH and temperature. Planta 161, 308–313.
Crossref |
open url image1

Kellomäki S, Wang K-Y (1997) Effects of elevated O3 and CO2 concentrations on photosynthesis and stomatal conductance in Scots pine. Plant, Cell and Environment 20, 995–1006. open url image1

Lange, OL , Tenhunen, JD , Harley, P ,  and  Walz, H (1985). Method for field measurements of O2-exchange. The diurnal changes in net photosynthesis and photosynthetic capacity of lichens under Mediterranean climatic conditions. In ‘Lichen physiology and cell biology’. pp. 23–39. (Plenum Publishing Corporation: New York)

Leßner, A (1994). ‘Die Beziehung zwischen Gaswechsel, Blattdemographie und Stickstoffhaushalt an immer- und wechselgrünen mediterranen Holzgewachsen.’ (Diploma Dissertation, Fakultät für Biologie, Chemie und Geowissenschaften der Universität Bayreuth: Germany)

Loreto F, Harley PC, di Marco G, Sharkey TD (1992) Estimation of mesophyll conductance to CO2 flux by three different methods. Plant Physiology 98, 1437–1443. open url image1

Martínez-Ferri E, Balaguer L, Valladares F, Chico JM, Manrique E (2000) Energy dissipation in drought-avoiding and drought-tolerant tree species at midday during the Mediterranean summer. Tree Physiology 20, 131–138.
PubMed |
open url image1

Mediavilla S, Escudero A (2003) Stomatal response to drought at a Mediterranean site: a comparative study of co-occurring woody species differing in leaf longevity. Tree Physiology 23, 987–996.
PubMed |
open url image1

Meletiou-Christou MS, Rhizopoulou S, Diamantoglou S (1994) Seasonal changes of carbohydrates, lipids and nitrogen content in sun and shade leaves from four Mediterranean evergreen sclerophylls. Environmental and Experimental Botany 34, 129–140.
Crossref | GoogleScholarGoogle Scholar | open url image1

Méthy M, Damesin C, Rambal S (1996) Drought and photosystem II activity in two Mediterranean oaks. Annales Des Sciences Forestieres 53, 255–262. open url image1

Millard P (1994) Measurement of the remobilisation of nitrogen for spring leaf growth of trees under field conditions. Tree Physiology 14, 1049–1054.
PubMed |
open url image1

Morecroft MD, Stokes VJ, Morison JIL (2003) Seasonal changes in the photosynthetic capacity of canopy oak (Quercus robur) leaves: the impact of slow development on annual carbon uptake. International Journal of Biometeorology 47, 221–226.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Niinemets Ü (2001) Climatic controls of leaf dry mass per area, density and thickness in trees and shrubs at the global scale. Ecology 82, 453–469. open url image1

Niinemets Ü (2002) Stomatal conductance alone does not explain the decline in foliar photosynthetic rates with increasing tree age and size in Picea abies and Pinus sylvestris. Tree Physiology 22, 515–535.
PubMed |
open url image1

Niinemets Ü, Kull O (1998) Stoichiometry of foliar carbon constituents varies along light gradients in temperate woody canopies: implications for foliage morphological plasticity. Tree Physiology 18, 467–479.
PubMed |
open url image1

Niinemets Ü, Lukjanova A (2003) Needle longevity, shoot growth and branching frequency in relation to site fertility and within-canopy light conditions in Pinus sylvestris. Annals of Forest Science 60, 195–208.
Crossref | GoogleScholarGoogle Scholar | open url image1

Niinemets Ü, Tenhunen JD (1997) A model separating leaf structural and physiological effects on carbon gain along light gradients for the shade-tolerant species Acer saccharum. Plant, Cell and Environment 20, 845–866.
Crossref | GoogleScholarGoogle Scholar | open url image1

Niinemets Ü, Seufert G, Steinbrecher R, Tenhunen JD (2002) A model coupling foliar monoterpene emissions to leaf photosynthetic characteristics in Mediterranean evergreen Quercus species. New Phytologist 153, 257–276.
Crossref | GoogleScholarGoogle Scholar | open url image1

