Stem heating results in hydraulic dysfunction in Symplocos tinctoria: implications for post-fire tree death.

Fire-induced heating of stems can impair plant water transport by deforming xylem and increasing vulnerability to cavitation, but it is not clear whether these effects can result in tree death, or how quickly this may occur. In field experiments, we heated stems of Symplocos tinctoria (L.) L'Hér saplings to 90 °C using a thin-film resistive heater, and we monitored stomatal conductance, leaf water potential, sap flow and hydraulic conductivity until stem death. Sap flow and stomatal conductance declined quickly after heating, while whole-plant hydraulic conductance and leaf water potential remained high for the first week. In fact, leaf water potential increased during the first days after heating, indicating that stomatal closure was not initially caused by leaf water deficit induced by impaired water transport. After 1 week, leaf water potential and whole-plant conductance declined below unheated controls, while stomatal conductance and sap flow continued declining, approaching zero after 2 weeks. To better understand the cause of these declines, we directly measured hydraulic conductivity of heated stems. Stems underwent a progressive decline in conductivity after heating, and by the time that samples were severely wilted or desiccated, the heated portion of stems had little or no conductivity. Importantly, conductivity of heated stems was not recovered by flushing stems to remove embolisms, suggesting the existence of physical occlusions. Scanning electron micrographs did not reveal deformed cell walls, nor did it identify alternative causes of blockages. These results reveal that stem heating can result in xylem dysfunction and mortality, but neither response is immediate. Dysfunction was likely caused by wound responses rather than embolism, but improved understanding of the mechanisms of heat-induced hydraulic failure is needed.

Herbaceous vegetation responses to experimental fire in savannas and forests depend on biome and climate.

Fire-vegetation feedbacks potentially maintain global savanna and forest distributions. Accordingly, vegetation in savanna and forest ecosystems should have differential responses to fire, but fire response data for herbaceous vegetation have yet to be synthesized across biomes. Here, we examined herbaceous vegetation responses to experimental fire at 30 sites spanning four continents. Across a variety of metrics, herbaceous vegetation increased in abundance where fire was applied, with larger responses to fire in wetter and in cooler and/or less seasonal systems. Compared to forests, savannas were associated with a 4.8 (±0.4) times larger difference in herbaceous vegetation abundance for burned versus unburned plots. In particular, grass cover decreased with fire exclusion in savannas, largely via decreases in C4 grass cover, whereas changes in fire frequency had a relatively weak effect on grass cover in forests. These differential responses underscore the importance of fire for maintaining the vegetation structure of savannas and forests.

Effects and response of the Cerrado ground-layer to frost along the canopy cover gradient.

Frost effects on savanna plant communities have been considered as analogous to those from fire, both changing community structure and filtering species composition. However, while frost impacts have been well-studied for the woody component of savannas, it is still poorly explored for the ground-layer community. Here, we investigated effects of frost in the Cerrado along a gradient of tree cover, focusing on ground-layer plant species, near the southern limit of the Cerrado in Brazil. We aimed to elucidate if the pattern already described for the tree layer also extends to the ground layer in terms of mimicking the effects of fire on vegetation structure and composition. We assessed how damage severity differs across species and across the tree-cover gradient, and we examined the recovery process after frost in terms of richness and community structure along the canopy cover gradient. Frost caused immediate and widespread dieback of the perennial ground-layer, with greatest impact on community structure where tree cover was lowest. However, frost did not reduce the number of species, indicating community resilience to this natural disturbance. Although frost mimicked the effects of fire in some ways, in other ways it differed substantially from fire. Unlike fire, frost increases litter cover and decreases the proportion of bare soil, likely hindering crucial processes for recovery of plant populations, such as seed dispersal, seed germination and plant resprouting. This finding calls attention to the risk of misguided conclusions when the ground layer is neglected in ecological studies of tropical savannas and grasslands.

Hydraulic segmentation does not protect stems from acute water loss during fire.

