A seascape dichotomy in the role of small consumers for coral reef energy fluxes

Biogeochemical fluxes through ecological communities underpin the functioning of ecosystems worldwide. These fluxes are often heavily influenced by small-bodied consumers, such as insects, worms, mollusks, or small vertebrates, which transfer energy and nutrients from autotrophic sources to larger animals. Although coral reefs are one of the most productive ecosystems in the world, we know relatively little about how small consumers make energy available to larger predators and how their roles may vary across reefs. Here, we use community-scale collections of small, bottom-dwelling ("cryptobenthic") reef fishes along with size spectrum analyses, stable isotopes, and demographic modeling to examine their role in harnessing and transferring carbon in two distinct coral reef habitats. Using a comprehensive dataset from Mo'orea (French Polynesia), we demonstrate that, despite only being separated by a narrow reef crest, forereef and backreef habitats harbor distinct communities of cryptobenthic fishes that play vastly divergent roles in carbon transfer. Forereef communities in Mo'orea are depauperate, largely consisting of predatory and planktivorous species that have comparatively high standing biomass (both individually and collectively). In these communities, the combination of size spectra and isotope values suggests important contributions of pelagic subsidies, but the rate of biomass production and turnover (i.e., the rate at which biomass is replenished) is relatively low. In contrast, cryptobenthic fish communities in the backreef are characterized by high abundances of the smallest bodied species, forming a traditional bottom-heavy trophic pyramid that is fueled by benthic autotrophs. In these communities, benthic productivity fuels rapid production and turnover of fish biomass, while pelagic energy channels are notably less productive. Our integrative approach demonstrates the utility of combining multiple methods (e.g., isotopically informed demographic models) to trace energy fluxes through small consumer communities in complex ecosystems. Furthermore, our results highlight that coral reef productivity dynamics are highly habitat-dependent and the role of the smallest coral reef consumers may be most pronounced in shallow systems with limited connectivity to the open ocean.

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