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.

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.

Disentangling how climate change can affect an aquatic food web by combining multiple experimental approaches.

Predicting the biological effects of climate change presents major challenges due to the interplay of potential biotic and abiotic mechanisms. Climate change can create unexpected outcomes by altering species interactions, and uncertainty over the ability of species to develop in situ tolerance or track environmental change further hampers meaningful predictions. As multiple climatic variables shift in concert, their potential interactions further complicate ecosystem responses. Despite awareness of these complexities, we still lack controlled experiments that manipulate multiple climatic stressors, species interactions, and prior exposure of species to future climatic conditions. Particularly studies that address how changes in water availability interact with other climatic stressors to affect aquatic ecosystems are still rare. Using aquatic insect communities of Neotropical tank bromeliads, we combined controlled manipulations of drought length and species interactions with a space-for-time transplant (lower elevations represent future climate) and a common garden approach. Manipulating drought length and experiment elevation revealed that adverse effects of drought were amplified at the warmer location, highlighting the potential of climatic stressors to synergistically affect communities. Manipulating the presence of omnivorous tipulid larvae showed that negative interactions from tipulids, presumably from predation, arose under drought, and were stronger at the warmer location, stressing the importance of species interactions in mediating community responses to climate change. The common garden treatments revealed that prior community exposure to potential future climatic conditions did not affect the outcome. In this powerful experiment, we demonstrated how complexities arise from the interplay of biotic and abiotic mechanisms of climate change. We stress that single species can steer ecological outcomes, and suggest that focusing on such disproportionately influential species may improve attempts at making meaningful predictions of climate change impacts on food webs.

Drought alters the trophic role of an opportunistic generalist in an aquatic ecosystem.

Abiotic change can alter species interactions by modifying species' trophic roles, but this has not been well studied. Until now, bromeliad-dwelling tipulid larvae were thought to positively affect other macroinvertebrates via a facilitative processing chain. However, under drought, we found the opposite. We performed two microcosm experiments in which we factorially manipulated water level and predation by tipulids, and measured the effects on mosquito and chironomid larvae. The experiments differed in whether high water was contrasted with low or no water, allowing us to distinguish between the effects of desiccation stress (no water) and increased encounter rates due to compression of habitat or reductions in prey mobility (low and no water). We also included a caged tipulid treatment to measure any non-consumptive effects. As well as directly reducing prey survival, reductions in water level indirectly decreased chironomid and mosquito survival by altering the trophic role of tipulids. Our results suggest that increased encounter rates with prey led to tipulids becoming predatory under simulated drought, as tipulids consumed prey under both low and no water. When water level was high, tipulids exerted negative non-consumptive effects on prey survival. Because opportunistic predators are common throughout aquatic ecosystems, the effects of drought on the trophic roles of species may be widespread. Such restructuring of food webs should be considered when attempting to predict the ecological effects of environmental change.

Trophic interactions determine the effects of drought on an aquatic ecosystem.

Species interactions can be important mediators of community and ecosystem responses to environmental stressors. However, we still lack a mechanistic understanding of the indirect ecological effects of stress that arise via altered species interactions. To understand how species interactions will be altered by environmental stressors, we need to know if the species that are vulnerable to such stressors also have large impacts on the ecosystem. As predators often exhibit certain traits that are linked to a high vulnerability to stress (e.g., large body size, long generation time), as well as having large effects on communities (e.g., top-down trophic effects), predators may be particularly likely to mediate ecological effects of environmental stress. Other functional groups, like facilitators, are known to have large impacts on communities, but their vulnerability to perturbations remains undocumented. Here, we use aquatic insect communities in bromeliads to examine the indirect effects of an important stressor (drought) on community and ecosystem responses. In a microcosm experiment, we manipulated predatory and facilitative taxa under a range of experimental droughts, and quantified effects on community structure and ecosystem function. Drought, by adversely affecting the top predator, had indirect cascading effects on the entire food web, altering community composition and decomposition. We identified the likely pathway of how drought cascaded through the food web from the top-down as drought -->predator --> shredder --> decomposition. This stress-induced cascade depended on predators exhibiting both a strong vulnerability to drought and large impacts on prey (especially shredders), as well as shredders exhibiting high functional importance as decomposers.

Drought sensitivity predicts habitat size sensitivity in an aquatic ecosystem.

Species and trophic richness often increase with habitat size. Although many ecological processes have been evoked to explain both patterns, the environmental stress associated with small habitats has rarely been considered. We propose that larger habitats may be species rich simply because their environmental conditions are within the fundamental niche of more species; larger habitats may also have more trophic levels if traits of predators render them vulnerable to environmental stress. We test this hypothesis using the aquatic insect larvae in water-filled bromeliads. In bromeliads, the probability of desiccation is greatest in small plants. For the 10 most common bromeliad insect taxa, we ask whether differences in drought tolerance and regional abundances between taxa predict community and trophic composition over a gradient of bromeliad size. First, we used bromeliad survey data to calculate the mean habitat size of occurrence of each taxon. Comparing the observed mean habitat size of occurrence to that expected from random species assembly based on differences in their regional abundances allowed us to obtain habitat size sensitivity indices (as Z scores) for the various insect taxa. Second, we obtained drought sensitivity indices by subjecting individual insects to drought and measuring the effects on relative growth rates in a mesocosm experiment. We found that drought sensitivity strongly, predicts habitat size sensitivity in bromeliad insects. However, an increase in trophic richness with habitat size could not be explained by an increased sensitivity of predators to drought, but rather by sampling effects, as predators were rare compared to lower trophic levels. This finding suggests that physiological tolerance to environmental stress can be relevant in explaining the universal increase in species with habitat size.

Indirect effects of predators control herbivore richness and abundance in a benthic eelgrass (Zostera marina) mesograzer community.

Herbivore communities can be sensitive to changes in predator pressure (top-down effects) and resource availability (bottom-up effects) in a wide range of systems. However, it remains unclear whether such top-down and bottom-up effects reflect direct impacts of predators and/or resources on herbivores, or are indirect, reflecting altered interactions among herbivore species. We quantified direct and indirect effects of bottom-up and top-down processes on an eelgrass (Zostera marina) herbivore assemblage. In a field experiment, we factorially manipulated water column nutrients (with Osmocote(™) slow-release fertilizer) and predation pressure (with predator exclusion cages) and measured the effects on herbivore abundance, richness and beta diversity. We examined likely mechanisms of community responses by statistically exploring the response of individual herbivore species to trophic manipulations. Predators increased herbivore richness and total abundance, in both cases through indirect shifts in community composition. Increases in richness occurred through predator suppression of common gammarid amphipod species (Monocorophium acherusicum and Photis brevipes), permitting the inclusion of rarer gammarid species (Aoroides columbiae and Pontogeneia rostrata). Increased total herbivore abundance reflected increased abundance of a caprellid amphipod species (Caprella sp.), concurrent with declines in the abundance of other common species. Furthermore, predators decreased beta diversity by decreasing variability in Caprella sp. abundance among habitat patches. Osmocote(™) fertilization increased nutrient concentrations locally, but nutrients dissipated to background levels within 3 m of the fertilizer. Nutrient addition weakly affected the herbivore assemblage, not affecting richness and increasing total abundance by increasing one herbivore species (Caprella sp.). Nutrient addition did not affect beta diversity. We demonstrated that assemblage-level effects of trophic manipulations on community structure are the result of distinct and often indirect responses of herbivore species. These results underscore the importance of understanding herbivore-herbivore interactions in a system commonly subjected to both eutrophication and overfishing.