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Characterizing the variability of benthic foraminifera in the northeastern Gulf of Mexico following the Deepwater Horizon event (2010-2012)

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Following the Deepwater Horizon (DWH) event in 2010 subsurface hydrocarbon intrusions (1000-1300 m) and an order of magnitude increase in flocculent hydrocarbon deposition caused increased concentrations of hydrocarbons in continental slope sediments. This study sought to characterize the variability [density, Fisher's alpha (S), equitability (E), Shannon (H)] of benthic foraminifera following the DWH event. A series of sediment cores were collected at two sites in the northeastern Gulf of Mexico from 2010 to 2012. At each site, three cores were utilized for benthic faunal analysis, organic geochemistry, and redox metal chemistry, respectively. The surface intervals (∼0-10 mm) of the sedimentary records collected in December 2010 at DSH08 and February 2011 at PCB06 were characterized by significant decreases in foraminiferal density, S, E, and H, relative to the down-core intervals as well as previous surveys. Non-metric multidimensional scaling (nMDS) analysis suggested that a 3-fold increase in polycyclic aromatic hydrocarbon (PAH) concentration in the surface interval, relative to the down-core interval, was the environmental driver of benthic foraminiferal variability. These records suggested that the benthic foraminiferal recovery time, following an event such as the DWH, was on the order of 1-2 years.
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Environmental Science and Pollution
Research
ISSN 0944-1344
Environ Sci Pollut Res
DOI 10.1007/s11356-016-7996-z
Characterizing the variability of benthic
foraminifera in the northeastern Gulf of
Mexico following the Deepwater Horizon
event (2010–2012)
P.T.Schwing, B.J.O’Malley,
I.C.Romero, M.Martínez-Colón,
D.W.Hastings, M.A.Glabach,
E.M.Hladky, A.Greco & D.J.Hollander
1 23
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RESEARCH ARTICLE
Characterizing the variability of benthic foraminifera
in the northeastern Gulf of Mexico following the Deepwater
Horizon event (20102012)
P. T. Schw i n g
1
&B. J. OMalley
1
&I. C. Romero
1
&M. Martínez-Colón
2
&D. W. Hastings
3
&
M. A. Glabach
1
&E. M. Hladky
1
&A. Greco
1
&D. J. Hollander
1
Received: 10 May 2016 /Accepted: 25 October 2016
#Springer-Verlag Berlin Heidelberg 2016
Abstract Following the Deepwater Horizon (DWH) event in
2010 subsurface hydrocarbon intrusions (10001300 m) and
an order of magnitude increase in flocculent hydrocarbon de-
position caused increased concentrations of hydrocarbons in
continental slope sediments. This study sought to characterize
the variability [density, Fishers alpha (S), equitability (E),
Shannon (H)] of benthic foraminifera following the DWH
event. A series of sediment cores were collected at two sites
in the northeastern Gulf of Mexico from 2010 to 2012. At
each site, three cores were utilized for benthic faunal analysis,
organic geochemistry, and redox metal chemistry, respective-
ly. The surface intervals (010 mm) of the sedimentary re-
cords collected in December 2010 at DSH08 and February
2011 at PCB06 were characterized by significant decreases
in foraminiferal density, S,E,andH, relative to the down-
core intervals as well as previous surveys. Non-metric multi-
dimensional scaling (nMDS) analysis suggested that a 3-fold
increase in polycyclic aromatic hydrocarbon (PAH) concen-
tration in the surface interval, relative to the down-core inter-
val, was the environmental driver of benthic foraminiferal
variability. These records suggested that the benthic
foraminiferal recovery time, following an event such as the
DWH, was on the order of 12years.
Keywords Benthic .Foraminifera .Ecology .Petroleum .
Gulf of Mexico .Deepwater Horizon
Introduction
The Deepwater Horizon (DWH) event released over 600 mil-
lion liters of oil into the Gulf of Mexico from April 20 to
July 12, 2010 (Atlas and Hazen 2011). Following the DWH
event (April 20July 12, 2010), continental slope sediments of
the northeastern Gulf of Mexico (nGoM) came in contact with
hydrocarbons through the direct impingement of subsurface
hydrocarbon intrusions (10001300 m) and an order of mag-
nitude increase in flocculent hydrocarbon deposition (Passow
et al. 2012; Ziervogel et al. 2012; Paris et al. 2012; Brooks
et al. 2015;Romeroetal.2015). The increase in flocculent
deposition was due to a marine oil snow sedimentation and
flocculent accumulation (MOSSFA) event (Daly et al. 2016).
