Ecological Impacts of the Deepwater Horizon Oil Spill: Implications for Immunotoxicity

The Deepwater Horizon (DWH) oil spill was the largest environmental disaster and response effort in U.S. history, with nearly 800 million liters of crude oil spilled. Vast areas of the Gulf of Mexico were contaminated with oil, including deep-ocean communities and over 1,600 kilometers of shoreline. Multiple species of pelagic, tidal, and estuarine organisms; sea turtles; marine mammals; and birds were affected, and over 20 million hectares of the Gulf of Mexico were closed to fishing. This article summarizes major federal and multistakeholder research efforts in response to the DWH spill, including laboratory oil dispersant testing, estimation of oil release rates and oil fate calculations, subsea monitoring, and postspill assessments. Impacts from shoreline oiling and wildlife exposures and the results of coastal condition assessments are summarized. Finally, implications of the Gulf oil spill for immunotoxicity to aquatic invertebrates, fish, birds, and mammals are discussed.

Ecological Impacts of the Deepwater Horizon Oil Spill:
Implications for Immunotoxicity
MACE G. BARRON
U.S. Environmental Protection Agency, ORD/NHEERL/GED, Gulf Breeze, Florida, USA
ABSTRACT
The Deepwater Horizon (DWH) oil spill was the largest environmental disaster and response effort in U.S. history, with nearly 800 mill
of crude oil spilled. Vast areas of the Gulf of Mexico were contaminated with oil, including deep-ocean communities and over 1,600 kilom
shoreline. Multiple species of pelagic,tidal,and estuarine organisms; sea turtles; marine mammals; and birds were affected,and over 20 million
hectares of the Gulf of Mexico were closed to fishing. Several large-scale field efforts were performed, including assessments of shoreline
life oiling and of coastal waters and sediments. The assessment of injuries, damages, and restoration options for the DWH spill is ongoing
petroleum and the polycyclic aromatic hydrocarbon component of oils are known to affect the immune systems of aquatic organisms and
immunotoxicity is not typically assessed during oil spills and has not been a focus of the DHW assessment. The effects of oil spill contam
immune responses are variable and often exposure dependent, but immunotoxic effects seem likely from the DHW spill based on the rep
of a variety of oils on both aquatic and wildlife species.
Keywords: oil spill; immunotoxicity; polycyclic aromatic hydrocarbons; environmental assessment.
INTRODUCTION
The Deepwater Horizon (DWH) oil rig exploded on April 20,
2010, initiating the discharge of over 800 million liters of oil into
the Gulf of Mexico over approximately three months (Table 1
and Figure 1).The DWH spill was the largest environmental
disaster and response effort in U.S. history and the second larg-
est oil spill in human history (Levy and Gopalakrishnan 2010;
National Commission 2011; Carriger and Barron 2011). Nearly
7 million liters of chemical dispersants were used, and for the
first time oil dispersants were used in deep-sea environments
(Table 1). This article summarizes major federal and multistake-
holder research efforts in response to the DWH spill, including
laboratory oil dispersant testing, estimation of oil release rates
and oil fate calculations,subsea monitoring,and postspill
assessments.Impacts from shoreline oiling and wildlife expo-
sures and the results of coastal condition assessments are summar-
ized. Finally, implications of the Gulf oil spill for immunotoxicity
to aquatic invertebrates, fish, birds, and mammals are discussed.
EPA DISPERSANT TESTING
One of the major areas of concern during the DWH spill was
the continuing application of large volumes of dispersant, both
in the deep ocean and in offshore surface areas of the Gulf of
Mexico. A total of 4 million liters of chemical dispersant was
used on the surface in over 400 air sorties,while 2.9 million
liters were applied at the well head. There were also concer
that some dispersants on the National Contingency Plan Pro
uctSchedule (U.S.EnvironmentalProtection Agency [EPA]
2011) contained constituents such as nonylphenol ethoxyla
that could degrade to endocrine-disrupting compounds.
