Ecotoxicology and Environmental Safety

www.elsevier.com/locate/ecoenv Ecotoxicology and Environmental Safety Editor Kurunthachalam Kannan Wadsworth Center, New York State Department of Health and Department of Environmental Health Sciences, State University of New York at Albany, New York, USA Associate Editors Richard D. Handy Paul Sibley Hyo-Bang Moon University of Plymouth School of Environmental Sciences Associate Professor Department of Biology University of Guelph Marine Environment Analytical Plymouth, Guelph, Ontario Laboratory (MEAL) Devon PL4 8AA N1G 2W1 Dept. of Marine Sci. and United Kingdom Canada Convergent Tech., Hanyang University, Korea Editorial Board Shashi Bhushan Agrawal Taisen Iguchi Ann Miracle Irena Twardowska Fernando Barbosa Jr Hisato Iwata Haruhiko Nakata Paule Vasseur Swaran J. S. Flora D. Johnson Jae-Sung Rhee Wen-Xiong Wang C.A.M. van Gestel Rai S. Kookana Susan Shaw Po-Keung Wong Helmut Greim Yi-Fan Li Louis A. Tremblay Tao Zhang Ecotoxicology and Environmental Safety 146 (2017) 1–3 Contents lists available at ScienceDirect Ecotoxicology and Environmental Safety journal homepage: www.elsevier.com/locate/ecoenv Editorial ff Following the Deepwater Horizon oil spill: What we know about the e ects of MARK oil on birds? The April 20, 2010 explosion and subsequent sinking of the Deepwater Horizon (DWH) mobile drilling unit in Mississippi Canyon Block 252 (MC252) resulted in 11 fatalities and the release of an unprecedented volume of South Louisiana sweet crude oil (507 million liters) into the Gulf of Mexico (GOM). This oil covered an area of 112,100 square kilometers, including more than 10% of the GOM shoreline. The Natural Resource Damage Assessment (NRDA) Trustee Council for this spill, which included the US Department of Interior, US Environmental Protection Agency, Department of Commerce, Department of Agriculture and the five affected states, conducted injury assessment activities from 2010 to 2015. Included as one of these injury assessments was the development of an avian toxicity testing program developed by the US Fish and Wildlife Service (USFWS) as part of their avian injury assessment program (for the full funding application see: https://www.doi.gov/sites/doi.gov/files/migrated/deepwaterhorizon/upload/AvianToxicity.pdf. Unlike many previous oil spills, the DWH event occurred for an extended period in warm waters resulting in both bird deaths and large numbers of birds that were observed alive. The Live Oiled Bird Model (LOBM) was developed by USFWS as a means of estimating injury to those groups of birds. One of the primary requirements for this model was a determination of the “fate” of the oiled birds. That is, the likelihood a bird would suffer adverse effects from oiling or die. Unfortunately, while there is was an extensive body of literature available from which to draw conclusions on the effects of heavy oiling on birds, the literature available for assessment of the adverse outcomes for birds with light to moderate oil coverage was largely unquantified prior to DWH. As part of their injury assessment, USFWS initiated the “Blood Physiology Study” (https://www.doi.gov/sites/doi.gov/files/migrated/ deepwaterhorizon/upload/Final-DOI-NRDA569AP-1-July-2011-2.pdf) to determine if there was a link between lighter oiling categories and one of the better understood toxic effects of ingested oil, hemolytic anemia. In an important migratory stopover point such as the GOM, this particular sublethal endpoint could have broad adverse impacts on flight ability and migratory success. Although limited in scope, the “Blood Physiology Study” did suggest that birds collected from oiled areas were suffering from hemolytic anemia in the form of reduced packed cell volume, and increased incidence of reticulocytes and Heinz bodies, regardless of whether oil was visible on their feathers or not. This study could not provide a definitive link between exposure to MC252 oil and toxicity. As a result, the USFWS commissioned a series of expert panels to provide input on planning a series of experimental studies that would accurately characterize the toxic effects of MC252 oil on birds. Studies were planned that would attempt to fill some of the gaps in our understanding of oil toxicity to birds and the adverse outcomes to flight abilities (refer to https://www.doi.gov/sites/doi.gov/files/migrated/deepwaterhorizon/upload/AvianToxicity.pdf for full study plans). In brief these studies were divided into oil ingestion studies that would attempt to produce comprehensive dose-response relationships between oil ingestion rates and the development of sublethal adverse outcomes, and studies that would explore the nature of the effects of oil on flight and thermoregulation. The initial goals of these studies were very broad due to the unknown experimental factors such as the exact nature of the toxicity of MC252 oil, the specific toxicological responses of the species involved and the more general issue of dose delivery of a noxious substance that requires ingestion. As these studies were part of the larger NRDA being undertaken