Seabirds subsidize terrestrial food webs and coral reefs in a tropical rat-invaded archipelago.

Abstract

Allochthonous resource fluxes mediated by organisms crossing ecosystem boundaries may be essential for supporting the structure and function of resource-limited environments, such as tropical islands and surrounding coral reefs. However, invasive species, such as black rats, thrive on tropical islands and disrupt the natural pathways of nutrient subsidies by reducing seabird colonies. Here, we used stable isotopes of nitrogen and carbon to examine the role of seabirds in subsidizing the terrestrial food webs and adjacent coral reefs in the Abrolhos Archipelago, Southwest Atlantic Ocean. By sampling invasive rats and multiple ecosystem compartments (soil, plants, grasshoppers, tarantulas, and lizards) within and outside seabird colonies, we showed that seabird subsidies led to an overall enrichment in 15 N across the food web on islands. However, contrary to other studies, δ15 N values were consistently lower within the seabird colonies, suggesting that a higher seabird presence might produce a localized depletion in 15 N in small islands influenced by seabirds. In contrast, the nitrogen content (%N) in plants and soils was higher inside the colonies, corresponding to a higher effect of seabirds at the base of the trophic web. Among consumers, lizards and invasive rats seemed to obtain allochthonous resources from subsidized terrestrial organisms outside the colony. Inside the colony, however, they showed a more direct consumption of marine matter, suggesting that subsidies benefit these native and invasive animals both directly and indirectly. Nonetheless, in coral reefs, scleractinian corals assimilated seabird-derived nitrogen only around the two smaller and lower-elevation islands, as demonstrated by the substantially higher δ15 N values in relation to the reference areas. This provides evidence that island morphology may influence the incorporation of seabird nutrients in coral reefs around rat-invaded islands, likely because guano lixiviation toward seawater is facilitated in small and low-elevation terrains. Overall, these results showed that seabirds affected small islands across all trophic levels within and outside colonies and that these effects spread outward to coral reefs, evidencing resiliency of seabird subsidies even within a rat-invaded archipelago. Because rats are consumers of seabird chicks and eggs, however, rat eradication could potentially benefit the terrestrial and nearshore ecosystems through increased subsides carried by seabirds.