The importance of belowground processes in drylandsfrom an individual to a whole plant community perspective

Resumen

Background A plant trait-based approach and the identification of functional trade-offs are key tools in plant ecology to link plant form and function. In the last decades, increasing attention has been given to root traits to integrate them with leaf and stem traits and achieve a whole-individual perspective of plant functional strategies. The gap between aboveground and belowground data is still very large, hampering the development of a general framework and theory describing plant functioning and sources of phenotypic variation. In this context, in drylands, where soil water and nutrients represent the main constraints for plant survival and development, plant strategies related to both water and nutrient use are of special interest, as they are directly connected to plant performance and community dynamics. A growing body of evidence points out that the spatial scale of the study strongly affects the observed patterns of trait coordination and functional trade-offs, because the processes that filter the traits shaping plant communities are spatial-scale dependent. Furthermore, evolutionary history exerts a strong effect on the functional characterization of the plant community, thus demanding its consideration when searching for plant functional trade-offs. Recently, increasing efforts have been carried out to characterize species distribution belowground, as a result of new straightforward techniques, such as DNA metabarcoding, which provide the necessary tools to investigate what for long has been coined the hidden part of plant communities. Given the importance of plant-plant and plant-soil (including both biotic and abiotic factors) interactions in arid environments, the assessment of both taxonomical and functional diversity patterns belowground will likely shed light on the mechanistic aspects of community assembly and species coexistence. Objectives In this work, we shifted the attention to the belowground plant community component, by integrating root traits in the analysis of plant water and nutrient use strategies in a whole-individual perspective. We used a fine spatial scale assessment of taxonomical and functional diversity patterns belowground, considering its link with both the aboveground compartment and with both soil abiotic and biotic factors. Main aims: Chapter 1 ❖ To assess the presence of water niche segregation between coexisting species through the use of water stable isotopes. ❖ To characterize the integration between plant water-use strategy and the leaf-level nutrient-use strategy accounting for the potential effect of evolutionary history. ❖ To determine the potential association between the water-use strategy and the leaf-level nutrient-use strategy with species performance in the plant community. Chapter 2 ❖ To compare whole-individual functional trade-offs observed at a local plant community scale with the described global functional trade-offs. ❖ To assess the potential association of both the root- and leaf-level nutrient-use strategy with the plant water-use strategy and species performance in the plant community. Chapter 3 ❖ To characterize and compare patterns of species richness and species spatial distribution between aboveground and belowground compartments, accounting for the potential variations across spatial scales. ❖ To evaluate the effect of soil heterogeneity in both aboveground and belowground patterns of species diversity. Chapter 4 ❖ To analyse plant belowground functional diversity and assess the presence of non-random functional patterns on community assembly. ❖ To determine the effect of soil heterogeneity and the microbial community in the belowground patterns. Methods Chapter 1 We sampled 24 perennial coexisting species growing in natural conditions in a rich semiarid Mediterranean shrubland. We measured leaf functional traits related to water- and nutrient-use and collected basal stems and/or root necks to extract stem water and estimate proportions of different soil water sources used by each species through isotopic techniques. Chapter 2 We carried out a common garden, rhizotron experiment with 23 coexisting species from the same Mediterranean shrubland. We measured 11 root functional traits related with the nutrient-use strategy and plant size, and leaf nutrient-use functional traits in individuals grown in optimal water and nutrient conditions. Chapter 3 We assessed the diversity of the aboveground and belowground plant communities at a very fine scale. We used a spatially explicit approach, establishing a 64m2 plot where all individuals were mapped aboveground, and where a regular grid of 94 soil cores was sampled belowground. DNA metabarcoding techniques previously optimized in our group were used to identify species in roots samples. Chapter 4 We integrated the functional trait variation assessed in chapters 1 and 2 with the belowground species diversity assessment from chapter 3. Results Chapter 1 We observed a strong water niche segregation between species during the phenological peak of our community and detected an important functional trade-off between water uptake depth and leaf traits related with the leaf economic spectrum, with a shallower water uptake related with more acquisitive strategies. Furthermore, we observed that a more conservative carbon and nutrient use strategy, as well as a saver leaf-level water use strategy, was positively correlated with species performance in natural conditions. Chapter 2 We observed functional trade-offs at the whole-plant level, which were only partly congruent with global trade-offs. Our results evidenced the strong relationship between a saver leaf-level water-use strategy and higher root tissue density. We also observed a partial coordination between both leaf- and root-level nutrient use and the water-use strategy, with a positive correlation between a saver leaf-level water use strategy, coordinated with a more conservative leaf- and root-nutrient use, and species performance in the field. Chapter 3 We detected high species diversity belowground at the neighbourhood scale of a few centimetres and a strong discrepancy with aboveground species diversity. The maximum similarity between aboveground and belowground compartments was encountered at very different scales. We also found that soil factors driving species richness aboveground and belowground partly matched when considering the shallower soil layer, while remarkably differed for larger depths. Chapter 4 We observed important non-random patterns indicating a strong functional root segregation as a response to belowground plant-plant competition. Our findings also pointed out to the significant and positive effect of soil fungi richness on the high root functional diversity observed in the topsoil layers. In deeper layers, we observed instead significant effects of both the microbiota and soil heterogeneity on plant functional diversity. Conclusions We found high functional variability in the study plant community, a rich Mediterranean shrubland, with a patent coordination between different aspects associated with the water- and nutrient-use strategy. Indeed, an acquisitive leaf nutrient-use strategy was associated with a greater use of shallow water sources from nutrient-rich topsoil layers, while a more conservative leaf nutrient-use strategy was linked to uptake of deeper water sources. Higher root tissue density was instead strongly associated with a saver leaf-level water use, a functional coordination that may be associated to higher mechanical support provided by higher root tissue density. As may be expected in drylands, a more conservative leaf- and root-level nutrient use strategy and a saver water-use strategy were positively related with species performance. Aboveground and belowground plant species diversities strongly differed and were driven by fine-scale deterministic processes mostly acting at different spatial scales. Deterministic processes, mostly attributable to competition, regulated non-random functional patterns observed belowground. Soil fungi richness positively affected the observed patterns in topsoil layers, while both microbiota richness and soil heterogeneity exerted a significant effect in deepest soil layers, supporting the idea that both plant-soil feedbacks and environmental filtering may exert a key role for species coexistence at local spatial scales. In this work, we elucidated key aspects related to plant functioning and local-scale community dynamics characterizing Mediterranean environments. One of the main novelties of this work was to find that while leaf- and root-level nutrient-use strategies were strongly coupled, they were associated to different key aspects of the plant water-use strategy. In addition, we showed the high belowground both taxonomical and functional diversity at a very fine spatial scale, and provided evidence that deterministic processes, especially plant-plant interactions, are importantly involved in the characterization of the belowground plant community.