Niinemets Ü, 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 and Environment 27, 293–313.
Crossref |
open url image1

Oliveira G, Werner C, Correia O (1996) Are ecophysiological responses influenced by crown position in cork-oak? Annales des Sciences Forestieres 53, 235–241. open url image1

Pereira JS, Tenhunen JD, Lange OL, Beyschlag W, Meyer A, David MM (1986) Seasonal and diurnal patterns in leaf gas exchange of Eucalyptus globulus trees growing in Portugal. Canadian Journal of Forest Research 16, 177–184. open url image1

Pereira, JS , Beyschlag, G , Lange, OL , Beyschlag, W ,  and  Tenhunen, JD (1987). Comparative phenology of four mediterranean shrub species growing in Portugal. In ‘Plant response to stress. Functional analysis in Mediterranean ecosystems’. pp. 503–513. (Springer-Verlag: Berlin)

Rambal, S (2001). Productivity of Mediterranean-type ecosystems. In ‘Terrestrial global productivity: past, present and future’. pp. 315–344. (Academic Press Inc.: San Diego)

Rambal S, Damesin C, Joffre R, Méthy M, Lo Seen D (1996) Optimisation of carbon gain in canopies of Mediterranean evergreen oaks. Annales des Sciences Forestieres 53, 547–560. open url image1

Rapp M, Ed Derfoufi F, Blanchard A (1992) Productivity and nutrient uptake in a holm oak (Quercus ilex L.) stand and during regeneration after clearcut. Vegetatio 99–100, 263–272.
Crossref |
open url image1

Reich PB, Kloeppel BD, Ellsworth DS, Walters MB (1995) Different photosynthesis-nitrogen relations in deciduous hardwood and evergreen coniferous tree species. Oecologia 104, 24–30. open url image1

Ripullone F, Grassi G, Lauteri M, Borghetti M (2003) Photosynthesis-nitrogen relationships: interpretation of different patterns between Pseudotsuga menziesii and Populus × euroamericana in a mini-stand experiment. Tree Physiology 23, 137–144.
PubMed |
open url image1

Robert B, Bertoni G, Sayag D, Masson P (1996) Assessment of mineral nutrition of cork oak through foliar analysis. Communications in Soil Science and Plant Analysis 27, 2091–2109. open url image1

Sabaté S, Sala A, Gracia CA (1995) Nutrient content in Quercus ilex canopies: seasonal and spatial variation within a catchment. Plant and Soil 168–169, 297–304. open url image1

Sala A, Tenhunen JD (1996) Simulations of canopy net photosynthesis and transpiration in Quercus ilex L. under the influence of seasonal drought. Agricultural and Forest Meteorology 78, 203–222.
Crossref | GoogleScholarGoogle Scholar | open url image1

Sala A, Sabaté S, Gracia C, Tenhunen JD (1994) Canopy structure within a Quercus ilex forested watershed: variations due to location, phenological development and water availability. Trees: Structure and Function 8, 254–261. open url image1

Sala i Serra A (1992) ‘Water relations, canopy structure and canopy gas exchange in a Quercus ilex forest: variation in time and space.’ PhD thesis. (Universitat de Barcelona, Facultat de Biologia, Departament d’ ecologia: Spain)

Saur E, Nambiar EKS, Fife DN (2000) Foliar nutrient retranslocation in Eucalyptus globulus. Tree Physiology 20, 1105–1112.
PubMed |
open url image1

Schoettle AW, Smith WK (1999) Interrelationships among light, photosynthesis and nitrogen in the crown of mature Pinus contorta ssp. latifolia. Tree Physiology 19, 13–22.
PubMed |
open url image1

Schulze E-D, Hall AE, Lange OL, Walz H (1982) A portable steady-state porometer for measuring the carbon dioxide and water vapour exchanges of leaves under natural conditions. Oecologia 53, 141–145.
Crossref |
open url image1