The EPA (2011) performedtwo phasesof laboratory
dispersant toxicity testing during the DWH spill to suppleme
existing dataavailableon the productschedule.Phase1
involved testing eight dispersants using standard toxicity bi
says with a fish and aquatic invertebrate species, as well as
vitro mammalian cellline assays(Hemmer,Barron,and
Greene 2011; Judson et al.2010).Phase 2 of the EPA’s spill
response testing determined the acute toxicity to two Gulf o
Mexico estuarine species of the eight dispersants mixed wit
South Louisiana crude oil.In vitro testing was focused on
determining ifany ofthe eightcommercialdispersants had
estrogenic or androgenic activity, as well as any activity in o
biological pathways,using a large battery of cell line assays.
Overall, no activity was observed in any androgen assay, tw
dispersants showed a weak estrogenic signal in one assay,
all dispersantsshowed minimalcytotoxicity (Judson etal.
2010).
Consistenttestmethodologies within a single laboratory
were used to assess the relative acute toxicity of the eight d
persants, including Corexit 9500A, the predominant dispers
applied during the DWH spill. Static acute toxicity tests wer
performed using mysid shrimp (Americamysisbahia)and
ray-finned fish,inland silverside (Menidia beryllina).For all
eight dispersants in both test species, the dispersants alone
less acute toxicity (3 to >5,600 ppm) than the mixtures of d
persant with South Louisiana crude oil (0.4–13 mg total petr
leum hydrocarbons/L). The acute toxicity to mysids (2.7 mg
Addresscorrespondenceto: Mace G. Barron, U.S. Environmental
ProtectionAgency,ORD/NHEERL/GED, 1 SabineIsland Drive, Gulf
Breeze, FL 32561; e-mail: [e-mail].
The author(s) declared no potential conflicts of interests with respect to the
authorship and/or publication of this article. The author(s) received no financial
support for the research and/or authorship of this article.
Abbreviations:DWH, DeepwaterHorizon;PAH, polycyclicaromatic
hydrocarbon; OPA, Oil Pollution Act.
315
Toxicologic Pathology,40: 315-320,2012
Copyright # 2012 by The Author(s)
ISSN: 0192-6233 print / 1533-1601 online
DOI: 10.1177/0192623311428474

and Menidia (3.5 mg/L) of South Louisiana crude oil was sim-
ilar to acute toxicity of the dispersant–oil mixtures. The results
were consistent with data available on the product schedule and
indicated that the toxicity of Corexit 9500A was generally sim-
ilar to other available dispersants when tested alone and as a
mixture with oil (Hemmer, Barron, and Greene 2011).
A laboratory efficacy study also was undertaken to determine
the effectiveness of the eight selected dispersants currently avail-
able on the product schedule (EPA, 2011). Tests were performed
on South Louisiana crude oilat 5 C to representtemperature
conditions for the deep-sea dispersant injection and 25C to rep-
resentsurface application conditions.The results showed that
only three of the eightdispersants,including Corexit9500A,
were more than 70% effective underoptimallaboratory test
conditions.
FLOW RATE ESTIMATES AND OIL BUDGET CALCULATIONS
The spill rates of the oil were highly uncertain during the
first eight weeks of the spill, with government and independent
scientistestimates generally increasing theirestimates from
0.8 to 9.5 million liters per day . A consensus estimate of th
Flow Rate Technical Group based on high-resolution videogr
phy, 9.8 million liters per day, was used in the calculation of
oil budget(FederalInteragency Solutions Group,2010).The
fate of the released oil was calculated by the team of scient
and engineersin the FederalInteragency SolutionsGroup
(2010),based on estimates of leak rate and surface behavior
dissolution, evaporation, weathering by emulsification, natu
and chemicaldispersion,in situ burning,and mechanical
recovery. Table 2 shows best-case, expected, and worst-cas
mates of oil fate from response efforts (i.e., mechanical reco
chemicaldispersion,burning),naturalprocesses (i.e.,physical
dispersion, evaporation, dissolution), and the amount of res
oil. These calculations show thatabout20% ofthe oilwas
recovered at the well head or through skimming and about
dissipated through natural processes (Table 2). There was h
uncertainty in the amount of oil chemically dispersed (10–2
and remaining as residual oil (11–30%) (Table 2).
