Using a Bottom-Up Approach to Scale Leaf Photosynthetic Traits of Oil Palm, Rubber, and Two Coexisting Tropical Woody Species

: Rainforest conversion to woody croplands impacts the carbon cycle via ecophysiological processes such as photosynthesis and autotrophic respiration. Changes in the carbon cycle associated with land-use change can be estimated through Land Surface Models (LSMs). The accuracy of carbon ﬂux estimation in carbon ﬂuxes associated with land-use change has been attributed to uncertainties in the model parameters affecting photosynthetic activity, which is a function of both carboxylation capacity ( V cmax ) and electron transport capacity ( J max ). In order to reduce such uncertainties for common tropical woody crops and trees, in this study we measured V cmax25 ( V cmax standardized to 25 ◦ C), J max25 ( J max standardized to 25 ◦ C) and light-saturated photosynthetic capacity ( A max ) of Elaeis guineensis Jacq. (oil palm), Hevea brasiliensis (rubber tree), and two native tree species, Eusideroxylon zwageri and Alstonia scholaris , in a converted landscape in Jambi province (Sumatra, Indonesia) at smallholder plantations. We considered three plantations; a monoculture rubber, a monoculture oil palm, and an agroforestry system (jungle rubber plantation), where rubber trees coexist with some native trees. We performed measurements on leaves at the lower part of the canopy, and used a scaling method based on exponential function to scale up photosynthetic capacity related traits to the top of the canopy. At the lower part of the canopy, we found (i) high V cmax25 values for H. brasiliensis from monoculture rubber plantation and jungle rubber plantation that was linked to a high area-based leaf nitrogen content, and (ii) low value of A max for E. guineensis from oil palm plantation that was due to a low value of V cmax25 and a high value of dark respiration. At the top of the canopy, A max varied much more than V cmax25 among different land-use types. We found that photosynthetic plantations. We demonstrate that photosynthetic capacity related traits measured at the lower part of the canopy can be successfully scaled up to the top of the canopy. We thus provide helpful new data that can be used to constrain LSMs that simulate land-use change related to rubber and oil palm expansion.


Introduction
Tropical forest conversions to different land use significantly impact water and carbon cycle dynamics by modifying carbon sequestration and carbon emission rates [1,2]. In Southeast Asia, Indonesia has one of the highest annual losses of rainforests worldwide [3], where forests have been deforested and converted to woody croplands, namely oil palm and rubber plantations [4]. One of the hotspots of land-use change in Indonesia has been Jambi's province in Sumatra Island, where the area of rubber plantations increased by 19%, and that of oil palm plantations by 85%, from 2000 to 2010 [5]. Land-use change (LUC) from native forest vegetation to rubber and oil palm plantations has increased the income of farmers of Jambi [4,6,7] while at the same time leading to significant ecological costs: decreases in above-ground and below-ground carbon stocks [8][9][10], reduction in soil nitrogen availability [11] and increases in soil N 2 O emissions following N fertilization [12]. Partly because of a lack of field data, it is still unclear to what extent these changes will impact water and carbon transfer between land surface and atmosphere. In consequence, and despite their importance for biogeochemical cycles, the impacts of LUC in the tropics are not well represented in Land Surface Models (LSMs).
In LSMs, the exchange of gases between plants and the atmosphere is represented at the leaf and canopy levels. One common method used to calculate fluxes of carbon and water vapor is the coupling of a mechanistic C 3 model of assimilation FvCB [13] to a stomatal conductance model (gs; Ball, Woodrow & Berry 1987 [14]). In the FvCB model, net leaf photosynthesis (A n ) of C 3 plants is simulated with the assumption that A n is equal to the lowest rate of three limiting biochemical processes: (1) the ribulose 1.5-bisphosphate (RuBP) saturation rate under low intercellular CO 2 concentrations (C i ), where the rate of A n is predicted by the properties of the Rubisco enzyme (V cmax ); (2) the rate of regeneration of RuBP at high C i , driven by light harvesting and electron transport (J max ); or (3) triose phosphate use limitation (TPU) [15]. Recent studies have shown that TPU rarely limits net photosynthesis [16,17]. To our knowledge, many LSMs do not consider TPU limitation or represent it non-mechanistically [18,19], as the evidence for the occurrence of TPU limitation in mature plants from natural ecosystems is scarce (Ellsworth et al. 2015 [20]).
Thus, photosynthetic capacity in LSMs is mainly represented by V cmax and J max , whose values are estimated from A n /C i curves. These parameters are often coupled, allowing J max to be estimated from V cmax [21,22]. V cmax and J max values in LSMs are frequently treated as fixed per plant functional type or linearly related to leaf nitrogen [23,24]. While V cmax and J max have been shown to have a substantial impact on global projections of the carbon cycle [25,26], the natural variability of these parameters is still not known for many plants or ecosystem types.
Since photosynthetic capacity is commonly expressed as the light-saturated photosynthetic rate (A max ) [27][28][29][30], we measured light response curves in addition to CO 2 response curves. Although we are aware that recently there has been standardization in the format of leaf gas exchange parameters [31], in this study we refer to A max as the typical maximum photosynthetic rate under optimal conditions in the field [30,[32][33][34], so that we can compare our estimates with the literature. We estimated A max , V cmax25 and J max25 (J max standardized to 25 • C) of rubber trees (H. brasiliensis) and oil palms (E. guineensis) in smallholder farmers monoculture plantations, as well as from a jungle rubber plantation [35], where rubber trees coexist with native trees [35,36]. In our study region, the tree species A. scholaris and E. zwageri are commonly found to coexist with rubber trees [9,29,37]. A. scholaris is considered to be a light-demanding species, and is principally grown for timber production [29], while E. zwageri is a mid-canopy species [37] and grows relatively slowly [38,39].
In this study, our aim is to determine the photosynthetic capacity and foliar traits of oil palm, rubber and two coexisting woody species growing in tropics. We limited our field measurements at the lower part of the canopy due to logistic constraints. Since estimates of V cmax25 and J max25 at the lower part of the canopy are not directly useful to the LSMs, we used a scaling method based on exponential function to scale up photosynthetic capacity-related traits to the top of the canopy [25,40,41]. The scaling method assumes that photosynthetic capacity at the canopy top is scaled with depth, such that photosynthetic capacity at the canopy top decreases exponentially with cumulative leaf area index [25]. The main objectives of our study were: (i) to estimate key physiological parameters (V cmax25 , J max25 , A max ) and leaf traits (LMA, leaf N), in two tropical tree crops (rubber and oil palm) and two native tree species at the lower part of the canopy; and (ii) to scale up photosynthetic capacity-related traits measured at the lower part of the canopy to the top of the canopy using a 'bottom-up' approach.