Increased concentrations of total petroleum hydrocarbons,
polycyclic aromatic hydrocarbons (PAHs), and hopanes
(Romero et al. 2015; Valentine et al. 2014), as well as changes
in redox conditions (Hastings et al. 2016) caused by the in-
creased flocculent deposition (410-fold background accumu-
lation) following the DWH event, were documented through-
out the surface 10 mm of sediment (Brooks et al. 2015).
Moderate to severe impacts on benthic megafauna have been
documented up to17 km southeast and 8.5 km northeast of the
wellhead (Montagna et al. 2013).
Prior to the DWH event, several foraminiferal surveys and
reviews were conducted throughout the nGoM (Phleger and
Parker 1951;Parker1954; Culver and Buzas 1983;Poag
1984; Denne and Sen Gupta 1991; Sen Gupta and Aharon
Responsible editor: Philippe Garrigues
Electronic supplementary material The online version of this article
(doi:10.1007/s11356-016-7996-z) contains supplementary material,
which is available to authorized users.
*P. T. Schwing
pschwing@mail.usf.edu
1
University of South Florida, College of Marine Science, 830 1st St.
SE, St. Petersburg, FL 33701, USA
2
Florida A&M University, School of the Environment, 1515S. Martin
L. King Blvd, Tallahassee, FL 32307, USA
3
Eckerd College, 4200 54th Ave. S, St. Petersburg, FL 33711, USA
Environ Sci Pollut Res
DOI 10.1007/s11356-016-7996-z
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1994; Buzas et al. 2007; Lobegeier and Sen Gupta 2008;and
Bernhard et al. 2008). In particular, Poag (1984)documented
two predominant facies in the nGoM between 1000 and
1300 m where Eponides spp.and Bulimina spp. dominated
the western and eastern slope of the DeSoto canyon, respec-
tively. Agglutinated taxa such as Saccorhiza ramosa,Reophax
spp., and Bathysiphon spp. were found to dominate living
bathyal and abyssal assemblages in the nGoM (Bernhard
et al. 2008, sites S36 and S42).
A few previous studies have thoroughly documented the
benthic foraminifera associated with chronic petroleum expo-
sure in the nGoM associated with natural seeps (Sen Gupta and
Aharon 1994; Lobegeier and Sen Gupta 2008;SenGuptaetal.
2009) in contrast to the short-term exposure following the
DWH event (this study). Two calcareous taxa (Bolivina
ordinaria and Gavelinopsis translucens) comprised 4672%
of foraminiferal communities at active seep sites at 650-m
water depth (Sen Gupta and Aharon 1994, site F13). Other
important calcareous taxa near natural hydrocarbon seeps in
the Mississippi Canyon (1000-m water depth) included
Eponides turgidus,Uvigerina peregrina,Nonionella iridea,
B. ordinaria,Bolivina lowmani,Bolivina albatrossi,Bulimina
aculeata,andEpistominella exigua (Lobegeier and Sen Gupta
2008; Sen Gupta et al. 2009). Lobegeier and Sen Gupta (2008)
found that seep sites in the Mississippi Canyon (10001100-m
water depth) were dominated by Bolivina spp. Benthic forami-
niferal densities near natural seep sites in the Mississippi
Canyon (MCP) ranged from 2 to 84 indiv./cm
3
,whichwasless
than a non-seep site south of the Mississippi Canyon (174
indiv./cm
3
) and a site in the DeSoto Canyon (102 indiv./cm
3
)
(Lobegeier and Sen Gupta 2008;SenGuptaetal.2009). These
surveys and reviews provide a pre-DWH context in which to
assess variability and dominant taxa of benthic foraminifera in
the records from this study following the DWH event.
The purpose of this study was to characterize the potential
impacts of the DWH event (e.g., increased PAH concentra-
tion, intensification of reducing sedimentary conditions) on
benthic foraminiferal variability (e.g., density, diversity). The
first objective was to establish similarities between previous
(baseline) foraminiferal surveys in the nGoM with the down-
core intervals of the cores collected for this study. The second
objective was to assess any potential impact of the DWH
event on the benthic foraminifera in the surface intervals by
contrasting them with previous surveys as well as the down-
core interval. The third objective was to then characterize
benthic foraminiferal variability in the surface interval over a
series of cores collected from 2010 to 2012 in the interest of
establishing a time of recovery from any assessed impact.
This study builds on the work of Schwing et al. (2015)but
is broader in scope and scale. This study characterizes benthic
foraminifera at the species level, applies ecological indices in
addition to density, and includes records collected beyond
February 2011.
