Demystifying the convergent ecological specialization of desiccation-tolerant vascular plants for water deficit.

BACKGROUND AND AIMS: Desiccation-tolerant vascular plants (DT plants) are able to tolerate the desiccation of their vegetative tissues; as a result, two untested paradigms can be found in the literature, despite contradictions to theoretical premises and empirical findings. First, it is widely accepted that DT plants form a convergent group of specialist plants to water deficit conditions. A derived paradigm is that DT plants are placed at the extreme end of stress tolerance. Here, we tested the hypotheses that DT plants (1) are in fact convergent specialists for water deficit conditions and (2) exhibit ecological strategies related to stress tolerance, conservative resource-use and survival. METHODS: We used biogeographical and functional-traits approaches to address the mentioned paradigms and assess the species' ecological strategies. For this, 27 DT plants were used and compared to 27 phylogenetically related desiccation-sensitive vascular plants (DS plants). KEY RESULTS: We could not confirm either of the two hypotheses. We found that despite converging in desiccation tolerance, DT plants differ in relation to the conditions in which they occur and the ecological strategies they use to deal with water deficit. We found that some DT plants exhibit advantageous responses for higher growth and resource acquisition, which are suitable responses to cope with more productive conditions or with higher disturbance. We discuss that the ability to tolerate desiccation could compensate for a drought vulnerability promoted by higher investment in growth and bring advantages to deal with quick and pronounced variation of water, rather than to drought solely. CONCLUSIONS: DT plants are not only selected by drought as an environmental constraint. The alternative functional designs could promote the diversity of ecological strategies, which preclude their convergence to the same resources and conditions. Thus, DT plants are a heterogeneous group of plants in how they deal with drought, despite their desiccation tolerance ability.

Functional assembly of tropical montane tree islands in the Atlantic Forest is shaped by stress tolerance, bamboo presence, and facilitation.

AIMS: Amidst the Campos de Altitude (Highland Grasslands) in the Brazilian Atlantic Forest, woody communities grow either clustered in tree islands or interspersed within the herbaceous matrix. The functional ecology, diversity, and biotic processes shaping these plant communities are largely unstudied. We characterized the functional assembly and diversity of these tropical montane woody communities and investigated how they fit within Grime's CSR (C-competitor, S-stress-tolerant, R-ruderal) scheme, what functional trade-offs they exhibit, and how traits and functional diversity vary in response to bamboo presence/absence. METHODS: To characterize the functional composition of the community, we sampled five leaf traits and wood density along transects covering the woody communities both inside tree islands and outside (i.e., isolated woody plants in the grasslands community). Then, we used Mann-Whitney test, t test, and variation partitioning to determine the effects of inside versus outside tree island and bamboo presence on community-weighted means, woody species diversity, and functional diversity. RESULTS: We found a general SC/S strategy with drought-related functional trade-offs. Woody plants in tree islands had more acquisitive traits than those within the grasslands. Trait variation was mostly taxonomically than spatially driven, and species composition varied between inside and outside tree islands. Leaf thickness, wood density, and foliar water uptake were unrelated to CSR strategies, suggesting independent trait dimensions and multiple drought-coping strategies within the predominant S strategy. Islands with bamboo presence showed lower Simpson diversity, lower functional dispersion, lower foliar water uptake, and greater leaf thickness than in tree islands without bamboo. CONCLUSIONS: The observed functional assembly hints toward large-scale environmental abiotic filtering shaping a stress-tolerant community strategy, and small-scale biotic interactions driving small-scale trait variation. We recommend experimental studies with fire, facilitation treatments, ecophysiological and recruitment traits to elucidate on future tree island expansion and community response to climate change.

Critical transitions in rainfall manipulation experiments on grasslands.

As a result of climate and land-use changes, grasslands have been subjected to intensifying drought regimes. Extreme droughts could interfere in the positive feedbacks between grasses and soil water content, pushing grasslands across critical thresholds of productivity and leading them to collapse. If this happens, systems may show hysteresis and costly management interventions might be necessary to restore predrought productivity. Thus, neglecting critical transitions may lead to mismanagement of grasslands and to irreversible loss of ecosystem services. Rainfall manipulation experiments constitute a powerful approach to investigate the risk of such critical transitions. However, experiments performed to date have rarely applied extreme droughts and have used resilience indices that disregard the existence of hysteresis. Here, we suggest how to incorporate critical transitions when designing rainfall manipulation experiments on grasslands and when measuring their resilience to drought. The ideas presented here have the potential to trigger a perspective shift among experimental researchers, into a new state where the existence of critical transitions will be discussed, experimentally tested, and largely considered when assessing and managing vegetation resilience to global changes.

Stomatal optimization based on xylem hydraulics (SOX) improves land surface model simulation of vegetation responses to climate.

Land surface models (LSMs) typically use empirical functions to represent vegetation responses to soil drought. These functions largely neglect recent advances in plant ecophysiology that link xylem hydraulic functioning with stomatal responses to climate. We developed an analytical stomatal optimization model based on xylem hydraulics (SOX) to predict plant responses to drought. Coupling SOX to the Joint UK Land Environment Simulator (JULES) LSM, we conducted a global evaluation of SOX against leaf- and ecosystem-level observations. SOX simulates leaf stomatal conductance responses to climate for woody plants more accurately and parsimoniously than the existing JULES stomatal conductance model. An ecosystem-level evaluation at 70 eddy flux sites shows that SOX decreases the sensitivity of gross primary productivity (GPP) to soil moisture, which improves the model agreement with observations and increases the predicted annual GPP by 30% in relation to JULES. SOX decreases JULES root-mean-square error in GPP by up to 45% in evergreen tropical forests, and can simulate realistic patterns of canopy water potential and soil water dynamics at the studied sites. SOX provides a parsimonious way to incorporate recent advances in plant hydraulics and optimality theory into LSMs, and an alternative to empirical stress factors.

