Long-term, large-scale experiment reveals the effects of seed limitation, climate, and anthropogenic disturbance on restoration of plant communities in a biodiversity hotspot.

Ecological restoration is essential for maintaining biodiversity in the face of dynamic, global changes in climate, human land use, and disturbance regimes. Effective restoration requires understanding bottlenecks in plant community recovery that exist today, while recognizing that these bottlenecks may relate to complex histories of environmental change. Such understanding has been a challenge because few long-term, well-replicated experiments exist to decipher the demographic processes influencing recovery for numerous species against the backdrop of multiyear variation in climate and management. We address this challenge through a long-term and geographically expansive experiment in longleaf pine savannas, an imperiled ecosystem and biodiversity hotspot in the southeastern United States. Using 48 sites at three locations spanning 480 km, the 8-y experiment manipulated initial seed arrival for 24 herbaceous plant species and presence of competitors to evaluate the impacts of climate variability and management actions (e.g., prescribed burning) on plant establishment and persistence. Adding seeds increased plant establishment of many species. Cool and wet climatic conditions, low tree density, and reduced litter depth also promoted establishment. Once established, most species persisted for the duration of the 8-y experiment. Plant traits were most predictive when tightly coupled to the process of establishment. Our results illustrate how seed additions can restore plant diversity and how interannual climatic variation affects the dynamics of plant communities across a large region. The significant effects of temperature and precipitation inform how future climate may affect restoration and conservation via large-scale changes in the fundamental processes of establishment and persistence.

High plant diversity and slow assembly of old-growth grasslands.

Earth's ancient grasslands and savannas-hereafter old-growth grasslands-have long been viewed by scientists and environmental policymakers as early successional plant communities of low conservation value. Challenging this view, emerging research suggests that old-growth grasslands support substantial biodiversity and are slow to recover if destroyed by human land uses (e.g., tillage agriculture, plantation forestry). But despite growing interest in grassland conservation, there has been no global test of whether old-growth grasslands support greater plant species diversity than secondary grasslands (i.e., herbaceous communities that assemble after destruction of old-growth grasslands). Our synthesis of 31 studies, including 92 timepoints on six continents, found that secondary grasslands supported 37% fewer plant species than old-growth grasslands (log response ratio = -0.46) and that secondary grasslands typically require at least a century, and more often millennia (projected mean 1,400 y), to recover their former richness. Young (<29 y) secondary grasslands were composed of weedy species, and even as their richness increased over decades to centuries, secondary grasslands were still missing characteristic old-growth grassland species (e.g., long-lived perennials). In light of these results, the view that all grasslands are weedy communities, trapped by fire and large herbivores in a state of arrested succession, is untenable. Moving forward, we suggest that ecologists should explicitly consider grassland assembly time and endogenous disturbance regimes in studies of plant community structure and function. We encourage environmental policymakers to prioritize old-growth grassland conservation and work to elevate the status of old-growth grasslands, alongside old-growth forests, in the public consciousness.

Spreaders, igniters, and burning shrubs: plant flammability explains novel fire dynamics in grass-invaded deserts.

Novel fire regimes are an important cause and consequence of global environmental change that involve interactions among biotic, climatic, and human components of ecosystems. Plant flammability is key to these interactions, yet few studies directly measure flammability or consider how multiple species with different flammabilities interact to produce novel fire regimes. Deserts of the southwestern United States are an ideal system for exploring how novel fire regimes can emerge when fire-promoting species invade ecosystems comprised of species that did not evolve with fire. In these deserts, exotic annual grasses provide fuel continuity across landscapes that did not historically burn. These fires often ignite a keystone desert shrub, the fire-intolerant creosote bush, Larrea tridentata (DC.) Coville. Ignition of Larrea is likely catalyzed by fuels produced by native plants that grow beneath the shrubs. We hypothesize that invasive and native species exhibit distinct flammability characteristics that in combination determine spatial patterns of fire spread and intensity. We measured flammability metrics of Larrea, two invasive grasses, Schismus arabicus and Bromus madritensis, and two native plants, the sub-shrub Ambrosia dumosa and the annual herb Amsinckia menziesii. Results of laboratory experiments show that the grasses carry fire quickly (1.32 cm/s), but burn for short duration (0.5 min) at low temperatures. In contrast, native plants spread fire slowly (0.12 cm/s), but burn up to eight times longer (4 min) and produced hotter fires. Additional experiments on the ignition requirements of Larrea suggest that native plants burn with sufficient temperature and duration to ignite dead Larrea branches (time to ignition, 2 min; temperature at ignition 692°C). Once burning, these dead branches ignite living branches in the upper portions of the shrub. Our study provides support for a conceptual model in which exotic grasses are "spreaders" of fire and native plants growing beneath shrubs are "igniters" of dead Larrea branches. Once burning, flames produced by dead branches engulf the entire shrub, resulting in locally intense fires without historical precedent in this system. We suggest that fire models and conservation-focused management could be improved by incorporating the distinct flammability characteristics and spatial distributions of spreaders, igniters, and keystone shrubs.

