Abstract
Plant functional traits and strategies hold the promise to explain species distribution, but few studies have linked multiple traits to multiple niche dimensions (i.e., light, water, and nutrients). Here, we analyzed for 29 liana species in a Chinese tropical seasonal rainforest how: (1) trait associations and trade-offs lead to different plant strategies; and (2) how these traits shape species’ niche dimensions. Eighteen functional traits related to light, water, and nutrient use were measured and species niche dimensions were quantified using species distribution in a 20-ha plot combined with data on canopy gaps, topographic water availability, and soil nutrients. We found a tissue toughness spectrum ranging from soft to hard tissues along which species also varied from acquisitive to conservative water use, and a resource acquisition spectrum ranging from low to high light capture and nutrient use. Intriguingly, each spectrum partly reflected the conservative–acquisitive paradigm, but at the same time, the tissue toughness and the resource acquisition spectrum were uncoupled. Resource niche dimensions were better predicted by individual traits than by multivariate plant strategies. This suggests that trait components that underlie multivariate strategy axes, rather than the plant strategies themselves determine species distributions. Different traits were important for different niche dimensions. In conclusion, plant functional traits and strategies can indeed explain species distributions, but not in a simple and straight forward way. Although the identification of global plant strategies has significantly advanced the field, this research shows that global, multivariate generalizations are difficult to translate to local conditions, as different components of these strategies are important under different local conditions.
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Introduction
Plant functional traits are morphological, physiological or phenological properties that affect plant growth, survival, and reproduction (Ackerly 2003), and hold the promise to explain plant species distribution patterns (McGill et al. 2006). Plant traits can be closely associated for biophysical reasons (e.g., larger leaves require more robust stems for mechanical support), because of allocation trade-offs (e.g., plants can invest limiting resources either in above or belowground organs), and/or because they reflect adaptations to similar environmental conditions. Trait associations, therefore, reflect ecological strategies of species to successfully complete their lifecycle in a specific environment (Grime 1974; Reich et al. 2003). Compared to the many studies that have evaluated trait spectra on broad spatial scales in the field (e.g., Wright et al. 2004) and within local communities (e.g., Fortunel et al. 2012), less studies have actually evaluated how traits affect plant performance in the field (but see, Poorter and Bongers 2006; Guimarães et al. 2018; Poorter et al. 2018), and even fewer studies have explicitly linked multiple traits to multiple dimensions of the plant niche (Sterck et al. 2011). Here, we evaluate for 29 liana species how leaf, stem, and root traits are associated, and how this shapes their light, water, and nutrient niche dimensions in a tropical seasonal rainforest.
Plant ecological strategies can explain the success of different species under different environmental conditions (Grime 2006; Westoby and Wright 2006). Since resource capture, use, and release are fundamental for plant functioning and performance, Díaz et al. (2004, 2016) proposed that, globally, plants show a trade-off between resource acquisition and conservation. For example, species with high specific leaf area and leaf nutrient concentrations can attain high photosynthetic rates and have the potential to be successful in high light environments, whereas species with higher tissue density and toughness can attain a longer life span, and therefore, persist in low light conditions (Wright and Westoby 2002; Poorter et al. 2006). These trait trade-offs are also known as the leaf economics spectrum (Wright et al. 2004). Similarly, species with cheap, soft stem wood and wide vessels can attain a higher hydraulic conductivity, gas exchange and growth, and can, therefore, achieve a competitive advantage in high resource environments (Santiago et al. 2004; van der Sande et al. 2019). By contrast, species with a high wood density are more resistant to drought-induced cavitation, mechanical damage, and pathogen attack, and can better survive under low resource conditions (Poorter et al. 2008; Cornwell et al. 2009).
