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Marine and Freshwater Research Marine and Freshwater Research Society
Advances in the aquatic sciences
RESEARCH ARTICLE

Oil exposure impairs predator–prey dynamics in larval red drum (Sciaenops ocellatus)

L. E. Rowsey A C , J. L. Johansen A B , A. J. Khursigara A and A. J. Esbaugh A
+ Author Affiliations
- Author Affiliations

A University of Texas at Austin, Marine Science Institute, Port Aransas, TX 78373, USA.

B New York University, Abu Dhabi, 129188, UAE.

C Corresponding author. Present address: University of New Brunswick, Saint John, NB, E2L 4L5, Canada. Email: lrowsey@unb.ca

Marine and Freshwater Research 71(1) 99-106 https://doi.org/10.1071/MF18263
Submitted: 24 July 2018  Accepted: 19 November 2018   Published: 1 February 2019

Abstract

The 2010 Deepwater Horizon (DWH) oil spill in the Gulf of Mexico was the largest spill in recent history and led to the exposure of many commercially and ecologically important fish species. Crude-oil exposure is known to result in compromised cardiorespiratory function and swim performance of fishes, presumably altering ecological performance by impairing the ability to capture prey or evade predators. However, this has yet to be empirically tested. This study assessed the impacts of oil exposure on thigmotaxis (avoidance of exposed areas), routine activity, and prey-capture ability in larval red drum (Sciaenops ocellatus) by using environmentally relevant concentrations of weathered-oil water-accommodated fractions (0–55.9 µg L–1 of total polycyclic aromatic hydrocarbons, ΣPAH). Oil exposure caused a dose-dependent increase in time spent in the exposed area of the arena, with an average three-fold increase at the highest dose, suggesting increased risk-taking. Although increased risk-taking resulted in 14% more area explored, oil-exposed individuals were significantly slower to catch prey and caught 67% less prey overall. Prey-capture ability did not appear to be related to cardiorespiratory or swimming impairments, because oil-exposed fish exhibited routine swim speeds and the distance travelled similar to those of the control, suggesting an alternate route of toxicity, such as cognitive impairments.

Additional keywords: Deepwater Horizon, development, oil spill, PAH, predator–prey interactions.


References

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

Brette, F., Machado, B., Cros, C., Incardona, J. P., Scholz, N. L., and Block, B. A. (2014). Crude oil impairs cardiac excitation–contraction coupling in fish. Science 343, 772–776.
Crude oil impairs cardiac excitation–contraction coupling in fish.Crossref | GoogleScholarGoogle Scholar | 24531969PubMed |

Brown, C., Laland, K., and Krause, J. (2008) ‘Fish Cognition and Behavior.’ (Wiley: Hoboken, NJ, USA.)

Brown, G. E., Ferrari, M. C. O., and Chivers, D. P. (2011) Learning about danger: chemical alarm cues and threat-sensitive assessment of predation risk by fishes. In ‘Fish Cognition and Behavior’. pp. 59–80. (Wiley-Blackwell: Hoboken, NJ, USA.)

Buskey, E. J., White, H. K., and Esbaugh, A. J. (2016). Impact of oil spills on marine life in the Gulf of Mexico: effects on plankton, nekton, and deep-sea benthos. Oceanography 29, 174–181.
Impact of oil spills on marine life in the Gulf of Mexico: effects on plankton, nekton, and deep-sea benthos.Crossref | GoogleScholarGoogle Scholar |

Carvalho, P. S. M., Kalil, D. C. B., Novelli, G. A. A., Bainy, A. C. D., and Fraga, A. P. M. (2008). Effects of naphthalene and phenanthrene on visual and prey capture endpoints during early stages of the dourado Salminus brasiliensis. Marine Environmental Research 66, 205–207.
Effects of naphthalene and phenanthrene on visual and prey capture endpoints during early stages of the dourado Salminus brasiliensis.Crossref | GoogleScholarGoogle Scholar |