Historical agriculture alters the effects of fire on understory plant beta diversity.

Land-use legacies are known to shape the diversity and distribution of plant communities, but we lack an understanding of whether historical land use influences community responses to contemporary disturbances. Because human-modified landscapes often bear a history of multiple land-use activities, this contingency can challenge our understanding of land-use impacts on plant diversity. We address this contingency by evaluating how beta diversity (the spatial variability of species composition), an important component of regional biodiversity, is shaped by interactions between historical agriculture and prescribed fire, two prominent disturbances that are often coincident in terrestrial ecosystems. At three study locations spanning 450 km in the southeastern United States, we surveyed longleaf pine woodland understory plant communities across 232 remnant and post-agricultural sites with differing prescribed fire regimes. Our results demonstrate that agricultural legacies are a strong predictor of beta diversity, but the direction of this land-use effect differed among the three study locations. Further, although beta diversity increased with prescribed fire frequency at each study location, this effect was influenced by agricultural land-use history, such that positive fire effects were only documented among sites that lacked a history of agriculture at two of our three study locations. Our study not only highlights the role of historical agriculture in shaping beta diversity in a fire-maintained ecosystem but also illustrates how this effect can be contingent upon fire regime and geographic location. We suggest that interactions among historical and contemporary land-use activities may help to explain dissimilarities in plant communities among sites in human-dominated landscapes.

Reproducible protocol for the extraction and semi-automated quantification of macroscopic charcoal from soil.

Charcoal fragments preserved in soils or sediments are used by scientists to reconstruct fire histories and thereby improve our understanding of past vegetation dynamics and human-plant relationships. Unfortunately, most published methods for charcoal extraction and analysis are incompletely described and are therefore difficult to reproduce. To improve the standardization and replicability of soil charcoal analysis, as well as to facilitate accessibility for non-experts, we developed a detailed, step-by-step protocol to isolate charcoal from soil and to efficiently count and measure charcoal fragments. The extraction phase involves the chemical soaking and wet sieving of soils followed by the collection of macrocharcoal (≥500 µm). The analysis phase is performed semi-automatically using the open-source software ImageJ to count and measure the area, length, and width of fragments from light stereo microscope images by means of threshold segmentation. The protocol yields clean charcoal fragments, a set of charcoal images, and datasets containing total charcoal mass, number of fragments, and morphological measurements (area, length, and width) for each sample. We tested and validated the protocol on 339 soil samples from tropical savannas and forests in eastern lowland Bolivia. We hope that this protocol will be a valuable resource for scientists in a variety of fields who currently study, or wish to study, macroscopic charcoal in soils as a proxy for past fires.

Understory plant communities and the functional distinction between savanna trees, forest trees, and pines.

Although savanna trees and forest trees are thought to represent distinct functional groups with different effects on ecosystem processes, few empirical studies have examined these effects. In particular, it remains unclear if savanna and forest trees differ in their ability to coexist with understory plants, which comprise the majority of plant diversity in most savannas. We used structural equation modeling (SEM) and data from 157 sites across three locations in the southeastern United States to understand the effects of broadleaf savanna trees, broadleaf forest trees, and pine trees on savanna understory plant communities. After accounting for underlying gradients in fire frequency and soil moisture, abundances (i.e., basal area and stem density) of forest trees and pines, but not savanna trees, were negatively correlated with the cover and density (i.e., local-scale species richness) of C4 graminoid species, a defining savanna understory functional group that is linked to ecosystem flammability. In analyses of the full understory community, abundances of trees from all functional groups were negatively correlated with species density and cover. For both the C4 and full communities, fire frequency promoted understory plants directly, and indirectly by limiting forest tree abundance. There was little indirect influence of fire on the understory mediated through savanna trees and pines, which are morefire tolerant than forest trees. We conclude that tree functional identity is an important factor that influences overstory tree relationships with savanna understory plant communities. In particular, distinct relationships between trees and C4 graminoids have implications for grass-tree coexistence and vegetation-fire feedbacks that maintain savanna environments and their associated understory plant diversity.