Smith, SD ,  and  Nobel, PS (1986). Deserts. In ‘Photosynthesis in contrasting environments. Topics in photosynthesis, 7’. pp. 13–62. (Elsevier Science Publishers: Amsterdam)

Sokal, RR ,  and  Rohlf, FJ (1995). ‘Biometry. The principles and practice of statistics in biological research.’ 3rd edn . (WH Freeman and Co.: New York)

Teixeira Filho J, Damesin C, Rambal S, Joffre R (1998) Retrieving leaf conductances from sap flows in a mixed Mediterranean woodland: a scaling exercise. Annales des Sciences Forestieres 55, 173–190. open url image1

Tenhunen JD, Lange OL, Gebel J, Beyschlag W, Weber JA (1984a) Changes in photosynthetic capacity, carboxylation efficiency and CO2 compensation point associated with midday stomatal closure and midday depression of net CO2 exchange of leaves of Quercus suber. Planta 162, 193–203.
Crossref |
open url image1

Tenhunen, JD , Meister, HP , Caldwell, MM ,  and  Lange, OL (1984b). Environmental constraints on productivity of the Mediterranean sclerophyll shrub Quercus coccifera. In ‘Proceedings of INTECOL workshop — rates of natural primary productivity and agricultural production’. b. pp. 33–53. (Institutio Agronomico Mediterraneo de Zaragoza: Zaragoza: Spain)

Tenhunen JD, Lange OL, Harley PC, Beyschlag W, Meyer A (1985) Limitations due to water stress on leaf net photosynthesis of Quercus coccifera in the Portugese evergreen shrub. Oecologia 67, 23–30.
Crossref |
open url image1

Tenhunen, JD , Beyschlag, W , Lange, OL ,  and  Harley, PC (1987). Changes during summer drought in leaf CO2 uptake rates of macchia shrubs growing in Portugal: limitations due to photosynthetic capacity, carboxylation efficiency and stomatal conductance. In ‘Plant response to stress. Functional analysis in Mediterranean ecosystems’. pp. 305–327. (Springer-Verlag: Berlin)

Tenhunen JD, Sala Serra A, Harley PC, Dougherty RL, Reynolds JF (1990) Factors influencing carbon fixation and water use by mediterranean sclerophyll shrubs during summer drought. Oecologia 82, 381–393.
Crossref |
open url image1

von Caemmerer S, Farquhar GD (1981) Some relationships between the biochemistry of photosynthesis and the gas exchange of leaves. Planta 153, 376–387.
Crossref |
open url image1

Weikert RM, Wedler M, Lippert M, Schramel P, Lange OL (1989) Photosynthetic performance, chloroplast pigments and mineral content of various needle age classes of spruce (Picea abies) with and without the new flush: an experimental approach for analysing forest decline phenomena. Trees: Structure and Function 3, 161–172. open url image1

Werner C, Ryel RJ, Correia O, Beyschlag W (2001a) Effects of photoinhibition on whole-plant carbon gain assessed with a photosynthesis model. Plant, Cell and Environment 24, 27–40.
Crossref | GoogleScholarGoogle Scholar | open url image1

Werner C, Ryel RJ, Correia O, Beyschlag W (2001b) Structural and functional variability within the canopy and its relevance for carbon gain and stress avoidance. Acta Oecologica 22, 129–138.
Crossref | GoogleScholarGoogle Scholar | open url image1

Wilson KB, Baldocchi DD, Hanson PJ (2001) Leaf age affects the seasonal pattern of photosynthetic capacity and net ecosystem exchange of carbon in a deciduous forest. Plant, Cell and Environment 24, 571–583.
Crossref | GoogleScholarGoogle Scholar | open url image1

Wright IJ, Reich PB, Westoby M, Ackerly DD, Baruch Z , et al . (2004) The world-wide leaf economics spectrum. Nature 428, 821–827.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Xu L, Baldocchi DD (2003) Seasonal trends in photosynthetic parameters and stomatal conductance in blue oak (Quercus douglasii) under prolonged summer drought and high temperature. Tree Physiology 23, 865–877.
PubMed |
open url image1