Warming of aquatic ecosystems disrupts aquatic-terrestrial linkages in the tropics.

Aquatic ecosystems are tightly linked to terrestrial ecosystems by exchanges of resources, which influence species interactions, community dynamics and functioning in both ecosystem types. However, our understanding of how this coupling responds to climate warming is restricted to temperate, boreal and arctic regions, with limited knowledge from tropical ecosystems. We investigated how warming aquatic ecosystems impact cross-ecosystem exchanges in the tropics, through the export of aquatic resources into the terrestrial environment and the breakdown of terrestrial resources within the aquatic environment. We experimentally heated 50 naturally assembled aquatic communities, contained within different-sized tank-bromeliads, to a 23.5-32°C gradient of mean water temperatures. The biomass, abundance and richness of aquatic insects emerging into the terrestrial environment all declined with rising temperatures over a 45-day experiment. Structural equation and linear mixed effects modelling suggested that these impacts were driven by deleterious effects of warming on insect development and survival, rather than being mediated by aquatic predation, nutrient availability or reduced body size. Decomposition was primarily driven by microbial activity. However, total decomposition by both microbes and macroinvertebrates increased with temperature in all but the largest ecosystems, where it decreased. Thus, warming decoupled aquatic and terrestrial ecosystems, by reducing the flux of aquatic resources to terrestrial ecosystems but variably enhancing or reducing terrestrial resource breakdown in aquatic ecosystems. In contrast with increased emergence observed in warmed temperate ecosystems, future climate change is likely to reduce connectivity between tropical terrestrial and aquatic habitats, potentially impacting consumers in both ecosystem types. As tropical ectotherms live closer to their thermal tolerance limits compared to temperate species, warming can disrupt cross-ecosystem dynamics in an interconnected tropical landscape and should be considered when investigating ecosystem-level consequences of climate change.

Os ecossistemas aquáticos estão intimamente ligados aos ecossistemas terrestres por meio das trocas de recursos, que influenciam as interações entre as espécies, a dinâmica da comunidade e o funcionamento de ambos os tipos de ecossistemas. No entanto, nosso entendimento de como esse acoplamento responde ao aquecimento do clima é restrito às regiões temperadas, boreais e árticas, com conhecimento limitado para os ecossistemas tropicais. Investigamos como o aquecimento dos ecossistemas aquáticos impacta as trocas entre os ecossistemas nos trópicos, por meio da exportação de recursos aquáticos para o ambiente terrestre e da decomposição dos detritos de origem terrestre no ambiente aquático. Nós aquecemos experimentalmente 50 comunidades aquáticas que habitam tanques de bromélias de diferentes tamanhos, submetidas a um gradiente de temperatura média da água variando de 23,5 a 32°C. Em um experimento de 45 dias, a biomassa, abundância e riqueza de insetos aquáticos emergindo para o ambiente terrestre diminuíram com o aumento da temperatura. Modelos lineares mistos e de equações estruturais sugerem que esses impactos foram causados por efeitos deletérios do aquecimento no desenvolvimento e sobrevivência dos insetos, ao invés de serem mediados por predadores aquáticos, disponibilidade de nutrientes ou tamanho corporal reduzido. A decomposição foi determinada principalmente pela atividade microbiana. A decomposição total por micro-organismos e macro invertebrados aumentou com a temperatura, exceto em ecossistemas maiores. Assim, o aquecimento dissociou os ecossistemas aquáticos e terrestres, reduzindo o fluxo de recursos aquáticos para os ecossistemas terrestres, mas aumentando ou reduzindo de forma variável a decomposição dos recursos terrestres nos ecossistemas aquáticos. Em contraste com o aumento da emergência observada em ecossistemas temperados aquecidos, as mudanças climáticas futuras provavelmente reduzirão a conectividade entre os habitats terrestres e aquáticos tropicais, impactando potencialmente os consumidores em ambos os tipos de ecossistemas. Como organismos ectotérmicos tropicais vivem mais perto dos seus limites de tolerância térmica em comparação com espécies temperadas, o aquecimento pode comprometer a dinâmica entre os ecossistemas em uma paisagem tropical interconectada e deve ser considerado ao investigar as consequências das mudanças climáticas no nível do ecossistema.