The heat plume associated with fire has been hypothesized to cause sufficient water loss from trees to induce embolism and hydraulic failure. However, it is unclear whether the water transport path remains sufficiently intact during scorching or burning of foliage to sustain high water loss. We measured water uptake by branches of Magnolia grandiflora while exposing them to a range of fire intensities and examined factors influencing continued water uptake after fire. Burning caused a 22-fold mean increase in water uptake, with greatest rates of water loss observed at burn intensities that caused complete consumption of leaves. Such rapid uptake is possible only with steep gradients in water potential, which would likely result in substantial cavitation of xylem and loss of conductivity in intact stems. Water uptake continued after burning was complete and was greatest following burn intensities that killed leaves but did not consume them. This post-fire uptake was mostly driven by rehydration of the remaining tissues, rather than evaporation from the tissues. Our results indicate that the fire plume hypothesis can be expanded to include a wide range of burning conditions experienced by plants. High rates of water loss are sustained during burning, even when leaves are killed or completely consumed.

Decadal changes in fire frequencies shift tree communities and functional traits.

Global change has resulted in chronic shifts in fire regimes. Variability in the sensitivity of tree communities to multi-decadal changes in fire regimes is critical to anticipating shifts in ecosystem structure and function, yet remains poorly understood. Here, we address the overall effects of fire on tree communities and the factors controlling their sensitivity in 29 sites that experienced multi-decadal alterations in fire frequencies in savanna and forest ecosystems across tropical and temperate regions. Fire had a strong overall effect on tree communities, with an average fire frequency (one fire every three years) reducing stem density by 48% and basal area by 53% after 50 years, relative to unburned plots. The largest changes occurred in savanna ecosystems and in sites with strong wet seasons or strong dry seasons, pointing to fire characteristics and species composition as important. Analyses of functional traits highlighted the impact of fire-driven changes in soil nutrients because frequent burning favoured trees with low biomass nitrogen and phosphorus content, and with more efficient nitrogen acquisition through ectomycorrhizal symbioses. Taken together, the response of trees to altered fire frequencies depends both on climatic and vegetation determinants of fire behaviour and tree growth, and the coupling between fire-driven nutrient losses and plant traits.

Flammability thresholds or flammability gradients? Determinants of fire across savanna-forest transitions.

Vegetation-fire feedbacks are important for determining the distribution of forest and savanna. To understand how vegetation structure controls these feedbacks, we quantified flammability across gradients of tree density from grassland to forest in the Brazilian Cerrado. We experimentally burned 102 plots, for which we measured vegetation structure, fuels, microclimate, ignition success and fire behavior. Tree density had strong negative effects on ignition success, rate of spread, fire-line intensity and flame height. Declining grass biomass was the principal cause of this decline in flammability as tree density increased, but increasing fuel moisture contributed. Although the response of flammability to tree cover often is portrayed as an abrupt, largely invariant threshold, we found the response to be gradual, with considerable variability driven largely by temporal changes in atmospheric humidity. Even when accounting for humidity, flammability at intermediate tree densities cannot be predicted reliably. Fire spread in savanna-forest mosaics is not as deterministic as often assumed, but may appear so where vegetation boundaries are already sharp. Where transitions are diffuse, fire spread is difficult to predict, but should become increasingly predictable over multiple fire cycles, as boundaries are progressively sharpened until flammability appears to respond in a threshold-like manner.

Better lucky than good: How savanna trees escape the fire trap in a variable world.

Fire controls tree cover in many savannas by suppressing saplings through repeated topkill and resprouting, causing a demographic bottleneck. Tree cover can increase dramatically if even a small fraction of saplings escape this fire trap, so modeling and management of savanna vegetation should account for occasional individuals that escape the fire trap because they are "better" (i.e., they grow faster than average) or because they are "lucky" (they experience an occasional longer-than-average interval without fire or a below-average fire severity). We quantified variation in growth rates and topkill probability in Quercus laevis (turkey oak) in longleaf pine savanna to estimate the percentage of stems expected to escape the fire trap due to variability in (1) growth rate, (2) fire severity, and (3) fire interval. For trees growing at the mean rate and exposed to the mean fire severity and the mean fire interval, no saplings are expected to become adults under typical fire frequencies. Introducing variability in any of these factors, however, allows some individuals to escape the fire trap. A variable fire interval had the greatest influence, allowing 8% of stems to become adults within a century. In contrast, introducing variation in fire severity and growth rate should allow 2.8% and 0.3% of stems to become adults, respectively. Thus, most trees that escape the fire trap do so because of luck. By chance, they experience long fire-free intervals and/or a low-severity fire when they are not yet large enough to resist an average fire. Fewer stems escape the fire trap by being unusually fast-growing individuals. It is important to quantify these sources of variation and their consequences to improve understanding, prediction, and management of vegetation dynamics of fire-maintained savannas. Here we also present a new approach to quantifying variation in fire severity utilizing a latent-variable model of logistic regression.

