Blocking then stinging as a case of two-step evolution of defensive cage architectures in herbivore-driven ecosystems.

Dense branching and spines are common features of plant species in ecosystems with high mammalian herbivory pressure. While dense branching and spines can inhibit herbivory independently, when combined, they form a powerful defensive cage architecture. However, how cage architecture evolved under mammalian pressure has remained unexplored. Here we show how dense branching and spines emerged during the age of mammalian radiation in the Combretaceae family and diversified in herbivore-driven ecosystems in the tropics. Phylogenetic comparative methods revealed that modern plant architectural strategies defending against large mammals evolved via a stepwise process. First, dense branching emerged under intermediate herbivory pressure, followed by the acquisition of spines that supported higher speciation rates under high herbivory pressure. Our study highlights the adaptive value of dense branching as part of a herbivore defence strategy and identifies large mammal herbivory as a major selective force shaping the whole plant architecture of woody plants.

The bii4africa dataset of faunal and floral population intactness estimates across Africa's major land uses.

Sub-Saharan Africa is under-represented in global biodiversity datasets, particularly regarding the impact of land use on species' population abundances. Drawing on recent advances in expert elicitation to ensure data consistency, 200 experts were convened using a modified-Delphi process to estimate 'intactness scores': the remaining proportion of an 'intact' reference population of a species group in a particular land use, on a scale from 0 (no remaining individuals) to 1 (same abundance as the reference) and, in rare cases, to 2 (populations that thrive in human-modified landscapes). The resulting bii4africa dataset contains intactness scores representing terrestrial vertebrates (tetrapods: ±5,400 amphibians, reptiles, birds, mammals) and vascular plants (±45,000 forbs, graminoids, trees, shrubs) in sub-Saharan Africa across the region's major land uses (urban, cropland, rangeland, plantation, protected, etc.) and intensities (e.g., large-scale vs smallholder cropland). This dataset was co-produced as part of the Biodiversity Intactness Index for Africa Project. Additional uses include assessing ecosystem condition; rectifying geographic/taxonomic biases in global biodiversity indicators and maps; and informing the Red List of Ecosystems.

Grazing lawns and overgrazing in frequently grazed grass communities.

Frequent grazing can establish high forage value grazing lawns supporting high grazer densities, but can also produce overgrazed grass communities with unpalatable or low grass basal cover, supporting few grazers. Attempts to create grazing lawns via concentrated grazing, with a goal to increase grazer numbers, are thus risky without knowing how environmental conditions influence the likelihood of each outcome. We collected grass species and trait data from 33 frequently grazed grass communities across eastern South Africa (28 sites) and the Serengeti National Park, Tanzania (five sites), covering wide rainfall (336-987 mm year-1) and soil (e.g., 44%-93% sand) gradients. We identified four grass growth forms using hierarchical clustering on principal components analyses of trait data and assessed trait-environment and growth form-environment relationships using fourth corner and principal components analyses. We distinguished two palatable grass growth forms that both attract yet resist grazers and comprise grazing lawns: (1) "lateral attractors" that spread vegetatively via stolons and rhizomes, and (2) "tufted attractors" that form isolated tufts and may have alternate tall growth forms. By contrast, (3) tough, upright, tufted "resisters," and (4) "avoiders" with sparse architectures or that grow appressed to the soil surface, are of little forage value and avoided by grazers. Grazing lawns occurred across a wide range of conditions, typically comprising lateral attractor grasses in drier, sandy environments, and tufted attractor grasses in wetter, low-sand environments. Resisters occurred on clay-rich soils in mesic areas, while avoiders were widespread but scarce. While grazing lawns can be established under most conditions, monitoring their composition and cover is important, as the potential for overgrazing seems as widely relevant. Tufted attractor-dominated lawns appear somewhat more vulnerable to degradation than lateral attractor-dominated lawns. Increased avoider and resister abundance both reduce forage value, although resisters may provide better soil protection.

Seasonal strategies differ between tropical and extratropical herbivores.

Seasonal diet shifts and migration are key components of large herbivore population dynamics, but we lack a systematic understanding of how these behaviours are distributed on a macroecological scale. The prevalence of seasonal strategies is likely related to herbivore body size and feeding guild, and may also be influenced by properties of the environment, such as soil nutrient availability and climate seasonality. We evaluated the distribution of seasonal dietary shifts and migration across large-bodied mammalian herbivores and determined how these behaviours related to diet, body size and environment. We found that herbivore strategies were consistently correlated with their traits: seasonal diet shifts were most prevalent among mixed feeding herbivores and migration among grazers and larger herbivores. Seasonality also played a role, particularly for migration, which was more common at higher latitudes. Both dietary shifts and migration were more widespread among extratropical herbivores, which also exhibited more intermediate diets and body sizes. Our findings suggest that strong seasonality in extratropical systems imposes pressure on herbivores, necessitating widespread behavioural responses to navigate seasonal resource bottlenecks. It follows that tropical and extratropical herbivores may have divergent responses to global change, with intensifying herbivore pressure in extratropical systems contrasting with diminishing herbivore pressure in tropical systems.