How much leaf area do insects eat? A data set of insect herbivory sampled globally with a standardized protocol.

Herbivory is ubiquitous. Despite being a potential driver of plant distribution and performance, herbivory remains largely undocumented. Some early attempts have been made to review, globally, how much leaf area is removed through insect feeding. Kozlov et al., in one of the most comprehensive reviews regarding global patterns of herbivory, have compiled published studies regarding foliar removal and sampled data on global herbivory levels using a standardized protocol. However, in the review by Kozlov et al., only 15 sampling sites, comprising 33 plant species, were evaluated in tropical areas around the globe. In Brazil, which ranks first in terms of plant biodiversity, with a total of 46,097 species, almost half (43%) being endemic, a single data point was sampled, covering only two plant species. In an attempt to increase knowledge regarding herbivory in tropical plant species and to provide the raw data needed to test general hypotheses related to plant-herbivore interactions across large spatial scales, we proposed a joint, collaborative network to evaluate tropical herbivory. This network allowed us to update and expand the data on insect herbivory in tropical and temperate plant species. Our data set, collected with a standardized protocol, covers 45 sampling sites from nine countries and includes leaf herbivory measurements of 57,239 leaves from 209 species of vascular plants belonging to 65 families from tropical and temperate regions. They expand previous data sets by including a total of 32 sampling sites from tropical areas around the globe, comprising 152 species, 146 of them being sampled in Brazil. For temperate areas, it includes 13 sampling sites, comprising 59 species. Thus, when compared to the most recent comprehensive review of insect herbivory (Kozlov et al.), our data set has increased the base of available data for the tropical plants more than 460% (from 33 to 152 species) and the Brazilian sampling was increased 7,300% (from 2 to 146 species). Data on precise levels of herbivory are presented for more than 57,000 leaves worldwide. There are no copyright restrictions. Please cite this paper when using the current data in publications; the authors request to be informed how the data is used in the publications.

Extreme rainfall events alter the trophic structure in bromeliad tanks across the Neotropics.

Changes in global and regional precipitation regimes are among the most pervasive components of climate change. Intensification of rainfall cycles, ranging from frequent downpours to severe droughts, could cause widespread, but largely unknown, alterations to trophic structure and ecosystem function. We conducted multi-site coordinated experiments to show how variation in the quantity and evenness of rainfall modulates trophic structure in 210 natural freshwater microcosms (tank bromeliads) across Central and South America (18°N to 29°S). The biomass of smaller organisms (detritivores) was higher under more stable hydrological conditions. Conversely, the biomass of predators was highest when rainfall was uneven, resulting in top-heavy biomass pyramids. These results illustrate how extremes of precipitation, resulting in localized droughts or flooding, can erode the base of freshwater food webs, with negative implications for the stability of trophic dynamics.

Precipitation and predation risk alter the diversity and behavior of pollinators and reduce plant fitness.

Biotic and abiotic factors may individually or interactively disrupt plant-pollinator interactions, influencing plant fitness. Although variations in temperature and precipitation are expected to modify the overall impact of predators on plant-pollinator interactions, few empirical studies have assessed if these weather conditions influence anti-predator behaviors and how this context-dependent response may cascade down to plant fitness. To answer this question, we manipulated predation risk (using artificial spiders) in different years to investigate how natural variation in temperature and precipitation may affect diversity (richness and composition) and behavioral (visitation) responses of flower-visiting insects to predation risk, and how these effects influence plant fitness. Our findings indicate that predation risk and an increase in precipitation independently reduced plant fitness (i.e., seed set) by decreasing flower visitation. Predation risk reduced pollinator visitation and richness, and altered species composition of pollinators. Additionally, an increase in precipitation was associated with lower flower visitation and pollinator richness but did not alter pollinator species composition. However, maximum daily temperature did not affect any component of the pollinator assemblage or plant fitness. Our results indicate that biotic and abiotic drivers have different impacts on pollinator behavior and diversity with consequences for plant fitness components. Even small variation in precipitation conditions promotes complex and substantial cascading effects on plants by affecting both pollinator communities and the outcome of plant-pollinator interactions. Tropical communities are expected to be highly susceptible to climatic changes, and these changes may have drastic consequences for biotic interactions in the tropics.