SUBSEA PLUME ASSESSMENT
An extensive assessment of deep-water plume size and t
jectory, and potential dissolved oxygen depressions due to
degradation and dispersion,was conducted during the DWH
spill. These subsea oceanographic assessments were perfor
TABLE 1.—Timeline of spill events and response actions of the BP
Deep Water Horizon (DWH) oil spill.
2010 Event and action
April 20 DWH rig explosion
April 25–30 Blowout preventer failure
Leak estimates to 0.8 million L/day
First oil reaches shorelines
First in situ burning
May 2–7 Leak estimates to 4 million L/day
First fishery closures
First relief well started, 110 million L oil in gulf
Containment dome failure/crystals
Shoreline booming begins
May 14–18 Riser intubation 20% collection
Fishery closures expanded
Deep-water dispersion
250 million L leaked
May 26–30 ‘‘Top kill’’ attempted, abandoned
380 million L leaked
Declared largest U.S. environmental disaster
Oiled wildlife reports increase
June 1–5 ‘‘Cut and cap’’ attempted
450 million L leaked
Fishery closures in approximately 40% of gulf
June 9–15 Deep-water plumes detected
Relief well drilling continues
Leak rate estimates increased to 9.5 million L/day
June 23–30 BP response costs at $2.4 billion
Hurricane Alex halts cleanup efforts
Pensacola Beach oiled; 640 million L leaked
Dispersant use continues (6.9 million L total)
July 11–16 New cap stops flow
800 million L spilled oil
July 22–27 Evacuation from Tropical Storm Bonnie
August 2–8 ‘‘Static kill’’ successful
Relief wells continue
September 19þ Well declared dead
Cleanup continues
Limited fishery closures
FIGURE 1.—Cumulative Deepwater Horizon oil distribution in the Gu
of Mexico (days oilpresent).Image downloaded August2011from
www.GeoPlatform.gov/gulfresponse.
TABLE 2.—Estimates of oil fate (best case, expected, worst case) as
percentage of the cumulative volume discharged during the
Deepwater Horizon spill (Federal Interagency Solutions Group 201
Oil fate Best case Expected Worst case
Direct recovery from well head 17 17 16
Naturally dispersed 13 13 12
Evaporated or dissolved 20 23 25
Chemically dispersed 29 16 10
Burned 6 5 5
Skimmed 4 3 2
Residual 11 23 30
316 BARRON TOXICOLOGIC PATHOLOGY

by the Joint AnalysisGroup (JAG 2011),consisting ofa
working group of multiple governmentagencies,the private
sector, and acadamia. JAG (2011) concluded that fluorescence
spectroscopy, dissolved oxygen, petroleum chemistry, and par-
ticle size verticalprofileswere indicative ofa deep-water
plume at 1,100 to 1,400 meters that was consistent with water
movement patterns near the well head.JAG (2011) also con-
cluded thatsubseadissolved oxygen depressionsdid not
approach hypoxic levels and were stable after July 28, 2010.
POSTSPILL ASSESSMENT
Large-scale sampling,monitoring,and assessmentof sub-
sea,onshore,and offshore waterand sedimentdata were
directed by the OperationalScience Advisory Team (OSAT
2010) to guide postspill oil removal. OSAT included represen-
tatives from BP and severalfederalagencies who compiled,
analyzed,and interpreted data (available as ofOctober23,
2010) from thousands of samples,research cruises,and field
efforts. The findings of OSAT (2010) included no deposits of
liquid-phase DWH oilbeyond the shoreline,no exceedences
of human health or dispersanttoxicity benchmarks,and less
than 1% incidence of water and sediment samples exceeding
aquatic toxicity benchmarks. OSAT (2010) concluded that the
DWH oil was weathering, but oil degradation rates were vari-
able. Of the over 20 million hectares (approximately 40%) of
closed fisheries in the Gulf of Mexico, the majority of state and
federal waters had been reopened. Deposits of oil entrained in
drilling mud and polycyclic aromatic hydrocarbon (PAH) con-
centrations exceeding aquatic toxicity benchmarks remained
within 3 kilometers of the well head. Tar mats in shallow near-
shore waters were identified as a sampling gap needing further
investigation (OSAT 2010).
