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.

Camera Trap Methods and Drone Thermal Surveillance Provide Reliable, Comparable Density Estimates of Large, Free-Ranging Ungulates.

Camera traps and drone surveys both leverage advancing technologies to study dynamic wildlife populations with little disturbance. Both techniques entail strengths and weaknesses, and common camera trap methods can be confounded by unrealistic assumptions and prerequisite conditions. We compared three methods to estimate the population density of white-tailed deer (Odocoileus virgnianus) in a section of Pilot Mountain State Park, NC, USA: (1) camera trapping using mark-resight ratios or (2) N-mixture modeling and (3) aerial thermal videography from a drone platform. All three methods yielded similar density estimates, suggesting that they converged on an accurate estimate. We also included environmental covariates in the N-mixture modeling to explore spatial habitat use, and we fit models for each season to understand temporal changes in population density. Deer occurred in greater densities on warmer, south-facing slopes in the autumn and winter and on cooler north-facing slopes and in areas with flatter terrain in the summer. Seasonal density estimates over two years suggested an annual cycle of higher densities in autumn and winter than in summer, indicating that the region may function as a refuge during the hunting season.

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.

The generality of cryptic dietary niche differences in diverse large-herbivore assemblages.

Ecological niche differences are necessary for stable species coexistence but are often difficult to discern. Models of dietary niche differentiation in large mammalian herbivores invoke the quality, quantity, and spatiotemporal distribution of plant tissues and growth forms but are agnostic toward food plant species identity. Empirical support for these models is variable, suggesting that additional mechanisms of resource partitioning may be important in sustaining large-herbivore diversity in African savannas. We used DNA metabarcoding to conduct a taxonomically explicit analysis of large-herbivore diets across southeastern Africa, analyzing ∼4,000 fecal samples of 30 species from 10 sites in seven countries over 6 y. We detected 893 food plant taxa from 124 families, but just two families-grasses and legumes-accounted for the majority of herbivore diets. Nonetheless, herbivore species almost invariably partitioned food plant taxa; diet composition differed significantly in 97% of pairwise comparisons between sympatric species, and dissimilarity was pronounced even between the strictest grazers (grass eaters), strictest browsers (nongrass eaters), and closest relatives at each site. Niche differentiation was weakest in an ecosystem recovering from catastrophic defaunation, indicating that food plant partitioning is driven by species interactions, and was stronger at low rainfall, as expected if interspecific competition is a predominant driver. Diets differed more between browsers than grazers, which predictably shaped community organization: Grazer-dominated trophic networks had higher nestedness and lower modularity. That dietary differentiation is structured along taxonomic lines complements prior work on how herbivores partition plant parts and patches and suggests that common mechanisms govern herbivore coexistence and community assembly in savannas.

First-year Acacia seedlings are anisohydric "water-spenders" but differ in their rates of water use.

PREMISE: First-year seedlings (FYS) of tree species may be a critical demographic bottleneck in semi-arid, seasonally dry ecosystems such as savannas. Given the highly variable water availability and potentially strong FYS-grass competition for water, FYS water-use strategies may play a crucial role in FYS establishment in savannas and, ultimately, in tree-grass competition and coexistence. METHODS: We examined drought responses in FYS of two tree species that are dominant on opposite ends of an aridity gradient in Serengeti, Acacia (=Vachellia) tortilis and A. robusta. In a glasshouse experiment, gas exchange and whole-plant hydraulic conductance (Kplant ) were measured as soil water potential (Ψsoil ) declined. Trajectory of the Ψleaf /Ψsoil relationship during drought elucidated the degree of iso/anisohydry. RESULTS: Both species were strongly anisohydric "water-spenders," allowing rapid wet-season C gain after pulses of moisture availability. Despite being equally vulnerable to declines in Kplant under severe drought, they differed in their rates of water use. Acacia tortilis, which occurs in the more arid regions, initially had greater Kmax , transpiration (E), and photosynthesis (Anet ) than A. robusta. CONCLUSIONS: This work demonstrates an important mechanism of FYS establishment in savannas: Rather than investing in drought tolerance, savanna FYS maximize gas exchange during wet periods at the expense of desiccation during dry seasons. FYS establishment appears dependent on high C uptake during the pulses of water availability that characterize habitats dominated by these species. This study increases our understanding of species-scale plant ecophysiology and ecosystem-scale patterns of tree-grass coexistence.

