Showing papers by "Lawren Sack published in 2016"

Meta-analysis reveals that hydraulic traits explain cross-species patterns of drought-induced tree mortality across the globe

Abstract: Drought-induced tree mortality has been observed globally and is expected to increase under climate change scenarios, with large potential consequences for the terrestrial carbon sink. Predicting mortality across species is crucial for assessing the effects of climate extremes on forest community biodiversity, composition, and carbon sequestration. However, the physiological traits associated with elevated risk of mortality in diverse ecosystems remain unknown, although these traits could greatly improve understanding and prediction of tree mortality in forests. We performed a meta-analysis on species’ mortality rates across 475 species from 33 studies around the globe to assess which traits determine a species’ mortality risk. We found that species-specific mortality anomalies from community mortality rate in a given drought were associated with plant hydraulic traits. Across all species, mortality was best predicted by a low hydraulic safety margin—the difference between typical minimum xylem water potential and that causing xylem dysfunction—and xylem vulnerability to embolism. Angiosperms and gymnosperms experienced roughly equal mortality risks. Our results provide broad support for the hypothesis that hydraulic traits capture key mechanisms determining tree death and highlight that physiological traits can improve vegetation model prediction of tree mortality during climate extremes.

The correlations and sequence of plant stomatal, hydraulic, and wilting responses to drought

Abstract: Climate change is expected to exacerbate drought for many plants, making drought tolerance a key driver of species and ecosystem responses. Plant drought tolerance is determined by multiple traits, but the relationships among traits, either within individual plants or across species, have not been evaluated for general patterns across plant diversity. We synthesized the published data for stomatal closure, wilting, declines in hydraulic conductivity in the leaves, stems, and roots, and plant mortality for 262 woody angiosperm and 48 gymnosperm species. We evaluated the correlations among the drought tolerance traits across species, and the general sequence of water potential thresholds for these traits within individual plants. The trait correlations across species provide a framework for predicting plant responses to a wide range of water stress from one or two sampled traits, increasing the ability to rapidly characterize drought tolerance across diverse species. Analyzing these correlations also identified correlations among the leaf and stem hydraulic traits and the wilting point, or turgor loss point, beyond those expected from shared ancestry or independent associations with water stress alone. Further, on average, the angiosperm species generally exhibited a sequence of drought tolerance traits that is expected to limit severe tissue damage during drought, such as wilting and substantial stem embolism. This synthesis of the relationships among the drought tolerance traits provides crucial, empirically supported insight into representing variation in multiple traits in models of plant and ecosystem responses to drought.

Corrigendum to: New handbook for standardised measurement of plant functional traits worldwide

Abstract: Plant functional traits are the features (morphological, physiological, phenological) that represent ecological strategies and determine how plants respond to environmental factors, affect other trophic levels and influence ecosystem properties. Variation in plant functional traits, and trait syndromes, has proven useful for tackling many important ecological questions at a range of scales, giving rise to a demand for standardised ways to measure ecologically meaningful plant traits. This line of research has been among the most fruitful avenues for understanding ecological and evolutionary patterns and processes. It also has the potential both to build a predictive set of local, regional and global relationships between plants and environment and to quantify a wide range of natural and human-driven processes, including changes in biodiversity, the impacts of species invasions, alterations in biogeochemical processes and vegetation–atmosphere interactions. The importance of these topics dictates the urgent need for more and better data, and increases the value of standardised protocols for quantifying trait variation of different species, in particular for traits with power to predict plant- and ecosystem-level processes, and for traits that can be measured relatively easily. Updated and expanded from the widely used previous version, this handbook retains the focus on clearly presented, widely applicable, step-by-step recipes, with a minimum of text on theory, and not only includes updated methods for the traits previously covered, but also introduces many new protocols for further traits. This new handbook has a better balance between whole-plant traits, leaf traits, root and stem traits and regenerative traits, and puts particular emphasis on traits important for predicting species' effects on key ecosystem properties. We hope this new handbook becomes a standard companion in local and global efforts to learn about the responses and impacts of different plant species with respect to environmental changes in the present, past and future.

Hydraulic basis for the evolution of photosynthetic productivity.

Abstract: Clarifying the evolution and mechanisms for photosynthetic productivity is a key to both improving crops and understanding plant evolution and habitat distributions. Current theory recognizes a role for the hydraulics of water transport as a potential determinant of photosynthetic productivity based on comparative data across disparate species. However, there has never been rigorous support for the maintenance of this relationship during an evolutionary radiation. We tested this theory for 30 species of Viburnum, diverse in leaf shape and photosynthetic anatomy, grown in a common garden. We found strong support for a fundamental requirement for leaf hydraulic capacity (Kleaf) in determining photosynthetic capacity (Amax), as these traits diversified across this lineage in tight coordination, with their proportionality modulated by the climate experienced in the species' range. Variation in Kleaf arose from differences in venation architecture that influenced xylem and especially outside-xylem flow pathways. These findings substantiate an evolutionary basis for the coordination of hydraulic and photosynthetic physiology across species, and their co-dependence on climate, establishing a fundamental role for water transport in the evolution of the photosynthetic rate. As photosynthesis requires water, its transport to and within leaves is a potential determinant of photosynthetic productivity. This comparison of 30 species of Viburnum shows how variations in venation architecture constrain photosynthetic rate.

