Skip to main content

Thank you for visiting 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:

Oil exposure disrupts early life-history stages of coral reef fishes via behavioural impairments

A Publisher Correction to this article was published on 02 August 2017

This article has been updated


Global demand for energy and oil-based products is progressively introducing petrogenic polycyclic aromatic hydrocarbons (PAHs) into sensitive marine environments, primarily from fossil-fuel exploration, transport, and urban and industrial runoff. These toxic pollutants are found worldwide, yet the long-term ecological effects on coral reef ecosystems are unknown. Here, we demonstrate that oil exposure spanning PAH concentrations that are environmentally relevant for many coastal marine ecosystems (≤5.7 μg l−1), including parts of the Great Barrier Reef, Red Sea, Asia and the Caribbean, causes elevated mortality and stunted growth rates in six species of pre-settlement coral reef fishes, spanning two evolutionarily distinct families (Pomacentridae and Lethrinidae). Furthermore, oil exposure alters habitat settlement and antipredator behaviours, causing reduced sheltering, shoaling and increased risk taking, all of which exacerbate predator-induced mortality during recruitment. These results suggest a previously unknown path, whereby oil and PAH exposure impair higher-order cognitive processing and behaviours necessary for the successful settlement and survival of larval fishes. This emphasizes the risks associated with industrial activities within at-risk ecosystems.

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

Access options

Buy this article

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

Figure 1: Schematic life cycle of coral reef fishes.
Figure 2: Excess mortality of crude oil HEWAF-exposed larval coral reef fishes.
Figure 3: Habitat settlement choice of crude oil HEWAF-exposed larval coral reef fish.
Figure 4: Antipredatory behaviour of crude oil HEWAF-exposed larval coral reef fishes during settlement.

Similar content being viewed by others

Change history

  • 02 August 2017

    In the version of this Article originally published, a statistic relating to the northern Great Barrier Reef was attributed to the Great Barrier Reef as a whole. The sentence should have read ‘In 2016 alone, more than 35% of corals on the northern Great Barrier Reef are estimated to have died following the worst bleaching event ever recorded’. This has been corrected in all versions of the Article.


  1. Readman, J. W. et al. Petroleum and PAH contamination of the Black Sea. Mar. Pollut. Bull. 44, 48–62 (2002).

    Article  CAS  PubMed  Google Scholar 

  2. Douben, P. E. PAHs: An Ecotoxicological Perspective (John Wiley & Sons, Chichester, 2003).

  3. Anderson, C. M., Mayes, M. & LaBelle, R. Update of Occurrence Rates for Offshore Oil Spills (OCS, BOEM and BSSE, 2012);

  4. Neff, J. M. in Sea Mammals and Oil: Confronting the Risks (eds Geraci, J. R. & St Aubin, D. J.) 1–34 (Academic Press, San Diego, 1990).

  5. Wang, Z. et al. Characteristics of Spilled Oils, Fuels, and Petroleum Products: 1. Composition and Properties of Selected Oils (US Environmental Protection Agency, BiblioGov, 2003).

  6. Carls, M. G., Rice, S. D. & Hose, J. E. Sensitivity of fish embryos to weathered crude oil: Part I. Low-level exposure during incubation causes malformations, genetic damage, and mortality in larval pacific herring (Clupea pallasi). Environ. Toxicol. Chem. 18, 481–493 (1999).

    Article  CAS  Google Scholar 

  7. Irie, K. et al. Effect of heavy oil on the development of the nervous system of floating and sinking teleost eggs. Mar. Pollut. Bull. 63, 297–302 (2011).

    Article  CAS  PubMed  Google Scholar 

  8. Negri, A. P. et al. Acute ecotoxicology of natural oil and gas condensate to coral reef larvae. Sci. Rep. 6, 21153 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Mager, E. M. et al. Acute embryonic or juvenile exposure to Deepwater Horizon crude oil impairs the swimming performance of mahi-mahi (Coryphaena hippurus). Environ. Sci. Technol. 48, 7053–7061 (2014).

    Article  CAS  PubMed  Google Scholar 

  10. Esbaugh, A. J. et al. The effects of weathering and chemical dispersion on Deepwater Horizon crude oil toxicity to mahi-mahi (Coryphaena hippurus) early life stages. Sci. Total Environ. 543, 644–651 (2016).

    Article  CAS  PubMed  Google Scholar 

  11. Basheer, C., Obbard, J. P. & Lee, H. K. Persistent organic pollutants in Singapore’s coastal marine environment: Part II, sediments. Water Air Soil Pollut. 149, 315–325 (2003).

    Article  CAS  Google Scholar 

  12. El-Sikaily, A., Khaled, A., El Nemr, A., Said, T. O. & Abd-Alla, A. M. Polycyclic aromatic hydrocarbons and aliphatics in the coral reef skeleton of the Egyptian Red Sea coast. Bull. Environ. Contam. Toxicol. 71, 1252–1259 (2003).

    Article  CAS  PubMed  Google Scholar 

  13. Jones, R. Environmental contamination associated with a marine landfill (‘seafill’) beside a coral reef. Mar. Pollut. Bull. 60, 1993–2006 (2010).

    Article  CAS  PubMed  Google Scholar 

  14. Kroon, F. J. et al. Identification, Impacts, and Prioritisation of Emerging Contaminants Present in the GBR and Torres Strait Marine Environments (Australian Government, 2015);

  15. Cisneros-Montemayor, A. M., Kirkwood, F. G., Harper, S., Zeller, D. & Sumaila, U. R. Economic use value of the Belize marine ecosystem: potential risks and benefits from offshore oil exploration. Nat. Resour. Forum 37, 221–230 (2013).

