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.

Predator-induced collapse of niche structure and species coexistence.

Biological invasions are both a pressing environmental challenge and an opportunity to investigate fundamental ecological processes, such as the role of top predators in regulating biodiversity and food-web structure. In whole-ecosystem manipulations of small Caribbean islands on which brown anole lizards (Anolis sagrei) were the native top predator, we experimentally staged invasions by competitors (green anoles, Anolis smaragdinus) and/or new top predators (curly-tailed lizards, Leiocephalus carinatus). We show that curly-tailed lizards destabilized the coexistence of competing prey species, contrary to the classic idea of keystone predation. Fear-driven avoidance of predators collapsed the spatial and dietary niche structure that otherwise stabilized coexistence, which intensified interspecific competition within predator-free refuges and contributed to the extinction of green-anole populations on two islands. Moreover, whereas adding either green anoles or curly-tailed lizards lengthened food chains on the islands, adding both species reversed this effect-in part because the apex predators were trophic omnivores. Our results underscore the importance of top-down control in ecological communities, but show that its outcomes depend on prey behaviour, spatial structure, and omnivory. Diversity-enhancing effects of top predators cannot be assumed, and non-consumptive effects of predation risk may be a widespread constraint on species coexistence.

Warfare and wildlife declines in Africa's protected areas.

Large-mammal populations are ecological linchpins, and their worldwide decline and extinction disrupts many ecosystem functions and services. Reversal of this trend will require an understanding of the determinants of population decline, to enable more accurate predictions of when and where collapses will occur and to guide the development of effective conservation and restoration policies. Many correlates of large-mammal declines are known, including low reproductive rates, overhunting, and habitat destruction. However, persistent uncertainty about the effects of one widespread factor-armed conflict-complicates conservation-planning and priority-setting efforts. Case studies have revealed that conflict can have either positive or negative local impacts on wildlife, but the direction and magnitude of its net effect over large spatiotemporal scales have not previously been quantified. Here we show that conflict frequency predicts the occurrence and severity of population declines among wild large herbivores in African protected areas from 1946 to 2010. Conflict was extensive during this period, occurring in 71% of protected areas, and conflict frequency was the single most important predictor of wildlife population trends among the variables that we analysed. Population trajectories were stable in peacetime, fell significantly below replacement with only slight increases in conflict frequency (one conflict-year per two-to-five decades), and were almost invariably negative in high-conflict sites, both in the full 65-year dataset and in an analysis restricted to recent decades (1989-2010). Yet total population collapse was infrequent, indicating that war-torn faunas can often recover. Human population density was also correlated (positively) with wildlife population trajectories in recent years; however, we found no significant effect, in either timespan, of species body mass, protected-area size, conflict intensity (human fatalities), drought frequency, presence of extractable mineral resources, or various metrics of development and governance. Our results suggest that sustained conservation activity in conflict zones-and rapid interventions following ceasefires-may help to save many at-risk populations and species.

Determinants of tree cover in tropical floodplains.

Tree cover differentiates forests from savannas and grasslands. In tropical floodplains, factors differentiating these systems are poorly known, even though floodplains cover 10% of the tropical landmass. Seasonal inundation potentially presents trees with both challenges (soil anoxia) and benefits (moisture and nutrient deposition), the relative importance of which may depend on ecological context, e.g. if floods alleviate water stress more in more arid ecosystems. Here, we use remotely sensed data across 13 large tropical and sub-tropical floodplain ecosystems on five continents to show that climatic water balance (i.e. precipitation-potential evapotranspiration) strongly increases floodplain tree cover in interaction with flooding, fire and topography. As predicted, flooding increases tree cover in more arid floodplains, but decreases tree cover in climatically wetter ones. As in uplands, frequent fire reduced tree cover, particularly in wet regions, but-in contrast with uplands-lower elevation and sandier soils decreased tree cover. Our results suggest that predicting the impacts of changing climate, land use and hydrology on floodplain ecosystems depends on considering climate-disturbance interactions. While outright wetland conversion proceeds globally, additional anthropogenic activities, including alteration of fire frequencies and dam construction, will also shift floodplain tree cover, especially in wet climates.

Does primary productivity modulate the indirect effects of large herbivores? A global meta-analysis.

