
==== Front
PeerJ
PeerJ
peerj
PeerJ
2167-8359
PeerJ Inc. San Diego, USA

17899
10.7717/peerj.17899
Biodiversity
Ecology
Plant Science
Natural Resource Management
Forestry
Stochastic process drives the dissimilarity in biodiversity patterns between Pinus kwangtungensis coniferous forest and evergreen deciduous broad-leaved mixed forest in karst area
Fan Xingying 1
Meng Longchenxi 2
Wang Yeheng 3
Zang Lipeng cafzanglp@163.com
24
1 School of Medicine and Health Management, Guizhou Medical University, Guiyang, Guizhou Province, China
2 Research Center of Forest Ecology, College of Forestry, Guizhou University, Guiyang, Guizhou Province, China
3 Zibo Real Estate Registration Center, Zibo, Shandong Province, China
4 Guizhou Libo Karst Forest Ecosystem National Observation and Research Station, Libo, Guizhou Province, China
Nazareno Alison
30 8 2024
2024
12 e1789923 1 2024
20 7 2024
©2024 Fan et al.
2024
Fan et al.
https://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, reproduction and adaptation in any medium and for any purpose provided that it is properly attributed. For attribution, the original author(s), title, publication source (PeerJ) and either DOI or URL of the article must be cited.

Pinus kwangtungensis is an endangered evergreen conifer tree species, and its in situ conservation has been considered one of the most critical issues. However, relative protection is limited by the lack of understanding of its community structure and underlying assembly processes. To study how the species diversity and assembly processes of Pinus kwangtungensis coniferous forest (CF) differed with regional climax community, this study established a series forest dynamic plots both in CF and evergreen deciduous broadleaved mixed forest (EDBM). By performing comparison analysis and PER-SIMPER approaches, we quantified the differences in species diversity and community assembly rules. The results showed that the species α-diversity of CF differed greatly from the EDBM both in species richness and evenness. In addition, the stochastic process acted a more important role in determining species composition, indicating the uncertainty in presence of species. The soil phosphorus and changeable calcium content were the main factors driving the differences in biodiversity, which the importance of soil nutrient factors in driving species composition. Our study highlighted that we should consider the community structure and ecological process when conducting conservation of Pinus kwangtungensis.

Community assembly rules
Pinus kwangtungensis
Species abundance distribution
Karst forest
Science and Technology Foundation Program of Guizhou Provincial Health Commissiongzwkj2023-482 Guizhou Provincial Key Technology R&D Program[2023]111 This work was supported by the Science and Technology Foundation Program of Guizhou Provincial Health Commission (gzwkj2023-482) and the Guizhou Provincial Key Technology R&D Program ([2023]111). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
==== Body
pmcIntroduction

High species extinction rates emphasize the importance of biodiversity conservation (Chen et al., 2021). However, relative protection is limited due to a lack of understanding of biodiversity patterns and underlying maintenance mechanisms, especially in those vegetation types distributed in special habitats (Alder et al., 2002; Feng et al., 2021). Pinus kwangtungensis, an endangered evergreen conifer tree species, is unique to the southern tropical zone of China. Due to its sensitivity to temperature and precipitation, its native habitat is limited to the southern subtropical zone or the upper part of the tropical northern edge (Wang & Cui, 2023). P. kwangtungensis coniferous forest (CF) typically comprises one dominant species, with high species richness in the understory (Cui et al., 2012). How to perform in situ conservation on such a unique community has been considered an essential issue in biodiversity conservation.

Understanding the community structure and species composition is the basis of biodiversity conservation since they are determined by confusing factors such as interspecific competition or stochastic processes (Feng et al., 2021; Magurran, 2021). Furthermore, biodiversity patterns encompass not only the number of species but also species evenness, indicating species distribution among different communities (He, Legendre & Lafrankie, 2010; McGill, 2011). Previous studies have focused on species richness while neglecting differences in evenness (Chao, Chiu & Jost, 2014; Ulrich et al., 2016). Hence, it is necessary to combine richness and evenness to better represent species diversity patterns, which emphasizes the importance of distinguishing the species composition (Matthews, Borges & Whittaker, 2014; McGill et al., 2007). The species abundance distribution (SAD) curve can display both richness and evenness, providing a visual representation of differences in species diversity patterns among communities (Chisholm et al., 2014; Xue et al., 2021). Since more than one mechanism can shape the SAD curve, quantifying the differences in SAD components can better display the biodiversity pattern and underlying processes (Muhic et al., 2023). For instance, a steep slope of the SAD curve usually alludes to species dominance or commonness, while a long tail of SAD indicates the species rarity (Magurran, 2021; McGill et al., 2007). Species dominance is to what extent the common species predominates the community, while the species rarity reflects the proportion of rare species in community abundance (Simons et al., 2017). Combining the species dominance and rarity can clearly describe species alpha diversity (α-diversity) among communities at regional scales.

Actual communities are formed by complicated ecological processes such as habitat filtering, limiting similarity, or stochastic processes (Chase, 2010; Franklin et al., 2013). Each ecological process influences the species composition and biodiversity patterns. For example, regional species pools can impact community composition, as studies have demonstrated a significant positive correlation between regional species pools and community species richness, serving as the foundation for determining community composition (Zobel, 1997). Interspecific interactions determine the survival and relative abundance of each given species in a local microhabitat (Burton et al., 2011). Abiotic factors reflect the strength of habitat filtering and is a crucial limiting factor in determining species occurrence, which play an important role in shaping community assembly (Su et al., 2023). The niche-based framework suggested that communities were equilibrium assemblages in which interspecific competition for limited resources and other biotic interactions determine the presence of species (Armas, Rodríguez-Echeverría & Pugnaire, 2011; Münkemüller et al., 2020; Ulrich et al., 2016; Zhou & Wang, 2023). On the other hand, the neutral-based assembly framework emphasized that community structure resulted from purely stochastic ecological drift, ultimately leading to ecologically equivalent species resulting from random dispersal and extinction (Hubbell, 2001; Loke & Chisholm, 2023). Recent studies preferred combining the two conflicting perspectives by linking stabilization mechanisms within species and fitness similarities among species after debating for over 20 years (Chesson, 2000; Leibold et al., 2022; Münkemüller et al., 2020). What differed was that which process acted as the first-order driver in the actual community (Loke & Chisholm, 2023; Münkemüller et al., 2020). Since SAD could well reflect the underlying mechanism driving the community structure (McGill et al., 2007; Ulrich et al., 2016), SAD model fitting became a more popular approach to reveal the underlying community assembly rules of local taxonomy, and was used to explain why and to what extent the species composition varied among communities (Gibert & Escarguel, 2019; Magurran, 2021; Matthews et al., 2019; Zhang et al., 2016).