Champagne, D. L., Hoefnagels, C. C. M., de Kloet, R. E., and Richardson, M. K. (2010). Translating rodent behavioral repertoire to zebrafish (Danio rerio): relevance for stress research. Behavioural Brain Research 214, 332–342.
Translating rodent behavioral repertoire to zebrafish (Danio rerio): relevance for stress research.Crossref | GoogleScholarGoogle Scholar | 20540966PubMed |

Claireaux, G., Désaunay, Y., Akcha, F., Aupérin, B., Bocquené, G., Budzinski, H., Cravedi, J.-P., Davoodi, F., Galois, R., Gilliers, C., Goanvec, C., Guérault, D., Imbert, N., Mazéas, O., Nonnotte, G., Nonnotte, L., Prunet, P., Sébert, P., and Vettier, A. (2004). Influence of oil exposure on the physiology and ecology of the common sole Solea solea: experimental and field approaches. Aquatic Living Resources 17, 335–351.
Influence of oil exposure on the physiology and ecology of the common sole Solea solea: experimental and field approaches.Crossref | GoogleScholarGoogle Scholar |

Claireaux, G., Theron, M., Prineau, M., Dussauze, M., Merlin, F. X., and Le Floch, S. (2013). Effects of oil exposure and dispersant use upon environmental adaptation performance and fitness in the European sea bass, Dicentrarchus labrax. Aquatic Toxicology 130–131, 160–170.
Effects of oil exposure and dispersant use upon environmental adaptation performance and fitness in the European sea bass, Dicentrarchus labrax.Crossref | GoogleScholarGoogle Scholar | 23411352PubMed |

Claireaux, G., Quéau, P., Marras, S., Le Floch, S., Farrell, A. P., Nicolas‐Kopec, A., Lemaire, P., and Domenici, P. (2018). Avoidance threshold to oil water-soluble fraction by a juvenile marine teleost fish. Environmental Toxicology and Chemistry 37, 854–859.
Avoidance threshold to oil water-soluble fraction by a juvenile marine teleost fish.Crossref | GoogleScholarGoogle Scholar | 29077219PubMed |

Collier, T. K., Anulacion, B. F., Arkoosh, M. R., Dietrich, J. P., Incardona, J. P., Johnson, L. L., Ylitalo, G. M., and Myers, M. S. (2013) 4. Effects on fish of polycyclic aromatic hydrocarbons (PAHS) and naphthenic acid exposures. In ‘Fish Physiology’. (Eds A. P. F. Keith, B. Tierney, and J. B. Colin.) Vol. 33, pp. 195–255. (Academic Press: Cambridge, MA, USA.)

Davoodi, F., and Claireaux, G. (2007). Effects of exposure to petroleum hydrocarbons upon the metabolism of the common sole Solea solea. Marine Pollution Bulletin 54, 928–934.
Effects of exposure to petroleum hydrocarbons upon the metabolism of the common sole Solea solea.Crossref | GoogleScholarGoogle Scholar | 17466342PubMed |

Diercks, A.-R., Highsmith, R. C., Asper, V. L., Joung, D., Zhou, Z., Guo, L., Shiller, A. M., Joye, S. B., Teske, A. P., Guinasso, N., Wade, T. L., and Lohrenz, S. E. (2010). Characterization of subsurface polycyclic aromatic hydrocarbons at the Deepwater Horizon site. Geophysical Research Letters 37, L20602.
Characterization of subsurface polycyclic aromatic hydrocarbons at the Deepwater Horizon site.Crossref | GoogleScholarGoogle Scholar |

Edmunds, R. C., Gill, J. A., Baldwin, D. H., Linbo, T. L., French, B. L., Brown, T. L., Esbaugh, A. J., Mager, E. M., Stieglitz, J., Hoenig, R., Benetti, D., Grosell, M., Scholz, N. L., and Incardona, J. P. (2015). Corresponding morphological and molecular indicators of crude oil toxicity to the developing hearts of mahi mahi. Scientific Reports 5, 17326.
Corresponding morphological and molecular indicators of crude oil toxicity to the developing hearts of mahi mahi.Crossref | GoogleScholarGoogle Scholar | 26658479PubMed |

