GoMRI-sponsored Special Section Articles
Effects of Oil on Terrestrial
Vertebrates: Predicting Impacts
of the Macondo Blowout
CHRISTINE M. BERGEON BURNS, JILL A. OLIN, STEFAN WOLTMANN, PHILIP C STOUFFER,
AND SABRINA S. TAYLOR
In addition to external oiling, marine oil spills may affect vertebrate animals through degradation of habitat; alterations in food web structure;
and contamination of resources by toxic compounds, including polycyclic aromatic hydrocarbons. These processes are not well understood for
vertebrates breeding and foraging in terrestrial ecosystems affected by oil, such as coastal marshes that were heavily oiled following the 2010
Macondo oil spill. Here, we review what is known about the ecological and physiological effects of oil exposure on vertebrates in general. We then
apply these concepts to salt-marsh vertebrates, with special reference to our ongoing monitoring of impacts and recovery in the seaside sparrow
(Ammodramus maritimus) and marsh rice rat (Oryzomys palustris) in Louisiana following the Macondo spill.
Keywords: coastal ecosystem, salt marsh, oil well blowout, trophic ecology, toxicology
T
he 2010 BP Deepwater Horizon (DWH) oil spill at the Macondo well was one of the worst environmental disasters to affect the United States and one of the largest marine
oil spills in history. The spill released an estimated 4.9 million
barrels (nearly 80,000,000 liters) over 87 days into the Gulf of
Mexico (GOM). The combination of depth (approximately
1600 meters [m]) and distance from shore (approximately
70 kilometers [km] south of the Louisiana coast) allowed
crude oil from the Macondo well to disperse widely, with
vast amounts reaching shorelines along the northern GOM.
Macondo oil in various states of degradation was detected
on shorelines of all five US states bordering the GOM for
many months after the well had been capped. The most
extreme oiling, however, occurred in the coastal marshes of
southeastern Louisiana, causing justifiable concern for species inhabiting these areas (Mendelssohn et al. 2012, Michel
et al. 2013).
The initial acute and often lethal effects of marine oil
spills on vertebrate organisms result from direct contact
with oil. Following oil spills, attention is naturally focused
on charismatic species, such as visibly oiled brown pelicans
(Pelecanus occidentalis). External oiling of seabird plumage
can result in reduced water-repellant properties, inadequate
thermoregulation, and death (Jenssen 1994). Mammals, particularly those with fur, can also suffer from external oiling
(Garshelis 1997). Other effects of acute oil exposure include
a compromised ability to deal with natural stressors, such
as compensation for oxygen deficiency by fish in hypoxic
areas (Whitehead 2013). These acute immediate effects of oil
spills on vertebrates are often devastating to individuals and
populations and are widely reported to the public, but they
may be relatively short lived.
The nonlethal effects associated with crude oil exposure
may not be immediately apparent, but they have the potential to persist for many years. Toxicity from chronic exposure to weathering oil (e.g., via ingestion of contaminated
items) can induce physiological responses—for example,
immunosuppression (Malcolm and Shore 2003). In addition,
because many vertebrates are top consumers, they are particularly vulnerable to habitat and trophic-level alterations
arising from damage to habitat structure and prey communities (Velando et al. 2005). Both the physiological and
ecological effects of oil on vertebrates can have important
consequences for fitness. As with acute effects, research on
chronic effects in vertebrates has largely been focused on
marine species, because oil spills of large magnitude generally occur in marine systems. In the case of the Macondo
blowout, however, approximately 1700 km of coastline was
oiled across the GOM, with 44.9% of the oiling occurring on
marsh habitat (50.8% on beaches, 4.3% on other shoreline
types) and 94.8% of all marsh oiling occurring in Louisiana
(Michel et al. 2013), posing risks for species inhabiting these
areas. Moreover, high organic carbon content and oftenanoxic conditions in marsh sediments can limit microbial
BioScience 64: 820–828. © The Author(s) 2014. Published by Oxford University Press on behalf of the American Institute of Biological Sciences. All rights
reserved. For Permissions, please e-mail: [email protected].
doi:10.1093/biosci/biu124
820 BioScience • September 2014 / Vol. 64 No. 9
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degradation, which can facilitate the persistence of oil contamination (Reddy et al. 2002). The extent of oiling and the
potential for persistence of oil in marshes highlight the need
to document the long-term responses of salt-marsh terrestrial vertebrate species.
