# Nutrient addition to a white sand tropical forest results in greater growth of saplings of canopy tree species than understorey specialist tree species

Giacomo Sellan, Jill Thompson, Rolando Robert, Francis Brearley

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Giacomo Sellan, Jill Thompson, Rolando Robert, Francis Brearley. Nutrient addition to a white sand tropical forest results in greater growth of saplings of canopy tree species than understorey specialist tree species. Forest Ecology and Management, 2025, 589, pp.122755. 10.1016/j.foreco.2025.122755. hal-05250908

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Submitted on 11 Sep 2025

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Nutrient addition to a white sand tropical forest results in greater growth of saplings of canopy tree species than understorey specialist tree species.

**Affiliations:**

¹ CIRAD - UMR EcoFoG, Campus Agronomique, Kourou 97310, French Guiana

² Department of Natural Sciences, Manchester Metropolitan University, Chester Street, Manchester, M1 5GD, UK

³ UK Centre for Ecology & Hydrology, Bush Estate, Penicuik, Midlothian, EH26 0QB, UK

⁴ Forest Research Centre, Sabah Forestry Department, PO Box 1407, 90715, Sandakan, Sabah, Malaysia.

**Corresponding author:** Giacomo Sellan, email: giacomo.sellan@cirad.fr

**Authors' contributions** GS, JT and FQB Conceptualization, JT, RR and FQB supervision, FQB and JT Funding acquisition, GS Methodology, GS Formal analysis, and GS, JT, RR and FQB Writing – original draft.

**Abstract:** In tropical rain forest understories, canopy tree saplings coexist with understorey specialist trees, in a highly competitive environment for light, space, and soil nutrients. To investigate the impact of increasing nutrient pollution from human activity, we assessed differences between canopy trees saplings and understory specialists in their crown structures, allometries, and growth rates in response to experimental nutrient fertilization.

In a nutrient-poor white sand forest in Sabah, Malaysian Borneo we measured tree size and crown dimensions for understorey specialists and canopy tree saplings (≤ 10 cm diameter) before and after experimental fertilization with nitrogen and calcium carbonate.

Results showed that saplings of canopy species were taller than understorey specialists for a given stem diameter, but crown allometries were similar. Three years of fertilization did not affect allometric relationships between diameter and tree height or crown dimensions, suggesting that these allometries are stable and resource-independent. However, relative crown radius growth rate and crown volume growth rate for canopy tree saplings were three times faster after N + CaCO₃ fertilization when compared to controls, demonstrating canopy tree saplings' crown plasticity to maximize access to light.

This study highlights different strategies employed by canopy and understorey species in the competitive forest understorey. Canopy saplings showed greater crown plasticity, investing added soil nutrients into crown expansion for enhanced light interception. Nitrogen deposition could thus advantage canopy species through increased competition with understory specialists resulting in potential species loss. The stability of the allometric relationships, when forests are subjected to nitrogen deposition supports their use for biomass estimation.

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**Keywords:** Allometry, Fertilization, Functional strategy, Lime, Nitrogen, Regeneration.

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# 1. Introduction

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The rain forest understorey is a very different environment from both the canopy surface and within the forest canopy. The atmosphere in the understorey is more humid (Chazdon and Pearcy 1991), and the light is composed of intermittent sun flecks totalling approximately 2 % of the total light incident on the forest canopy (Chazdon and Pearcy 1991). Given that only a fraction of the light reaching the canopy arrives in the understorey, competition among small trees for light is strong in this forest layer (Montgomery and Chazdon 2002; Brenes-Arguedas et al. 2011). Soil nutrient availability for small trees is reduced as most of these resources are used by overstorey trees, which have a greater volume of fine roots and more leaves (Ali and Yan 2017; Coomes and Grubb 1998; Guo et al. 2017) than small trees (Rollinson et al. 2021). The less extensive root system also makes small trees more sensitive to drought and evaporative stress. Small trees in the rain forest understorey thus experience stronger competition for resources than canopy trees. Although the understorey is of utmost importance for the early stages of forest regeneration, this forest layer remains understudied. Furthermore, in the few studies that have investigated the understorey strata, analyses distinguishing between the different strategies of understorey tree specialist species and saplings of canopy tree species are rare (but see Sagar et al. 2008; Aranha et al. 2023).

