Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Atolls are globally important sites for tropical seabirds

Nature Ecology & Evolution volume 8, pages 1907–1915 (2024)Cite this article

Subjects

Abstract

Seabirds play critical roles on islands. By catalysing terrestrial and marine productivity through guano nutrient input, seabirds support natural island functioning. In the Indo-Pacific, atolls comprise one-third of all islands but only ~0.02% of island area. The importance of atolls as seabird nesting grounds has been historically neglected except on a few key atolls. We compiled a global dataset of seabird surveys on atolls and modelled seabird distribution and nutrient deposition on all Indo-Pacific atolls. We found that atolls are breeding sites for 37 species, ranging from a few dozen to more than 3 million individuals per atoll. In total, an estimated 31.2 million seabirds nest on atolls, or ~25% of the tropical seabirds of the world. For 14 species, more than half of their global populations nest on atolls. Seabirds forage more than 10,000–100,000 km² around an atoll and deposit, on average, 65,000 kg N and 11,000 kg P per atoll per year, thus acting as major nutrient pumps within the tropical Indo-Pacific. Our findings reveal the global importance of atolls for tropical seabirds. Given global change, conservation will have to leverage atoll protection and restoration to preserve a relevant fraction of the tropical seabirds of the world.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on SpringerLink
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: Seabird colonies on the 280 Indo-Pacific atolls.
Fig. 2: Percentage of the global population of seabird species found on atolls.
Fig. 3: Seabird-derived nitrogen inputs on atolls.
Fig. 4: The reciprocal relationship between seabirds and atolls.

Similar content being viewed by others

Data availability

All raw data can be accessed under https://doi.org/10.5281/zenodo.12622076 (ref. 61). Marine data were obtained from EU Copernicus Marine Service Information (https://data.marine.copernicus.eu/products last accessed 24 May 2023). Tropical cyclone and storm data were obtained from the Historical Hurricane Tracks database of NOAA (https://coast.noaa.gov/hurricanes/ last accessed 25 Feb 2023). Data on ENSO-driven rainfall anomalies were obtained from the Global Precipitation Climatology Project of JISAO (http://research.jisao.washington.edu/data/gpcp/ last accessed 24 May 2023). Seabird trait data were from the AVONET trait database (https://opentraits.org/datasets/avonet last accessed 1 December 2023).

Code availability

All statistical code can be accessed from https://doi.org/10.5281/zenodo.12622076 (ref. 61).

References

  1. Sandin, S. A. et al. Harnessing island-ocean connections to maximise marine benefits of island conservation. Proc. Natl Acad. Sci. USA 119, e2122354119 (2022).

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  3. Grant, M. L., Bond, A. L. & Lavers, J. L. The influence of seabirds on their breeding, roosting, and nesting grounds: a systematic review and meta-analysis. J. Anim. Ecol. 91, 1266–1289 (2022).

    Article  PubMed  Google Scholar 

  4. 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 phosphorous cycle. Nat. Commun. 9, 246 (2018).

    Article  PubMed  Google Scholar 

  5. Anderson, W. B. & Polis, G. A. Nutrient fluxes from water to land: seabirds affect plant nutrient status on Gulf of California islands. Oecologia 118, 324–332 (1999).

    Article  PubMed  Google Scholar 

  6. Nunn, P. D., Kumar, L., Eliot, I. & McLean, R. F. Classifying Pacific islands. Geosci. Lett. 3, 7 (2016).

    Article  Google Scholar 

  7. Goldberg, W. M. Atolls of the world: revisiting the original checklist. Atoll Res. Bull. 610, 1–47 (2016).

    Article  Google Scholar 

  8. Stoddart, D. R. Biogeography of the tropical Pacific. Pac. Sci. 46, 276–293 (1992).

    Google Scholar 

  9. McMahon, A. & Santos, I. R. Nitrogen enrichment and speciation in a coral reef lagoon driven by groundwater inputs of bird guano. J. Geophys. Res. Oceans 122, 7218–7236 (2017).

    Article  Google Scholar 

  10. 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  CAS  PubMed  Google Scholar 

  11. Aharon, P. & Veeh, H. H. Isotope studies of insular phosphates explain atoll phosphatization. Nature 309, 614–617 (1984).