Here, we provide a broad overview of known chronic
physiological and ecological effects of oil on vertebrates,
focusing on mammals, birds, reptiles, and amphibians.
Given the paucity of data from terrestrial systems, we provide a framework for identifying such effects in terrestrial
vertebrate species in particular, especially those with a high
risk of exposure to oiled habitats following the DWH spill.
We introduce our ongoing studies on two abundant species
that reside in salt marshes along the northern GOM year
round: the seaside sparrow (Ammodramus maritimus) and
the marsh rice rat (Oryzomys palustris).
Physiological effects of oil on terrestrial vertebrates
There are several classes of molecular hydrocarbons present
in crude oil. One group, the aromatics (including polycyclic
aromatic hydrocarbons [PAHs]), poses a significant threat
to wildlife because of toxic and mutagenic effects (Akcha
et al. 2003). Both the chemical composition and the toxicity
of oil can change as it degrades in the environment (e.g., via
weathering by microbes). However, contaminants such as
PAHs are some of the last components of oil to degrade and
can persist in the environment for many years, even where
oil is no longer visually apparent (Mendelssohn et al. 2012).
Uptake and metabolism. In order for oil metabolites to have a
direct biological effect on terrestrial vertebrates, they must
enter the individual, typically via ingestion, inhalation, or
absorption (Smith et al. 2007). For most organisms, the
primary route of PAH exposure in oil-affected habitats is
through the ingestion of contaminated soils, sediments, and
diet items. Consequently, species that feed heavily on sediment-associated invertebrates tend to be at greater risk of
PAH exposure relative to higher-order consumers (Brooks
et al. 2009). However, PAHs seldom exhibit food web bioaccumulation and biomagnification; therefore, their potential
for transfer up the food chain is limited (Neff 1979). This
is primarily associated with the increased capacity of vertebrates, including birds and mammals, to metabolize and
subsequently eliminate PAH residues.
PAHs can be detected soon after exposure across a wide
range of vertebrate organisms and tissues. For example,
field studies have identified PAHs in the blood of birds
(e.g., Alonso-Alvarez et al. 2007) and in turtle eggs (e.g.,
Holliday et al. 2007), and lab work has detected PAHs in
snake skins (Jones et al. 2009). Following their uptake,
PAHs are metabolized by hepatic cytochrome P450 (CYP)
oxygenase or mixed-function oxygenase enzymes (Oris and
Roberts 2013). Metabolism can also occur in ovo (Malcolm
and Shore 2003). Because of this biotransformation, direct
measurement of oil components such as total PAH in tissues is not always an accurate reflection of exposure. Rather,
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the various isoforms of CYP (e.g., CYP1A) or CYP-related
enzymes (e.g., ethoxyresorufin-O-deethylase [EROD]) that
are upregulated in the presence of PAH are often used as
indirect biomarkers of crude oil or PAH exposure (e.g.,
Head and Kennedy 2007). For example, captive rats exposed
to crude oil showed a dose-dependent increase in several
hepatic CYP-linked enzymes (Khan et al. 2001). Field studies
of sea ducks potentially exposed to crude oil from the Exxon
Valdez spill indicated elevated levels of these biomarkers in
oiled areas even decades later (e.g., Esler et al. 2010).
Toxicity in terrestrial vertebrates. Although molecular biomarkers
such as CYP1A can be indicative of relative PAH exposure,
they alone may not imply harm or biological significance
(Oris and Roberts 2013). Adverse health effects associated
with PAH exposure often result from the formation of PAH
metabolites, which have been demonstrated to be genotoxic
(Neff 1979). Specifically, these metabolites can bind to and
damage DNA, forming DNA adducts (i.e., the binding of
DNA to a chemical contaminant). For example, captive rats
exposed to naturally contaminated soils with a wide range
of PAHs were found to have a subset of these PAHs in the
liver and significant upregulation of EROD, and induction of
DNA adducts resulted (Fouchécourt et al. 1999). If the DNA
adduct is not repaired, otherwise normal cells can malfunction, leading to mutations and cancer (Akcha et al. 2003).
