Tropical forests are vulnerable in terms of functional redundancy
Introduction
Understanding the relationship between biodiversity and ecosystem function can contribute to the designing of conservation for tropical ecosystems (Slade et al., 2011). Quantifying and understanding this relationship is important, because the development of human society has been almost always accompanied by loss of species and their natural habitats (Cardinale et al., 2012). In ecosystems, species with different traits syndromes may perform different functions, thus, the loss of biodiversity will have a direct impact on ecosystem functioning. Understanding the ecosystem functioning not only considers the number of species, but also the functional characteristics of each species. Functional traits are defined as morpho-physio-phenological traits which influence fitness through their effect on individual performance including growth, survival, and reproduction in a given habitat (Schmitt et al., 2020; Violle et al., 2007). These traits are important in species' response to environmental changes, and their effects on ecological processes (Lohbeck et al., 2012). Functional diversity (FD) refers to the variation of traits between species or organisms in functional spaces (Carmona et al., 2016b). FD is a vital factor affecting ecosystem maintenance and function, and could reflect the resource dynamics, stability, anti-interference ability and resilience of ecosystems (Sanaphre-Villanueva et al., 2016; Schmitt et al., 2019). FD combines species and ecosystem properties, thus, various ecosystem functions, could be analyzed by using different combinations of traits, which played an important role in revealing the interaction mechanism between biodiversity and ecosystem functioning (Mason et al., 2013). FD could be decomposed into three primary components, including functional richness, functional evenness and functional dispersion (Carmona et al., 2016b). Each of the three indices provides different facets of information about the distribution of species in functional traits space (Mason et al., 2012).
The importance of diversity in controlling the stability of ecosystems has been a focus of debate (Flöder and Hillebrand, 2012; Mougi and Kondoh, 2012). However, it is consensus that the loss of a single species or functional groups can lead to degradation of ecosystem functions (González-Maya et al., 2016). The framework of functional redundancy is central in theories connecting changes in ecosystem function with species loss (Rosenfeld, 2002). The loss of particular functions caused by species loss might threaten ecosystem processes more serious than the loss of species per se (Naeem et al., 2012). Functional redundancy refers to the diversity of species performing similar functions in an ecosystem (Pillar et al., 2013). It depends on how species are distributed across functional groups (Fonseca and Ganade, 2001; Guillemot et al., 2011). Functional redundancy may ensure that the loss of ecosystem functions caused by some species loss be compensated (Mouillot et al., 2014). The level of functional redundancy in community could modulate the effects of local species loss on community stability. Species loss should have no impact if many species perform similar functions, but have critical effect if each species performs unique functions (Fonseca and Ganade, 2001). In contrast, low level of functional redundancy might cause a potential decrease of functional diversity following species loss, thus resulting in ecosystem functions vulnerability. Changes in richness of species with differing functional traits can affect the functional composition of communities, with important consequences for ecosystem functioning (Gallagher et al., 2013). Analyses of functional vulnerability may help us to understand the potential changes in ecosystem functions caused by species loss or decrease of functional diversity.
Tropical forests are one of the most species-diverse ecosystems on earth (Sterck et al., 2014), which plays an important role for maintaining biodiversity and regulating global climate (Bonan, 2008). When species-rich tropical forest community loses species, it is generally assumed that high functional redundancy level could buffer against the decrease of functional diversity (Fonseca and Ganade, 2001; Pillar et al., 2013). Recent studies demonstrate that global change accompanied with shifts in species composition can affect the stability and resilience of tropical forests (Sande et al., 2016). Whether a tropical forest community can be considered functionally redundant as a whole, and thus be more stable and resilient, will depend upon the distribution of species among functional groups (Guillemot et al., 2011). Understanding the functional diversity and functional redundancy of tropical forest communities has important implications for the conservation of topical forest ecosystems in a changing environment.
Different types of tropical forest vegetation are composed of species with differing traits. Changes in the composition and distribution of plant functional traits across different vegetation types may result in changes in community functional characteristics and the differences in stabilities of different vegetation types (Kraft et al., 2008). The analysis of community functional structure characteristics among different tropical vegetation types can help us to understand the relationship between biodiversity and ecosystem functioning, and to examine the possible response mechanism of ecosystem function to potential diversity loss.
