Ontogenetic Variation in Light Requirements of Juvenile Rainforest

Home , Shade tolerance

Functional Ecology 2008, 22, 454–459 doi: 10.1111/j.1365-2435.2008.01384.x BlackwellOntogenetic 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

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 of these species might therefore be expected to be more ontogenetically stable than those of pioneer species QUANTIFYING MINIMUM LIGHT REQUIREMENTS with short leaf lifetimes. (MLRS) Here we relate ontogenetic variation in shade tolerance to leaf life span differences among 13 coexisting evergreens in a The 10th percentile of the distribution of each species in relation to temperate rainforest. We compared the minimum light levels light availability (percentage of canopy openness) was used as an approximation of the lowest light levels tolerated by each species naturally occupied by three juvenile size classes of the 13 spe- (Fig. 1). This parameter, referred to hereafter as the MLR, was cal- cies, and measured leaf life span in low light. We addressed culated for each size class of each species. Only species represented three questions: (i) Do light requirements vary significantly in each size class on at least 20 sampling plots were considered. We between size classes? (ii) Do species’ ranks change significantly stress that our scores are an inversion of traditional shade tolerance between size classes? (iii) Is the magnitude of any ontogenetic ratings (Donoso 1989) that is, shade-tolerant taxa such as Myrceu- shift in minimum light requirements (MLRs) correlated with genia planipes have low values for this index, and light-demanders interspecific variation in leaf life span? such as Aristotelia chilensis score high (Fig. 1).

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Table 1. Leaf life spans (mean ± SE) of saplings in low light (2%–5% canopy openness), and results of resampling tests for signiﬁcant variation in MLRs across three height classes (10–50, 50–100, 100–200 cm) of each of 13 species. MLRs were computed as the 10th percentile of the distribution of light environments (percentage of canopy openness) occupied by each height class

P-values for height class comparisons Leaf life span (year) Species (mean ± SE) 1 vs. 3 1 vs. 2 2 vs. 3

Aristotelia chilensis (Elaeocarpaceae) 0·8 ± 0·1 0·006 0·178 0·02 Azara lanceolata (Flacourtiaceae) 2·2 ± 0·3 < 0·001 < 0·001 0·097 Dasyphyllum diacanthoides (Asteraceae) 2·7 ± 0·4 < 0·001 0·017 0·237 Eucryphia cordifolia (Cunionaceae) 2·8 ± 0·2 0·697 0·907 0·59 Lomatia ferruginea (Proteaceae) 2·8 ± 0·3 0·029 0·956 0·055 Caldcluvia paniculata (Cunoniaceae) 2·9 ± 0·2 0·009 0·574 0·054 Amomyrtus luma (Myrtaceae) 3·3 ± 0·3 < 0·001 < 0·001 0·091 Rhaphithamnus spinosus (Verbenaceae) 3·6 ± 0·4 0·201 0·087 0·679 Luma apiculata (Myrtaceae) 3·8 ± 0·2 0·003 0·023 0·343 Laureliopsis philippiana (Atherospermataceae) 4·7 ± 0·6 0·832 0·997 0·834 Myrceugenia planipes (Myrtaceae) 5·0 ± 0·2 0·132 0·239 0·645 Gevuina avellana (Proteaceae) 5·2 ± 0·4 0·231 0·628 0·544 Aextoxicon punctatum (Aextoxicaceae) 5·3 ± 0·3 0·53 0·958 0·562

three size classes, as an indicator of MLR. The absolute difference (corresponding to a two-tail test) in MLR among size classes was then taken as an indicator of changing light requirements. To estimate the significance of observed differences, light levels were rand- omized among size classes and differences in MLR recalculated. This procedure was repeated 1000 times. The proportion of samples showing greater than observed difference between each pairwise combination of size classes gives the probability that such a difference between size classes could arise by chance (Table 1). Kendall’s coefficient of concordance was used to test significance of agreement of species MLR ranks across size classes.

LEAF LIFE SPAN

Leaf life spans of 11 of the 13 species were estimated by monitoring leaf survival over 12 months. All leaves were marked on the main stem of five to six 100–200-cm tall saplings of each species, growing at microsites with 2%–5% canopy openness as measured by the LAI-2000. Plants were relocated 12 months later, and leaf mortality during this period used to estimate average leaf life span. As leaf longevities were < 1 year on most individuals of A. chilensis, abscission scars were counted to determine mortality of new leaves initiated after the start of the study period. Leaf longevity (year) was estimated as:

ni Fig. 1. MLRs of three juvenile size classes of 13 evergreens in a Chilean −+ (nnif ) m n rainforest. Solid lines denote species with statistically signiﬁcant changes (P < 0·05) in MLR between the smallest and largest height where n = initial number of leaves, n = final number surviving from classes; dotted lines indicate no signiﬁcant change across this size range. i f = ni, and mn mortality of new leaves initiated since the first census. Static demographic methods were used estimate leaf life spans of the other two species, Eucryphia cordifolia and Dasyphyllum diacan- STATISTICAL ANALYSIS thoides. The end of previous seasons’ extension growth in these We used a resampling approach to test for significant variation in species is marked by persistent cataphylls (E. cordifolia) or by resting MLR of each species across size classes (Table 1). The distribution bud scars which remain visible for several years (D. diacanthoides), of light environment data was normalized by log 10 transformation permitting reconstruction of recent growth history and ready before analysis. For each species, we computed the 10th percentile delimitation of foliage cohorts. We estimated mean leaf life spans of of the distribution of light environments occupied by each of the these species by inspecting 10 saplings growing at microsites with