Fire, grazers, and browsers interact with grass competition to determine tree establishment in an African savanna.

In savanna ecosystems, fire and herbivory alter the competitive relationship between trees and grasses. Mechanistically, grazing herbivores favor trees by removing grass, which reduces tree-grass competition and limits fire. Conversely, browsing herbivores consume trees and limit their recovery from fire. Herbivore feeding decisions are in turn shaped by risk-resource trade-offs that potentially determine the spatial patterns of herbivory. Identifying the dominant mechanistic pathways by which fire and herbivores control tree cover remains challenging, but is essential for understanding savanna dynamics. We used an experiment in the Serengeti ecosystem and a simple simulation driven by experimental results to address two main aims: (1) determine the importance of direct and indirect effects of grass, fire, and herbivory on seedling establishment and (2) establish whether predators determine the spatial pattern of successful seedling establishment via effects on mesoherbivore distribution. We transplanted tree seedlings into plots with a factorial combination of grass and herbivores (present/absent) across a lion-kill-risk gradient in the Serengeti, burning half of the plots near the end of the experiment. Ungrazed grass limited tree seedling survival directly via competition, indirectly via fire, and by slowing seedling growth, which drove higher seedling mortality during fires. These effects restricted seedling establishment to below 18% and, in conjunction with browsing, resulted in seedling establishment dropping below 5%. In the absence of browsing and fire, grazing drove a 7.5-fold increase in seedling establishment. Lion predation risk had no observable impact on herbivore effects on seedling establishment. The severe negative effects of grass on seedling mortality suggests that regional patterns of tree cover and fire may overestimate the role of fire in limiting tree cover, with regular fires representing a proxy for the competitive effects of grass.

Mixed-species groups of Serengeti grazers: a test of the stress gradient hypothesis.

Understanding the role of species interactions within communities is a central focus of ecology. A key challenge is to understand variation in species interactions along environmental gradients. The stress gradient hypothesis posits that positive interactions increase and competitive interactions decrease with increasing consumer pressure or environmental stress. This hypothesis has received extensive attention in plant community ecology, but only a handful of tests in animals. Furthermore, few empirical studies have examined multiple co-occurring stressors. Here we test predictions of the stress gradient hypothesis using the occurrence of mixed-species groups in six common grazing ungulate species within the Serengeti-Mara ecosystem. We use mixed-species groups as a proxy for potential positive interactions because they may enhance protection from predators or increase access to high-quality forage. Alternatively, competition for resources may limit the formation of mixed-species groups. Using more than 115,000 camera trap observations collected over 5 yr, we found that mixed-species groups were more likely to occur in risky areas (i.e., areas closer to lion vantage points and in woodland habitat where lions hunt preferentially) and during time periods when resource levels were high. These results are consistent with the interpretation that stress from high predation risk may contribute to the formation of mixed-species groups, but that competition for resources may prevent their formation when food availability is low. Our results are consistent with support for the stress gradient hypothesis in animals along a consumer pressure gradient while identifying the potential influence of a co-occurring stressor, thus providing a link between research in plant community ecology on the stress gradient hypothesis, and research in animal ecology on trade-offs between foraging and risk in landscapes of fear.

Soil nutrients and precipitation are major drivers of global patterns of grass leaf silicification.

Grasses accumulate high concentrations of silicon (Si) in their tissues, with potential benefits including herbivore defense, improved water balance, and reduced leaf construction costs. Although Si is one of the most widely varying leaf constituents among individuals, species, and ecosystems, the environmental forces driving this variation remain elusive and understudied. To understand relationships between environmental factors and grass Si accumulation better, we analyzed foliar chemistry of grasses from 17 globally distributed sites where nutrient inputs and grazing were manipulated. These sites span natural gradients in temperature, precipitation, and underlying soil properties, which allowed us to assess the relative importance of soil moisture and nutrients across variation in climate. Foliar Si concentration did not respond to large mammalian grazer exclusion, but significant variation in herbivore abundance among sites may have precluded the observation of defoliation effects at these sites. However, nutrient addition consistently reduced leaf Si, especially at sites with low soil nitrogen prior to nutrient addition. Additionally, a leaf-level trade-off between Si and carbon (C) existed that was stronger at arid sites than mesic sites. Our results suggest soil nutrient limitation favors investment in Si over C-based leaf construction, and that fixing C is especially costly relative to assimilating Si when water is limiting. Our results demonstrate the importance of soil nutrients and precipitation as key drivers of global grass silicification patterns.

