Nacho Villar

The urgent need to mitigate and adapt to climate change necessitates a comprehensive understanding of carbon cycling dynamics. Traditionally, global carbon cycle models have focused on vegetation, but recent research suggests that animals can play a significant role in carbon dynamics under some circumstances, potentially enhancing the effectiveness of nature-based solutions to mitigate climate change. However, links between animals, plants, and carbon remain unclear. We explored the complex interactions between defaunation and ecosystem carbon in Earth's most biodiverse and carbon-rich biome, tropical rainforests. Defaunation can change patterns of seed dispersal, granivory, and herbivory in ways that alter tree species composition and, therefore, forest carbon above- and belowground. Most studies we reviewed show that defaunation reduces carbon storage 0−26% in the Neo- and Afrotropics, primarily via population declines in large-seeded, animal-dispersed trees. However, Asian forests are not predicted to experience changes because their high-carbon trees are wind dispersed. Extrapolating these local effects to entire ecosystems implies losses of ∼1.6 Pg CO₂ equivalent across the Brazilian Atlantic Forest and 4−9.2 Pg across the Amazon over 100 years and of ∼14.7−26.3 Pg across the Congo basin over 250 years. In addition to being hard to quantify with precision, the effects of defaunation on ecosystem carbon are highly context dependent; outcomes varied based on the balance between antagonist and mutualist species interactions, abiotic conditions, human pressure, and numerous other factors. A combination of experiments, large-scale comparative studies, and mechanistic models could help disentangle the effects of defaunation from other anthropogenic forces in the face of the incredible complexity of tropical forest systems. Overall, our synthesis emphasizes the importance of—and inconsistent results when—integrating animal dynamics into carbon cycle models, which is crucial for developing climate change mitigation strategies and effective policies.

Foraging is essential for animal survival, as it provides the nutritional resources to sustain metabolism and all activities that animals undertake. Communal latrines are sites where multiple individuals of the same species defecate and can have multiple functions. Latrine behavior has been recorded in many animal species, including lowland tapirs (Tapirus terrestris), which consume a wide variety of plants and fruits and defecate large piles of dung, sometimes containing many seeds. Due to the concentration of seeds and other defecated material, latrines may thus serve as direct sources of food for other vertebrates, including insectivores feeding on invertebrates attracted to dung. Here, we studied which vertebrate animals were recorded foraging in tapir latrines, how long they spent foraging on latrines, and how their foraging behavior varied with the time of day and days since tapir defecation. Since tapirs are generalist foragers with a large diet breadth, we expected that their feces might attract vertebrate foragers with a variety of dietary habits (e.g., frugivores, granivores, omnivores, insectivores) in distinct foraging periods within a day. We also expected that the foraging events would be greatest in the days immediately following tapir defecation. We monitored 27 tapir latrines with camera traps for six months, recording foraging vs. non-foraging behaviors. We observed nine vertebrate species foraging in tapir latrines with five frequent foragers: the frugivores Guerlinguetus brasiliensis (50% of total foraging records) and Tinamus solitarius (16%, also a granivore) and the omnivores Turdus albicollis (18%), Chamaeza campanisona (10%) and Odontophorus capueira (6%). Foraging and non-foraging events throughout the day differed significantly for G. brasiliensis (p= 0.006), T. solitarius (p= 0.01), and C. campanisona (p= 0.001), and all species were diurnal, foraging between 05:00 h and 18:00 h. The foraging probability of C. campanisona and T. albicollis was affected by the time lapse since tapir defecation. Our study highlights that communal latrines such as those maintained by lowland tapirs can be an important resource supply for some vertebrate consumers with different diets and could contribute to maintaining diversity in tropical forests. We call for future studies to inspect the importance of latrines as foraging sites for other species and ecosystems.