A second OSAT (2011) assessment was conducted specifi-
cally to determine if beach cleanup should continue.OSAT
(2011) reported that 80% of PAHs in the residual oil present
in the beach environmenthad been depleted,and there were
minimal risks of leaching of buried oil. The report concluded
that there would be greater impacts to wildlife from continuing
beach cleanup compared with leaving the residual oil in place.
There were continuing risks to shore birds from ingestion of
residual oil (e.g., tar balls) and to the eggs and hatchlings of sea
turtles from buried oil (OSAT 2011).
IMPACT ASSESSMENT
Shoreline Oiling
More than 1,600 kilometers of Gulf of Mexico shoreline was
visibly oiled during the DWH spill (Figure 2). Maximum oiling
occurred along the shorelines and barrier islands of Louisiana,
Mississippi,Alabama,and western Florida,as wellas in the
wetland areas ofLouisiana (e.g.,Barataria Bay).Shoreline
cleaning and naturalprocesseshave removed a substantial
amount of the oil from these areas,leaving a limited number
of areas with cleanup still in progress (Figure 2).
Wildlife Oiling
Reported wildlife oiling during the DWH spillincluded
observations of oiled birds, sea turtles, and dolphins (Figure
There were nearly 10,000 bird observations,including 2,085
categorized as visibly oiled alive and 2,303 visibly oiled dea
(U.S. Fish and Wildlife Service 2011).Figure 4 shows the
spatial distribution of sea turtle observations,with most dead
turtles observed near shore and live turtles observed off sho
Oil impacts on marine mammals included 140 dead animals
and numerous dolphin strandings (Figure 3 and Figure 5).
FIGURE 2.—Maximum shoreline oiling observed during the Deepwat
Horizon spill(top panel)and shorelinecleanup progressas of
January 2011 (lower panel).Image downloaded August2011 from
www.GeoPlatform.gov/gulfresponse.
FIGURE 3.—Cumulative wildlife oiling observations reported to the
Unified Area Command (UAC) during the Deepwater Horizon spill.
Summarized from U.S. Fish and Wildlife Service (2011).
Vol. 40,No. 2, 2012 GULF OIL SPILL IMPACTS 317

Coastal Condition
The impacts ofthe DWH spillon the condition ofnear
coastalareas and estuaries were assessed using a variety of
sedimentand waterquality indicators,including analytical
chemistry measurements in water,sediment,and tissues,and
benthic organism surveys and toxicity testing.Sampling was
performed between Apriland September,with the indicators
(including specific chemicalanalytes)and sample locations
varying across the surveys. Baseline information was available
from previous regional surveys (e.g., EPA 2008). Comparison
of the condition information across surveys indicated some
impacts during the spill but minimal impacts after the well was
capped (OSAT 2010).
Natural Resource Damage Assessment
The Oil Pollution Act of 1990 (OPA) establishes liability for
the discharge and substantialthreatof a discharge of oilto
navigable waters and shorelines.A major goalof OPA is to
restore the natural resources and services that are lost as a result
of oil spills.The responsibility foracting on behalfof the
public lies with designated federal,state,tribal,and natural
resource trustees. OPA directs trustees to return injured natural
resources and services to the condition they would have been in
if the incident had not occurred and to recover compensation
for interim lossesof such naturalresourcesand services
through the restoration, rehabilitation, replacement, or acquisi-
tion of equivalent natural resources or services.
The trustees for the DWH spillinclude the U.S.Depart-
ments of Commerce, Interior and Defense and the five affected
states (Texas,Louisiana,Mississippi,Alabama,and Florida).
The Natural Resource Damage Asssessment is ongoing and has
included over 90 offshore cruises and 30,000 samples of water,
sediment,tissues,and oil from the deep-ocean,offshore,and
coastal areas (National Oceanic and Atmospheric Association
and U.S. Department of the Interior 2011). Transmitters have
been placed in whale sharks,bluefin tuna,and sperm whales
to assess exposures to pelagic species. Other activities inclu
complex modeling ofoil distribution,fate,and effects and
toxicity testing of multiple species.Over 7,000 kilometers of
shoreline have been surveyed for oil impacts. The conclusio
of the Natural Resource Damage Assessment are not expec
for several years (Carriger and Barron 2011).