    Article  CAS  Google Scholar 

  12. Gillham, M. E. Vegetation of sea and shore-bird colonies on Aldabra atoll. Atoll Res. Bull. 200, 1–20 (1977).

    Article  Google Scholar 

  13. Appoo, J., Bunbury, N., Jaquemet, S. & Graham, N. A. J. Seabird nutrient subsidies enrich mangrove ecosystems and are exported to nearby coastal habitats. iScience 27, 109404 (2024).

    Article  PubMed  Google Scholar 

  14. Benkwitt, C. E., Carr, P., Wilson, S. K. & Graham, N. A. J. Seabird diversity and biomass enhance cross-ecosystem nutrient subsidies. Proc. R. Soc. B. 289, 20220195 (2022).

    Article  CAS  PubMed  Google Scholar 

  15. Graham, N. A. J. et al. Seabirds enhance coral reef productivity and functioning in the absence of invasive rats. Nature 559, 250–253 (2018).

    Article  CAS  PubMed  Google Scholar 

  16. Savage, C. Seabird nutrients are assimilated by corals and enhance coral growth rates. Sci. Rep. 9, 4284 (2019).

    Article  PubMed  Google Scholar 

  17. 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  Google Scholar 

  18. Benkwitt, C. E. et al. Seabirds boost coral reef resilience. Sci. Adv. 9, eadj0390 (2023).

    Article  CAS  PubMed  Google Scholar 

  19. Steibl, S. et al. Rethinking atoll futures: local resilience to global challenges. Trends Ecol. Evol. 39, 258–266 (2024).

    Article  PubMed  Google Scholar 

  20. Berr, T. et al. Seabird and reef conservation must include coral islands. Trends Ecol. Evol. 38, 490–494 (2023).

    Article  PubMed  Google Scholar 

  21. Barnett, J. et al. Nature-based solutions for atoll habitability. Philos. Trans. R. Soc. B 377, 20210124 (2022).

    Article  Google Scholar 

  22. Dias, M. P. et al. Threats to seabirds: a global assessment. Biol. Conserv. 237, 525–537 (2019).

    Article  Google Scholar 

  23. Courchamp, F., Hoffmann, B. D., Russell, J. C., Leclerc, C. & Bellard, C. Climate change, sea-level rise, and conservation: keeping island biodiversity afloat. Trends Ecol. Evol. 29, 127–130 (2014).

    Article  PubMed  Google Scholar 

  24. Guidelines for Using a Global Standard for the Identification of Key Biodiversity Areas. Version 1.1 (IUCN, 2020).

  25. Bar-On, Y. M., Phillips, R. & Milo, R. The biomass distribution on Earth. Proc. Natl Acad. Sci. USA 115, 6506–6511 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Birds of the World (Cornell Lab of Ornithology, 2020); https://birdsoftheworld.org/bow/home

  27. IUCN Red List for Birds (BirdLife International, 2018); https://www.birdlife.org

  28. Wilson, L. J. et al. Modelling the spatial distribution of ammonia emissions from seabirds in the UK. Environ. Poll. 131, 173–185 (2004).

    Article  CAS  Google Scholar 

  29. Spennemann, D. H. R. Japanese economic exploitation of central Pacific seabird populations, 1898–1915. Pac. Stud. 21, 1–41 (1998).

    Google Scholar 

  30. Trevail, A. M. et al. Tracking seabird migration in the tropical Indian Ocean reveals basin-scale conservation need. Curr. Biol. 33, 5247–5256 (2023).

    Article  CAS  PubMed  Google Scholar 

  31. Thaxter, C. B. et al. Seabird foraging ranges as a preliminary tool for identifying candidate Marine Protected Areas. Biol. Conserv. 156, 53–61 (2012).

    Article  Google Scholar 

  32. de la Peña-Lastra, S. Seabird droppings: effects on a global and local level. Sci. Total Environ. 754, 142148 (2021).

    Article  PubMed  Google Scholar 

  33. Chown, S. L., Gaston, K. J. & Williams, P. H. Global patterns in species richness of pelagic seabirds: the Procellariiformes. Ecography 21, 342–350 (1998).