An often-overlooked question of the biodiversity crisis is how natural hazards contribute to species extinction risk. To address this issue, we explored how four natural hazards, earthquakes, hurricanes, tsunamis, and volcanoes, overlapped with the distribution ranges of amphibians, birds, mammals, and reptiles that have either narrow distributions or populations with few mature individuals. To assess which species are at risk from these natural hazards, we combined the frequency and magnitude of each natural hazard to estimate their impact. We considered species at risk if they overlapped with regions where any of the four natural hazards historically occurred (n = 3,722). Those species with at least a quarter of their range subjected to a high relative impact were considered at high risk (n = 2,001) of extinction due to natural hazards. In total, 834 reptiles, 617 amphibians, 302 birds, and 248 mammals were at high risk and they were mainly distributed on islands and in the tropics. Hurricanes (n = 983) and earthquakes (n = 868) affected most species, while tsunamis (n = 272), and volcanoes (n = 171) affected considerably fewer. The region with the highest number of species at high risk was the Pacific Ring of Fire, especially due to volcanoes, earthquakes, and tsunamis, while hurricane-related high-risk species were concentrated in the Caribbean Sea, Gulf of Mexico, and northwestern Pacific Ocean. Our study provides important information regarding the species at risk due to natural hazards and can help guide conservation attention and efforts to safeguard their survival.

Natural enemies play an important role in controlling plant population growth and vegetation dynamics. Tropical rainforests host the greatest diversity of herbivores, from large mammalian ungulates to microscopic pathogens, generating and maintaining plant diversity. By feeding on the same resources, large mammalian herbivores may interfere with plant consumption and leaf damage by important enemy guilds such as invertebrate herbivores and pathogens, triggering indirect trophic cascades. However, the impact of local extinctions of large herbivores on plant–enemy interactions is relatively unknown. We experimentally tested the effects of defaunation of large mammalian herbivores (e.g. peccaries, tapirs and brocket deer; hereafter, large herbivores) on the leaf damage of 3350 understorey plants in tropical rainforests of Brazil. We examined leaf damage in 10,050 leaves from 333 morphospecies by assigning the area consumed or damaged by five guilds of insect herbivores and leaf pathogens within 86 paired open-closed plots and investigating the joint effects of defaunation and plant phylogenetic diversity. Plants released from large herbivores had 9% less leaf damage; this difference was due to the lower leaf pathogens incidence (29%) rather than insect herbivory. Evolutionary distinctness was positively correlated with leaf damage in a similar way in all treatments, suggesting additive effects of defaunation and phylogenetic diversity. Total and pathogenic leaf damage (but not insect damage) decreased with plant richness across treatments, and large herbivores exclusion resulted in increased plant species richness. This suggests that large herbivores exclusion leads to a dilution of total and pathogens' leaf damage by increasing plant species richness. Our results suggest that indirect effects of large herbivores decrease the dilution potential of plant communities against pathogens and rather reinforce their top-down impact on vegetation, demonstrating a previously overlooked cascading effect of large herbivore extinction on forest ecosystems. Synthesis: The extinction of large mammalian herbivores can lead to a decrease in pathogen-driven leaf damage, a previously unknown indirect effect in forest ecosystems, which might have consequences for plant fitness and ultimately for plant diversity. Large herbivores and plant pathogens might have synergistic effects in regulating the diversity of plant communities in some of the most diverse ecosystems on Earth.

