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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.

References

  1. Polis, G. A., Anderson, W. B. & Holt, R. D. Toward an integration of landscape and food web ecology: the dynamics of spatially subsidized food webs. Annu. Rev. Ecol. Syst. 28, 289–316 (1997).

    Article  Google Scholar 

  2. Doughty, C. E. et al. Global nutrient transport in a world of giants. Proc. Natl Acad. Sci. USA 113, 868–873 (2016).

    Article  ADS  PubMed  CAS  Google Scholar 

  3. Croll, D. A., Maron, J. L., Estes, J. A., Danner, E. M. & Byrd, G. V. Introduced predators transform subarctic islands from grassland to tundra. Science 307, 1959–1961 (2005).

    Article  ADS  PubMed  CAS  Google Scholar 

  4. Fukami, T. et al. Above- and below-ground impacts of introduced predators in seabird-dominated island ecosystems. Ecol. Lett. 9, 1299–1307 (2006).

    Article  PubMed  Google Scholar 

  5. Bump, J. K., Tischler, K. B., Schrank, A. J., Peterson, R. O. & Vucetich, J. A. Large herbivores and aquatic-terrestrial links in southern boreal forests. J. Anim. Ecol. 78, 338–345 (2009).

    Article  PubMed  Google Scholar 

  6. Hocking, M. D. & Reynolds, J. D. Impacts of salmon on riparian plant diversity. Science 331, 1609–1612 (2011).

    Article  ADS  PubMed  CAS  Google Scholar 

  7. Bouchard, S. S. & Bjorndal, K. A. Sea turtles as biological transporters of nutrients and energy from marine to terrestrial ecosystems. Ecology 81, 2305–2313 (2000).

    Article  Google Scholar 

  8. Jones, H. P. et al. Severity of the effects of invasive rats on seabirds: a global review. Conserv. Biol. 22, 16–26 (2008).

    Article  PubMed  Google Scholar 

  9. Otero, X. L., De La Peña-Lastra, S., Pérez-Alberti, A., Ferreira, T. O. & Huerta-Diaz, M. A. Seabird colonies as important global drivers in the nitrogen and phosphorus cycles. Nat. Commun. 9, 246 (2018).

    Article  ADS  PubMed  PubMed Central  CAS  Google Scholar 

  10. Polis, G. A. & Hurd, S. D. Linking marine and terrestrial food webs: allocthonous input from the ocean supports high secondary productivity on small islands and coastal land communities. Am. Nat. 147, 396–423 (1996).

    Article  Google Scholar 

  11. McCauley, D. J. et al. From wing to wing: the persistence of long ecological interaction chains in less-disturbed ecosystems. Sci. Rep. 2, 409 (2012).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  12. Shatova, O., Wing, S. R., Gault-Ringold, M., Wing, L. & Hoffmann, L. J. Seabird guano enhances phytoplankton production in the Southern Ocean. J. Exp. Mar. Biol. Ecol. 483, 74–87 (2016).

    Article  CAS  Google Scholar 

  13. MacNeil, M. A. et al. Recovery potential of the world’s coral reef fishes. Nature 520, 341–344 (2015).

    Article  ADS  PubMed  CAS  Google Scholar 

  14. Carr, P. in Important Bird Areas in the United Kingdom Overseas Territories (ed. Sanders, S. M.) 37–55 (Royal Society for the Protection of Birds, Sandy, 2006).

  15. Young, H. S., McCauley, D. J., Dunbar, R. B. & Dirzo, R. Plants cause ecosystem nutrient depletion via the interruption of bird-derived spatial subsidies. Proc. Natl Acad. Sci. USA 107, 2072–2077 (2010).

    Article  ADS  PubMed  Google Scholar 

  16. Szpak, P., Longstaffe, F. J., Millaire, J.-F. & White, C. D. Stable isotope biogeochemistry of seabird guano fertilization: results from growth chamber studies with maize (Zea mays). PLoS ONE 7, e33741 (2012).