Canopy tree and understorey specialist species have different ecological strategies. The seedlings and saplings of tree species that have the potential to reach the forest canopy (including mid-storey and emergent tree species - hereafter canopy trees) grow in the forest understorey where they compete with understorey tree specialists, which do not have the potential to grow tall enough to reach the canopy. Understorey specialist species are shade-
66 tolerant and slow-growing and can remain in the understorey for many years (Hubau et al.
67 2019). Most understorey specialists grow and reproduce in the low light of this environment,
68 while other understorey species might remain small and non-reproductive until there is
69 increased light availability, such as in a canopy gap, in order to produce flowers and seeds
70 (Gentry & Emmons 1987). Given the slow air movement in the sheltered forest understorey,
71 wind pollination is a rare strategy in the understory, while it is more common in canopy tree
72 species.

73 Canopy trees comprise 80 % of a tropical rain forests' biomass (Hubau et al. 2019), but
74 understorey specialists may store carbon longer than similar tree size classes (Hubau et al.
75 2019), as the individuals of understorey specialists can be older than saplings of canopy
76 species of the same size. As extreme examples, in the Democratic Republic of Congo, Hubau
77 et al. (2019), found that one individual of understorey specialist species (15.6 cm diameter)
78 was 329 years old, and Orivel et al. (2011) in French Guiana estimated that an understorey
79 specialist tree (6 cm diameter) was 350 years old. Understorey specialists that are adapted to
80 grow and reproduce in a shaded environment do not need to grow tall and with large
diameters (Guo et al. 2017). Canopy species, in contrast, show an increase in relative diameter
81 growth rate the larger their diameter (Guo et al. 2017), which is likely related to their
82 necessity to reach the canopy to reproduce, before they are damaged by a branchfall or
defoliated by herbivores.
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85 Species from these two ecological strategies, understorey versus canopy species, may also
86 have different crown structures, and their structure might change throughout ontogenetic
87 development (Sterck and Bongers 1998), although there is not yet a consensus for a clear
dichotomy in crown structure for these contrasting strategies (Loubota Panzou et al. 2018).
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For example, understorey specialists have deeper and wider crowns than canopy saplings for the same tree height in South-east Asia (Kohyama et al. 2003, Central America (Bohlman and O'Brien 2006) and West Africa (Poorter et al. 2003). This is thought to be an adaptation to shade, where the understorey specialists retain their leaves and lower branches, which grow horizontally, to capture more light and minimise self-shading (Sterck and Bongers 2001). In Central Africa, on the other hand, saplings of canopy species have been reported to have deeper and wider crowns than understorey specialists at the same height (Loubota Panzou et al. 2018), although they only considered trees > 10 cm diameter. Some canopy tree species as juveniles compensate for the low light by producing much larger and thinner leaves (Rozendaal et al. 2006). The allometry of a tree relates the dimensions (e.g. crown depth) as a function of its size (e.g. diameter) by a scaling exponent, which is the slope parameter of the power regression between the two variables.

The growth rate of stem diameter, stem height and different sectors of the crown may be mediated by the availability of soil nutrients. In a temperate forest, for example Ibanez et al. (2016) found that experimental nitrogen fertilization increased canopy trees' height for a given diameter and changed the allometric calculations, thus nitrogen changed the tree resource allocation, which if not taken into account could potentially bias forest carbon estimations. Fertilization has also been found to influence the growth of understorey specialists. In tropical China Mao et al. (2018, 2021), found that the growth (and species diversity) of understorey specialists was reduced after experimental fertilization with nitrogen and phosphorus. In a previous analysis from our study site (Sellan et al. 2019) we found that the understorey trees of the smallest size classes (irrespective of their growth strategy) were the most strongly affected by soil nutrients in terms of their spatial distributions. The contrasting and inconsistent responses of small trees growth to soil
113 fertilization seen in the literature could be the result of divergent responses of understorey
114 specialist species, and saplings of canopy species, to nutrient addition, which might not have
115 been distinguished in previous studies. To our knowledge, no study has compared saplings of
116 canopy species and understorey specialist species' allometry and growth rates, in response
117 to nutrient addition (but see Atikah et al. 2014 for differences in saplings' allometry
118 throughout a fertility gradient). Understanding the impact of nutrient addition on different
119 forest tree species is fundamental to predicting the potential biodiversity changes if, as seen
120 in China, the loss of specialist understorey trees (Mao et al. 2018, 2021) is driven by a selective
121 advantage for canopy tree species. The deposition of atmospheric nitrogen (Sellan et al. 2023)
122 and other atmospheric elements such as phosphorus (Bobbink et al. 2010; Ponette-González
123 et al. 2016; Sundarambal et al. 2010) are increasing in our study area in Borneo as well as
124 throughout the tropics. While in temperate forests nitrogen deposition generally increases
125 carbon sequestration (de Vries et al. 2009), the effects of nitrogen deposition on tropical
126 forests vary (Wright et al., 2018). In tropical dry climates, for example, the forests show
127 different responses to nutrient addition based on forest successional stage, soil parent
128 material, and rainfall regime (Powers et al., 2015). In Central African tropical forests,
129 increased phosphorus deposition can amplify carbon sinks to an extent comparable to the
130 combined effects of rising CO2 and climate change (Goll et al., 2022). However, uncertainties
131 remain regarding the overall impact of nutrient deposition on forest ecosystems, highlighting
132 the need for large-scale experiments and continued monitoring of nutrient deposition in
133 tropical regions (Powers et al., 2015; Goll et al., 2022) and particularly in the most nutrient-
134 poor tropical forests (Sellan et al. 2023).