Seasonal dietary changes increase the abundances of savanna herbivore species.

African savannas are home to the world's last great megafaunal communities, but despite ongoing population declines, we only poorly understand the constraints on savanna herbivore abundances. Seasonal diet shifts (except migration) have received little attention, despite a diversity of possible dietary strategies. Here, we first formulate two theoretical models that predict that both mixed feeding and migratory grazing increase population sizes. These predictions are borne out in comprehensive data across African savanna parks: Mixed feeders are the most abundant herbivores in Africa, alongside a few migratory grazer populations. Overall, clear mixed-feeder dominance may reflect a historical pattern or may instead mirror a general global decline in specialists. Regardless, mixed feeders dominate the savannas of the present and future.

Savanna tree evolutionary ages inform the reconstruction of the paleoenvironment of our hominin ancestors.

Ideas on hominin evolution have long invoked the emergence from forests into open habitats as generating selection for traits such as bipedalism and dietary shifts. Though controversial, the savanna hypothesis continues to motivate research into the palaeo-environments of Africa. Reconstruction of these ancient environments has depended heavily on carbon isotopic analysis of fossil bones and palaeosols. The sparsity of the fossil record, however, imposes a limit to the strength of inference that can be drawn from such data. Time-calibrated phylogenies offer an additional tool for dating the spread of savanna habitat. Here, using the evolutionary ages of African savanna trees, we suggest an initial tropical or subtropical expansion of savanna between 10 and 15 Ma, which then extended to higher latitudes, reaching southern Africa ca. 3 Ma. Our phylogenetic estimates of the origin and latitudinal spread of savannas broadly correspond with isotopic age estimates and encompass the entire hominin fossil record. Our results are consistent with the savanna hypothesis of early hominin evolution and reignite the debate on the drivers of savanna expansion. Our analysis demonstrates the utility of phylogenetic proxies for dating major ecological transitions in geological time, especially in regions where fossils are rare or absent or occur in discontinuous sediments.

Fire and grazing determined grasslands of central Madagascar represent ancient assemblages.

The ecology of Madagascar's grasslands is under-investigated and the dearth of ecological understanding of how disturbance by fire and grazing shapes these grasslands stems from a perception that disturbance shaped Malagasy grasslands only after human arrival. However, worldwide, fire and grazing shape tropical grasslands over ecological and evolutionary timescales, and it is curious Madagascar should be a global anomaly. We examined the functional and community ecology of Madagascar's grasslands across 71 communities in the Central Highlands. Combining multivariate abundance models of community composition and clustering of grass functional traits, we identified distinct grass assemblages each shaped by fire or grazing. The fire-maintained assemblage is primarily composed of tall caespitose species with narrow leaves and low bulk density. By contrast, the grazer-maintained assemblage is characterized by mat-forming, high bulk density grasses with wide leaves. Within each assemblage, levels of endemism, diversity and grass ages support these as ancient assemblages. Grazer-dependent grasses can only have co-evolved with a now-extinct megafauna. Ironically, the human introduction of cattle probably introduced a megafaunal substitute facilitating modern day persistence of a grazer-maintained grass assemblage in an otherwise defaunated landscape, where these landscapes now support the livelihoods of millions of people.

Large herbivore conservation in a changing world: Surface water provision and adaptability allow wildebeest to persist after collapse of long-range movements.

Large herbivores, particularly wide-ranging species, are extensively impacted by land use transformation and other anthropogenic barriers to movement. The adaptability of a species is, therefore, crucial to determining whether populations can persist in ever smaller subsets of their historical home ranges. Access to water, by drinking or from forage moisture, is an essential requirement, and surface water provision is thus a long-established, although controversial, conservation practice. In the arid Kgalagadi Transfrontier Park (KTP), South Africa, surface water provision in the 1930s facilitated the establishment of a sedentary wildebeest (Connochaetes taurinus) population in a region historically accessed only in the wet season, via now collapsed long-distance movements. Here, we investigate the behaviour and diet of this wildebeest population, and how these relate to water in the landscape, to better understand the process of transitioning from a mobile to sedentary population. Data from 26 monthly surveys reveal that wildebeest distributions are shaped by water availability and salinity, shade, forage, season and possibly predator detectability. Areas with saline or no water are used predominantly in the wet season when forage moisture is high. Wet season movements beyond the study area mean the timing of wildebeest grazing in these regions matches historical timing. Grass utilization field data suggest that the KTP grazer population experiences forage deficits during the dry season, when ~80% of grass tufts are grazed and C:N and crude protein levels decline. Nonetheless, dung isotope data show that wildebeest meet their crude protein intake requirements during the dry season, likely by consuming unprecedentedly high levels of browse (>33%). While restoring the full historical range and movements of most large herbivore populations is not possible, these findings highlight that understanding the behavioural and dietary adaptability of a species can augment 'next best' efforts to conserve viable populations while home ranges contract.