Does climate directly influence NPP globally

Abstract: The need for rigorous analyses of climate impacts has never been more crucial. Current textbooks state that climate directly influences ecosystem annual net primary productivity (NPP), emphasizing the urgent need to monitor the impacts of climate change. A recent paper challenged this consensus, arguing, based on an analysis of NPP for 1247 woody plant communities across global climate gradients, that temperature and precipitation have negligible direct effects on NPP and only perhaps have indirect effects by constraining total stand biomass (Mtot )a nd stand age (a). The authors of that study concluded that the length of the growing season (lgs) might have a minor influence on NPP, an effect they considered not to be directly related to climate. In this article, we describe flaws that affected that study’s conclusions and present novel analyses to disentangle the effects of stand variables and climate in determining NPP. We re-analyzed the same database to partition the direct and indirect effects of climate on NPP, using three approaches: maximum-likelihood model selection, independent-effects analysis, and structural equation modeling. These new analyses showed that about half of the global variation in NPP could be explained by Mtot combined with climate variables and supported strong and direct influences of climate independently of Mtot, both for NPP and for net biomass change averaged across the known lifetime of the stands (ABC = average biomass change). We show that lgs is an important climate variable, intrinsically correlated with, and contributing to mean annual temperature and precipitation (Tann and Pann), all important climatic drivers of NPP. Our analyses provide guidance for statistical and mechanistic analyses of climate drivers of ecosystem processes for predictive modeling and provide novel evidence supporting the strong, direct role of climate in determining vegetation productivity at the global scale.

The Developmental Basis of Stomatal Density and Flux.

Abstract: Equations for stomatal density and maximum theoretical stomatal conductance as functions of stomatal initiation rate, epidermal cell size, and stomatal size enable scaling from development to flux.

Density-dependent seedling mortality varies with light availability and species abundance in wet and dry Hawaiian forests

Abstract: Summary Conspecific density may contribute to patterns of species assembly through negative density dependence (NDD) as predicted by the Janzen-Connell hypothesis, or through facilitation (positive density dependence; PDD). Conspecific density effects are expected to be more negative in darker and wetter environments due to higher pathogen abundance and more positive in stressful, especially dry, environments (stress-gradient hypothesis). For NDD to contribute to maintaining diversity, it should be apparent at the community-wide scale as a negative correlation between seedling recruitment, growth or survival and conspecific adult abundance (community compensatory trend; CCT). We examined seedling survival in relation to con- and heterospecific adults within 10 m and con- and heterospecific seedlings within 1 m for 13 species within two 4-ha permanent plots located in dry and wet forests in Hawaii. We also examined interactions between conspecific density and light and species’ commonness. For all species pooled, adult conspecific effects were positive (PDD) in both dry and wet forests, though they were stronger in the dry forest. In contrast, seedling conspecific effects were negative (NDD), though only significantly so in the wet forest. The strength and direction of density effects varied with understorey light such that seedlings had the highest survival where both adult conspecific density and light were high but the lowest survival where seedling conspecific density and light were high. In the wet forest, the most common species showed positive effects of adult conspecifics, but the less common species showed negative adult conspecific effects. We found mixed evidence for a CCT: seedling survival was positively correlated with basal area, but negatively correlated with tree density (stems ha−1). Thus, it remains unclear whether NDD is a diversity-maintaining mechanism in these forests. Synthesis. Overall, we found that positive conspecific effects influenced seedling mortality patterns more than negative interactions did, even in tropical wet forest where NDD is predicted to drive species’ abundances. Additionally, the strength and direction of density effects varied with forest type, PAR, and species’ abundance, underscoring the need to consider abiotic factors and species’ life-history traits in tests of density dependence hypotheses.

Plant hydraulics as a central hub integrating plant and ecosystem function: meeting report for 'Emerging Frontiers in Plant Hydraulics' (Washington, DC, May 2015).