Previous studies examined the community assembly rules mainly by performing SAD fitting on each community and comparing the significance of deviation from the null models to identification of the main first-order driver (i.e., niche- or dispersal-assembly processes) (Chase & Myers, 2011; Lim, Fine & Mittelbach, 2015; Münkemüller et al., 2020). However, typical SAD fitting approaches based on α-diversity could not directly examine which process determined the difference in species composition between two communities. Gibert & Escarguel (2019) developed the permutation-based algorithm building on Clarke’s similarity percentage (PER-SIMPER) (Clarke, 1993) to directly examine which first-order assembly dominates the dissimilarity between communities. An empirical SIMPER profile is the relative contribution of each taxon to the overall average dissimilarity (OAD) between two or more groups of taxonomic assemblages, depicting the contribution of each taxon to the mean inter-group beta diversity (β-diversity) compared with intra-group β-diversity (Clarke, 1993). The PER-SIMPER, which combined the empirical SIMPER profile with null SIMPER profiles generated from permutation on the data set, could well distinguish the first-order assembly driving the dissimilarity between groups of taxonomic assemblages (Gibert & Escarguel, 2019). The SIMPER profiles were generated based on the null hypothesis: (1) the taxon distribution was driven only by the number and breadth of available niche space, indicating the niche-based assembly; (2) the taxon distribution was dominated by the potential dispersal ability, regardless of the niche breadth under assemblage, indicating the dispersal-based assembly. Whether the empirical SIMPER results from niche- or dispersal-assembly processes can be evaluated by comparing the empirical SIMPER profile with the permutation SIMPER profiles (Gibert & Escarguel, 2019).

Recent studies suggested that CF in Maolan National Nature Reserve is far away from its native habitats, and the regional climax community of the natural reserve is subtropical karst evergreen and deciduous broad-leaved mixed forest (EDBM). Therefore, the occurrence of CF and its differences from EDBM have been an interesting issue for ecologists. Previous studies on P. kwangtungensis focused on population, community characteristics, interspecific interactions, limiting habitat factors, and its potential geographical distribution under global climate change (Cui et al., 2012; Hou-Lin et al., 2007; Wang & Cui, 2023; Yuan-Zhi et al., 2006). However, no study currently compared the biodiversity pattern and the underlying community assembly rules between CF and the regional climax community, though these served as the crucial theoretical foundation for the situ conservation of P. kwangtungensis. Therefore, according to the standard manual (Condit, 1998) for the standard handbook of forest dynamic plot (FDPs) establishment, we established a series of FDPs to explore the abovementioned issues (Wang & Cui, 2023). By comparing the species composition and performing SAD fitting, we aimed to solve the questions: (1) to what extent did the CF differ from the EDBM in biodiversity pattern? (2) Whether the niche-based assembly processes determined the difference in species composition between CF and EDBM? (3) Whether the dispersal-based assembly processes determined the difference in species composition between CF and EDBM?

Materials & Methods

Study area and plot establishment

This study was conducted in Maolan National Nature Reserve, Yunnan-Guizhou Plateau, Southwest China. The reserve has a typical subtropical climate, with an annual temperature of 15.1 °C and annual rainfall of 1,374 mm. The highest temperature occurs in July (mean temperature of 15.1 °C), while the lowest is in January (5.2 °C). More than 80% of precipitation concentrates from May to October. Unlike typical subtropical evergreen broad-leaved forests, the karst area forms a different vegetation type with mixed evergreen and deciduous broad-leaved species due to its more heterogeneous habitats and poorer soil conditions. However, the evergreen coniferous forest featured by P. kwangtungensis usually distributes on the upper slopes due to the relatively less soil.

However, due to the greater than 50 m distance between each plot, which aims to avoid the confusing impacts of spatial autocorrelation, and P. kwangtungensis is normally distributed in habitats with higher altitudes or deeper slopes, we only established nine FDPs for both CF and EDBM.

To explore the difference in species diversity pattern between CF and EDBM and find out the driving factors of the difference, we received the field survey approval from the Maolan National Nature Reserve Administration of Guizhou Province and a series of FDPs were established in each vegetation type from September to November 2021. Since the least distance between any two sampling plots should be more than 50 m to avoid the impacts from spatial autocorrelation and ecotone, we established nine 20 m × 20 m FDPs in centralized distribution area of CF. In addition, to ensure the uniformity of repetition, we also established nine 20 m × 20 m FDPs in EDBM. Thus, a total of 18 20 m × 20 m FDPs were established in the study area (Table 1). In each FDP, the information of locations, elevation and soil conditions was recorded. All individuals in the plots were mapped, tagged, and identified to species, Furthermore, the diameter at breast height was measured to calculate species importance value (IV) (Eq. (1)), and determine vegetation community types. (1) IV=Rf+Rd+Rdo/3

where Rf is the relative frequency, Rd is the relative density, Rdo is the relative significance.

10.7717/peerj.17899/table-1 Table 1 Basic information of the established plots: Pinus kwangtungensis coniferous forest (CF); evergreen deciduous broad-leaved mixed forest (EDBM).

Vegetation types	Number	Area (m2)	Elevation (m)	Slope	Latitude	Longitude	
CF	9	400	852–950	20°–60°	25°35′35″–25°36′16″	107°42′21″–107°42′31″	
EDBM	9	400	743–840	7°–32°	25°11′46″–25°14′03″	107°54′55″–107°56′02″	

To explore how the abiotic factors influence the species composition, we collected the top layer of soil (0–20 cm) without the litter at five points in each FDP, and the soil samples were mixed to determine the soil physicochemical properties. A total of five indices, including soil pH value, soil water content, soil total nitrogen content, soil total phosphorus content, and soil exchangeable calcium content were measured. The soil pH was obtained by measuring soil suspension through a pH meter (PH500T, INESA, Shanghai, China). The soil total nitrogen content and soil exchangeable calcium content were determined through Elemental Analyzers (UNICUBE trace, Elementar, Langenselbold, Germany). The soil total phosphorus content was determined spectrophotometrically at 700 nm by a continuous flow automated analyzer (AA3, Bran+Luebbe, Norderstedt, Germany).

