Determinants of microbiome composition: Insights from free-ranging hybrid zebras (Equus quagga × grevyi).

The composition of mammalian gut microbiomes is highly conserved within species, yet the mechanisms by which microbiome composition is transmitted and maintained within lineages of wild animals remain unclear. Mutually compatible hypotheses exist, including that microbiome fidelity results from inherited dietary habits, shared environmental exposure, morphophysiological filtering and/or maternal effects. Interspecific hybrids are a promising system in which to interrogate the determinants of microbiome composition because hybrids can decouple traits and processes that are otherwise co-inherited in their parent species. We used a population of free-living hybrid zebras (Equus quagga × grevyi) in Kenya to evaluate the roles of these four mechanisms in regulating microbiome composition. We analysed faecal DNA for both the trnL-P6 and the 16S rRNA V4 region to characterize the diets and microbiomes of the hybrid zebra and of their parent species, plains zebra (E. quagga) and Grevy's zebra (E. grevyi). We found that both diet and microbiome composition clustered by species, and that hybrid diets and microbiomes were largely nested within those of the maternal species, plains zebra. Hybrid microbiomes were less variable than those of either parent species where they co-occurred. Diet and microbiome composition were strongly correlated, although the strength of this correlation varied between species. These patterns are most consistent with the maternal-effects hypothesis, somewhat consistent with the diet hypothesis, and largely inconsistent with the environmental-sourcing and morphophysiological-filtering hypotheses. Maternal transmittance likely operates in conjunction with inherited feeding habits to conserve microbiome composition within species.

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.

Trait-based sensitivity of large mammals to a catastrophic tropical cyclone.

Extreme weather events perturb ecosystems and increasingly threaten biodiversity1. Ecologists emphasize the need to forecast and mitigate the impacts of these events, which requires knowledge of how risk is distributed among species and environments. However, the scale and unpredictability of extreme events complicate risk assessment1-4-especially for large animals (megafauna), which are ecologically important and disproportionately threatened but are wide-ranging and difficult to monitor5. Traits such as body size, dispersal ability and habitat affiliation are hypothesized to determine the vulnerability of animals to natural hazards1,6,7. Yet it has rarely been possible to test these hypotheses or, more generally, to link the short-term and long-term ecological effects of weather-related disturbance8,9. Here we show how large herbivores and carnivores in Mozambique responded to Intense Tropical Cyclone Idai, the deadliest storm on record in Africa, across scales ranging from individual decisions in the hours after landfall to changes in community composition nearly 2 years later. Animals responded behaviourally to rising floodwaters by moving upslope and shifting their diets. Body size and habitat association independently predicted population-level impacts: five of the smallest and most lowland-affiliated herbivore species declined by an average of 28% in the 20 months after landfall, while four of the largest and most upland-affiliated species increased by an average of 26%. We attribute the sensitivity of small-bodied species to their limited mobility and physiological constraints, which restricted their ability to avoid the flood and endure subsequent reductions in the quantity and quality of food. Our results identify general traits that govern animal responses to severe weather, which may help to inform wildlife conservation in a volatile climate.

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 Difficulty of Predicting Evolutionary Change in Response to Novel Ecological Interactions: A Field Experiment with Anolis Lizards.

AbstractDetermining whether and how evolution is predictable is an important goal, particularly as anthropogenic disturbances lead to novel species interactions that could modify selective pressures. Here, we use a multigeneration field experiment with brown anole lizards (Anolis sagrei) to test hypotheses about the predictability of evolution. We manipulated the presence/absence of predators and competitors of A. sagrei across 16 islands in the Bahamas that had preexisting brown anole populations. Before the experiment and again after roughly five generations, we measured traits related to locomotor performance and habitat use by brown anoles and used double-digest restriction enzyme-associated DNA sequencing to estimate genome-wide changes in allele frequencies. Although previous work showed that predators and competitors had characteristic effects on brown anole behavior, diet, and population sizes, we found that evolutionary change at both phenotypic and genomic levels was difficult to forecast. Phenotypic changes were contingent on sex and habitat use, whereas genetic change was unpredictable and not measurably correlated with phenotypic changes, experimental treatments, or other environmental factors. Our work shows how differences in ecological context can alter evolutionary outcomes over short timescales and underscores the difficulty of forecasting evolutionary responses to multispecies interactions in natural conditions, even in a well-studied system with ample supporting ecological information.

Ecology: How mesopredators run with the big dogs.

Food webs are indispensable maps of community organization, but most are crudely drawn - an inconvenient truth that ecologists must confront. A new DNA metabarcoding study quantifies predator-prey interactions and ecological-network structure with long-overdue precision, supplying insight into how large and small carnivores coexist.