Abstract: Water plays a central role in plant biology and the efficiency of water transport throughout the plant affects both photosynthetic rate and growth, an influence that scales up deterministically to the productivity of terrestrial ecosystems. Moreover, hydraulic traits mediate the ways in which plants interact with their abiotic and biotic environment. At landscape to global scale, plant hydraulic traits are important in describing the function of ecological communities and ecosystems. Plant hydraulics is increasingly recognized as a central hub within a network by which plant biology is connected to palaeobiology, agronomy, climatology, forestry, community and ecosystem ecology and earth-system science. Such grand challenges as anticipating and mitigating the impacts of climate change, and improving the security and sustainability of our food supply rely on our fundamental knowledge of how water behaves in the cells, tissues, organs, bodies and diverse communities of plants. A workshop, 'Emerging Frontiers in Plant Hydraulics' supported by the National Science Foundation, was held in Washington DC, 2015 to promote open discussion of new ideas, controversies regarding measurements and analyses, and especially, the potential for expansion of up-scaled and down-scaled inter-disciplinary research, and the strengthening of connections between plant hydraulic research, allied fields and global modelling efforts.

Drought tolerance as a driver of tropical forest assembly: resolving spatial signatures for multiple processes.

Abstract: Spatial patterns in trait variation reflect underlying community assembly processes, allowing us to test hypotheses about their trait and environmental drivers by identifying the strongest correlates of characteristic spatial patterns. For 43 evergreen tree species (> 1 cm dbh) in a 20-ha seasonal tropical rainforest plot in Xishuangbanna, China, we compared the ability of drought-tolerance traits, other physiological traits, and commonly measured functional traits to predict the spatial patterns expected from the assembly processes of habitat associations, niche-overlap-based competition, and hierarchical competition. We distinguished the neighborhood-scale (0-20 m) patterns expected from competition from larger-scale habitat associations with a wavelet method. Species' drought tolerance and habitat variables related to soil water supply were strong drivers of habitat associations, and drought tolerance showed a significant spatial signal for influencing competition. Overall, the traits most strongly associated with habitat, as quantified using multivariate models, were leaf density, leaf turgor loss point (π(tlp); also known as the leaf wilting point), and stem hydraulic conductivity (r2 range for the best fit models = 0.27-0.36). At neighborhood scales, species spatial associations were positively correlated with similarity in π(tlp), consistent with predictions for hierarchical competition. Although the correlation between π(tlp) and interspecific spatial associations was weak (r2 < 0.01), this showed a persistent influence of drought tolerance on neighborhood interactions and community assembly. Quantifying the full impact of traits on competitive interactions in forests may require incorporating plasticity among individuals within species, especially among specific life stages, and moving beyond individual traits to integrate the impact of multiple traits on whole-plant performance and resource demand.

Causes of variation in leaf-level drought tolerance within an Amazonian forest

Abstract: Amazonian tree communities have already been seriously impacted by extreme natural droughts, and intense droughts are predicted to increase in frequency. However, our current knowledge of Amazonian tree species’ responses to water stress remains limited, as plant trait databases include few drought tolerance traits, impeding the application and predictive power of models. Here we explored how leaf water potential at turgor loss point (πtlp), a determinant of leaf drought tolerance, varies with species life history, season, tree size and irradiance within a forest in French Guiana. First, we provided a further direct validation of a rapid method of πtlp determination based on osmometer measurements of leaf osmotic potential at full hydration for five Amazonian tree species. Next, we analysed a dataset of 131 πtlp values for a range of species, seasons, size (including saplings), and leaf exposure. We found that early-successional species had less drought-tolerant leaves than late-successional species. Species identity was the major driver of πtlp variation, whereas season, canopy tree size and leaf exposure explained little variation. Shifts in πtlp from saplings to canopy trees varied across species, and sapling leaf drought tolerance was a moderate predictor of canopy tree leaf drought tolerance. Given its low within-species variability, we propose that πtlp is a robust trait, and is useful as one index of species’ drought tolerance. We also suggest that measuring this trait would considerably advance our knowledge on leaf drought tolerance in hyperdiverse communities and would thus likely shed light on the resilience of such vulnerable species-rich ecosystem.

Osmotic and hydraulic adjustment of mangrove saplings to extreme salinity

Abstract: Salinity tolerance in plant species varies widely due to adaptation and acclimation processes at the cellular and whole-plant scales. In mangroves, extreme substrate salinity induces hydraulic failure and ion excess toxicity and reduces growth and survival, thus suggesting a potentially critical role for physiological acclimation to salinity. We tested the hypothesis that osmotic adjustment, a key type of plasticity that mitigates salinity shock, would take place in coordination with declines in whole-plant hydraulic conductance in a common garden experiment using saplings of three mangrove species with different salinity tolerances (Avicennia germinans L., Rhizophora mangle L. and Laguncularia racemosa (L.) C.F. Gaertn., ordered from higher to lower salinity tolerance). For each mangrove species, four salinity treatments (1, 10, 30 and 50 practical salinity units) were established and the time trajectories were determined for leaf osmotic potential (Ψs), stomatal conductance (gs), whole-plant hydraulic conductance (Kplant) and predawn disequilibrium between xylem and substrate water potentials (Ψpdd). We expected that, for all three species, salinity increments would result in coordinated declines in Ψs, gs and Kplant, and that the Ψpdd would increase with substrate salinity and time of exposure. In concordance with our predictions, reductions in substrate water potential promoted a coordinated decline in Ψs, gs and Kplant, whereas the Ψpdd increased substantially during the first 4 days but dissipated after 7 days, indicating a time lag for equilibration after a change in substratum salinity. Our results show that mangroves confront and partially ameliorate acute salinity stress via simultaneous reductions in Ψs, gs and Kplant, thus developing synergistic physiological responses at the cell and whole-plant scales.