Differences in biodiversity patterns between CF and EDBM

Using the Margalef index, Shannon-Wiener index (Eq. (2)), Pielou’s evenness index (Eq. (3)), and rarefied richness (sampled 10 individuals), a one-way analysis of variance (ANOVA) was performed to test the differences in α-diversity between CF and EDBM. Shannon-Wiener index (H) can indicate the diversity pattern of a community due to its sensitivity to variations in species richness and evenness of species abundance. Pielou’s evenness index (E) is usually used to reflect the evenness of species abundance. Rarefied richness is used to characterize the species richness by controlling the confusing effects of sample size (Heck Jr, Van Belle & Simberloff, 1975). Additionally, the skewness of log-transformed species abundance depicts SAD symmetry and better quantifies the shape of SAD (Magurran, 2005). Usually, negative skewness refers to a higher proportion of rare species, while positive skewness reflects strong species dominance compared with a lognormal SAD (Fig. 1).

10.7717/peerj.17899/fig-1 Figure 1 Display of skewness of log-transformed species abundance data depicts SAD symmetry.

Metric multidimensional scaling (MDS) analysis was conducted on obtained SADs to examine the differences in species composition between communities (Norden et al., 2009). The similarity in species composition between types of FDPs was evaluated through the Chao-Jaccard abundance-based estimator (Chao et al., 2005). This approach can find a stable solution using several random starts, and standardizes the scaling in the result by a principal components rotation (Oksanen et al., 2013). This analysis was performed by using the “metaMDS” of the package “vegan” (Oksanen et al., 2013) in R3.4.2 (R Development Core Team, 2022). (2) H=−∑i=1SPilnPi

where s is the total number of species in the plot; Pi is the relative abundance of species i. (3) E=H/Hmax

where H is the actual Shannon-Wiener index while Hmax is the maximum of it, calculated by ln s.

Examination of the first-order assembly process between CF and EDBM

Following the PER-SIMPER framework proposed by Gibert & Escarguel (2019), this study examines the first-order assembly process influencing the dissimilarity in SADs between CF and EDBM. Based on Clarke (1993) SIMPER analysis, Gibert & Escarguel (2019) developed the PER-SIMPER analysis, which introduces a random permutation-based step. SIMPER analysis is a distance-based procedure that computes the relative contribution of each taxon to the OAD among groups of taxonomic assemblages. The Bray–Curtis coefficient for abundance was employed in SIMPER analysis to quantify the contribution of each taxon to the dissimilarity among groups of taxonomic assemblages (Clarke, 1993; Legendre & Legendre, 1998). Utilizing the empirical SIMPER pattern of a taxon locality occurrence data set, the PER-SIMPER analyzes 1,000 independently randomized occurrence data tables by fixing column or row to form the null SIMPER profile distribution (95% confidence intervals) of dispersal- and niche-assembly process. In addition, both sample richness and taxon uniquity remained unchanged under a maximally constrained null model. A third null SIMPER profile distribution was generated, corresponding to the null hypothesis that both dispersal- and niche-assembly processes dominate the taxonomic assembly. The null distribution closest to (if not including) the empirical SIMPER profile indicates the primary driver contributing to the observed taxonomic occurrence structuring among groups (details about the null permutation can be found in the paper of Gibert & Escarguel (2019)). For each permutation model, the empirical SIMPER profile is compared with the null SIMPER profiles by computing the logarithm of the sum of squared deviations between two profiles (E is as follows): E=Log10∑i=1i=pγ¯inull−γ¯iobs2

where γ¯i=δiδ¯ is the contribution of the ratio of δ to the mean of δ. Lower E indicates a closer similarity between the two compared SIMPER profiles. Thus, a PER-SIMPER analysis was conducted on SADs between CF and EDBM, using the “PER-SIMPER” function in R3.4.2 software (R Development Core Team, 2022).

Determination of abiotic factors on α-diversity

Redundancy analysis (RDA) is a multivariate statistical approach based on principal component analysis that is used to examine the correlation between explanatory variables (i.e., environmental factors) and response variables (i.e., species composition). Abiotic factors could play a crucial various role in shaping community structure (Xu et al., 2018). Therefore, RDA was used to examine the influence of soil physicochemical properties on dissimilarities in species composition between CF and EDBM in this study. This analysis was performed with the “vegan” package in R3.4.2 (R Development Core Team, 2022).

Results

Difference in α-diversity between CF and EDBM

CF had a total of 46 species and was dominated by P. kwangtungensis, with an IV of 0.43. EDBM had a total of 128 species and was dominated by Boniodendron minus, with an IV of 0.06 (File S2). By comparing species diversity between CF and EDBM, significant differences were found in the Shannon-Wiener index, Margalef richness, Pielou evenness, rarefied richness, and skewness (Fig. 2), indicating significant differences in both components (species richness and evenness) of α-diversity between CF and EDBM. Even after controlling the impacts of abundance, the species richness of EDBM was still significantly higher than that of CF (Fig. 2D). In addition, the EDBM showed higher species dominance compared to CF (Fig. 2E). MDS result also showed that the species composition of CF was significantly different from that of EDBM (Fig. 2F).

10.7717/peerj.17899/fig-2 Figure 2 α-diversity between CF and EDBM.

(A) The Shannon–Weiner index; (B) the Margalef richness; (C) the Pielou Evenness; (D) the rarefied species richness; (E) the skewness between communities; (F) the species composition between communities. The red box reflected the Pinus kwangtungensis. coniferous forest (CF), while the blue box indicated the subtropical karst evergreen and deciduous broad-leaved mixed forest (EDBM). Significant differences were marked by different letters.

First-order assembly processes driving dissimilarity in species composition between CF and EDBM

Results of PER-SIMPER analysis showed that the lowest E-values for dispersal- and niche-assembly profile, indicating that both niche-assembly and dispersal-assembly processes drove the dissimilarity in species composition between CF and EDBM (Fig. 3). Additionally, compared with niche-assembly process, the dispersal-assembly process had a lower E-values, indicating a more contribution of dispersal-assembly process to the dissimilarity in species composition.