Top-down control by large herbivores is a well-known driver of plant diversity structure and productivity. Yet, for forest ecosystems the sign and magnitude of herbivore control across resource gradients is not well understood. We conducted a series of replicated large herbivore exclusion experiments in defaunated and non-defaunated Atlantic forests of Brazil to evaluate the effects of large herbivores on tropical plant communities. We hypothesized that the top-down impact of large herbivores on seedling recruitment, species richness, diversity and productivity would change across a natural gradient in the density of a key plant resource, the palm Euterpe edulis, which is thought to act as a foundation species. We found both positive (agonistic) and negative (antagonistic) spatially-structured effects of large herbivores on plant communities driven by an interaction between large herbivores and palm density on non-defaunated sites, but not on defaunated sites. Indeed, through its interaction with large herbivores, palm trees were able to regulate the spatial structure of seedling communities. In the non-defaunated forest, the negative impact of large herbivores on plant recruitment and species richness decreased substantially as palms became more abundant and canopy cover decreased. Furthermore, large herbivores caused a 185% increase but a 194% decrease in aboveground seedling productivity in areas of high and low palm density, respectively. In contrast, in the defaunated forest we did not find any consistent large herbivore impacts on plant recruitment or species richness across the gradient of palm density, and herbivore activity consistently had negative effects on seedling productivity. Analyses using camera trap data indicate that white-lipped peccaries (Tayassu peccari) played a key role in modulating recruitment and seedling productivity, while tapirs (Tapirus terrestris) contributed significantly to an increase in plant diversity, hence playing a functionally complementary role. Our results demonstrate that a key interaction between large forest-dwelling tropical herbivores and their palm resource results in landscape-scale modulation of plant communities through positive and negative spatially-structured feedbacks, and support the view that palms might act as foundation species in tropical forests. Anthropogenic pressures posed by defaunation and illegal palm harvesting in the Neotropics might lead to the functional loss of this interaction and the collapse of the spatial structure along palm density gradients, with cascading effects on the dynamics and productivity of tropical forests.

The world’s terrestrial biomes are broadly classified according to the dominant plant growth forms that define ecosystem structure and processes. Although the abundance and distribution of different plant growth forms can be strongly determined by factors such as climate and soil composition, large mammalian herbivores have a strong impact on plant communities, thus defaunation (the local or functional extinction of large animals) has the potential to alter the compositional structure of plant growth forms in natural ecosystems. Tropical rainforests sustain a high diversity of growth forms, including trees, palms, lianas, shrubs, herbs and bamboos, all of which play important ecosystem functions. Here, we experimentally evaluate how large mammalian herbivores affect the dominance, diversity and coexistence of these major tropical forest plant growth forms, by monitoring communities of saplings on the understorey in 43 paired exclusion plots in a long-term replicated exclusion experiment in the understorey of the Atlantic forest of Brazil. Over the course of 10 years large herbivore exclusion decreased diversity among growth forms, increased the absolute abundance of palms and trees (22% and 38% respectively) and increased the diversity of species within these two groups, to the detriment of other growth forms. Furthermore, all pairwise relationships between growth forms were positive on plots where herbivores had access, whereas several strong negative relationships emerged in plots where herbivores were excluded. This occurred despite strong background directional temporal trends affecting plant communities in both experimental treatments across the region. Synthesis. Our work indicates that the defaunation alters growth form dominance by favouring palms and trees while eroding diversity among growth forms and coexistence on a temporal scale. Large herbivore mammals promote diversity among growth forms, preventing the hyper-dominance of trees and palms, yet without supressing the diversity of species within growth forms. We argue that large herbivore mammals affect growth forms through several non-mutually exclusive mechanisms, including herbivory, seed dispersal and physical disturbance, as well as differential effects linked to the morphological and physiological adaptations of growth forms. We conclude that defaunation might lead to profound impacts on important ecosystem functions underpinned by growth form diversity, and result in vertical and horizontal structural simplification of tropical rainforests.

How species persist in fragmented habitats is essential to understanding species resilience in response to increasing anthropogenic pressures. It has been suggested that expansion in dietary niche allows populations to persist in human-modified landscapes, yet this hypothesis has been poorly tested in highly diverse ecosystems such as tropical forests where frugivory is ubiquitous. Here, we measured dietary niche expansion of a large forest-dwelling mammal, the white-lipped peccary (Tayassu pecari), in the Atlantic Forest, Brazil, by comparing its diet using stable carbon (δ¹³C) and nitrogen (δ¹⁵N) isotopes. We collected hair of white-lipped peccaries in three continuous and three fragmented forests and compared δ¹³C and δ¹⁵N values, resource use and isotopic niches among populations and between forest types. We also tested the relationship between isotopic values of the populations and the forest cover percentage. White-lipped peccaries fed mainly on forest sources (C₃ resources), especially in continuous forests, but 28% of the individuals in fragmented sites also incorporated C₄ resources to some extent. In fragmented forests, the populations had isotopic niches from 3- to 3.6-fold the size of those in continuous forests. This niche expansion was due to the consumption of food items with higher δ¹⁵N values and C₄ crops. Differences among populations were larger among fragmented forests, suggesting variable site-specific strategies to cope with habitat loss. The mean isotopic values of white-lipped peccary populations were negatively correlated with the loss of forest cover. Some small forest fragments might still retain relatively high habitat quality, and white-lipped peccaries might be able to capitalize on such variety of resources, shifting their diets from those observed in continuous forests. We suggest that high dietary flexibility and dietary expansion toward consumption of non-forest resources might facilitate the persistence of large frugivores in fragmented habitats.