Why are leaves hydraulically vulnerable

Abstract: Author(s): Sack, Lawren; Buckley, Thomas N; Scoffoni, Christine | Abstract: As plant tissues dehydrate, water transport efficiency declines, a process typically attributed to air obstruction (embolism) in the xylem. Trifilo et al. (pages 5029-5039) dissect leaf hydraulic vulnerability and show that both xylem and living tissues may be important. If confirmed and clarified, an important role for outsidexylem hydraulic decline will change our understanding of how plants transport water and control biosphere carbon and water fluxes.

Trait convergence and diversification arising from a complex evolutionary history in Hawaiian species of Scaevola

Abstract: Species variation in functional traits may reflect diversification relating to convergence and/or divergence depending on environmental pressures and phylogenetic history. We tested trait-environment relationships and their basis in finer-scale evolutionary processes among nine extant Hawaiian species of Scaevola L. (Goodeniaceae), a taxon with a complex history of three independent colonizations by different phylogenetic lineages, parallel ecological specialization, and homoploid hybridization events in Hawai'i. Using a wild population for each species, we evaluated traits related to plant function (morphology, leaf and wood anatomy, nutrient and carbon isotope composition). Hawaiian Scaevola species were distributed across coastal, dry forest and wet forest environments; multivariate environmental analysis using abiotic and biotic factors further showed that species from distantly related lineages inhabited similar environments. Many traits correlated with environment (based on the multivariate environmental analysis), considering both distantly related species and more closely related species. Scaevola species within shared habitats generally showed trait convergence across distantly related lineages, particularly among wet forest species. Furthermore, trait diversification through divergence was extensive among closely related Scaevola species that radiated into novel environments, especially in plant morphology and traits affecting water relations. Homoploid hybrid-origin species were "intermediate" compared to their ancestral parent species, and possessed trait combinations relevant for their current habitat. The diversity in functional traits reflected strong influences of both ecology and evolutionary history in native Hawaiian Scaevola species, and trait correspondence with environment was due to the combination of multiple processes within the taxon: trait pre-adaptation and filtering, evolutionary convergence, divergence, and hybridization.

Repeated range expansion and niche shift in a volcanic hotspot archipelago: radiation of Hawaiian Euphorbia (Euphorbiaceae)

Abstract: Aim The taxon cycle hypothesis describes the cyclic movement of taxa during range expansion and contraction, accompanied by an evolutionary shift from open and often coastal vegetation to closed, and often inland forest vegetation in island systems. The Hawaiian Archipelago is an ideal system to test this hypothesis given the linear fashion of island formation and a relatively well-understood geological history. Location Hawaiian Islands. Methods We sampled 153 individuals in 15 of the 16 native species of Hawaiian Euphorbia section Anisophyllum on six major Hawaiian Islands, plus 11 New World close relatives, to elucidate the biogeographic movement of this lineage along the Hawaiian island chain. We used a concatenated chloroplast DNA data set of more than eight kilobases in aligned length and applied maximum likelihood and Bayesian inference for phylogenetic reconstruction. Connectivity among islands and habitat types was estimated using BayesTraits. Age and phylogeographic patterns were co-estimated using BEAST. In addition, we used nuclear ribosomal ITS and the low-copy genes LEAFY and G3pdhC to investigate the reticulate relationships within this radiation. Results We estimate that Hawaiian Euphorbia first arrived on Kauai or Niihau ca. 5 million years ago and subsequently diverged into 16 species on all major Hawaiian Islands. During this process Euphorbia dispersed from older to younger islands in a stepping-stone fashion through open, dispersal-prone habitats. Taxa that occupy closed vegetation on Kauai and Oahu evolved in situ from open vegetation taxa of the same island. Consequently, widespread species tend to occupy habitats with open vegetation, whereas single island endemic species predominantly occur in habitats with closed canopy and are only found on the two oldest islands of Kauai and Oahu. Main conclusions The spatial and temporal patterns of dispersal and range shifts in Hawaiian Euphorbia support an intra-volcanic-archipelago version of the taxon cycle hypothesis.