Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Relating leaf photosynthetic rate to whole-plant growth: drought and shade effects on seedlings of four Quercus species

José L. Quero A B E F , Rafael Villar B , Teodoro Marañón C , Regino Zamora A , Dolores Vega B and Lawren Sack D
+ Author Affiliations
- Author Affiliations

A Grupo de Ecología Terrestre, Departamento de Ecología, Facultad de Ciencias, Universidad de Granada, 18071 Granada, Spain.

B Área de Ecología, Facultad de Ciencias, Universidad de Córdoba, 14071 Cordoba, Spain.

C Instituto de Recursos Naturales y Agrobiología, CSIC, PO Box 1052, 41080 Seville, Spain.

D Department of Ecology and Evolutionary Biology, University of California, Los Angeles, 621 Charles E. Young Drive South, Los Angeles, CA 90095-1606, USA.

E Present address: Forest Ecology and Forest Management Group, Centre for Ecosystem Studies, Wageningen University, PO Box 47, 6700 AA Wageningen, The Netherlands.

F Corresponding author. Email: jose.queroperez@wur.nl

Functional Plant Biology 35(8) 725-737 https://doi.org/10.1071/FP08149
Submitted: 17 May 2008  Accepted: 25 July 2008   Published: 19 September 2008

Abstract

Understanding the impacts of combined resource supplies on seedlings is critical to enable prediction of establishment growth, and forest dynamics. We investigated the effects of irradiance and water treatments on absolute growth, and relative growth rate (RGR) and its components, for seedlings of four Quercus species differing in leaf habit and with a wide variation in seed mass. Plants were grown for 6.5 months at three levels of irradiance (100, 27, and 3% daylight), and treated during the last 2.5 months with two watering treatments (frequent watering v. suspended watering). Both shade and drought reduced seedling growth rates, with a significant interaction: under full irradiance the drought treatment had a stronger impact on RGR and final biomass than under deep shade. For three species, seed mass was positively related to absolute growth, with stronger correlations at lower irradiance. The evergreen species grew faster than the deciduous species, though leaf habit accounted for a minor part of the interspecific variation in absolute growth. Seedling biomass was determined positively either by RGR or seed mass; RGR was positively linked with net assimilation rate (NAR) and leaf mass fraction (LMF), and seed mass was negatively linked with RGR and LMF, but positively linked with NAR. Seedling RGR was not correlated with light-saturated net photosynthetic rate, but was strongly correlated with the net carbon balance estimated, from photosynthetic light-response curves, considering daily variation in irradiance. These findings suggest an approach to applying short-term physiological measurements to predict the RGR and absolute growth rate of seedlings in a wide range of combinations of irradiance and water supplies.

Additional keywords: biomass allocation, carbon balance, growth analysis, leaf habit, Mediterranean oak, relative growth rate, seed mass, specific leaf area.


Acknowledgements

We thank to SCAI of University of Cordoba for greenhouse facilities, and F. Conde, M. A. Calero, C. Sánchez-Casimiro, L. Bejarano, A. Murillo, J. Rubio, F. J. Morilla and M. A. Núñez for their help during the experiment. G. Quero gave logistic support. This study was supported by the grant FPI-MEC to JLQ (BES-2003–1716), and by the coordinated Spanish MEC projects HETEROMED (REN2002–04041) and DINAMED (CGL2005–05830). This research is part of the REDBOME and GLOBIMED networks on forest ecology (http://www.ugr.es/~redbome/; http://www.globimed.net/).


References


Abrams MD, Mostoller SA (1995) Gas exchange, leaf structure and nitrogen in contrasting successional tree species growing in open and understory sites during a drought. Tree Physiology 15, 361–370.
PubMed |
open url image1

Abrams MD, Kloeppel BD, Kubiske MD (1992) Ecophysiological and morphological responses to shade and drought in two contrasting ecotypes of Prunus serotina. Tree Physiology 10, 343–355.
PubMed |
open url image1

Amaral J (1990) Quercus. In ‘Flora Ibérica’. (Eds S Castroviejo, M Laínz, G López González, P Montserrat, F Muñoz Garmendia, J Paiva, L Villar) pp. 15–36. (Real Jardín Botánico CSIC: Madrid)