Other recognized toxic effects of PAH on vertebrates include
reproductive dysfunction, immunosuppression, and edema
(Malcolm and Shore 2003). However, most of what is known
about PAH metabolism comes from captive studies, in which
dosing may not reflect natural levels. There are relatively few
field studies of toxicity that link physiological consequences
with vertebrate exposure to PAHs. This is particularly true for
terrestrial species, and most of this work has been conducted
on birds. For instance, a study of yellow-legged gulls (Larus
michahellis) following the Prestige oil spill near Spain found
blood parameters indicative of hepatic and renal damage in
adults from oiled colonies, some of which correlated with
total PAH present in blood (Alonso-Alvarez et al. 2007).
Similar work was conducted on marine species following the
Exxon Valdez oil spill (e.g., Golet et al. 2002). Such effects may
be expected in terrestrial amphibians, reptiles, and mammals
but remain poorly studied.
Developmental effects. The detrimental effects of PAH and
crude oil exposure on developing avian embryos have long
been recognized (e.g., Grau et al. 1977). Exposure may result
from maternal transfer or topical exposure (e.g., oil being
passed from incubating birds’ feathers to eggshells). Much
of the experimental work to date has been conducted in
model bird organisms (e.g., chicken [Gallus gallus domesticus], mallard [Anas platyrhynchos]) and has involved either
the injection of toxicants into various components of the
egg or the application of crude oil to egg shells. The consequences include damage to cells, developmental abnormalities, a reduction in body measurements, and reduced survival
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(Albers 2006). A recent study showed decreased hatching
success of mallards when weathered oil collected from the
GOM following the DWH spill was applied to egg shells,
although the rate of deformities in hatchlings did not differ
significantly from controls (Finch et al. 2011). Eggs of freeliving terrestrial vertebrates are frequently assayed for PAHs
and used as bioindicators of environmental contamination
(e.g., Holliday et al. 2007), but less work has been done on the
potential biological effects of exposure. In addition to effects
in utero or in ovo, juveniles may experience toxicity from
contaminated prey items (e.g., Alonso-Alvarez et al. 2007).
Depending on the species, adults may or may not consume
the same prey items that they deliver to their offspring; therefore, independent consideration of these groups is warranted.
Taxon-specific considerations. Few generalizations can be made
about the effect of oil on particular terrestrial vertebrate
taxa. Indeed, even two rodent species sharing the same
environment may differ in their sensitivity to pollutants
such as PAHs, presumably because of differences in life
history or physiology (Smith et al. 2002). However, some
broad patterns have been suggested: Secondary poisoning
(e.g., by ingesting contaminated prey items) is thought to
be more common than poisoning from the original source
(e.g., oil in the sediment) in birds. Inhalation as a route of
exposure may be more relevant to animals spending significant time in or near the contaminated sediment or water
(e.g., rodents) than other taxa. Uptake through the skin is
particularly important in amphibians (Smith et al. 2007),
especially in the presence of ultraviolet light, which may
increase PAH toxicity (Malcolm and Shore 2003). Following
exposure, shorter-lived species (e.g., some rodents) may be
less affected by the carcinogenic effects of PAHs than are
longer-lived species (e.g., turtles), because they are likely to
die before tumors develop or significantly affect their fitness
(Malcolm and Shore 2003). Lactational or placental transfer
of toxins is an important potential route of maternal transfer in mammals, whereas developmental exposure to toxins
occurs during egg formation in other groups (Smith et al.
2007). Finally, humans living and working in coastal areas
may be exposed via routes similar to those of other vertebrates in close and consistent contact with the oiled sediment (e.g., prey ingestion, inhalation), although perhaps to
a lesser extent. Research on free-living terrestrial vertebrate
responses to contamination can therefore be useful as a sentinel for potential human effects, but to our knowledge, little
work has specifically compared the effects of contamination
in free-living human and nonhuman vertebrates in this way
(but see Espinosa-Reyes et al. 2010).
