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.

Grazing herbivores reduce herbaceous biomass and fire activity across African savannas.

Fire and herbivory interact to alter ecosystems and carbon cycling. In savannas, herbivores can reduce fire activity by removing grass biomass, but the size of these effects and what regulates them remain uncertain. To examine grazing effects on fuels and fire regimes across African savannas, we combined data from herbivore exclosure experiments with remotely sensed data on fire activity and herbivore density. We show that, broadly across African savannas, grazing herbivores substantially reduce both herbaceous biomass and fire activity. The size of these effects was strongly associated with grazing herbivore densities, and surprisingly, was mostly consistent across different environments. A one-zebra increase in herbivore biomass density (~100 kg/km2 of metabolic biomass) resulted in a ~53 kg/ha reduction in standing herbaceous biomass and a ~0.43 percentage point reduction in burned area. Our results indicate that fire models can be improved by incorporating grazing effects on grass biomass.

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.

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.

Herbivores and nutrients control grassland plant diversity via light limitation.

Human alterations to nutrient cycles and herbivore communities are affecting global biodiversity dramatically. Ecological theory predicts these changes should be strongly counteractive: nutrient addition drives plant species loss through intensified competition for light, whereas herbivores prevent competitive exclusion by increasing ground-level light, particularly in productive systems. Here we use experimental data spanning a globally relevant range of conditions to test the hypothesis that herbaceous plant species losses caused by eutrophication may be offset by increased light availability due to herbivory. This experiment, replicated in 40 grasslands on 6 continents, demonstrates that nutrients and herbivores can serve as counteracting forces to control local plant diversity through light limitation, independent of site productivity, soil nitrogen, herbivore type and climate. Nutrient addition consistently reduced local diversity through light limitation, and herbivory rescued diversity at sites where it alleviated light limitation. Thus, species loss from anthropogenic eutrophication can be ameliorated in grasslands where herbivory increases ground-level light.

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.

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.

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.

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.

The effect of fire on habitat selection of mammalian herbivores: the role of body size and vegetation characteristics.

Given the role of fire in shaping ecosystems, especially grasslands and savannas, it is important to understand its broader impact on these systems. Post-fire stimulation of plant nutrients is thought to benefit grazing mammals and explain their preference for burned areas. However, fire also reduces vegetation height and increases visibility, thereby potentially reducing predation risk. Consequently, fire may be more beneficial to smaller herbivores, with higher nutritional needs and greater risks of predation. We tested the impacts of burning on different sized herbivores' habitat preference in Serengeti National Park, as mediated by burning's effects on vegetation height, live : dead biomass ratio and leaf nutrients. Burning caused a less than 4 month increase in leaf nitrogen (N), and leaf non-N nutrients [copper (Cu), potassium (K), and magnesium (Mg)] and a decrease in vegetation height and live : dead biomass. During this period, total herbivore counts were higher on burned areas. Generally, smaller herbivores preferred burned areas more strongly than larger herbivores. Unfortunately, it was not possible to determine the vegetation characteristics that explained burned area preference for each of the herbivore species observed. However, total herbivore abundance and impala (Aepyceros melampus) preference for burned areas was due to the increases in non-N nutrients caused by burning. These findings suggest that burned area attractiveness to herbivores is mainly driven by changes to forage quality and not potential decreases in predation risk caused by reductions in vegetation height.

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.

Predicting invasion in grassland ecosystems: is exotic dominance the real embarrassment of richness?

Invasions have increased the size of regional species pools, but are typically assumed to reduce native diversity. However, global-scale tests of this assumption have been elusive because of the focus on exotic species richness, rather than relative abundance. This is problematic because low invader richness can indicate invasion resistance by the native community or, alternatively, dominance by a single exotic species. Here, we used a globally replicated study to quantify relationships between exotic richness and abundance in grass-dominated ecosystems in 13 countries on six continents, ranging from salt marshes to alpine tundra. We tested effects of human land use, native community diversity, herbivore pressure, and nutrient limitation on exotic plant dominance. Despite its widespread use, exotic richness was a poor proxy for exotic dominance at low exotic richness, because sites that contained few exotic species ranged from relatively pristine (low exotic richness and cover) to almost completely exotic-dominated ones (low exotic richness but high exotic cover). Both exotic cover and richness were predicted by native plant diversity (native grass richness) and land use (distance to cultivation). Although climate was important for predicting both exotic cover and richness, climatic factors predicting cover (precipitation variability) differed from those predicting richness (maximum temperature and mean temperature in the wettest quarter). Herbivory and nutrient limitation did not predict exotic richness or cover. Exotic dominance was greatest in areas with low native grass richness at the site- or regional-scale. Although this could reflect native grass displacement, a lack of biotic resistance is a more likely explanation, given that grasses comprise the most aggressive invaders. These findings underscore the need to move beyond richness as a surrogate for the extent of invasion, because this metric confounds monodominance with invasion resistance. Monitoring species' relative abundance will more rapidly advance our understanding of invasions.