Methods
Field methods
Sediment cores were collected at two sites in the nGoM (Fig. 1)
using an Ocean Instruments MC-800 multicoring system, which
collects eight cores (diameter 10 cm, length up to 70 cm) simul-
taneously. At each site, three cores were utilized for (1) benthic
foraminiferal faunal analysis, (2) organic geochemistry, and (3)
redox metal chemistry. Two sites [PCB06 (29° 5.99N, 87°
15.93 W, 1043-m depth) and DSH08 (29° 7.25N, 87° 51.93
W, 1143-m depth)] were chosen for benthic foraminiferal faunal
analysis due to preliminary organic geochemistry results sug-
gesting the presence of recently deposited oil-derived hydrocar-
bons (Romero et al. 2015), and each site was located at a water
depth that was within the range of the documented primary
hydrocarbon plume (10001300m)(Kessleretal.2011). Sites
PCB06 and DSH08 were sampled in December 2010, February
2011, September 2011, and August 2012.
Foraminiferal sample preparation
Cores were refrigerated (4 °C) and subsampled by extrusion at
2-mm intervals for the upper 50 mm, with the exception of the
December 2010 DSH08 core (2 mm for the top 20 mm and 10-
mm intervals for the remainder of the core) using a calibrated,
threaded-rod extrusion device (Engstrom 1993; Valsangkar
2007). Subsamples were freeze dried prior to analysis and there-
fore not viable for staining. Every other subsample was analyzed.
Median depth values are reported (e.g., 02mmisreportedas
1mm,46 mm is reported as 5 mm, and so on). Freeze-dried
subsamples were weighed and washed with a sodium
hexametaphosphate solution through a 63-μm sieve to disaggre-
gate detrital particles from foraminiferal tests. The fraction re-
maining on the sieve (>63 μm) was dried in an oven at 32 °C
for 12 h, weighed again, and stored at room temperature. Grain
size data are reported as coarse fraction mass [CFM (g)], which is
the dry mass of sediment remaining on the sieve (>63 μm).
Between 200 and 400 individuals from every other sample from
the upper 50 mm of each core were identified to the species level
and counted (total of 100 samples, 25,991 individual foraminif-
era). The fraction of the sample that was identified was then
weighed. The use of at least 200 individuals per sample is in
agreement with studies that have 200 or less individuals per
sample in low-density assemblages (Schönfeld 2012 and
references therein). It was necessary to count between 200 and
400 individuals per sample to distinguish 2% significant variabil-
ity between samples (Patterson and Fishbein 1989). The majority
of the samples in this study satisfied this requirement. The only
samples that did not satisfy this number of individual counts are
the surface-most intervals of DSH08 (Dec. 2010) and PCB06
(Feb 2011). Every individual from the two uppermost samples
from DSH08 (December 2010) and PCB06 (February 2011) was
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identified due to low total counts (14152 individuals). With 50
individuals counted (DSH08 Dec. 2010, 1 mm), the minimum
estimated error ranged between 4 and 7% depending on the
frequency of the species. With 1020 individuals counted
(PCB06 Feb 2011, 1 and 5 mm), the minimum estimated error
ranged between 6 and 15% depending on the frequency of the
species. S. ramosa fragment counts were divided by three to
convert to individual counts for density, relative abundance,
and index calculations (Kurbeweit et al. 2000; Enge et al.
2011). Taxonomic references included the following:
dOrbigny (1826,1839),Williamson(1858), Jones and Parker
(1860), Parker and Jones (1865), Brady (1878,1879,1884),
Cushman (1922,1923,1927), Stewart and Stewart (1930),
Phleger and Parker (1951), Parker et al. (1953), and Parker
(1954). Representative species were mounted on aluminum stubs
with a double-sided tape, coated with a thin layer of Au/Pd, and
photographed in a Hitachi S-3500-N scanning electron
microscope.
Foraminiferal density
Total foraminiferal density was reported as individuals per
unit volume (indiv./cm
3
) (Scott and Medioli 1980; Osterman
2003; Rowe and Kennicutt 2009; Sen Gupta et al. 2009). The
values were normalized to the known wet volume of each
sample based on the diameter of the core tube (10 cm) and
the thickness of each sample (2 or 5 mm).
