Biomass allocation and leaf life span in relation to light interception by tropical forest plants during the first years of secondary succession

Abstract

Journal of EcologyVolume 96, Issue 6 p. 1211-1221 Free Access Biomass allocation and leaf life span in relation to light interception by tropical forest plants during the first years of secondary succession N. Galia Selaya, N. Galia Selaya Section of Plant Ecology and Biodiversity, Institute of Environmental Biology, Utrecht University, P.O. Box 80084, 3508 TB Utrecht, The Netherlands; Programa Manejo de Bosques de la Amazonía Boliviana (PROMAB), Casilla 107, Riberalta, Bolivia;andSearch for more papers by this authorRoelof J. Oomen, Roelof J. Oomen Section of Plant Ecology and Biodiversity, Institute of Environmental Biology, Utrecht University, P.O. Box 80084, 3508 TB Utrecht, The Netherlands;Search for more papers by this authorJordie J. C. Netten, Jordie J. C. Netten Section of Plant Ecology and Biodiversity, Institute of Environmental Biology, Utrecht University, P.O. Box 80084, 3508 TB Utrecht, The Netherlands; Department of Aquatic Ecology and Water Quality Management, Wageningen University, P.O. Box 47, 6700 AA Wageningen, The NetherlandsSearch for more papers by this authorMarinus J. A. Werger, Marinus J. A. Werger Section of Plant Ecology and Biodiversity, Institute of Environmental Biology, Utrecht University, P.O. Box 80084, 3508 TB Utrecht, The Netherlands;Search for more papers by this authorNiels P. R. Anten, Corresponding Author Niels P. R. Anten Section of Plant Ecology and Biodiversity, Institute of Environmental Biology, Utrecht University, P.O. Box 80084, 3508 TB Utrecht, The Netherlands; *Correspondence author. E-mail: n.p.r.anten@uu.nlSearch for more papers by this author N. Galia Selaya, N. Galia Selaya Section of Plant Ecology and Biodiversity, Institute of Environmental Biology, Utrecht University, P.O. Box 80084, 3508 TB Utrecht, The Netherlands; Programa Manejo de Bosques de la Amazonía Boliviana (PROMAB), Casilla 107, Riberalta, Bolivia;andSearch for more papers by this authorRoelof J. Oomen, Roelof J. Oomen Section of Plant Ecology and Biodiversity, Institute of Environmental Biology, Utrecht University, P.O. Box 80084, 3508 TB Utrecht, The Netherlands;Search for more papers by this authorJordie J. C. Netten, Jordie J. C. Netten Section of Plant Ecology and Biodiversity, Institute of Environmental Biology, Utrecht University, P.O. Box 80084, 3508 TB Utrecht, The Netherlands; Department of Aquatic Ecology and Water Quality Management, Wageningen University, P.O. Box 47, 6700 AA Wageningen, The NetherlandsSearch for more papers by this authorMarinus J. A. Werger, Marinus J. A. Werger Section of Plant Ecology and Biodiversity, Institute of Environmental Biology, Utrecht University, P.O. Box 80084, 3508 TB Utrecht, The Netherlands;Search for more papers by this authorNiels P. R. Anten, Corresponding Author Niels P. R. Anten Section of Plant Ecology and Biodiversity, Institute of Environmental Biology, Utrecht University, P.O. Box 80084, 3508 TB Utrecht, The Netherlands; *Correspondence author. E-mail: n.p.r.anten@uu.nlSearch for more papers by this author First published: 15 October 2008 https://doi.org/10.1111/j.1365-2745.2008.01441.xCitations: 39AboutSectionsPDF ToolsRequest permissionExport citationAdd to favoritesTrack citation ShareShare Give accessShare full text accessShare full-text accessPlease review our Terms and Conditions of Use and check box below to share full-text version of article.I have read and accept the Wiley Online Library Terms and Conditions of UseShareable LinkUse the link below to share a full-text version of this article with your friends and colleagues. Learn more.Copy URL Share a linkShare onFacebookTwitterLinked InRedditWechat Summary 1 We related above-ground biomass allocation to light interception by trees and lianas growing in three tropical rain forest stands that were 0.5, 2 and 3-year-old regeneration stages after slash and burn agriculture. 