Alternative plant designs: consequences for community assembly and ecosystem functioning.

BACKGROUND: Alternative organism designs (i.e. the existence of distinct combinations of traits leading to the same function or performance) are a widespread phenomenon in nature and are considered an important mechanism driving the evolution and maintenance of species trait diversity. However, alternative designs are rarely considered when investigating assembly rules and species effects on ecosystem functioning, assuming that single trait trade-offs linearly affect species fitness and niche differentiation. SCOPE: Here, we first review the concept of alternative designs, and the empirical evidence in plants indicating the importance of the complex effects of multiple traits on fitness. We then discuss how the potential decoupling of single traits from performance and function of species can compromise our ability to detect the mechanisms responsible for species coexistence and the effects of species on ecosystems. Placing traits in the continuum of organism integration level (i.e. traits hierarchically structured ranging from organ-level traits to whole-organism traits) can help in choosing traits more directly related to performance and function. CONCLUSIONS: We conclude that alternative designs have important implications for the resulting trait patterning expected from different assembly processes. For instance, when only single trade-offs are considered, environmental filtering is expected to result in decreased functional diversity. Alternatively, it may result in increased functional diversity as an outcome of alternative strategies providing different solutions to local conditions and thus supporting coexistence. Additionally, alternative designs can result in higher stability of ecosystem functioning as species filtering due to environmental changes would not result in directional changes in (effect) trait values. Assessing the combined effects of multiple plant traits and their implications for plant functioning and functions will improve our mechanistic inferences about the functional significance of community trait patterning.

Chlorophyll fluorescence varies more across seasons than leaf water potential in drought-prone plants.

Among the effects of environmental change, the intensification of drought events is noteworthy, and tropical vegetation is predicted to be highly vulnerable to it. However, it is not clear how tropical plants in drought-prone habitats will respond to this change. In a coastal sandy plain environment, we evaluated the response of six plant species to water deficits across seasons, the relationship between their morpho-physiological traits, and which traits would be the best descriptors of plants' response to drought. Regardless of leaf succulence and phenology, responses between seasons were most strongly related to chlorophyll fluorescence. In this study we have demonstrated that a better comprehension of how tropical species from drought-prone habitats cope with changes in water availability can be based on seasonal variation in leaf water potential and chlorophyll fluorescence. Temporal variation in leaf water potential and chlorophyll fluorescence was found useful for differentiating between groups of sandy soil species that are responsive or unresponsive to water availability. However, chlorophyll fluorescence appeared to be a more sensitive descriptor of their seasonal and short-term responses.

Retain or repel? Droplet volume does matter when measuring leaf wetness traits.

BACKGROUND AND AIMS: Leaf wetness is an important characteristic linked to a plant's strategies for water acquisition, use and redistribution. A trade-off between leaf water retention (LWR) and hydrophobicity (LWH) may be expected, since a higher LWH/lower LWR may enhance photosynthesis, while the opposite combination may increase the leaf water uptake (LWU). However, the validation of the ecological meaning of both traits and the influence of droplet volume when measuring them have been largely neglected. METHODS: To address these questions, LWR and LWH of 14 species were measured using droplets of between 5 and 50 µL. Furthermore, the ability of those species to perform LWU was evaluated through leaf submergence in water. The droplet-volume effect on absolute values and on species ranking for LWR and LWH was tested, as well as the influence of water droplet volume on the relationship between leaf wetness traits and LWU. KEY RESULTS: Variations in droplet volume significantly affected the absolute values and the species ranking for both LWR and LWH. The expected negative correlation between leaf wetness traits was not observed, and they were not validated as a proxy for LWU. CONCLUSIONS: The water droplet volume does matter when measuring leaf wetness traits. Therefore, it is necessary to standardize the methodological approach used to measure them. The use of a standard 5 µL droplet for LWH and a 50 µL droplet for LWR is proposed. It is cautioned that the validation of both traits is also needed before using them as proxies to describe responses and effects in functional approaches.

Are leaf physiological traits related to leaf water isotopic enrichment in restinga woody species?

During plant-transpiration, water molecules having the lighter stable isotopes of oxygen and hydrogen evaporate and diffuse at a faster rate through the stomata than molecules having the heavier isotopes, which cause isotopic enrichment of leaf water. Although previous models have assumed that leaf water is well-mixed and isotopically uniform, non-uniform stomatal closure, promoting different enrichments between cells, and different pools of water within leaves, due to morpho-physiological traits, might lead to inaccuracies in isotopic models predicting leaf water enrichment. We evaluate the role of leaf morpho-physiological traits on leaf water isotopic enrichment in woody species occurring in a coastal vegetation of Brazil known as restinga. Hydrogen and oxygen stable isotope values of soil, plant stem and leaf water and leaf traits were measured in six species from restinga vegetation during a drought and a wet period. Leaf water isotopic enrichment relative to stem water was more homogeneous among species during the drought in contrast to the wet period suggesting convergent responses to deal to temporal heterogeneity in water availability. Average leaf water isotopic enrichment relative to stem water during the drought period was highly correlated with relative apoplastic water content. We discuss this observation in the context of current models of leaf water isotopic enrichment as a function of the Péclet effect. We suggest that future studies should include relative apoplastic water content in isotopic models.