Comment on “Multitissue Molecular, Genomic, and Developmental

Correspondence/Rebuttal pubs.acs.org/est

Comment on “Multitissue Molecular, Genomic, and Developmental Effects of the Deepwater Horizon Oil Spill on Resident Gulf Killifish (Fundulus grandis)”

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erspective is needed on Dubansky et al.1 concerning their study of fish eggs exposed to sediments from oiled locations along the Gulf of Mexico (GOM) following the Deepwater Horizon oil spill (DHOS). The materials presented and cited are not persuasive of the authors’ notion that their observations of developmental effects on eggs “are predictive of population-level effects in fish exposed to sediments from oiled locations...” I do not disagree with the authors’ observation of effects on killifish eggs exposed in the laboratory to oiled sediment collected from three locations along the Gulf. Others have observed similar developmental effects from oil exposure on the eggs of other fish species2−6 as well as on killifish eggs from heavy metals7,8 and other oils.9,10 Also, I do not disagree with the judgment of the authors and others1,4,9 that such effects in exposed embryos compromise the survivability of the hatching larvae. However, I do not find the materials to offer a convincing prediction of population-level effects for several reasons. First, to support their notion, the authors cite research work following the Exxon Valdez Oil Spill (EVOS) to the effect that the exposure of salmon and herring eggs during the EVOS led to population-level effects; however, research conducted for almost 25 years since then does not support such populationlevel effects. Concerning salmon and the EVOS, recent reviews11,12 reveal a course of events that argues against premature predictions of population-level effects. For example, initial reporting of mortality of salmon eggs from oil exposure in the field was found to be confounded by sampling artifacts in subsequent Trustee and Exxon-sponsored research.11,13,14 Despite initial concerns, the outcome of years of research is that no EVOS effects on salmon were evident at the population level.11,12 For herring and EVOS, studies by Trustee-sponsored scientists and Exxon-sponsored scientists both observed localized effects on eggs and larvae exposed to oil during the spill year (1989), both did not observe these effects the next year (1990), and both did not observe effects at the population level.6,15−19 Several sets of data indicate the lack of populationlevel effects from the EVOS on herring: High herring biomasses in 1990 and 1991, no change in age composition, postspill recruitment patterns for which abundance and timing matched expectation, and lack of correlation between oil exposure and biomass levels. Two independent age structured assessment (ASA) models of the Prince William Sound (PWS) herring population did not find elevated adult mortality in the spill years.20,21 Further, one ASA model analysis 20 used covariates to find that natural and anthropogenic factors were significant in the population dynamics of PWS herring while oil exposure was not. Second, the exposure is characterized for three sampling locations and two times. This level of effort and study design is inadequate to assess the exposure of the killifish population at any level higher that the sites specifically sampled. © 2014 American Chemical Society

Third, the Dubansky study exposed the killifish eggs to high levels of oil in sediment but did not determine any effects thresholds. When the extent of the marsh oiling is fully revealed in the public domain, the application of thresholds to the spatial distribution of oiling levels will be helpful in estimating the potential for elevated mortality or other effects on the killifish eggs. Earlier work on oil and killifish eggs9,10 does include some information on dose response with other oils but without more detailed quantification of effects and characterization of the PAH concentrations, the application of these earlier results to spatial distribution data can only be tentative. Fourth, biomarkers at the biochemical level (e.g., CYP1A) have proved to be useful indicators of exposure when used with other information, but CYP1A results alone do not indicate injury.22−24 The genomic results in the Dubansky study appear to align with the CYP1A results as another indicator of exposure. The patchy nature of the oil distribution in the EVOS led to difficulties in determining the exposure of fish on a fine scale over a broad area.19,25 A similar situation probably pertains in the DHOS. One lesson learned from the EVOS is that exposure levels need to be “measured directly rather than inferred indirectly”.25 Oris and Roberts 24 discuss the difficulties and promise in using genomics for regulatory assessments in oil spills and conclude that substantial research is needed before employing these techniques to assess cause-and-effect relationships in the field. Fifth, compensatory mechanisms influence the population dynamics of fish populations.26 Such mechanisms make fish populations resilient to effects at the egg and larval stages. Year class strength and recruitment in fish are not determined at the egg stage but usually at the late larval or early juvenile stage27,28 so that effects at the egg stage do not necessarily translate to effects at the population level and most frequently do not. Preliminary research concerning juvenile fish rearing in GOM sea grass beds following the DHOS revealed no catastrophic declines in the juvenile fish abundance or shifts in species composition in the year following the spill.29 Similarly, a beforeafter study of marsh species (including Fundulus grandis) found “little evidence for severe or persistent oil-induced impacts on marsh-associated nekton in coastal Alabama” after the DHOS.30 Although these studies focus on portions of the nekton, they exemplify the kind of studies needed to make inferences at the population level. Overall, the Dubansky study1 demonstrates that exposure to oiled sediments in the laboratory adversely affects the survival potential of larvae hatching from exposed eggs and, therefore, aligns with previous research. However, by themselves, the study’s outcomes are not predictive of population-level effects on fish exposed to oil along GOM shorelines following the DHOS. More information on the distribution of oiling levels in Published: June 19, 2014 7677

