Effect of Differential Growth Dynamics Among Dominant Species Regulates Species Diversity in Subtropical Forests: Empirical Evidence from the Mass Ratio Hypothesis

Abstract

The Mass Ratio Hypothesis states that the growth dynamics of dominant species influence forest species diversity by regulating the niches of subordinate and transient species. However, this prediction has not yet been empirical confirmed in subtropical forests over long term. Using data from 1995 to 2017, we examined how dominant tree species regulate species evenness and richness by analyzing their height and diameter growth in three clear-cut forests (Castanopsis carlesii (Hemsl.) Hayata, Castanopsis fissa (Champ. ex Benth.) Rehder & E. H. Wilson, and Cunninghamia lanceolata (Lamb.) Hook. stands), combined with the mean value of species niche breadth (measures the diversity of resources a species utilizes) across the community, including separate analyzes for subordinate (persistently coexisting with dominants species) and transient species (temporarily occurring species). Our results showed that an increase in height and diameter growth of dominant species had a negative effect on niche breadth of subordinate species, which in turn reduced species evenness (p < 0.01) but showed no significant relationship with species richness (p ≥ 0.05). Growth dynamics of dominants had no significant influence on the niche breadth of transient species. The early-fast growing dominant C. lanceolata significantly restricted the niche breadth of subordinate species (1.16 ± 0.23), resulting in relatively low evenness (0.49 ± 0.11). Conversely, the late-fast growing dominant C. carlesii promoted niche expansion (6.62 ± 1.20), resulting in higher evenness (0.81 ± 0.02). C. fissa -dominated strands with intermediate growth increments, exhibited moderate species evenness. These findings provide long-term empirical support for the Mass Ratio Hypothesis by demonstrating that growths of dominant species modulate niche partitioning in subordinates and thereby shape species diversity in subtropical forest communities.

1. Introduction

The restoration of biodiversity in disturbed forests is essential for maintenance of ecosystem functions and services [1,2]. This restoration process involves complex ecological mechanisms, including abiotic filters, dispersal limitation and source effects, as well as species interactions [3,4,5,6,7]. Within the domain of species interactions, the Mass Ratio Hypothesis remains a central framework [8,9]. Grime’s theory posits that ecosystem processes are primarily governed by the biological traits of dominant species [10,11,12]. For instance, the height and diameter growth of dominant species may alter understory microenvironments, thereby shaping species coexistence patterns and community diversity [13,14,15,16]. Despite the theoretical and practical significance of understanding how the growth dynamics of dominant species influence biodiversity, empirical knowledge on this relationship remains scarce [17,18]. This knowledge gap substantially hinders the formulation of sustainable management strategies.

According to Grime’s theory, the regulatory effects of dominant tree species on forest biodiversity are primarily expressed through their dual influence on the ecological niches of subordinate species and transient species. Subordinate species, though consistently present in the community, are not dominant and often exploit unoccupied resources through niche complementarity with dominant species [19]. Transient species, on the other hand, are typical opportunists that depend on disturbance events, especially the period before dominant trees achieve full canopy closure, to expand their ecological niches [8]. The theory predicts that there are two main consequences when dominant species have strategies for early and fast growth. First, stronger resource competition narrows the niche breadth available of subordinate species [20]. Second, rapid canopy closure shortens the window during which transient species can access light and space [21]. In contrast, when dominant species grow later and more slowly, these two regulatory pathways may promote species diversity [22]. Although these predictions are theoretically compelling and supported by short-term studies of ecosystem recovery [6,23,24,25,26], there is limited long-term evidence [19]. Some changes in species diversity, such as increases in species evenness, may take decades to manifest following disturbance [27]. Thus, understanding how the growth dynamics of dominant species regulate species diversity requires long-term ecological monitoring, which can clarify how shifts in subordinate and transient niches influence species diversity.