2 Stem height and diameter, leaf angle, the vertical distribution of total above-ground biomass and leaf longevity were measured in individuals of three short-lived pioneers (SLP), four later successional species (LS) and three lianas (L). Daily light capture per individual (Φd) was calculated with a canopy model. Mean daily light interception per unit leaf area (Φarea), leaf mass (Φleaf mass) and above-ground mass (Φmass) were used as measures of instantaneous efficiency of biomass use for light capture. 3 With increasing stand age, vegetation height and leaf area index increased while light at the forest floor declined from 34 to 5%. The SLP, Trema micanthra and Ochroma pyramidale, dominated the canopy early in succession and became three times taller than the other species. SLP had lower leaf mass fractions and leaf area ratios than the other groups and this difference increased with stand age. 4 Over time, the SLP intercepted increasingly more light per unit leaf mass than the other species. Lianas, which in the earliest stage were self-supporting and started climbing later on, gradually became taller at a given mass and diameter than the trees. Yet, they were not more efficient than trees in light interception. 5 SLP had at least three-fold shorter leaf life spans than LS and lianas. Consequently, total light interception calculated over the mean life span of leaves (Φleaf mass total = Φarea × SLAdeath leaves× leaf longevity) was considerably lower for the SLP than for the other groups. 6 Synthesis. We suggest that early dominance in secondary forest is associated with a high rate of leaf turnover which in turn causes inefficient long-term use of biomass for light capture, whereas persistence in the shade is associated with long leaf life spans. This analysis shows how inherent tradeoffs in crown and leaf traits drive long-term competition for light, and it presents a conceptual tool to explain why early dominants are not also the long-term dominants. Introduction During the fallow period of slash-and-burn agriculture in tropical forests, both herbaceous and woody plant species rapidly colonize the site. Short-lived pioneer trees (SLP) establish early in succession and dominate the canopy throughout the first 10–20 years. Long-lived pioneer trees and some late successional species are also present from the early stage onwards, initially grow in the shade of the SLP but replace them in the top of the canopy later in succession (Whitmore 1989). Lianas are thought to be more abundant in early successional forest than in old growth forest (Putz 1984; De Walt et al. 2000). These changes in size probably result, in part, from differences in morphology and biomass investment patterns between species and from inherent differences in growth rates. In this study, we focus on the effects of differences in the morphology and investment patterns of species during the first 3 years of secondary succession. Vegetation height, leaf area index and basal area increase and light at the forest floor decreases as succession proceeds (Brown & Lugo 1990, Saldarriaga 1994; Peña-Claros 2003). Hence, competitive interactions for light probably play an important role in determining the course of succession (Werger et al. 2002). Species that are able to grow tall can deploy their foliage in the upper layers of the canopy and capture the greater part of available photosynthetically active radiation (Hirose & Werger 1995). Investment in height improves access to light but incurs construction and maintenance costs (Givnish 1982). Much research has focussed on understanding the mechanisms by which tree species differing widely in height coexist in tropical forest. Early studies (Horn 1971; Kohyama 1987; Kohyama & Hotta 1991) focussed on how crown structure influenced light acquisition. It was proposed that shade tolerant species should have shallow broad crowns with minimal leaf overlap thus maximizing light capture. Conversely, sun species should produce narrow crowns investing more of their resources in vertical growth by which they are better able to compete with neighbours and thus secure future light acquisition (Kohyama 1987; Kohyama & Hotta 1991; Sheil et al. 2006). Contrary to these predictions, later successional shade tolerant species are often found to have deeper crowns with more layers than pioneer species (e.g. Kitajima et al. 2005; Sterck et al. 2006). To maintain rapid growth, pioneers may have to shed older leaves and branches