Ern, R., and Esbaugh, A. J. (2016). Hyperventilation and blood acid–base balance in hypercapnia exposed red drum (Sciaenops ocellatus). Journal of Comparative Physiology – B. Biochemical, Systemic, and Environmental Physiology 186, 447–460.
Hyperventilation and blood acid–base balance in hypercapnia exposed red drum (Sciaenops ocellatus).Crossref | GoogleScholarGoogle Scholar | 26922790PubMed |

Esbaugh, A. J., and Cutler, B. (2016). Intestinal Na+, K+, 2Cl– cotransporter 2 plays a crucial role in hyperosmotic transitions of a euryhaline teleost. Physiological Reports 4, e13028.
Intestinal Na+, K+, 2Cl cotransporter 2 plays a crucial role in hyperosmotic transitions of a euryhaline teleost.Crossref | GoogleScholarGoogle Scholar | 27881573PubMed |

Esbaugh, A. J., Mager, E. M., Stieglitz, J. D., Hoenig, R., Brown, T. L., French, B. L., Linbo, T. L., Lay, C., Forth, H., Scholz, N. L., Incardona, J. P., Morris, J. M., Benetti, D. D., and Grosell, M. (2016). The effects of weathering and chemical dispersion on Deepwater Horizon crude oil toxicity to mahi-mahi (Coryphaena hippurus) early life stages. Science of the Total Environment A 543, 644–651.
The effects of weathering and chemical dispersion on Deepwater Horizon crude oil toxicity to mahi-mahi (Coryphaena hippurus) early life stages.Crossref | GoogleScholarGoogle Scholar |

Fodrie, F. J., Able, K. W., Galvez, F., Heck, J. K. L., Jensen, O. P., López-Duarte, P. C., Martin, C. W., Turner, R. E., and Whitehead, A. (2014). Integrating organismal and population responses of estuarine fishes in macondo spill research. Bioscience 64, 778–788.
Integrating organismal and population responses of estuarine fishes in macondo spill research.Crossref | GoogleScholarGoogle Scholar |

Gallaway, B. J., Gazey, W. J., Cole, J. G., and Fechhelm, R. G. (2007). Estimation of potential impacts from offshore liquefied natural gas terminals on red snapper and red drum fisheries in the Gulf of Mexico: an alternative approach. Transactions of the American Fisheries Society 136, 655–677.
Estimation of potential impacts from offshore liquefied natural gas terminals on red snapper and red drum fisheries in the Gulf of Mexico: an alternative approach.Crossref | GoogleScholarGoogle Scholar |

Hamilton, T. J., Morrill, A., Lucas, K., Gallup, J., Harris, M., Healey, M., Pitman, T., Schalomon, M., Digweed, S., and Tresguerres, M. (2017). Establishing zebrafish as a model to study the anxiolytic effects of scopolamine. Scientific Reports 7, 15081.
Establishing zebrafish as a model to study the anxiolytic effects of scopolamine.Crossref | GoogleScholarGoogle Scholar | 29118373PubMed |

Hicken, C. E., Linbo, T. L., Baldwin, D. H., Willis, M. L., Myers, M. S., Holland, L., Larsen, M., Stekoll, M. S., Rice, S. D., Collier, T. K., Scholz, N. L., and Incardona, J. P. (2011). Sublethal exposure to crude oil during embryonic development alters cardiac morphology and reduces aerobic capacity in adult fish. Proceedings of the National Academy of Sciences of the United States of America 108, 7086–7090.
Sublethal exposure to crude oil during embryonic development alters cardiac morphology and reduces aerobic capacity in adult fish.Crossref | GoogleScholarGoogle Scholar | 21482755PubMed |