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.

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.

Change in dominance determines herbivore effects on plant biodiversity.

Herbivores alter plant biodiversity (species richness) in many of the world's ecosystems, but the magnitude and the direction of herbivore effects on biodiversity vary widely within and among ecosystems. One current theory predicts that herbivores enhance plant biodiversity at high productivity but have the opposite effect at low productivity. Yet, empirical support for the importance of site productivity as a mediator of these herbivore impacts is equivocal. Here, we synthesize data from 252 large-herbivore exclusion studies, spanning a 20-fold range in site productivity, to test an alternative hypothesis-that herbivore-induced changes in the competitive environment determine the response of plant biodiversity to herbivory irrespective of productivity. Under this hypothesis, when herbivores reduce the abundance (biomass, cover) of dominant species (for example, because the dominant plant is palatable), additional resources become available to support new species, thereby increasing biodiversity. By contrast, if herbivores promote high dominance by increasing the abundance of herbivory-resistant, unpalatable species, then resource availability for other species decreases reducing biodiversity. We show that herbivore-induced change in dominance, independent of site productivity or precipitation (a proxy for productivity), is the best predictor of herbivore effects on biodiversity in grassland and savannah sites. Given that most herbaceous ecosystems are dominated by one or a few species, altering the competitive environment via herbivores or by other means may be an effective strategy for conserving biodiversity in grasslands and savannahs globally.

Identifying drivers of spatial variation in occupancy with limited replication camera trap data.

Occupancy models are widely used in camera trap studies to analyze species presence, abundance, and geographic distribution, among other important ecological quantities. These models account for imperfect detection using a latent variable to distinguish between true presence/absence and observed detection of a species. Under certain experimental setups, parameter estimation in a latent variable framework can be challenging. Several studies have issued guidelines on the number of independent replicated observations (surveys) needed for each unchanging occupancy field (season) to ensure reliable estimation. In this paper, we present a spatio-temporal occupancy model, and show through a simulation study that it can be fit to data obtained from a single survey per season, so long as the number of seasons is sufficiently large. We include an application using camera-trap data on the Thomson's gazelle in the Serengeti in Tanzania.

Herbivory and eutrophication mediate grassland plant nutrient responses across a global climatic gradient.

Plant stoichiometry, the relative concentration of elements, is a key regulator of ecosystem functioning and is also being altered by human activities. In this paper we sought to understand the global drivers of plant stoichiometry and compare the relative contribution of climatic vs. anthropogenic effects. We addressed this goal by measuring plant elemental (C, N, P and K) responses to eutrophication and vertebrate herbivore exclusion at eighteen sites on six continents. Across sites, climate and atmospheric N deposition emerged as strong predictors of plot-level tissue nutrients, mediated by biomass and plant chemistry. Within sites, fertilization increased total plant nutrient pools, but results were contingent on soil fertility and the proportion of grass biomass relative to other functional types. Total plant nutrient pools diverged strongly in response to herbivore exclusion when fertilized; responses were largest in ungrazed plots at low rainfall, whereas herbivore grazing dampened the plant community nutrient responses to fertilization. Our study highlights (1) the importance of climate in determining plant nutrient concentrations mediated through effects on plant biomass, (2) that eutrophication affects grassland nutrient pools via both soil and atmospheric pathways and (3) that interactions among soils, herbivores and eutrophication drive plant nutrient responses at small scales, especially at water-limited sites.

Pyrodiversity interacts with rainfall to increase bird and mammal richness in African savannas.

Fire is a fundamental process in savannas and is widely used for management. Pyrodiversity, variation in local fire characteristics, has been proposed as a driver of biodiversity although empirical evidence is equivocal. Using a new measure of pyrodiversity (Hempson et al.), we undertook the first continent-wide assessment of how pyrodiversity affects biodiversity in protected areas across African savannas. The influence of pyrodiversity on bird and mammal species richness varied with rainfall: strongest support for a positive effect occurred in wet savannas (> 650 mm/year), where species richness increased by 27% for mammals and 40% for birds in the most pyrodiverse regions. Range-restricted birds were most increased by pyrodiversity, suggesting the diversity of fire regimes increases the availability of rare niches. Our findings are significant because they explain the conflicting results found in previous studies of savannas. We argue that managing savanna landscapes to increase pyrodiversity is especially important in wet savannas.