dx.doi.org/10.1021/es405220v | Environ. Sci. Technol. 2014, 48, 7677−7678

Environmental Science & Technology

Correspondence/Rebuttal

stages of Pacific herring, (Clupea pallasi), in Prince William Sound, Alaska. Can. J. Fish. Aquat. Sci. 1996, 53 (10), 2337−2342. (16) Pearson, W. H. Why did the Prince William Sound, Alaska, Pacific herring (Clupea pallasi) fisheries collapse in 1993 and 1994? Review of hypotheses. Can. J. Fish. Aquat. Sci. 1999, 56 (4), 711−737. (17) Pearson, W. H.; et al. Hypotheses concerning the decline and poor recovery of Pacific herring in Prince William Sound, Alaska. Rev. Fish Biol. Fish 2012, 22 (1), 95−135. (18) Pearson, W. H.; Elston, R. A.; Humphrey, K.; Deriso, R. B. Pacific herring. In Oil in the Environment: Legacies and Lessons of the Exxon Valdez Oil Spill; Wiens, J. A., Ed.; Cambridge University Press: Cambridge, U.K., 2013; pp 292−317. (19) Rice, S. D.; Carls, M. G. Executive summary. In Prince William Sound Herring: An Updated Synthesis of Population Declines and Lack of RecoveryFinal Report; Rice, S. D., Carls, M. G., Eds.; Exxon Valdez Trustee Council: Anchorage, AK, 2007. (20) Deriso, R. B.; Maunder, M. N.; Pearson, W. H. Incorporating covariates into fisheries stock assessment models with application to Pacific herring. Ecol. Appl. 2008, 18 (5), 1270−1286. (21) Hulson, P. J. F.; et al. Data conflicts in fishery models: incorporating hydroacoustic data into the Prince William Sound Pacific herring assessment model. ICES J. Mar. Sci. 2008, 65 (1), 25− 43. (22) Lee, R. F.; Anderson, J. W. Significance of cytochrome P450 system responses and levels of bile fluorescent aromatic compounds in marine wildlife following oil spills. Mar. Pollut. Bull. 2005, 50 (7), 705−723. (23) Incardona, J. P.; et al. Aryl hydrocarbon receptor-independent toxicity of weathered crude oil during fish development. Environ. Health Perspect. 2005, 113 (12), 1755−1762. (24) Oris, J. T.; Roberts, A. P. Cytochrome P450 1A (CYP1A) as a biomarker in oil spill assessments. In Oil in the Environment: Legacies and Lessons of the Exxon Valdez Oil Spill; Wiens, J. A., Ed.; Cambridge University Press: Cambridge, U.K., 2013; pp 201−219. (25) Wiens, J. A. Science and oil spills: The broad perspective. In Oil in the Environment: Legacies and Lessons of the Exxon Valdez Oil Spill, Wiens, J. A., Ed.; Cambridge University Press: Cambridge, U.K., 2013; pp 423−445. (26) Rothschild, B. Dynamics of Marine Fish Populations; Harvard University Press: Cambridge, MA, 1986. (27) Leggett, W. C.; Deblois, E. Recruitment in marine fishes: is it regulated by starvation and predation in the egg and larval stages? Neth. J. Sea Res. 1994, 32 (2), 119−134. (28) Brown, E. D.; Norcross, B. L. Effect of herring egg distribution and environmental factors on year-class strength and adult distribution: preliminary results from Prince William Sound, Alaska. In Herring: Expectations for a New Millennium; Funk, F., et al., Eds.; University of Alaska Sea Grant: Fairbanks, 2001; pp 335−345. (29) Fodrie, F. J.; Heck, K. L. Response of coastal fishes to the Gulf of Mexico oil disaster. PloS ONE 2011, 6 (7), e21609. (30) Moody, R. M.; Cebrian, J.; Heck, K. L. Internanual recruitment dynamics for resident and transient marsh species: Evidence for a lack of impact by the Macondo Oil Spill. PloS ONE 2013, 8 (3), e58376.

the marsh spawning habitat, a species-specific and oil-specific threshold for effects, and analysis of killifish abundance and distribution are needed to assess population-level effects from the DHOS on this important marsh fish.