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.

Spatial guilds in the Serengeti food web revealed by a Bayesian group model.

Food webs, networks of feeding relationships in an ecosystem, provide fundamental insights into mechanisms that determine ecosystem stability and persistence. A standard approach in food-web analysis, and network analysis in general, has been to identify compartments, or modules, defined by many links within compartments and few links between them. This approach can identify large habitat boundaries in the network but may fail to identify other important structures. Empirical analyses of food webs have been further limited by low-resolution data for primary producers. In this paper, we present a Bayesian computational method for identifying group structure using a flexible definition that can describe both functional trophic roles and standard compartments. We apply this method to a newly compiled plant-mammal food web from the Serengeti ecosystem that includes high taxonomic resolution at the plant level, allowing a simultaneous examination of the signature of both habitat and trophic roles in network structure. We find that groups at the plant level reflect habitat structure, coupled at higher trophic levels by groups of herbivores, which are in turn coupled by carnivore groups. Thus the group structure of the Serengeti web represents a mixture of trophic guild structure and spatial pattern, in contrast to the standard compartments typically identified. The network topology supports recent ideas on spatial coupling and energy channels in ecosystems that have been proposed as important for persistence. Furthermore, our Bayesian approach provides a powerful, flexible framework for the study of network structure, and we believe it will prove instrumental in a variety of biological contexts.

Body size and the division of niche space: food and predation differentially shape the distribution of Serengeti grazers.

1. Theory predicts that small grazers are regulated by the digestive quality of grass, while large grazers extract sufficient nutrients from low-quality forage and are regulated by its abundance instead. In addition, predation potentially affects populations of small grazers more than large grazers, because predators have difficulty capturing and handling large prey. 2. We analyse the spatial distribution of five grazer species of different body size in relation to gradients of food availability and predation risk. Specifically, we investigate how the quality of grass, the abundance of grass biomass and the associated risks of predation affect the habitat use of small, intermediate and large savanna grazers at a landscape level. 3. Resource selection functions of five mammalian grazer species surveyed over a 21-year period in Serengeti are calculated using logistic regressions. Variables included in the analyses are grass nitrogen, rainfall, topographic wetness index, woody cover, drainage lines, landscape curvature, water and human habitation. Structural equation modelling (SEM) is used to aggregate predictor variables into 'composites' representing food quality, food abundance and predation risk. Subsequently, SEM is used to investigate species' habitat use, defined as their recurrence in 5 × 5 km cells across repeated censuses. 4. The distribution of small grazers is constrained by predation and food quality, whereas the distribution of large grazers is relatively unconstrained. The distribution of the largest grazer (African buffalo) is primarily associated with forage abundance but not predation risk, while the distributions of the smallest grazers (Thomson's gazelle and Grant's gazelle) are associated with high grass quality and negatively with the risk of predation. The distributions of intermediate sized grazers (Coke's hartebeest and topi) suggest they optimize access to grass biomass of sufficient quality in relatively predator-safe areas. 5. The results illustrate how top-down (vegetation-mediated predation risk) and bottom-up factors (biomass and nutrient content of vegetation) predictably contribute to the division of niche space for herbivores that vary in body size. Furthermore, diverse grazing assemblages are composed of herbivores of many body sizes (rather than similar body sizes), because these herbivores best exploit the resources of different habitat types.

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.

Landscape-scale analyses suggest both nutrient and antipredator advantages to Serengeti herbivore hotspots.

Mechanistic explanations of herbivore spatial distribution have focused largely on either resource-related (bottom-up) or predation-related (top-down) factors. We studied direct and indirect influences on the spatial distributions of Serengeti herbivore hotspots, defined as temporally stable areas inhabited by mixed herds of resident grazers. Remote sensing and variation in landscape features were first used to create a map of the spatial distribution of hotspots, which was tested for accuracy against an independent data set of herbivore observations. Subsequently, we applied structural equation modeling to data on soil fertility and plant quality and quantity across a range of sites. We found that hotspots in Serengeti occur in areas that are relatively flat and located away from rivers, sites where ungulates are less susceptible to predation. Further, hotspots tend to occur in areas where hydrology and rainfall create conditions of relatively low-standing plant biomass, which, coupled with grazing, increases forage quality while decreasing predation risk. Low-standing biomass and higher leaf concentrations of N, Na, and Mg were strong direct predictors of hotspot occurrence. Soil fertility had indirect effects on hotspot occurrence by promoting leaf Na and Mg. The results indicate that landscape features contribute in direct and indirect ways to influence the spatial distribution of hotspots and that the best models incorporated both resource- and predation-related factors. Our study highlights the collective and simultaneous role of bottom-up and top-down factors in determining ungulate spatial distributions.