and reallocate resources to support new leaf growth in the canopy (Kikuzawa 1995; Kitajima et al. 1997, 2002; Hikosaka 2005; Boonman et al. 2006; Sterck et al. 2006), the result being a relatively shallow crown. For shade tolerant species the production of a broad crown may not only facilitate efficient light capture but may also entail additional costs of producing extra branches (Valladares et al. 2002). A further understanding of how light competition between species shapes succession requires a quantitative analysis relating biomass allocation, crown structure and biomass turnover to light acquisition. Hirose and Werger (1995) used a modelling approach to compare above-ground biomass expenditure to light acquisition for different species coexisting in a temperate grassland. They found that on a daily basis short subordinate species absorbed less light per unit of leaf area (Φarea) than did tall dominant species but equal or more light per unit of above-ground mass (Φmass) (Hirose & Werger 1995; Anten & Hirose 1999). Similar Φmass values between short and tall species were also observed in several young secondary tropical forest stands (Selaya et al. 2007; van Kuijk et al. 2008). However, this similarity in mass-use efficiency for light capture appears to be limited to relatively open stands (with LAI values of less than 2.5 to 3.5) (Anten & Hirose 1999; Werger et al. 2002; Aan et al. 2006). In such stands, enough light penetrates to deeper layers of the canopy such that shorter species can compensate for a lower Φarea by having a large leaf area per unit mass (LAR). The question arises how light capture efficiencies will compare between different species as the LAI increases during succession. Lianas use other plants for support, and thus need to invest less in thickening their stems and branches than do self-supporting species. Consequently, they can achieve greater length per unit of stem biomass and allocate a larger proportion of their resources to production of additional leaves or to reproduction than can self-supporting species (Putz 2005). This suggests that lianas might exhibit greater light capture per unit of mass than trees. Yet only one study (Selaya & Anten 2008) has tested this idea and found that in a 4-year-old successional forest stand, lianas were more efficient than later successional species but not when compared with SLP. In the studies listed above, light capture relative to mass (Φmass) was calculated based on the standing biomass at a single point in time. They therefore do not account for costs associated with the continuous production and loss of leaves and branches, the rate of which, as noted above, may differ strongly between species. Consequently, it is important to analyse the long-term biomass-use efficiency for light capture including costs associated with turnover as well as the changing light climate during succession (Niinemets 2006). We hypothesize that early dominance of species in a regenerating secondary forest is associated with biomass allocation patterns that facilitate a high instantaneous light interception at leaf level. As the vegetation becomes denser and taller during the first years of succession a strong investment of biomass and a high leaf turnover will be necessary to maintain this efficiency. Consequently, we hypothesize that SLP will have a lower long-term efficiency for biomass use of light capture than later successional species (LS). We also expect that once climbing lianas species, given their habit to rely on trees for support, will have higher Φmass compared to the LS but not compared to the SLP. To test these hypotheses we employ a canopy model based on earlier grasslands models, modified to incorporate specific features of forest trees. This model incorporates the dynamics of the leaf turnover, albeit in a simplified manner, and thus enables us to quantify long-term use of biomass for light capture (Φleaf mass total, the amount of light captured during a leaf's life). In combination with field measurements this model enables us to relate interspecific differences in biomass allocation, crown structure, leaf inclination angles, and leaf turnover to light interception. Methods model calculations of whole-plant light