Download Effects of Oil Spills on Terrestrial Arthropods in Coastal Wetlands

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Effects of Oil Spills on Terrestrial
Arthropods in Coastal Wetlands
STEVEN C. PENNINGS, BRITTANY D. M c CALL, AND LINDA HOOPER-BUI
Coastal wetlands are important to human well-being and vulnerable to oil spills. Research on biotic effects of oil has been focused on microbes,
plants, and benthic invertebrates, neglecting terrestrial arthropods. We review how oil affects terrestrial arthropods in coastal marshes and
suggest future research topics. Terrestrial arthropods play important ecological roles in coastal marshes, affecting primary production and
decomposition and providing food to terrestrial and marine vertebrates. Some species are pests and disease vectors for humans and livestock.
Terrestrial arthropods are sensitive to oil exposure and are suppressed even in lightly oiled sites where plants are not affected. Some arthropods
later reinhabit oiled marshes, which demonstrates that portions of the arthropod community may be resilient to oil exposure. However, oil that
remains in sediments may affect terrestrial populations for years after the spill. The sensitivity of arthropods to oil exposure makes them useful
indicators of marsh health following environmental impacts.
Keywords: Deepwater Horizon, insects, Macondo, oil spill, salt marsh
C
oastal salt marshes, although they occupy a small area of the globe, provide numerous ecosystem services to humanity, such as supporting recreationally and
commercially important food webs, moderating coastal
disturbances, storing carbon and nitrogen, and transforming
nutrients (Costanza et al. 1997, Pennings and Bertness 2001,
Barbier et al. 2011, Shepard et al. 2011, Spencer and Harvey
2012). In a number of studies, the threats that oil spills
pose to these habitats have been examined; however, these
studies have been focused on some taxa, particularly soil
microbes, plants, and benthic invertebrates, and others have
been neglected. Here, we review what little is known about
how oil spills affect the terrestrial arthropod community in
salt marshes and identify areas in which future research is
needed (figure 1).
Oil spills represent a major environmental threat to coastal
marshes, because these marshes are low-energy and anoxic
environments; therefore, the dispersal and decomposition of
oil are slow, and oil may persist within the soil for decades
(Teal and Howarth 1984, Hester and Mendelssohn 2000,
Peacock et al. 2005). This persistent oil may have long-lasting
effects on flora and fauna and may impede the recovery of
the system (Culbertson et al. 2007, 2008). There are welldocumented impacts of oil contamination on salt marsh
soil properties, infauna, and plant populations (Decker and
Fleeger 1984, Pezeshki et al. 2000, Pezeshki and DeLaune
2002, DeLaune et al. 2003, Mishra et al. 2012, Silliman et al.
2012, Brunner et al. 2013). Benthic invertebrate populations,
including resident “marine arthropods,” such as intertidal
crabs and the fish and invertebrate populations that use
salt marshes as temporary feeding or nursery grounds,
have also received attention (Pezeshki et al. 2000, Andrade
et al. 2004, Culbertson et al. 2007, Whitehead et al. 2011). In
contrast, there has been almost no study of the effects of oil
exposure on the salt marsh terrestrial arthropod community
(figure 2), which, for the purposes of this article, we define as
Hexapoda (including insects and springtails) and Arachnida
(including spiders, mites, and pseudoscorpions).