Ecological impacts of oil on vertebrates
In addition to the detrimental effects of PAH exposure, degradation of preferred habitats and foraging resources may
alter demographic processes and, ultimately, population persistence. Quantifying the effect of oil spills on terrestrial vertebrate populations is challenging, however, given a frequent
822 BioScience • September 2014 / Vol. 64 No. 9
lack of baseline data on population sizes, habitat use, and
foraging strategies of species residing in affected areas (see
Henkel et al. 2012).
The availability of suitable, uncontaminated habitat is a
prerequisite for population recovery from oil-spill-related
impacts. Some mobile fauna simply avoid contaminated
areas. For example, a number of marine birds reduced their
occupancy of oil-contaminated intertidal shoreline habitats for up to 2.5 years following the Exxon Valdez oil spill
(Wiens et al. 2004). However, some species are less capable of
abandoning preferred habitats, particularly those with small
home ranges, high site fidelity, or reliance on specific nesting
habitats. In these cases, behavior or ecological interactions
may be altered. In Alaska, river otters (Lontra canadensis),
whose coastal habitat was heavily oiled following the Exxon
Valdez oil spill, selected different habitat characteristics and
maintained larger home ranges in oiled habitats for more
than 1 year following the oil spill (Bowyer et al. 1995). Aside
from coping with reduced habitat quality, individuals may be
faced with increased intra- and interspecific competition in
new habitats. For example, a West African black turtle species (Pelusios niger) that changed its habitat use following an
oil spill in the Niger Delta experienced increased competition with a congener (Pelusios castaneus) already resident in
the new habitat (Luiselli et al. 2006).
Decreased availability of preferred prey resources (e.g., as
a result of PAH contamination) may cause species to alter
their diet or forage in potentially lower-quality ­
habitats
(Henkel et al. 2012). This can lead to species-, population-, and community-level effects through changes in
trophic interactions that propagate up or down trophic
levels, and reduced growth, survival, or reproductive fitness can carry over into subsequent seasons. Following
the 2003 Prestige oil spill, the reproductive success of
European shag (Phalacrocorax aristotelis) declined: Nestling
survival was significantly lower; chick growth and overall productivity also tended to be lower after the oil spill
than before it. These changes were, in part, attributed to a
decrease in the percentage of preferred forage fish prey (e.g.,
sand eel, Gymnammodytes semisquamatus; Velando et al.
2005). Similarly, Hebert and colleagues (2006) demonstrated
changes in seabird foraging ecology from an aquatic- to
terrestrial-based diet, attributable to declining populations
of preferred prey fish species associated with human stocking of predatory fishes. Crucially, such changes in seabird
foraging ecology have been correlated with declining egg
energy content and reproductive potential in these populations (Paterson et al. 2014). An alteration in the assemblages
of prey species or a reduced abundance of preferred prey
following the DWH spill may similarly have negative effects
on terrestrial salt-marsh vertebrate species.
Consequences of the Macondo blowout for resident
terrestrial salt-marsh vertebrates
Despite many potential effects, there is not yet a consensus
regarding long-term responses of terrestrial vertebrates to
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the Macondo blowout. For a more thorough understanding of the chronic effects of the DWH spill on terrestrial
vertebrates breeding in coastal Louisiana salt marshes, we
must first identify the animals at risk and consider exposure
pathways in these species. It is then essential to examine both
the physiological burden of toxicity and the interacting ecological effects that result from habitat alterations.
Study organisms. Salt marshes are often characterized by high
productivity of a few dominant plant species (e.g., Spartina
alterniflora and Juncus roemerianus), whereas isolation, high
salinity, flooding, and low structural heterogeneity may be
responsible for a relatively low species richness of terrestrially foraging vertebrates (Greenberg et al. 2006). For example, amphibians are absent from GOM coastal salt marshes.