10.7717/peerj.17899/fig-3 Figure 3 Results of PER-SIMPER analysis.

The orange box indicated the dispersal-assembly process, while the black box indicated the niche-assembly process. The blue box represented both processes dominating the first-order assembly process. Lower E-values showed a more significant influence of the process on the dissimilarities between groups of plots.

Abiotic factors influencing the α-diversity

Results of RDA showed that the soil physicochemical properties determined the difference in α-diversity between CF and EDBM (Fig. 4). Additionally, the soil exchangeable calcium content, soil total phosphorus content, soil water content, and soil pH value had influence on the difference in α-diversity. Specifically, soil exchangeable calcium content and soil total phosphorus content showed a positive relationship with Margalef index, and a negative relationship with the other α-diversity indices. Soil total nitrogen had a relatively minor impact on the community composition.

10.7717/peerj.17899/fig-4 Figure 4 Results of RDA.

The α-diversity indices were denoted by red letters, while the groups of plots were shown in black letters. The blue lines indicated the soil physicochemical properties.

Discussion

This study compared the α-diversity, identified the first-order assembly process, and revealed the strong uniqueness in CF. However, both niche-assembly and dispersal-assembly process drove the dissimilarity in species composition between CF and EDBM, with the dispersal-assembly process making a greater contribution. The results indicate that there is a high degree of uncertainty in the occurrence of species within the CF community, particularly for rare species.

Difference in α-diversity between CF and regional climax community

By comparing the CF with a typical regional climax community (EDBM), it was found that both the species richness and evenness of the CF were significantly lower (Fig. 2). The average individual density of the CF (0.297 individuals/m2) was also lower than that of the EDBM (0.377 individuals/m2). According to the species–energy hypothesis (Akatov et al., 2023), more individuals would increase species accumulation within the same regional scope, which might be one possible reason for the higher species richness of EDBM compared to CF (Chu et al., 2019; McGill, 2011). However, the rarefied richness of the EDBM was notably higher than that of the CF, indicating that the species richness of the CF remained lower even after controlling the cumulative effects of individuals. The biotic and abiotic filtering frameworks may play an important role (Münkemüller et al., 2020). The dominance of the CF was markedly lower than that of the EDBM, showing a high dominance of the EDBM (Fig. 3). The higher abundance and larger size of individuals compressed the ecological niche space of other species, indicating a much higher competitive ability of P. kwangtungensis compared to others, which limited colonization and survival of other species and formed monodominant species pattern (Stanley Harpole & Tilman, 2006; Wang & Cui, 2023). Similar patterns have been found in many evergreen coniferous forests, such as naturally occurring Pinus roxburghii forests in tropical regions, as well as artificially planted forests such as Pinus massoniana, Cryptomeria japonica, and Cunninghamia lanceolata, where evergreen coniferous species dominate and exhibit low species richness patterns (Sloan, Zimmerman & Sabat, 2007; Wang & Cui, 2023; Zang et al., 2021b). Meanwhile, the lack of subdominant species in CF allowed the colonization of rare species, contributing more to the difference in species composition (Lamanna et al., 2017; Zhang et al., 2014). This phenomenon could also be a primary factor leading to the scarcity of species under such biotic conditions. Some researchers have pointed out that evergreen coniferous species commonly exhibit allelopathy, which could inhibit the establishment of other tree species, thereby reducing species richness (Ehlers, Charpentier & Grøndahl, 2013). Other studies also showed that poor light resources and soil conditions in evergreen coniferous forests could also be limiting factors for species diversity patterns. For example, low light resource quality in evergreen coniferous forests limits the establishment of shade-tolerant tree species (Loke & Chisholm, 2023; Wang & Cui, 2023). This study showed that the CF had almost no shade-tolerant pioneer tree species, which supported the view to some extent. In addition, the CF is shade-intolerant, similar to deciduous broad-leaved tree species in eco-strategy. Therefore, the presence of CF somewhat restricts the ecological niche space of deciduous broad-leaved tree species, reducing species richness (especially in broad-leaved tree species (Cui et al., 2012; Wang & Cui, 2023)). In contrast, the EDBM is mixed with both evergreen and deciduous broad-leaved tree species. More deciduous broad-leaved tree species can increase species richness and evenness, resulting in a higher level of species diversity. Such diversity patterns also emphasized the importance of considering reducing deciduous tree species when performing P. kwangtungensis conservation to reduce the severe competition for lights. High habitat heterogeneity can also change species diversity patterns (Bar-Massada, Kent & Carmel, 2014; Brown et al., 2013). The habitat heterogeneity hypothesis suggests that increasing heterogeneity leads to an increase in small habitat types that can support plant growth and survival. The differing quality of small habitats can support the survival of different life forms, thereby maintaining a higher level of diversity (Bar-Massada, Kent & Carmel, 2014; Franklin et al., 2013). This study found that although both the CF and the EDBM were formed on limestone (as the parent rock), the microhabitat of the CF was relatively homogeneous without the presence of gullies, exposed rocks, or surface patterns. The EDBM exhibited higher levels of horizontal habitat heterogeneity, which provided a non-biological environmental foundation for maintaining diversity patterns and further promoted greater species diversity (Bar-Massada, Kent & Carmel, 2014; Brown et al., 2013; Franklin et al., 2013; Wang & Cui, 2023).

