Fire frequency drives decadal changes in soil carbon and nitrogen and ecosystem productivity.

Fire frequency is changing globally and is projected to affect the global carbon cycle and climate. However, uncertainty about how ecosystems respond to decadal changes in fire frequency makes it difficult to predict the effects of altered fire regimes on the carbon cycle; for instance, we do not fully understand the long-term effects of fire on soil carbon and nutrient storage, or whether fire-driven nutrient losses limit plant productivity. Here we analyse data from 48 sites in savanna grasslands, broadleaf forests and needleleaf forests spanning up to 65 years, during which time the frequency of fires was altered at each site. We find that frequently burned plots experienced a decline in surface soil carbon and nitrogen that was non-saturating through time, having 36 per cent (±13 per cent) less carbon and 38 per cent (±16 per cent) less nitrogen after 64 years than plots that were protected from fire. Fire-driven carbon and nitrogen losses were substantial in savanna grasslands and broadleaf forests, but not in temperate and boreal needleleaf forests. We also observe comparable soil carbon and nitrogen losses in an independent field dataset and in dynamic model simulations of global vegetation. The model study predicts that the long-term losses of soil nitrogen that result from more frequent burning may in turn decrease the carbon that is sequestered by net primary productivity by about 20 per cent of the total carbon that is emitted from burning biomass over the same period. Furthermore, we estimate that the effects of changes in fire frequency on ecosystem carbon storage may be 30 per cent too low if they do not include multidecadal changes in soil carbon, especially in drier savanna grasslands. Future changes in fire frequency may shift ecosystem carbon storage by changing soil carbon pools and nitrogen limitations on plant growth, altering the carbon sink capacity of frequently burning savanna grasslands and broadleaf forests.

Consistent physiological, ecological and evolutionary effects of fire regime on conservative leaf economics strategies in plant communities.

The functional response of plant communities to disturbance is hypothesised to be controlled by changes in environmental conditions and evolutionary history of species within the community. However, separating these influences using direct manipulations of repeated disturbances within ecosystems is rare. We evaluated how 41 years of manipulated fire affected plant leaf economics by sampling 89 plant species across a savanna-forest ecotone. Greater fire frequencies created a high-light and low-nitrogen environment, with more diverse communities that contained denser leaves and lower foliar nitrogen content. Strong trait-fire coupling resulted from the combination of significant intraspecific trait-fire correlations being in the same direction as interspecific trait differences arising through the turnover in functional composition along the fire-frequency gradient. Turnover among specific clades helped explain trait-fire trends, but traits were relatively labile. Overall, repeated burning led to reinforcing selective pressures that produced diverse plant communities dominated by conservative resource-use strategies and slow soil nitrogen cycling.

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.

Disease and fire interact to influence transitions between savanna-forest ecosystems over a multi-decadal experiment.

Global change is shifting disturbance regimes that may rapidly change ecosystems, sometimes causing ecosystems to shift between states. Interactions between disturbances such as fire and disease could have especially severe effects, but experimental tests of multi-decadal changes in disturbance regimes are rare. Here, we surveyed vegetation for 35 years in a 54-year fire frequency experiment in a temperate oak savanna-forest ecotone that experienced a recent outbreak of oak wilt. Different fire regimes determined whether plots were savanna or forest by regulating tree abundance (r2  = 0.70), but disease rapidly reversed the effect of fire exclusion, increasing mortality by 765% in unburned forests, but causing relatively minor changes in frequently burned savannas. Model simulations demonstrated that disease caused unburned forests to transition towards a unique woodland that was prone to transition to savanna if fire was reintroduced. Consequently, disease-fire interactions could shift ecosystem resilience and biome boundaries as pathogen distributions change.

Low-intensity frequent fires in coniferous forests transform soil organic matter in ways that may offset ecosystem carbon losses.