A species pool is known as the selections from the local or regional flora (Zobel and Dupré, 1998). This, from a conservative point of view, suggests that local species assemblages with different taxonomic composition and richness belong to different species pools. As demonstrated by the species pool hypothesis (Zobel and Scheiner, 2016), variations in plant species diversity and composition are dependent primarily on the availability of species from a species pool or the flora in a region.
In this study, we investigated 6 plant functional traits (specific leaf area, leaf dry matter content, stem-specific density, leaf nitrogen concentration, leaf phosphorus concentration, and maximum species height, respectively) of woody plants in 17 1-ha forest dynamics plots (FDPs) across six old-growth tropical forest types in a tropical nature reserve on Hainan island of China. Previous studies showed that the six functional traits had strong correlations with ecosystem functions, such as nutrient cycling, productivity, carbon storage, soil fertility and natural hazard prevention etc. (Bello et al., 2010). In order to assess the functional community features across the six old-growth tropical forest types in the study region. First, we measured functional diversity (including functional richness FRic, functional evenness FEve, and functional divergence FDiv) and functional redundancy based on trait probability density (TPD) (Carmona et al., 2019). Second, we built functional entity (FE) based on levels of trait similarity. Each FE comprises a unique trait category combination (Mouillot et al., 2014). Depending on the distribution of species among FEs, we evaluated the functional redundancy, functional over-redundancy and functional vulnerability for the 17 1-ha FDPs across the six old-growth tropical forest types. We also performed a series of sensitivity analyses to assess the robustness of the research results. Specifically, we mainly addressed the following questions: a) How do functional features vary with tropical forest types, and how are the functional indices related to species richness? b) Can the expected benefits of functional insurances from high species richness offset the community's functional vulnerability? c) Are species with a combination of unique traits are also rare which should be conserved with priority in the species-rich tropical forests?
Section snippets
Study sites
The study was conducted in the Bawangling National Nature Reserve (BNNR, 18°57′–19°11′N, 109°03′–109°17′E) on Hainan Island, China, which is at the northern edge of the Asian tropical forest zone (Fig. S1). The BNNR is about 500 km2, with an elevation range of about 100-1654 m a.s.l.. The climate in the reserve is the tropical monsoon, the mean annual precipitation ranges from 1751 mm at 100 m a. s. l. to 2806 mm at 1000 m a. s. l., with a wet season from May to October and a dry season from
Variation of functional diversity across the six old-growth tropical forest types
The tropical montane rain forest and tropical lowland rain forest (the two zonal vegetation types) had higher values of FRic, FEve and FDiv than other four forest types. FRic, FEve and FDiv were positively correlated with the species richness (Fig. 1 A, B, C).
Variation of functional redundancy based on TPD and FE respectively across the six old-growth tropical forest types
Whether based on TPD or FE, the functional redundancy was the highest in the tropical montane rain forest, followed by tropical lowland rain forest, tropical coniferous forest, tropical deciduous monsoon rain forest, tropical montane
Functional diversity across the six old-growth tropical forest types
In the present study, the FRic and functional niche hypervolumes showed upward trend with increasing species richness across the six old-growth tropical forest types. However, FRic and functional niche hypervolume (see supplementary material) did not consistently varied with species richness gradient across the six old-growth tropical forest types (Figs. 1, S2). The shape of the relationship between functional richness and species richness depends on the number and nature of functional traits
Conclusion
Global change is leading to shifts in forest species composition (Sande et al., 2016), these shifts may affect the functional structure and stability of tropical forests. Our results suggested that tropical forest types with high species richness had greater functional diversity and redundancy, and relatively lower functional vulnerability. However, the expected benefits of functional insurances from high species richness may not offset the community's functional vulnerability. Our results
CRediT authorship contribution statement
Shuzi Zhang: Writing, Data curation, Writing - original draft, Visualization, Investigation. Runguo Zang: Conceptualization, Methodology, Writing - original draft, Investigation, Validation, Supervision.
Declaration of competing interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgements
This research was financially supported by the National Key Research and Development Program of China (2016YFC0503103) and National Natural Science Foundation of China (41771059, 41671047, 31270474, 30430570, 30901143). We thank Prof. David Mouillot and Sébastien Villéger who helped us in analyzing data. We are grateful to the Ph.D students of Prof. Runguo Zang (especially Dr. Yunfeng Huang, Dr. Yi Ding, Dr. Wande Liu, Dr. Wenxing Long, Dr. Xinghui Lu, Dr. Junyan Zhang and Dr. Yong Jiang) and
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