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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 productivity1, yet the implications are poorly understood owing to human disruptions of natural flows2. When abundant, seabirds feeding in the open ocean transport large quantities of nutrients onto islands, enhancing the productivity of island fauna and flora3,4. 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 (δ15N) values in soils and shrubs, reflecting pelagic nutrient sources. These higher values of δ15N 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.

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Fig. 1: Seabird densities, biomass and nitrogen input to islands with and without rats in the Chagos Archipelago.
Fig. 2: Nitrogen isotope signals from islands to reefs in the presence and absence of invasive rats.
Fig. 3: Growth of herbivorous damselfish on coral reefs adjacent to islands with and without rats.
Fig. 4: Biomass and functioning of reef-fish communities adjacent to islands with and without rats.

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Acknowledgements

This research was supported by the Australian Research Council’s Centre of Excellence Program (CE140100020), a Royal Society University Research Fellowship awarded to N.A.J.G. (UF140691), and a Tier II NSERC Canada Research Chair awarded to M.A.M. We thank the British Indian Ocean Territory section of the British Foreign and Commonwealth Office for permission to conduct the study, and J. Turner for organizing the expedition. Animal ethics for fish collection were approved by James Cook University (approval number A2166). Thanks to J. Lokrantz for graphics help with Figs. 1, 2, and J. Barlow, S. Keith, and R. Evans for comments on the manuscript.

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Nature thanks Y. Cherel, N. Knowlton and S. Wing for their contribution to the peer review of this work.

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N.A.J.G. conceived the study with S.K.W.; N.A.J.G., S.K.W. and P.C. collected the data; N.A.J.G., M.A.M., S.J. and A.S.H. developed and implemented the analyses; N.A.J.G. led the writing of the manuscript with S.K.W., M.A.M., S.J., A.S.H. and P.C.

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Correspondence to Nicholas A. J. Graham.

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Extended data figures and tables

Extended Data Fig. 1 Primary production and potential prey biomass and production in areas accessible to seabirds foraging around the Chagos Islands.

a, Recorded foraging ranges for seabird species that feed on smaller prey (light tone, 0.1–9 g individual wet weight) or larger prey (dark tone, 1–50 g individual wet weight; broken lines indicate that greater ranges are expected for two of the species thus foraging area calculations assumed that the foraging range is the radius of the foraging area). b, Primary production in the foraging area. c, Modelled biomass. d, Production of fauna in the foraging area. Median and 90% uncertainty intervals on the basis of 10,000 simulations to assess the effects of parameter uncertainty39 on biomass or production estimates are shown. Biomass and production were estimated for fauna in the prey size ranges consumed by each bird species, and expressed as wet and nitrogen (N) weight, respectively.

Extended Data Table 1 Species-specific foraging locations, foraging distances and foraging observations from Chagos
Extended Data Table 2 Islands used in the study

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Graham, N.A.J., Wilson, S.K., Carr, P. et al. Seabirds enhance coral reef productivity and functioning in the absence of invasive rats. Nature 559, 250–253 (2018). https://doi.org/10.1038/s41586-018-0202-3

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