Antúnez I, Retamosa EC, Villar R (2001) Relative growth rate in phylogenetically related deciduous and evergreen woody species. Oecologia 128, 172–180.
Crossref | GoogleScholarGoogle Scholar | open url image1

Aranda I, Castro L, Pardos M, Gil L, Pardos JA (2005) Effects of the interaction between drought and shade on water relations, gas exchange and morphological traits in cork oak Quercus suber L. seedlings. Forest Ecology and Management 210, 117–129.
Crossref | GoogleScholarGoogle Scholar | open url image1

Ashton PMS (1992) Some measurements of the microclimate within a Sri Lankan tropical rainforest. Agricultural and Forest Meteorology 59, 217–235.
Crossref | GoogleScholarGoogle Scholar | open url image1

Canham CD, Berkowitz AR, Kelly VR, Lovett GM, Ollinger SV, Schnurr J (1996) Biomass allocation and multiple resource limitation in tree seedlings. Canadian Journal of Forest Research 26, 1521–1530.
Crossref | GoogleScholarGoogle Scholar | open url image1

Castro J (1999) Seed mass versus seedling performance in Scots pine: a maternally dependent trait. New Phytologist 144, 153–161.
Crossref | GoogleScholarGoogle Scholar | open url image1

Coomes DA, Grubb PJ (2000) Impacts of root competition in forests and woodlands: a theoretical framework and review of experiments. Ecological Monographs 70, 171–207. open url image1

Cornelissen JHC, Castro-Díez P, Hunt R (1996) Seedling growth, allocation and leaf attributes in a wide range of woody plant species and types. Journal of Ecology 84, 755–765.
Crossref | GoogleScholarGoogle Scholar | open url image1

De Luís M, García-Cano MF, Cortina J, Raventós J, González-Hidalgo JC, Sánchez JR (2001) Climatic trends, disturbances and short-term vegetation dynamics in a Mediterranean shrubland. Forest Ecology and Management 147, 25–37.
Crossref | GoogleScholarGoogle Scholar | open url image1

Demmig-Adams B, Adams WW (1996) The role of xanthophyll cycle carotenoids in the protection of photosynthesis. Trends in Plant Science 1, 21–26.
Crossref | GoogleScholarGoogle Scholar | open url image1

Ellsworth DS, Reich PB (1992) Water relations and gas exchange of Acer saccharum seedlings in contrasting natural light and water regimes. Tree Physiology 10, 1–20.
PubMed |
open url image1

Engelbrecht BMJ, Comita LS, Condit R, Kursar TA, Tyree MT, Turner BL, Hubbell SP (2007) Drought sensitivity shapes species distribution patterns in tropical forests. Nature 447, 80–82.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Espelta JM, Cortés P, Mangirón M, Retana J (2005) Differences in biomass partitioning, leaf nitrogen content and water use efficiency (δ13C) result in similar performance of seedlings of two Mediterranean oak species. Ecoscience 12, 447–454.
Crossref | GoogleScholarGoogle Scholar | open url image1

García LV (2004) Escaping the Bonferroni iron claw in ecological studies. Oikos 105, 657–663.
Crossref | GoogleScholarGoogle Scholar | open url image1

Garnier E, Shipley B, Roumet C, Laurent G (2001) A standardized protocol for the determination of specific leaf area and leaf dry matter content. Functional Ecology 15, 688–695.
Crossref | GoogleScholarGoogle Scholar | open url image1

Givnish TJ (1988) Adaptation to sun and shade: a whole-plant perspective. Australian Journal of Plant Physiology 15, 63–92. open url image1

Gómez-Aparicio L, Zamora R, Gómez JM, Hódar JA, Castro J, Baraza E (2004) Applying plant facilitation to forest restoration: a meta-analysis of the use of shrubs as nurse plants. Ecological Applications 14, 1128–1138.
Crossref | GoogleScholarGoogle Scholar | open url image1

Gómez-Aparicio L, Valladares F, Zamora R, Quero JL (2005) Response of tree seedlings to the abiotic heterogeneity generated by nurse shrubs: an experimental approach at different scales. Ecography 28, 757–768.
Crossref | GoogleScholarGoogle Scholar | open url image1