    Article  ADS  PubMed  PubMed Central  CAS  Google Scholar 

  17. Lorrain, A. et al. Seabirds supply nitrogen to reef-building corals on remote Pacific islets. Sci. Rep. 7, 3721 (2017).

    Article  ADS  PubMed  PubMed Central  CAS  Google Scholar 

  18. MaMahon. K. W., Johnson, B. J., Ambrose, W. G. Ocean Ecogeochemistry: a review. Oceanogr. Mar. Biol. Annu. Rev. 51, 327–374 (2013).

    Google Scholar 

  19. Mora, C. Ecology of Fishes on Coral Reefs (Cambridge Univ. Press, Cambridge, 2015).

    Book  Google Scholar 

  20. Bellwood, D. R., Hughes, T. P., Folke, C. & Nyström, M. Confronting the coral reef crisis. Nature 429, 827–833 (2004).

    Article  ADS  PubMed  CAS  Google Scholar 

  21. Hoey, A. S. & Bellwood, D. R. Cross-shelf variation in the role of parrotfishes on the Great Barrier Reef. Coral Reefs 27, 37–47 (2008).

    Article  ADS  Google Scholar 

  22. Perry, C. T., Kench, P. S., O’Leary, M. J., Morgan, K. M. & Januchowski-Hartley, F. Linking reef ecology to island building: parrotfish identified as major producers of island-building sediment in the Maldives. Geology 43, 503–506 (2015).

    Article  ADS  Google Scholar 

  23. Sheppard, C. R. C. et al. Coral bleaching and mortality in the Chagos Archipelago. Atoll Res. Bull. 613, 1–26 (2017).

    Article  Google Scholar 

  24. Shantz, A. A. & Burkepile, D. E. Context-dependent effects of nutrient loading on the coral–algal mutualism. Ecology 95, 1995–2005 (2014).

    Article  PubMed  Google Scholar 

  25. D’Angelo, C. & Wiedenmann, J. Impacts of nutrient enrichment on coral reefs: new perspectives and implications for coastal management and reef survival. Curr. Opin. Environ. Sustain. 7, 82–93 (2014).

    Article  Google Scholar 

  26. Graham, N. A. J., Jennings, S., MacNeil, M. A., Mouillot, D. & Wilson, S. K. Predicting climate-driven regime shifts versus rebound potential in coral reefs. Nature 518, 94–97 (2015).

    Article  ADS  PubMed  CAS  Google Scholar 

  27. Gove, J. M. et al. Near-island biological hotspots in barren ocean basins. Nature Commun. 7, 10581 (2016).

    Article  ADS  CAS  Google Scholar 

  28. Keitt, B. et al. Best practice guidelines for rat eradication on tropical islands. Biol. Conserv. 185, 17–26 (2015).

    Article  Google Scholar 

  29. Brooke, M. de L. et al. Seabird population changes following mammal eradications on islands. Anim. Conserv. 21, 3–12 (2018).

    Article  Google Scholar 

  30. Hughes, T. P. et al. Spatial and temporal patterns of mass bleaching of corals in the Anthropocene. Science 359, 80–83 (2018).

    Article  ADS  PubMed  CAS  Google Scholar 

  31. Wenban-Smith, N. & Carter, M. Chagos: a History: Exploration, Exploitation, Expulsion (Chagos Conservation Trust, London, 2016).

    Google Scholar 

  32. Sheppard, C. R. C. et al. Reefs and islands of the Chagos Archipelago, Indian Ocean: why it is the world’s largest no-take marine protected area. Aquat. Conserv. 22, 232–261 (2012).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  33. Graham, N. A. J. et al. Human disruption of coral reef trophic structure. Curr. Biol. 27, 231–236 (2017).

    Article  PubMed  CAS  Google Scholar 

  34. .Readman, J. W. et al. in Coral Reefs of the United Kingdom Overseas Territories (ed. Sheppard, C. R. C.) 283–298 (Springer, Dordrecht, 2013).