    Article  Google Scholar 

  16. Burns, K. A. PAHs in the Great Barrier Reef Lagoon reach potentially toxic levels from coal port activities. Estuar. Coast. Shelf Sci. 144, 39–45 (2014).

    Article  CAS  Google Scholar 

  17. Harriss, R. Arctic offshore oil: great risks in an evolving ocean. Environ. Sci. Policy Sust. Dev. 58, 18–29 (2016).

    Article  Google Scholar 

  18. Conservation International Economic Values of Coral Reefs, Mangroves, and Seagrasses: A Global Compilation (Center for Applied Biodiversity Science, 2008);

  19. Wilkinson, C. Status of Coral Reefs of the World: 2008 (Global Coral Reef Monitoring Network and Reef and Rainforest Research Centre, 2008);

  20. Jackson, J. B. C., Donovan, M. K., Cramer, K. L. & Lam, V. V. Status and Trends of Caribbean Coral Reefs: 1970–2012 (Global Coral Reef Monitoring Network and IUCN, 2014);

  21. Hughes, T. P. et al. Global warming and recurrent mass bleaching of corals. Nature 543, 373–377 (2017).

    Article  CAS  PubMed  Google Scholar 

  22. Almany, G. R., Berumen, M. L., Thorrold, S. R., Planes, S. & Jones, G. P. Local replenishment of coral reef fish populations in a marine reserve. Science 316, 742–744 (2007).

    Article  CAS  PubMed  Google Scholar 

  23. Almany, G. R. & Webster, M. S. The predation gauntlet: early post-settlement mortality in reef fishes. Coral Reefs 25, 19–22 (2006).

    Article  Google Scholar 

  24. McCormick, M. I. & Hoey, A. S. Larval growth history determines juvenile growth and survival in a tropical marine fish. Oikos 106, 225–242 (2004).

    Article  Google Scholar 

  25. Incardona, J. P. et al. Deepwater Horizon crude oil impacts the developing hearts of large predatory pelagic fish. Proc. Natl Acad. Sci. USA 111, E1510–E1518 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Brette, F. et al. Crude oil impairs cardiac excitation-contraction coupling in fish. Science 343, 772–776 (2014).

    Article  CAS  PubMed  Google Scholar 

  27. Xu, E. G. et al. Time-and oil-dependent transcriptomic and physiological responses to Deepwater Horizon oil in mahi-mahi (Coryphaena hippurus) embryos and larvae. Environ. Sci. Technol. 50, 7842–7851 (2016).

    Article  CAS  PubMed  Google Scholar 

  28. Wellington, G. M. & Victor, B. C. Planktonic larval duration of one hundred species of Pacific and Atlantic damselfishes (Pomacentridae). Mar. Biol. 101, 557–567 (1989).

    Article  Google Scholar 

  29. Basheer, C., Obbard, J. P. & Lee, H. K. Persistent organic pollutants in Singapore’s coastal marine environment: Part I, seawater. Water Air Soil Pollut. 149, 295–313 (2003).

    Article  CAS  Google Scholar 

  30. Hoare, D. J. & Krause, J. Social organisation, shoal structure and information transfer. Fish Fish. 4, 269–279 (2003).

    Article  Google Scholar 

  31. Schnörr, S. J., Steenbergen, P. J., Richardson, M. K. & Champagne, D. L. Measuring thigmotaxis in larval zebrafish. Behav. Brain Res. 228, 367–374 (2012).

    Article  PubMed  Google Scholar 

  32. Hixon, M. A. in Ecology of Fishes on Coral Reefs (ed. Mora, C.) 41–52 (Cambridge Univ. Press, Cambridge, 2015).

  33. Domenici, P. & Blake, R. The kinematics and performance of fish fast-start swimming. J. Exp. Biol. 200, 1165–1178 (1997).

    CAS  PubMed  Google Scholar 

  34. Bolker, B. M. et al. Generalized linear mixed models: a practical guide for ecology and evolution. Trends Ecol. Evol. 24, 127–135 (2009).

    Article  PubMed  Google Scholar 

  35. Bates, D., Maechler, M., Bolker, B. & Walker, S. Fitting linear mixed-effects models using lme4. J. Stat. Softw. 67, 1–48 (2015).

Download references


The authors thank the staff from the Lizard Island Research Station and R. Ern for logistical support and P. van der Sleen for illustration assistance. This research was made possible by a grant from the Lizard Island Research Foundation and The Gulf of Mexico Research Initiative (GMRI).

Author information

Authors and Affiliations



J.L.J. and A.J.E. conceived the idea. J.L.J. designed the experiments. J.L.J., B.J.M.A. and J.L.R. performed the experiments. J.L.J. and B.J.M.A. analysed the data. J.L.J. wrote the manuscript with input from B.J.M.A., J.L.R. and A.J.E.

Corresponding author

Correspondence to Jacob L. Johansen.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Additional information

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

Corrected online: Publisher correction 2 August 2017

A correction to this article is available online at

Electronic supplementary material

Supplementary Information

Supplementary Figures 1–4, Supplementary Table 1

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Johansen, J.L., Allan, B.J.M., Rummer, J.L. et al. Oil exposure disrupts early life-history stages of coral reef fishes via behavioural impairments. Nat Ecol Evol 1, 1146–1152 (2017).

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI:

This article is cited by


Quick links

Nature Briefing Anthropocene

Sign up for the Nature Briefing: Anthropocene newsletter — what matters in anthropocene research, free to your inbox weekly.

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