Grant OM, Incoll LD, McNeilly T (2005) Variation in growth response to availability of water in Cistus albidus populations from different habitats. Functional Plant Biology 32, 817–829.
Crossref | GoogleScholarGoogle Scholar | open url image1

de Groot CC, Marcelis LFM, van de Boogaard R, Lambers H (2002) Interactive effects of nitrogen and irradiance on growth and partitioning of dry mass and nitrogen in young tomato plants. Functional Plant Biology 29, 1319–1328.
Crossref | GoogleScholarGoogle Scholar | open url image1

Holmgren M (2000) Combined effects of shade and drought on tulip poplar seedlings: trade-off in tolerance or facilitation? Oikos 90, 67–78.
Crossref | GoogleScholarGoogle Scholar | open url image1

Hunt R, Causton DR, Shipley B, Askew AP (2002) A modern tool for classical plant growth analysis. Annals of Botany 90, 485–488.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

IPCC (2007) ‘Climate change 2007. The physical science basis: working group I contribution to the fourth assessment report of the IPCC.’ (Cambridge University Press: Cambridge)

Ke G, Werger MJA (1999) Different responses to shade of evergreen and deciduous oak seedlings and the effect of acorn size. Acta Oecologica 20, 579–586.
Crossref | GoogleScholarGoogle Scholar | open url image1

Kruger EL, Volin JC (2006) Re-examining the empirical relation between plant growth and leaf photosynthesis. Functional Plant Biology 33, 421–429.
Crossref | GoogleScholarGoogle Scholar | open url image1

Loveys BR, Scheurwater I, Pons TL, Fitter AH, Atkin OK (2002) Growth temperature influences the underlying components of relative growth rate: an investigation using inherently fast- and slow-growing plant species. Plant, Cell & Environment 25, 975–987.
Crossref | GoogleScholarGoogle Scholar | open url image1

Maestre FT, Cortina J, Bautista S, Bellot J, Vallejo R (2003) Small-scale environmental heterogeneity and spatio-temporal dynamics of seedling survival in a degraded semiarid ecosystem. Ecosystems 6, 630–643.
Crossref | GoogleScholarGoogle Scholar | open url image1

Marañón T, Grubb PG (1993) Physiological basis and ecological significance of the seed size and relative growth rate relationship in Mediterranean annuals. Functional Ecology 7, 591–599.
Crossref | GoogleScholarGoogle Scholar | open url image1

Marañón T, Zamora R, Villar R, Zavala MA, Quero JL, Pérez-Ramos I, Mendoza I, Castro J (2004) Regeneration of tree species and restoration under contrasted Mediterranean habitats: field and glasshouse experiments. International Journal of Ecology and Environmental Sciences 30, 187–196. open url image1

Matthes U, Larson DW (2006) Microsite and climatic controls of tree population dynamics: an 18-year study on cliffs. Journal of Ecology 94, 402–414.
Crossref | GoogleScholarGoogle Scholar | open url image1

Montgomery R (2004) Relative importance of photosynthetic physiology and biomass allocation for tree seedling growth across a broad light gradient. Tree Physiology 24, 155–167.
PubMed |
open url image1

Montgomery RA, Chazdon RL (2002) Light gradient partitioning by tropical tree seedlings in the absence of canopy gaps. Oecologia 131, 165–174.
Crossref | GoogleScholarGoogle Scholar | open url image1

Niinemets U (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 U, Valladares F (2004) Photosynthetic acclimation to simultaneous and interacting environmental stresses along natural light gradients: optimality and constraints. Plant Biology 6, 254–268.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Niinemets U, Valladares F (2006) Tolerance to shade, drought, and waterlogging of temperate Northern hemisphere trees and shrubs. Ecological Monographs 76, 521–547.
Crossref | GoogleScholarGoogle Scholar | open url image1

Niinemets U, Tenhunen JD, Beyschlag W (2004) Spatial and age-dependent modifications of photosynthetic capacity in four Mediterranean oak species. Functional Plant Biology 31, 1179–1193.
Crossref | GoogleScholarGoogle Scholar | open url image1

Paz H, Martínez-Ramos M (2003) Seed mass and seedling performance within eight species of Psychotria (Rubiaceae). Ecology 84, 439–450.
Crossref | GoogleScholarGoogle Scholar | open url image1