The importance of terrestrial arthropods
Terrestrial arthropods play an important role in the ecology of coastal salt marshes (figure 3). They occur at high
densities, up to several thousand individuals per square
meter (Denno et al. 2000, 2002, 2005, Wimp et al. 2010). The
community is not as diverse as those found in terrestrial
grasslands because of the low plant diversity of salt marshes,
but terrestrial arthropods nevertheless represent a major
component of multicellular biodiversity in salt marshes,
with 100 or more species in Spartina alterniflora stands
alone (Pfeiffer and Wiegert 1981, Wimp et al. 2010). Similar
levels of species richness can be found in stands of other
salt marsh plant species, such as Juncus roemerianus and
Distichlis spicata (Rey and McCoy 1997). Other insects are
abundant in wet sediments or marsh pools (Campbell and
Denno 1978, Kelts 1979, Ward and FitzGerald 1983, Barnby
et al. 1985). The taxonomic composition varies among sites,
but, typically, Diptera and Heteroptera (formerly Hemiptera
and Homoptera) are most abundant, followed by Coleoptera,
BioScience 64: 789–795. © The Author(s) 2014. Published by Oxford University Press on behalf of the American Institute of Biological Sciences. All rights
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doi:10.1093/biosci/biu118
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Figure 1. Oiled marsh at Barataria Bay, Louisiana, in 2010. The Spartina alterniflora grasses at the leading edge of the
marsh were heavily coated with oil and have died. A floating boom intended to keep oil out of the marsh has washed
into the marsh and is contributing to crushing oiled vegetation. Behind the heavily oiled area, lightly oiled S. alterniflora
appears healthy, but does it support a functioning arthropod community? Photograph: Steven C. Pennings.
Collembola, Hymenoptera, Orthoptera, and Thysanoptera
(Davis and Gray 1966, Foster and Treherne 1976, Rey and
McCoy 1997). This taxonomic diversity provides an extra­
ordinary opportunity to explore how vulnerability to oil
varies among species as a function of physiology, life history,
and microhabitat use.
Terrestrial arthropods affect primary production and
nutrient cycling in salt marshes. Herbivorous taxa, such
as planthoppers, stem-boring flies and beetles, and grasshoppers, affect plant growth (Denno et al. 2002, Finke
and Denno 2004, Stiling and Moon 2005, Jiménez et al.
2012). Detritivorous taxa, such as Collembola (springtails),
affect the transfer of plant primary production into the
decomposer food web (Rusek 1998). Predatory taxa, such
as spiders, and parasitoids, such as wasps, can affect the
densities of both herbivores and detritivores, which indirectly affects the rates of herbivory and detritivory (Denno
et al. 2002, 2005, Stiling and Moon 2005). Because many of
790 BioScience • September 2014 / Vol. 64 No. 9
the ecosystem services provided by salt marshes depend
on vigorous plant growth and the decomposition of plant
detritus, terrestrial arthropods may play a larger role than is
usually realized in mediating salt marsh ecosystem services.
How invertebrates affect ecosystem services, however, is not
well documented for any habitat type (Prather et al. 2013),
including salt marshes, and so the magnitude of this role
remains to be determined.
Terrestrial arthropods provide valuable nutrient linkages
that connect disparate parts of the ecosystem. In particular,
terrestrial arthropods represent an important trophic link
to both terrestrial and marine vertebrates. Both migratory
birds, such as painted buntings, and marsh residents, such
as seaside sparrows, feed on a variety of insects and spiders
associated with marsh plants (Pfeiffer and Wiegert 1981,
Brittain et al. 2012). Some passerine birds pick the insects
off the exterior of the plants (Kale 1964, Brittain et al.
2012), whereas others drill into the plants and consume
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Figure 2. Representative arthropods from coastal salt marshes in the United States. (a) Prokelisia sp. planthopper
(photograph: Chuan-Kai Ho); (b) Chaetopsis sp. fly whose larvae are stem-boring herbivores; (c) Conocephalus aigialus,
an omnivore (photograph: Liz Wason); (d) Hogna sp., a predator; (e) Ischnodemus badius, an herbivore; (f) Chlorochroa
senilis, an herbivore; (g) Orchelimum fidicinium, an omnivore; (h) a salticid spider, likely Marpissa sp. Unless specified
otherwise, photographs: Jim Sheehan.
stem-boring insects concealed within (Xiong et al. 2010).
Many other shorebirds that are not primarily insectivores
nevertheless include insects as a component of their diets
(Kelts 1979, Pfeiffer and Wiegert 1981, Rey and McCoy
1997).
