Linking resource- and disturbance-based models to explain tree-grass coexistence in savannas.

Savannas cover a significant fraction of the Earth's land surface. In these ecosystems, C3 trees and C4 grasses coexist persistently, but the mechanisms explaining coexistence remain subject to debate. Different quantitative models have been proposed to explain coexistence, but these models make widely contrasting assumptions about which mechanisms are responsible for savanna persistence. Here, we show that no single existing model fully captures all key elements required to explain tree-grass coexistence across savanna rainfall gradients, but many models make important contributions. We show that recent empirical work allows us to combine many existing elements with new ideas to arrive at a synthesis that combines elements of two dominant frameworks: Walter's two-layer model and demographic bottlenecks. We propose that functional rooting separation is necessary for coexistence and is the crux of the coexistence problem. It is both well-supported empirically and necessary for tree persistence, given the comprehensive grass superiority for soil moisture acquisition. We argue that eventual tree dominance through shading is precluded by ecohydrological constraints in dry savannas and by fire and herbivores in wet savannas. Strong asymmetric grass-tree competition for soil moisture limits tree growth, exposing trees to persistent demographic bottlenecks.

African savanna grasses outperform trees across the full spectrum of soil moisture availability.

Models of tree-grass coexistence in savannas make different assumptions about the relative performance of trees and grasses under wet vs dry conditions. We quantified transpiration and drought tolerance traits in 26 tree and 19 grass species from the African savanna biome across a gradient of soil water potentials to test for a trade-off between water use under wet conditions and drought tolerance. We measured whole-plant hourly transpiration in a growth chamber and quantified drought tolerance using leaf osmotic potential (Ψosm ). We also quantified whole-plant water-use efficiency (WUE) and relative growth rate (RGR) under well-watered conditions. Grasses transpired twice as much as trees on a leaf-mass basis across all soil water potentials. Grasses also had a lower Ψosm than trees, indicating higher drought tolerance in the former. Higher grass transpiration and WUE combined to largely explain the threefold RGR advantage in grasses. Our results suggest that grasses outperform trees under a wide range of conditions, and that there is no evidence for a trade-off in water-use patterns in wet vs dry soils. This work will help inform mechanistic models of water use in savanna ecosystems, providing much-needed whole-plant parameter estimates for African species.

Structural diversity and tree density drives variation in the biodiversity-ecosystem function relationship of woodlands and savannas.

Positive biodiversity-ecosystem function relationships (BEFRs) have been widely documented, but it is unclear if BEFRs should be expected in disturbance-driven systems. Disturbance may limit competition and niche differentiation, which are frequently posited to underlie BEFRs. We provide the first exploration of the relationship between tree species diversity and biomass, one measure of ecosystem function, across southern African woodlands and savannas, an ecological system rife with disturbance from fire, herbivores and humans. We used > 1000 vegetation plots distributed across 10 southern African countries and structural equation modelling to determine the relationship between tree species diversity and above-ground woody biomass, accounting for interacting effects of resource availability, disturbance by fire, tree stem density and vegetation type. We found positive effects of tree species diversity on above-ground biomass, operating via increased structural diversity. The observed BEFR was highly dependent on organismal density, with a minimum threshold of c. 180 mature stems ha-1 . We found that water availability mainly affects biomass indirectly, via increasing species diversity. The study underlines the close association between tree diversity, ecosystem structure, environment and function in highly disturbed savannas and woodlands. We suggest that tree diversity is an under-appreciated determinant of wooded ecosystem structure and function.

Root vascular traits differ systematically between African savanna tree and grass species, with implications for water use.