In subtropical regions, forests are dominated by late-fast growing and early-fast growing tree species. Compared to late-fast growing species, early-fast growing species typically reach rapid growth phases in height and diameter at earlier stage [28,29,30,31]. Based on the Mass Ratio Hypothesis, these differences in growth increments may influence forest species diversity by altering resource niches available to subordinate species [8,20] and changing the temporal window during which transient species can expand their ecological niches [21]. Existing studies generally support that early-fast growing forests tend to have lower species diversity compared to those dominated by late-fast growing species [32,33,34]. However, most studies have attributed these differences primarily to regeneration modes [35,36], while potential role of dominant species growth dynamics, particularly height and diameter, in shaping diversity patterns has received little attention [37,38]. This gap limits our ability to effectively guide forest ecosystem restoration and sustainable management.

To address this, we stduied subtropical forests in eastern China to (i) assess how the growth strategies of dominant tree species influence the recovery of species diversity and (ii) explore the underlying mechanisms based on changes in niche breadth of subordinate and transient species. We established 216 plots (5 × 5 m) across three clear-cut forests [39,40], each dominated by one of the three tree species with distinct growth increments: C. carlesii (late-fast growing), C. fissa (intermediate-fast growing), and C. lanceolata (early-fast growing). Forest regeneration was monitored from 1995 to 2017 through repeated community inventories and destructive sampling of dominant species in 2019 quantified their growth dynamics.Based on Grime’s theory [8] and the known growth patterns of subtropical tree species [28,30], we hypothesized that (i) late-fast growing species would be more effectively to restore species richness and evenness than early-fast growing dominant species, because their delayed diameter growth reduces competition for resources, while their late height growth postpones canopy closure, thereby promoting species coexistence; and (ii) dominant species influence forest species diversity by simultaneously modifying the niche breadths of subordinate and transient species.

2. Materials and Methods

2.1. Study Area

The study site is located in Wuping County, Fujian Province, at the southernmost extent of the Wuyi Mountains (25°9′ N, 116°4′ E), with elevations ranging from 400 to 650 m. The region lies at at the southern boundary boundary of the mid-subtropical zone, where the South Subtropical Rainforest and Mid-Subtropical Evergreen Broadleaf Forest vegetation zones converge. It has a mean annual temperature of 18.2 °C, average annual precipitation of 1542 mm, and mean relative humidity of 80% [39]. Under natural conditions, the tree layer is dominated by species plants such as C. carlesii, Castanopsis fargesii Franch., Pinus massoniana Lamb., Machilus versicolora S. K. Lee & F. N. Wei, and Elaeocarpus decipiens Hemsl. The shrub layer commonly includes like Syzygium buxifolium Hook. et Arn, Loropetalum chinense (R. Br.) Oliver, Sapium discolor (Champ.ex Benth.) Muell.-ARG., Rhaphiolepis indica (Linnaeus) Lindley, and Ilex pubescens Hook. et Arn. The herbaceous layer is dominated by Dicranopteris dichotoma (Houtt.) Nakaike, Gahnia tristis Nees, and Alpinia japonica Hayata [40].

2.2. Experiment Design and Surveys

This experiment began in February 1993 with pre-logging assessments of community structure in permanent plots [41]. Clear-cutting was carried out in 1994 using chainsaws for tree felling and bucking, and with logs removed by skidder tractors. Following slash-and-burn treatment, three different regeneration strategies were applied. In the C. carlesii forest, regeneration was left to occur naturally without further human intervention. The canopy is characterized by C. fargesii, C. fissa, M. versicolora, and Castanopsis faberi Hance. Typical shrub species include S. buxifolium, Tarenna mollissima (Hook. et Arn.) Robins., and I. pubescens, while herbaceous species include G. tristis and Woodwardia japonica (L. f.) Sm. In the C. fissa forest, regeneration was assisted—naturally regenerated C. fissa seedlings were retained as much as possible while fewer than 300 stems ha⁻¹ of C. lanceolata were planted. From 1995 to 1998, brush clearing was conducted every May, including cutting woody shrubs at ground level and trimming herbaceous vegetation to a height of less than 5 cm. Typical tree species in this forest include C. lanceolata, Choerospondias axillaris (Roxb.) B. L. Burtt & A. W. Hill, C. carlesii, and C. faberi. The shrub layer is dominated by Pseudosasa cantori (Munro) Keng f. and T. mollissima, while herbaceous species are presented by Dicranopteris pedata and W. japonica. In the C. lanceolata forest, regeneration was entirely artificial. From September to December 1994, surface vegetation (logging residues, shrubs, etc.) was removed and site preparation was carried out to a depth of 30–50 cm. In March to April 1995, C. lanceolata seedlings were planted at a density of 2500 stems ha⁻¹. Brush clearing was conducted twice a year (May and September) from 1995 to 1998, within a radius of 0.5–1 m around each target tree. The dominant tree species in this forest are C. lanceolata and C. axillaris, with P. cantori dominating the shrub layer and D. pedata and W. japonica as representative herbaceous species. Perminant plot locations of these three types of forests are shown in Figure 1. Photos of forest landscapes and dominant tree species for each forest type can be found in the Supplementary Figure S1.