Benthic foraminiferal relative abundance
The relative abundance was reported for all identified species
representing greater than 2% of the entire sample. In addition,
foraminiferal species that were not present in at least 5% of the
samples (Parker and Arnold 2003) were eliminated. There was
not more than one unidentified species per genus, so no grouping
by genus was needed. Relative abundances for the surface (0
10 mm) and down-core (1050 mm) intervals (integrated all
increments) of each record (core) were reported to the nearest
whole number and were calculated using the total number of
counts for each interval (4004000 individuals) (Patterson and
Fishbein 1989).
Benthic foraminiferal ecological indices
Three ecological indices were used to characterize benthic
foraminiferal variability between down-core (1050 mm)
and surface (010 mm) intervals, as well as for comparison
with previous foraminiferal surveys in the nGoM. Fishers
alpha index (S) was utilized to provide a parameter of species
richness (Hammer and Harper 2006). The Shannon index (H)
accounted for the heterogeneity (diversity) of each sample
(Magurran 1988,SpellerbergandFedor2003. The equitabil-
ity index (E) measured the evenness based on Hand number
of species (Magurran 1988).
Organic geochemistry
EPA methods (EPA 2007a,b) and QA/QC protocols were
followed for the analysis of polycyclic aromatic hydrocarbons
(PAHs). Freeze-dried samples were extracted under high temper-
ature (100 °C) and pressure (1500 psi) with a solvent mixture 9:1
v/vdichloromethane/methanol (MeOH) using an Accelerated
Solvent Extraction system (ASE 2000, Dionex). Two extraction
blanks were included with each set of samples (1520 samples).
The aromatic fraction was separated using solid-phase extraction
(SiO
2
/C
3
-CN, 1 g/0.5 g, 6 mL) and hexane/dichloromethylene
(3:1, v/v) as the solvent. PAHs were quantified using a gas
chromatograph/mass spectrometric detector (GC/MS) in full-
scan mode (m/z50550) and splitless injections of 1 μL. Oven
temperature was 60 °C for 8 min, increased to 290 °C at a rate of
6 °C/min and held for 4 min, then increased to 340 °C at a rate of
14 °C/min, and held at the upper temperature for 5 min.
Concentrations of PAHs were calculated using response factors
by comparison with a known standard mixture (16-unsubstituted
EPA priority and selected isomers: Ultrascientific US-106N PAH
mix, NIST 1491a) and were corrected for the recovery of the
Fig. 1 The location of the
DSH08 and PCB06 sampling
sites with reference to the
Deepwater Horizon (DWH,black
triangle) platform and previous
benthic foraminifera survey sites
including seep site F13 (Sen
Gupta and Aharon 1994),
Mississippi canyon sites (MCP;
Lobegeier and Sen Gupta 2008;
Sen Gupta et al. 2009), Desoto
Canyon site (S36; Lobegeier and
Sen Gupta 2008; Bernhard et al.
2008), and West Florida Slope
site (S42; Bernhard et al. 2008)
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surrogate standard (d
10
-acenaphthene, d
10
-phenanthrene, d
10
-
fluoranthene, d
12
-benz(a)anthracene, d
12
-benzo(a)pyrene, d
14
-
dibenz(ah)anthracene, d
14
-benzo(ai)perylene). Recoveries from
spiked samples were generally within 60120%. High-
molecular-weight (HMW, 46 rings) and low-molecular-weight
(LMW, 203 rings) PAH concentrations are reported. Detailed
methods can be found in Romero et al. (2015). Organic geo-
chemistry data were included in the supplementary materials.
Redox-sensitive metal concentrations
Subsamples were freeze dried, weighed, and digested in a
Milestone Ethos EZ microwave oven using concentrated,
trace metal-grade HNO
3
at 165 °C and high pressure
(25 bar) (Hastings et al. 2016). The digestate was diluted
and analyzed using an Agilent 7500cx ICP-MS. Manganese
(Mn) and Rhenium (Re) concentrations are reported (for
detailed methods, see Hastings et al. 2016). Redox metal con-
centration data were included in the supplementary materials.
Multivariate analysis
Non-metric multidimensional scaling (nMDS) was utilized to
define the relative control of several environmental parameters
(PAH concentrations, redox metal concentrations, grain size) on
benthic foraminiferal variability (raw individual counts) through-
out each core. These environmental parameters were chosen as
indicators of changes in sedimentary input, petroleum input, and
redoxcline variability (Brooks et al. 2015; Hastings et al. 2016;
Romero et al. 2015). Bray-Curtis similarity (%) was represented
as distance between each sampling interval, and environmental
parameters were represented as vectors on each nMDS plot. The
length and orientation of the environmental vectors relative to
each homogeneous cluster allow for the determination of influ-
ence of each environmental parameter on benthic foraminiferal
variability for each sampling depth. nMDS plots were created
using PAST paleontological statistics software. Axes were cho-
sen based on the least change between ordinated and ranked
distances (i.e., ranked to ordinated distances ratio closest to 1)
(Shepard plot) (Hammer and Harper 2006).