Ecological response to altered rainfall differs across the Neotropics.

There is growing recognition that ecosystems may be more impacted by infrequent extreme climatic events than by changes in mean climatic conditions. This has led to calls for experiments that explore the sensitivity of ecosystems over broad ranges of climatic parameter space. However, because such response surface experiments have so far been limited in geographic and biological scope, it is not clear if differences between studies reflect geographic location or the ecosystem component considered. In this study, we manipulated rainfall entering tank bromeliads in seven sites across the Neotropics, and characterized the response of the aquatic ecosystem in terms of invertebrate functional composition, biological stocks (total invertebrate biomass, bacterial density) and ecosystem fluxes (decomposition, carbon, nitrogen). Of these response types, invertebrate functional composition was the most sensitive, even though, in some sites, the species pool had a high proportion of drought-tolerant families. Total invertebrate biomass was universally insensitive to rainfall change because of statistical averaging of divergent responses between functional groups. The response of invertebrate functional composition to rain differed between geographical locations because (1) the effect of rainfall on bromeliad hydrology differed between sites, and invertebrates directly experience hydrology not rainfall and (2) the taxonomic composition of some functional groups differed between sites, and families differed in their response to bromeliad hydrology. These findings suggest that it will be difficult to establish thresholds of "safe ecosystem functioning" when ecosystem components differ in their sensitivity to climatic variables, and such thresholds may not be broadly applicable over geographic space. In particular, ecological forecast horizons for climate change may be spatially restricted in systems where habitat properties mediate climatic impacts, and those, like the tropics, with high spatial turnover in species composition.

Consumptive effects and mismatch in predator-prey turnover rates cause inversion of biomass pyramids.

The mismatch between the turnover rates of predators and prey is one of the oldest explanations for the existence of inverted trophic pyramids. To date, the hypotheses regarding trophic pyramids have all been based on consumptive trophic links between predators and prey, and the relative contribution of non-consumptive effects is still unknown. In this study, we investigated if the inversion of pyramids in bromeliad ecosystems is driven by (i) a rapid colonization of organisms having short cohort interval production (CPI), and (ii) the prevalence of consumptive or non-consumptive effects of top predators. We used a manipulative experiment to investigate the patterns of prey colonization and to partition the net effects of the dominant predator (damselfly larvae) on biomass pyramids into consumptive (uncaged damselfly larvae) and non-consumptive effects (caged damselfly larvae). Consumptive effects of damselflies strengthened the inversion of trophic pyramids. Non-consumptive effects, however, did not affect the shape of biomass pyramids. Instead, the rapid colonization of organisms with predominantly short CPI sustained the large biomass of top predators found in natural bromeliad ecosystems. Prey colonized bromeliads rapidly, but this high production was never visible as standing stock because damselflies reduce prey densities by more than a magnitude through direct consumption. Our study adds to the growing evidence that there are a variety of possible ways that biomass can be trophically structured. Moreover, we suggest that the strength of biomass pyramids inversion may change with the time of ecological succession as prey communities become more equitable.

Warming weakens facilitative interactions between decomposers and detritivores, and modifies freshwater ecosystem functioning.