    Article  Google Scholar 

  34. Paleczny, M., Hammill, E., Karpouzi, V. & Pauly, D. Population trends of the World’s monitored seabirds, 1950–2010. PLoS ONE 10, e0129342 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  35. Reynolds, M. H. et al. Will the effect of sea-level rise create ecological traps for Pacific island seabirds? PLoS ONE 10, e0136773 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  36. Stoddart, D. R., Benson, C. W. & Peake, J. F. Ecological change and effects of phosphate mining on Assumption Island. Atoll Res. Bull. 136, 121–146 (1970).

    Google Scholar 

  37. Choisnard, N. et al. Tracing the fate of seabird-derived nitrogen in a coral reef using nitrate and coral skeleton nitrogen isotopes. Limnol. Oceanogr. 9999, 1–16 (2024).

    Google Scholar 

  38. Heywood, K. J., Stevens, D. P. & Bigg, G. R. Eddy formation behind the tropical island of Aldabra. Deep-Sea Res. 43, 555–578 (1996).

    Article  Google Scholar 

  39. Altieri, K. E., Fawcett, S. E. & Hastings, M. G. Reactive nitrogen cycling in the atmosphere and ocean. Ann. Rev. Earth Planet Sci. 49, 523–550 (2021).

    Article  CAS  Google Scholar 

  40. Riddick, S. N. et al. Global assessment of the effect of climate change on ammonia emissions from seabirds. Atmos. Environ. 184, 212–223 (2018).

    Article  CAS  Google Scholar 

  41. Longley-Wood, K., Engels, M., Lafferty, K. D., McLaughlin, J. P. & Wegmann, A. Transforming Palmyra atoll to native-tree dominance will increase net carbon storage and reduce dissolved organic carbon reef runoff. PLoS ONE 17, e0262621 (2022).

    Article  CAS  PubMed  Google Scholar 

  42. Anderson, R. C. & Shimal, M. A checklist of birds of the Maldives. Indian BIRDS Monogr. 3, 1–52A (2020).

    Google Scholar 

  43. Steibl, S. & Laforsch, C. The importance of the Maldives as a wintering ground for migratory birds of the Central Asian flyway. J. Asian Ornith. 37, 80–87 (2021).

    Google Scholar 

  44. Berr, T. et al. Human visitation disrupts natural determinants of breeding seabird communities on coral reef islands. Glob. Ecol. Conserv. 48, e02732 (2023).

    Google Scholar 

  45. Russell, J. C., Meyer, J.-Y., Holmes, N. D. & Pagad, S. Invasive alien species on islands: impacts, distribution, interactions and management. Environ. Conserv. 44, 359–370 (2017).

    Article  Google Scholar 

  46. Ashmole, N. P. The regulation of numbers of tropical oceanic birds. Ibis 103, 458–473 (1963).

    Article  Google Scholar 

  47. Carr, P. et al. Potential benefits to breeding seabirds of converting abandoned coconut plantations to native habitats after invasive predator eradication. Restor. Ecol. 29, e13386 (2021).

    Article  Google Scholar 

  48. Spatz, D. R. et al. The global contribution of invasive vertebrate eradication as a key island restoration tool. Sci. Rep. 12, 13391 (2022).

    Article  CAS  PubMed  Google Scholar 

  49. Spatz, D. R. et al. Tracking the global application of conservation translocation and social attraction to reverse seabird declines. Proc. Natl Acad. Sci. USA 120, e2214574120 (2023).

    Article  CAS  PubMed  Google Scholar 

  50. Fosberg, F. R. Classification of emergent reef surfaces. Atoll Res. Bull. 292, 29–36 (1985).

    Google Scholar 

  51. Stoddart, D. R. & Steers, J. A. in Biology and Geology of Coral Reefs (eds Jones, O. A. & Endean, R.) 59–105 (Academic Press, 1977).

  52. Amerson, A. B. Jr. Ornithology of the Marshall and Gilbert islands. Atoll Res. Bull. 127, 1–348 (1969).

    Article  Google Scholar 

  53. Schreiber, R. W. & Schreiber, E. A. Central Pacific seabirds and the El Niño Southern Oscillation: 1982 to 1983 perspectives. Science 225, 713–716 (1984).

    Article  CAS  PubMed  Google Scholar 

  54. Harper, G. A. & Bunbury, N. Invasive rats on tropical islands: their population biology and impacts on native species. Glob. Ecol. Conserv. 3, 607–627 (2015).