The impact of shifting disturbance regimes on soil carbon (C) storage is a key uncertainty in global change research. Wildfires in coniferous forests are becoming more frequent in many regions, potentially causing large C emissions. Repeated low-intensity prescribed fires can mitigate wildfire severity, but repeated combustion may decrease soil C unless compensatory responses stabilize soil organic matter. Here, we tested how 30 years of decadal prescribed burning affected C and nitrogen (N) in plants, detritus, and soils in coniferous forests in the Sierra Nevada mountains, USA. Tree basal area and litter stocks were resilient to fire, but fire reduced forest floor C by 77% (-36.4 Mg C/ha). In mineral soils, fire reduced C that was free from minerals by 41% (-4.4 Mg C/ha) but not C associated with minerals, and only in depths ≤ 5 cm. Fire also transformed the properties of remaining mineral soil organic matter by increasing the proportion of C in a pyrogenic form (from 3.2% to 7.5%) and associated with minerals (from 46% to 58%), suggesting the remaining soil C is more resistant to decomposition. Laboratory assays illustrated that fire reduced microbial CO2 respiration rates by 55% and the activity of eight extracellular enzymes that degrade cellulosic and aromatic compounds by 40-66%. Lower decomposition was correlated with lower inorganic N (-49%), especially ammonium, suggesting N availability is coupled with decomposition. The relative increase in forms of soil organic matter that are resistant to decay or stabilized onto mineral surfaces, and the associated decline in decomposition suggest that low-intensity fires may promote mineral soil C storage in pools with long mean residence times in coniferous forests.

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

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.

Edge fires drive the shape and stability of tropical forests.

In tropical regions, fires propagate readily in grasslands but typically consume only edges of forest patches. Thus, forest patches grow due to tree propagation and shrink by fires in surrounding grasslands. The interplay between these competing edge effects is unknown, but critical in determining the shape and stability of individual forest patches, as well the landscape-level spatial distribution and stability of forests. We analyze high-resolution remote-sensing data from protected Brazilian Cerrado areas and find that forest shapes obey a robust perimeter-area scaling relation across climatic zones. We explain this scaling by introducing a heterogeneous fire propagation model of tropical forest-grassland ecotones. Deviations from this perimeter-area relation determine the stability of individual forest patches. At a larger scale, our model predicts that the relative rates of tree growth due to propagative expansion and long-distance seed dispersal determine whether collapse of regional-scale tree cover is continuous or discontinuous as fire frequency changes.

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.

Nutrient limitation in tropical savannas across multiple scales and mechanisms.

Nutrients have been hypothesized to influence the distribution of the savanna biome through two possible mechanisms. Low nutrient availability may restrict growth rates of trees, thereby allowing for intermittent fires to maintain low tree cover; alternatively, nutrient deficiency may even place an absolute constraint on the ability of forests to form, independent of fire. However, we have little understanding of the scales at which nutrient limitation operates, what nutrients are limiting, and the mechanisms that influence how nutrient limitation regulates savanna-forest transitions. Here, I review literature, synthesize existing data, and present a simple calculation of nutrient demand to evaluate how nutrient limitation may regulate the distribution of the savanna biome. The literature primarily supports the hypothesis that nutrients may interact dynamically with fire to restrict the transition of savanna into forest. A compilation of indirect metrics of nutrient limitation suggest that nitrogen and phosphorus are both in short supply and may limit plants. Nutrient demand calculations provided a number of insights. First, trees required high rates of nitrogen and phosphorus supply relative to empirically determined inputs. Second, nutrient demand increased as landscapes approached the transition point between savanna and forest. Third, the potential for fire-driven nutrient losses remained high throughout transitions, which may exaggerate limitation and could be a key feedback stabilizing the savanna biome. Fourth, nutrient limitation varied between functional groups, with fast-growing forest species having substantially greater nutrient demand and a higher susceptibility to fire-driven nutrient losses. Finally, African savanna trees required substantially larger amounts of nutrients supplied at greater rates, although this varied across plant functional groups. In summary, the ability of nutrients to control transitions emerges at individual and landscape scales, and is regulated through different mechanisms based on spatial (differences in underlying geology), temporal (stage in biome transition) and biological (species traits and community composition) variability.

Aridity, not fire, favors nitrogen-fixing plants across tropical savanna and forest biomes.