Host phylogeny and functional traits differentiate gut microbiomes in a diverse natural community of small mammals.

Differences in the bacterial communities inhabiting mammalian gut microbiomes tend to reflect the phylogenetic relatedness of their hosts, a pattern dubbed phylosymbiosis. Although most research on this pattern has compared the gut microbiomes of host species across biomes, understanding the evolutionary and ecological processes that generate phylosymbiosis requires comparisons across phylogenetic scales and under similar ecological conditions. We analysed the gut microbiomes of 14 sympatric small mammal species in a semi-arid African savanna, hypothesizing that there would be a strong phylosymbiotic pattern associated with differences in their body sizes and diets. Consistent with phylosymbiosis, microbiome dissimilarity increased with phylogenetic distance among hosts, ranging from congeneric sets of mice and hares that did not differ significantly in microbiome composition to species from different taxonomic orders that had almost no gut bacteria in common. While phylosymbiosis was detected among just the 11 species of rodents, it was substantially weaker at this scale than in comparisons involving all 14 species together. In contrast, microbiome diversity and composition were generally more strongly correlated with body size, dietary breadth, and dietary overlap in comparisons restricted to rodents than in those including all lineages. The starkest divides in microbiome composition thus reflected the broad evolutionary divergence of hosts, regardless of body size or diet, while subtler microbiome differences reflected variation in ecologically important traits of closely related hosts. Strong phylosymbiotic patterns arose deep in the phylogeny, and ecological filters that promote functional differentiation of cooccurring host species may disrupt or obscure this pattern near the tips.

Mechanisms of individual variation in large herbivore diets: Roles of spatial heterogeneity and state-dependent foraging.

Many populations of consumers consist of relatively specialized individuals that eat only a subset of the foods consumed by the population at large. Although the ecological significance of individual-level diet variation is recognized, such variation is difficult to document, and its underlying mechanisms are poorly understood. Optimal foraging theory provides a useful framework for predicting how individuals might select different diets, positing that animals balance the "opportunity cost" of stopping to eat an available food item against the cost of searching for something more nutritious; diet composition should be contingent on the distribution of food, and individual foragers should be more selective when they have greater energy reserves to invest in searching for high-quality foods. We tested these predicted mechanisms of individual niche differentiation by quantifying environmental (resource heterogeneity) and organismal (nutritional condition) determinants of diet in a widespread browsing antelope (bushbuck, Tragelaphus sylvaticus) in an African floodplain-savanna ecosystem. We quantified individuals' realized dietary niches (taxonomic richness and composition) using DNA metabarcoding of fecal samples collected repeatedly from 15 GPS-collared animals (range 6-14 samples per individual, median 12). Bushbuck diets were structured by spatial heterogeneity and constrained by individual condition. We observed significant individual-level partitioning of food plants by bushbuck both within and between two adjacent habitat types (floodplain and woodland). Individuals with home ranges that were closer together and/or had similar vegetation structure (measured using LiDAR) ate more similar diets, supporting the prediction that heterogeneous resource distribution promotes individual differentiation. Individuals in good nutritional condition had significantly narrower diets (fewer plant taxa), searched their home ranges more intensively (intensity-of-use index), and had higher-quality diets (percent digestible protein) than those in poor condition, supporting the prediction that animals with greater endogenous reserves have narrower realized niches because they can invest more time in searching for nutritious foods. Our results support predictions from optimal foraging theory about the energetic basis of individual-level dietary variation and provide a potentially generalizable framework for understanding how individuals' realized niche width is governed by animal behavior and physiology in heterogeneous landscapes.

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.

Dynamic landscapes of fear: understanding spatiotemporal risk.

The landscape of fear (LOF) concept posits that prey navigate spatial heterogeneity in perceived predation risk, balancing risk mitigation against other activities necessary for survival and reproduction. These proactive behavioral responses to risk can affect individual fitness, population dynamics, species interactions, and coexistence. Yet, antipredator responses in free-ranging prey often contradict expectations, raising questions about the generality and scalability of the LOF framework and suggesting that a purely spatial, static LOF conceptualization may be inadequate. Here, we outline a 'dynamic' LOF framework that explicitly incorporates time to account for predictable spatiotemporal variation in risk-resource trade-offs. This integrated approach suggests novel predictions about predator effects on prey behaviors to refine understanding of the role predators play in ecological communities.

Large-herbivore nemabiomes: patterns of parasite diversity and sharing.

