Abstract
The 2010 explosion of the Deepwater Horizon (DWH) oil rig led to the release of millions of barrels of oil in the Gulf of Mexico. Oil in aquatic ecosystems exerts toxicity through multiple mechanisms, including photo-induced toxicity following co-exposure with UV radiation. The timing and location of the spill coincided with both fiddler crab reproduction and peak yearly UV intensities, putting early life stage fiddler crabs at risk of injury due to photo-induced toxicity. The present study assessed sensitivity of fiddler crab larvae to photo-induced toxicity during co-exposure to a range of environmentally relevant dilutions of high-energy water accommodated fractions of DWH oil, and either <10, 50, or 100% ambient sunlight, achieved with filters that allowed for variable UV penetration. Solar exposures (duration: 7-h per day) were conducted for two consecutive days, with a dark recovery period (duration: 17-h) in between. Survival was significantly decreased in treatments the presence of >10% UV and relatively low concentrations of oil. Results of the present study indicate fiddler crab larvae are sensitive to photo-induced toxicity in the presence of DWH oil. These results are of concern, as fiddler crabs play an important role as ecosystem engineers, modulating sediment biogeochemical processes via burrowing action. Furthermore, they occupy an important place in the food web in the Gulf of Mexico.
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References
Alloy MM et al. (2015) Photo-induced toxicity of Deepwater Horizon slick oil to blue crab (Callinectes sapidus) larvae. Environ Toxicol Chem 34:2061–2066
Alloy M et al. (2016) Ultraviolet radiation enhances the toxicity of Deepwater Horizon oil to mahi-mahi (Coryphaena hippurus) embryos. Environ Sci Technol 50:2011–2017
Alloy M et al. (2017) Co-exposure to sunlight enhances the toxicity of naturally weathered Deepwater Horizon oil to early lifkage red drum (Sciaenops ocellatus) and speckled seatrout (Cynoscion nebulosus) Environ Toxicol Chem 36:780–785. https://doi.org/10.1002/etc.3640
Boese BL et al. (1997) Photoinduced toxicity of fluoranthene to seven marine benthic crustaceans. Arch Environ Contam Toxicol 32:389–393
Bridges K et al. (in press) Estimating incident ultraviolet (UV) radiation exposure in the Northern Gulf of Mexico during the Deepwater Horizon oil spill. Integr Environ Assess Manag
Brodie RJ et al. (2007) Larval mortality during export to the sea in the fiddler crab Uca minax. Mar Biol 152:1283–1291
Christy JH (1983) Female choice in the resource-defense mating system of the sand fiddler crab, Uca pugilator. Behav Ecol Sociobiol 12:169–180
Deepwater Horizon Natural Resource Damage Assessment Trustees (2016) Deepwater Horizon oil spill: final programmatic damage assessment and restoration plan and final programmatic environmental impact statement. http://www.gulfspillrestoration.noaa.gov/restoration-planning/gulf-plan
Diamond SA (2003) Photoactivated toxicity in aquatic environments. UV effects in aquatic organisms and ecosystems. Wiley, New York, pp 219–250
Epifanio CE (1995) Transport of blue crab (Callinectes sapidus) larvae in the waters off Mid-Atlantic states. Bull Mar Sci 57:713–725
Epifanio CE et al. (1988) Dispersal and recruitment of fiddler crab larvae in the Delaware River estuary. Mar Ecol Prog Ser 43:181–188
Finch BE, Stubblefield WA (2016) Photo-enhanced toxicity of fluoranthene to Gulf of Mexico marine organisms at different larval ages and ultraviolet light intensities. Environ Toxicol Chem 35:1113–1122. https://doi.org/10.1002/etc.3250
Forth HP et al. (2017a) Characterization of dissolved and particulate phases of water accommodated fractions used to conduct aquatic toxicity testing in support of the deepwater horizon natural resource damage assessment. Environ Toxicol Chem 36:1460–1472
Forth HP et al. (2017b) Characterization of oil and water accommodated fractions used to conduct aquatic toxicity testing in support of the deepwater horizon oil spill natural resource damage assessment. Environ Toxicol Chem 36:1450–1459
Franco ME et al. (2017) Crude oil toxicity to fiddler crabs (Uca longisignalis and Uca panacea) from the northern Gulf of Mexico: impacts on bioturbation, oxidative stress, and histology of the hepatopancreas. Environ Toxicol Chem 37:491–500. https://doi.org/10.1002/etc.3982
Huang X-D et al. (1997) Mechanistic quantitative structure-activity relationship model for the photoinduced toxicity of polycyclic aromatic hydrocarbons: II. An empirical model for the toxicity of 16 polycyclic aromatic hydrocarbons to the duckweed Lemna gibba L. G-3. Environ Toxicol Chem 16:2296–2303