Results
Down-core intervals
The majority of all the records were composed of 22 dominant
species (>2% relative abundance) (Plate 1;Table1). The most
abundant (>10%) in the down-core (1050 mm) interval of
PCB06 throughout all collections are (in order of abundance)
Sphaeroidina bulloides,U. peregrina,B. aculeata,Saccorhiza
ramosa,Cibicidoides kullenbergi,Bulimina alazenensis,
Archimerismus subnodosus,andUvigerina pigmaea
(Table 1). The most abundant (>10%) in the down-core (10
50 mm) interval of DSH08 throughout all collections are (in
order of abundance) B. aculeata,Praeglobobulimina pupoides,
U. peregrina,Gyroidina altiformis,B. lowmani,B. alazenensis,
S. bulloides,andBulimina striata mexicana (Table 1).
In the down-core interval (>10 mm), mean foraminiferal
density from PCB06 ranged from 45 to 98 indiv./cm
3
(1σ=8
27, n= 37) from December 2010 to August 2012 (Figs. 2and
4a; Table 2). Over this period, the mean density range was
higher at DSH08 (81154 indiv./cm
3
,1σ=2756, n=36)
(Figs. 3and 4b; Table 2).
Over the course of this study, the mean Sin the down-core
interval did not vary (S=910, 1σ=1,n= 39) at PCB06 but
varied between 19 and 30 (1σ=12, n= 36) at DSH08 (Figs. 2,
3,and4c, d; Table 3). Mean Ein the down-core interval did not
vary at either site (Figs. 2,3,and4e, f; Table 3). The mean H
also did not vary (H=2.4,1σ=0.10.2, n= 39) in the down-
core interval from PCB06 but did vary between 3.2 and 3.6
(1σ=0.1,n= 36) at DSH08 (Figs. 2,3,and4g, h; Table 3).
Surface interval
The most abundant (>10%) in the surface (010 mm) interval
of PCB06 throughout all collections are (in order of abundance)
B. alazenensis,S. bulloides,U. peregrina,B. aculeata,
U. pigmaea,Hyperammina elongata,Bolivina spathulata,
S. ramosa,andC. kullenbergi. The most abundant (>10%) in
the surface (010 mm) interval of DSH08 throughout all col-
lections are (in order of abundance) B. aculeata,P
. pupoides,
U. peregrina,G. altiformis,B. striata mexicana,B. alazenensis,
B. spathulata,andUzbekistania charoides (Table 1). There was
some notable variability in the relative abundance over time in
the surface interval (010 mm) at both sites. At PCB06, the
largest coefficient of change occurred in the relative abundance
of B. alazenensis, with 58% in February 2011, when the other
three time stamps ranged from 2 to 12%. At DSH08, there was
an overall decrease in B. aculeata from 20% in December 2010
to 8% in August 2012 as well as in P. pupoides from 20% in
December 2010 to 4% in August 2012.
With the exception of the February 2011 record (4 indiv./cm
3
,
1σ=6,n= 3), the surface (010 mm) interval mean foraminiferal
densityrangedfrom51to98indiv./cm
3
(1σ=627, n=10)for
PCB06. The December 2010 mean foraminiferal density from
DSH08 was 17 indiv./cm
3
(1σ= 19, n= 3), whereas the density
records collected after December 2010 (February 2011August
2012) ranged from 86 to 110 indiv./cm
3
(1σ=1166, n=9)
(Table 2).
The mean S(S=3,1σ=1,n=3)andH(H=1.4,1σ=0.1,
n= 3) in the surface interval from the PCB06 February 2011
record were noticeably lower than the other three surface inter-
vals [(S=811, 1σ=1,n= 10) and (H=2.52.6, 1σ=0.1,
n=10)](Fig.4c, d; Table 3). The mean S(S= 14, 1σ=2,n=3)
and H(H=2.7,1σ=0.2,n= 3) in the surface interval from the
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DSH08 December 2010 record were also noticeably lower than
in the other three surface intervals [(S=2235, 1σ=1,n=9)
and (H=3.43.8, 1σ=0.1,n= 9)] (Fig. 4a, b, g, h; Table 3).