Amidst global shifts in the distribution and abundance of wildlife and livestock, we have only a rudimentary understanding of ungulate parasite communities and parasite-sharing patterns. We used qPCR and DNA metabarcoding of fecal samples to characterize gastrointestinal nematode (Strongylida) community composition and sharing among 17 sympatric species of wild and domestic large mammalian herbivore in central Kenya. We tested a suite of hypothesis-driven predictions about the role of host traits and phylogenetic relatedness in describing parasite infections. Host species identity explained 27-53% of individual variation in parasite prevalence, richness, community composition and phylogenetic diversity. Host and parasite phylogenies were congruent, host gut morphology predicted parasite community composition and prevalence, and hosts with low evolutionary distinctiveness were centrally positioned in the parasite-sharing network. We found no evidence that host body size, social-group size or feeding height were correlated with parasite composition. Our results highlight the interwoven evolutionary and ecological histories of large herbivores and their gastrointestinal nematodes and suggest that host identity, phylogeny and gut architecture-a phylogenetically conserved trait related to parasite habitat-are the overriding influences on parasite communities. These findings have implications for wildlife management and conservation as wild herbivores are increasingly replaced by livestock.

Ecological consequences of large herbivore exclusion in an African savanna: 12 years of data from the UHURU experiment.

Diverse communities of large mammalian herbivores (LMH), once widespread, are now rare. LMH exert strong direct and indirect effects on community structure and ecosystem functions, and measuring these effects is important for testing ecological theory and for understanding past, current, and future environmental change. This in turn requires long-term experimental manipulations, owing to the slow and often nonlinear responses of populations and assemblages to LMH removal. Moreover, the effects of particular species or body-size classes within diverse LMH guilds are difficult to pinpoint, and the magnitude and even direction of these effects often depends on environmental context. Since 2008, we have maintained the Ungulate Herbivory Under Rainfall Uncertainty (UHURU) experiment, a series of size-selective LMH exclosures replicated across a rainfall/productivity gradient in a semiarid Kenyan savanna. The goals of the UHURU experiment are to measure the effects of removing successively smaller size classes of LMH (mimicking the process of size-biased extirpation) and to establish how these effects are shaped by spatial and temporal variation in rainfall. The UHURU experiment comprises three LMH-exclusion treatments and an unfenced control, applied to nine randomized blocks of contiguous 1-ha plots (n = 36). The fenced treatments are MEGA (exclusion of megaherbivores, elephant and giraffe), MESO (exclusion of herbivores ≥40 kg), and TOTAL (exclusion of herbivores ≥5 kg). Each block is replicated three times at three sites across the 20-km rainfall gradient, which has fluctuated over the course of the experiment. The first 5 years of data were published previously (Ecological Archives E095-064) and have been used in numerous studies. Since that publication, we have (1) continued to collect data following the original protocols, (2) improved the taxonomic resolution and accuracy of plant and small-mammal identifications, and (3) begun collecting several new data sets. Here, we present updated and extended raw data from the first 12 years of the UHURU experiment (2008-2019). Data include daily rainfall data throughout the experiment; annual surveys of understory plant communities; annual censuses of woody-plant communities; annual measurements of individually tagged woody plants; monthly monitoring of flowering and fruiting phenology; every-other-month small-mammal mark-recapture data; and quarterly large-mammal dung surveys. There are no copyright restrictions; notification of when and how data are used is appreciated and users of UHURU data should cite this data paper when using the data.

Dietary abundance distributions: Dominance and diversity in vertebrate diets.

Diet composition is among the most important yet least understood dimensions of animal ecology. Inspired by the study of species abundance distributions (SADs), we tested for generalities in the structure of vertebrate diets by characterising them as dietary abundance distributions (DADs). We compiled data on 1167 population-level diets, representing >500 species from six vertebrate classes, spanning all continents and oceans. DADs near-universally (92.5%) followed a hollow-curve shape, with scant support for other plausible rank-abundance-distribution shapes. This strong generality is inherently related to, yet incompletely explained by, the SADs of available food taxa. By quantifying dietary generalisation as the half-saturation point of the cumulative distribution of dietary abundance (sp50, minimum number of foods required to account for 50% of diet), we found that vertebrate populations are surprisingly specialised: in most populations, fewer than three foods accounted for at least half the diet. Variation in sp50 was strongly associated with consumer type, with carnivores being more specialised than herbivores or omnivores. Other methodological (sampling method and effort, taxonomic resolution), biological (body mass, frugivory) and biogeographic (latitude) factors influenced sp50 to varying degrees. Future challenges include identifying the mechanisms underpinning the hollow-curve DAD, its generality beyond vertebrates, and the biological determinants of dietary generalisation.

Ecology: A revolution in resource partitioning.

Resource partitioning stabilizes species coexistence but has long been difficult to measure. DNA metabarcoding reveals previously hidden dimensions of this problem and insights relevant for understanding and fostering coexistence - not just among wild carnivores, but also between carnivores and people.