Many studies have shown that for these reasons leaf, stem, and root traits are closely coupled (e.g., Reich et al. 2003; Freschet et al. 2010). However, leaf and hydraulic traits are also observed to be decoupled, with leaf economics spectrum corresponding to light capture and tissue longevity, and the hydraulics spectrum to water use and leaf temperature maintenance (Li et al. 2015). Similarly, root traits may be decoupled from leaf and stem traits, as roots have to deal with the acquisition of many different water and nutrient resources, and can obtain these resources in different ways, through mycorrhizae, nitrogen-fixing bacteria, or root exudates (Weemstra et al. 2016).
The species niche is defined as the n-dimensional hypervolume of environmental and biotic conditions under which a species can grow and reproduce (Hutchinson 1957), and therefore, reflects multiple niche dimensions. Henceforth, we often use the word “niche” to refer to one of the specific dimensions of the niche (i.e., nutrients, water, or light). Although spatial distribution patterns might also emerge from dispersal limitation (Hubbell 2001), niche theory predicts that species can differ in their distribution when they occupy places with distinct environmental conditions, are functionally different, and specialized for those conditions (Hutchinson 1957). Global plant strategies in resource capture and use (i.e., the acquisitive–conservative continuum, or the fast-slow continuum), are thought to explain species distribution and niches (Grime 1974; Díaz et al. 2004). Indeed, differential species distributions have been related to different species tolerances to shade (Sterck et al. 2006), drought (Engelbrecht et al. 2007; Condit et al. 2013), and nutrient stress (Baltzer and Thomas 2010). The idea is that the same conservative trait values allow plants to occupy low resource niches everywhere (Reich 2014), which has rarely been tested, because most studies have quantified only one component of the multidimensional resource niche (either water, light, or nutrients), but rarely the combination. Similarly, it is assumed that the whole trait package determines the niches, but it can be that different components of these global strategies are relevant for different dimensions of the resource niches. This study explores, therefore, the importance of traits and plant strategies for different dimensions (i.e., light, water, and nutrients) of the resource niche.
We focus on lianas (woody vines) as our study system. Lianas are an important component of tropical forest systems as they comprise up to 25% of the woody stems and 35% of the species, thus contributing substantially to forest structure and ecosystem functioning (Schnitzer 2015). Trait associations and trait-environment linkages may be different for lianas and trees. Since lianas are structural parasites, they may compete more efficiently for light (Estrada-Villegas and Schnitzer 2018), and may, therefore, show stronger trait associations with the light niche dimension than trees. Similarly, because lianas tend to have wide vessels, they are hydraulically more efficient, and stronger water spenders (van der Sande et al. 2019) and may, therefore, show stronger trait associations with the (topographic) water niche dimension than trees. By having acquisitive trait values, lianas would also have an advantage on fertile soils where they can attain high photosynthetic rates and rapid growth (Pasquini et al. 2015).
Here, we evaluated 18 leaf, stem, and root traits from 29 dominant liana species, and linked these to the light, water, and nutrient niche dimensions of the species in a permanent sample plot in a tropical seasonal rainforest of ** liana distribution (the first PCA axis had a significant positive effect on liana soil niches, Fig. 3c). This indicates that liana species with more acquisitive trait values (softer tissues, greater water use) can take advantage of these conditions and dominate high soil resource niches.
When resource niches were predicted based on individual traits, then acquisitive trait values indeed often increased the resource niche (i.e., P, K, Zn, stomatal pore index, and thinner leaves increased different resource niches), but not always (e.g., a high leaf nitrogen concentration decreased the soil water, P, and K niche, Table 3). Plant strategies are inherently multivariate and thought to better explain the species niche (Grime 2006). Yet, in our case, individual traits were better predictors of the species niche dimensions than the multivariate strategy axes (i.e., the R2 was higher; Table S3 and Table S4). This indicates that different components of the multivariate strategy axes, rather than the main strategies themselves are important for different niche dimensions, although it could be, of course, that additional PCA axes, and less obvious axes of plant trait variation, could explain additional variation.