PREMISE: Belowground functional traits play a significant role in determining plant water-use strategies and plant performance, but we lack data on root traits across communities, particularly in the tropical savanna biome, where vegetation dynamics are hypothesized to be strongly driven by tree-grass functional differences in water use. METHODS: We grew seedlings of 21 tree and 18 grass species (N = 5 individuals per species) from the southern African savanna biome under greenhouse conditions and collected fine-root segments from plants for histological analysis. We identified and measured xylem vessels in 539 individual root cross sections. We then quantified six root vascular anatomy traits and tested them for phylogenetic signals and tree-grass differences in trait values associated with vessel size, number, and hydraulic conductivity. RESULTS: Grass roots had larger root xylem vessels than trees, a higher proportion of their root cross-sectional area comprised vessels, and they had higher estimated axial conductivities than trees, while trees had a higher number of vessels per root cross-sectional area than grasses did. We found evidence of associations between trait values and phylogenetic relatedness in most of these traits across tree species, but not grasses. CONCLUSIONS: Our findings support the hypothesis that grass roots have higher water transport capacity than tree roots in terms of maximum axial conductivity, consistent with the observation that grasses are more "aggressive" water users than trees under conditions of high soil moisture availability. Our study identifies root functional traits that may drive differential responses of trees and grasses to soil moisture availability.

Anthropogenic modifications to fire regimes in the wider Serengeti-Mara ecosystem.

Fire is a key driver in savannah systems and widely used as a land management tool. Intensifying human land uses are leading to rapid changes in the fire regimes, with consequences for ecosystem functioning and composition. We undertake a novel analysis describing spatial patterns in the fire regime of the Serengeti-Mara ecosystem, document multidecadal temporal changes and investigate the factors underlying these patterns. We used MODIS active fire and burned area products from 2001 to 2014 to identify individual fires; summarizing four characteristics for each detected fire: size, ignition date, time since last fire and radiative power. Using satellite imagery, we estimated the rate of change in the density of livestock bomas as a proxy for livestock density. We used these metrics to model drivers of variation in the four fire characteristics, as well as total number of fires and total area burned. Fires in the Serengeti-Mara show high spatial variability-with number of fires and ignition date mirroring mean annual precipitation. The short-term effect of rainfall decreases fire size and intensity but cumulative rainfall over several years leads to increased standing grass biomass and fuel loads, and, therefore, in larger and hotter fires. Our study reveals dramatic changes over time, with a reduction in total number of fires and total area burned, to the point where some areas now experience virtually no fire. We suggest that increasing livestock numbers are driving this decline, presumably by inhibiting fire spread. These temporal patterns are part of a global decline in total area burned, especially in savannahs, and we caution that ecosystem functioning may have been compromised. Land managers and policy formulators need to factor in rapid fire regime modifications to achieve management objectives and maintain the ecological function of savannah ecosystems.

Rooting depth varies differentially in trees and grasses as a function of mean annual rainfall in an African savanna.

A significant fraction of the terrestrial biosphere comprises biomes containing tree-grass mixtures. Forecasting vegetation dynamics in these environments requires a thorough understanding of how trees and grasses use and compete for key belowground resources. There is disagreement about the extent to which tree-grass vertical root separation occurs in these ecosystems, how this overlap varies across large-scale environmental gradients, and what these rooting differences imply for water resource availability and tree-grass competition and coexistence. To assess the extent of tree-grass rooting overlap and how tree and grass rooting patterns vary across resource gradients, we examined landscape-level patterns of tree and grass functional rooting depth along a mean annual precipitation (MAP) gradient extending from ~ 450 to ~ 750 mm year-1 in Kruger National Park, South Africa. We used stable isotopes from soil and stem water to make inferences about relative differences in rooting depth between these two functional groups. We found clear differences in rooting depth between grasses and trees across the MAP gradient, with grasses generally exhibiting shallower rooting profiles than trees. We also found that trees tended to become more shallow-rooted as a function of MAP, to the point that trees and grasses largely overlapped in terms of rooting depth at the wettest sites. Our results reconcile previously conflicting evidence for rooting overlap in this system, and have important implications for understanding tree-grass dynamics under altered precipitation scenarios.

Trade-offs between growth and maturation: the cost of reproduction for surviving environmental extremes.