Incardona, J. P., Collier, T. K., and Scholz, N. L. (2004). Defects in cardiac function precede morphological abnormalities in fish embryos exposed to polycyclic aromatic hydrocarbons. Toxicology and Applied Pharmacology 196, 191–205.
Defects in cardiac function precede morphological abnormalities in fish embryos exposed to polycyclic aromatic hydrocarbons.Crossref | GoogleScholarGoogle Scholar | 15081266PubMed |

Incardona, J. P., Gardner, L. D., Linbo, T. L., Brown, T. L., Esbaugh, A. J., Mager, E. M., Stieglitz, J. D., French, B. L., Labenia, J. S., Laetz, C. A., Tagal, M., Sloan, C. A., Elizur, A., Benetti, D. D., Grosell, M., Block, B. A., and Scholz, N. L. (2014). Deepwater Horizon crude oil impacts the developing hearts of large predatory pelagic fish. Proceedings of the National Academy of Sciences of the United States of America 111, E1510–E1518.
Deepwater Horizon crude oil impacts the developing hearts of large predatory pelagic fish.Crossref | GoogleScholarGoogle Scholar | 24706825PubMed |

Johansen, J. L., and Esbaugh, A. J. (2017). Sustained impairment of respiratory function and swim performance following acute oil exposure in a coastal marine fish. Aquatic Toxicology 187, 82–89.
Sustained impairment of respiratory function and swim performance following acute oil exposure in a coastal marine fish.Crossref | GoogleScholarGoogle Scholar | 28395197PubMed |

Johansen, J. L., Allan, B. J. M., Rummer, J. L., and Esbaugh, A. J. (2017). Oil exposure disrupts early life-history stages of coral reef fishes via behavioural impairments. Nature Ecology & Evolution 1, 1146–1152.
Oil exposure disrupts early life-history stages of coral reef fishes via behavioural impairments.Crossref | GoogleScholarGoogle Scholar |

Khursigara, A. J., Perrichon, P., Martinez Bautista, N., Burggren, W. W., and Esbaugh, A. J. (2017). Cardiac function and survival are affected by crude oil in larval red drum, Sciaenops ocellatus. The Science of the Total Environment 579, 797–804.
Cardiac function and survival are affected by crude oil in larval red drum, Sciaenops ocellatus.Crossref | GoogleScholarGoogle Scholar | 27865530PubMed |

Lima, S. L., and Bednekoff, P. A. (1999a). Back to the basics of antipredatory vigilance: can nonvigilant animals detect attack? Animal Behaviour 58, 537–543.
Back to the basics of antipredatory vigilance: can nonvigilant animals detect attack?Crossref | GoogleScholarGoogle Scholar | 10479369PubMed |

Lima, S. L., and Bednekoff, P. A. (1999b). Temporal variation in danger drives antipredator behavior: the predation risk allocation hypothesis. American Naturalist 153, 649–659.
Temporal variation in danger drives antipredator behavior: the predation risk allocation hypothesis.Crossref | GoogleScholarGoogle Scholar | 29585647PubMed |

Lonthair, J., Ern, R., and Esbaugh, A. J. (2017). Early life stages of an estuarine-dependent fish are tolerant of ocean acidification. ICES Journal of Marine Science 74, 1042–1050.
Early life stages of an estuarine-dependent fish are tolerant of ocean acidification.Crossref | GoogleScholarGoogle Scholar |

Mager, E. M., Esbaugh, A. J., Stieglitz, J. D., Hoenig, R., Bodinier, C., Incardona, J. P., Scholz, N. L., Benetti, D. D., and Grosell, M. (2014). Acute embryonic or juvenile exposure to Deepwater Horizon crude oil impairs the swimming performance of mahi-mahi (Coryphaena hippurus). Environmental Science & Technology 48, 7053–7061.
Acute embryonic or juvenile exposure to Deepwater Horizon crude oil impairs the swimming performance of mahi-mahi (Coryphaena hippurus).Crossref | GoogleScholarGoogle Scholar |