Peñuelas J, Filella I, Comas P (2002) Changed plant and animal life cycles from 1952–2000 in the Mediterranean region. Global Change Biology 8, 531–544.
Crossref | GoogleScholarGoogle Scholar | open url image1

Piñol J, Terradas J, Lloret F (1998) Climate warming, wildfire, hazard and wildfire occurrence in coastal eastern Spain. Climatic Change 38, 345–357.
Crossref | GoogleScholarGoogle Scholar | open url image1

Poorter H, Remkes C (1990) Leaf area ratio and net assimilation rate of 24 wild species differing in relative growth rate. Oecologia 83, 553–559.
Crossref | GoogleScholarGoogle Scholar | open url image1

Poorter H, Remkes C, Lambers H (1990) Carbon and nitrogen economy of 24 wild-species differing in relative growth-rate. Plant Physiology 94, 621–627.
PubMed |
open url image1

Poorter L (1999) Growth responses of 15 rain-forest tree species to a light gradient: the relative importance of morphological and physiological traits. Functional Ecology 13, 396–410.
Crossref | GoogleScholarGoogle Scholar | open url image1

Poorter L (2001) Light-dependent changes in biomass allocation and their importance for growth of rain forest tree species. Functional Ecology 15, 113–123.
Crossref | GoogleScholarGoogle Scholar | open url image1

Poorter L, Rose SA (2005) Light-dependent changes in the relationship between seed mass and seedling traits: a meta-analysis for rain forest tree species. Oecologia 142, 378–387.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Quero JL (2006) SADIE como herramienta de cuantificación de la heterogeneidad espacial: casos prácticos en el Parque Nacional de Sierra Nevada (Granada, España). Ecosistemas 15, 40–47. open url image1

Quero JL, Villar R, Marañón T, Zamora R (2006) Interactions of drought and shade effects on four Mediterranean Quercus species: physiological and structural leaf responses. New Phytologist 170, 819–834.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Quero JL, Villar R, Marañón T, Zamora R, Poorter L (2007) Seed mass effect in four Mediterranean Quercus species (Fagaceae) growing in contrasting light environments. American Journal of Botany 94, 1795–1803.
Crossref | GoogleScholarGoogle Scholar | open url image1

Reich PB, Walters MB, Ellsworth DS (1992) Leaf lifespan in relation to leaf, plant and stand characteristics among diverse ecosystems. Ecological Monographs 62, 365–392.
Crossref | GoogleScholarGoogle Scholar | open url image1

Reich PB, Tjoelker MG, Walters MB, Vanderklein DW, Bushena C (1998) Close association of RGR, leaf and root morphology, seed mass and shade tolerance in seedlings of nine boreal tree species grown in high and low light. Functional Ecology 12, 327–338.
Crossref | GoogleScholarGoogle Scholar | open url image1

Ruiz-Robleto J, Villar R (2005) Relative growth rate and biomass allocation in ten woody species with different leaf longevity using phylogenetic independent contrasts PICs. Plant Biology 7, 484–494.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Sack L (2004) Responses of temperate woody seedlings to shade and drought: do trade-offs limit potential niche differentiation? Oikos 107, 110–127.
Crossref | GoogleScholarGoogle Scholar | open url image1

Sack L, Grubb PJ (2001) Why do species of woody seedlings change rank in relative growth rate between low and high irradiance? Functional Ecology 15, 145–154.
Crossref | GoogleScholarGoogle Scholar | open url image1

Sack L, Grubb PJ (2002) The combined impacts of deep shade and drought on the growth and biomass allocation of shade-tolerant woody seedlings. Oecologia 131, 175–185.
Crossref | GoogleScholarGoogle Scholar | open url image1

Sack L, Grubb PJ, Marañón T (2003) The functional morphology of juvenile plants tolerant of strong summer drought in shaded forest understories in southern Spain. Plant Ecology 168, 139–163.
Crossref | GoogleScholarGoogle Scholar | open url image1