Terrestrial arthropods are also eaten by multiple species of estuarine fish (Pfeiffer and Wiegert 1981). Insects
often represent 20%–60% of the diet of small estuarine
fish (Harrington and Harrington 1961, 1972, Kelts 1979)
and can approach 100% of the diet when insects are most
abundant (Harrington and Harrington 1961). Insects living
on the marsh surface or in pools are most vulnerable to fish
predation (Harrington and Harrington 1961), but fish also
eat insects that typically avoid being submerged. The Gulf
killifish, Fundulus grandis, nudges Spartina stems to knock
arthropods onto the water, where it can easily consume
them. Small fish such as Fundulus spp. may also jump out
of the water to capture insects perching on exposed vegetation (Rey and McCoy 1997). Moreover, as the tide comes in,
Prokelisia planthoppers and other insects get caught in the
surface tension of the water, which makes them easy prey
for fish (Harrington and Harrington 1972, Kneib and Stiven
1978, Rey and McCoy 1997). The smaller fish that feed in
the marsh are, in turn, food for larger fish of recreational
and commercial importance (Kneib 1997). Therefore, by
supporting populations of birds and fish, terrestrial arthropods contribute indirectly to supporting a range of coastal
industries, including ecotourism (bird watching), hunting,
and recreational and commercial fisheries.
In contrast to these beneficial effects, terrestrial arthropods in salt marshes also have negative effects on human
societies and economies (Linley 1976, Kay and Russell
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2013). A number of mosquitoes, biting gnats, and biting flies
pass through their larval stages in marsh muds and ponds
(Axtell 1976). These species can represent a major irritant to
humans and livestock and can spread malaria, heartworm,
filariasis, encephalitis, and other diseases (Axtell 1976, Linley
1976, O’Meara 1976). Efforts to control these taxa, especially
mosquitoes, have led to widespread human modification
(ditches or impoundments) of marsh habitats (Daiber 1986,
Crain et al. 2009, Gedan et al. 2009).
Responses of terrestrial arthropods to oil spills
The work to date suggests that terrestrial arthropods might
be more sensitive to oil exposure than are plants (McCall
and Pennings 2012). Following the BP Deepwater Horizon’s
Macondo oil spill, McCall and Pennings (2012) sampled
replicated sites in Louisiana and Mississippi in August 2010
and 2011. Some sites were exposed to oil; reference sites
showed no visible signs of oil. The oiled sites typically had a
band of heavily oiled dead S. alterniflora up to 5 meters (m)
wide at the leading edge of the marsh (Silliman et al. 2012,
Michel et al. 2013). McCall and Pennings (2012) sampled
terrestrial arthropods 1–2 m behind this band, in stands of
S. alterniflora that appeared healthy, despite some oil on the
soil surface and bases of the plant stems. Abiotic conditions,
such as soil organic content, water content, and soil salinity,
and plant variables such as height, the percentage cover of
live plants, and the percentage cover of dead plant material
did not differ between the oiled and the control sites. S. alterniflora leaf nitrogen content, however, was higher at the oiled
sites, for reasons that are not clear.
In this zone of moderate oiling and putatively healthy S.
alterniflora plants, the total densities of terrestrial arthropods
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Grasshoppers
Birds
Planthoppers
Spiders
Springtails
Plants
Decomposing plant
materials
Fishes
Figure 3. Terrestrial arthropods play an important
role in mediating ecological processes and supporting
higher trophic levels in the salt marsh. Herbivorous taxa,
such as planthoppers and grasshoppers, affect plant
biomass. Detritivorous taxa, such as springtails, affect
the decomposition of dead plant material. All of these,
plus arthropod predators, such as spiders, are eaten by
insectivorous birds and small fish. Graphic: John Norton.
were cut in half immediately after the oil came ashore
(McCall and Pennings 2012). This effect was broadly similar
across five feeding guilds: predators, sucking herbivores,
stem-boring herbivores, parasitoids, and detritivores. This
result is important because it indicates that terrestrial
arthropod densities may be sharply reduced by oil exposure
in areas in which plants appear unaffected. In areas with
heavy oil exposure, where plants are obliterated and the
marsh surface is covered with a layer of tar, there is no ambiguity about the impacts of an oil spill, but if a lightly oiled
marsh supports vigorous plant growth, casual observers or
investigators focusing on primary production might easily
conclude that the area was unaffected, although marsh function might, in fact, be significantly impaired.