135 In this study we focussed on a white sand heath forest in Borneo. This forest type is extremely
136 nutrient-poor and hosts high levels of plant endemism (Garcia et al. 2016). We answered the
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following questions: i) Do crown allometries differ between understorey specialists and

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saplings of canopy tree species? ii) Are crown allometries of understorey specialists and

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saplings of canopy species affected by nutrient addition? iii) Does the relative growth rate of

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crown and trunk of understorey specialists and saplings of canopy species change after

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nutrient addition?

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## 2. Methods

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### 2.1 Study area

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We carried out this study in the Kabili-Sepilok Forest Reserve, Sabah, Malaysian Borneo

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(5°51′N, 117°58′E). The climate is equatorial, with a mean annual rainfall of c. 3000 mm and

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a mean annual temperature of 26 °C (Nilus 2003). The reserve hosts three main soil-forest

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associations. The fertile tall alluvial forest, the mid-statured forest on sandstone and the

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infertile short white sand (a.k.a. heath) forest (Nilus 2003; Sellan et al. 2021). Here we focus

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on the white sand heath forest that has low soil available nitrogen (mean of 8.5 ± 1.1 µg g⁻¹

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ammonium concentration and mean of 0.59 ± 0.1 µg g⁻¹ nitrate concentration; Sellan et al.

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2019).

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### 2.2 Experimental setup and measurements

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In 2016 we installed 16 forest plots for this experimental study. The plots were 15 m x 15 m

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and spaced at least 30 m from each other, to avoid cross-contamination during nutrient

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additions. Full details of the experimental set-up are given in Sellan et al. (2020). In summary,

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we treated four replicate plots with nitrogen, four plots with lime (CaCO₃), and four plots with

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a combination of nitrogen and lime. The remaining four plots were left untreated as controls.

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We added nitrogen in the form of urea at a rate of 50 kg N ha⁻¹ year⁻¹. The aim of the liming

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treatment was to increase soil pH to make it similar to the surrounding lowland evergreen
rain forest (pH ~5). In the first year we treated the CaCO₃ addition plots at a rate of 5.56 Mg CaCO₃ ha⁻¹ year⁻¹ and in subsequent years reduced the amount of CaCO₃ to 1.11 Mg CaCO₃ ha⁻¹ year⁻¹ to avoid increasing soil pH higher than the surrounding lowland forest. In the plots treated with the mixture of nitrogen and CaCO₃ we kept the same rate of chemical additions throughout (50 kg N ha⁻¹ year⁻¹ and 1.11 Mg CaCO₃ ha⁻¹ year⁻¹). The plots were treated approximately every 6 months (see Sellan et al. 2020 and Sellan 2019). The rationale behind the choice of these treatments is that heath forest is known to be limited by either nitrogen, by the extreme soil acidity (caused by the sandy texture of the soil), or by a mixture of the two (Luizao et al. 2007). Given the lack of soil iron and aluminium, soil phosphorus is unlocked and has a greater concentration in the heath forest than the other two soil-forest associations (Sellan et al. 2021).

In April 2016, before the fertilizer treatments were started, all trees ≥ 1 cm DBH (diameter at breast height 1.3 m from the ground) were permanently tagged, identified to species and diameter measured at DBH in all plots. On ~25 random individuals per plot, comprised of understorey specialists and canopy tree species with DBH ≤10 cm, we also measured tree height, height from ground to the first branch, and distance from the tree stem to the maximum crown extent in the four cardinal directions to give crown radii. We measured crown dimensions for a total of 388 individuals from 64 species (90 individuals from 9 understorey species and 298 individuals from 55 canopy tree species). In 2019 after three years of fertilizer treatments, we re-measured the DBH of all trees in all plots, and for the 388 individuals used for crown measurements in 2016 we again measured tree height, height to the first branch and four crown radii. In 2019 we also measured height and crown dimensions for a further ~80 randomly selected individuals within each plot. We measured these further trees to increase the number of individuals per plot. We thus added 1275 random individuals
184 in 2019, making a total of 1663 individuals from 99 species (mean of 16 individuals per species,
185 ranging from 1 to 190 individuals per species). We measured DBH with callipers for small
186 individuals (≥ 1, < 3 cm DBH) and a diameter measuring tape for trees with DBH ≥ 3 cm. Tree
187 heights were measured with a TruPulse 200B laser rangefinder (Laser Technology, Centennial,
188 CO, US), or with a measuring tape for small individuals, and crown radii were measured with
189 a measuring tape.