Tropical savannas are hypothesized to be hot spots of nitrogen-fixer diversity and activity because of the high disturbance and low nitrogen characteristic of savanna landscapes. Here we compare the abundances of nitrogen-fixing and non-fixing trees in both tropical savannas and tropical forests under climatically equivalent conditions, using plant inventory studies across 566 plots in South America and Africa. A single factor, aridity, explained 19-54% of the variance in fixer abundance, and unexpectedly was more important than fire frequency, biome, and continent. Nitrogen fixers were more abundant in arid environments; as a result, African savannas, which tend to be drier, were richer in nitrogen fixers than South American savannas. Fixer abundance converged on similar levels in forests in both continents. We conclude that climate plays a greater role than fire in determining the distribution of nitrogen fixers across tropical savanna and forest biomes.

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.

Trade-offs between savanna woody plant diversity and carbon storage in the Brazilian Cerrado.

Incentivizing carbon storage can be a win-win pathway to conserving biodiversity and mitigating climate change. In savannas, however, the situation is more complex. Promoting carbon storage through woody encroachment may reduce plant diversity of savanna endemics, even as the diversity of encroaching forest species increases. This trade-off has important implications for the management of biodiversity and carbon in savanna habitats, but has rarely been evaluated empirically. We quantified the nature of carbon-diversity relationships in the Brazilian Cerrado by analyzing how woody plant species richness changed with carbon storage in 206 sites across the 2.2 million km(2) region at two spatial scales. We show that total woody plant species diversity increases with carbon storage, as expected, but that the richness of endemic savanna woody plant species declines with carbon storage both at the local scale, as woody biomass accumulates within plots, and at the landscape scale, as forest replaces savanna. The sharpest trade-offs between carbon storage and savanna diversity occurred at the early stages of carbon accumulation at the local scale but the final stages of forest encroachment at the landscape scale. Furthermore, the loss of savanna species quickens in the final stages of forest encroachment, and beyond a point, savanna species losses outpace forest species gains with increasing carbon accumulation. Our results suggest that although woody encroachment in savanna ecosystems may provide substantial carbon benefits, it comes at the rapidly accruing cost of woody plant species adapted to the open savanna environment. Moreover, the dependence of carbon-diversity trade-offs on the amount of savanna area remaining requires land managers to carefully consider local conditions. Widespread woody encroachment in both Australian and African savannas and grasslands may present similar threats to biodiversity.

Fire alters ecosystem carbon and nutrients but not plant nutrient stoichiometry or composition in tropical savanna.

Fire and nutrients interact to influence the global distribution and dynamics of the savanna biome, but the results of these interactions are both complex and poorly known. A critical but unresolved question is whether short-term losses of carbon and nutrients caused by fire can trigger long-term and potentially compensatory responses in the nutrient stoichiometry of plants, or in the abundance of dinitrogen-fixing trees. There is disagreement in the literature about the potential role of fire on savanna nutrients, and, in turn, on plant stoichiometry and composition. A major limitation has been the lack of fire manipulations over time scales sufficiently long for these interactions to emerge. We use a 58-year, replicated, large-scale, fire manipulation experiment in Kruger National Park (South Africa) in savanna to quantify the effect of fire on (1) distributions of carbon, nitrogen, and phosphorus at the ecosystem scale; (2) carbon: nitrogen: phosphorus stoichiometry of above- and belowground tissues of plant species; and (3) abundance of plant functional groups including nitrogen fixers. Our results show dramatic effects of fire on the relative distribution of nutrients in soils, but that individual plant stoichiometry and plant community composition remained unexpectedly resilient. Moreover, measures of nutrients and carbon stable isotopes allowed us to discount the role of tree cover change in favor of the turnover of herbaceous biomass as the primary mechanism that mediates a transition from low to high 'soil carbon and nutrients in the absence of fire. We conclude that, in contrast to extra-tropical grasslands or closed-canopy forests, vegetation in the savanna biome may be uniquely adapted to nutrient losses caused by recurring fire.

Carbon accumulation and nitrogen pool recovery during transitions from savanna to forest in central Brazil.