by USFWS, they were conducted within the limitations of litigation sensitive work, including stringent quality assurance/quality control (QA/QC) and sample and data retention, which unfortunately somewhat limited the number of experiments that could be conducted within the time frame for the NRDA. However, the benefits of such work include access to samples and data for the larger scientific community. Nonetheless, these studies were able to build on previous oil toxicity studies to develop dosing methods that will be of great use to future studies of oil toxicity, and provide a more in-depth understanding of the adverse outcomes on avian physiology and flight behavior. The first set of studies suggested by the expert panels were pilot oral dosing studies to determine if methods described in the literature were applicable to the species available/chosen for study. Earlier oral ingestion studies were either conducted through gavage of juvenile or subadult birds for short periods of time or through feeding trials for longer duration studies. In general, accurate dosing was difficult due to issues with regur- gitation or rapid elimination. These same issues were experienced with the oral dosing studies designed for the DWH avian toxicity testing program. All four species tested in the pilot oral dosing study (Dean et al., 2017a) either regurgitated the oil, as in the homing pigeon, or displayed rapid defecation (western sandpiper, laughing gull and double-crested cormorant). Despite the challenge of accurate dosing during these studies, there were changes in blood chemistry and oxidative stress markers in the double-crested cormorant that indicated early stages of oil toxicity. De- termination of hemolytic anemia was somewhat hampered by a lack of agreement between slide readers on the presence and number of Heinz bodies present in the samples collected, resulting in a shift to the use of electron microscopy for definitive proof of Heinz body identification for each species. Further modifications were made to dosing methods for the western sandpiper, laughing gull and double-crested cormorant to determine if http://dx.doi.org/10.1016/j.ecoenv.2017.08.068 Available online 09 September 2017 0147-6513/ © 2017 Published by Elsevier Inc. Editorial Ecotoxicology and Environmental Safety 146 (2017) 1–3 better oral dose delivery could be achieved. Oral dose delivery method development was not continued because the field flight work showed that a single application of oil to feathers caused irreversible damage to feather structure in this species, making investigation of changes in flight performance without toxicity a priority for the NRDA, as some migratory birds would have experienced similar light oiling during stopover. Western sandpiper dosing methods could not be changed because the only additional option for dosing was to inject oil into meal worms, and this resulted in significant leakage of oil from the meal worms. Instead the method was altered to reduce daily dose amount and increase the period of exposure. Once again there were few changes in standard plasma biochemistry measurements, but due to the success of the pigeon flight work, a switch was made to focus on the effects of oil applied to feathers on flight and thermoregulation in western sandpipers. Further method development for direct oral dosing of laughing gulls was achieved through injection of oil into the body cavity of dead feeder fish that made up part of the captive diet (Horak et al., 2017). Laughing gulls, like many other species of gulls, can take advantage of variations in food sources, and as such they are adept at discerning the quality of food resources. In our case this meant that if oil was detected by the birds, through visual, olfactory or taste cues, the birds were unlikely to consume the treated fish. This presented a considerable challenge for the scientists and technical staff tasked with dosing, and while they were able to achieve dosing rates comparable to the nominal doses, it was not without intensive work on the part of the researchers, making the dosing method in its current state very difficult to replicate for this species. The study was successful in that the direction of the endpoint changes observed for laughing gulls was similar to that observed in the double-crested cormorants, but to a lesser extent. Further method development for oral dosing is required in this species to determine if results were confounded due to dose delivery, or if this particular species is not as sensitive to the effects of oil. In the case of the double-crested cormorants, fingerling catfish readily survived injection of oil into the body cavity under anaesthetic (Cunningham et al., 2017). These fish were consumed normally by the cormorants throughout the course of the day, achieving dose rates similar to nominal doses. Dosing at the higher rate of 10 ml/kg body weight/day resulted in anemia by day 7 and oil intoxication by day 14 of dosing, indicating that this method of oral dosing was suitable for this species.

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