The UN declaration of the Decade of Ecosystem Restoration 2021–2030 emphasizes the need for effective measures to restore ecosystems and safeguard biodiversity. Large herbivores regulate many ecosystem processes and functions; yet, their potential as a nature-based solution to buffer against long-term temporal declines in biodiversity associated with global change and restore diversity in secondary forests remains unknown. By means of an exclusion experiment, we tested experimentally the buffering effects of large wild herbivores to avert against long-term biodiversity collapse in old-growth and secondary tropical forests in the Atlantic Forest of Brazil where sapling abundance and species richness declined c. 20% over the course of 10 years. The experiment comprised 50 large herbivore exclosure-open control plot pairs (25 at the old-growth forest and 25 at the secondary forest), where 2 m² were monitored in every plot during a 10-year period. Large herbivores were able to decelerate diversity declines and compositional change in the species-rich old-growth forest, but only decelerated compositional change in the secondary forest. In contrast, declines in species richness and abundance were unaffected by large herbivores on either forest. The buffering effects of large herbivores were strongly nonlinear and contingent on the initial level of diversity at the patch scale: highly diverse communities suffered the strongest collapse in the absence of large herbivores. Thus, larger buffering effects of large herbivores on the old-growth forest are the logical consequence of large herbivores buffering the many high diversity plant communities found in this forest. Conversely, as the secondary forest held fewer high diversity patches, buffering effects on the secondary forest were weak. Synthesis and applications. Our study indicates that large herbivores have moderate yet critical effects on slowing down community change and diversity loss of highly diverse plant communities, thus suggesting that the conservation of (and potentially trophic rewilding with) large herbivores is a fundamental nature-based solution for averting the global collapse of the strongholds of biodiversity. Its buffering effects on biodiversity loss operate at very small spatial scales, are likely contingent on successional stage and are most effective in old-growth or high diversity secondary forests.

Tropical rainforests are populated by large frugivores that feed upon fruit-producing woody species, yet their role in regulating the cycle of globally important biogeochemical elements such as nitrogen is still unknown. This is particularly relevant because tropical forests play a prominent role in the nitrogen cycle and are becoming rapidly defaunated. Furthermore, frugivory is not considered in current plant-large herbivore-nutrient cycling frameworks exclusively focused on grazers and browsers. Here we used a long-term replicated paired control-exclusion experiment in the Atlantic Forest of Brazil, where peccaries and tapirs are the largest native frugivores, to examine the impact of large ground-dwelling frugivores on modulating soil nitrogen cycling, considering their effects across a gradient of abundance of a hyper-dominant palm. We found that both large frugivores and dominant palms play a substantial role in modulating ammonium availability and nitrification rates. Large frugivores increased ammonium by 95%, which also increased additively with palm abundance. Nitrification rates increased with palm abundance in the presence of large frugivores, but not on exclosure plots. Large frugivores also stimulated the regulation of the functions of soil-nitrifying microorganisms, and modulated the landscape-scale variance in nitrogen availability. Such joint effects of large frugivores and palms are consistent with the notion of ‘fruiting lawns’. Our study indicates that frugivory plays a pivotal role in zoogeochemistry in tropical forests by regulating and structuring the nitrogen cycle, urging to accommodate frugivory in plant-large herbivore-nutrient cycling frameworks. It also indicates that defaunation, deforestation and illegal palm and timber harvesting seriously affect nitrogen cycling in tropical forests, that play a prominent role in the global cycle of this nutrient. A free Plain Language Summary can be found within the Supporting Information of this article.