    Google Scholar 

  55. Bezanson, J., Karpinski, S., Shah, V. B. & Edelman, A. Julia: a fast dynamic language for technical computing. Preprint at https://doi.org/10.48550/arXiv.1209.5145 (2012).

  56. Ge, H., Xu, K. & Ghahramani, Z. Turing: a language for flexible probabilistic inference. PMLR 84, 1682–1690 (2018).

    Google Scholar 

  57. Dray, S. et al. adespatial: multivariate multiscale spatial analysis. R package version 0.3-3 https://cran.r-project.org/web/packages/adespatial/index.html (2018).

  58. Tobias, J. A. et al. AVONET: morphological, ecological and geographical data for all birds. Ecol. Lett. 25, 581–597 (2022).

    Article  PubMed  Google Scholar 

  59. Schmidt, S. et al. Atmospheric concentrations of ammonia and nitrogen dioxide at a tropical coral cay with high seabird density. J. Environ. Monit. 12, 460–465 (2010).

    Article  CAS  PubMed  Google Scholar 

  60. Miller, M. et al. Refining seabird marine protected areas by predicting habitat inside foraging range—a case study from the global tropics. Preprint at Authorea https://doi.org/10.22541/au.168903191.10497767/v1 (2023).

  61. Steiger, S. Atoll-seabirds: pre-publication release. Zenodo 10.5281/zenodo.12622076 (2024).

Download references

Acknowledgements

Financial support for S. Steibl was provided by a Walter Benjamin-fellowship (STE 3139/1) of the German Research Foundation.

Author information

Author notes

  1. These authors contributed equally: Sebastian Steibl, Simon Steiger.

Authors and Affiliations

  1. School of Biological Sciences, University of Auckland, Auckland, New Zealand

    Sebastian Steibl & James C. Russell

  2. Department of Medicine Solna, Karolinska Institute, Stockholm, Sweden

    Simon Steiger

  3. The Nature Conservancy, Sacramento, CA, USA

    Alex S. Wegmann & Nick D. Holmes

  4. Ecology, Evolution and Marine Biology, University of California, Santa Barbara, CA, USA

    Hillary S. Young

  5. Institute of Zoology, Zoological Society of London, London, UK

    Peter Carr

Authors
  1. Sebastian Steibl
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Simon Steiger
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Alex S. Wegmann
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Nick D. Holmes
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Hillary S. Young
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Peter Carr
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. James C. Russell
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

S. Steibl and S. Steiger designed the study and conducted the model development and data analysis. S. Steibl compiled the datasets. All authors contributed to the interpretation, writing and proofing of the manuscript and have agreed to the submission of the final version.

Corresponding author

Correspondence to Sebastian Steibl.

Ethics declarations

Competing interests

The authors declare no competing interests.

Peer review

Peer review information

Nature Ecology & Evolution thanks Sophie Laran and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

Additional information

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Extended data

Extended Data Fig. 1 Atoll contribution to global seabird populations.

Colour code indicates which atolls host a colony of a seabird species that constitutes >1% of the estimated global population of this species. Bird icons indicate to which taxonomic group the species on a given atoll belongs to (albatross, boobies, frigatebirds, petrel/shearwater, tern, tropicbird).

Extended Data Fig. 2 Seabird-driven phosphorous input on atolls.

For each Indo-Pacific atoll (n = 280), the estimated breeding seabird-derived phosphorous input in kg P per year is calculated using bioenergetic models (a). Each data point shows the P input for an atoll, with boxplots indicating the 5%, 25%, median, 75%, and 95% quantiles, and violin plot the underlying probability density distribution. For the six species groups of seabirds, the imported phosphorous per atoll-colony is presented (b). Boxplots indicate the 5%, 25%, median, 75%, and 95% quantiles of the P input per atoll and species.

Supplementary information

Supplementary Information

Supplementary data, including Figs. 1–9 and Tables 1–4.

Reporting Summary

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Steibl, S., Steiger, S., Wegmann, A.S. et al. Atolls are globally important sites for tropical seabirds. Nat Ecol Evol 8, 1907–1915 (2024). https://doi.org/10.1038/s41559-024-02496-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41559-024-02496-4

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing