Size‐Dependent Variation in Shoot Light‐Harvesting Efficiency in Shade‐Intolerant Conifers

Shoots and foliage elements of shade‐intolerant conifers strongly vary in size, but the effects of size on shoot light‐harvesting efficiency have not been quantified. We investigated shoot adaptation to seasonal average integrated quantum flux density in gymnosperms Pinus palustris Mill., P. patula Schlect. & Cham., and P. radiata D. Don. and angiosperm Casuarina glauca Sieb. ex Spreng. In addition, P. sylvestris L., sampled from infertile and fertile sites, and P. taeda L. were included to test for general correlations among shoot architecture and size. All studied species possess needle‐like photosynthetic elements. A shoot model was fitted to the data to separate the determinants of shoot light‐harvesting efficiency. The model estimated shoot light harvesting on the basis of angular distribution of foliage surface areas, degree of spatial clumping, foliage area density in shoot volume, and beam path length in shoot volume. Increases in irradiance primarily led to greater foliage aggregation, greater foliage area density in shoot volume, and to a minor degree, to changes in foliage area angular distribution. Greater foliage aggregation resulted in lower efficiency of light harvesting but greater investment of foliar biomass in high light where the photosynthetic returns are greater. The species behave similarly except that the light‐harvesting characteristics of P. patula, which has long, strongly bending needles, were independent of light. In all species, the shoots were larger in higher irradiance, and the fraction of biomass in shoot axis increased with increasing irradiance, indicating greater costs for light harvesting in high light. There were further significant species differences in light‐harvesting efficiency that were linked to differences in foliage and shoot size. Foliage element length varied between 1.1 and 31.4 cm and shoot axis length between 1.2 and 36.5 cm among the species, leading to 4 orders of magnitude variation in shoot cylinder volume and three orders of magnitude variation in foliage area density (ρ); ρ decreased with increasing foliage element length and shoot volume. The degree of foliage clumping scaled positively with ρ and negatively with foliage element length. Foliage clumping was positively associated with foliage dry mass to shoot silhouette area ratio, signifying a trade‐off between efficient light harvesting and large photosynthetic biomass accumulation. These data demonstrate a general increase of light‐harvesting efficiency with increasing length of foliage elements, but they also demonstrate that this increase is limited by enhanced bending of longer foliage elements and by augmented support costs.

[1]  M. Agrawal,et al.  Litterfall, litter decomposition and nutrient release in five exotic plant species planted on coal mine spoils , 2001 .

[2]  P. Stenberg,et al.  Importance of needle age and shoot structure on canopy net photosynthesis of balsam fir (Abies balsamea): a spatially inexplicit modeling analysis. , 2001, Tree physiology.

[3]  H. L. Allen,et al.  An Investigation of the Impacts of Elevated Carbon Dioxide, Irrigation, and Fertilization on the Physiology and Growth of Loblolly Pine , 1998 .

[4]  F. James Rohlf,et al.  Biometry: The Principles and Practice of Statistics in Biological Research , 1969 .

[5]  Eshetu Yirdaw,et al.  Photosynthetically active radiation transmittance of forest plantation canopies in the Ethiopian highlands , 2004 .

[6]  M. Battaglia.  The Influence of Overstory Structure on Understory Light Availability in a Longleaf Pine (Pinus palustris Mill.) Forest , 2000 .

[7]  M. Shelton,et al.  Regenerating uneven-aged stands of loblolly and shortleaf pines: the current state of knowledge , 2000 .

[8]  J. Duivenvoorden,et al.  Strong effects of a plantation with Pinus patula on Andean subpáramo vegetation: a case study from Colombia , 2003 .

[9]  Fernando Valladares,et al.  Convergence in light capture efficiencies among tropical forest understory plants with contrasting crown architectures: a case of morphological compensation. , 2002, American journal of botany.

[10]  D. Brockway,et al.  Gap-phase regeneration in longleaf pine wiregrass ecosystems , 1998 .

[11]  D. Ellsworth.  Seasonal CO(2) assimilation and stomatal limitations in a Pinus taeda canopy. , 2000, Tree physiology.

[12]  F. Bazzaz,et al.  Trade-off Between Light- and Nitrogen-use Efficiency in Canopy Photosynthesis , 1998 .

[13]  Alessandro Cescatti,et al.  Light capture efficiency decreases with increasing tree age and size in the southern hemisphere gymnosperm Agathis australis , 2005, Trees.

[14]  R. Zorer,et al.  Structural acclimation and radiation regime of silver fir (Abies alba Mill.) shoots along a light gradient , 2003 .

[15]  J. Monteith,et al.  The Radiation Regime and Architecture of Plant Stands. , 1983 .

[16]  Hiroyuki Muraoka,et al.  Crown architecture in sun and shade environments: assessing function and trade-offs with a three-dimensional simulation model. , 2005, The New phytologist.

[17]  F. Valladares.  Light Heterogeneity and Plants: from Ecophysiology to Species Coexistence and Biodiversity , 2003 .

[18]  P. Stenberg,et al.  Shoot structure, canopy openness, and light interception in Norway spruce , 1999 .

[19]  M. Warren,et al.  Soil macrofauna and litter nutrients in three tropical tree plantations on a disturbed site in Puerto Rico , 2002 .

[20]  K. Langeland.  Identification and biology of nonnative plants in Florida's natural areas , 2008 .

[21]  Phillip M. Dougherty,et al.  Effect of carbon dioxide, fertilization and irrigation on loblolly pine branch morphology , 1997, Trees.

[22]  J. Ross.  The radiation regime and architecture of plant stands , 1981, Tasks for vegetation sciences 3.

[23]  Ü. Niinemets,et al.  Structural determinants of leaf light-harvesting capacity and photosynthetic potentials , 2006 .

[24]  D. Richardson.  Forestry Trees as Invasive Aliens , 1998 .

[25]  S. Linder.  Responses to Water and Nutrients in Coniferous Ecosystems , 1987 .

[26]  D. Teketay,et al.  Effects of canopy cover and understory environment of tree plantations on richness, density and size of colonizing woody species in southern Ethiopia , 2004 .

[27]  Pauline Stenberg,et al.  Shoot structure, light interception, and distribution of nitrogen in an Abies amabilis canopy. , 1998, Tree physiology.

[28]  Vertical gradients and tree-to-tree variation in shoot morphology and foliar nitrogen in an old-growth Pinus strobus stand , 2003 .

[29]  Alessandro Cescatti,et al.  Constraints on light interception efficiency due to shoot architecture in broad-leaved Nothofagus species. , 2004, Tree physiology.

[30]  J. Chen,et al.  Defining leaf area index for non‐flat leaves , 1992 .

[31]  D. Sprugel,et al.  Effects of light on shoot geometry and needle morphology in Abies amabilis. , 1996, Tree physiology.

[32]  Fernando Valladares,et al.  Tradeoffs Between Irradiance Capture and Avoidance in Semi-arid Environments Assessed with a Crown Architecture Model , 1999 .

[33]  Ülo Niinemets,et al.  Total foliar area and average leaf age may be more strongly associated with branching frequency than with leaf longevity in temperate conifers , 2003 .

[34]  D. Richardson,et al.  Ecology and biogeography of Pinus: an introduction , 1998 .

[35]  D. Ellsworth,et al.  Dependence of needle architecture and chemical composition on canopy light availability in three North American Pinus species with contrasting needle length. , 2002, Tree physiology.

[36]  Robert W. Pearcy,et al.  The functional morphology of light capture and carbon gain in the Redwood forest understorey plant Adenocaulon bicolor Hook , 1998 .

[37]  K. Rajendran,et al.  Biomass and nutrient distribution and their return of Casuarina equisetifolia inoculated with biofertilizers in farm land , 2004 .

[38]  T. Nilson.  A theoretical analysis of the frequency of gaps in plant stands , 1971 .

[39]  Ü. Niinemets,et al.  Site fertility and the morphological and photosynthetic acclimation of Pinus sylvestris needles to light. , 2001, Tree physiology.

[40]  Ülo Niinemets,et al.  Effects of light availability and tree size on the architecture of assimilative surface in the canopy of Picea abies: variation in shoot structure , 1995 .

[41]  K. Niklas.  Biomechanical Attributes of the Leaves of Pine Species , 1991 .

[42]  A. Takenaka,et al.  Effects of leaf blade narrowness and petiole length on the light capture efficiency of a shoot , 1994, Ecological Research.

[43]  Alessandro Cescatti,et al.  Modification of light-acclimation of Pinus sylvestris shoot architecture by site fertility , 2002 .

[44]  L. López-Mata,et al.  The Pines of Mexico and Central America , 1991 .

[45]  Stephen L. Rathbun,et al.  The Population Dynamics of a Long-Lived Conifer (Pinus palustris) , 1988, The American Naturalist.

[46]  Ü. Niinemets,et al.  Light-acclimation of cladode photosynthetic potentials in Casuarina glauca: trade-offs between physiological and structural investments. , 2005, Functional plant biology : FPB.

[47]  J. D. Rienzo,et al.  Basal area growth curves for Pinus patula in two areas of the Calamuchita Valley, Córdoba, Argentina , 1999 .

[48]  G. Campbell.  Extinction coefficients for radiation in plant canopies calculated using an ellipsoidal inclination angle distribution , 1986 .

[49]  P. Stenberg,et al.  Shoot structure and photosynthetic efficiency along the light gradient in a Scots pine canopy. , 2001, Tree physiology.

[50]  C. Critchley,et al.  Photosynthetic adaptation : chloroplast to landscape , 2004 .

[51]  Robert W. Pearcy,et al.  Plastic Phenotypic Response to Light of 16 Congeneric Shrubs From a Panamanian Rainforest , 2000 .

[52]  S. Hale,et al.  Comparison of film and digital hemispherical photography across a wide range of canopy densities , 2002 .

[53]  R. H. Berg.  A calcium oxalate-secreting tissue in branchlets of the Casuarinaceae , 1994, Protoplasma.

[54]  Robert A. Mickler,et al.  The Productivity and Sustainability of Southern Forest Ecosystems in a Changing Environment , 1998, Ecological Studies.