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Ontogenetic Variation in Light Requirements of Juvenile Rainforest

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Ontogenetic Variation in Light Requirements of Juvenile Rainforest Functional Ecology 2008, 22, 454–459 doi: 10.1111/j.1365-2435.2008.01384.x OntogeneticBlackwell Publishing Ltd variation in light requirements of juvenile rainforest evergreens C. H. Lusk*,1, D. S. Falster1, C. K. Jara-Vergara2, M. Jimenez-Castillo2, A. Saldaña-Mendoza3 1Department of Biological Sciences, Macquarie University, NSW 2109, Australia; 2Nucleo FORECOS, Facultad de Ciencias Forestales, Universidad Austral de Chile, Valdivia, Chile; and 3Departamento de Botánica, Universidad de Concepción, Concepción, Chile Summary 1. Although shade tolerance is often assumed to be a fixed trait of species, recent work has reported size-related changes in the relative and absolute light requirements of woody taxa. We hypothesized that, in evergreen forests, light requirements of shade-tolerant species that accumulate multiple foliage cohorts will be more stable during juvenile ontogeny than those of intolerant species with short leaf lifetimes. 2. We quantified the light environments occupied by three size classes of 13 coexisting evergreens in a temperate rainforest, to determine how size influenced their relative shade tolerance. Minimum light requirements (MLRs) of species were estimated by computing the 10th percentile of the distribution of juveniles in relation to percentage canopy openness, for each size class. Leaf life span in low light (2%–5% canopy openness) was estimated by recording survival of marked leaves over 12 months, or retrospectively on species with clearly discernible foliage cohorts. 3. Agreement of ranks of species’ MLR across size classes was significant, although not strong (Kendall’s W = 0·159, P = 0·02). MLRs of the most shade-tolerant species changed little between size-classes, whereas those of most of the less-tolerant species rose with increasing size. 4. Shift in MLR across size-classes was negatively correlated with leaf life span, possibly because of the effects of leaf life span on biomass distribution and whole-plant carbon balance. Survival of light-demanding species with short leaf lifetimes may thus depend on their encountering increasing light levels as they grow taller, whereas progressive accumulation of an extensive leaf area by late-successional taxa enables them to continue to tolerate low light despite increasing size. 5. Results suggest that shade-tolerance differences between evergreens become increasingly apparent with increasing size. In identifying a relationship with leaf life span, this work also provides a basis for predicting changes in species’ light requirements during juvenile ontogeny. Key-words: canopy openness, sapling, seedling, shade tolerance, temperate rainforest scale (Montgomery & Chazdon 2002; Poorter & Arets Introduction 2003). In some temperate regions, foresters and ecologists have Interspecific variation in light requirements is widely regarded devised shade tolerance scales based on semi-quantitative as one of the most important aspects of functional diversity or subjective assessments (Fowells 1965; Donoso 1989; in woody plant communities (Wright 2002; Reich et al. 2003; Ellenberg 1991). More recently, shade tolerance variation has Gilbert et al. 2006). Succession in humid forests arises mainly been approached more quantitatively by monitoring survival because of a well-documented trade-off between survival rates in low light (Kitajima 1994; Kobe et al. 1995; Lusk 2002) in low light and growth under open conditions (Kobe et al. or by comparing the range of light environments naturally 1995; Wright 2002), and as old-growth forests are a shifting occupied by juveniles of different species (Davies 1998; Lusk mosaic of light environments, differences in shade tolerance & Reich 2000). contribute to the maintenance of species richness at landscape Shade tolerance is often tacitly assumed to be a fixed trait of species, both in classifications devised by foresters and ecologists (Fowells 1965; Ellenberg 1991), and in attempts to *Correspondence author. E-mail: [email protected] explain species coexistence on the basis of light gradient © 2008 The Authors. Journal compilation © 2008 British Ecological Society Ontogenetic change in light requirements 455 partitioning (Hubbell et al. 1999). However, there is evidence Materials and methods that both absolute and relative light requirements of species can change during development. Givnish (1988) argued that whole-plant light compensation points must increase SPECIES DISTRIBUTIONS IN RELATION TO CANOPY as woody plants grow bigger, due to a declining ratio of OPENNESS autotrophic to heterotrophic tissues, and mechanical require- Sampling was carried out in the low-altitude forests (350–440 m ments for increasing