190 **2.3 Analyses**

191 First, we classified whether the species in our plots were, or were not, understorey specialists,
192 using a combination of published data (e.g. Nilus 2003) and expert opinion (Postar Miun, pers.
193 comm.; Ferry Slik, pers. comm.). Most understorey specialist tree species can reproduce
194 without reaching direct sunlight, i.e. they do not need to reach the forest canopy. We also
195 follow the classification of Hubau et al. (2019) who defined understorey specialists as trees
196 that do not grow larger than 15 cm DBH. Hubau et al. (2019) worked in Central African forests
197 (mean canopy height of 30 m – 35 m; Kearsley et al. 2017), with a similar canopy height to the
198 white sand forest we study (28 m; Sellan et al. 2019). To classify the tree species as an
199 understorey specialist or canopy tree, we used the forest survey dataset of Nilus (2003) in the
200 full Kabili-Sepilok Forest Reserve (lowland, sandstone and white sand heath forest), in which
201 the diameter of every individual ≥ 5 cm DBH was measured and identified within 36 ha of
202 undisturbed forest. From this dataset, species with ≥ 20 individuals, of which 95 % of the
203 individuals had a DBH ≥ 5 cm DBH and < 15 cm (thus did not reach the forest canopy) were
204 considered understorey specialists. A threshold of < 15 cm DBH was used to categorize tree
205 strategy because trees ≥ 15 cm DBH are likely to intercept direct sunlight with their crown,
206 whereas trees < 15 cm DBH are usually under the canopy (Hubau et al. 2019). This
classification was conservative when compared to studies that classified understorey specialist tree species with a larger maximum DBH < 25 cm in subtropical China (Quo et al. 2017). For rare species (< 20 individuals in Nilus (2003) dataset) or species in our dataset and not in Nilus (2003) we sought the expertise of Dr. Ferry Slik (Universiti Brunei Darussalam, Brunei Darussalam) and the local field botanist Postar Miun (Forest Research Centre, Sabah, Malaysia), who, based upon their substantial experience and personal observations in this forest, assigned species to understorey or canopy types. All species that were not classified as understorey specialists with these methods, and species determined to genus only, were classified as canopy tree species.

After classifying understorey specialist and canopy trees, our analyses were carried out using measured tree saplings ≥ 1 and ≤ 10 cm DBH at the start of the study in 2016. We calculated individual tree crown volume as C = π*R²*D, where R is the mean crown radius (mean of the four cardinal measurements) and D is crown depth, calculated by subtracting the height to the first main branch above the ground from the total tree height. The simplicity of the formula to calculate crown volume does not affect the scaling exponent (i.e. the slope of the power regression), as we were interested in the relative change in crown volume with respect to height. The same scaling exponent was obtained when considering more complex formulas to describe the volume of a crown. We fitted the allometric relationships using the log-transformed power model (Sellan et al. 2017):

$$ \log(Y) = \beta + \alpha * \log(X) + e $$

where Y is the dependent variable (i.e. individual tree height, crown volume, mean crown radius and crown depth), β is the intercept, α is the scaling exponent (slope), X is the independent variable and e is the error term.
Throughout this study we compared the two classes ‘understory specialists’ and ‘canopy species’ pooling all species in these two categories. This pooling follows the assumption that the different species considered as e.g. understory specialists all have the same allometric exponent. We tested this assumption with a sensitivity analysis (S.I. Figure 1) where we selected first all species with more than 20 measured individuals (following Kohyama et al. 2003) and then all species with more than 10 measured individuals (to include more species in the sensitivity analysis). The allometric exponent obtained by the DBH vs total tree height scaling in both cases (species with > 20 measured individuals and species with > 10 measured individuals) showed that the species in each category had a scaling exponent more similar to other species from its same category than from the other category. Tree allometry between understorey specialists and canopy tree saplings were compared using all 388 individuals measured in 2016, before the experimental fertilization, and the additional individuals from the control plots in 2019 (i.e. no fertilizer added). The difference between the scaling exponents was tested with Student’s t-tests that used Satterthwaite’s method (Harrison et al. 2018). This t-test was obtained from linear mixed models with the following formula:

$$\log(\text{Variable}_1) = \beta + a * \log(\text{DBH}) * \text{Strategy} + E$$

where Variable₁ was either height, crown volume, crown radius or crown depth, β was the intercept and Strategy was a categorical variable with two levels (understorey or canopy species). The E error term included species as a random effect to account for the different number of individuals sampled for each species (the reason why we used linear mixed models). We then assessed the significance for each level of the fixed effect using the *lmertest* R package (version 3.1-1; Kuznetsova et al. 2017). This package calculates pairwise t-tests among levels of the fixed effect, and derives the p-values using the Satterthwaite's
approximation to estimate degrees of freedom, which is a conservative method to obtain t-tests' p-values (Kuznetsova et al. 2017). To see whether three years of N and CaCO₃ addition changed the trees' allometric relationships for each strategy we compared the scaling exponents of tree allometries between understorey specialists and canopy tree saplings (using Student's t-tests as described above). The linear mixed models for this analysis were as follows:

$$ \log(\text{Variable}_1) = \beta + a * \log(\text{DBH}) * \text{Strategy} * \text{Treatment} + E $$

The model structure and variables were the same as above for species strategy canopy versus understory, but also included Treatment as a categorical variable with four levels (control, +N, +CaCO₃, +N +CaCO₃).

To assess whether the relative stem DBH growth rate differed between understorey specialists and canopy tree saplings after three years of fertilizer treatments, we calculated the DBH growth rate relative to the initial diameter using the DBH measurements from 2016 as initial diameter (stems ≥ 1 and ≤ 10 cm DBH only) and measurements from 2019 as final diameters for all individuals in fertilized and control plots. This analysis was repeated for relative annual growth rates of tree height, mean crown radius, and crown depth. From these results we calculated the mean at the plot level and compared all growth rates (DBH, tree height, crown radius, crown depth and crown volume) for the fertilizer versus control treatments using separate two factor ANOVA tests for understorey specialists and canopy tree saplings. All analyses were performed with R (R Core Team 2023).

## 3. Results

Only 10 out of 99 species were classified as understorey specialists (Supplementary Table 1) in the study plots. Nonetheless, these 10 species of understorey specialists comprised 51 %
276 of all stems ≤ 10 cm DBH. Throughout the plots, the understorey specialists represented 49 %
277 of the individuals measured in control plots, 37 % of the individuals measured in +N plots, 52
278 % of the individuals measured in + CaCO₃ plots, and 58 % of the individuals measured in
279 +N+CaCO₃ plots. The most abundant understory specialist species throughout all the plots
280 was *Gaertnera junghuhniana* (Rubiaceae), a non-shrub tree that grows a single sympodial
281 stem and it is not known to grow larger than 10 cm DBH.

282 The allometric relationship for DBH vs tree height (388 trees measured in 2016, and 345
283 additional individuals only from the four control plots measured in 2019) was significantly
284 different between understorey specialist species (0.68 ± 0.05 95 % CI) and species of canopy
285 tree saplings (0.78 ± 0.03 95 % CI). Canopy saplings were taller for a given DBH than
286 understorey specialist species for all the considered tree DBHs, i.e. a significantly greater
287 intercept (Student's t-tests p < 0.001) (Figure 1a). No other allometric relationships were
288 significantly different between understorey specialists and canopy tree saplings (Figure 1).
289 Notably, the intercepts (but not the slopes) of the crown depth and crown volume scaling
290 with DBH were significantly different between the two strategies, showing understorey
291 specialists having a shallower (and thus overall smaller) crown when compared to canopy
292 species (Figure 1).

293 After three years of fertilization, we found no significant differences in DBH vs height nor DBH
294 vs crown dimension allometries for either of the two tree species strategy groups, nor for any
295 of the four different fertilizer treatments (all Student's t-tests with p > 0.05; Figure 2,
296 Supplementary Table 2). There was also no statistical difference among fertilizer treatments
297 for the mean growth rates of any of the other measured parameters (Table 1). For saplings
298 of canopy species, after +N+CaCO₃ addition the rates of growth for crown radius (ANOVA F =
299 2.98; p < 0.001) and crown volume (ANOVA F = 5.73; p < 0.05) increased significantly and
300 were more rapid than for control saplings, whereas for understorey specialists none of the
301 fertilization treatments had any significant effect on the growth rates and the allometric
302 relationships (Figure 3).