Life-history trade-offs and the costs of reproduction are central concepts in evolution and ecology. Episodic climatic events such as drought and extreme temperatures provide strong selective pressures that can change the balance of these costs and trade-offs. We used size-structured matrix models parameterized from field and laboratory studies to examine the effect of periodic drought on two species of aquatic salamanders (greater siren, Siren lacertina; lesser siren, Siren intermedia) that differ in size at reproduction and maximum body size. Post-drought body size distributions of the larger species (S. lacertina) are consistent with size-dependent mortality. Smaller individuals were extirpated from the population during each drought while large animals persisted, a pattern that contrasted with that seen in several ectotherms. This appears to be largely explained by estivation proficiency and a positive relationship between body size and estivation potential. Increased body size, however, may come at the cost of fecundity and maturation rate compared to a closely related congener. The cost of somatic allocation in this case may manifest itself via reduced per-capita competitive ability, which (at least in simulation studies) allows the smaller, fast-maturing species to outcompete the larger, slow-maturing species when drought is minimal or nonexistent.

Effects of migratory animals on resident parasite dynamics.

Migratory animals can bring parasites into resident animal (i.e., non-migratory) home ranges (transport effects) and exert trophic effects that either promote or reduce parasite exposure to resident hosts. Here, we examine the importance of these transport and trophic effects and their interactions for resident parasite dynamics. We propose that migrant transport and trophic effects are impacted by the number of migratory animals entering a resident's home range (migration intensity), the amount of time that migrants spend within a resident's home range (migration duration), and the timing of migrant-resident interactions. We then incorporate migration intensity, duration, and timing into a framework for exploring the net impact of migrant trophic and transport effects on resident animal parasite prevalence.

Interplay of competition and facilitation in grazing succession by migrant Serengeti herbivores.

Competition, facilitation, and predation offer alternative explanations for successional patterns of migratory herbivores. However, these interactions are difficult to measure, leaving uncertainty about the mechanisms underlying body-size-dependent grazing-and even whether succession occurs at all. We used data from an 8-year camera-trap survey, GPS-collared herbivores, and fecal DNA metabarcoding to analyze the timing, arrival order, and interactions among migratory grazers in Serengeti National Park. Temporal grazing succession is characterized by a "push-pull" dynamic: Competitive grazing nudges zebra ahead of co-migrating wildebeest, whereas grass consumption by these large-bodied migrants attracts trailing, small-bodied gazelle that benefit from facilitation. "Natural experiments" involving intense wildfires and rainfall respectively disrupted and strengthened these effects. Our results highlight a balance between facilitative and competitive forces in co-regulating large-scale ungulate migrations.

Inferring animal population distributions from individual tracking data: theoretical insights and potential pitfalls.

Animal population-level phenomena are often inferred from large tracking data sets obtained from only a few individuals. Two key challenges are to understand how these two scales are related, and to identify the factors that influence the extent to which small samples consisting of a few individuals can predict spatial patterns at the population scale. We used a simple spatially explicit theoretical model to explore some of the factors that affect inferences made at the population level from individual tracking data. We adopted a 'mixtures of correlated random walks' approach to simulate two discrete movement modes with different step lengths and turning angles in a hypothetical ungulate population with contrasting population sizes and sampling intensities. Movement state was assumed to be influenced by habitat type (patch or matrix) and social cues. We explored the predictive power of a tracked population subsample by regressing the space-use map generated by a few randomly chosen individuals against the map generated by the entire population (the 'true' map) for different scenarios (e.g. random and clumped habitat distributions) and parameter values. We show that the predictive power of the tracking sample varies nonlinearly and often counter-intuitively with factors such as habitat preference, the spatial context of the landscape and the importance of social interactions. We suggest that movement models coupled with individual tracking data can be used with Monte Carlo simulations to improve tracking studies by better understanding the links between detailed individual movement data and population distributions.

Impacts of large herbivores on terrestrial ecosystems.