Light niche
We hypothesized that the light niche of lianas would increase with traits that increase carbon gain, for example, through increased light capture ability (large leaf area and high specific leaf area), high leaf N and P concentrations, and fast gas exchange (high stomatal density, length, and pore index). We indeed found that the light niche was predicted by the multivariate nutrient and carbon acquisition axis (PC2; Fig. 3d and Table S4). The light niche mainly increased with leaf phosphorus and zinc concentrations, and to a lesser extent with vessel density and stomatal pore index (which have a large relative importance; Table 3 and Table S3). Leaf zinc concentration has rarely been studied in tropical rainforests. Zinc helps with the production of a plant hormone responsible for stem elongation and leaf expansion (Lines-Kelly 1992), which should especially be important for lianas with their climbing life form. Light-demanding lianas tend to have wide vessels that increase the water transport capacity of the stem (van der Sande et al. 2019), thus allowing for fast gas exchange. Similarly, a high stomatal pore index allows for a high stomatal conductance and gas exchange (Bidwell 1974) to optimally benefit from the high irradiance.
Water niche
We hypothesized that the water niche would be best predicted by water transport traits (i.e., vessel diameter, leaf venation, and stomata). We found that species with large stomatal pore index (i.e., high gas exchange), thin leaves that desiccate easily and large leaf P occupied topographically wet habitats. Species with dense leaf venation and large leaf N occupied dry habitats, for which we do not have a clear explanation (Table 3). Other studies have shown that within the same community, the topographic water niche is determined by a suite of traits (Cosme et al. 2017; Oliveira et al. 2019). For example, Amazonian rainforest tree species from higher and relatively drier plateaus had lower SLA, denser wood, narrower vessels, lower hydraulic conductivity, and stronger resistance against drought-induced cavitation than species from lower-lying wet valleys (Cosme et al. 2017; Oliveira et al. 2019). We used a rather coarse measure (topographic water availability) to quantify the water niche. Future studies should really measure soil moisture at different soil depths to increase our understanding of the water niche. Nevertheless, water is probably not a strongly limiting factor in our moist and shaded forest; in **shuangbanna, fog drip contributes 5% of the annual rainfall, with 86% of the fog drip occurring in the dry season, thus alleviating the effect of seasonal drought (Liu et al. 2004).
Nutrient niche
We hypothesized that liana nutrient niches would increase with traits that reflect nutrient requirements and use and especially with leaf P because P is often limiting in old weathered and leached tropical soils (Vitousek et al. 2010). Soil nutrient niches were indeed closely associated with leaf nutrient concentrations; soil nutrient niches increased with leaf P (for soil P and K), and leaf K (for soil P and N), and decreased with leaf N (for soil P and K; Table 3, Fig. 3b). In addition, soil K niches could also be predicted by the multivariate tissue toughness spectrum (Table S4, Fig. 3c), with species bearing softer tissues occupying higher resource niches. Species with tough and persistent tissues can retain nutrients for a longer time in their leaves and branches, and as a result have lower nutrient requirements, and can better persist under low soil resource conditions (Aerts 1996).
Functional traits were not associated with liana abundance
We hypothesized that in this humid, light-limited forest, conservative trait values that increase shade tolerance (e.g., high wood density and low specific leaf area) would increase the abundance of liana species. Surprisingly, none of these traits had a significant effect on liana abundance (Table 3, Fig. 4, Table S3), despite the fact that we included several traits belonging to the leaf economics spectrum and stem economics spectrum that are thought to be generally important for plant strategies and functioning (Wright et al. 2004; Chave et al. 2009). Previous studies have shown that under low light conditions, tree species with conservative trait values such as low SLA, high wood density and leaf dry matter content attain higher abundance at the sapling stage (Reich et al. 1997; Cornwell and Ackerly 2010) because they can retain their hardly acquired carbon for longer periods of time. Similarly, in Panama, these conservative traits are able to predict the abundance of trees, but not of lianas (van der Sande et al. 2019). Perhaps in this Panamanian study as well as in our study, no relationships between traits and liana abundance were found because relatively large lianas were studied (with a stem diameter > 1 cm) which already have most of their leaves in the forest canopy, and hence, are not light limited. Stronger effects of light on lianas might be expected in the seedling stage, during which more individuals are found in shaded conditions. We found that stomatal density tended to shape liana abundance (Table 3). Denser but smaller stomata may allow for a better control of gas exchange during drought or sun flecks (Düring 2015; Voelker et al. 2016).