interception Model calculations were used to estimate daily light interception of individual plants both in absolute terms and per unit leaf area and mass, and above-ground mass. To this end, we used the model from Selaya et al. (2007). A detailed explanation can be found there, and we only briefly describe it here. The model is very similar to previous two-dimensional canopy models (e.g. Anten 1997; Depury & Farquhar 1997). It considers 9 m2 subplots around target plants and thus assumes that within these plots vegetation structure is horizontally homogenous. Based on light measurements, we found this to be a reasonable assumption for our stands. The model assumes horizontal layers of 0.25 m thickness, and calculates the light interception of target plants within each layer as a function of its leaf area and leaf angle distribution and that of the other plants in the subplot (see eqns 1–8 in Selaya et al. (2007)). This calculation takes differences in leaf angle and vertical leaf area distribution between target individuals and surrounding vegetation into account. Whole plant light capture is calculated as the summation of the light attained in every layer (eqn 9 in Selaya et al. (2007)). This value was subsequently integrated over the day (Φd), taking account of the daily courses of direct and diffuse irradiance above the canopy and the solar inclination as a function of the latitude (11° S 66.1° W) and date following Gates (1980). Light interception per unit of area Φarea, leaf mass Φleaf mass and total above-ground mass Φmass were calculated by dividing Φd by the leaf area (A), leaf mass (LM) and total above-ground mass (M) (Hirose & Werger 1995; Selaya et al. 2007) as: (eqn 1) (eqn 2) (eqn 3) These parameters were interpreted as instantaneous efficiencies of leaf area or biomass use for light interception (Hirose & Werger 1995). We also estimated total efficiency of biomass use for light interception as the total amount of light intercepted over the mean time that a leaf spends on the plant (Φleaf mass total, mol g−1). This efficiency was calculated by multiplying the amount of light per leaf area intercepted daily, with the SLA of death leaves and the mean leaf life spans (Leaflong). (eqn 4) This calculation was done for the seven species for which we had leaf turnover data (Trema, Ochroma, Cecropia, Couratari, Rinereocarpus, Brosimum and Uncaria, see full species names below). The Φarea value in this calculation is the combined average for the three stages. Thus, our calculation represents the first 3 years of succession only. The SLAdead leaves was introduced in the model to account for the cost in leaf biomass construction. It was determined on fully yellowed, non-withered leaves that were about to drop of the branch. The latter was determined by testing how easily they drop off the plant. Table 1 presents a list of the most common symbols. Table 1. List of most common symbols and abbreviations Variables Definition Units LAI Leaf area index m2 m−2 SLA Specific leaf area cm2 g−1 LMR Leaf mass ratio g g−1 LAR Leaf area ratio cm2 g−1 PPFD Photosynthetically photon flux density mol m−2 s−1 Φd Light attained by an individual plant per day mol plant−1 day−1 Φarea Light per leaf area per day mol m−2 day−1 Φleaf mass Light per leaf mass per day mol g−1 day−1 Φmass Light per total above-ground mass per day mol g−1 day−1 Φleaf mass total Total light per leaf mass per mean leaf longevity mol g−1 study site and plant material We studied three secondary forest stands of 0.5, 2 and 3-year-old after field abandonment, growing near Riberalta, in the Bolivian Amazon (11° S 66.1° W). Mean annual temperature is 26 °C and rainfall 1780 mm with a dry season lasting from May to September (Selaya 2007). The forest has been classified as lowland evergreen forest (Hueck & Sebert 1972). Many of the results for the youngest stand are taken from Selaya et al. (2007) and are used here for comparative purposes only. The stands were all forest regeneration stages in a slash-and-burn cycle and had been cultivated with rice, maize and cassava for about 3 years prior to abandonment. In each stand, plots of 0.75 ha at least 20 m away from the edge were selected to avoid the influence of the surrounding forest. All