First-order assembly process driving the dissimilarity in species composition

The results showed that both the CF and the EDBM were primarily driven by dispersal- and niche-assembly processes, with the stochastic process playing a slightly larger role in determining species composition differences (Fig. 3). This indicated that the community assembly of CF may be mainly controlled by stochastic processes relative to deterministic processes. The CF community exhibited monodominance with a sharp decline in the number of individuals of other species (Fig. 2E). Both results indicated that apart from P. kwangtungensis, the number of individuals of other tree species was extremely few, with a significant variation in presence between plots (Fig. 2F). This reflected the uncertainty of companion species in the CF, indicating strong stochasticity on the occurrence of other species (Matthews et al., 2019; McGill, 2011). From the perspective of species occurrence, neutral processes dominate the probability of occurrence of most species, especially the rare species. These results could also be driven by demographic, phylogenetic and biogeographic histories of individuals, populations and species. In contrast, the EDBM are mostly common species sharing the same regional species pool (Chen et al., 2019). Functional traits adapt to variations in abiotic factors, while convergence of a trait value suggests co-occurring species often appeared in similar abiotic conditions, leading to stronger habitat filtering (Pappas, Fatichi & Burlando, 2016; Xu et al., 2018). Therefore, changes in functional traits and abiotic factors may by one of the factors in community assembly process. Maolan National Nature Reserve is a typical karst area where strong habitat filtering effects and habitat heterogeneity restrict the dispersal and colonization of most species (Gu et al., 2019; Wang et al., 2023). When species disperse into this region, which species become companion species is largely randomized in CF. Thus, although the α-diversity of CF is totally different from that of the EDBM, no certain evidence was found to support the necessity of such patterns.

Abiotic factors driving the difference in α-diversity

The results of this study showed that the soil exchangeable calcium content and soil total phosphorus content were the main factors driving the difference in α-diversity between the CF and EDBM. Previous studies showed that the phosphorus content of soils was the limiting factor on species diversity in tropical or subtropical forests (Wang et al., 2023; Zang et al., 2021a). However, our results indicated that the soil total nitrogen content had no effect on the regional difference in species diversity among different vegetation types (Fig. 4). The varied speeds of biological cycles in different soil nutrients might be one possible reason (Alvarez-Clare, Mack & Brooks, 2013; Wang et al., 2023). The view of phosphorus limitation was mainly due to the relatively slow phosphorus cycle (Alvarez-Clare, Mack & Brooks, 2013). Previous studies showed that the soil available phosphorus came from rock decay, which was relatively slow and limited the speed of phosphorus cycling (Laliberté et al., 2015; Zotz & Asshoff, 2010). More phosphorus was fixed in the plant tissue with increasing biomass, decreasing the available phosphorus content (Alvarez-Clare, Mack & Brooks, 2013). Additional studies suggested that the H2PO42− tended to form insoluble complexes with Al3+ or Fe3+ under acidic soils (Laliberté et al., 2015; Zang et al., 2021a). However, our previous studies on karst restoration showed no significant phosphorus limitation, as nitrogen cycling may be more limiting to nutrient content than phosphorus cycling (Laliberté et al., 2015; Turner, Brenes-Arguedas & Condit, 2018; Wang et al., 2023). Such nitrogen limitation also supported the idea that the EDBM still performed potential succession compared with subtropical evergreen broad-leaved forests. Thus, the soil nitrogen content might dominate the soil fertility, driving the species diversity patterns. In addition, higher calcium content has been one key component of soil physicochemical properties in karst areas. A growing body of studies showed that diversity had a higher dependence on the soil calcium content (Batalha et al., 2015; Guo et al., 2019; Guo et al., 2017; Guo et al., 2015), which is also clearly demonstrated in this study.

Conclusions

P. kwangtungensis is an endangered species which has a narrow distribution. This study quantified the differences in species diversity and community assembly between the P. kwangtungensis coniferous forest and the evergreen and deciduous broadleaved forest within the Maolan National Nature Reserve, and found that the P. kwangtungensis coniferous forest had a lower species richness and evenness compared with the evergreen and deciduous broadleaved forest in the same reserve. However, such difference resulted possibly from both stochastic processes and deterministic processes with stochastic processes contributing more. Thus, our study suggested that the stochastic processes dominated the difference in species composition between the two vegetation types, indicating to a certain extent, the auxiliary species contributing less in shaping P. kwangtungensis community structure. Such patterns emphasized the importance of tree species selection in P. kwangtungensis conservation. In addition, our study suggested that soil calcium and phosphorus contents played more important roles in driving species diversity pattern of P. kwangtungensis coniferous forest in local scales, emphasizing the importance of soil fertile in driving the species pattern and community assembly rules, as well as its growth, development and distribution. Therefore, we should consider more whether the soil nutrient conditions could well meet the requirements of Pinus kwangtungensis when conducting conservation projects.

Plant functional traits could be another effective perspective in determining community assembly rules, due to it is more sustainable to changes in environments. However, our study quantified the community assembly rules based on the species abundance distribution, which might lack of the information of how the traits respond to the various habitats. Further analysis should perform the verification both from the phylogenic and functional perspective.

Supplemental Information

10.7717/peerj.17899/supp-1 File S1 Species abundance of Pinus kwangtungensis and conifer-broadleaf forest

10.7717/peerj.17899/supp-2 File S2 Species importance value (IV) of different vegetation types: Pinus kwangtungensis coniferous forest (CF); evergreen deciduous broad-leaved mixed forest (EDBM)

We thank the Maolan National Nature Reserve Administration of Guizhou Province for the assistance with the establishment of our forest dynamic plots, as well as ensuring our safety in the field. We thank Essentialslink Language Services for its linguistic assistance during the preparation of this manuscript. Lastly, we extend our appreciation to the reviewers for providing valuable feedback on the manuscript.

Additional Information and Declarations

Competing Interests

Author Contributions

Data Availability

Yeheng Wang is employed by Zibo Real Estate Registration Center.

Xingying Fan analyzed the data, prepared figures and/or tables, authored or reviewed drafts of the article, and approved the final draft.

Longchenxi Meng analyzed the data, prepared figures and/or tables, authored or reviewed drafts of the article, and approved the final draft.

Yeheng Wang analyzed the data, authored or reviewed drafts of the article, and approved the final draft.

Lipeng Zang conceived and designed the experiments, analyzed the data, prepared figures and/or tables, authored or reviewed drafts of the article, and approved the final draft.