How functional are functional traits?
Plant functional traits and strategies can indeed explain species distribution, but not in a simple and straightforward way as we hoped for. This research shows that (1) global trait economics spectra can also be found in local plant communities, but part of these trait economics spectra can be uncoupled, (2) it is the underlying components (i.e., individual traits), rather than plant strategies (i.e., overall trait syndromes) themselves that determine the species niche, and (3) different traits are important for different niches. Although identifying global plant strategies has significantly advanced the field, this study shows that global, multivariate generalizations are difficult to translate into local conditions, as different components of these strategies may be important under different local conditions.
This study brings us back to the key question about the functionality, validity, and predictability of the ‘functional ecology approach’. Perhaps the field of functional ecology faces such a strong tension between generalization versus contextualization because functionality is, by definition, context dependent. This tension makes the field not only more complicated, but also more interesting and exciting.
Future studies could include more process-based traits (e.g., cavitation vulnerability and leaf specific conductivity) or whole-plant traits (e.g., biomass allocation), and especially root traits (e.g., rooting depth, mycorrhizae, root exudates) to unravel links between traits and soil water and nutrient niches. Similarly, future studies could quantify the species niche by taking spatial autocorrelation into account (cf. Harms et al. 2001).
Conclusions
We evaluated the functional trait associations and strategies among 29 lianas species, and the correlations between resource niches and functional traits. Lianas showed two orthogonal trait spectra, from tissue toughness and water conservation to tissue softness and rapid water acquisition, and a secondary spectrum in nutrient and carbon acquisition. Liana species with more acquisitive trait values occupied higher light, water and nutrient resource niches, but different traits were important for different niche dimensions. Instead of local plant abundance, traits may better explain species distributions and their presence along gradients of resource availability.
Data availability
Species mean trait data are available from the TRY database, and data on species traits and niches are available from Data Archiving and Networked Services (DANS): https://doi.org/10.17026/dans-xej-j7kf
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Acknowledgements
We thank the National Forest Ecosystem Research Station at **shuangbanna for field work support. We thank the Public Technology Service Center, **shuangbanna Tropical Botanical Garden, Chinese Academy of Sciences for foliage and soil nutrient analyses. We are particularly indebted to Ke-Yan Zhang, Yan **ao, and **ao-Long Bai for their assistance with lab work, and Yan-Lei Du from Lanzhou University for root analysis. We thank two anonymous reviewers for their helpful and constructive comments.
Funding
This work was supported by the National Natural Science Foundation of China (31870385; 32061123003), the CAS “Light of West China” program to JLZ, the National Key Basic Research Program of China (2014CB954100) and the canopy foundation (Stichting het Kronendak). QL was supported by State Scholarship Fund from China Scholarship Council.
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QL, FJS, JLZ and LP conceived the ideas and designed methodology. QL, AS, EK, LQS and MC collected the data. QL, AS and EK analyzed the data. QL led the writing of the manuscript and all the authors contributed critically to the drafts and gave final approval for publication.
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Communicated by Christiane Roscher.
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Liu, Q., Sterck, F.J., Zhang, JL. et al. Traits, strategies, and niches of liana species in a tropical seasonal rainforest. Oecologia 196, 499–514 (2021). https://doi.org/10.1007/s00442-021-04937-4
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DOI: https://doi.org/10.1007/s00442-021-04937-4