Ontogenetic change in light requirements 457

Fig. 2. Correlation of leaf life span with MLRs of rainforest Fig. 3. Correlation of leaf life span with proportional change in evergreens in three height classes. Black symbols and solid line show MLRs across three height classes. relationship for 10–50-cm tall juveniles (r = 0·60, P = 0·032). Grey symbols and long-dashed line = 50–100 cm tall juveniles (r = 0·83, P < 0·0001). White symbols and short-dashed line = 100–200-cm tall juveniles (r = 0·88, P < 0·0001). could be attributed to random variation and small sample sizes, the more substantial rank changes shown by Azara lanceolata suggest a stronger upward trend in MLR than those 2%–5% canopy openness as measured by the LAI-2000, and deter- of any of its associates. We are aware of few published data mining the age of the youngest foliage cohort that had undergone directly comparable to ours. A somewhat different problem is c. 50% mortality. Estimates of mean leaf life span were averaged for addressed by studies documenting variation in the average the 10 individuals of each species. light environments occupied by suites of tree species during the course of their lives (Clark & Clark 1992; Poorter et al. 2005). Many of the rank changes in those studies appeared to Results reflect differences in maximum height, with short-statured Agreement of ranks of species’ MLRs across size classes was species eventually being overtopped by taller ones (Clark & significant, although not strong (Kendall’s W = 0·159, P = 0·02). Clark 1992; Poorter et al. 2005). However, physiological MLRs of seven species increased significantly between mechanisms similar to those discussed in the present study height classes 1 and 3 (Fig 1; Table 1). The other six species, could also have some influence on their results. A study of 31 which showed no significant ontogenetic variation, included Neotropical evergreens (Gilbert et al. 2006) showed that the three most shade-tolerant trees in this forest (M. planipes, seedling survival of was strongly correlated overall with survival Aextoxicon punctatum, Laureliopsis philippiana), which of the same taxa at the sapling stage, despite numerous (and occupied the lowest three rankings in the largest size class. sometimes substantial) rank changes between size classes. Interspecific variation in MLRs was thus wider in the largest However, Gilbert et al. (2006) did not compare species’ survival height class (log-variance = 0·051), than in the medium (log- in a common light environment, nor were light environments variance = 0·023) and small (log-variance = 0·027) height class. standardized between the two size classes, making it difficult Leaf life spans ranged from < 1 year in A. chilensis to to compare our results directly with theirs. ≥ 5 years in Gevuina avellana and A. punctatum (Table 1). The effect of size on light requirements appeared to depend Leaf life spans were negatively correlated with MLR in all size on species’ successional status. Species considered or shown classes (Fig. 2). However, in the smallest size class the corre- to be tolerant of shade, especially M. planipes, A. punctatum lation was modest (r = 0·60) and driven mainly by one outlier, and L. philippiana (Donoso 1989; Figueroa & Lusk 2001; Lusk A. chilensis (Fig. 2). The correlation between leaf life span 2002), had low MLRs, which did not change significantly and MLR became progressively stronger with increasing size, between height classes (Fig. 1, Table 1). In contrast, MLRs of rising to 0·88 in the largest size class (Fig. 2). As a result, leaf most of the less-tolerant species underwent ontogenetic life span was negatively correlated with proportional change increases (Fig. 1). Light requirements of the 13 species were in MLR across the three size classes (Fig. 3). thus most clearly differentiated in the largest size class. Again there are few directly comparable data: Kneeshaw et al. (2006) found that shade-tolerance differences between seven Discussion boreal tree species became slightly less marked with increasing Although most species underwent rank changes, there was size, although that study was based on variation in survival significant agreement of species light requirements across rates at a given growth rate, rather than the range of light height classes (Fig. 1). While some of the minor rank changes environments naturally occupied by species.