the stands were surrounded by old growth forest. Because this study includes data from only three successional stands, the generality of the conclusions that can be drawn about these forests is somewhat limited. In each stand, 10 of the most common species were selected based on an inventory of the species composition in a number of plots of secondary forest stands from 1–25 years and also in mature forest (N.G. Selaya, unpublished data) and on a previous study on species diversity and abundance along a chronosequence (Peña-Claros 2003) . Trema micrantha, Ochroma pyramidale and Cecropia ficifolia were found to be present from land abandonment to about 4–25 years and were denoted as short-lived pioneers (SLP). Couratari guianensis, Rinereocarpus uleii, Brosimum lactescens and Pseudolmedia laevis were common from land abandonment but showed a peak in abundance between 30–100 years. The latter species was classified as shade tolerant by Peña-Claros (2003). To avoid any confusion in terminology we denote all four species as later successional (LS, i.e. later than the SLP). The lianas (L) Uncaria guianensis, Combretum gracilis, and Adenocalymma impressum showed an occurrence pattern similar to the LS but were treated as a separate group due to their climbing growth habit. Hereafter species are named by their generic name only. In each stand, we selected 10–20 individuals per species of different heights such that they covered the height range with which each species occurred in the stand. We carefully avoided resprouts as these may have a different carbon balance than plants growing from seeds. Each sampled individual had germinated within 3 months after field abandonment. canopy structure and light (ppfd) distribution in subplots Canopy structure and light distribution were determined during the rainy season following Selaya et al. (2007). In each stand about 60 subplots of 9 m2 were established (in line with the model assumption, see above) such that they contained at least one of the selected plants (Table 2). Photosynthetic Photon Flux Density (PPFD, 400–700 nm) was measured at vertical increments of 25 cm in each of the subplots with an SF 80 Line Sensor (Decagon devices Ltd., UK). PPFD above the canopy was measured simultaneously with a point Li-190 SA Quantum sensor (LiCor, Lincoln, USA) connected to a data logger LI1000 (LiCor). Average leaf area index (LAI, m2 m−2) and average leaf angle distribution in each subplot were measured with the LAI-2000 Plant Canopy Analyzer (LiCor). An above canopy measurement followed by four below canopy measurements, viewing from each corner to the centre of the subplot was taken. A view cap of 45° was used to restrict the lens field of view. PPFD and LAI measurements were taken under an overcast sky or at sunset. The vertical distribution of leaves in the canopy was measured using the point method, lifting a scaled pole from the bottom to the top of the canopy and recording the height at which the tip of the pole touched a leaf. The procedure was repeated at the centre of every square meter of each 9 m2 subplot, for nine replicates per subplot. Table 2. Vegetation height, LAI (leaf area index) and light (PPFD) at the forest floor of secondary forest stands of 0.5, 2 and 3 years old. Different letters denote differences at P < 0.05 Year Vegetation height (cm) LAI (m2 m−2) PPFD at forest floor (%) N Mean SE N Mean SE N Mean SE 0.6 63 177 5.45a 60 1.66 0.06a 61 34.36 4.40a 2 60 606 17.41b 71 3.54 0.10b 79 5.20 0.39b 3 59 781 18.06c 61 3.68 0.11b 58 4.74 0.30b stem traits, crown structure and above-ground biomass allocation in individual plants Total height, height at the first leaf or branch with leaves, stem diameter at 0.3 and 1.30 m height were measured on all target plants. When individuals did not reach 0.3 m height, the stem diameter was measured at 10 cm. Individuals were stratified in horizontal layers of 0.25 m and the inclination angles of five randomly selected leaves were measured in each layer using a hand-held protractor. The distribution of the above-ground biomass was determined by means of destructive harvesting. Individuals were harvested and clipped every 0.25 m in height. The samples of stems, branches, petioles and leaves of each 0.25 