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304 **4. Discussion**

305 Tropical rain forest understoreys are very competitive environments where light is scarce and
306 nutrients are often limiting (Montgomery and Chazdon 2002). Trees compete for light
307 through height growth and changes in crown shape (e.g. branches growing towards canopy
308 gaps) to maximize light capture, so we anticipated that understorey specialist trees and
309 canopy tree species, with different light requirements, would show different growth rates and
310 crown allometries. As nutrient availability is low in this white sand forest, we also thought
311 that growth rate and crown size may also be affected by soil nutrient availability. We
312 therefore tested whether understory saplings of canopy trees and understory specialists did
313 have different allometries, and also if their stem and crown growth rates responded
314 differently to nutrient fertilization. In our white sand forest study site, we found that 51 % of
315 the stems were from understorey specialist species among trees with stems ≥ 1 and ≤ 10 cm
316 DBH. This is unusual as in other South-east Asian forests such as the Pasoh Forest Reserve
317 (Peninsular Malaysia) and Lambir (Sarawak, Malaysian Borneo) Janzen (1977) found that
318 saplings of canopy species were dominant with 60 % of understorey stems. These saplings in
319 lowland South East Asian forests were generally from the dominant family Dipterocarpaceae
320 (Janzen 1977; LaFrankie 2005), which contrasts with our heath forest study site where
321 Dipterocarpaceae represent few individuals (19 %).
The steeper slope of the allometric scaling between DBH vs tree height of canopy saplings in comparison to understorey specialists in this Bornean heath forest agrees with results for West African forests (Poorter et al. 2003). This is probably due to the asymmetric competition for light where tall canopy trees require more light and understorey specialists need to be extremely shade-tolerant, to the point where they can reproduce at small sizes and without ever reaching direct sunlight. Individuals from these species thus do not need to grow tall to outcompete their neighbours. Canopy saplings, on the other hand, significantly increase their growth rate, and notably grow taller without any further increase in their DBH as soon as they are free from light competition, either by overcoming the shading from other individuals' crowns, or by developing a more extensive root system for accessing water and soil nutrients (Guo et al. 2017; Loubota Panzou et al. 2018; Xiao et al. 2021). For saplings of canopy species, the higher value of the intercept of crown volume and crown depth scaling with DBH highlights that canopy saplings have deeper crowns for a given DBH than understorey specialists, although no difference was found for crown radius. This result agrees with Loubota-Panzou et al. (2018) in the Republic of Congo and Sterck & Bongers (1998) in French Guyana. Canopy species invest much of their resources into height growth, while understorey specialists often cope with the low light understorey environment by reducing self-shading of their leaves, increased specific leaf area and through horizontal branch growth (Valladares et al. 2002; Kohyama et al. 2003; Poorter et al. 2004), to obtain sufficient light for photosynthesis without the need to grow tall. It was unexpected, therefore, that understorey specialists did not have a wider crown when compared to saplings of canopy species. It is possible that understorey specialist species and saplings of canopy species have similar crown sizes when in the understorey, and the architectural strategies rely upon differences in resource investments into leaf area and leaf density on branches.
We found that the addition of nitrogen fertilizer for three years did not alter the slopes of the allometric relationships between tree diameter (DBH) and crown dimensions for either understorey specialists or canopy saplings. This is in agreement with the results obtained by Ibanez et al. (2016) for *Acer saccharum* in temperate forest in the USA, who also found no significant change in the slope of the allometric relationship, but did find an increase in mean height for a given DBH after 18 years of experimental fertilization. Similarly, in three Bornean rain forest types the allometric scaling for tree saplings did not change along a fertility gradient (Atikah et al. 2014). Our results from our heath forest study are also similar to a previous study in a Congolese forest (Sellan et al. 2017), where we found that tree crown and height allometries were similar in a pristine forest with strong resource competition, compared to a young secondary forest with less nutrients, greater light availability and less competition. We believe that all allometric scalings are thus independent of soil nutrients and are evolutionarily stable (Simini et al. 2010). Trees in the understorey are subject to a significant morphological constraint that maintains a consistent ratio of relative growth rates across their dimensions as they increase in size, at least for the early sapling stage for both canopy tree species and for understorey specialists. Based on our results we suggest that potential increased nitrogen deposition from pollution will thus not influence tree dimension allometric relationships in this heath forest. Given the importance of tree allometry for calculating forest biomass (e.g. Jucker et al. 2022) it is reassuring that the widespread nitrogen deposition through the tropics will likely not introduce bias into the estimation of forest biomass, when employing current allometric methods. Nonetheless, it is important to note that nitrogen deposition does induce changes in overall biomass, which will be detectable through increases in tree height (Ibanez et al. 2016)
The most notable result from our heath forest study was the more rapid growth of the tree crown radius and crown volume in saplings of canopy species, over the three years of simultaneous addition of N and CaCO3. As soil nitrogen is in short supply in this white sand heath forest and trees require nitrogen together with light and CO2 to produce carbohydrates for tree growth, the additional nitrogen fertilizer could allow the crown to expand laterally (depending upon tree crown competition in the canopy) to enlarge the light-harvesting surface. In a Tibetan grassland, the addition of nitrogen was linked to a shift in plant competition from underground resources to light acquisition (Xiao et al 2021) which may also be the case in our white sand forest. The change in nitrogen availability during our experiment, and the corresponding height growth in canopy saplings suggests an important investment of resources into aboveground biomass (Feng et al. 2023) which increases light interception. This was also seen for young Douglas firs in Canada, which increased leaf biomass at a given DBH after nitrogen fertilization in a nitrogen poor site (Grier et al. 1984). In our heath forest experiment, it is not clear why this pattern was only seen for N and CaCO3 together and not seen for nitrogen addition alone, although the addition of nitrogen alone did produce a positive non significant trend of increased rate of diameter growth of canopy saplings.