Comment on "The global tree restoration potential".

Bastin et al's estimate (Reports, 5 July 2019, p. 76) that tree planting for climate change mitigation could sequester 205 gigatonnes of carbon is approximately five times too large. Their analysis inflated soil organic carbon gains, failed to safeguard against warming from trees at high latitudes and elevations, and considered afforestation of savannas, grasslands, and shrublands to be restoration.

Correction to: Allocation to leaf area and sapwood area affects water relations of co-occurring savanna and forest trees.

The original version of this article unfortunately contained a mistake. The Electronic supplementary material (ESM) was accompanying this article by mistake.

Comment on "The extent of forest in dryland biomes".

Bastin et al (Reports, 12 May 2017, p. 635) infer forest as more globally extensive than previously estimated using tree cover data. However, their forest definition does not reflect ecosystem function or biotic composition. These structural and climatic definitions inflate forest estimates across the tropics and undermine conservation goals, leading to inappropriate management policies and practices in tropical grassy ecosystems.

The biodiversity cost of carbon sequestration in tropical savanna.

Tropical savannas have been increasingly viewed as an opportunity for carbon sequestration through fire suppression and afforestation, but insufficient attention has been given to the consequences for biodiversity. To evaluate the biodiversity costs of increasing carbon sequestration, we quantified changes in ecosystem carbon stocks and the associated changes in communities of plants and ants resulting from fire suppression in savannas of the Brazilian Cerrado, a global biodiversity hotspot. Fire suppression resulted in increased carbon stocks of 1.2 Mg ha-1 year-1 since 1986 but was associated with acute species loss. In sites fully encroached by forest, plant species richness declined by 27%, and ant richness declined by 35%. Richness of savanna specialists, the species most at risk of local extinction due to forest encroachment, declined by 67% for plants and 86% for ants. This loss highlights the important role of fire in maintaining biodiversity in tropical savannas, a role that is not reflected in current policies of fire suppression throughout the Brazilian Cerrado. In tropical grasslands and savannas throughout the tropics, carbon mitigation programs that promote forest cover cannot be assumed to provide net benefits for conservation.

Convergence of bark investment according to fire and climate structures ecosystem vulnerability to future change.

Fire regimes in savannas and forests are changing over much of the world. Anticipating the impact of these changes requires understanding how plants are adapted to fire. In this study, we test whether fire imposes a broad selective force on a key fire-tolerance trait, bark thickness, across 572 tree species distributed worldwide. We show that investment in thick bark is a pervasive adaptation in frequently burned areas across savannas and forests in both temperate and tropical regions where surface fires occur. Geographic variability in bark thickness is largely explained by annual burned area and precipitation seasonality. Combining environmental and species distribution data allowed us to assess vulnerability to future climate and fire conditions: tropical rainforests are especially vulnerable, whereas seasonal forests and savannas are more robust. The strong link between fire and bark thickness provides an avenue for assessing the vulnerability of tree communities to fire and demands inclusion in global models.

Stomatal acclimation to vapour pressure deficit doubles transpiration of small tree seedlings with warming.