m layer thus obtained were put separately in plastic bags and kept fresh to be processed in the laboratory. Digital photographs of a representative sample of leaves were taken. Leaf area was calculated using the Sigma Scan Pro 5 (SPSS Inc). All samples were then oven dried at 70 °C for about 5 days and weighed to obtain the dry mass values. Thus light capture of individual plants could be calculated as a function of their vertical leaf area distribution relative to the distribution of the total leaf area in the subplot. For each individual the leaf mass ratio LMR (leaf mass per above-ground mass, in g g−1), specific leaf area SLA (leaf area per leaf mass, in cm2 g−1) and leaf area ratio LAR (leaf area per above-ground mass, in cm2 g−1) were calculated. Crown depth (fraction of stem length with leaves to total stem length, in %) was also calculated. Stem dry mass density was estimated for segments that ranged between 30 to 100 cm in length. The volume was calculated as 0.25D^2πL, where L is the segment length and D the diameter measured in the middle of the segment. leaf longevity Leaf longevity was measured on twenty individuals of each species. Individuals grew within the 6 months old stand, which was 20 months old at the end of the leaf dynamics measurements. Leaf dynamics were followed on cohorts on each branch of the selected plants. At the first census we counted the leaves on each cohort and marked the newest one. Every 60 days, the number of leaves lost, and newly produced leaves were counted and the youngest expanded leaf was marked. These censuses were repeated every 60 days for a period of 12–14 months. Leaf life span was calculated as the number of leaves on the plant, divided by the average of the leaf production and the leaf death rate (eqn 15 in King 1994). Dead or yellow leaves that were still on the plant were collected and their area and weight was measured. For the tree Pseudolmedia and the two lianas Combretum and Adenocalymma, we did not obtain sufficiently accurate data, and leaf longevity and associated calculations are thus only presented for the other seven species. statistics Differences in vegetation height, LAI and PPFD at the forest floor between stands were tested with an anova. Pair-wise post hoc Bonferroni tests were used to test differences among stand pairs. Within each stand the effect of species on height, biomass, diameter, crown depth, Φd, Φarea, Φleaf mass, Φmass and Φleaf mass total were tested with a mixed general linear model anova. As individuals sampled within each subplot (see above) were not statistically independent, subplot was entered as a random factor. Variables were log transformed to meet the assumptions of homogeneity of variances of the Levene's test. Species effects on leaf longevity were tested with a one-way anova as plants used for this measurement were not selected in subplots. Pair-wise post hoc Sidak tests were used to test differences among species. A second-order polynomial regression was done to test the linearity of the relationships between height, biomass, and diameter. ancova was applied with height as the dependent variable and diameter and above-ground biomass as covariates, as well as an ancova with LMR, LAR, SLA, Φd, and Φarea as the dependent variables and either height or mass as covariates with species as a fixed factor and subplot as a random factor. In the regression analyses the choice of independent vs. dependent variable was based on causal relationships assumed in the model. Height and light interception were analysed as dependent variables against mass or diameter (in the case of height) as independent variables, to indicate how efficiently a given amount of mass is converted into height or used for light interception. SLA, LMR and LAR (LAR = SLA * LMR) were analysed against height, because we assumed that due to biomechanical constraints, as plants grow taller, they have to invest disproportionably in support at the expense of leaves (LMR) and because height is strongly correlated with light availability (SLA). Results canopy structure and light vertical distribution The stands differed in canopy height, LAI (leaf area index) and percentage of light at the forest floor (anova at P < 0.05, Table 2). Canopy