We hypothesize that when understorey trees are given fertilizer and are no longer nitrogen limited, they invest more resources into faster height and crown growth to access more light.

We speculate that saplings of canopy species with additional nitrogen, which invest in height growth but do not reach sufficient light, may suffer greater mortality, when compared to shade-tolerant understorey specialists. Among canopy saplings, the least shade-tolerant species are more likely to be outcompeted, and their higher mortality may reduce overall tree species biodiversity. For the same reason, we expect that in nutrient-poor forests, such as the
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Bornean white sand forest in our study, there may be stronger competition for soil nutrients than light, and there would thus be fewer understorey specialist species than forests on more fertile soil. Shade tolerant understorey specialists can withstand stronger competition for light and thus may have an advantage for increasing crown dimensions in a nutrient-poor soil.

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We speculate that understorey specialist species in our experiment might have invested the added nitrogen into other processes such as chemical defences against herbivory or seed production (which we did not measure), rather than biomass, structure and growth.

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## 5. Conclusion

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In this study we examined how nutrient fertilization affects crown allometry and growth of understorey specialist species versus saplings of canopy tree species in a tropical heath forest in Borneo. The key findings are that understorey specialist species and saplings of canopy species have distinct allometric scaling relationships, with canopy saplings investing more in height growth, compared to understorey specialists. Nitrogen fertilization did not significantly alter the allometric relationships for either canopy tree species or understory specialist functional groups, suggesting that naturally low levels of nitrogen in this heath forest soil do not affect these architectural forms and they are relatively evolutionarily stable. However, the combined addition of nitrogen and lime ($CaCO_3$) led to a more rapid increase in crown radius and volume for canopy saplings, indicating a shift in resource allocation towards aboveground growth, although without an alteration of the allometric relationships. The addition of nitrogen with lime to the soil increases the competitive ability of canopy saplings, and may lead to a change in species abundances with the potential loss of less competitive species. Furthermore, the stability of the allometric relationship validates the use of current allometric models for biomass calculations under increasing nitrogen deposition.
416 Acknowledgements

417 This research was funded by Manchester Metropolitan University's former Environmental

418 Science Research Centre. We would like to thank the Sabah Biodiversity Council, the Soil

419 Chemistry section, Ecology section and Herbarium staff from Sabah Forest Research Centre

420 and in particular the research assistants Juanis Runcin, Jemson Jumian, Spincer Sitim, Lioba

421 Sawadon and Yun Len Lee. We thank the Universita di Padova for lending the laser

422 rangefinder. We are indebted to Ferry Slik and Postar Miun for the identification of rare tree

423 species' strategies. We sincerely thank the editor and reviewers for their thoughtful and

424 insightful comments on our manuscript.

425 6. Declarations

426 **Funding** The fieldwork was funded by Manchester Metropolitan University internal funding.

427 **Conflicts of interest/Competing interests** NA

428 **Ethics approval** NA

429 **Consent to participate** NA

430 **Consent for publication** NA

431 **Availability of data and material** The diameter data of trees in the fertilised and control plots

432 measured between 2016 and 2018 are available at Environmental data centre

433 (https://doi.org/10.5285/d5ea9e2c-f053-4631-aead-a8a5557488c6). The supplementary data is

434 available upon request.