Experimental Sites
We conducted our measurements in Jambi Province of the island of Sumatera, Indonesia. The region's climate is tropical maritime, and the rainy season goes from October through April, with the rest of the year being relatively dry [42][43][44]. The average monthly rainfall in the drier season (161 mm month −1 ) is 38% lower than in the rainy season (261 mm month −1 ). The mean annual temperature and mean annual precipitation measured at Jambi airport are 26.7 ± 0.2 • C and 2235 ± 381 mm, respectively [42,45]. Measurements were conducted in three land-use types on loam Acrisol soils: a monoculture oil palm plantation (S 01 • [9]. All study sites were owned by local smallholders. The oil palm plantation was 16 years old at sampling, with an average height of 12 meters [9]. The oil palm plantation received fertilization rates of 68-30-99 kg N, P, K ha −1 year −1 [46]. The rubber trees in the monoculture rubber plantation and jungle rubber were of similar age (about 14 years old), with an average height of 13 meters, and the monoculture rubber plantation, jungle rubber plantation and oil palm stem density were about 440 ha −1 and 525 ha −1 and 140 ha −1 , respectively [9]. Rubber cultivars differ in clone types [47]. In Sumatra, the most widely planted clone is PB 260 [48], which is characterized by a high production potential and strength against wind disturbances [49]. It is also one of the latexproducing clones recommended for their high yield characteristic [50]. In contrast, there is no single oil palm cultivar used in Jambi. Based on local farmers' communication, the oil palm cultivars are DP Marihat, DP Bah Jambi, DP Sucfindo LaMe, DP Dolok Sinumbah and DP LAVROS.
In the jungle rubber plantation, two native trees, E. zwageri (EZ) and A. scholaris (AS), coexisted with the rubber trees. In this study, we use the term "native trees or forests" to refer to these two native tree species together. The native trees were about 20 meters tall, with a stem density of 525 ha −1 . Based on their Latin names, we use 'HBm' and 'HBj' to refer to rubber from the monoculture rubber plantation and jungle rubber plantation, respectively, while we use 'EG' to refer to oil palm. The trees E. zwageri and A. scholaris are referred to as EZ and AS, respectively. We also use 'OPP' and 'RP' to refer to oil palm plantation and rubber plantation, respectively, while we use 'JRP' to refer to jungle rubber plantation.