  35. Bibby, C. J., Burgess, N. B. & Hill, D. A. Bird Census Techniques (Academic, London, 1992).

    Google Scholar 

  36. McGowan, A., Broderick, A. C. & Godley, B. J. Seabird populations of the Chagos Archipelago: an evaluation of IBA sites. Oryx 42, 424–429 (2008).

    Article  Google Scholar 

  37. del Hoyo, J., Elliott, A., Sargatal, J., Christie, D. A. & de Juana, E. (eds) Handbook of the Birds of the World Alive (Lynx Edicions, Barcelona, 2017).

    Google Scholar 

  38. Krzywinski, M. & Altman, N. Visualizing samples with box plots. Nat. Methods 11, 119–120 (2014).

    Article  PubMed  CAS  Google Scholar 

  39. Jennings, S. & Collingridge, K. Predicting consumer biomass, size-structure, production, catch potential, responses to fishing and associated uncertainties in the world’s marine ecosystems. PLoS ONE 10, e0133794 (2015).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  40. Aumont, O. & Bopp, L. Globalizing results from ocean in situ iron fertilization studies. Glob. Biogeochem. Cycles 20, GB2017 (2006).

    Article  ADS  CAS  Google Scholar 

  41. Mendez, L. et al. Geographical variation in the foraging behaviour of the pantropical red-footed booby. Mar. Ecol. Prog. Ser. 568, 217–230 (2017).

    Article  ADS  Google Scholar 

  42. Schmidtko, S., Johnson, G. C. & Lyman, J. M. MIMOC: A global monthly isopycnal upper-ocean climatology with mixed layers. J. Geophys. Res. 118, 1658–1672 (2013).

    Article  ADS  Google Scholar 

  43. IOC, IHC, BODC. The GEBCO Digital Atlas. (BODC, 2008).

  44. Ashmole, N. P. Body size, prey size, and ecological segregation in five sympatric tropical terns (Aves: Laridae). Syst. Zool. 17, 292–304 (1968).

    Article  Google Scholar 

  45. Harrison, C. S., Hida, T. S. & Seki, M. P. Hawaiian seabird feeding ecology. Wildl. Monogr. 85, 3–71 (1983).

    Google Scholar 

  46. Wiebe, P. H., Boyd, S. H. & Cox, J. L. Relationships between zooplankton displacement volume, wet weight, dry weight and carbon. Fish Bull. 73, 777–786 (1975).

    Google Scholar 

  47. Jennings, S. & Cogan, S. M. Nitrogen and carbon stable isotope variation in northeast Atlantic fishes and squids. Ecology 96, 2568 (2015).

    Article  Google Scholar 

  48. Martiny, A. C., Vrugt, J. A. & Lomas, M. W. Concentrations and ratios of particulate organic carbon, nitrogen, and phosphorus in the global ocean. Sci. Data 1, 140048 (2014).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  49. Martiny, A. C., Vrugt, J. A., Primeau, F. W. & Lomas, M. W. Regional variation in the particulate organic carbon to nitrogen ratio in the surface ocean. Glob. Biogeochem. Cycles 27, 723–731 (2013).

    Article  CAS  Google Scholar 

  50. Crossland, C. J., Hatcher, B. G. & Smith, S. V. Role of coral reefs in global ocean production. Coral Reefs 10, 55–64 (1991).

    Article  ADS  Google Scholar 

  51. Hatcher, B. G. Coral reef primary productivity. A hierarchy of pattern and process. Trends Ecol. Evol. 5, 149–155 (1990).

    Article  PubMed  CAS  Google Scholar 

  52. Salvatier, J., Wiecki, T. V. & Fonnesbeck, C. Probabilistic programming in Python using PyMC3. PeerJ Comput. Sci. 2, e55 (2016).