Vegetation surveys in the permanent plots were conducted in 1993 (pre-logging baseline), 1995, 1998, 2000, 2005, and 2017. All woody plants were identified using the Flora of China http://www.iplant.cn/foc (accessed from 1 June 2017 to 30 September 2017) and the taxonomic literature [42]. For each survey, individuals with a diameter at breast height (DBH) ≥ 2 cm and height (H) ≥ 2 m were tagged, mapped, and assigned unique identification numbers. Based on species ranking by basal area and abundance prior to clear-cutting, all species were classified into three functional groups: dominant, subordinate, and transient species [8,19]. Detailed classifications are provided in Supplementary Table S1.

2.3. Growth Analysis of Dominant Species

The analysis of the growth dynamics of height and diameter of dominant trees was conducted in October 2019. For this purpose, we harvested trees to examine their growth patterns. In order to minimize the disturbance of the permanent monitoring forests while fulfilling the minimum statistical requirements, three dominant trees were harvested from each forest plots of the C. carlesii, C. fissa, and C. lanceolata. We selected trees that were healthy, free of pests and diseases, located in the canopy layer, and whose diameter at breast height (DBH) and total height were close to the stand average. After felling, we measured the diameter at breast height (DBH), crown length, total tree height, and stem diameter at one-quarter, one-half, and three-quarters of total height. Stems were sectioned at 2-meter intervals; for basal segment, the central cross-section was used due to collar swelling. The tree age was determined from annual rings on breast-height disc [43] and cross-validated with DBH records from community surveys (see Figure S2 and Table S2 for details) and previous studies [44,45]. Due to the narrow and unclear tree-ring widths of C. carlesii and C. lanceolata during the first and second decades of monitoring, respectively (Supplementary Figure S2), the age interval was determined to be 2 years. In contrast, C. fissa exhibited consistently wider and clearer tree rings, allowing use of a 1 year interval. Diameters for each age class were measured directly from discs using a ruler. The age at each sampling height was calculated by subtracting the number of rings at that disc from the total tree age. Following Pretzsch [46], annual growth increments for tree height and DBH (θ) were calculated using the formula:

$$\theta ={(V}_a-V_b)/(a-b),$$

(1)

where Vₐ and V_b is the tree height or cumulative radial growth at age a and b and a = 1, 2, …, n, b = 1, 2, …, n.

2.4. Statistical Analysis

Species diversity was assessed based on species richness and evenness. Species richness (S) was defined as the total number of woody plant species recorded across all forest plots (72 plots of 5 × 5 m each). Species evenness (J) was calculated using the following formula:

$$J=(-{\sum }_{i=1}^S{P}_i\mathit{ln}{P}_i)/lnS,$$

(2)

where S is the total number of species, and P_i is the proportion of individuals of the i-th species relative to the total number of individuals [47].

Niche breadth (B) is calculated as:

$$B={\displaystyle \frac{1}{{\sum }_{i=1}^n{p}_i^2}},$$

(3)

where p_i is the relative abundance of a given species in the i-th plot, and n is the number of plots, i = 1,2,3…n [48].