Drought-response strategies of savanna herbivores.

Climate models predict increases in drought frequency and severity worldwide, with potential impacts on diverse systems, including African savannas. These droughts pose a concern for the conservation of savanna mammal communities, such that understanding how different species respond to drought is vital.Because grass decreases so consistently during droughts, we predict that grass-dependent species (grazers and mixed feeders) will respond strongly to drought, whether by changing diets, seeking drought refugia, or suffering mortality.A recent severe but heterogeneous drought in Kruger National Park, South Africa, afforded a rare opportunity to test these hypotheses in situ-crucial, given the central role of landscape-scale movement as a potential herbivore strategy. We used herbivore dung as a proxy, integrating spatial distributions (dung counts) with diet composition (carbon isotope analysis of dung).As predicted, browsers showed little response to drought. However, mixed feeders switched their diets to incorporate more C3 trees/forbs, but did not move. Meanwhile, grazers and megaherbivores instead moved toward drought refugia. Synthesis and applications: The responses we observed by savanna herbivores are largely amplifications of typical dry season strategies and reflect constraints imposed by body size and feeding ecology. Grazers may be at particular risk from increased drought frequency and spatial extent if drought refugia become decreasingly available. Conservation strategies should recognize these constraints and work to facilitate the diverse responses of herbivores to drought.

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.

A unified framework for plant life-history strategies shaped by fire and herbivory.

Fire and herbivory both remove aboveground biomass. Environmental factors determine the type and intensity of these consumers globally, but the traits of plants can also alter their propensity to burn and the degree to which they are eaten. To understand plant life-history strategies associated with fire and herbivory we need to describe both response and effect functional traits, and how they sort within communities, along resource gradients, and across evolutionary timescales. Fire and herbivore functional traits are generally considered separately, but there are advances made in understanding fire that relate to herbivory, and vice versa. Moreover, fire and herbivory interact: the presence of one consumer affects the type and intensity of the other. Here, we present a unifying conceptual framework to understand plant strategies that enable tolerance and persistence to fire and herbivory. Using grasses as an example, we discuss how flammability and fire tolerance, palatability, and grazing tolerance traits might organize themselves in ecosystems exposed to these consumers, and how these traits might have evolved with reference to other strong selective processes, like aridity. Our framework can be used to predict both the diversity of life-history strategies and plant species diversity under different consumer regimes.

Alternate Grassy Ecosystem States Are Determined by Palatability-Flammability Trade-Offs.

Fire and mammalian grazers both consume grasses, and feedbacks between grass species, their functional traits, and consumers have profound effects on grassy ecosystem structure worldwide, such that savanna and grassland states determined by fire or grazing can be considered alternate states. These parallel savanna-forest alternate states, which likewise have myriad cascading ecosystem impacts.

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.

The consequences of replacing wildlife with livestock in Africa.

The extirpation of native wildlife species and widespread establishment of livestock farming has dramatically distorted large mammal herbivore communities across the globe. Ecological theory suggests that these shifts in the form and the intensity of herbivory have had substantial impacts on a range of ecosystem processes, but for most ecosystems it is impossible to quantify these changes accurately. We address these challenges using species-level biomass data from sub-Saharan Africa for both present day and reconstructed historical herbivore communities. Our analyses reveal pronounced herbivore biomass losses in wetter areas and substantial biomass increases and functional type turnover in arid regions. Fire prevalence is likely to have been altered over vast areas where grazer biomass has transitioned to above or below the threshold at which grass fuel reduction can suppress fire. Overall, shifts in the functional composition of herbivore communities promote an expansion of woody cover. Total herbivore methane emissions have more than doubled, but lateral nutrient diffusion capacity is below 5% of past levels. The release of fundamental ecological constraints on herbivore communities in arid regions appears to pose greater threats to ecosystem function than do biomass losses in mesic regions, where fire remains the major consumer.

Spiny plants, mammal browsers, and the origin of African savannas.