Warming is among the major drivers of changes in biotic interactions and, in turn, ecosystem functioning. The decomposition process occurs in a chain of facilitative interactions between detritivores and microorganisms. It remains unclear, however, what effect warming may have on the interrelations between detritivores and microorganisms, and the consequences for the functioning of natural freshwater ecosystems. To address these gaps, we performed a field experiment using tank bromeliads and their associated aquatic fauna. We manipulated the presence of bacteria and detritivorous macroinvertebrates (control, "bacteria," and "bacteria + macroinvertebrates") under ambient and warming scenarios, and analyzed the effects on the microorganisms and ecosystem functioning (detritus mass loss, colored dissolved organic matter, and nitrogen flux). We applied antibiotic solution to eliminate or reduce bacteria from control bromeliads. After 60 days incubation, bacterial density was higher in the presence than in the absence of macroinvertebrates. In the absence of macroinvertebrates, temperature did not influence bacterial density. However, in the presence of macroinvertebrates, bacterial density decreased by 54% with warming. The magnitude of the effects of organisms on ecosystem functioning was higher in the combined presence of bacteria and macroinvertebrates. However, warming reduced the overall positive effects of detritivores on bacterial density, which in turn, cascaded down to ecosystem functioning by decreasing decomposition and nitrogen flux. These results show the existence of facilitative mechanisms between bacteria and detritivores in the decomposition process, which might collapse due to warming. Detritivores seem to contribute to nutrient cycling as they facilitate bacterial populations, probably by increasing nutrient input (feces) in the ecosystem. However, increased temperature mitigated these beneficial effects. Our results add to a growing research body that shows that warming can affect the structure of aquatic communities, and highlight the importance of considering the interactive effects between facilitation and climatic drivers on the functioning of freshwater ecosystems.

Food web structure shaped by habitat size and climate across a latitudinal gradient.

Habitat size and climate are known to affect the trophic structure and dynamics of communities, but their interactive effects are poorly understood. Organisms from different trophic levels vary in terms of metabolic requirements and heat dissipation. Indeed, larger species such as keystone predators require more stable climatic conditions than their prey. Likewise, habitat size disproportionally affects large-sized predators, which require larger home ranges and are thus restricted to larger habitats. Therefore, food web structure in patchy ecosystems is expected to be shaped by habitat size and climate variations. Here we investigate this prediction using natural aquatic microcosm (bromeliad phytotelmata) food webs composed of litter resources (mainly detritus), detritivores, mesopredators, and top predators (damselflies). We surveyed 240 bromeliads of varying sizes (water retention capacity) across 12 open restingas in SE Brazil spread across a wide range of tropical latitudes (-12.6° to -27.6°, ca. 2,000 km) and climates (Δ mean annual temperature = 5.3°C). We found a strong increase in predator-to-detritivore mass ratio with habitat size, which was representative of a typical inverted trophic pyramid in larger ecosystems. However, this relationship was contingent among the restingas; slopes of linear models were steeper in more stable and favorable climates, leading to inverted trophic pyramids (and top-down control) being more pronounced in environments with more favorable climatic conditions. By contrast, detritivore-resource and mesopredator-detritivore mass ratios were not affected by habitat size or climate variations across latitudes. Our results highlight that the combined effects of habitat size, climate and predator composition are pivotal to understanding the impacts of multiple environmental factors on food web structure and dynamics.

Dominant predators mediate the impact of habitat size on trophic structure in bromeliad invertebrate communities.

Local habitat size has been shown to influence colonization and extinction processes of species in patchy environments. However, species differ in body size, mobility, and trophic level, and may not respond in the same way to habitat size. Thus far, we have a limited understanding of how habitat size influences the structure of multitrophic communities and to what extent the effects may be generalizable over a broad geographic range. Here, we used water-filled bromeliads of different sizes as a natural model system to examine the effects of habitat size on the trophic structure of their inhabiting invertebrate communities. We collected composition and biomass data from 651 bromeliad communities from eight sites across Central and South America differing in environmental conditions, species pools, and the presence of large-bodied odonate predators. We found that trophic structure in the communities changed dramatically with changes in habitat (bromeliad) size. Detritivore : resource ratios showed a consistent negative relationship with habitat size across sites. In contrast, changes in predator: detritivore (prey) ratios depended on the presence of odonates as dominant predators in the regional pool. At sites without odonates, predator: detritivore biomass ratios decreased with increasing habitat size. At sites with odonates, we found odonates to be more frequently present in large than in small bromeliads, and predator: detritivore biomass ratios increased with increasing habitat size to the point where some trophic pyramids became inverted. Our results show that the distribution of biomass amongst food-web levels depends strongly on habitat size, largely irrespective of geographic differences in environmental conditions or detritivore species compositions. However, the presence of large-bodied predators in the regional species pool may fundamentally alter this relationship between habitat size and trophic structure. We conclude that taking into account the response and multitrophic effects of dominant, mobile species may be critical when predicting changes in community structure along a habitat-size gradient.