Future climate change is expected to increase temperature (T) and atmospheric vapour pressure deficit (VPD) in many regions, but the effect of persistent warming on plant stomatal behaviour is highly uncertain. We investigated the effect of experimental warming of 1.9-5.1 °C and increased VPD of 0.5-1.3 kPa on transpiration and stomatal conductance (gs ) of tree seedlings in the temperate forest understory (Duke Forest, North Carolina, USA). We observed peaked responses of transpiration to VPD in all seedlings, and the optimum VPD for transpiration (Dopt ) shifted proportionally with increasing chamber VPD. Warming increased mean water use of Carya by 140% and Quercus by 150%, but had no significant effect on water use of Acer. Increased water use of ring-porous species was attributed to (1) higher air T and (2) stomatal acclimation to VPD resulting in higher gs and more sensitive stomata, and thereby less efficient water use. Stomatal acclimation maintained homeostasis of leaf T and carbon gain despite increased VPD, revealing that short-term stomatal responses to VPD may not be representative of long-term exposure. Acclimation responses differ from expectations of decreasing gs with increasing VPD and may necessitate revision of current models based on this assumption.

Corrigendum: Enhancing Heat Tolerance of the Little Dogwood Cornus canadensis L. f. with Introduction of a Superoxide Reductase Gene from the Hyperthermophilic Archaeon Pyrococcus furiosus.

[This corrects the article on p. 26 in vol. 7, PMID: 26858741.].

Enhancing Heat Tolerance of the Little Dogwood Cornus canadensis L. f. with Introduction of a Superoxide Reductase Gene from the Hyperthermophilic Archaeon Pyrococcus furiosus.

Production of reactive oxygen species (ROS) can be accelerated under various biotic and abiotic stresses causing lipid peroxidation, protein degradation, enzyme inactivation, and DNA damage. Superoxide reductase (SOR) is a novel antioxidant enzyme from Pyrococcus furiosus and is employed by this anaerobic hyperthermophilic archaeon for efficient detoxification of ROS. In this study, SOR was introduced into a flowering plant Cornus canadensis to enhance its heat tolerance and reduce heat induced damage. A fusion construct of the SOR gene and Green Fluorescent Protein gene (GFP) was introduced into C. canadensis using Agrobacterium-mediated transformation. Heat tolerance of the GFP-SOR expressing transgenic plants was investigated by observing morphological symptoms of heat injury and by examining changes in photosynthesis, malondialdehyde (MDA), and proline levels in the plants. Our results indicate that the expression of the P. furiosus SOR gene in the transgenic plants alleviated lipid peroxidation of cell membranes and photoinhibition of PS II, and decreased the accumulation of proline at 40°C. After a series of exposures to increasing temperatures, the SOR transgenic plants remained healthy and green whereas most of the non-transgenic plants dried up and were unable to recover. While it had previously been reported that expression of SOR in Arabidopsis enhanced heat tolerance, this is the first report of the successful demonstration of improved heat tolerance in a non-model plant resulting from the introduction of P. furiosus SOR. The study demonstrates the potential of SOR for crop improvement and that inherent limitations of plant heat tolerance can be ameliorated with P. furiosus SOR.

Shifts in functional traits elevate risk of fire-driven tree dieback in tropical savanna and forest biomes.

Numerous predictions indicate rising CO2 will accelerate the expansion of forests into savannas. Although encroaching forests can sequester carbon over the short term, increased fires and drought-fire interactions could offset carbon gains, which may be amplified by the shift toward forest plant communities more susceptible to fire-driven dieback. We quantify how bark thickness determines the ability of individual tree species to tolerate fire and subsequently determine the fire sensitivity of ecosystem carbon across 180 plots in savannas and forests throughout the 2.2-million km(2) Cerrado region in Brazil. We find that not accounting for variation in bark thickness across tree species underestimated carbon losses in forests by ~50%, totaling 0.22 PgC across the Cerrado region. The lower bark thicknesses of plant species in forests decreased fire tolerance to such an extent that a third of carbon gains during forest encroachment may be at risk of dieback if burned. These results illustrate that consideration of trait-based differences in fire tolerance is critical for determining the climate-carbon-fire feedback in tropical savanna and forest biomes.

Temperature alone does not explain phenological variation of diverse temperate plants under experimental warming.