Ontogenetic changes in light requirements were correlated grow taller. Self-shading is likely to reduce the efficiency with interspecific variation in leaf life span (Figs 2 and 3). The of light interception as plants grow taller (Lusk et al. 2006b), accretion of multiple leaf cohorts by shade-tolerant evergreens although some broadleaved species are surprisingly adept at (Williams, Field & Mooney 1989; King 1994; Lusk 2002), minimizing self-shading by repositioning old leaves through plus a probable ontogenetic decline in allocation to roots bending of petioles, with substantial consequences for carbon (Lusk 2004), enables these species to maintain their LAR as gain (Gálvez & Pearcy 2003). Different architectural models seedlings grow larger (Lusk 2004). This suggests conservation (Hallé, Oldeman & Tomlinson 1978) could also have differing of the relationship of carbon gain to respiratory demands, consequences for the allometry of light interception, and although progressive loss of older leaf cohorts in juveniles hence for ontogenetic variation in light requirements. Finally, > 1 m tall means that this isometry of leaf area with plant ontogenetic trends in herbivory could also influence both the biomass cannot continue indefinitely. In contrast, light- absolute and relative light requirements of species. Herbivore demanding species such as A. chilensis and A. lanceolata have pressure has been shown to significantly influence light more marked differences between turnover rates of foliage requirements (DeWalt, Denslow & Ickes 2004); if increasing and woody tissues (Bongers & Popma 1990; Lusk 2004). In size makes plants more attractive to vertebrate herbivores shaded understoreys, where their relatively fast foliage (Boege & Marquis 2005), their impact could contribute to turnover cannot be compensated by high leaf production ontogenetic increases in the MLRs of species with short- rates, increasing age and size of light-demanding evergreens lived, relatively palatable foliage. must thus inevitably be associated with an increasing ratio of If differences in leaf life span do drive ontogenetic heterotrophic to autotrophic tissues. In order to survive, they divergence in the behaviour of light-demanding and shade- must therefore encounter increasing light levels as they grow tolerant species, there is no reason to expect such a pattern in taller, enabling higher carbon gain per unit leaf area. deciduous forests. The gulf between turnover rates of foliage Our approach of relating the distribution of juvenile trees and woody tissues in all deciduous species should result in an to present canopy openness may slightly underestimate ontogenetic decline in LAR, irrespective of shade tolerance MLRs (Lusk et al. 2006a). Because of the dynamic nature of level. Light requirements of all deciduous trees should forest light environments, some individuals were probably therefore increase as they grow taller. Kneeshaw et al. (2006) sampled in light environments below their whole-plant light reported that saplings of four out of five boreal deciduous compensation points, as carbohydrate reserves could enable trees had lower understorey survival than conspecific juvenile trees to persist for some time in light environments in seedlings, although their expression of survival in function of which their net carbon gain is negative. As there is evidence growth (rather than light availability) makes comparisons that shade-tolerant species have larger carbohydrate reserves problematic. than their light-demanding associates (Poorter & Kitajima Evergreen conifers are likely to show a different pattern 2007; but see Lusk & Piper 2007), this sort of underestimation again. Small leaves and lack of petiole development make it could be greater in the former, leading to an over-estimation difficult for conifers to accumulate multiple leaf cohorts of species differences in MLR. However, this sort of error without incurring considerable self-shading (Lusk et al. 2006b). would not affect our conclusions about ontogenetic trends. Thus, although some conifers accumulate as many as 20 It is unlikely that spatial autocorrelation of forest light foliage cohorts (Lusk 2001), and are able to conserve their environments has any bearing on our conclusions. Nicotra, LAR for many years during juvenile ontogeny (Lusk et al. 2006b), Chazdon & Iriarte (1999) found that light environments in an this does not necessarily translate into isometry of light inter- old-growth tropical rainforest showed spatial dependence ception and carbon gain with plant mass. Light requirements at scales of up to 25 m. This scale of pattern suggests some of most evergreen conifers therefore seem likely to rise with degree of dependence between successive observations increasing size, although this ontogenetic trend may be steeper spaced 2–10 m apart on our transects. If some species (e.g. in light-demanders than in shade-tolerant taxa. those with large seeds) are more clumped than others Understanding coexistence of tree species, and develop- (Dalling, Hubbell & Silvera 1998), spatial autocorrelation of ment of silvicultural programs in mixed forests, will require light environments will not affect all species equally. However, knowledge of species light requirements throughout their it is not evident how this sort of pattern could influence our developmental trajectories (Poorter et al. 2005). This paper measurements of ontogenetic variation in species’ light shows that work on saplings can detect shade tolerance requirements. differences not evident from comparisons of seedlings, but Other traits besides leaf life span could also influence which may nevertheless have considerable bearing on forest ontogenetic shifts in light requirements. Leaf mass per area regeneration patterns. In identifying a relationship with leaf increases during juvenile ontogeny (Sack, Maranon & Grubb life span, this work also provides a basis for predicting changes 2002; Lusk 2004), at least partly as a result of increasing leaf in species’ light requirements during juvenile ontogeny. thickness (Kenzo et al. 2006). Unless offset by shifts in other traits (e.g. declining allocation to roots), the higher Acknowledgements respiration rates associated with thicker leaves, as well as the We thank FONDECYT for support through grant no. 1980084, CONAF for rising cost of producing photosynthetic surface area, are likely facilitating access to Parque Nacional Puyehue, and an anonymous reviewer to inflate whole-plant light compensation points as plants for constructive criticism.

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