Large herbivores play unique ecological roles and are disproportionately imperiled by human activity. As many wild populations dwindle towards extinction, and as interest grows in restoring lost biodiversity, research on large herbivores and their ecological impacts has intensified. Yet, results are often conflicting or contingent on local conditions, and new findings have challenged conventional wisdom, making it hard to discern general principles. Here, we review what is known about the ecosystem impacts of large herbivores globally, identify key uncertainties, and suggest priorities to guide research. Many findings are generalizable across ecosystems: large herbivores consistently exert top-down control of plant demography, species composition, and biomass, thereby suppressing fires and the abundance of smaller animals. Other general patterns do not have clearly defined impacts: large herbivores respond to predation risk but the strength of trophic cascades is variable; large herbivores move vast quantities of seeds and nutrients but with poorly understood effects on vegetation and biogeochemistry. Questions of the greatest relevance for conservation and management are among the least certain, including effects on carbon storage and other ecosystem functions and the ability to predict outcomes of extinctions and reintroductions. A unifying theme is the role of body size in regulating ecological impact. Small herbivores cannot fully substitute for large ones, and large-herbivore species are not functionally redundant - losing any, especially the largest, will alter net impact, helping to explain why livestock are poor surrogates for wild species. We advocate leveraging a broad spectrum of techniques to mechanistically explain how large-herbivore traits and environmental context interactively govern the ecological impacts of these animals.

A disease-mediated trophic cascade in the Serengeti and its implications for ecosystem C.

Tree cover is a fundamental structural characteristic and driver of ecosystem processes in terrestrial ecosystems, and trees are a major global carbon (C) sink. Fire and herbivores have been hypothesized to play dominant roles in regulating trees in African savannas, but the evidence for this is conflicting. Moving up a trophic scale, the factors that regulate fire occurrence and herbivores, such as disease and predation, are poorly understood for any given ecosystem. We used a Bayesian state-space model to show that the wildebeest population eruption that followed disease (rinderpest) eradication in the Serengeti ecosystem of East Africa led to a widespread reduction in the extent of fire and an ongoing recovery of the tree population. This supports the hypothesis that disease has played a key role in the regulation of this ecosystem. We then link our state-space model with theoretical and empirical results quantifying the effects of grazing and fire on soil carbon to predict that this cascade may have led to important shifts in the size of pools of C stored in soil and biomass. Our results suggest that the dynamics of herbivores and fire are tightly coupled at landscape scales, that fire exerts clear top-down effects on tree density, and that disease outbreaks in dominant herbivores can lead to complex trophic cascades in savanna ecosystems. We propose that the long-term status of the Serengeti and other intensely grazed savannas as sources or sinks for C may be fundamentally linked to the control of disease outbreaks and poaching.

Responses to alternative rainfall regimes and antipoaching in a migratory system.

Migratory ungulates may be particularly vulnerable to the challenges imposed by growing human populations and climate change. These species depend on vast areas to sustain their migratory behavior, and in many cases come into frequent contact with human populations outside protected areas. They may also act as spatial coupling agents allowing feedbacks between ecological systems and local economies, particularly in the agropastoral subsistence economies found in the African savanna biome. We used HUMENTS, a spatially realistic socioecological model of the Greater Serengeti Ecosystem in East Africa, to explore the potential impacts of changing climate and poaching on the migratory wildebeest (Connochaetes taurinus) population, the fire regime, and habitat structure in the ecosystem, as well as changes in the size and economic activities of the human population outside the protected area. Unlike earlier models, the HUMENTS model predicted only moderate declines in the wildebeest population associated with an increasing human population over the next century, with a gradual expansion of agriculture, more poaching, and increases in fire frequency and reduced tree density. Changes in rainfall were predicted to have strong asymmetric effects on the size and economic activity of the human population and on livestock, and more moderate effects on wildlife and other ecological indicators. Conversely, antipoaching had a stronger effect on the ecological portion of the system because of its effect on wildebeest (and therefore on fire and habitat structure), and a weaker effect on the socioeconomic component, except in areas directly adjacent to the protected-area boundary, which were affected by crop-raiding and the availability of wildlife as a source of income. The results highlight the strong direct and indirect effects of rainfall on the various components of socioecological systems in semiarid environments, and the key role of mobile wildlife populations as agents of spatial coupling between the human-dominated and natural portions of ecosystems. They also underscore the fundamental importance of considering the spatial configuration of hunting refuges across the landscape in relation to human populations.