Sánchez-Gómez D, Valladares F, Zavala MA (2006) Performance of seedlings of Mediterranean woody species under experimental gradients of irradiance and water availability: trade-offs and evidence for niche differentiation. New Phytologist 170, 795–806.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Shipley B (2000) ‘Cause and correlation in biology. A user’s guide to path analysis, structural equations and causal inference.’ (Cambridge University Press: Cambridge)

Shipley B (2002) Trade-offs between net assimilation rate and specific leaf area in determining relative growth rate: relationship with daily irradiance. Functional Ecology 16, 682–689.
Crossref | GoogleScholarGoogle Scholar | open url image1

Shipley B (2006) Net assimilation rate, specific leaf area and leaf mass ratio: which is most closely correlated with relative growth rate? A meta-analysis. Functional Ecology 20, 565–574.
Crossref | GoogleScholarGoogle Scholar | open url image1

Smith T, Huston M (1989) A theory of the spatial and temporal dynamics of plant communities. Vegetatio 83, 49–69.
Crossref | GoogleScholarGoogle Scholar | open url image1

Takashima T, Hikosaka K, Hirose T (2004) Photosynthesis or persistence: nitrogen allocation in leaves of evergreen and deciduous Quercus species. Plant, Cell & Environment 27, 1047–1054.
Crossref | GoogleScholarGoogle Scholar | open url image1

Tattini M, Guido L, Morassi-Bonzi L, Pinelli 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 Phillyrea latifolia to high solar radiation. New Phytologist 167, 457–470.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Thornley JHM (1976) ‘Mathematical models in plant physiology.’ (Academic Press: New York)

Valladares F (2003) Light heterogeneity and plants: from ecophysiology to species coexistence and biodiversity. In ‘Progress in botany’. (Eds K Esser, U Lüttge, W Beyschlag, J Murata) pp. 439–471. (Springer-Verlag: Heidelberg)

Valladares F, Pearcy RW (2002) Drought can be more critical in the shade than in the sun: a field study of carbon gain and photo-inhibition in a Californian shrub during a dry El Niño year. Plant, Cell & Environment 25, 749–759.
Crossref | GoogleScholarGoogle Scholar | open url image1

Van Andel J , Biere A (1989) Ecological significance of variability in growth rate and plant productivity. In ‘Causes and consequences of variation in growth rate and productivity of higher plants’. (Eds H Lambers, ML Cambridge, H Konings, TL Pons) pp. 257–268. (SPB Academic Publishing Company: Amsterdam)

Veenendaal EM, Swaine MD, Agyeman VK, Blay D, Abebrese IK, Mullins CE (1996) Differences in plant and soil water relations in and around a forest gap in West Africa during the dry season may influence seedling establishment and survival. Journal of Ecology 83, 83–90. open url image1

Villar R, Held AA, Merino J (1995) Dark leaf respiration in light and darkness of an evergreen and a deciduous plant species. Plant Physiology 107, 421–427.
PubMed |
open url image1

Villar R , Ruiz-Robleto J , Quero JL , Poorter H , Valladares F , Marañón T (2004) Tasas de crecimiento en especies leñosas: aspectos funcionales e implicaciones ecológicas. In ‘Ecología del bosque mediterráneo en un mundo cambiante’. (Ed. F Valladares) pp. 191–227. (Ministerio de Medio Ambiente: Madrid)

Villar R, Marañón T, Quero JL, Panadero P, Arenas F, Lambers H (2005) Variation in relative growth rate of 20 Aegilops species (Poaceae) in the field: the importance of net assimilation rate or specific leaf area depends on the time scale. Plant and Soil 272, 11–27.
Crossref | GoogleScholarGoogle Scholar | open url image1

Walters MB, Reich PB (1999) Low-light carbon balance and shade tolerance in the seedlings of woody plants: do winter deciduous and broad-leaved evergreen species differ? New Phytologist 143, 143–154.
Crossref | GoogleScholarGoogle Scholar | open url image1

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

Zar JH (1984) ‘Biostatistical analysis.’ (Prentice Hall: Englewood Cliffs, NJ)

Zavala MA, de la Parra RB (2005) A mechanistic model of tree competition and facilitation for Mediterranean forests: scaling from leaf physiology to stand dynamics. Ecological Modelling 188, 76–92.
Crossref | GoogleScholarGoogle Scholar | open url image1