How climate, topography, soils, herbivores, and fire control forest-grassland coexistence in the Eurasian forest-steppe.

Recent advances in ecology and biogeography demonstrate the importance of fire and large herbivores - and challenge the primacy of climate - to our understanding of the distribution, stability, and antiquity of forests and grasslands. Among grassland ecologists, particularly those working in savannas of the seasonally dry tropics, an emerging fire-herbivore paradigm is generally accepted to explain grass dominance in climates and on soils that would otherwise permit development of closed-canopy forests. By contrast, adherents of the climate-soil paradigm, particularly foresters working in the humid tropics or temperate latitudes, tend to view fire and herbivores as disturbances, often human-caused, which damage forests and reset succession. Towards integration of these two paradigms, we developed a series of conceptual models to explain the existence of an extensive temperate forest-grassland mosaic that occurs within a 4.7 million km2 belt spanning from central Europe through eastern Asia. The Eurasian forest-steppe is reminiscent of many regions globally where forests and grasslands occur side-by-side with stark boundaries. Our conceptual models illustrate that if mean climate was the only factor, forests should dominate in humid continental regions and grasslands should prevail in semi-arid regions, but that extensive mosaics would not occur. By contrast, conceptual models that also integrate climate variability, soils, topography, herbivores, and fire depict how these factors collectively expand suitable conditions for forests and grasslands, such that grasslands may occur in more humid regions and forests in more arid regions than predicted by mean climate alone. Furthermore, boundaries between forests and grasslands are reinforced by vegetation-fire, vegetation-herbivore, and vegetation-microclimate feedbacks, which limit tree establishment in grasslands and promote tree survival in forests. Such feedbacks suggest that forests and grasslands of the Eurasian forest-steppe are governed by ecological dynamics that are similar to those hypothesised to maintain boundaries between tropical forests and savannas. Unfortunately, the grasslands of the Eurasian forest-steppe are sometimes misinterpreted as deforested or otherwise degraded vegetation. In fact, the grasslands of this region provide valuable ecosystem services, support a high diversity of plants and animals, and offer critical habitat for endangered large herbivores. We suggest that a better understanding of the fundamental ecological controls that permit forest-grassland coexistence could help us prioritise conservation and restoration of the Eurasian forest-steppe for biodiversity, climate adaptation, and pastoral livelihoods. Currently, these goals are being undermined by tree-planting campaigns that view the open grasslands as opportunities for afforestation. Improved understanding of the interactive roles of climate variability, soils, topography, fire, and herbivores will help scientists and policymakers recognise the antiquity of the grasslands of the Eurasian forest-steppe.

Resilience and restoration of tropical and subtropical grasslands, savannas, and grassy woodlands.

Despite growing recognition of the conservation values of grassy biomes, our understanding of how to maintain and restore biodiverse tropical grasslands (including savannas and open-canopy grassy woodlands) remains limited. To incorporate grasslands into large-scale restoration efforts, we synthesised existing ecological knowledge of tropical grassland resilience and approaches to plant community restoration. Tropical grassland plant communities are resilient to, and often dependent on, the endogenous disturbances with which they evolved - frequent fires and native megafaunal herbivory. In stark contrast, tropical grasslands are extremely vulnerable to human-caused exogenous disturbances, particularly those that alter soils and destroy belowground biomass (e.g. tillage agriculture, surface mining); tropical grassland restoration after severe soil disturbances is expensive and rarely achieves management targets. Where grasslands have been degraded by altered disturbance regimes (e.g. fire exclusion), exotic plant invasions, or afforestation, restoration efforts can recreate vegetation structure (i.e. historical tree density and herbaceous ground cover), but species-diverse plant communities, including endemic species, are slow to recover. Complicating plant-community restoration efforts, many tropical grassland species, particularly those that invest in underground storage organs, are difficult to propagate and re-establish. To guide restoration decisions, we draw on the old-growth grassland concept, the novel ecosystem concept, and theory regarding tree cover along resource gradients in savannas to propose a conceptual framework that classifies tropical grasslands into three broad ecosystem states. These states are: (1) old-growth grasslands (i.e. ancient, biodiverse grassy ecosystems), where management should focus on the maintenance of disturbance regimes; (2) hybrid grasslands, where restoration should emphasise a return towards the old-growth state; and (3) novel ecosystems, where the magnitude of environmental change (i.e. a shift to an alternative ecosystem state) or the socioecological context preclude a return to historical conditions.