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 spatial distribution of African savannah herbivores: species associations and habitat occupancy in a landscape context.

Herbivores play an important role in determining the structure and function of tropical savannahs. Here, we (i) outline a framework for how interactions among large mammalian herbivores, carnivores and environmental variation influence herbivore habitat occupancy in tropical savannahs. We then (ii) use a Bayesian hierarchical model to analyse camera trap data to quantify spatial patterns of habitat occupancy for lions and eight common ungulates of varying body size across an approximately 1100 km(2) landscape in the Serengeti ecosystem. Our results reveal strong positive associations among herbivores at the scale of the entire landscape. Lions were positively associated with migratory ungulates but negatively associated with residents. Herbivore habitat occupancy differed with body size and migratory strategy: large-bodied migrants, at less risk of predation and able to tolerate lower quality food, were associated with high NDVI, while smaller residents, constrained to higher quality forage, avoided these areas. Small herbivores were strongly associated with fires, likely due to the subsequent high-quality regrowth, while larger herbivores avoided burned areas. Body mass was strongly related to herbivore habitat use, with larger species more strongly associated with riverine and woodlands than smaller species. Large-bodied migrants displayed diffuse habitat occupancy, whereas smaller species demonstrated fine-scale occupancy reflecting use of smaller patches of high-quality habitat. Our results demonstrate the emergence of strong positive spatial associations among a diverse group of savannah herbivores, while highlighting species-specific habitat selection strongly determined by herbivore body size.This article is part of the themed issue 'Tropical grassy biomes: linking ecology, human use and conservation'.

Leaf thickness controls variation in leaf mass per area (LMA) among grazing-adapted grasses in Serengeti.

Leaf mass per area (LMA) is a primary plant functional trait that represents the cost of constructing a leaf. Ultimately, plants modify LMA by altering leaf thickness (LT), leaf dry matter content (LDMC), or both. While LMA can be modified through both of these constituents, studies of LMA have found that there is variation in whether LT or LDMC changes are responsible for LMA-and the relationships change depending on the species or functional groups being compared. In this study, we used a phylogenetic framework to determine that evolutionary shifts in LMA are driven by LT, and not LDMC, among 45 Serengeti grass species. We considered two alternative hypotheses that could result in evolutionary correlation of LMA on LT but not LDMC: either (1) LT is more labile than LDMC-and is therefore a less costly means to change LMA or (2) LDMC is tightly coupled to a different dimension of leaf variation (e.g., leaf hydraulics), leaving LT as the source of variation in LMA. LT was not more labile than LDMC, leading us to conclude that the evolution of LMA has been shaped by LT because LDMC is responding to other demands on leaf physiology. We speculate that leaf hydraulics provide this constraint on LDMC. The decoupling of LDMC from LT may allow plants to better optimize resource allocation in ecosystems where gradients in light competition, herbivory, and aridity place competing demands on leaf economics.

Comment on "Worldwide evidence of a unimodal relationship between productivity and plant species richness".

Fraser et al. (Reports, 17 July 2015, p. 302) report a unimodal relationship between productivity and species richness at regional and global scales, which they contrast with the results of Adler et al. (Reports, 23 September 2011, p. 1750). However, both data sets, when analyzed correctly, show clearly and consistently that productivity is a poor predictor of local species richness.

Integrative modelling reveals mechanisms linking productivity and plant species richness.

How ecosystem productivity and species richness are interrelated is one of the most debated subjects in the history of ecology. Decades of intensive study have yet to discern the actual mechanisms behind observed global patterns. Here, by integrating the predictions from multiple theories into a single model and using data from 1,126 grassland plots spanning five continents, we detect the clear signals of numerous underlying mechanisms linking productivity and richness. We find that an integrative model has substantially higher explanatory power than traditional bivariate analyses. In addition, the specific results unveil several surprising findings that conflict with classical models. These include the isolation of a strong and consistent enhancement of productivity by richness, an effect in striking contrast with superficial data patterns. Also revealed is a consistent importance of competition across the full range of productivity values, in direct conflict with some (but not all) proposed models. The promotion of local richness by macroecological gradients in climatic favourability, generally seen as a competing hypothesis, is also found to be important in our analysis. The results demonstrate that an integrative modelling approach leads to a major advance in our ability to discern the underlying processes operating in ecological systems.