Some generalist reptiles and mammals may be present (e.g.,
American alligator, Alligator mississippiensis; coyote, Canis
latrans; raccoon, Procyon lotor; white-tailed deer, Odocoileus
virginianus), but these become increasingly rare with distance away from freshwater, which reduces their vulnerability to oil in marshes directly adjacent to the GOM (Lowry
and Pratt 1974, Dundee and Rossman 1996). A variety of
migratory landbirds can be found using the marsh in winter; Nelson’s sparrow (Ammodramus nelsoni) winters almost
exclusively in coastal marshes (Shriver et al. 2011) and may
be vulnerable to oil spills. However, the terrestrial vertebrate
species most vulnerable to population-level consequences
of the DWH spill are the small number of salt-marsh specialists and year-round residents. A few reptiles (e.g., the
salt-marsh snake, Nerodia clarkii; the diamondback terrapin,
Malaclemys terrapin) and birds (e.g., the seaside sparrow; the
clapper rail, Rallus longirostris) are almost entirely restricted
to coastal marshes. Of these, the seaside sparrow is by far the
numerically dominant bird species. Marsh rice rats are not
restricted to salt marsh, but this species is exceptional among
mammals in its abundance and success in coastal GOM salt
marshes.
Selecting representative sentinel organisms for assessing
contamination risk can often be difficult, because both biotic
and abiotic factors can affect the degree of exposure, and
the effects can be quite species specific (Smith et al. 2007).
Given how few terrestrial vertebrates are resident at high
densities in GOM salt marshes, seaside sparrows and marsh
rice rats are obvious focal species because of their abundance
and strong association with marsh environments across the
Gulf coast. These species are likely to play an important
ecological role as some of the top consumers in this ecosystem. Combined with their high potential for exposure, these
characteristics rank them quite high relative to other saltmarsh vertebrates as crude oil biomonitors (sensu Golden
and Rattner 2002). Previous studies in seaside sparrows and
marsh rice rats have demonstrated the utility of the species
as bioindicators of mercury and polychlorinated biphenyl
exposure, respectively (Smith et al. 2002, Warner et al. 2010).
Our group began studying the seaside sparrow late in 2011
and the marsh rice rat in spring of 2013 (figure 1). These
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studies are ongoing; some of the primary research questions
being addressed are outlined below.
The seaside sparrow (figure 2) is of interest to conservation biologists for a number of reasons. The species
has a tendency to form localized, morphologically distinct populations recognized as subspecies. Two of these
(Ammodramus maritima pelonota and Ammodramus maritima nigrescens) have gone extinct in the past 30 years; the
latter (the dusky seaside sparrow) went extinct shortly after
being listed as endangered under the Endangered Species
Act (McDonald 1988, Post and Greenlaw 2009). A third
population (the Cape Sable seaside sparrow, Ammodramus
maritima ­mirabilis) is currently on the Endangered Species
List. Along the coast of the GOM, four of the five recognized
subspecies occupy small geographic ranges, and seaside
sparrows are considered a species of conservation concern
in all five Gulf Coast states. Despite the loss of vast areas
of marsh in southeast Louisiana over the past 100 years,
the species remains relatively abundant and is amenable
to both collection and mark–recapture studies. This small
(around 20-gram) songbird feeds on invertebrates and seeds
and spends a considerable amount of time foraging on the
ground (Post and Greenlaw 2009).
The marsh rice rat (figure 1a) inhabits salt marshes along
the GOM and Atlantic coasts but, unlike the seaside sparrow,
can also be found in freshwater marshes as far inland as Illinois
(Eubanks et al. 2011). Several subspecies are recognized, but
recent molecular work has suggested that there are two clades
that may represent distinct genetic species, with a boundary
located somewhere near the Mississippi–Alabama border
(Hanson et al. 2010). It has been suggested that this species
may be susceptible to local population extinction (Kruchek
2004), and an isolated subspecies endemic to the Everglades of
Florida, the silver rice rat (Oryzomys palustris natator), is federally endangered. Population density of marsh rice rats has been
linked to vegetation structure, with rats appearing to prefer
areas with thicker cover (Eubanks et al. 2011). When upland
habitat is present, it may serve as a refuge during wetland
flooding (Kruchek 2004); however, these semiaquatic rodents
are heavily dependent on wetland habitat and are good swimmers. The species is known to eat wetland vegetation, aquatic
invertebrates, and bird eggs (Post 1981, Kruchek 2004). Marsh
rice rats are the only rodents that we have captured on our
study plots and are present in large numbers, permitting both
mark–recapture work and collection.