Opposing rainfall and plant nutritional gradients best explain the wildebeest migration in the Serengeti.

Multiple hypotheses have been proposed to explain the annual migration of the Serengeti wildebeest, but few studies have compared distribution patterns with environmental drivers. We used a rainfall-driven model of grass dynamics and wildebeest movement to generate simulated monthly wildebeest distributions, with wildebeest movement decisions depending on 14 candidate models of adaptive movement in response to resource availability. We used information-theoretic approaches to compare the fits of simulated and observed monthly distribution patterns at two spatial scales over a 3-year period. Models that included the intake rate and nitrogen (N) concentration of green grass and the suppressive effect of tree cover on grass biomass provided the best model fits at both spatial scales tested, suggesting that digestive constraints and protein requirements may play key roles in driving migratory behavior. The emergence of a migration was predicted to be dependent on the ability of the wildebeest to track changes in resource abundance at relatively large scales (>80-100 km). When movement decisions are based solely on local resource availability, the wildebeest fail to migrate across the ecosystem. Our study highlights the potentially key role of strong and countervailing seasonally driven rainfall and fertility gradients--a consistent feature of African savanna ecosystems--as drivers of long-distance seasonal migrations in ungulates.

Grazers, browsers, and fire influence the extent and spatial pattern of tree cover in the Serengeti.

Vertebrate herbivores and fire are known to be important drivers of vegetation dynamics in African savannas. It is of particular importance to understand how changes in herbivore population density, especially of elephants, and fire frequency will affect the amount of tree cover in savanna ecosystems, given the critical importance of tree cover for biodiversity, ecosystem function, and human welfare. We developed a spatially realistic simulation model of vegetation, fire, and dominant herbivore dynamics, tailored to the Serengeti ecosystem of east Africa. The model includes key processes such as tree-grass competition, fire, and resource-based density dependence and adaptive movement by herbivores. We used the model to project the ecosystem 100 years into the future from its present state under different fire, browsing (determined by elephant population density), and grazing (with and without wildebeest present) regimes. The model produced the following key results: (1) elephants and fire exert synergistic negative effects on woody cover; when grazers are excluded, the impact of fire and the strength of the elephant-fire interaction increase; (2) at present population densities of 0.15 elephants/km2, the total amount of woody cover is predicted to remain stable in the absence of fire, but the mature tree population is predicted to decline regardless of the fire regime; without grazers present to mitigate the effects of fire, the size structure of the tree population will become dominated by seedlings and mature trees; (3) spatial heterogeneity in tree cover varies unimodally with elephant population density; fire increases heterogeneity in the presence of grazers and decreases it in their absence; (4) the marked rainfall gradient in the Serengeti directly affects the pattern of tree cover in the absence of fire; with fire, the woody cover is determined by the grazing patterns of the migratory wildebeest, which are partly rainfall driven. Our results show that, in open migratory ecosystems such as the Serengeti, grazers can modulate the impact of fire and the strength of the interaction between fire and browsers by altering fuel loads and responding to the distribution of grass across the landscape, and thus exert strong effects on spatial patterns of tree cover.

Elephants, fire, and frost can determine community structure and composition in Kalahari Woodlands.

Fire, elephants, and frost are important disturbance factors in many African savannas, but the relative magnitude of their effects on vegetation and their interactions have not been quantified. Understanding how disturbance shapes savanna structure and composition is critical for predicting changes in tree cover and for formulating management and conservation policy. A simulation model was used to investigate how the disturbance regime determines vegetation structure and composition in a mixed Kalahari sand woodland savanna in western Zimbabwe. The model consisted of submodels for tree growth, tree damage caused by disturbance, mortality, and recruitment that were parameterized from field data collected over a two-year period. The model predicts that, under the current disturbance regime, tree basal area in the study area will decline by two-thirds over the next two decades and become dominated by species unpalatable to elephants. Changes in the disturbance regime are predicted to greatly modify vegetation structure and community composition. Elephants are the primary drivers of woodland change in this community at present-day population densities, and their impacts are exacerbated by the effects of fire and frost. Frost, in particular, does not play an important role when acting independently but appears to be a key secondary factor in the presence of elephants and/or fire. Unlike fire and frost, which cannot suppress the woodland phase on their own in this ecosystem, elephants can independently drive the vegetation to the scrub phase. The results suggest that elephant and fire management may be critical for the persistence of certain woodland communities within dry-season elephant habitats in the eastern Kalahari, particularly those dominated by Brachystegia spiciformis and other palatable species.