Magnuson, J. T., Khursigara, A. J., Allmon, E. B., Esbaugh, A. J., and Roberts, A. P. (2018). Effects of Deepwater Horizon crude oil on ocular development in two estuarine fish species, red drum (Sciaenops ocellatus) and sheepshead minnow (Cyprinodon variegatus). Ecotoxicology and Environmental Safety 166, 186–191.
Effects of Deepwater Horizon crude oil on ocular development in two estuarine fish species, red drum (Sciaenops ocellatus) and sheepshead minnow (Cyprinodon variegatus).Crossref | GoogleScholarGoogle Scholar | 30269013PubMed |

Mendelssohn, I. A., Andersen, G. L., Baltz, D. M., Caffey, R. H., Carman, K. R., Fleeger, J. W., Joye, S. B., Lin, Q., Maltby, E., Overton, E. B., and Rozas, L. P. (2012). Oil impacts on coastal wetlands: implications for the Mississippi River Delta ecosystem after the Deepwater Horizon oil spill. Bioscience 62, 562–574.
Oil impacts on coastal wetlands: implications for the Mississippi River Delta ecosystem after the Deepwater Horizon oil spill.Crossref | GoogleScholarGoogle Scholar |

Nelson, D., Heuer, R. M., Cox, G. K., Stieglitz, J. D., Hoenig, R., Mager, E. M., Benetti, D. D., Grosell, M., and Crossley, D. A. (2016). Effects of crude oil on in situ cardiac function in young adult mahi-mahi (Coryphaena hippurus). Aquatic Toxicology 180, 274–281.
Effects of crude oil on in situ cardiac function in young adult mahi-mahi (Coryphaena hippurus).Crossref | GoogleScholarGoogle Scholar | 27768947PubMed |

Nelson, D., Stieglitz, J. D., Cox, G. K., Heuer, R. M., Benetti, D. D., Grosell, M., and Crossley, D. A. (2017). Cardio-respiratory function during exercise in the cobia, Rachycentron canadum: the impact of crude oil exposure. Comparative Biochemistry and Physiology – Toxicology & Pharmacology 201, 58–65.
Cardio-respiratory function during exercise in the cobia, Rachycentron canadum: the impact of crude oil exposure.Crossref | GoogleScholarGoogle Scholar |

Pan, Y. K., Ern, R., and Esbaugh, A. J. (2016). Hypoxia tolerance decreases with body size in red drum Sciaenops ocellatus. Journal of Fish Biology 89, 1488–1493.
Hypoxia tolerance decreases with body size in red drum Sciaenops ocellatus.Crossref | GoogleScholarGoogle Scholar | 27328965PubMed |

Pan, Y. K., Khursigara, A. J., Johansen, J. L., and Esbaugh, A. J. (2018). The effects of oil induced respiratory impairment on two indices of hypoxia tolerance in Atlantic croaker (Micropogonias undulates). Chemosphere 200, 143–150.
The effects of oil induced respiratory impairment on two indices of hypoxia tolerance in Atlantic croaker (Micropogonias undulates).Crossref | GoogleScholarGoogle Scholar | 29477763PubMed |

Preisser, E. L., Orrock, J. L., and Schmitz, O. J. (2007). Predator hunting mode and habitat domain alter nonconsumptive effects in predator–prey interactions. Ecology 88, 2744–2751.
Predator hunting mode and habitat domain alter nonconsumptive effects in predator–prey interactions.Crossref | GoogleScholarGoogle Scholar | 18051642PubMed |

Reddy, C. M., Arey, J. S., Seewald, J. S., Sylva, S. P., Lemkau, K. L., Nelson, R. K., Carmichael, C. A., McIntyre, C. P., Fenwick, J., Ventura, G. T., Van Mooy, B. A. S., and Camilli, R. (2012). Composition and fate of gas and oil released to the water column during the Deepwater Horizon oil spill. Proceedings of the National Academy of Sciences of the United States of America 109, 20229–20234.
Composition and fate of gas and oil released to the water column during the Deepwater Horizon oil spill.Crossref | GoogleScholarGoogle Scholar | 21768331PubMed |