allocation to stem construction. The a.s.l.) of Parque Nacional Puyehue (40°39′ S, 72°11′ W) located in allometry of juvenile trees is often inconsistent with the latter the western foothills of the Andean range in south-central Chile. of Givnish’s arguments (Niklas 1995; Lusk et al. 2006b), This area experiences a maritime temperate climate, with an average and we are not aware of empirical tests of the hypothesized annual precipitation of around 3500 mm (Almeyda & Saez 1958). increase in compensation points. However, monitoring of The old-growth rainforest at this altitude on the western foothills of the Andes is comprised exclusively of broad-leaved evergreens juvenile trees in a West African rainforest showed that (Lusk, Chazdon & Hofmann 2006a). individuals of most species tended to occupy brighter Distributions of juvenile trees were quantified in relation to environments as they grew taller (Poorter et al. 2005). There canopy openness measurements made with a pair of LAI-2000 are also reports of ontogenetic rank changes in the average canopy analysers (Li-Cor, Lincoln, NE). One instrument was used light environments occupied by coexisting species (Clark & to take measurements at each sampling point, while the other, placed Clark 1992; Poorter et al. 2005), and in low light survival at the centre of a 2-ha clearing, was programmed to take readings at (Kneeshaw et al. 2006). If such cross-overs were widespread, 30-s intervals. Integration of data from the two instruments enabled a multi-dimensional view of species light requirements might estimation of percentage diffuse irradiance at each sampling point be required to understand forest dynamics, and species within the forest, equivalent to percentage of canopy openness over coexistence in old-growth forests (Grubb 1977; Poorter et al. the quasi-hemispherical (148º) field of view perceived by the LAI- 2005). This idea is disputed by Gilbert et al. (2006), who found 2000 sensors. Measurements were made on overcast days, using the full 148º field of view, over a period of about 4 years from 2000 to that seedlings and saplings of Neotropical woody plants 2003. Measurements with the LAI-2000 are a good surrogate of showed similar growth-survival trade-offs at seedling and spatial variation in mean daily photosynthetic photon flux density sapling stages, despite extensive rank changes. within a stand (Machado & Reich 1999). Interspecific differences in leaf life span might be expected Sampling was carried out on a series of transects run through to influence ontogenetic variation in light requirements of old-growth stands including tree-fall gaps of varied sizes. Sets of broadleaved evergreens (King 1994; Lusk 2004). Young parallel transects were run through accessible stands, spaced at least seedlings of pioneer species often develop a large ratio of leaf 20 m apart, the angle and number of transects depending on terrain, area to plant biomass (leaf area ratio, LAR), leading to access considerations and proximity to forest margins. At 1608 favourable short-term carbon balance and relatively rapid sample points spaced at random intervals (2–10 m apart) along growth even in low light (Kitajima 1994; Walters & Reich transects, canopy openness measurements were made at 50, 100 and 1999; Lusk 2004). However, their short leaf lifetimes lead to a 200 cm height with the LAI-2000. Presence of tree and large shrub species was recorded in three height classes in a circular plot of 1-m steep ontogenetic decline in low light LAR (Lusk 2004), because diameter, centred on the sample point. Juveniles 10–50 cm tall were in the understorey they are unable to compensate their high recorded as associated with the light level measured at 50 cm of height. leaf loss rates (due to senescence, herbivory and mechanical Juveniles 50–100 cm tall were referred to the light level measured at damage) with high leaf production rates (Bongers & Popma 100 cm of height, and individuals 100–200 cm tall were referred 1990; Lusk 2002). Whole-plant light compensation points to the light level measured at 200 cm of height. Although up to 20 (Givnish 1988) of such taxa therefore seem likely to increase individuals of some species were found in some plots, only presence rapidly as they grow larger. Species with long-lived leaves, on or absence data are used in the present analysis. the other hand, are better able to conserve their ratio of leaf One of the study species (Eucryphia) frequently reproduces by area to biomass as they grow bigger, through accumulation of basal shoots and root suckers as well as seedlings (Donoso, Escobar many overlapping leaf cohorts: this pattern is seen in late- & Urrutia 1985). For the purposes of evaluating light requirements in successional shade-tolerant evergreens (Lusk 2004). Light the present study, however, we counted only juveniles of seedling origin. requirements
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