Incardona JP et al. (2012) Potent phototoxicity of marine bunker oil to translucent herring embryos after prolonged weathering. PLoS ONE 7:e30116
Jeffrey WH et al. (1996) Diel and depth profiles of DNA photodamage in bacterioplankton exposed to ambient solar ultraviolet radiation. Mar Ecol Prog Ser 137:283–291
Karentz D (1994) Ultraviolet Tolerance Mechanisms in Antarctic Marine Organisms. In: Weiler CS, Penhale PA (eds) Ultraviolet Radiation in Antarctica: Measurements and Biological Effects. American Geophysical Union, Washington, D. C, pp 93–110. https://doi.org/10.1029/AR062p0093
Lampi MA et al. (2007) A predictive quantitative structure-activity relationship model for the photoinduced toxicity of polycyclic aromatic hydrocarbons to Daphnia magna with the use of factors for photosensitization and photomodification. Environ Toxicol Chem 26:406–415
Morris J et al. (2015) Deepwater Horizon oil spill natural resource damage assessment comprehensive toxicity testing program: overview, methods, and results. Technical Report. Prepared by Abt Associates, Boulder, CO, for National Oceanic and Atmospheric Administration Assessment and Restoration Division, Seattle, WA. 16 December, Section 5.12.2 Technical Reports, https://www.doi.gov/deepwaterhorizon/adminrecord
Mouton Jr. EC, Felder DL (1995) Reproduction of the fiddler crabs Uca longisignalis and Uca spinicarpa in a Gulf of Mexico Salt Marsh. Estuaries Coasts 18:469–481
Newsted JL, Giesy JP (1987) Predictive models for photoinduced acute toxicity of polycyclic aromatic hydrocarbons to Daphnia magna, Strauss (Cladocera, Crustacea). Environ Toxicol Chem 6.:445–461
Oris JT, Giesy JP (1987) The photo-induced toxicity of polycyclic aromatic hydrocarbons to larvae of the fathead minnow (Pimephales promelas). Chemosphere 16:1395–1404
Pelletier MC et al. (1997) Phototoxicity of individual polycyclic aromatic hydrocarbons and petroleum to marine invertebrate larvae and juveniles. Environ Toxicol Chem 16:2190–2199
Ravindra K et al. (2008) Atmospheric polycyclic aromatic hydrocarbons: source attribution, emission factors and regulation. Atmos Environ 42:2895–2921
Roberts AP et al. (2017) Review of the photo-induced toxicity of environmental contaminants. Comp Biochem Physiol C Toxicol Pharmacol 191:160–167
Spehar RL et al. (1999) Comparative toxicity of fluoranthene to freshwater and saltwater species under fluorescent and ultraviolet light. Arch Environ Contam Toxicol 37:496–502
Sweet LE et al. (2017) Exposure to ultraviolet radiation late in development increases the toxicity of oil to mahi‐mahi (Coryphaena hippurus) embryos. Environ Toxicol Chem 36:1592–1598. https://doi.org/10.1002/etc.3687
Tedetti M, Sempéré R (2006) Penetration of ultraviolet radiation in the marine environment: a review. Photochem Photobiol 82:389–397
Thurman C (1982) On the distinctness of the fiddler crabs Uca minx (leconte) and Uca longisignalis salmon & atsaides in their region of sympatry (Decapoda Brachyura, Ocypodidae). Crustaceana 43:37–50
Vasilkov A et al. (2001) Global mapping of underwater UV irradiances and DNA-weighted exposures using total ozone mapping spectrometer and sea-viewing wide field-of-view sensor data products. J Geophys Res Oceans 106:27205–27219
Villafane VE et al. (2004) Annual patterns of ultraviolet radiation effects on temperate marine phytoplankton off Patagonia, Argentina. J Plankton Res 26:167–174
Xue WL, Warshawsky D (2005) Metabolic activation of polycyclic and heterocyclic aromatic hydrocarbons and DNA damage: a review. Toxicol Appl Pharmacol 206:73–93
Zengel S et al. (2016) Deepwater Horizon oil spill impacts on salt marsh fiddler crabs (Uca spp.). Estuaries Coasts 39:1154–1163
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This study was conducted within the Deepwater Horizon Natural Resource Damage Assessment (NRDA) investigation, which was cooperatively conducted by NOAA and other Federal and State Trustees. The scientific results and conclusion of this publication are those of the authors and do not necessarily represent the view of NOAA or any other natural resource Trustee for the BP/Deepwater Horizon NRDA.
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Damare, L.M., Bridges, K.N., Alloy, M.M. et al. Photo-induced toxicity in early life stage fiddler crab (Uca longisignalis) following exposure to Deepwater Horizon oil. Ecotoxicology 27, 440–447 (2018). https://doi.org/10.1007/s10646-018-1908-6
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DOI: https://doi.org/10.1007/s10646-018-1908-6