To obtain data on the growth of dominant species corresponding to the temporal dynamics of niche breadth in associated and transient species, we divided the annual growth data of tree height and diameter at breast height (DBH) into three time periods corresponding to the community surveys: 1995–2000, 2000–2005, and 2005–2017. For each dominant species (C. carlesii, C. fissa, and C. lanceolata), the mean annual increments in tree height and DBH were calculated for each time period. Principal component analysis (PCA) was then used to evaluate how these two growth metrics influenced the mean niche breadth of associate and transient species. Subsequently, linear mixed-effects models (LMMs) were applied to examine the relationships between factor loadings on the first two principal component axes and species richness and evenness. The basic form of the model was:

$$y_{ij}={\beta }_0+{\beta }_1·x_{ij}+{\mu }_{i1}+{\mu }_{i2}+{ϵ}_{ij},$$

(4)

where $y_{ij}$ is the annual growth in height or DBH of the dominant tree species, $x_{ij}$ is the mean niche breadth of different functional groups, ${\beta }_0$ is the global intercept, ${\beta }_1$ is the fixed-effect coefficient. The random intercepts were specified as $u_{i1}~N(0,{\sigma }_u^2)$ representing temporal variation, and, $u_{i2}~N(0,{\sigma }_u^2)$, representing the effect of different regeneration modes on species richness or evenness. The residual error was modeled as ${ϵ}_i~N(0,{\sigma }^2)$ is the residual error term. Hierarchical partitioning analysis was further employed to estimate the relative contributions of dominant species growth dynamics, subordinate and transient mean niche breadth and regeneration mode to species diversity [49]. Model validation included tests for normality of residuals (Shapiro–Wilk test, p ≥ 0.05; confirmed by Q–Q plots) and homogeneity of variance (Levene’s test, p ≥ 0.05; no trends observed in residuals vs. fitted values). When assumptions of normality were violated (e.g., annual height and diameter growth of C. carlesii from 1995 to 2000, species richness, and species evenness; Shapiro–Wilk test, p < 0.05), non-parametric tests Kruskal–Wallis test were applied. These were used to compare annual height and diameter growth among dominant species across different time periods, as well as differences in average niche breadth of subordinate species, average niche breadth of temporary species, species richness, and species evenness among forest types. All statistical analyses were conducted using R software (v. 4.1.2), and all graphical outputs were generated using SigmaPlot (v. 14.0).

3. Results

3.1. Growth Dynamics of Three Dominant Tree Species

As shown in Figure 2a, C. lanceolata entered its rapid diameter growth phase earliest, followed by C. fissa, while C. carlesii entered last. This temporal differentiation resulted in distinct diameter growth dynamics among the three species from 1995 to 2017. During 1995–2000, C. lanceolata exhibited a clear advantage in annual diameter increment (0.93 ± 0.13 cm year⁻¹; p < 0.05). Between 2000 and 2017, growth patterns reversed, with C. fissa gradually became dominant (2000–2005: 1.24 ± 0.07 cm year⁻¹; 2005–2017: 0.93 ± 0.25 cm year⁻¹). Meanwhile, C. carlesii accelerated (2000–2005: 0.30 ± 0.12 cm year⁻¹; 2005–2017: 0.84 ± 0.32 cm year⁻¹) but remained comparatively lower. In terms of height growth (Figure 2b), C. lanceolata also entered the fast-growth stage earlier than the other two species. Species differences were generally small, except during 2000–2005, when the annual height increment of C. lanceolata was significantly higher than that of C. fissa and C. carlesii (p < 0.05). These interspecific differences in diameter and height increment dynamics reflect distinct growth patterns: late-fast growth in C. carlesii, mid-fast growth in C. fissa, and early-fast growth in C. lanceolata.