The expansion of tropical forest into savanna may potentially be a large carbon sink, but little is known about the patterns of carbon sequestration during transitional forest formation. Moreover, it is unclear how nutrient limitation, due to extended exposure to fire-driven nutrient losses, may constrain carbon accumulation. Here, we sampled plots that spanned a woody biomass gradient from savanna to transitional forest in response to differential fire protection in central Brazil. These plots were used to investigate how the process of transitional forest formation affects the size and distribution of carbon (C) and nitrogen (N) pools. This was paired with a detailed analysis of the nitrogen cycle to explore possible connections between carbon accumulation and nitrogen limitation. An analysis of carbon pools in the vegetation, upper soil, and litter shows that the transition from savanna to transitional forest can result in a fourfold increase in total carbon (from 43 to 179 Mg C/ha) with a doubling of carbon stocks in the litter and soil layers. Total nitrogen in the litter and soil layers increased with forest development in both the bulk (+68%) and plant-available (+150%) pools, with the most pronounced changes occurring in the upper layers. However, the analyses of nitrate concentrations, nitrate:ammonium ratios, plant stoichiometry of carbon and nitrogen, and soil and foliar nitrogen isotope ratios suggest that a conservative nitrogen cycle persists throughout forest development, indicating that nitrogen remains in low supply relative to demand. Furthermore, the lack of variation in underlying soil type (>20 cm depth) suggests that the biogeochemical trends across the gradient are driven by vegetation. Our results provide evidence for high carbon sequestration potential with forest encroachment on savanna, but nitrogen limitation may play a large and persistent role in governing carbon sequestration in savannas or other equally fire-disturbed tropical landscapes. In turn, the link between forest development and nitrogen pool recovery creates a framework for evaluating potential positive feedbacks on savanna-forest boundaries.

Fire frequency and type regulate the response of soil carbon cycling and storage to fire across soil depths and ecosystems: A meta-analysis.

Fire is a very common disturbance in terrestrial ecosystems and can give rise to significant effects on soil carbon (C) cycling and storage. Here, we conducted a global meta-analysis on the response of soil C cycling and storage across soil profiles (organic layer, 0-5 cm, 0-10 cm, 0-20 cm, and 20-100 cm) to fire reported in 308 studies across 383 sites and examined the role of fire frequency, fire type, soil type, ecosystem type, and post-fire time in regulating the response of soil C dynamics to fire. Overall, we found soil C cycling and storage were more responsive to one fire and wildfire as compared to frequent fire and prescribed fire, respectively. Soil respiration significantly decreased by 22 ± 9% by one fire, but was not significantly affected by frequent fire across ecosystems. One fire significantly reduced soil C content in the organic, 0-10 cm, and 20-100 cm layers by 27 ± 16%, 10 ± 9%, and 33 ± 18%, respectively, while frequent fire significantly reduced soil C content at a depth of 0-5 cm and 0-20 cm by 29 ± 8% and 16 ± 12%, respectively. Soil C cycling and storage showed little response to frequent prescribed fire. In addition, the response of soil C cycling and storage varied among different soil and ecosystem types, with a stronger response being observed in forest than in grassland. Within 20 years post-fire, soil C cycling and storage tended to recover only after one fire but not after frequent fire. We also found that soil physicochemical properties and microbial communities were more responsive to one fire than frequent fire, which could indirectly affect the effects of fire on soil C cycling and storage. The results of our study have filled some critical gaps in previous meta-analyses in fire ecology.

Global stocks and capacity of mineral-associated soil organic carbon.

Soil is the largest terrestrial reservoir of organic carbon and is central for climate change mitigation and carbon-climate feedbacks. Chemical and physical associations of soil carbon with minerals play a critical role in carbon storage, but the amount and global capacity for storage in this form remain unquantified. Here, we produce spatially-resolved global estimates of mineral-associated organic carbon stocks and carbon-storage capacity by analyzing 1144 globally-distributed soil profiles. We show that current stocks total 899 Pg C to a depth of 1 m in non-permafrost mineral soils. Although this constitutes 66% and 70% of soil carbon in surface and deeper layers, respectively, it is only 42% and 21% of the mineralogical capacity. Regions under agricultural management and deeper soil layers show the largest undersaturation of mineral-associated carbon. Critically, the degree of undersaturation indicates sequestration efficiency over years to decades. We show that, across 103 carbon-accrual measurements spanning management interventions globally, soils furthest from their mineralogical capacity are more effective at accruing carbon; sequestration rates average 3-times higher in soils at one tenth of their capacity compared to soils at one half of their capacity. Our findings provide insights into the world's soils, their capacity to store carbon, and priority regions and actions for soil carbon management.

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.