Ivory poaching and the rapid evolution of tusklessness in African elephants.

Understanding the evolutionary consequences of wildlife exploitation is increasingly important as harvesting becomes more efficient. We examined the impacts of ivory poaching during the Mozambican Civil War (1977 to 1992) on the evolution of African savanna elephants (Loxodonta africana) in Gorongosa National Park. Poaching resulted in strong selection that favored tusklessness amid a rapid population decline. Survey data revealed tusk-inheritance patterns consistent with an X chromosome­linked dominant, male-lethal trait. Whole-genome scans implicated two candidate genes with known roles in mammalian tooth development (AMELX and MEP1a), including the formation of enamel, dentin, cementum, and the periodontium. One of these loci (AMELX) is associated with an X-linked dominant, male-lethal syndrome in humans that diminishes the growth of maxillary lateral incisors (homologous to elephant tusks). This study provides evidence for rapid, poaching-mediated selection for the loss of a prominent anatomical trait in a keystone species.

The gastrointestinal nematodes of plains and Grevy's zebras: Phylogenetic relationships and host specificity.

Equids are chronically infected with parasitic strongyle nematodes. There is a rich literature on horse strongyles, but they are difficult to identify morphologically and genetic studies on strongyles infecting other equid species are few, hampering studies of host specificity. We sequenced expelled worms from two sympatric zebra species in central Kenya to expand the strongyle phylogeny and used DNA metabarcoding on faecal samples to genetically characterize zebra nemabiomes for the first time. We generated sequences for several species new to public genetic reference databases, all of which are typical strongyles in wild zebras (i.e., the three species of Cylindropharynx and Cyathostomum montgomeryi), and identified their closest relatives. We also discovered an apparent fungus infecting a quarter of the expelled Crossocephalus viviparus worms, a hyperabundant nematode species in the family Atractidae, hinting at the possibility that zebra host-parasite dynamics may involve a zebra-fungus mutualism. The two zebra species had similar nemabiomes; we found a complete overlap in the list of nematode species they carry and very similar prevalence (i.e., proportion of hosts infected) for the different nematode species. Our study suggests limited host-specificity in zebra strongyles and high potential for transmission between the plains zebra and the endangered Grevy's zebra.

Large herbivores suppress liana infestation in an African savanna.

African savannas are the last stronghold of diverse large-mammal communities, and a major focus of savanna ecology is to understand how these animals affect the relative abundance of trees and grasses. However, savannas support diverse plant life-forms, and human-induced changes in large-herbivore assemblages-declining wildlife populations and their displacement by livestock-may cause unexpected shifts in plant community composition. We investigated how herbivory affects the prevalence of lianas (woody vines) and their impact on trees in an East African savanna. Although scarce (<2% of tree canopy area) and defended by toxic latex, the dominant liana, Cynanchum viminale (Apocynaceae), was eaten by 15 wild large-herbivore species and was consumed in bulk by native browsers during experimental cafeteria trials. In contrast, domesticated ungulates rarely ate lianas. When we experimentally excluded all large herbivores for periods of 8 to 17 y (simulating extirpation), liana abundance increased dramatically, with up to 75% of trees infested. Piecewise exclusion of different-sized herbivores revealed functional complementarity among size classes in suppressing lianas. Liana infestation reduced tree growth and reproduction, but herbivores quickly cleared lianas from trees after the removal of 18-y-old exclosure fences (simulating rewilding). A simple model of liana contagion showed that, without herbivores, the long-term equilibrium could be either endemic (liana-tree coexistence) or an all-liana alternative stable state. We conclude that ongoing declines of wild large-herbivore populations will disrupt the structure and functioning of many African savannas in ways that have received little attention and that may not be mitigated by replacing wildlife with livestock.

Resource availability and heterogeneity shape the self-organisation of regular spatial patterning.

Explaining large-scale ordered patterns and their effects on ecosystem functioning is a fundamental and controversial challenge in ecology. Here, we coupled empirical and theoretical approaches to explore how competition and spatial heterogeneity govern the regularity of colony dispersion in fungus-farming termites. Individuals from different colonies fought fiercely, and inter-nest distances were greater when nests were large and resources scarce-as expected if competition is strong, large colonies require more resources and foraging area scales with resource availability. Building these principles into a model of inter-colony competition showed that highly ordered patterns emerged under high resource availability and low resource heterogeneity. Analysis of this dynamical model provided novel insights into the mechanisms that modulate pattern regularity and the emergent effects of these patterns on system-wide productivity. Our results show how environmental context shapes pattern formation by social-insect ecosystem engineers, which offers one explanation for the marked variability observed across ecosystems.