Savannas first began to spread across Africa during the Miocene. A major hypothesis for explaining this vegetation change is the increase in C4 grasses, promoting fire. We investigated whether mammals could also have contributed to savanna expansion by using spinescence as a marker of mammal herbivory. Looking at the present distribution of 1,852 tree species, we established that spinescence is mainly associated with two functional types of mammals: large browsers and medium-sized mixed feeders. Using a dated phylogeny for the same tree species, we found that spinescence evolved at least 55 times. The diversification of spiny plants occurred long after the evolution of Afrotherian proboscideans and hyracoids. However, it is remarkably congruent with diversification of bovids, the lineage including the antelope that predominantly browse these plants today. Our findings suggest that herbivore-adapted savannas evolved several million years before fire-maintained savannas and probably, in different environmental conditions. Spiny savannas with abundant mammal herbivores occur in drier climates and on nutrient-rich soils, whereas fire-maintained savannas occur in wetter climates on nutrient-poor soils.

Competing consumers: contrasting the patterns and impacts of fire and mammalian herbivory in Africa.

Fire and herbivory are the two consumers of above-ground biomass globally. They have contrasting impacts as they differ in terms of selectivity and temporal occurrence. Here, we integrate continental-scale data on fire and herbivory in Africa to explore (i) how environmental drivers constrain these two consumers and (ii) the degree to which each consumer affects the other. Environments conducive to mammalian herbivory are not necessarily the same as those conducive to fire, although their spheres of influence do overlap-especially in grassy ecosystems which are known for their frequent fires and abundance of large mammalian herbivores. Interactions between fire and herbivory can be competitive, facultative or antagonistic, and we explore this with reference to the potential for alternative ecosystem states. Although fire removes orders of magnitude more biomass than herbivory their methane emissions are very similar, and in the past, herbivores probably emitted more methane than fire. We contrast the type of herbivory and fire in different ecosystems to define 'consumer-realms'.This article is part of the themed issue 'Tropical grassy biomes: linking ecology, human use and conservation'.

A continent-wide assessment of the form and intensity of large mammal herbivory in Africa.

Megafaunal extinctions and a lack of suitable remote sensing technology impede our understanding of both the ecological legacy and current impacts of large mammal herbivores in the Earth system. To address this, we reconstructed the form and intensity of herbivory pressure across sub-Saharan Africa ~1000 years ago. Specifically, we modeled and mapped species-level biomass for 92 large mammal herbivores using census data, species distributions, and environmental covariates. Trait-based classifications of these species into herbivore functional types, and analyses of their biomass surfaces, reveal four ecologically distinct continental-scale herbivory regimes, characterized by internally similar forms and intensities of herbivory pressure. Associations between herbivory regimes, fire prevalence, soil nutrient status, and rainfall provide important insights into African ecology and pave the way for integrating herbivores into global-scale studies.

Ecology of grazing lawns in Africa.

Grazing lawns are a distinct grassland community type, characterised by short-stature and with their persistence and spread promoted by grazing. In Africa, they reveal a long co-evolutionary history of grasses and large mammal grazers. The attractiveness to grazers of a low-biomass sward lies in the relatively high quality of forage, largely due to the low proportion of stem material in the sward; this encourages repeat grazing that concomitantly suppresses tall-grass growth forms that would otherwise outcompete lawn species for light. Regular grazing that prevents shading and maintains sward quality is thus the cornerstone of grazing lawn dynamics. The strong interplay between abiotic conditions and disturbance factors, which are central to grazing lawn existence, can also cause these systems to be highly dynamic. Here we identify differences in growth form among grazing lawn grass species, and assess how compositional differences among lawn types, as well as environmental variables, influence their maintenance requirements (i.e. grazing frequency) and vulnerability to degradation. We also make a clear distinction between the processes of lawn establishment and lawn maintenance. Rainfall, soil nutrient status, grazer community composition and fire regime have strong and interactive influences on both processes. However, factors that concentrate grazing pressure (e.g. nutrient hotspots and sodic sites) have more bearing on where lawns establish. Similarly, we discuss the relevance of enhanced rates of nitrogen cycling and of sodium levels to lawn maintenance. Grazer community composition and density has considerable significance to grazing lawn dynamics; not all grazers are adapted to foraging on short-grass swards, and differences in body size and relative mouth dimensions determine which species are able to convert tall-grass swards into grazing lawns under different conditions. Hence, we evaluate the roles of different grazers in lawn dynamics, as well as the benefits that grazer populations derive from having access to grazing lawns. The effects of grazing lawns can extend well beyond their borders, due to their influence on grazer densities, behaviour and movements as well as fire spread, intensity and frequency. Variation in the area and proportion of a landscape that is grazing lawn can thus have a profound impact on system dynamics. We provide a conceptual model that summarises grazing lawn dynamics, and identify a rainfall range where we predict grazing lawns to be most prevalent. We also examine the biodiversity associated with grazing lawn systems, and consider their functional contribution to the conservation of this biodiversity. Finally, we assess the utility of grazing lawns as a resource in a rangeland context.