Walter H. Pearson*

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Stantec Consulting Services, Inc. 2321 Club Meridian Drive Suite E, Okemos, Michigan 48864, United States

AUTHOR INFORMATION

Corresponding Author

*Phone: (616) 610-4614; e-mail: [email protected]. Notes

The authors declare the following competing financial interest(s): This research was supported by BP Exploration & Production, Inc.

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REFERENCES

(1) Dubansky, B.; et al. Multitissue molecular, genomic, and developmental effects of the Deepwater Horizon oil spill on resident gulf killifish (Fundulus grandis). Environ. Sci. Technol. 2013, 47 (10), 5074−5082. (2) Linden, O. Biological effects of oil on early development of the Baltic herring Clupea harengus membras. Mar. Biol. 1978, 45 (3), 273− 283. (3) Smith, R. L.; Cameron, J. A. Effect of water soluble fraction of Prudhoe Bay crude oil on embryonic development of Pacific herring. Trans. Am. Fish. Soc. 1979, 108 (1), 70−75. (4) von Westernhagen, H. Sublethal effects of pollutants on fish eggs and larvae. In Fish Physiology, Vol. 11, The Physiology of Developing Fish, Part A, Eggs and Larvae; Hoar, W. S., Randall, D. J., Eds.; Academic Press: San Diego, CA, 1988, pp 253−346. (5) Pearson, W. H., et al. Oil Effects on Spawning Behavior and Reproduction in Pacific Herring (Clupea harengus pallasi); American Petroleum Institute: Washington, DC, 1985. (6) Pearson, W. H.; Moksness, E.; Skalski, J. R. A field and laboratory assessment of oil spill effects on survival and reproduction of Pacific herring following the Exxon Valdez spill. In Exxon Valdez Oil Spill: Fate and Effects in Alaskan Waters; Wells, P. G., Butler, J. N., Hughes, J. S., Eds.; American Society for Testing and Materials: Philadelphia, 1995; pp 626−661. (7) Weis, P.; Weis, J. S. Effects of heavy metals on development of the killifish Fundulus heteroclitus. J. Fish. Biol. 1977, 11, 49−54. (8) Weis, P. Metallothionein and mercury tolerance in the killifish Fundulus heteroclitus. Mar. Environ. Res. 1984, 14 (1−4), 153−166. (9) Linden, O.; et al. The combined effect of salinity, temperature and oil on the growth pattern of embryos of the killifish, Fundulus heteroclitus Walbaum. Mar. Environ. Res 1980, 3 (2), 129−144. (10) Couillard, C. M. A microscale test to measure petroleum oil toxicity to mummichog embryos. Environ. Toxicol. 2002, 17 (3), 195− 202. (11) Brannon, E. L.; et al. Review of the Exxon Valdez oil spill effects on pink salmon in Prince William Sound, Alaska. Rev. Fish. Sci. 2012, 20 (1), 20−60. (12) Brannon, E. L.; Cronin, M. A.; Maki, A. W.; Moulton, L. L.; Parker, K. R. Oiling effects on pink salmon. In Oil in the Environment: Legacies and Lessons of the Exxon Valdez Oil Spill; Wiens, J. A., Ed.; Cambridge University Press: Cambridge, U.K., 2013; pp 263−291. (13) Craig A. K., Willette, T. M.; Evans, D. G.; Bue, B. G. Injury to Pink Salmon Embryos in Prince William SoundField monitoring. Restoration Project 98191A-1. Exxon Valdez Oil Spill Restoration Project Final Report; Exxon Valdez Oil Spill Trustee Council, Alaska Resources Library and Information Services: Anchorage, AK, 2002. (14) Thedinga, J. F.; Carls, M. G.; Maselko, J. M.; Heintz, R. A.; Rice, S. D. Resistance of naturally spawned pink salmon eggs to mechanical shock. Alaska Fish. Res. Bull 2005, 11, 37−43. (15) Brown, E. D.; Norcross, B. L.; Short, J. W. Introduction to studies on the effects of the Exxon Valdez oil spill on early life history 7678

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