Rooker, J. R., Kitchens, L. L., Dance, M. A., Wells, R. J. D., Falterman, B., and Cornic, M. (2013). Spatial, temporal, and habitat-related variation in abundance of pelagic fishes in the Gulf of Mexico: potential implications of the Deepwater Horizon oil spill. PLoS One 8, e76080.
Spatial, temporal, and habitat-related variation in abundance of pelagic fishes in the Gulf of Mexico: potential implications of the Deepwater Horizon oil spill.Crossref | GoogleScholarGoogle Scholar | 24130759PubMed |

Schnörr, S. J., Steenbergen, P. J., Richardson, M. K., and Champagne, D. L. (2012). Measuring thigmotaxis in larval zebrafish. Behavioural Brain Research 228, 367–374.
Measuring thigmotaxis in larval zebrafish.Crossref | GoogleScholarGoogle Scholar | 22197677PubMed |

Stewart, W. J., Johansen, J. L., and Liao, J. C. (2017). A non-toxic dose of cobalt chloride blocks hair cells of the zebrafish lateral line. Hearing Research 350, 17–21.
A non-toxic dose of cobalt chloride blocks hair cells of the zebrafish lateral line.Crossref | GoogleScholarGoogle Scholar | 28412580PubMed |

Stieglitz, J. D., Mager, E. M., Hoenig, R. H., Benetti, D. D., and Grosell, M. (2016). Impacts of Deepwater Horizon crude oil exposure on adult mahi-mahi (Coryphaena hippurus) swim performance. Environmental Toxicology and Chemistry 35, 2613–2622.
Impacts of Deepwater Horizon crude oil exposure on adult mahi-mahi (Coryphaena hippurus) swim performance.Crossref | GoogleScholarGoogle Scholar | 27018209PubMed |

Treit, D., and Fundytus, M. (1988). Thigmotaxis as a test for anxiolytic activity in rats. Pharmacology, Biochemistry, and Behavior 31, 959–962.
Thigmotaxis as a test for anxiolytic activity in rats.Crossref | GoogleScholarGoogle Scholar | 3252289PubMed |

Watson, C. J., Nordi, W. M., and Esbaugh, A. J. (2014). Osmoregulation and branchial plasticity after acute freshwater transfer in red drum, Sciaenops ocellatus. Comparative Biochemistry and Physiology – A. Molecular & Integrative Physiology 178, 82–89.
Osmoregulation and branchial plasticity after acute freshwater transfer in red drum, Sciaenops ocellatus.Crossref | GoogleScholarGoogle Scholar |

Xu, E. G., Mager, E. M., Grosell, M., Pasparakis, C., Schlenker, L. S., Stieglitz, J. D., Benetti, D., Hazard, E. S., Courtney, S. M., Diamante, G., Freitas, J., Hardiman, G., and Schlenk, D. (2016). Time- and oil-dependent transcriptomic and physiological responses to Deepwater Horizon oil in mahi-mahi (Coryphaena hippurus) embryos and larvae. Environmental Science & Technology 50, 7842–7851.
Time- and oil-dependent transcriptomic and physiological responses to Deepwater Horizon oil in mahi-mahi (Coryphaena hippurus) embryos and larvae.Crossref | GoogleScholarGoogle Scholar |

Xu, E. G., Khursigara, A. J., Magnuson, J., Hazard, E. S., Hardiman, G., Esbaugh, A. J., Roberts, A. P., and Schlenk, D. (2017). Larval red drum (Sciaenops ocellatus) sublethal exposure to weathered Deepwater Horizon crude oil: developmental and transcriptomic consequences. Environmental Science & Technology 51, 10162–10172.
Larval red drum (Sciaenops ocellatus) sublethal exposure to weathered Deepwater Horizon crude oil: developmental and transcriptomic consequences.Crossref | GoogleScholarGoogle Scholar |