The work to date also suggests that some terrestrial arthropods are resilient to oil exposure. McCall and Pennings
(2012) resampled their sites a year after oil came ashore and
found that the total densities of terrestrial arthropods had
completely recovered. The recovery was statistically similar
across the five feeding guilds studied, although there were
792 BioScience • September 2014 / Vol. 64 No. 9
hints that detritivores had increased in abundance beyond
their initial densities, a result that would be consistent with
the initial oil exposure’s creating a large pulse of decomposing organic matter along the edges of the marshes. The rapid
recovery of terrestrial arthropods is important because it
suggests that this group of organisms is quite resilient to oil
exposure, able to rapidly bounce back even if it is sharply
suppressed by the initial oil exposure.
Directions for future research
Before taking resilience as the last word on the topic, however, we must emphasize how much remains to be understood about the responses of the arthropod community
to oil exposure. The responses of salt marsh terrestrial
arthropods to oil spills are likely to vary as a function of oil
exposure and the ecological characteristics of the plant and
arthropod community.
Oil exposure is a function of weathering, the amount of
oil reaching an area, and the persistence of the oil in the
sediments. The circumstances of the Macondo spill allowed
extensive weathering of oil prior to contact with the shoreline (Peterson et al. 2012). Spills closer to shore will have
more toxic petroleum that is still intact when the oil washes
ashore, which could lead to greater and longer-lasting
impacts. Oil impacts will also increase with the total amount
of oil reaching an area. McCall and Pennings (2012) examined areas with moderate oil exposure and did not examine
nearby areas where plants had been completely killed by
heavy oil exposure. Obviously, in the latter areas, a natural
arthropod assemblage will not recover until the plant community recovers—if then. Recovery in revegetated areas may
have unique trajectories, and this remains to be assessed.
Recovery trajectories are likely to differ between areas that
are lightly and those that are heavily oiled because of the persistence of oil in the soil. Oil persists in marsh soils for years
or decades (Teal and Howarth 1984, Peacock et al. 2005,
Culbertson et al. 2007, 2008). This residual oil will continue
to affect terrestrial arthropods as it volatilizes, is brought to
the surface by burrowing organisms or erosion, or affects the
quality of plants used as food or habitat. Heavily oiled sites,
with a larger amount of oil incorporated into the soil, may
represent locations with greater and longer-lasting impacts
on the arthropod community. For example, in the case of the
Macondo oil spill, two toxic aromatic components of the oil
are recalcitrant in the marshes that fringe the northern Gulf
of Mexico (Turner et al. 2014b). The aromatic compounds
naphthalene and methylnaphthalene, both of which are toxic
to insects, have increased a thousandfold in concentration in
the sediment in 1000 days since the oil came ashore (Turner
et al. 2014). These volatile aromatic components may be
released from the sediments into the water when the marsh
is inundated by seawater and are released into the air when
the marsh is exposed. Under the latter conditions, these
compounds can strongly affect the arthropod community.
The responses of salt marsh terrestrial arthropods to oil
spills may also vary as a function of ecological characteristics
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of the plant and arthropod community. Most of the work to
date on oil impacts on terrestrial arthropods has been done
in stands of S. alterniflora. Although this is the most abundant
salt marsh plant along most of the Gulf and Atlantic coasts of
the United States, other species, such as Spartina patens and
Juncus spp., are equally or more abundant in some locations,
and there is evidence that oiling has a more severe impact
on some of these other plant species than on S. alterniflora
(Lin and Mendelssohn 2012). Even if S. alterniflora marshes
are resilient to moderate oiling, marshes dominated by other
plant species—and their associated arthropods—may not be.