Indirect effects of large mammalian herbivores (LMH), while much less studied than those of apex predators, are increasingly recognized to exert powerful influences on communities and ecosystems. The strength of these effects is spatiotemporally variable, and several sets of authors have suggested that they are governed in part by primary productivity. However, prior theoretical and field studies have generated conflicting results and predictions, underscoring the need for a synthetic global analysis. We conducted a meta-analysis of the direction and magnitude of large mammalian herbivore-initiated indirect interactions using 67 published studies comprising 456 individual responses. We georeferenced 41 of these studies (comprising 253 responses from 33 locations on five continents) to a satellite-derived map of primary productivity. Because predator assemblages might also influence the impact of large herbivores, we conducted a similar analysis using a global map of large carnivore species richness. In general, LMH reduced the abundance of other consumer species and also tended to reduce consumer richness, although the latter effect was only marginally significant. There was a pronounced reduction in the strength of negative (i.e. suppressive, due e.g., to competition) indirect effects of LMH on consumer abundance in more productive ecosystems. In contrast, positive (facilitative) indirect effects were not significantly correlated with productivity, likely because these comprised a more heterogeneous array of mechanisms. We found no effect of carnivore species richness on herbivore-initiated indirect effect strength. Our findings help to resolve the fundamental problem of ecological contingency as it pertains to the strength of an understudied class of multitrophic interactions. Moreover, these results will aid in predicting the indirect effects of anthropogenic wildlife declines and irruptions, and how these effects might be mediated by climatically driven shifts in resource availability. To the extent that intact ungulate guilds help to suppress populations of small animals that act as agricultural pests and disease reservoirs, the negative impacts of large mammal declines on human well-being may be relatively stronger in low-productivity areas.

Context-dependent symbioses and their potential roles in wildlife diseases.

It is well known in ecology, evolution and medicine that both the nature (commensal, parasitic and mutualistic) and outcome (symbiont fitness, survival) of symbiotic interactions are often context-dependent. Less is known about the importance of context-dependence in symbioses involved in wildlife disease. We review variable symbioses, and use the amphibian disease chytridiomycosis to demonstrate how understanding context-dependence can improve the understanding and management of wildlife diseases. In chytridiomycosis, the host-pathogen interaction is context-dependent; it is strongly affected by environmental temperature. Skin bacteria can also modify the interaction; some bacteria reduce amphibians' susceptibility to chytridiomycosis. Augmentation of protective microbes is being considered as a possible management tool, but informed application of bioaugmentation requires understanding of how the interactions between host, beneficial bacteria and pathogen depend upon environmental context. The community-level response of the amphibian skin microbiota to environmental conditions may explain the relatively narrow range of environmental conditions in which past declines have occurred. Environmental context affects virulence and the protection provided by mutualists in other host-pathogen systems, including threatened bats and corals. Increased focus on context-dependence in interactions between wildlife and their symbionts is likely to be crucial to the future investigation and management of emerging diseases of wildlife.

Trophic rewilding revives biotic resistance to shrub invasion.

Trophic rewilding seeks to rehabilitate degraded ecosystems by repopulating them with large animals, thereby re-establishing strong top-down interactions. Yet there are very few tests of whether such initiatives can restore ecosystem structure and functions, and on what timescales. Here we show that war-induced collapse of large-mammal populations in Mozambique's Gorongosa National Park exacerbated woody encroachment by the invasive shrub Mimosa pigra-considered one of the world's 100 worst invasive species-and that one decade of concerted trophic rewilding restored this invasion to pre-war baseline levels. Mimosa occurrence increased between 1972 and 2015, a period encompassing the near extirpation of large herbivores during the Mozambican Civil War. From 2015 to 2019, mimosa abundance declined as ungulate biomass recovered. DNA metabarcoding revealed that ruminant herbivores fed heavily on mimosa, and experimental exclosures confirmed the causal role of mammalian herbivory in containing shrub encroachment. Our results provide mechanistic evidence that trophic rewilding has rapidly revived a key ecosystem function (biotic resistance to a notorious woody invader), underscoring the potential for restoring ecological health in degraded protected areas.

Cascading impacts of large-carnivore extirpation in an African ecosystem.

Populations of the world's largest carnivores are declining and now occupy mere fractions of their historical ranges. Theory predicts that when apex predators disappear, large herbivores become less fearful, occupy new habitats, and modify those habitats by eating new food plants. Yet experimental support for this prediction has been difficult to obtain in large-mammal systems. After the extirpation of leopards and African wild dogs from Mozambique's Gorongosa National Park, forest-dwelling antelopes [bushbuck (Tragelaphus sylvaticus)] expanded into treeless floodplains, where they consumed novel diets and suppressed a common food plant [waterwort (Bergia mossambicensis)]. By experimentally simulating predation risk, we demonstrate that this behavior was reversible. Thus, whereas anthropogenic predator extinction disrupted a trophic cascade by enabling rapid differentiation of prey behavior, carnivore restoration may just as rapidly reestablish that cascade.