height increased with the time after field abandonment from 1.8 m at 6 months to 7.8 m at 3 years succession. The mean leaf area index (LAI) increased from 1.7 to 3.7 and light (PPFD) at the forest floor decreased from 34% at 6 months to 4.5% at 3 years. The LAI and light at the forest floor differed significantly in the stand of 6 months compared with the stands of 2 and 3 years old but not between the two older stands. allometry and biomass allocation The species differed in height, stem diameter and above-ground mass in all the three stands (anova at P < 0.05, Table 3). The SLP Trema and Ochroma, which were the most frequent species across all stands, were the tallest and the ones with the greatest above-ground mass. Differences in height between these two species and the others, including the other SLP Cecropia, gradually increased with stand age. Pseudolmedia was the shortest species and its individuals had the lowest mass in all stands except in the 3-year-old one where Rinereocarpus showed the lowest mass values. Plant height differed considerably within species. For the tallest species Ochroma the height range was 0.5–2.2 m and 1.0–9.9 m and for the shortest species Pseudolmedia it was 0.1–0.6 m and 0.4–1.9 m in the 0.5 and 3 y/o stands respectively. The dominant species Trema and Ochroma had shallower crowns than LS and liana species (data not shown). Table 3. Mean height, above-ground mass, stem diameter, leaf mass ratio (LMR), specific leaf area (SLA), leaf area ratio (LAR) and whole-plant daily light interception (Φd) of three short-lived pioneer species (SLP), four later successional species (LS) and three lianas (L) in stands of 0.5, 2 and 3 years old. Different letters denote differences between species within a successional stage at P < 0.05 after Sidak or Games Howell (G-H) tests Stand age Trema (SLP) Ochroma (SLP) Cecropia (SLP) Couratari (SLP) Rinereocarpus (LS) Years Mean SE Mean SE Mean SE Mean SE Mean SE Height (cm) 0.5 140.13 12.22a 129.22 12.56a 73.71 7.31abc 96.59 8.18ab 86.27 9.37abc 2 344.93 39.31a 307.71 43.53ab 228.86 29.69abc 172.78 16.35b 138.41 15.08cd 3 477.11 42.40a 524.65 64.47a 252.22 22.69ab 165.15 24.77bcd 69.94 8.14d Mass (g) 0.5 63.50 14.63abc 115.76 20.68a 38.07 9.02abc 67.83 9.53ab 27.35 4.03bc 2 447.54 171.47a 576.24 200.34a 138.63 35.50ab 170.53 32.53ab 132.73 41.57ab 3 1163.59 300.96a 2443.41 807.92a 137.40 38.76b 337.69 136.03b 16.39 3.49c Diameter (cm) 0.5 1.00 0.10bc 1.40 0.11a 1.39 0.09ab 0.88 0.07cd 0.67 0.05cde 2 2.13 0.30ab 3.01 0.50ab 1.81 0.21ab 1.35 0.10abc 0.95 0.11cd 3 3.07 0.34a 5.19 0.99a 1.82 0.12ab 1.50 0.24bc 0.53 0.05e LMR 0.5 0.36 0.02d 0.39 0.02d 0.37 0.02d 0.61 0.02ab 0.47 0.03cd 2 0.11 0.01g 0.21 0.02f 0.26 0.03ef 0.50 0.02ab 0.36 0.03cd 3 0.09 0.01e 0.14 0.01d 0.21 0.01c 0.50 0.02a 0.52 0.03a SLA (cm2 g) 0.5 188.19 5.42abc 151.29 2.79c 153.41 2.36c 121.12 2.29de 227.67 6.17a 2 197.40 9.46ab 171.50 6.47bc 205.71 12.59ab 128.28 4.04d 247.56 6.44a 3 187.42 10.75bcd 172.18 11.36bcd 217.00 7.28b 138.05 5.14e 291.24 11.57a LAR (cm2 g) 0.5 68.24 4.96cd 58.65 3.18d 57.15 3.50d 73.76 2.52bcd 106.38 7.62ab 2 20.57 1.85e 35.41 4.08d 55.58 7.84cd 64.79 4.00bc 91.05 7.33ab 3 15.36 1.03f 23.69 2.96f 44.49 2.79e 69.55 4.73cd 155.79 12.39a Φd (mol day−1) 0.5 9.83 2.15ab 18.11 4.01a 4.30 1.21bc 9.04 1.52ab 4.36 0.75bc 2 14.62 6.30ab 24.57 10.00a 3.88 1.34abc 4.20 0.95ab 4.89 1.25ab 3 38.67 11.92ab 94.40 31.35a 3.97 1.18bc 6.17 2.53bc 0.34 0.05c Stand age Brosimum (LS) Pseudolmedia (LS) Adenocalymma (L) Combretum (L) Uncaria (L) Years Mean SE Mean SE Mean SE Mean SE Mean SE Height (cm) 0.5 64.53 9.41b 22.38 3.27d 95.84 6.82ab 97.13 6.01ab 60.13 10.24c 2 146.00 23.24cd 74.20 8.57e 139.80 26.18de 216.61 24.94abc 196.27 35.75bcd 3 88.74 13.59cd 80.21 11.71cd 175.45 27.22bc 289.37 29.72ab Mass (g) 0.5 29.60 10.05c 3.05 0.76d 52.10 8.96ab 56.85 10.89ab 32.47 9.87c 2 89.46 33.02bc 15.57 3.40c 51.11 10.67bc 89.61 20.47ab 131.19 34.53ab 3 35.58 12.23bc 32.70 10.75bc 48.25 8.16bc 123.74 28.81bc Diameter (cm) 0.5 0.63 0.09e 0.30 0.03f 0.71 0.06cde 0.78 0.06cde 0.79 0.08de 2 0.67 0.09d 0.41 0.05e 0.66 0.06d 0.75 0.07d 1.06 0.14bcd 3 0.55 0.08e 0.63 0.08de 0.64 0.06d 0.96 0.10cd LMR 0.5 0.58 0.02abc 0.72 0.02a 0.53 0.02bc 0.49 0.02bc 0.61 0.03ab 2