The effects of oil exposure are also likely to vary among
arthropod species. For example, species that live on the soil
surface or low in the canopy, such as hunting spiders and
Collembola, are likely to be exposed to more oil (either
as liquid or as volatiles) than are species that live high in
the plant canopy, such as planthoppers or web-building
spiders. Similarly, the terrestrial arthropods occupying wet
sediments and marsh ponds will be more exposed to oil than
those living in the vegetation canopy above and, therefore,
will likely be more affected. (In fact, applications of diesel
oil were historically used in Florida to control salt marsh
mosquitoes by suffocating the larvae [Foster and Treherne
1976].) In addition, arthropod species will differ in how easily they can recolonize disturbed patches, with those that can
fly likely recolonizing faster than those that cannot (Denno
1994, Lundberg and Moberg 2003, Armitage et al. 2013).
We currently know little about the survival of arthropods
that recolonize oiled patches. It is possible that arthropods
colonizing oiled patches have a high mortality rate because
of residual oil, in which case the previously oiled patches
would be ecological traps. In other words, a natural density
of arthropods might not indicate a healthy ecosystem if
the arthropods are dying at a high rate and simply being
replaced by unsuspecting migrants that will soon share
the same fate. In the same way, sea otter subpopulations in
Alaska that inhabit areas with significant residual oil from
the Exxon Valdez spill continued to act as sinks on the overall population for at least 15 years after the spill, with chronic
mortality equaling the initial acute mortality at the time of
the spill (Monson et al. 2011).
Finally, the dynamics of the recolonization of a disturbed
patch almost certainly depend on the landscape cover and
arrangement of patches that are heavily, lightly, and not oiled
(Denno 1994). In particular, if extensive stands of marshes in
a particular area were oiled and no healthy marsh remained
in the immediate area, there would be no local source of
arthropods to recolonize the disturbed areas.
These points essentially lay out a research agenda for future
work on the effects of oil on terrestrial arthropods in coastal
wetlands. As this essay has made clear, we currently know
very little about this topic, and great uncertainties remain.
Continued sampling of salt marsh arthropod communities
is needed in order to better characterize these communities
and to understand what can be lost following an oil spill or
other environmental insult. Mesocosm experiments will be
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useful in teasing apart details about how different arthropod
species respond to and recover from various oiling scenarios.
Investigations into oil dosage and weathering and how plant
recovery and microbial biodegradation affect arthropod resilience will lend valuable insights into the mechanisms behind
functional recovery of the entire system. Additional field
studies will be crucially important in testing hypotheses about
landscape processes and for transferring laboratory results to
more-realistic conditions. In particular, although heavily oiled
sites typically receive the most attention, we suggest that more
attention needs to be paid to lightly oiled sites, which are more
common, especially with the passage of time after the initial
spill (Michel et al. 2013). Because terrestrial arthropods appear
to be more sensitive to oil exposure than salt marsh plants,
many scenarios of oil exposure could create salt marshes that
appear healthy to the casual observer but that are, in fact,
devoid of terrestrial arthropods and the ecosystem functions
that they support. For this reason, we encourage the further
study of terrestrial arthropods as a useful indicator of marsh
health following oil spills or other environmental impacts
(Campbell and Denno 1976, Barnby et al. 1985).
Acknowledgments
We thank the National Science Foundation (for grants
no. OCE10-45221, no. OCE06-20959, no. DEB-1044599),
the Gulf of Mexico Research Initiative Coastal Waters
Consortium, and the Northern Gulf Institute for financial
support. This work is a contribution of the Georgia Coastal
Ecosystems program, part of the Long Term Ecological
Research Network. The financial sources supporting this
research had no role in the design or execution of the study,
the data analysis, the decision to publish, or manuscript
preparation. We thank two anonymous reviewers for helpful
comments that improved the manuscript.
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GoMRI-sponsored Special Section Articles
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Steven C. Pennings ([email protected]) and Brittany D. McCall are affiliated
with the Department of Biology and Biochemistry at the University of Houston,
in Houston, Texas. Linda Hooper-Bui is affiliated with the Department of
Environmental Science in the School of Coast and Environment at Louisiana
State University, in Baton Rouge.
September 2014 / Vol. 64 No. 9 • BioScience 795