3.2. Effect of Dominant Species Growth Dynamics on Subordinate and Transient Species Niche Breadth

Based on principal component analysis, we evaluated how differences in growth dynamics (height and diameter) among dominant tree species influence the mean niche breadths of subordinate and transient species. The first two principal components explained 97.63% of the total variance. The first principal component (PC1) accounted for 87.33% of the variation and primarily reflected the influence of dominants’ growth dynamics on the mean niche breadth of subordinate species (Figure 3a). The second principal component (PC2) explained 10.60% of the variation and, mainly represented the effects on the niche breadth of transient specie. The three dominant species were clearly separated along PC1 (Figure 3b,c). Compared to C. carlesii, which entered the fast growth phase later, the early-fast growth of C. lanceolata significantly reduced the mean niche breadth of subordinate species (see Supplementary Figure S3). In contrast, the effects of dominants growth dynamics on PC2 showed no significant differences among the species (Figure 3d).

3.3. Relationship Between Effect of Dominant Tree Growth and Species Diversity

Mixed-effects linear regression analysis revealed a significant negative correlation between species evenness and PC1 (Figure 4a, R²_marginal = 0.37, R²_conditional= 0.75, p < 0.01). This relationship indicates that lower species evenness is associated with dominance by early-fast growing species and a consequent narrowing of subordinate species niche breadth (Figure 4c). However, there was no significant correlation between species evenness and PC2 (Figure S4, R²_marginal = 0.02, R²_conditional = 0.67). Although species richness in C. lanceolata forests was significantly lower than that in C. carlesii and C. fissa forests (Figure 4d), this variation was not related to the effects of dominant species growth dynamics (Figure 4b and Figure S4).

4. Discussion

4.1. The Differential Growth Dynamics Among Dominant Tree Species Affect the Species Evenness

Our results demonstrate that the growth dynamics of dominant species are a key driver of species evenness, providing experimental evidence in support of Grime’s hypothesis [8]. Consistent with our first hypothesis, the late-fast growing dominant species C. carlesii was more conducive to enhancing forest species evenness than the early-fast growing C. lanceolata. This difference is primarily attributable to their contrasting effects on the niche breadth of subordinate species. The rapid growth of C. lanceolata may restrict niche expansion of subordinate species through multiple pathways: (1) its early-fast height growing accelerates canopy closure, creating a steep vertical light gradient [50,51]; (2) rapid stem thickening with crown expansion intensifies interspecific competition [15,52]; and (3) coordinated root and stem development reduces the availability of spatial, water, and soil nutrients [53,54,55]. In contrast, the late-fast growth strategy of C. carlesii may provide a more stable resource supply and a longer window of opportunity for niche differentiation between subordinate species [56], thereby supporting higher species evenness in forests it dominates. These findings contribute to a better understanding of the mechanisms that maintain biodiversity in subtropical forests and, more importantly, provide practical insights for biodiversity conservation. In logged forest ecosystems, promoting the dominance of late-fast growing species may represent a more effective strategy for fostering species-diverse forests than traditional management approaches that favor early-fast grower.

Contrary to our second hypothesis, dominant species growth dynamics had no significant effect on the niche breadth of transient species. This finding contradicts with previous studies [21,37]. For example, Falster and Westoby [21] proposed that early-fast vertical growth of dominant species accelerates canopy closure, thereby narrowing the temporal window for transient species to access resources and restricting their niche expansion. Such a pattern was not observed in this study, which may be explained by the specific leaf morphological traits of the dominant species investigated. Field observations revealed that C. carlesii and C. fissa possess broad, ovate to elliptic leaves arranged in dense layers, whereas C. lanceolata has slender needles with a sparser leaf arrangement (Figure S1). Thus, although C. lanceolata exhibited earlier height growth, its narrow leaves and sparse canopy structure may have permitted greater light to penetrate penetration, sustaining light gaps that supported transient species [57,58]. In contrast, despite the slower height growth of C. carlesii and C. fissa in the early phases, their broader leaves and denser foliage might have created an understory light conditions no more favorable than that under C. lanceolata canopies [59]. Additionally, the gradient in height growth increments among the three dominant species may not have been sufficiently pronounced to generate detectable differences in the response of transient species. Although C. lanceolata showed a significantly greater height increment than the other two species between 2000 and 2005, height growth dynamics differences in other periods, limiting the overall effect on transient niche breadth. Our results suggest, the suppressive effect of dominants on the niche expansion of transient species’ niche expansion is not universal, but context-dependent. Multiple interacting factors, including leaf morphology, canopy structure, and magnitude of interspecific growth differentiation shape the outcomes. These findings offer new insight into species coexistence mechanisms following forest disturbance and provide practical guidance for selecting and configuring of dominant species in ecological restoration.