435 **Code availability** NA
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590

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594 **8. Tables and Figures**

595

<table><caption>Table 1: Annual growth rates (mean ± standard error) relative to the initial size of five structural characters of trees (≥1 and ≤ 10 cm DBH) from fertilized and unfertilized plots in the white sand heath forest in the Kabili-Sepilok Forest Reserve, Sabah, Malaysian Borneo.</caption><thead><tr><th rowspan="2">Treatment</th><th>DBH</th><th>Tree height</th><th>Crown depth</th><th>Crown radius</th><th>Crown volume</th></tr><tr><th>mm<sup>-1</sup> yr<sup>-1</sup></th><th>cm<sup>-1</sup> yr<sup>-1</sup></th><th>cm<sup>-1</sup> yr<sup>-1</sup></th><th>cm<sup>-1</sup> yr<sup>-1</sup></th><th>m<sup>-3</sup> yr<sup>-1</sup></th></tr></thead><tbody><tr><td>Control</td><td>5.32 (±4.40)</td><td>4.32 (±3.06)</td><td>9.52 (±8.06)</td><td>5.00 (±3.99)</td><td>0.23 (±0.17)</td></tr><tr><td>N</td><td>4.95 (±1.32)</td><td>4.10 (±2.90)</td><td>8.65 (±13.94)</td><td>5.56 (±2.96)</td><td>0.29 (±0.20)</td></tr><tr><td>N+CaCO<sub>3</sub></td><td>3.89 (±1.16)</td><td>4.46 (±2.24)</td><td>9.11 (±5.61)</td><td>9.54 (±6.27)</td><td>0.41 (±0.27)</td></tr><tr><td>CaCO<sub>3</sub></td><td>3.76 (±1.94)</td><td>4.23 (±2.96)</td><td>8.24 (±7.93)</td><td>6.69 (±3.84)</td><td>0.25 (±0.92)</td></tr></tbody></table>

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<figure><img src="image_2.png" /><figcaption>Figure 1: Logarithmically-transformed allometric relationships of DBH (cm) with; A) total tree height (m), B) crown volume (m³), C) mean crown radius (m) and D) crown depth (m) of unfertilized trees ≥ 1 and ≤ 10 cm DBH from the white sand forest in the Kabili-Sepilok Forest Reserve, Sabah, Malaysian Borneo. The unbroken orange regression line and round data points represent canopy saplings, whereas the blue dashed regression line and triangular data points represent understorey specialist species. The ± 95% confidence intervals in each panel around the regression lines are given in each panel. Significance was calculated with Student t-tests and significantly different allometric scaling exponents are in bold characters. These</figcaption></figure>
figures include the 388 trees measured in 2016 and the additional 397 trees from control plots
added in 2019.

<figure><img src="image_3.png" /><figcaption>Figure 2: Comparison of the allometries between DBH (cm) and; A) total tree height (m), B) crown volume (m³), C) crown radius (m) and D) crown depth (m) across four different fertilizer</figcaption></figure>
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treatments for canopy saplings (left plot In each panel) and understorey specialist (right plot

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in each panel) for trees ≥ 1 and ≤ 10 cm DBH from the white sand forest in the Kabili-Sepilok

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Forest Reserve, Sabah, Malaysian Borneo. Canopy tree and understorey specialist figures have

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the same Y-axis scale. The orange full line with round data points represents the control

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treatment, the green dashed line with triangular data points represents CaCO₃ treatment, the

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blue dashed line with squared data point represents the N treatment, and the purple dashed

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line with plus shaped data point represents N + CaCO₃ treatment. Negative logs represent

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values less than one. None of the treatments influenced significantly the allometries.

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<figure><img src="image_4.png" /></figure>

<figure><img src="image_5.png" /></figure>

<figure><img src="image_6.png" /></figure>

<figure><img src="image_7.png" /></figure>

<figure><img src="image_8.png" /></figure>

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Figure 3: Relative annual growth rate calculated over three years of experimental fertilizer addition (N and CaCO₃) in the heath forest of the Kabili-Sepilok Forest Reserve, Sabah, Malaysian Borneo. The box plots show mean growth per plot and are grouped per treatment and species strategy. Here we show the growth rates of; A) DBH (cm year⁻¹), B) tree height (m year⁻¹), C) crown radius (Rcro, m year⁻¹), D) crown volume (Vcro, m³ year⁻¹) and E) crown depth (Dcro, m year⁻¹) between understorey specialist species and canopy saplings. In this figure, the horizontal lines represent the median, the boxes represent the interquartile range
637 of the data, the whiskers represent the data spread beyond the interquartile range and the

638 dots represent the outliers.