    Article  CAS  Google Scholar 

  53. Gelman, A. et al. Bayesian Data Analysis Vol. 2 (CRC, Boca Raton 2014).

    MATH  Google Scholar 

  54. Campana, S. E. Otolith science entering the 21st century. Mar. Freshw. Res. 56, 485–495 (2005).

    Article  Google Scholar 

  55. Pardo, S. A., Cooper, A. B. & Dulvy, N. K. Avoiding fishy growth curves. Methods Ecol. Evol. 4, 353–360 (2013).

    Article  Google Scholar 

  56. Wilson, S. K., Graham, N. A. J. & Polunin, N. V. C. Appraisal of visual assessments of habitat complexity and benthic composition on coral reefs. Mar. Biol. 151, 1069–1076 (2007).

    Article  Google Scholar 

  57. Letourneur, Y. Length–weight relationships of some marine fish species in Reunion Island, Indian Ocean. Naga 21, 37–39 (1998).

    Google Scholar 

  58. Wilson, S. K. et al. Exploitation and habitat degradation as agents of change within coral reef fish communities. Glob. Chang. Biol. 14, 2796–2809 (2008).

    Article  ADS  Google Scholar 

  59. Ong, L. & Holland, K. N. Bioerosion of coral reefs by two Hawaiian parrotfishes: species, size differences and fishery implications. Mar. Biol. 157, 1313–1323 (2010).

    Article  Google Scholar 

  60. McDuie, F., Weeks, S. J., Miller, M. G. R. & Congdon, B. C. Breeding tropical shearwaters use distant foraging sites when self-provisioning. Mar. Ornithol. 43, 123–129 (2015).

    Google Scholar 

  61. Calabrese, L. Foraging Ecology and Breeding Biology of Wedge-Tailed Shearwater (Puffinus Pacificus) and Tropical Shearwater (Puffinus Bailloni) on Aride Island Nature Reserve, Seychelles : Tools for Conservation. PhD thesis, Université Pierre et Marie Curie-Paris VI (2015).

  62. Pennycuick, C. J., Schaffner, F. C., Fuller, M. R., Obrecht, H. H. III & Sternberg, L. Foraging flights of the white-tailed tropicbird (Phaethon lepturus): radiotracking and doubly-labelled water. Colon. Waterbirds 13, 96–102 (1990).

    Article  Google Scholar 

  63. Jaquemet, S., Le Corre, M., Marsac, F., Potier, M. & Weimerskirch, H. Foraging habitats of the seabird community of Europa Island (Mozambique Channel). Mar. Biol. 147, 573–582 (2005).

    Article  Google Scholar 

  64. Gilardi, J. D. Sex-specific foraging distributions of brown boobies in the eastern tropical Pacific. Colon. Waterbirds 15, 148–151 (1992).

    Article  Google Scholar 

  65. Weimerskirch, H., Le Corre, M., Jaquemet, S. & Marsac, F. Foraging strategy of a tropical seabird, the red-footed booby, in a dynamic marine environment. Mar. Ecol. Prog. Ser. 288, 251–261 (2005).

    Article  ADS  Google Scholar 

  66. Surman, C. A. & Wooller, R. D. Comparative foraging ecology of five sympatric terns at a sub-tropical island in the eastern Indian Ocean. J. Zool. (Lond.) 259, 219–230 (2003).

    Article  Google Scholar 

  67. Bourne, W. R. P. & Simmons, K. E. L. The distribution and breeding success of seabirds on and around Ascension in the tropical Atlantic Ocean. Atl. Seabirds 3, 187–202 (2001).

    Google Scholar 

  68. Dunlop, J. N. Foraging range, marine habitat and diet of bridled terns breeding in Western Australia. Corella 21, 77–82 (1997).

    Google Scholar 

  69. Hulsman, K. & Smith, G. Biology and growth of the black-naped tern (Sterna sumatrana): A hypothesis to explain the relative growth rates of inshore, offshore and pelagic feeders. Emu 88, 234–242 (1988).

    Article  Google Scholar 

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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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