Seabirds enhance coral reef productivity and functioning in the absence of invasive rats

Abstract

Biotic connectivity between ecosystems can provide major transport of organic matter and nutrients, influencing ecosystem structure and productivity, yet the implications are poorly understood owing to human disruptions of natural flows. When abundant, seabirds feeding in the open ocean transport large quantities of nutrients onto islands, enhancing the productivity of island fauna and flora. Whether leaching of these nutrients back into the sea influences the productivity, structure and functioning of adjacent coral reef ecosystems is not known. Here we address this question using a rare natural experiment in the Chagos Archipelago, in which some islands are rat-infested and others are rat-free. We found that seabird densities and nitrogen deposition rates are 760 and 251 times higher, respectively, on islands where humans have not introduced rats. Consequently, rat-free islands had substantially higher nitrogen stable isotope (δN) values in soils and shrubs, reflecting pelagic nutrient sources. These higher values of δN were also apparent in macroalgae, filter-feeding sponges, turf algae and fish on adjacent coral reefs. Herbivorous damselfish on reefs adjacent to the rat-free islands grew faster, and fish communities had higher biomass across trophic feeding groups, with 48% greater overall biomass. Rates of two critical ecosystem functions, grazing and bioerosion, were 3.2 and 3.8 times higher, respectively, adjacent to rat-free islands. Collectively, these results reveal how rat introductions disrupt nutrient flows among pelagic, island and coral reef ecosystems. Thus, rat eradication on oceanic islands should be a high conservation priority as it is likely to benefit terrestrial ecosystems and enhance coral reef productivity and functioning by restoring seabird-derived nutrient subsidies from large areas of ocean.

The meaning of the term ‘function’ in ecology: A coral reef perspective

“…consumption rate per individual), to provide an overall estimate of the magnitude of a function over a unit area (e.g. rates of grazing on reefs or bioerosion m −2 ) (Bellwood et al, ; Graham et al, ; Perry & Alvarez‐Filip, ). The advantage of this approach is that functional impacts can be estimated at an individual, population, species, functional group or community level and can be expressed as a rate‐based process in terms of its spatial impact (function per unit area).…”

Coral reef ecology in the Anthropocene

“…These so‐called “internal waves” can raise nutrient concentrations in the shallows (Aston et al, ; Leichter, Stewart, & Miller, ; Wang, Dai, & Chen, ), which in turn can promote heterotrophic feeding and growth rates in corals (Fox et al, ; Leichter & Salvatore, ; Williams et al, ), and ultimately drive broad spatial transitions in benthic functional group dominance around islands (Aston et al, ). Coral reefs are also hydrodynamically connected by additional physical processes such as lagoonal outflow and surface downwelling that can move allochthonous nutrient sources between reef habitats (Williams et al, ) and, in the absence of confounding local human impacts, enhance reef productivity and function (Graham et al, ).…”

“…Humans are also re‐structuring coral reef microbial communities (Kelly et al, ), and promoting the abundance of disease‐causing bacteria and viruses (Dinsdale et al, ). Remarkably, human‐introduced invasive rats can lower fish growth rates and levels of herbivory on reefs by predating on seabirds that would otherwise deliver offshore nutrient subsidies to shallow waters bordering the islands (Graham et al, ).…”

The good, the bad, but not the ugly

“…Nick Graham, one of our Assistant Editors, was recently lead author for a remarkable paper in Nature (Graham et al ., ) which revealed the remarkable biotic connectivity of terrestrial and aquatic ecosystems in the northern atolls of the Chagos Archipelago, located in the central Indian Ocean. The importance of spatial subsidies of nutrients among disparate ecosystems in a recipient system was recently demonstrated in Journal of Fish Biology (Samways et al ., ), where marine‐derived nutrients were shown to enter river ecosystems through anadromous fishes.…”

“…However, Graham et al . () linked three ecosystems: rats, birds and fish. In short, his international group of researchers showed that coral islands that are rat‐free have a >750‐times greater seabird density and a 250‐times greater nitrogen deposition rate than rat‐infested islands.…”