MDS analysis
With the exception of the December 2010 record from DSH08
(0.24) and the February 2011 record from PCB06 (0.14) due to
low number of total counts in the surface interval (010 mm),
the stress value was below 0.10 for all other records. According
to the multivariate analysis, three predominant intervals are
clearly segregated with depth (010, 1030, and >30 mm)
in nearly every record (Fig. 5). The surface interval (010 mm)
groups solely with PAH concentration (7585% similarity) in
the early PCB06 records (December 2010 and February 2011).
The surface intervals in the later PCB06 records (September
2011, August 2012) as well as all DSH08 records group with
PAH concentrations, manganese (7585% similarity) and in
the case of the September 2011 record from PCB06 with grain
size [CFM(g)]. In nearly every record, the intermediate interval
(1030 mm) groups with manganese concentrations (7585%
similarity). The deepest interval (>30 mm) groups with rheni-
um concentrations (7585% similarity) and the coarse fraction
[CFM(g)] in nearly every record.
Discussion
There were 3-fold increases in PAH concentrations (Romero
et al. 2015) and intensified reducing conditions (Hastings et al.
2016), amongst sedimentological, microbial, and radioisotope
evidence (Brooks et al. 2015), which all indicated that the
surface 10 mm was affected by the DWH event at both
DSH08 and PCB06. This resulted in approximately 6
10 mm of sediment accumulation in a 45-month period in
late 2010 (Brooks et al. 2015). Following this period, accu-
mulation rates decreased gradually back to pre-DWH condi-
tions throughout late 2011 and 2012 (1mmperyear)
Plate 1 Scanning electron microscope (SEM) images of the most abun-
dant species from PCB06 and DSH08: 1 Archimerismus subnodosus
(Brady 1884), 2 Bolivina lowmani (Phleger and Parker 1951), 3
Bolivina simplex (Phleger and Parker 1951), 4 Bolivina spathulata
(Williamson 1858), 5 Bulimina aculeata (dOrbigny 1826), 6 Bulimina
alazanensis (Cushman 1927), 7 Bulimina striata mexicana (Cushman
1922), 8 Cassidulina laevigata (dOrbigny 1826), 9 Cibicidoides
kullenbergi (Parker et al. 1953), 10 Eponides turgidus (Phleger and
Parker 1951), 11 Globobulimina affinis (dOrbigny 1839), 12a
Gyroidina altiformis (spiral view) (Stewart and Stewart 1930), 12b.
Gyroidina altiformis (profile view) (Stewart and Stewart 1930), 13
Hormosina globulifera (Brady 1879), 14 Hyperammina elongata
(Brady 1878), 15 Oridorsalis tenerus (Brady 1884), 16a Osangularia
culter (spiral view) (Parker and Jones 1865), 16b Osangularia culter
(umbilical view) (Parker and Jones 1865), 17 Praeglobobulimina
pupoides (dOrbigny 1846), 18 Saccorhiza ramosa (Brady 1879), 19
Sphaeroidina bulloides (dOrbigny 1826), 20 Usbekistania charoides
(Jones and Parker 1860), 21 Uvigerina peregrina (Cushman 1923), 22
Uvigerina pygmaea (dOrbigny 1826). Scale bars =100μm
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Tabl e 1 Relative abundance of
species representing greater than
2% for each collection at PCB06
and DSH08 for the surface
(010 mm) and down-core
(1050 mm) intervals
Species Percent
Dec 2010 Feb 2011 Sep 2011 Aug 2012
PCB06
010 mm
Archimerismus subnodosus 22
Bolivina lowmani 7
Bolivina spathulata 43 6
Bulimina aculeata 21 6 5 8
Bulimina alazanensis 258612
Bulimina marginata 3
Cibicidoides kullenbergi 74
Cibicidoides pachyderma 4
Cibicidoides robertsonianas 2
Cribrostomoides subglobulosum 3
Hormosina globulifera 3
Hyperammina elongata 14
Hyperammina friabilis 8
Hyperammina laevigata 2
Osangularia culter 3
Saccorhiza ramosa 92
Sphaeroidina bulloides 15 26 19
Usbekistania charoides 42
Uvigerina peregrina 21 19
Uvigerina pigmaea 2122
<2% 21 13 19 19
1050 mm
Archimerismus subnodosus 443
Bulimina aculeata 11 11 5 6
Bulimina alazanensis 2755
Cibicidoides kullenbergi 6104
Cibicidoides pachyderma 6
Hormosina globulifera 33
Hyperammina elongata 37
Hyperammina friabilis 2
Oridorsalis tenerus 4
Osangularia culter 2
Saccorhiza ramosa 11 7 5
Sphaeroidina bulloides 29 30 27 35
Uvigerina peregrina 542217
Uvigerina pigmaea 33 4
<2% 26 20 20 21
DSH08 Dec 2010 Feb 2011 Sep 2011 Aug 2012
010 mm
Bolivina albatrossi 23
Bolivina lowmani 34
Bolivina simplex 4
Bolivina spathulata 444
Bolivina striatula 2
Bulimina aculeata 20 19 14 8
Bulimina alazanensis 4442
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(Brooks et al. 2015). It follows that the surface 10 mm at these
sites was potentially impacted by the DWH event, and there-
fore, the following objectives of the study can be addressed:
(1) establishing similarities between previous (baseline) fora-
miniferal surveys in the nGoM with the down-core intervals
(section 4.1), (2) assessing potential impacts of the DWH
event on the benthic foraminifera in the surface intervals by
contrasting them with previous surveys (section 4.2.1) as well
as down-core interval (section 4.2.2), and (3) characterizing
benthic foraminiferal variability in the surface intervals in the
interest of establishing a time of recovery from the assessed
impact (section 4.3).