Exposure potential. The degree and duration of exposure to
oil or its components in terrestrial vertebrates will affect
the magnitude of any physiological response and is highly
dependent on the pattern of oiling in the environment.
Following the DWH spill, the pattern of oiling in coastal salt
marsh was complex: Some shorelines showed no evidence of
oiling, whereas others were heavily oiled. On the oiled sites,
the marsh behind the shoreline often consisted of a patchwork of oiled and unoiled areas, determined on the basis
of the Shoreline Cleanup Assessment Technique (SCAT)
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Figure 1. Searching for seaside sparrow nests in 2012 in Plaquemines Parish, Louisiana. This plot had been exposed to
oil in 2011. Abundance and reproductive success can be compared among plots with varying degrees of exposure to oil.
(a) Ear-tagged marsh rice rat captured on the marsh in 2013. (b) Seaside sparrow perched above an oiled marsh in 2011.
(c) The oiled marsh surface in 2011. Photographs: Philip C Stouffer.
program (Michel et al. 2013). We established replicate study
areas on the basis of SCAT data in order to compare unoiled
areas with sites that experienced moderate-to-heavy oiling.
In the absence of prespill data, a multiplot design provides
an opportunity to examine the magnitude, reproducibility,
and variance in population- and individual-level responses
to oiling (Skalski 2000). In addition to our long-term study
sites, plots were added in spring 2013 because of concerns
about sample size and potential oil redistribution following Hurricane Isaac in August 2012. Collection of sediment
samples for PAH analysis on all plots is ongoing and allows
the interpretation of vertebrate data with respect to complex
spatial and temporal patterns of oiling among locations.
Exposure to oil and our interpretation of response variables may also depend on animal movements, both daily
and seasonal. For daily movements, we may not expect to see
differences between individuals captured on oiled sites and
those from unoiled sites if they use both areas (e.g., while
foraging). Radiotelemetry and mark–recapture are being
used to examine these movements in our study species.
Among seaside sparrows, our data indicate that individuals
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generally have restricted movements (within a few hundred
meters of their nest) during the breeding season, which suggests that we may indeed expect differences among plots,
because individuals are consistently experiencing these local
environments. However, we do not yet understand the scale
of movements outside of the breeding season. Although seaside sparrows are typically considered nonmigratory, fewer
marked birds are present on Mississippi breeding grounds
in winter than in summer (Mark Woodrey, Mississippi
State University Coastal Research and Extension Center,
Grand Bay National Estuarine Research Reserve, Moss Point,
Mississippi, personal communication, 2 December 2013).
Preliminary population genetic analyses suggest considerable gene flow among seaside sparrows from the mid-Texas
coast to Mississippi. Both migration and dispersal suggest
that the physiological effects of oil have the potential to be
observed well outside of oiled areas (e.g., Henkel et al. 2012).
Assessing the physiological impacts of Macondo blowout in resident terrestrial vertebrates. PAHs contained in crude oil can
persist in the environment for many years, potentially
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Figure 2. A seaside sparrow captured on the salt marsh
in Plaquemines Parish, Louisiana, in 2012. This bird was
captured on a plot that was not visibly oiled in 2011. In
seaside sparrows and marsh rice rats, individual-level
condition and cytochrome P450 (e.g., CYP1A) enzyme
biomarkers can be compared for animals living on
plots with varying levels of exposure to oil.
Photograph: Philip C Stouffer.
Figure 3. The percentage of seaside sparrow nests that
survived to fledging on oiled (n = 3) and unoiled (n = 3)
plots studied in 2012; a fourth oiled plot was added in
2013. The number of nests with a known outcome (fledge
or fail) is included within each bar; the figure does not
reflect nests with unknown fates (13% overall).
creating long-term physiological effects in terrestrial vertebrates (Mendelssohn et al. 2012). For example, Exxon Valdez
oil persisted in sediment for at least 16 years (Short et al. 2007),
and harlequin ducks (Histrionicus histrionicus) showed evidence of PAH exposure even 20 years later (Esler et al. 2010).