The following information was supplied regarding data availability:

Raw data showing species abundance in Pinus kwangtungensis and conifer-broadleaf forests are available in the Supplemental Files.
==== Refs
References

Akatov et al. (2023) Akatov VV Akatova TV Afanasyev DF Eskina TG Sazonets NM Sushkova EG Chefranov SG 2023 Effect of dominants on the species richness of plant communities in the context of the species-energy hypothesis Biology Bulletin Reviews 13 238 246 10.1134/S2079086423030027
Alder et al. (2002) Alder D Oavika F Sanchez M Silva JNM Van der Hout P Wright HL 2002 A comparison of species growth rates from four moist tropical forest regions using increment-size ordination International Forestry Review 4 196 205 10.1505/IFOR.4.3.196.17398
Alvarez-Clare, Mack & Brooks (2013) Alvarez-Clare S Mack MC Brooks M 2013 A direct test of nitrogen and phosphorus limitation to net primary productivity in a lowland tropical wet forest Ecology 94 1540 1551 10.1890/12-2128.1 23951714
Armas, Rodríguez-Echeverría & Pugnaire (2011) Armas C Rodríguez-Echeverría S Pugnaire FI 2011 A field test of the stress-gradient hypothesis along an aridity gradient Journal of vegetation science 22 818 827 10.1111/j.1654-1103.2011.01301.x
Bar-Massada, Kent & Carmel (2014) Bar-Massada A Kent R Carmel Y 2014 Environmental heterogeneity affects the location of modelled communities along the niche–neutrality continuum Proceedings of the Royal Society of London B 281 20133249
Batalha et al. (2015) Batalha M Pipenbaher N Bakan B Kaligarič M Škornik S 2015 Assessing community assembly along a successional gradient in the North Adriatic Karst with functional and phylogenetic distances Oecologia 178 1205 1214 10.1007/s00442-015-3295-5 25800875
Brown et al. (2013) Brown C Burslem D Illian J Bao L Brockelman W Cao M Chang L Dattaraja H Davies S Gunatilleke C 2013 Multispecies coexistence of trees in tropical forests: spatial signals of topographic niche differentiation increase with environmental heterogeneity Proceedings of the Royal Society of London B 280 20130502 10.1098/rspb.2013.0502
Burton et al. (2011) Burton JI Mladenoff DJ Clayton MK Forrester JA 2011 The roles of environmental filtering and colonization in the fine-scale spatial patterning of ground-layer plant communities in north temperate deciduous forests Journal of Ecology 99 764 776 10.1111/j.1365-2745.2011.01807.x
Chao et al. (2005) Chao A Chazdon RL Colwell RK Shen TJ 2005 A new statistical approach for assessing compositional similarity based on incidence and abundance data Ecology Letters 8 148 159 10.1111/j.1461-0248.2004.00707.x
Chao, Chiu & Jost (2014) Chao A Chiu C-H Jost L 2014 Unifying species diversity, phylogenetic diversity, functional diversity, and related similarity and differentiation measures through Hill numbers Annual Review of Ecology, Evolution, and Systematics 45 297 324 10.1146/annurev-ecolsys-120213-091540
Chase (2010) Chase JM 2010 Stochastic community assembly causes higher biodiversity in more productive environments Science 328 1388 1391 10.1126/science.1187820 20508088
Chase & Myers (2011) Chase JM Myers JA 2011 Disentangling the importance of ecological niches from stochastic processes across scales Philosophical Transactions of the Royal Society B 366 2351 2363 10.1098/rstb.2011.0063
Chen et al. (2019) Chen L Swenson NG Ji N Mi X Ren H Guo L Ma K 2019 Differential soil fungus accumulation and density dependence of trees in a subtropical forest Science 366 124 128 10.1126/science.aau1361 31604314
Chen et al. (2021) Chen Y Wang Y Liew JH Wang PL 2021 Development of a methodological framework for evaluating biodiversity of built urban green infrastructures by practitioners Journal of Cleaner Production 303 127009 10.1016/j.jclepro.2021.127009
Chesson (2000) Chesson P 2000 Mechanisms of maintenance of species diversity Annual Review of Ecology and Systematics 31 343 366 10.1146/annurev.ecolsys.31.1.343
Chisholm et al. (2014) Chisholm RA Condit R Rahman KA Baker PJ Bunyavejchewin S Chen Y-Y Chuyong G Dattaraja HS Davies S Ewango CEN Gunatilleke CVS Nimal Gunatilleke IAU Hubbell S Kenfack D Kiratiprayoon S Lin Y Makana J-R Pongpattananurak N Pulla S Punchi-Manage R Sukumar R Su S-H Sun IF Suresh HS Tan S Thomas D Yap S 2014 Temporal variability of forest communities: empirical estimates of population change in 4000 tree species Ecology Letters 17 855 865 10.1111/ele.12296 24805976
Chu et al. (2019) Chu C Lutz JA Král K Vrška T Yin X Myers JA Abiem I Alonso A Bourg N Burslem DFRP Cao M Chapman H Condit R Fang S Fischer GA Gao L Hao Z Hau BCH He Q Hector A Hubbell SP Jiang M Jin G Kenfack D Lai J Li B Li X Li Y Lian J Lin L Liu Y Liu Y Luo Y Ma K McShea W Memiaghe H Mi X Ni M O’Brien MJ De Oliveira AA Orwig DA Parker GG Qiao X Ren H Reynolds G Sang W Shen G Su Z Sui X Sun IF Tian S Wang B Wang X Wang X Wang Y Weiblen GD Wen S Xi N Xiang W Xu H Xu K Ye W Zhang B Zhang J Zhang X Zhang Y Zhu K Zimmerman J Storch D Baltzer JL Anderson-Teixeira KJ Mittelbach GG He F 2019 Direct and indirect effects of climate on richness drive the latitudinal diversity gradient in forest trees Ecology Letters 22 245 255 10.1111/ele.13175 30548766
Clarke (1993) Clarke KR 1993 Non-parametric multivariate analyses of changes in community structure Australian Journal of Ecology 18 117 143 10.1111/j.1442-9993.1993.tb00438.x
Condit (1998) Condit R 1998 Tropical forest census plots: methods and results from Barro Colorado Island, Panama and a comparison with other plots Springer Science & Business Media New York