Comparison of down-core intervals with previous
foraminiferal surveys
In general, there were similarities between the down-core records
of benthic foraminifera from this study and those from previous
studies in the nGoM between 1000- and 1300-m water depth.
The most dominant agglutinated species (S. ramosa) in PCB06
agreed with the findings of Bernhard et al. (2008). The dominant
calcareous taxa throughout the down-core records from this
study were primarily B. aculeata and U. peregrina, which agreed
with dominant taxa reported by Poag (1984), Denne and Sen
Gupta (1991), and Sen Gupta et al. (2009).
Tabl e 1 (continued)
Species Percent
Dec 2010 Feb 2011 Sep 2011 Aug 2012
Bulimina striata mexicana 4562
Cassidulina laevigata 333
Eponides turgidus 2
Globocassidulina subglobosa 3
Gyroidina altiformis 4446
Osangularia culter 2
Paratrochammina challengeri 32
Praeglobobulimina pupoides 20 7 6 4
Saccorhiza ramosa 3
Sphaeroidina bulloides 233
Usbekistania charoides 353
Uvigerina peregrina 31312
Uvigerina pigmaea 32
<2% 25 36 39 49
1050 mm
Bolivina lowmani 3446
Bolivina simplex 35
Bolivina spathulata 2
Bulimina aculeata 22 17 15 8
Bulimina alazanensis 3332
Bulimina striata mexicana 3232
Cassidulina laevigata 333
Eponides turgidus 2222
Globobulimina affinis 3
Gyroidina altiformis 7546
Osangularia culter 3
Paratrochammina challengeri 2
Praeglobobulimina pupoides 7171315
Sphaeroidina bulloides 4332
Usbekistania charoides 32
Uvigerina peregrina 3 4 12 8
Uvigerina pigmaea 2
<2% 34 38 33 40
Blank spaces represent <2% relative abundance
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Assessing impacts of the Deepwater Horizon event
on benthic foraminifera
Comparison of surface intervals with previous foraminiferal
surveys
The initial approach to assess impact to benthic foraminiferal
variability by environmental parameters was a comparison of
density, S,E,H, and dominant taxa from surface intervals in this
study to previous surveys of control sites and natural hydrocar-
bon seeps.
The densities from previous studies [control sites with no
hydrocarbon influence, 102(DeSoto Canyon)-174(South of
Mississippi Canyon) indiv./cm
3
] were similar to the surface
intervals from DSH08 with the exception of the record from
December 2010 (Sen Gupta et al. 2009). The surface interval
densities at PCB06 were all noticeably lower than those re-
ported from previous studies.
The densities in the surface intervals from DSH08
Dec. 2010 and PCB06 Feb 2011 agreed with the significantly
lower densities found at natural seeps (284 indiv/cm
3
)(Sen
Gupta et al. 2009). This supported the claim that the increased
concentration of hydrocarbons was the dominant control of
foraminiferal density in the surface intervals.
While there are no active natural seeps at DSH08 and
PCB06, it was worthwhile to compare the benthic foraminifera
at these sites in the context of short-term oil-derived hydrocar-
bon exposure (DWH) to the previous records of benthic fora-
minifera present at natural seep sites (chronic, long-term expo-
sure). The dominant species in the surface intervals were not
entirely similar to those found at natural seep sites in the
Mississippi Canyon (1000-m water depth) (Lobegeier and
Sen Gupta 2008;SenGuptaetal.2009). While there were
common species that were dominant (B. lowmani,
B. aculeata,E. turgidus,H. elongata,U. peregrina), several
species that dominate seep sites were not present (e.g.,
B. ordinaria,G. translucens) (Sen Gupta and Aharon 1994;
Lobegeier and Sen Gupta 2008). However, it is difficult to
directly compare the benthic foraminiferal community at these
sites to natural seep sites due to differing microenvironments.
