This blog post is provided by Pablo Augusto P. Antiqueira. Pablo is a shortlisted candidate for the 2022 Elton Prize, for work on Warming and top predator loss drive direct and indirect effects on multiple trophic groups within and across ecosystems.

This blog post is also available in Portuguese.

The current era is profoundly marked by anthropogenic changes, causing ecological and geological alterations. High species extinction rates and climate change are among the main anthropic consequences that harm and modify ecosystems. Warming, for example, predicted for the following decades, may directly affect biodiversity due to the physiological limitations of organisms or through changes in trophic relationships (e.g., predator-prey interactions), altering the patterns of species diversity and ecosystem functioning. However, some important biological groups, such as predators, may be more sensitive to these impacts, and their extinctions can reorganize or rewire the food web interactions with a variety of cascading indirect effects on the ecosystem functioning.

Considering that the flow of matter and energy connect ecosystems, often through organisms that move between different compartments, anthropogenic effects can propagate between multiple trophic levels within and across ecosystems. For example, changes in aquatic ecosystems can affect aquatic species of different trophic levels, as well as the interaction between them. In addition, many aquatic organisms (e.g., insects) have complex life cycles, with an aquatic larval phase and a terrestrial adult phase – and any alterations in the aquatic ecosystem may decrease or increase the emergence of these organisms to the terrestrial ecosystem, thus affecting terrestrial consumers that feed on them (e.g., spiders and ants). Therefore, anthropogenic changes may be more intense than previously thought, with direct and indirect effects that extend to multiple trophic levels within and across ecosystems.

Freshwater environments are susceptible to climate change and biodiversity loss, with high species extinction rates. Given this scenario, there is a critical need for studies that empirically and objectively address the effect of environmental and biotic changes on biodiversity in freshwater systems and their connection with terrestrial ecosystems. However, one of the significant limitations of carrying out empirical studies on the impact of climate change on ecosystems is the difficulty of conducting field experiments (i.e., realistically) while identifying the ecological mechanisms that occur in the system. Tank-bromeliads (Bromeliacea), an almost exclusively neotropical plant, are naturally well-suited micro ecosystems for such investigations as they support a rich fauna of micro-organisms (e.g., bacteria, algae, fungi, and microfauna) and metazoans (multiple groups of invertebrates, mainly arthropods) in a detritus-based food web (Figure 1). Furthermore, tank-bromeliads are composed of two different compartments—the aquatic and terrestrial —which are interconnected by insect emergence used as resources by various terrestrial predators with varying strategies of hunting that use bromeliads as foraging sites (e.g., cursorial and web-building spiders, ants, centipedes) (Figure 1). 

Our study evaluated experimentally, using tank bromeliads as a study system (Figure 2), how the increase in temperature, predicted for the following decades, and trophic downgrading caused by top predator losses, affect the trophic relationships in three connected compartments of the food web: i) aquatic microbiota (algae, ciliates, flagellates, and zooplankton), ii) aquatic macro-organisms (macroinvertebrates) and iii) multiple terrestrial predators from different functional groups, from more active (cursorial spiders and ants) to stationary ones (e.g., web-building spiders). We found that impacts of warming and trophic downgrading on each aquatic (macro and microorganisms) and terrestrial food web compartments depended on the functional group, trophic level, and the community component investigated, i.e., abundance or richness. 

Figure 2. Images from top left to bottom right: 1. Pablo Antiqueira sampling water from tank-bromeliad to evaluate communities of aquatic microfauna and algae community. Photo credits: Gustavo Migliorini. 2-5. Experimental bromeliads in an Atlantic Rainforest understorey, as well as the details of tank-bromeliad top view and the aquarium heaters and temperature sensor inside the tanks. Photo credits: Pablo Antiqueira. 6. A damselfly larva (Leptagrion andromache), a top predator inhabiting tank-bromeliad ecosystem, preying on a beetle larva (Scirtidae, a common detritivore group inhabiting this ecosystem). Photo creditz: Pablo Antiqueira

The trophic downgrading substantially impacted all three compartments of the food web. In the aquatic macrofauna compartment, trophic downgrading increased the richness and abundance of filter-feeding organisms (mosquito larvae – Culicidae), directly and indirectly, through increased detritivore richness, probably through a facilitative interaction. For example, detritivore activity generates fine particles of organic matter, feces, and microorganisms that feed on this material, which filter feeders consume. Thus, the increase in aquatic detritivores after the extinction of top predators also benefited filter-feeding organisms, increasing their richness and abundance. On the other hand, the trophic downgrading decreased algal richness in the microfauna compartment by decreasing nutrient input from the predators’ biological activities (e.g., feces and prey carcasses).

Furthermore, the increase in aquatic filter feeders due to trophic downgrading triggered an increase in terrestrial predators through a cascade effect across ecosystems. The more active terrestrial predators responded more to aquatic trophic downgrading via an increase in the macrofauna species richness than more stationary terrestrial predators. Warming did not affect aquatic micro-organisms or macro-organisms but increased the abundance of web-building terrestrial predators. Our results provide novel evidence on how warming and trophic downgrading can affect the food web of macro- and micro-organisms, not only in the aquatic ecosystem but also in the adjacent terrestrial ecosystem through cross-ecosystem effects.

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