Cui et al. (2012) Cui TAO Xiao-Xiao LI Qing-Chun W Guo-Fa CUI 2012 Relationships between geographical distribution of endangered Pinus kwangtungensis and climate in China Plant Science Journal 30 577 583 10.3724/SP.J.1142.2012.60577
Ehlers, Charpentier & Grøndahl (2013) Ehlers BK Charpentier A Grøndahl E 2013 An allelopathic plant facilitates species richness in the Mediterranean garrigue Journal of Ecology 102 176 185
Feng et al. (2021) Feng G Huang J Xu Y Li J Zang R 2021 Disentangling environmental effects on the tree species abundance distribution and richness in a subtropical forest Frontiers in plant science 12 622043 10.3389/fpls.2021.622043 33828571
Franklin et al. (2013) Franklin J Keppel G Webb EL Seamon JO Rey SJ Steadman DW Wiser SK Drake DR 2013 Dispersal limitation, speciation, environmental filtering and niche differentiation influence forest tree communities in West Polynesia Journal of Biogeography 40 988 999 10.1111/jbi.12038
Gibert & Escarguel (2019) Gibert C Escarguel G 2019 PER-SIMPER—a new tool for inferring community assembly processes from taxon occurrences Global Ecology and Biogeography 28 374 385 10.1111/geb.12859
Gu et al. (2019) Gu L-P Kong J-J Chen K Guo Y-Q 2019 Monitoring soil biological properties during the restoration of a phosphate mine under different tree species and plantation types Ecotoxicology and Environmental Safety 180 130 138 10.1016/j.ecoenv.2019.05.001 31082576
Guo et al. (2019) Guo Y Chen HYH Mallik AU Wang B Li D Xiang W Li X 2019 Predominance of abiotic drivers in the relationship between species diversity and litterfall production in a tropical karst seasonal rainforest Forest Ecology and Management 449 117452 10.1016/j.foreco.2019.117452
Guo et al. (2017) Guo Y Wang B Mallik AU Huang F Xiang W Ding T Wen S Lu S Li D He Y Li X 2017 Topographic species–habitat associations of tree species in a heterogeneous tropical karst seasonal rain forest, China Journal of Plant Ecology 10 450 460 10.1093/jpe/rtw057
Guo et al. (2015) Guo Y Wang B Xiang W Ding T Lu S Huang F Li D Wen S He Y Li X 2015 Density-dependent effects of tree species in a 15 ha seasonal rain forest plot in northern tropical karst in Nonggang, Guangxi, southern China Chinese Science Bulletin 60 1602 1611 10.1360/N972014-00892
He, Legendre & Lafrankie (2010) He F Legendre P Lafrankie JV 2010 Spatial pattern of diversity in a tropical rain forest in Malaysia Journal of Biogeography 23 57 74
Heck Jr, Van Belle & Simberloff (1975) Heck Jr KL Van Belle G Simberloff D 1975 Explicit calculation of the rarefaction diversity measurement and the determination of sufficient sample size Ecology 56 1459 1461 10.2307/1934716
Hou-Lin et al. (2007) Hou-Lin W Shen-Yu M Min D Bin Z Xiao-Qing S Jian-Ting FU 2007 Ecological characteristics of Pinus kwangtungensis community at Yang dongshan-Shierdushui Nature Reserve, Lechang, Guangdong Ecological Science 26 2 115 119
Hubbell (2001) Hubbell SP 2001 The unified neutral theory of biodiversity and biogeography Princeton University Press Princeton
Laliberté et al. (2015) Laliberté E Lambers H Burgess TI Wright SJ 2015 Phosphorus limitation, soil-borne pathogens and the coexistence of plant species in hyperdiverse forests and shrublands New Phytologist 206 507 521 10.1111/nph.13203 25494682
Lamanna et al. (2017) Lamanna JA Mangan SA Alonso A Bourg NA Brockelman WY Bunyavejchewin S Chang LW Chiang JM Chuyong GB Clay K 2017 Plant diversity increases with the strength of negative density dependence at the global scale Science 356 1389 1392 10.1126/science.aam5678 28663501
Legendre & Legendre (1998) Legendre P Legendre L 1998 Numerical ecology Elsevier Science Amsterdam
Leibold et al. (2022) Leibold MA Govaert L Loeuille N Meester LD Urban MC 2022 Evolution and community assembly across spatial scales Annual Review of Ecology, Evolution, and Systematics 53 299 326 10.1146/annurev-ecolsys-102220-024934
Lim, Fine & Mittelbach (2015) Lim JY Fine PVA Mittelbach GG 2015 Assessing the latitudinal gradient in herbivory Global Ecology and Biogeography 24 1106 1112 10.1111/geb.12336
Loke & Chisholm (2023) Loke LHL Chisholm RA 2023 Unveiling the transition from niche to dispersal assembly in ecology Nature 618 537 542 10.1038/s41586-023-06161-x 37286612
Magurran (2005) Magurran AE 2005 Species abundance distributions: pattern or process? Functional Ecology 19 177 181 10.1111/j.0269-8463.2005.00930.x
Magurran (2021) Magurran AE 2021 Measuring biological diversity Current Biology 31 R1174 R1177 10.1016/j.cub.2021.07.049 34637726
Matthews, Borges & Whittaker (2014) Matthews TJ Borges PA Whittaker RJ 2014 Multimodal species abundance distributions: a deconstruction approach reveals the processes behind the pattern Oikos 123 533 544 10.1111/j.1600-0706.2013.00829.x
Matthews et al. (2019) Matthews TJ Sadler JP Kubota Y Woodall CW Pugh TAM 2019 Systematic variation in North American tree species abundance distributions along macroecological climatic gradients Global Ecology and Biogeography 28 601 611 10.1111/geb.12879
McGill (2011) McGill BJ 2011 Linking biodiversity patterns by autocorrelated random sampling American Journal of Botany 98 481 502 10.3732/ajb.1000509 21613141
McGill et al. (2007) McGill BJ Etienne RS Gray JS Alonso D Anderson MJ Benecha HK Dornelas M Enquist BJ Green JL He F Hurlbert AH Magurran AE Marquet PA Maurer BA Ostling A Soykan CU Ugland KI White EP 2007 Species abundance distributions: moving beyond single prediction theories to integration within an ecological framework Ecology Letters 10 995 1015 10.1111/j.1461-0248.2007.01094.x 17845298
Muhic et al. (2023) Muhic F Ala-Aho P Noor K Welker JM Klöve B Marttila H 2023 Flushing or mixing? Stable water isotopes reveal differences in arctic forest and peatland soil water seasonality Hydrological Processes 37 e14811 10.1002/hyp.14811