Use of N stable isotope and microbial analyses to define wastewater influence in Mobile Bay, AL.

We assessed short-term ecological and potential human health effects of wastewater treatment plant (WTP) effluent by measuring delta 15N per thousand and microbial concentrations in oysters and suspended particulate matter (SPM). We also tested male-specific bacteriophage (MSB) as an alternative to fecal coliforms, to assess potential influence of wastewater contamination on shellfish. WTP effluent did not affect oyster growth or survival, but SPM and oysters acquired wastewater-specific delta 15N per thousand. delta 15N values were depleted near the WTP, typical of low-level processed wastewater. Fecal coliform and MSB concentrations were higher in samples taken closest to the WTP, and MSB values were significantly correlated with delta 15N per thousand in oyster tissues. Overall, oysters demonstrated relatively rapid integration and accumulation of wastewater-specific delta 15N per thousand and indicator microorganisms compared to water samples. These data suggest oysters were superior sentinels compared to water, and MSB was a more reliable indicator of wastewater influence on shellfish than fecal coliforms.

Cool temperatures reduce antifungal activity of symbiotic bacteria of threatened amphibians--implications for disease management and patterns of decline.

Chytridiomycosis, caused by the fungus Batrachochytrium dendrobatidis (Bd), is a widespread disease of amphibians responsible for population declines and extinctions. Some bacteria from amphibians' skins produce antimicrobial substances active against Bd. Supplementing populations of these cutaneous antifungal bacteria might help manage chytridiomycosis in wild amphibians. However, the activity of protective bacteria may depend upon environmental conditions. Biocontrol of Bd in nature thus requires knowledge of how environmental conditions affect their anti-Bd activity. For example, Bd-driven amphibian declines have often occurred at temperatures below Bd's optimum range. It is possible these declines occurred due to reduced anti-Bd activity of bacterial symbionts at cool temperatures. Better understanding of the effects of temperature on chytridiomycosis development could also improve risk evaluation for amphibian populations yet to encounter Bd. We characterized, at a range of temperatures approximating natural seasonal variation, the anti-Bd activity of bacterial symbionts from the skins of three species of rainforest tree frogs (Litoria nannotis, Litoria rheocola, and Litoria serrata). All three species declined during chytridiomycosis outbreaks in the late 1980s and early 1990s and have subsequently recovered to differing extents. We collected anti-Bd bacterial symbionts from frogs and cultured the bacteria at constant temperatures from 8 °C to 33 °C. Using a spectrophotometric assay, we monitored Bd growth in cell-free supernatants (CFSs) from each temperature treatment. CFSs from 11 of 24 bacteria showed reduced anti-Bd activity in vitro when they were produced at cool temperatures similar to those encountered by the host species during population declines. Reduced anti-Bd activity of metabolites produced at low temperatures may, therefore, partially explain the association between Bd-driven declines and cool temperatures. We show that to avoid inconsistent antifungal activity, bacteria evaluated for use in chytridiomycosis biocontrol should be tested over a range of environmental temperatures spanning those likely to be encountered in the field.

Short-term exposure to warm microhabitats could explain amphibian persistence with Batrachochytrium dendrobatidis.

Environmental conditions can alter the outcomes of symbiotic interactions. Many amphibian species have declined due to chytridiomycosis, caused by the pathogenic fungus Batrachochytrium dendrobatidis (Bd), but many others persist despite high Bd infection prevalence. This indicates that Bd's virulence is lower, or it may even be a commensal, in some hosts. In the Australian Wet Tropics, chytridiomycosis extirpated Litoria nannotis from high-elevation rain forests in the early 1990 s. Although the species is recolonizing many sites, no population has fully recovered. Litoria lorica disappeared from all known sites in the early 1990 s and was thought globally extinct, but a new population was discovered in 2008, in an upland dry forest habitat it shares with L. nannotis. All frogs of both species observed during three population censuses were apparently healthy, but most carried Bd. Frogs perch on sun-warmed rocks in dry forest streams, possibly keeping Bd infections below the lethal threshold attained in cooler rain forests. We tested whether short-term elevated temperatures can hamper Bd growth in vitro over one generation (four days). Simulating the temperatures available to frogs on strongly and moderately warmed rocks in dry forests, by incubating cultures at 33°C for one hour daily, reduced Bd growth below that of Bd held at 15°C constantly (representing rain forest habitats). Even small decreases in the exponential growth rate of Bd on hosts may contribute to the survival of frogs in dry forests.