Article | Published:

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

Nature Ecology & Evolutionvolume 1pages11461152 (2017) | Download Citation


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.

Access optionsAccess options

Rent or Buy article

Get time limited or full article access on ReadCube.


All prices are NET prices.

Additional information

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

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. 1.

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

  2. 2.

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

  3. 3.

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

  4. 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. 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. 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).

  7. 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).

  8. 8.

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

  9. 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).

  10. 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).

  11. 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).

  12. 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).

  13. 13.

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

  14. 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. 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).

  16. 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).

  17. 17.

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

  18. 18.

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

  19. 19.

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

  20. 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. 21.

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

  22. 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).

  23. 23.

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

  24. 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).

  25. 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).

  26. 26.

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

  27. 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).

  28. 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).

  29. 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).

  30. 30.

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

  31. 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).

  32. 32.

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

  33. 33.

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

  34. 34.

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

  35. 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


  1. Department of Marine Science, University of Texas, Marine Science Institute, Port Aransas, TX, 78373, USA

    • Jacob L. Johansen
    •  & Andrew J. Esbaugh
  2. Pelagic Fish Group, Institute of Marine Research, Bergen, 5005, Norway

    • Bridie J. M. Allan
  3. Australian Research Council Centre of Excellence for Coral Reef Studies, James Cook University, Townsville, QLD, 4811, Australia

    • Jodie L. Rummer


  1. Search for Jacob L. Johansen in:

  2. Search for Bridie J. M. Allan in:

  3. Search for Jodie L. Rummer in:

  4. Search for Andrew J. Esbaugh in:


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.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Jacob L. Johansen.

Electronic supplementary material

  1. Supplementary Information

    Supplementary Figures 1–4, Supplementary Table 1

About this article

Publication history