Sampling Procedure and Gas Exchange Measurements
We performed measurements on two trees or two palms that occurred close to the center of the 50 m × 50 m plot from 8th to 29th May 2017. The measurements were conducted between 8:00 am and 2:00 pm local time. In the case of rubber and native trees, we selected a branch from the lower part of every tree and used a 5-meter ladder to access the branch. We assumed that at the lower part of the canopy, canopy bottoms are shade-prone, and thus all leaves are at least temporarily shaded. Two fully expanded matured leaves were identified per branch. Matured leaves were identified based on visual assessment of leaf color and size-this method has been used by Albert et al. [51]. CO 2 and H 2 O gas exchanges were measured using a portable photosynthesis system (LI-6800; LiCor Biosciences, Lincoln, NE, USA) with a 3 × 3 cm 2 leaf chamber. The LI-6800 is an open gas exchange system, whereby the measurements of photosynthesis and transpiration are based on the differences in CO 2 and H 2 O in an air stream that is entering (reference) and exiting the leaf (sample). The air stream flows through both the reference and sample gas analyzers and splits in the sensor head rather than the console, meaning that the conditioned air does not flow through two different tubes until the head. The head has a valve system that partitions the flow between the reference and sample gas analyzers. The valves also vent chamber air when matching the gas analyzers. It took about 20 minutes for the leaf to reach steady state conditions. Then, a light response curve was generated to determine the light saturation point (1500-1600 µmol photon m −2 s −1 ). After the completion of the light response curve, we again allowed about 20 minutes for the same leaf to reach steady state conditions. Next, a CO 2 response curve on the same leaf was generated. Response curves of net photosynthesis (gross photosynthesis minus respiration, A net ) versus C i (A net /C i ), where C i is the CO 2 concentration inside the leaf, and net photosynthesis versus photosynthetically active radiation (Q in ) (A net /Q in ), was determined on four leaves from the same branch during each measurement period. For the A net /C i curves, leaves were acclimated in the chamber for about 10 minutes until A net did not change over time. The A net /C i curves measurements were performed at a leaf temperature of 25 • C, a relative humidity of 70% and a photosynthetically active radiation of 1500 µmol photon m −2 s −1 in all cases. The CO 2 response curve (A net /C i ) was then initiated with eight levels of CO 2 (400, 200, 0, 400, 600, 800, 1000 and 1200 µmol CO 2 mol −1 air). After completing the A net /C i curve, CO 2 concentration was kept constant at 400 µmol mol −1 air, and Q in was sequentially lowered from 1500 to 1300, 1100, 900, 700, 500, 300, 100 and 0 µmol photon m −2 s −1 . We completed all of the CO 2 response curves and then performed the light response curves. Because photosynthesis has diurnal patterns e.g., [52], we ensured that am and pm measurements were equally represented.
In the case of oil palm, we selected a matured frond from the lower part of every palm and like in the case of trees, we used a 5-meter ladder to access the frond. Two fully matured leaf-lets from the center of the frond were identified per frond. As for trees, it took about 20 minutes for a leaf-let to reach steady state conditions. Next, a light response curve was generated to determine the light saturation point (1500-1600 µmol photon m −2 s −1 ). After the completion of the light response curve, we allowed 20 minutes for the same leaf to reach steady state conditions. Finally, a CO 2 response curve on the same leaf-let was generated. We completed all of the CO 2 response curves and then performed the light response curves by following the similar protocol as for trees. Like for trees, we ensured that am and pm measurements for oil palms were equally represented. We also performed measurements on juvenile (young) trees/palms of all species. However, these young trees/palms were 'parasiting' under the planted canopy, instead of being planted on clearings left by missing adult trees, and therefore we did not consider comparing those data-sets with those used in the present study.

Response Curve Analyses
The estimates of V cmax25 , J max25 , and R d were generated for the A/C i curves by fitting the FvCB model [13,53] using the Plantecophys R package [54]. The general form of FvCB model used is expressed as where A net is the net rate of CO 2 assimilation, A c is the gross photosynthesis rate when Rubisco activity is limiting, A j when RuBP-regeneration is limiting and R d the rate of dark respiration. A c and A j are non-linear functions of the chloroplastic CO 2 concentration (C c ), both of the form k 1 (C c Γ*)/(k 2 +C c ), where Γ* is the CO 2 compensation point without R d , and k 1 and k 2 are different parameter combinations for A c and A j . For a detailed description of these functions and the various parameters' temperature dependence, readers are referred to Medlyn et al. [55]. We used the default settings of the fitaci function from the Plantecophys package but provided the values of CO 2 concentration in the cuvette (CO 2 S), C i , leaf temperature, net photosynthesis, photosynthetically active radiation as an input. The fitaci function fits the FvCB model using the hyperbolic minimum of A c and A j , yielding estimates of V cmax , J max , and R d and their standard errors. The hyperbolic minimum of A c and A j is described by: where θ is a shape parameter, set to 0.99, and A m is the hyperbolic minimum of A c and A j . The response of A net to Q in was fitted to the non-rectangular hyperbolic function [56] described as from which A net is calculated as where A max is the maximum rate of photosynthesis at saturating irradiance, R d is the rate of respiration in the dark, θ defines the convexity of the response curve, and ε, the initial slope of the curve, is the photosynthetic light-use efficiency.

Leaf Nutrient Status and Specific Leaf Area
Following the gas exchange measurements, the same leaves were taken as samples in a dry paper envelope. The specific leaf area (SLA) was measured by cutting a disk with a size of 11.34 cm 2 , then using a ratio of cut-area dry weight to total dry weight from the laboratory-a method that we adopted from Norby et al. [57]. This study refers to the inverse of SLA as the leaf mass per area ratio (LMA). The sampled leaves were dried for 72 h at 60 • C in an oven. The leaf carbon and nitrogen concentrations were analyzed using a CN analyzer (Vario EL Cube; Elementar Analysis Systems GmbH, Hanau, Germany). Leaf phosphorus, potassium and other element concentrations (e.g., Sulphur, Calcium, etc.) were determined by pressure digestion with concentrated HNO 3 , and the digests were analyzed using inductively coupled plasma atomic emission spectrometry (iCAP 6300 Duo VIEW ICP Spectrometer, Thermo Fischer Scientific GmbH, Dreieich, Germany).
To keep it simple, in this study we followed Norby et al.'s [57] approach in determining the leaf nutrient contents. Norby et al. [57] also performed measurements in a tropical setting. We acknowledge that measurements on leaf chlorophyll or chlorophyll ratios might have provided further insights. These measurements could be a valuable direction for future research-where we compare and contrast strengths and weaknesses of the various methods used to derive leaf contents.

Theory for Within-Canopy Gradients in Photosynthetic Capacity
Generally, plant canopies have vertical gradients in physiological processes that relates to maximum carboxylation rates (V cmax25 ), maximum light-saturated photosynthetic rates (A max ), area-based leaf nitrogen content (N a ) and LMA [58,59]. Canopy models often decrease leaf photosynthetic capacity with depth in the canopy using an exponential profile of leaf nitrogen content [25,40,41]. In land surface models (e.g., CLM4) [25], V cmax25 is specified at the canopy top and is scaled with depth using the function where LAI is the cumulative leaf area index and K n is the extinction coefficient for V cmax . A relatively high K n value indicates a more rapid extinction of solar radiation than a relatively low K n value, and implies a steeper decline in photosynthetic capacity through the canopy with respect to the leaf area index (LAI) [25]. This exponential saturation model does not consider some of the processes that could improve the scaled up estimate. First, it does not consider variations in leaf lifetimes [60], leaf angles and size [61,62] along the vertical canopy profile. Second, the method does not consider individual tree heights [63,64] and within-and between-species variations in nutrient concentrations [65]. Third, it does not include effects of direct versus diffuse radiation [66]. Finally, although the decline in photosynthetically critical elements such as nitrogen and phosphorus with increasing depth in plant canopies can be considerable, this decline may be never to the same extent that it matches the reduction in radiation with canopy depth [67,68]. However, the scaling up algorithm has been successfully applied in a number of studies [65,[69][70][71], so by combining 'isolated dataset for only one stratum' from this study with 'K n ' estimates from previous studies, we are able to present a model that is more conceptual rather than quantitative, and can be used for the parameterization of the gas exchange when developing models for CO 2 exchange in tropical settings. The maximum electron transport rate (J max_top ), leaf respiration rate (R d_top ), and other photosynthetic parameters (A max_top , LMA _top , N a_top ) at the top of the canopy are similarly scaled with canopy depth. Using previous studies, we estimate K n values for our oil palm plantation, rubber plantation and jungle rubber plantation canopies (see in Appendix A for details).

Measured Data-Sets
LAI measurements were performed in May until mid-June 2018 at five locations in five subplots (a total of 25 measurements per land-use type (or per plantation plot)) in a 50 m × 50 m plot using the LAI-2200 plant canopy analyzer (LiCOR, Biosciences, Lincoln, NE, USA). We placed the LAI-2200 plant canopy analyzer in different positions so as to capture the spatial heterogeneity, and these 25 measurements were representative of the plant community. The measurements were conducted in oil palm plantation, rubber plantation, jungle rubber plantation and forests on sunny days (see in Appendix B for further details). To compare our up-scaled estimate of leaf mass per area and leaf nitrogen content at the top of the canopy with measurements, we obtained measured data from Kotowska et al. [43], which was measured at the same site and on a similar plant age.

Scaling Up Photosynthetic Capacity and Data Availability
After 'K n ' values were estimated for every land-use type, we use 'inversion technique' to estimate the photosynthetic capacity at the top of the canopy. Basically, we inverted Equation (5), wherein The maximum electron transport rate (J max_top ), leaf respiration rate (R d_top ) and other photosynthetic parameters (A max_top , LMA _top , N a_top ) at the top of the canopy are similarly scaled with canopy depth (see in Appendix C for further details). All of the original data set related to photosynthetic capacity is publicly available through https: //github.com/ashehad/Photosynthetic_capacity_tropics/ (access on 16 February 2021).
A summarized version of the data can be also found in the same repository. To show what the scaling of photosynthetic capacity means to the land surface models (e.g., CLM5) [72,73], as an example, we obtained the baseline (default) values of maximum carboxylation rate (V cmax_top ) and N a_top from CLM5 for tropical evergreen forests and compared it with the values of maximum carboxylation rate (V cmax_top ) and N a_top using the scaling method applied in this study for a potential tropical evergreen forest.

Variation of Photosynthetic Capacity at the Lower Part of the Canopy
Values of V cmax25 ranged from 5.7 to 47 µmol CO 2 m −2 s −1 among all species (Figure 1a) at the lower part of the canopy. HBm and HBi species exhibited the highest values of V cmax25 (Figure 1a), while EZ species had the lowest values (Figure 1a)-a similar trend was noted for J max25 (Figure 1b). Values of J max25 ranged from 16 to 10.7 µmol electron m −2 s −1 among all species (Figure 1b) at the lower part of the canopy. No considerable difference in leaf nitrogen content (N a ) values was found among EG, HBm and HBj species (Figure 1c). EZ species had the lowest N a values (Figure 1c). N a values ranged from 0.74 to 1.49 g N m −2 among all species (Figure 1c). https://github.com/ashehad/Photosynthetic_capacity_tropics/ (access on 16 February 2021).
A summarized version of the data can be also found in the same repository. To show what the scaling of photosynthetic capacity means to the land surface models (e.g., CLM5) [72,73], as an example, we obtained the baseline (default) values of maximum carboxylation rate (Vcmax_top) and Na_top from CLM5 for tropical evergreen forests and compared it with the values of maximum carboxylation rate (Vcmax_top) and Na_top using the scaling method applied in this study for a potential tropical evergreen forest.

Variation of Photosynthetic Capacity at the Lower Part of the Canopy
Values of Vcmax25 ranged from 5.7 to 47 μmol CO2 m −2 s −1 among all species (Figure 1a) at the lower part of the canopy. HBm and HBi species exhibited the highest values of Vcmax25 (Figure 1a), while EZ species had the lowest values (Figure 1a)-a similar trend was noted for Jmax25 (Figure 1b). Values of Jmax25 ranged from 16 to 10.7 μmol electron m −2 s −1 among all species (Figure 1b) at the lower part of the canopy. No considerable difference in leaf nitrogen content (Na) values was found among EG, HBm and HBj species (Figure 1c). EZ species had the lowest Na values (Figure 1c). Na values ranged from 0.74 to 1.49 g N m −2 among all species (Figure 1c).  (Vcmax25, a), maximum electron transport rate (Jmax25, b) and leaf nitrogen content (Na) (c) of leaves of monoculture oil palm (EG), monoculture rubber tree (HBm), jungle rubber tree (HBj), and two native tree species (EZ and AS) measured at the lower part of the canopy. The data included mature oil palm and mature trees.
AS species had the highest values of Amax (Figure 2a). Overall, species' means of Amax varied more than four-fold (from 3.2 to 13.3 μmol CO2 m −2 s −1 ) (Figure 2a). Within species, AS species had the highest values of A max (Figure 2a). Overall, species' means of A max varied more than four-fold (from 3.2 to 13.3 µmol CO 2 m −2 s −1 ) (Figure 2a). Within species, R d varied much more than A max (Figure 1a,b). The species' R d values ranged from 0.2 to 1.31 µmol CO 2 m −2 s −1 (Figure 2b) at the lower part of the canopy. EZ species had the least R d and LMA values (Figure 2b,c). Among species, low-and high-LMA values were 29 and 61.5 g m −2 , respectively (Figure 2c). Rd varied much more than Amax (Figure 1a,b). The species' Rd values ranged from 0.2 to 1.31 μmol CO2 m −2 s −1 (Figure 2b) at the lower part of the canopy. EZ species had the least Rd and LMA values (Figure 2b,c). Among species, low-and high-LMA values were 29 and 61.5 g m −2 , respectively (Figure 2c).  (Amax, a), non-photorespiratory respiration (Rd, b) and leaf mass per area ratio (LMA) (c) of leaves of monoculture oil palm (EG), monoculture rubber tree (HBm), jungle rubber tree (HBj), and two native tree species (EZ and AS) measured at the lower part of the canopy. The data included matured oil palm and matured trees.  Mean (with standard error bars, n = 4) light-saturated net photosynthesis (A max , (a)), non-photorespiratory respiration (R d , (b)) and leaf mass per area ratio (LMA) (c) of leaves of monoculture oil palm (EG), monoculture rubber tree (HBm), jungle rubber tree (HBj), and two native tree species (EZ and AS) measured at the lower part of the canopy. The data included matured oil palm and matured trees.

Extinction of Light in the Canopy Profile
Oil palm plantation (OPP) had the highest K n value (0.32 m 2 m −2 ; Figure 3a

Variation of Photosynthetic Capacity at the Top of the Canopy
OPP, RP and JRP exhibited similar Vcmax25 values at the top of the canopy (~69.4 μmol CO2 m −2 s −1 ; Figure 4a)), while values of Jmax25 at the top of canopy ranged from 142 to 183 μmol electron m −2 s −1 among these three plantations (Figure 4b). At the top of the canopy, the Jmax25: Vcmax25 ratio ranged from 2.1 to 2.7 μmol electron μmol −1 CO2 among all the three plantations (Figure 4a,b), wherein both OPP and RP had a lower Jmax25: Vcmax25 ratio than the JRP (Figure 4a,b).  Figure 4a)), while values of J max25 at the top of canopy ranged from 142 to 183 µmol electron m −2 s −1 among these three plantations (Figure 4b). At the top of the canopy, the J max25 : V cmax25 ratio ranged from 2.1 to 2.7 µmol electron µmol −1 CO 2 among all the three plantations (Figure 4a,b), wherein both OPP and RP had a lower J max25 : V cmax25 ratio than the JRP (Figure 4a,b).
At the top of the canopy, A max varied considerably among different plantations (

Area-Based Leaf Nitrogen Content and Leaf Mass Per Area
At the top of the canopy, the scaling method used in this study estimated the largest N a value for the OPP, while it estimated the least for the RP and JRP (3.6 versus~2.6 g N m −2 ; Figure 5a). For the OPP, the estimated N a value at the top of the canopy via the scaling method was underestimated compared to the field measurements (3.6 versus 5.6 g N m −2 ; Figure 5a). However, there were little differences in N a values at the top of the canopy between the scaling method and measurements for RP and JRP (Figure 5a).
In line with the field measurements, the scaling method used in this study estimated the highest value of LMA at the top of the canopy for the OPP (133.5 g m −2 ; Figure 5a). There was a considerable difference in LMA values at the top of the canopy between the scaling method and measurements for JRP (117 versus 94 g m −2 ; Figure 5b).
From the lower part of the canopy to the top, N a values increased from 1.5 to 3.7 g N m −2 in OPP, whereas N a values increased from 1.43 to 2.36 g N m −2 in RB (Figure 1c,  Figure 5a). In the case of LMA, from the lower part of the canopy to the top, its values increased from 54.5 to 133.5 g m −2 , whereas LMA values increased from 45.9 to 75.8 g m −2 in RB (Figure 2c, Figure 5b).

Area-Based Leaf Nitrogen Content and Leaf Mass Per Area
At the top of the canopy, the scaling method used in this study estimated the largest Na value for the OPP, while it estimated the least for the RP and JRP (3.6 versus ~2.6 g N m −2 ; Figure 5a). For the OPP, the estimated Na value at the top of the canopy via the scaling method was underestimated compared to the field measurements (3.6 versus 5.6 g N m −2 ; Figure 5a). However, there were little differences in Na values at the top of the canopy between the scaling method and measurements for RP and JRP (Figure 5a).

Within-Canopy Gradients for Forest Ecosystems
Forests had the lowest K n value (0.15 m 2 m −2 ) compared to oil palm plantations, rubber plantations and jungle rubber plantations (Figure 3a). On the contrary, forests had the highest leaf area index value (6 m 2 m −2 ) compared to oil palm plantations, rubber plantations and jungle rubber plantations (Figure 3b). The N a : V cmax25_top ratio using the scaling method is higher than the default CLM5 model (0.064 versus 0.05 g N s/µmol CO 2 ). In line with the field measurements, the scaling method used in this study estimated the highest value of LMA at the top of the canopy for the OPP (133.5 g m −2 ; Figure 5a). There was a considerable difference in LMA values at the top of the canopy between the scaling method and measurements for JRP (117 versus 94 g m −2 ; Figure 5b).
From the lower part of the canopy to the top, Na values increased from 1.5 to 3.7 g N m −2 in OPP, whereas Na values increased from 1.43 to 2.36 g N m −2 in RB (Figure 1c, Figure  5a). In the case of LMA, from the lower part of the canopy to the top, its values increased from 54.5 to 133.5 g m −2 , whereas LMA values increased from 45.9 to 75.8 g m −2 in RB (Figure 2c, Figure 5b).

Within-Canopy Gradients for Forest Ecosystems
Forests had the lowest Kn value (0.15 m 2 m −2 ) compared to oil palm plantations, rubber plantations and jungle rubber plantations (Figure 3a). On the contrary, forests had the highest leaf area index value (6 m 2 m −2 ) compared to oil palm plantations, rubber plantations and jungle rubber plantations (Figure 3b). The Na: Vcmax25_top ratio using the scaling method is higher than the default CLM5 model (0.064 versus 0.05 g N s/μmol CO2).

Interspecific Variability in Photosynthetic Traits at the Bottom of the Canopy
In our study, the high V cmax25 values for H. brasiliensis from monoculture rubber plantation or jungle rubber plantation can be due to a high area-based leaf nitrogen content (Figure 1c). It is worth noting that for the H. brasiliensis from monoculture rubber plantation or jungle rubber plantation, our measured value of V cmax25 (~45 µmol CO 2 m −2 s −1 ) is higher than the value reported by Kumagai et al. [74], who observed V cmax25 values of 30 µmol CO 2 m −2 s −1 at the bottom of the canopy. The difference in V cmax25 can be linked to differences in LAI, where our studied rubber plantation had much lower LAI than that of Kumagai et al. [74] (2.3 m 2 m −2 versus 3.89 m 2 m −2 ). A low LAI could mean a high canopy openness, more light penetration, and thus a high V cmax25 at the lower part of the canopy. The relatively low value of A max (4.2 µmol CO 2 m −2 s −1 ) for E. guineensis from oil palm plantation at the bottom of the canopy is due to a lower value of V cmax25 and J max25 (Figure 1a,b) and a relatively high R d value (Figure 2b).

Light Extinction in the Canopy Profile
The high K n value in oil palm plantation suggests that a relatively large amount of light is extinct in the oil palm plantation compared to monoculture rubber plantation or jungle rubber plantation. Subsequently, from the top to the lower part of the canopy, photosynthetic capacity declines faster in oil palm plantation than monoculture rubber plantation or jungle rubber plantation. Our estimate of K n for forests (0.15 m 2 m −2 ) is in agreement with the values from Kattge et al. [24] that showed variations from 0.13 to 0.23. The K n value for forests in this study is also closer to Bonan et al. [25] (0.11 m 2 m −2 ), who derived it from observations. In general, the light extinction approach is more valid for spatially uniform plant canopy than non-uniform plant canopy, as non-uniform plant canopy is usually characterized by a mosaic solar radiation pattern [75,76]. Therefore, for non-uniform plant canopies, we posit that there could be uncertainties associated with estimating the photosynthesis parameters at the top of the canopy using the up-scaling procedure used in this study.

Photosynthetic Trait Variability at the Top of the Canopy
The value of V cmax25 estimated by the scaling method for E. guineensis at the top of the canopy (V cmax25 = 69 µmol CO 2 m −2 s −1 ) is similar to those reported by Rival [77] (V cmax25 = 74 µmol CO 2 m −2 s −1 ). For the monoculture rubber plantation, our estimate of V cmax25 at the top of the canopy (V cmax25 = 73 ± µmol CO 2 m −2 s −1 ) is closer to the value reported by Kumagai et al. [74], who observed V cmax25 values of 70 µmol CO 2 m −2 s −1 . Our estimate of V cmax25 at the top of the canopy for a potential forest ecosystem that consist of the two native tree species (V cmax25 = 36 µmol CO 2 m −2 s −1 ) is comparable with values reported from other tropical forest sites [28,78,79]. Overall, the higher V cmax25 and J max25 of rubber trees and oil palms compared to the forest ecosystem that consist of the two native tree species were in line with the findings of Leuning et al. [80], who reported that these photosynthetic capacity parameters are more commonly higher in agricultural than non-agricultural species.
In our study, the estimate of A max of H. brasiliensis in the monoculture rubber plantation at the top of the canopy was 16.8 µmol CO 2 m −2 s −1 -this value is slightly higher than the value (A max = 13.1 µmol CO 2 m −2 s −1 ) reported on two-year-old rubber seedlings grown in the field [81]. In the case of E. guineensis, the estimate of A max at the top of the canopy was 10.3 µmol CO 2 m −2 s −1 , which is slightly lower than Corley [82] (A max = 14 µmol CO 2 m −2 s −1 ).
The scaling method estimated the highest value of A max (24.1 µmol CO 2 m −2 s −1 ) in the jungle rubber plantation at the top of the canopy. The reason for this is due to a relatively high leaf nitrogen content ( Figure 5a); this reason is also supported by the measurements from the top of the canopy (Figure 5a) [43].

Limitations and Implications of Scaling Method Used in This Study
In this study, we did not perform diurnal integrative assessments of the light environment. This is important especially for studying diurnal patterns of photosynthesis, looking at diurnal shading patterns and investigating the inhibition of photosynthesis, e.g., [83]. Our up-scaled values of photosynthetic capacity related traits from the lower part of the canopy to the top of the canopy suffer from a couple of shortcomings. First, we used the leaf area index estimates from the similar month, but from a subsequent year. Second, we have studied only two native tree species from the jungle rubber plantation.
Our up-scaled values of photosynthetic capacity-related traits from the lower part of the canopy to the top of the canopy matched reasonably well with the previous measurements from our studied sites, e.g., [43] as well as from the literature [74,77]. This indicates that our data can be integrated with the land surface models (e.g., CLM5) [72,73]. As an example, for a potential tropical evergreen forest ecosystem, our estimated N a : V cmax25_top ratio using the scaling method was higher than the default CLM5 [72,73] model because mainly the area-based leaf nitrogen content at the top of the canopy was 30% higher, as a result of the scaling method than the default CLM5. It is worth noting that measurements at our study sites indicate a 2-fold area-based leaf nitrogen content at the top of the canopy compared to the default CLM5. The high N a : V cmax25_top ratio suggests that if CLM5 is parameterized with our estimates from the scaling method, the transpiration estimate of CLM5 will have greater sensitivity than the default CLM5. We do acknowledge, however, that the transpiration estimate of CLM5 is also sensitive to other parameters, such as the stomatal slope that relates stomatal conductance to photosynthesis [73].

Conclusions
We can conclude that the photosynthetic capacity-related traits measured at the lower part of the canopy can be successfully scaled up to the top of the canopy, especially for closed and uniform plant canopies. Future measurement efforts for species studied in this study should focus on upper canopy locations, so that our study's data-sets can be combined and the variability of leaf traits in the vertical canopy profile can be investigated.

Acknowledgments:
We thank George Ofori Ankomah from the University of Goettingen for measuring the leaf area index at the studied rubber plantations. Finally, we thank the village leaders and farmers for allowing us to conduct our research on their land.

Conflicts of Interest:
The authors declare no conflict of interest.

Appendix A. Estimating K n Values of Plantations
In a large-scale commercial oil palm plantation (LSCOPP) in Jambi, where Meijide et al. [84] measured V cmax25 in the vertical canopy profile, where the V cmax25 value at the bottom was 13.1 µmol CO 2 m −2 s −1 , while at the top of the canopy it was 42 µmol CO 2 m −2 s −1 . Since the leaf area index at LSCOPP has been 3.64 m 2 m −2 [85,86], we have from which K n value can be determined for the LSCOPP. We assume that the estimate of 'K n ' at LSOPP will be similar at our studied oil palm plantation site.
from which K n value can be determined for the RPC. As for the oil palm plantation case, we assume that the estimate of 'K n ' at RPC will be similar at our studied rubber plantation site.
To determine 'K n ' values for forest site in Jambi, we used the value of V cmax25 (53 µmol CO 2 m −2 s −1 ) as measured at the top of the canopy at a tropical forest site in Bariri, Indonesia [87] to calculate the value of 'K n '. Lloyd et al. [59] analyzed many tropical forest canopies and found that the K n value scales with V max25 using the following relation where high values of K n results in steeper declines in photosynthetic capacity through the canopy profile with respect to the cumulative leaf area index. Finally, to estimate 'K n ' values for jungle rubber plantation, we summed the K n values of forests and rubber plantation and then halved it.

Appendix B. Leaf Area Index Measurements
A 50 m × 50 m plot was established by the EFForTS project in oil palm plantation, rubber plantation, jungle rubber plantation and forest [42]. Each plot contained five subplots measuring 5 × 5 m, which was unevenly laid at specific locations. LAI measurements were conducted in May until mid-June 2018 at five positions in all five subplots established within each of the plantation plot using the LAI-2200 plant canopy analyzer. LAI data were obtained from above and below canopy readings taken simultaneously in each subplot with two LAI-2200 devices. All measurements were taken with view cap-free wands under diffused sky conditions. Optical sensors were covered and packed into its protective case at the slightest detection of precipitation to avoid any potential optical damage to the sensors and other sensitive parts of the device. Wands were always orientated towards the magnetic north with the use of a compass (LI-COR, Inc., Lincoln, NE, USA2017). The above canopy readings were captured by mounting a 10-second autolog wand (reference sensor) facing the sky on a 2 m sturdy tripod with an accurate leveling bubble. This was positioned in nearby open areas to the core plots of at least 200 m × 200 m range with surrounding vegetation height less than 3.5 m to ensure a sensor's view of the sky across a wide azimuth [88]. The below canopy readings in each plot were taken concurrently with that of the reference sensor at five positions within each subplot, to obtain accurate measurement of canopy transmission (LI-COR, Inc., 2017). The distance between designated reference sensor locations (open areas) and core plots for below canopy readings was less than 1 km, to ensure uniform sky brightness between the two-sensor locations for canopy measurements. LAI values for subplots were averaged out for the respective plantation plots.

Appendix C. Calculation of the Photosynthetic Capacity Using the Scaling Method
To estimate the value of V cmax25 at the top of the canopy (V cmax25_top ) at our studied oil palm plantation, we substituted the measured value of V cmax25 at the bottom of the canopy, and the derived value of K n and the measured value of leaf area index at our studied oil palm plantation in the following equation: A similar form of the equation was used to estimate values of J max25_top , N a_top , A max_top , R d_top and LMA _top .
For our studied rubber plantation site, we substituted the measured value of V cmax25 at the bottom of the canopy, and the derived value of K n and the measured value of leaf area index at our studied rubber plantation in equation A5. We used a similar form of equation A5 as was used to estimate values of J max25_top , N a_top , A max_top , R d_top and LMA _top for the rubber plantation.
Using a similar approach (as in above), we estimated values of V cmax25_top , J max25_top , N a_top , A max_top , R d_top and LMA _top for jungle rubber plantation by using its K n value and the measured value of leaf area index. We also used a similar approach (as in above) to estimate values of V cmax25_top and N a_top for a potential tropical evergreen forest ecosystem by using its K n value and the measured value of leaf area index. To determine the V cmax25 values at the lower part of the canopy for the potential tropical evergreen forest ecosystem, we summed the V cmax25 values of the two native tree species and then halved it. We followed the same method to obtain the N a values at the lower part of the canopy for the potential tropical evergreen forest ecosystem.