IMPLICATIONS FOR IMMUNOTOXICITY
Oil and the PAHs present in oil are known to be immuno-
toxic in a diversity ofaquatic and wildlife species (Briggs,
Gershwin,and Anderson1997;Gallowayand Depledge
2001; Jenssen 1996; Reynaud and Deschaux 2006). Howeve
there is generally limited information on immune responses
relative to other endpoints monitored in oil spills. The immu
systems of vertebrates, including fish, appear to be conserv
across species,whereas invertebrate immune systems appear
more primitive (Galloway and Depledge 2001;Reynaud and
Deschaux 2006).Studies have shown thatboth the adaptive
and innate immune systemsof vertebratesrespond to oil
exposure,with apparentmechanisms ofaction thatinclude
P450-mediated biotransformation,aryl hydrocarbon receptor
binding,and calcium mobilizaton (Reynaud and Deschaux
2006).The adaptive,specific immunity and lymphoid path-
waysappearto be absentin invertebrates(Galloway and
Depledge 2001).Phagocytosisappearsto be importantin
invertebrate immune responses,as are circulating hemocytes.
Invertebrates also appear to have cytotoxic reactions simila
to the naturalkiller cells of vertebratesand have proteins
similar to cytokines (Galloway and Depledge 2001).
A diversity of immunotoxic responses has been assessed
and PAH exposures, with selected examples shown in Table
The results are often contraditory,with immunosuppression,
inflammation,hemolyticanemia,decreased leukocytesand
FIGURE 4.—Spatial distribution of live and dead sea turtles observed
during theDeepwaterHorizon spill.Imagedownloaded August
2011 from www.GeoPlatform.gov/gulfresponse.NMFS ¼ National
Marine Fisheries Service. FIGURE 5.—Spatialdistributionof marinemammalstrandings
observed during the DeepwaterHorizon spill.Image downloaded
from August2011 www.GeoPlatform.gov/gulfresponse.NMFS ¼
National Marine Fisheries Service.
318 BARRON TOXICOLOGIC PATHOLOGY

phagocytes, and impaired phagocytosis appearing to be common
responses across species (Table 3). The immunotoxic effects of
petroleum are correlated with the PAH component of oil and
are exposureand speciesdependent(Payneand Fancey
1989; Reynaud and Deschaux 2006). Studies with aquatic inver-
tebrateshaveshown impaired cellularimmunity.Sensitive
immunotoxic responses in fish exposed to petroleum products
and PAH include macrophage respiratory burst and lymphocyte
proliferation (Reynaud and Deschaux 2006).Cell-mediated
immunity seems to be a sensitive endpoint in oiled birds, whereas
antibody production appears less sensitive to oil exposure. Recent
studies in both fish and mammals exposed to heavy petroleum
show modulation of expression of immune system–related genes
(Bowen et al. 2007; Mos et al. 2008; Nakayama et al. 2008).
Although petroleum and the PAH componentof oils are
known to affect the immune systems of aquatic organisms and
wildlife,immunotoxicity is not typically assessed during oil
spills. Immunotoxiceffectsdo not appearto have been
assessed or reported during the DHW spill,and it is unclear
if they are being assessed in the NaturalResource Damage
Assessment.Immunotoxic effects seem likely based on the
reported effects of a variety of oils on both aquatic and wild-
life species.Possibleecologicalimpactsfrom the DWH
resulting from immunotoxicity may include impaired diseas
resistance and increased parasitism that could lead to slowe
population recoveries.
ACKNOWLEDGMENTS
I thank my many EPA colleagues who worked on the DWH
spill, with special thanks to Michael Hemmer, Virginia Engle
Jan Kurtz, Robyn Conmy, Albert Venosa, John Carriger, Gre-
gory Wilson, and Marc Greenberg for discussions and inform
tion included in this article. I thank the Society for Toxicolog
Pathology for the invitation to present this work, and my EP
colleagues Deborah Vivian for graphical support, Steve Jord
for editing, and Douglas Wolf for review. This is GED contri-
bution 1433. The opinions expressed in this work are those
the author and do not represent the policies or opinions of t
U.S. EPA.
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