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.

Functional mismatch in a bumble bee pollination mutualism under climate change.

Ecological partnerships, or mutualisms, are globally widespread, sustaining agriculture and biodiversity. Mutualisms evolve through the matching of functional traits between partners, such as tongue length of pollinators and flower tube depth of plants. Long-tongued pollinators specialize on flowers with deep corolla tubes, whereas shorter-tongued pollinators generalize across tube lengths. Losses of functional guilds because of shifts in global climate may disrupt mutualisms and threaten partner species. We found that in two alpine bumble bee species, decreases in tongue length have evolved over 40 years. Co-occurring flowers have not become shallower, nor are small-flowered plants more prolific. We argue that declining floral resources because of warmer summers have favored generalist foraging, leading to a mismatch between shorter-tongued bees and the longer-tubed plants they once pollinated.

Revisiting the two-layer hypothesis: coexistence of alternative functional rooting strategies in savannas.

The two-layer hypothesis of tree-grass coexistence posits that trees and grasses differ in rooting depth, with grasses exploiting soil moisture in shallow layers while trees have exclusive access to deep water. The lack of clear differences in maximum rooting depth between these two functional groups, however, has caused this model to fall out of favor. The alternative model, the demographic bottleneck hypothesis, suggests that trees and grasses occupy overlapping rooting niches, and that stochastic events such as fires and droughts result in episodic tree mortality at various life stages, thus preventing trees from otherwise displacing grasses, at least in mesic savannas. Two potential problems with this view are: 1) we lack data on functional rooting profiles in trees and grasses, and these profiles are not necessarily reflected by differences in maximum or physical rooting depth, and 2) subtle, difficult-to-detect differences in rooting profiles between the two functional groups may be sufficient to result in coexistence in many situations. To tackle this question, I coupled a plant uptake model with a soil moisture dynamics model to explore the environmental conditions under which functional rooting profiles with equal rooting depth but different depth distributions (i.e., shapes) can coexist when competing for water. I show that, as long as rainfall inputs are stochastic, coexistence based on rooting differences is viable under a wide range of conditions, even when these differences are subtle. The results also indicate that coexistence mechanisms based on rooting niche differentiation are more viable under some climatic and edaphic conditions than others. This suggests that the two-layer model is both viable and stochastic in nature, and that a full understanding of tree-grass coexistence and dynamics may require incorporating fine-scale rooting differences between these functional groups and realistic stochastic climate drivers into future models.

Predicted impact of barriers to migration on the Serengeti wildebeest population.

The Serengeti wildebeest migration is a rare and spectacular example of a once-common biological phenomenon. A proposed road project threatens to bisect the Serengeti ecosystem and its integrity. The precautionary principle dictates that we consider the possible consequences of a road completely disrupting the migration. We used an existing spatially-explicit simulation model of wildebeest movement and population dynamics to explore how placing a barrier to migration across the proposed route (thus creating two disjoint but mobile subpopulations) might affect the long-term size of the wildebeest population. Our simulation results suggest that a barrier to migration--even without causing habitat loss--could cause the wildebeest population to decline by about a third. The driver of this decline is the effect of habitat fragmentation (even without habitat loss) on the ability of wildebeest to effectively track temporal shifts in high-quality forage resources across the landscape. Given the important role of the wildebeest migration for a number of key ecological processes, these findings have potentially important ramifications for ecosystem biodiversity, structure, and function in the Serengeti.