Münkemüller et al. (2020) Münkemüller T Gallien L Pollock LJ Barros C Carboni M Chalmandrier L Mazel F Mokany K Roquet C Smyčka J Talluto MV Thuiller W 2020 Dos and don’ts when inferring assembly rules from diversity patterns Global Ecology and Biogeography 29 1212 1229 10.1111/geb.13098
Norden et al. (2009) Norden N Chazdon RL Chao A Jiang Y-H Vílchez-Alvarado B 2009 Resilience of tropical rain forests: tree community reassembly in secondary forests Ecology Letters 12 385 394 10.1111/j.1461-0248.2009.01292.x 19379133
Oksanen et al. (2013) Oksanen J Blanchet FG Kindt R Legendre P Minchin PR O’Hara RB Simpson GL Solymos P Stevens MHH Wagner H 2013 vegan: community ecology package http://vegan.r-forge.r-project.org/ R package version 2.0-7
Pappas, Fatichi & Burlando (2016) Pappas C Fatichi S Burlando P 2016 Modeling terrestrial carbon and water dynamics across climatic gradients: does plant trait diversity matter? New Phytologist 209 137 151 10.1111/nph.13590 26389742
R Development Core Team (2022) R Development Core Team 2022 R: A language and environment for statistical computing. 4.2.1 ed R Foundation for Statistical Computing Vienna
Simons et al. (2017) Simons NK Lewinsohn T Blüthgen N Buscot F Boch S Daniel R Gossner MM Jung K Kaiser K Müller J Prati D Renner SC Socher SA Sonnemann I Weiner CN Werner M Wubet T Wurst S Weisser WW 2017 Contrasting effects of grassland management modes on species-abundance distributions of multiple groups Agriculture, Ecosystems & Environment 237 143 153 10.1016/j.agee.2016.12.022
Sloan, Zimmerman & Sabat (2007) Sloan SA Zimmerman JK Sabat AM 2007 Phenology of Plumeria alba and its herbivores in a tropical dry forest Biotropica 39 195 201 10.1111/j.1744-7429.2006.00249.x
Stanley Harpole & Tilman (2006) Stanley Harpole W Tilman D 2006 Non-neutral patterns of species abundance in grassland communities Ecology Letters 9 15 23 10.1111/j.1461-0248.2005.00836.x 16958864
Su et al. (2023) Su L Du H Zeng F Peng W Wang H Wang K Lu M Song T 2023 Environmental and spatial contributions to tree community assembly across life stages and scales in evergreen-deciduous broadleaf karst forests, southwest China Journal of Forestry Research 34 1323 1331 10.1007/s11676-022-01587-x
Turner, Brenes-Arguedas & Condit (2018) Turner BL Brenes-Arguedas T Condit R 2018 Pervasive phosphorus limitation of tree species but not communities in tropical forests Nature 555 7696 367 370 10.1038/nature25789 29513656
Ulrich et al. (2016) Ulrich W Kusumoto B Shiono T Kubota Y 2016 Climatic and geographic correlates of global forest tree species–abundance distributions and community evenness Journal of Vegetation Science 27 295 305 10.1111/jvs.12346
Wang et al. (2023) Wang S Chen D Liu Q Zang L Zhang G Sui M Dai Y Zhou C Li Y Yang Y Ding F 2023 Dominant influence of plants on soil microbial carbon cycling functions during natural restoration of degraded karst vegetation Journal of Environmental Management 345 118889 10.1016/j.jenvman.2023.118889 37666128
Wang & Cui (2023) Wang J Cui G 2023 Protection mechanism and empirical study on the endangered status of Pinus kwangtungensis Agronomy Journal 115 71 80 10.1002/agj2.21102
Xu et al. (2018) Xu J Chai Y Wang M Dang H Guo Y Chen Y Zhang C Li T Zhang L Yue M 2018 Shifts in plant community assembly processes across growth forms along a habitat severity gradient: a test of the plant functional trait approach Frontiers in Plant Science 9 180 10.3389/fpls.2018.00180 29497437
Xue et al. (2021) Xue R Zhao K Yu X Stirling E Liu S Ye S Ma B Xu J 2021 Deciphering sample size effect on microbial biogeographic patterns and community assembly processes at centimeter scale Soil Biology and Biochemistry 156 108218 10.1016/j.soilbio.2021.108218
Yuan-Zhi et al. (2006) Yuan-Zhi Y Lu Z Bei-Guang C Zhi-Yao S 2006 Characteristics of rare and endangered Pinus kwangtungensis forest Journal of South China Agricultural University 27 70 73
Zang et al. (2021a) Zang L Xu H Li Y Zang R 2021a Conspecific negative density dependence of trees varies with plant functional traits and environmental conditions across scales in a 60-ha tropical rainforest dynamics plot Biotropica 53 693 702 10.1111/btp.12910
Zang et al. (2021b) Zang L Zhang G He Y Liu Q Chen D 2021b Effects of close-to-nature namagement on biodiversity and species coexistence of shrubs and herbs in Pinus massoniana monoculture plantations of Central Guizhou Journal of Mountain Agriculture and Biology 40 21 28
Zhang et al. (2014) Zhang J Cheng K Zang R Ding Y 2014 Environmental filtering of species with different functional traits into plant assemblages across a tropical coniferous-broadleaved forest ecotone Plant and Soil 380 361 374 10.1007/s11104-014-2088-7
Zhang et al. (2016) Zhang S Zang R Huang Y Ding Y Huang J Lu X Liu W Long W Zhang J Jiang Y 2016 Diversity maintenance mechanism changes with vegetation type and the community size in a tropical nature reserve Ecosphere 7 1 15
Zhou & Wang (2023) Zhou L Wang S 2023 The bright side of ecological stressors Trends in Ecology & Evolution 38 568 578 10.1016/j.tree.2023.01.010 36906435
Zobel (1997) Zobel M 1997 The relative of species pools in determining plant species richness: an alternative explanation of species coexistence? Trends in Ecology & Evolution 12 266 269 10.1016/S0169-5347(97)01096-3 21238064
Zotz & Asshoff (2010) Zotz G Asshoff R 2010 Growth in epiphytic bromeliads: response to the relative supply of phosphorus and nitrogen Plant Biology 12 108 113 10.1111/j.1438-8677.2009.00216.x 20653893