Anthropogenic climate change has altered temperate forest phenology, but how these trends will play out in the future is controversial. We measured the effect of experimental warming of 0.6-5.0 °C on the phenology of a diverse suite of 11 plant species in the deciduous forest understory (Duke Forest, North Carolina, USA) in a relatively warm year (2011) and a colder year (2013). Our primary goal was to dissect how temperature affects timing of spring budburst, flowering, and autumn leaf coloring for functional groups with different growth habits, phenological niches, and xylem anatomy. Warming advanced budburst of six deciduous woody species by 5-15 days and delayed leaf coloring by 18-21 days, resulting in an extension of the growing season by as much as 20-29 days. Spring temperature accumulation was strongly correlated with budburst date, but temperature alone cannot explain the diverse budburst responses observed among plant functional types. Ring-porous trees showed a consistent temperature response pattern across years, suggesting these species are sensitive to photoperiod. Conversely, diffuse-porous species responded differently between years, suggesting winter chilling may be more important in regulating budburst. Budburst of the ring-porous Quercus alba responded nonlinearly to warming, suggesting evolutionary constraints may limit changes in phenology, and therefore productivity, in the future. Warming caused a divergence in flowering times among species in the forest community, resulting in a longer flowering season by 10-16 days. Temperature was a good predictor of flowering for only four of the seven species studied here. Observations of interannual temperature variability overpredicted flowering responses in spring-blooming species, relative to our warming experiment, and did not consistently predict even the direction of flowering shifts. Experiments that push temperatures beyond historic variation are indispensable for improving predictions of future changes in phenology.

Are winter-active species vulnerable to climate warming? A case study with the wintergreen terrestrial orchid, Tipularia discolor.

In the eastern United States, winter temperature has been increasing nearly twice as fast as summer temperature, but studies of warming effects on plants have focused on species that are photosynthetically active in summer. The terrestrial orchid Tipularia discolor is leafless in summer and acquires C primarily in winter. The optimum temperature for photosynthesis in T. discolor is higher than the maximum temperature throughout most of its growing season, and therefore growth can be expected to increase with warming. Contrary to this hypothesis, experimental warming negatively affected reproductive fitness (number of flowering stalks, flowers, fruits) and growth (change in leaf area from 2010 to 2012) in T. discolor. Temperature in June-July was critical for flowering, and mean July temperature greater than 29 °C (i.e., 2.5 °C above ambient) eliminated reproduction. Warming of 1.2 °C delayed flowering by an average of 10 days and fruiting by an average of 5 days. Warming of 4.4 °C reduced relative growth rates by about 60%, which may have been partially caused by the direct effects of temperature on photosynthesis and respiration. Warming indirectly increased vapor pressure deficit (VPD) by 0.2-0.5 kPa, and leaf-to-air VPD over 1.3 kPa restricted stomatal conductance of T. discolor to 10-40% of maximum conductance. These results highlight the need to account for changes in VPD when estimating temperature responses of plant species under future warming scenarios. Increasing temperature in the future will likely be an important limiting factor to the distribution of T. discolor, especially along the southern edge of its range.

Size-dependent enhancement of water relations during post-fire resprouting.

In resprouting species, fire-induced topkill causes a reduction in height and leaf area without a comparable reduction in the size of the root system, which should lead to an increase in the efficiency of water transport after fire. However, large plants undergo a greater relative reduction in size, compared with small plants, so we hypothesized that this enhancement in hydraulic efficiency would be greatest among large growth forms. In the ecotone between long-leaf pine (Pinus palustris Mill.) savannas and wetlands, we measured stomatal conductance (gs), mid-day leaf water potential (Ψleaf), leaf-specific whole-plant hydraulic conductance (KL.p), leaf area and height of 10 species covering a range of growth forms in burned and unburned sites. As predicted, KL.p was higher in post-fire resprouts than in unburned plants, and the post-fire increase in KL.p was positively related to plant size. Specifically, large-statured species tended to undergo the greatest relative reductions in leaf area and height, and correspondingly experienced the greatest increases in KL.p. The post-fire increase in KL.p was smaller than expected, however, due to a decrease in absolute root hydraulic conductance (i.e., not scaled to leaf area). The higher KL.p in burned sites was manifested as an increase in gs rather than an increase in Ψleaf. Post-fire increases in gs should promote high rates of photosynthesis for recovery of carbohydrate reserves and aboveground biomass, which is particularly important for large-statured species that require more time to recover their pre-fire size.