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.

Natural climate solutions for the United States.

Limiting climate warming to <2°C requires increased mitigation efforts, including land stewardship, whose potential in the United States is poorly understood. We quantified the potential of natural climate solutions (NCS)-21 conservation, restoration, and improved land management interventions on natural and agricultural lands-to increase carbon storage and avoid greenhouse gas emissions in the United States. We found a maximum potential of 1.2 (0.9 to 1.6) Pg CO2e year-1, the equivalent of 21% of current net annual emissions of the United States. At current carbon market prices (USD 10 per Mg CO2e), 299 Tg CO2e year-1 could be achieved. NCS would also provide air and water filtration, flood control, soil health, wildlife habitat, and climate resilience benefits.

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.

Clarifying the confusion: old-growth savannahs and tropical ecosystem degradation.

Ancient tropical grassy biomes are often misrecognized as severely degraded forests. I trace this confusion to several factors, with roots in the nineteenth century, including misinterpretations of the nature of fire in savannahs, attempts to reconcile savannah ecology with Clementsian succession, use of physiognomic (structural) definitions of savannah and development of tropical degradation frameworks focused solely on forests. Towards clarity, I present two models that conceptualize the drivers of ecosystem degradation as operating in both savannahs and forests. These models highlight how human-induced environmental changes create ecosystems with superficially similar physiognomies but radically different conservation values. Given the limitation of physiognomy to differentiate savannahs from severely degraded forests, I present an alternative approach based on floristic composition. Data from eastern lowland Bolivia show that old-growth savannahs can be reliably distinguished by eight grass species and that species identity influences ecosystem flammability. I recommend that scientists incorporate savannahs in tropical degradation frameworks alongside forests, and that savannah be qualified as old-growth savannah in reference to ancient grassy biomes or derived savannah in reference to deforestation. These conceptual advances will require attention not only to tree cover, but also to savannah herbaceous plant species and their ecologies.This article is part of the themed issue 'Tropical grassy biomes: linking ecology, human use and conservation'.

Land-use history and contemporary management inform an ecological reference model for longleaf pine woodland understory plant communities.

Ecological restoration is frequently guided by reference conditions describing a successfully restored ecosystem; however, the causes and magnitude of ecosystem degradation vary, making simple knowledge of reference conditions insufficient for prioritizing and guiding restoration. Ecological reference models provide further guidance by quantifying reference conditions, as well as conditions at degraded states that deviate from reference conditions. Many reference models remain qualitative, however, limiting their utility. We quantified and evaluated a reference model for southeastern U.S. longleaf pine woodland understory plant communities. We used regression trees to classify 232 longleaf pine woodland sites at three locations along the Atlantic coastal plain based on relationships between understory plant community composition, soils (which broadly structure these communities), and factors associated with understory degradation, including fire frequency, agricultural history, and tree basal area. To understand the spatial generality of this model, we classified all sites together and for each of three study locations separately. Both the regional and location-specific models produced quantifiable degradation gradients-i.e., progressive deviation from conditions at 38 reference sites, based on understory species composition, diversity and total cover, litter depth, and other attributes. Regionally, fire suppression was the most important degrading factor, followed by agricultural history, but at individual locations, agricultural history or tree basal area was most important. At one location, the influence of a degrading factor depended on soil attributes. We suggest that our regional model can help prioritize longleaf pine woodland restoration across our study region; however, due to substantial landscape-to-landscape variation, local management decisions should take into account additional factors (e.g., soil attributes). Our study demonstrates the utility of quantifying degraded states and provides a series of hypotheses for future experimental restoration work. More broadly, our work provides a framework for developing and evaluating reference models that incorporate multiple, interactive anthropogenic drivers of ecosystem degradation.