4.2. Changes in Species Richness Were Unrelated to the Dominant Species Growth Dynamics

This study found that the effect of growth of the dominant species on the niche breadth of subordinate and transient species did not significantly explain the changes in species richness. This pattern is probably due to the fact that the impact of the dominant species on the forest ecosystem did not reach critical thresholds. Previous studies have shown that dominant species begin to affect local species richness when their biomass reaches 60% of total forest biomass, with significant effects emerging above 85% [60,61,62]. In our study systems, the basal area proportions of C. carlesii (10.37–27.80%) and C. fissa (1.55–52.77%) within their respective stands (Supplementary Table S3) remained below these thresholds, which may explain why the growth dynamics of dominant species did not show a significant influence on species richness.

Our findings indicate that regeneration mode accounted for most of the variation in species richness (Supplementary Table S4), suggesting that it may be the primary driver underlying differences in species richness among C. carlesii, C. fissa, and C. lanceolata forests. Naturally regenerated C. carlesii forests exhibited high species richness, likely due to post-logging cessation of human disturbance. This recovery strategy promotes stable habitats that enhance subordinate species sprouting and seed germination of subordinate species while facilitating transient species colonization [63,64]. In contrast, assisted natural regenerated C. fissa forests involved low-frequency understory clearing (once annually from 1995 to 1998), which may have suppressed sprouting regeneration of some subordinate species (e.g., Castanopsis, Machilus, and Ormosia) while having a relatively minor effect on seed-dispersed transient species [65,66]. As a result, the forests still maintained relatively high species richness. By comparison, C. lanceolata were managed with intensive site preparation (1994) and high-frequency understory clearing (twice annually from 1995 to 1998). Both practices are known to substantially damage subordinate regeneration and reduce transient species density [67,68], leading to a continuous decline in species richness following clear-cutting.

It is important to note that this study did not account for several environmental variables that may influence species richness, such as spatial distance from reference vegetation, the distribution of logging residues, and the availability of seed resources in the soil [27,69,70]. These factors may indirectly regulate forest species richness by shaping dispersal capacity and germination potential. Future studies should incorporate these environmental drivers to better elucidate the mechanisms underlying species richness maintenance in logged forests.

4.3. Implications for Forest Management

Understanding how dominant tree species shape community diversity is critical for sustainable forest management. In subtropical regions, increasing demand for forest products has led to the conversion of most forests into timber plantations, leaving only strictly forests largely intact [71]. These plantations are commonly established with early-fast growing species such as C. lanceolata and C. fissa [72]. Although this approach ensures high timber yields in the short term, our findings show that it constrains the community niche space and ultimately lowers species diversity over the long-term. For logged forests, promoting communities dominated by late-fast growing species (e.g., C. carlesii) could provide an effective complement to current forest management practices. This study highlights the importance long-term monitoring of forest community dynamics under diverse management regimes, with particular attention to the population trajectories of late-fast growing species, to guide strategies that reconcile timber production with biodiversity conservation.

5. Conclusions

Based on 22-years of long-term monitoring of subtropical forests in eastern China, this study demonstrated the regulatory mechanism of dominant species’ the growth dynamics in shaping community biodiversity. Consistent with our hypothesis, late-fast growing dominant species were more effective than early-fast growing species in enhancing species evenness, primarily by expanding the niche breadth of subordinate species. These results provide empirical supports for the Mass Ratio theory in subtropical forest ecosystems and underscore the pivotal role of dominant species in regulating biodiversity. Our results provide not only an important theoretical understanding, but also practical guidance for ecological restoration, by suggesting that prioritizing late-fast growing species may be a more effective strategy to promote stable and species-rich forests in the region.