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On the basis of what is known about the foraging and breeding
ecology of seaside sparrows and marsh rice rats, these species
both face a high likelihood of PAH exposure over the longer
term following the DWH spill—for example, via contact with
oiled sediment or through the ingestion of contaminated prey.
Therefore, we are collecting individuals of both species for
long-term study of hepatic CYP1A gene expression, which
will be used as a proxy of PAH exposure, with upregulation
predicted in individuals living in oiled environments relative
to those living in reference areas, particularly in the several
years immediately following the spill. Ecological work linking
PAH exposure across trophic levels also has the potential to
provide insights into ingestion as a potential route of exposure
and may be an avenue worth exploring.
However, we must connect exposure metrics with individual- and population-level effects (Hinton et al. 2005). In
short-lived species such as seaside sparrows and marsh rice
rats, cancerous effects of PAH are less likely than short-term
consequences. Developmental malformations in offspring or
shifting life-history characteristics (e.g., life span or fecundity)
may be more relevant, although detecting such effects is not
trivial. We are beginning to explore circulating stress hormones
(e.g., corticosterone) as a potential link between oil exposure
and health consequences in seaside sparrows, following similar work on other species (e.g., Romero and Wikelski 2002).
Hormones are of interest because they can act systemically to
simultaneously adjust multiple behavioral, morphological, and
physiological traits to cope with environmental challenges but
may also be vulnerable to endocrine disruption by environmental contaminants (Wikelski and Cooke 2006).
Perhaps most crucial to understanding impacts and
recovery, researchers must track the population size and
fitness measures of free-living animals exposed to contaminants over time. Our ongoing work on terrestrial vertebrate
responses to the Macondo blowout is addressing the abundance and reproductive success of these species in our study
areas. Estimates of bird density are generated on each plot
twice each breeding season with standardized point counts.
Our first 2 years of data indicate a tremendous decrease in
abundance that may be attributable to Hurricane Isaac inundating our study sites between the 2012 and 2013 breeding
seasons (Stouffer et al. 2013). Analyses of the patterns of
seaside sparrow and marsh rice rat abundance across oiled
and unoiled study areas await the collection of additional
data. Preliminary seaside sparrow nesting data combined
from 2012 and 2013 indicate that nests on unoiled sites were
significantly more likely to fledge than those on oiled sites
(likelihood ratio, G(1) = 10.9, p = .001; figure 3). This work
is also ongoing, and eventual long-term analyses will require
a detailed consideration of potentially confounding variables
across study sites (Parker et al. 2013).
Assessing the ecological impacts of the Macondo blowout on
­resident terrestrial vertebrates. Widespread habitat alterations
across Louisiana marshes following the Macondo spill have
the potential to affect ecosystem structure and function
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with cascading adverse effects for higher trophic levels.
Specifically, direct contact with oil from the Macondo spill
caused almost complete mortality of the two dominant
Louisiana salt-marsh plant species relative to unoiled reference locations (figure 1c; Lin and Mendelssohn 2012). In
addition, heavy oiling of marshes weakens the underlying
soil, creating a deep undercut of the upper marsh edge and
thereby increasing shoreline erosion rates (McClenachan
et al. 2013). These physical changes to salt-marsh ecosystem
structure following the Macondo spill likely contributed to
marked declines in abundance of invertebrate species, including insects, spiders, and crabs (McCall and Pennings 2012),
along Louisiana marshes; it remains to be seen whether PAH
exposure may have also contributed to their decline. On the
basis of what is known about the diet of seaside sparrow and
marsh rice rat, the declines in these prey resources may have
consequences for the species’ overall ecology. For example, a
reduction in primary consumer abundance can restrict the
abundance of secondary consumers by driving these higher
consumers to forage for alternative resources or to move to
different locations in search of available prey (Rush et al.
2010a). Movements could affect the extent of contact with
oiled marsh habitat but could also lead to increased intraand interspecific competition. Moreover, marsh rice rats and
seaside sparrows may compete for both prey and nesting
sites (Post 1981). Increased competition between these two
common species could have important demographic consequences for either or both species. Tracking changes in the
movement patterns of terrestrial vertebrates coupled with
prey community metrics (e.g., composition, diversity, abundance) is therefore essential for understanding the ecological
impacts of oil on species’ demography.
Importantly, however, it is necessary to connect changes
in prey populations with actual changes in a predator’s
foraging ecology. To address this, the diet of these species
is being determined through gut-content analyses of adults
and through nestling throat ligatures. Prey switching has
not been documented in terrestrial salt-marsh vertebrates
following an oil spill. However, using stable isotopes of
carbon and nitrogen, clapper rails were observed to use different invertebrate prey species depending on the nesting
habitat within estuaries (Rush et al. 2010b). We are using
similar tools (e.g., stable isotopes of carbon and nitrogen and
fatty acids) to determine whether the potentially reduced
abundance of invertebrate prey species poses consequences
to fitness or reproductive success in marsh rice rats and
seaside sparrows. Specifically, dietary linkages among multiple trophic levels, from primary producers to secondary
­consumers, are being characterized, and through these trophic linkages, we anticipate a greater understanding of the
energy flow and food web structure of salt-marsh communities and how they respond to disturbance. However, cascading ecological effects in the seaside sparrow or the marsh
rice rat may be delayed if they are mediated through changes
in inter­mediary populations (i.e., prey; Peterson et al. 2003),
which warrants long-term monitoring.
826 BioScience • September 2014 / Vol. 64 No. 9
Conclusions
Substantial advances have been made in recent years regarding the complex molecular and cellular mechanisms involved
in physiological responses to pollutants. Still, determining
the broad population- and community-level consequences
is necessary to establish the ecological relevance of pollution (Hinton et al. 2005). In the aftermath of the Macondo
blowout, the most comprehensive ecotoxicological studies
must consider both broad and focused perspectives (Fodrie
et al. 2014). For terrestrial vertebrates, our challenges are
to understand the links of oil exposure (e.g., via SCAT and
sediment PAH data) to cellular responses (e.g., CYP1A
expression), to individual outcomes (e.g., hormone levels,
nesting success), to population dynamics (e.g., density and
distribution), and to community structure (e.g., trophic
shifts). In the field, these challenges are compounded by
changes in these relationships over the course of recovery
and by the lack of baseline data and the irregularity of oil in
the salt marsh. Furthermore, the effects of multiple interacting stressors in these ecosystems remain poorly understood.
For example, the loss of marsh habitat in coastal Louisiana
due to development, hurricanes, subsidence, salinization, or
erosion (Craig 1979) could complicate our interpretations if
the focal populations are found to be declining following the
Macondo spill, particularly in the absence of corroborative
data. Other naturally encountered stressors, such as pathogens, may also vary with exposure to oil, again complicating
the interpretation of costs to species (Whitehead 2013). The
ecological and physiological effects of oil outlined above can,
themselves, interact (e.g., shifts in prey resources following
a spill could result in a concurrent shift in PAH exposure
when ingestion is a primary route of exposure), each with
potential consequences to fitness. The work outlined here
provides a framework for identifying the complex effects of
oil on terrestrial vertebrates in salt marshes; long-term study
and an integrative approach are clearly essential for success
in this endeavor.
Acknowledgments
Financial support was provided by a grant from BP and the
Gulf of Mexico Research Initiative to the Coastal Waters
Consortium and by the Louisiana Department of Wildlife
and Fisheries. We are grateful for field assistance provided
by R. Eileen Butterfield, Tracy Burkhard, Richard Gibbons,
Mark Herse, Ryan Leeson, Emilie Ospina, Laura Southcott,
and Joseph Welklin. We thank three anonymous reviewers
for insightful comments that improved the manuscript.
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Christine M. Bergeon Burns ([email protected]) and Jill A. Olin
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