The seep sites used for comparison were often dominated by
bacterial (Beggiatoa) mats, which are primarily low oxygen and
high hydrogen sulfide environments (Panieri 2005).
Globocassidulina subglobosa is known to be abundant un-
der depleted oxygen conditions due to increased organic sed-
imentation (Sen Gupta and Machain-Castillo 1993; Panieri
2005). G. subglobosa is significantly abundant only in the
2010 DSH08 record, which is consistent with a MOSSFA
event.
This suggested that benthic foraminifera from these sites
that were impacted by a short-term release of oil-derived hy-
drocarbons, such as the DWH event, respond differently than
Fig. 2 Compilation of benthic foraminiferal density, S,E,H,PAH
concentrations (LMW-blue diamonds, HMW-black squares), and Mn
and Re concentrations with depth for each collection at PCB06 with
reference to the surface interval (010 mm). Y-axes are depth in
millimeters. For the S,E,andHplots, the blue circles are raw data and
the green circles are a three-point running mean. Black lines represent the
down-core (1050 mm) mean
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benthic foraminifera impacted continuously by natural
sources and are subject to quite different environments.
It is evident from the comparison of the surface intervals in
this study to previous studies, both control sites and natural
seep sites, that the DSH08 and PCB06 sites were impacted in
December 2010 and February 2011, respectively. This com-
parison also suggests that despite differences in community
structure, short-term (DWH) and long-term (seeps) exposure
to hydrocarbons can limit benthic foraminiferal density at
these water depths.
Comparing the surface intervals to down-core intervals
The second approach to assess impact to benthic foraminiferal
variability by environmental parameters was a comparison of
density, S,E,andHfrom the down-core intervals to the sur-
face intervals in each record. There was a notable and signif-
icant decrease (relative to the down-core interval) in density in
the surface interval of the December 2010 and February 2011
records from DSH08 and PCB06, respectively. This decrease
was also noted by Schwing et al. (2015) at the generic level.
The mean density and Hdecrease significantly in the
December 2010 DSH08 record from the down-core interval
to the surface interval (Figs. 3and 4b, d; Tables 2and 3).
These indices also decreased significantly in the February
2011 PCB06 record from the down-core interval to thesurface
interval (Figs. 2and 4a, c; Tables 2and 3). Decreases between
the down-core and surface intervals were not observed in any
of the other records.
The decreases in density, S,E,andHin the surface intervals at
DSH08 in December 2010 and PCB06 in February 2011 were
synchronous with increased accumulation (Brooks et al. 2015)
and settling rates (Passow et al. 2012) of marine oil snow, which
caused reducing conditions (Hastings et al. 2016) in the surface
sediments as well as increased concentrations of potentially toxic
hydrocarbons (Romero et al. 2015). Schwing et al. (2015) found
that the decrease in foraminiferal density was not caused by
dilution of the benthic foraminifera by increased particulate input
from the water column, but likely by increased PAH concentra-
tions. Accordingly, we argue below that the decrease in density
was caused by increased petroleum hydrocarbon concentrations.
In the December 2010 and February 2011 records from both
sites, samples from the surface interval grouped (7580% simi-
larity) with PAH concentrations, especially low-molecular-
weight PAHs (Fig. 5). Total PAH concentrations prior to the
DWH event in the Desoto canyon ranged from 0 to
147 ng g
1
(Wade et al. 2008). Following the DWH event, total
PAH concentrations at DSH08 and PCB06 ranged from 267 to
363 ng g
1
(Romero et al. 2015). PAHs have been shown to
cause increased mortality, decreases in density, and inhibition
of reproduction in benthic foraminifera over a broad range of
concentrations (363 ng g
1
to4.9mgg
1
) (Yanko et al. 1999;
Ernstetal.2006; Mojtahid et al. 2006;DiLeonardoetal.2007;
Schwing et al. 2015). Denoyelle et al. (2012) found that concen-
trations of oil-laden drilling mud (non-aqueous based mud) can
Fig. 3 Compilation of benthic
foraminiferal density, S,E,H,
PAH concentrations (LMW-blue
diamonds, HMW-black squares),
Mn and Re concentrations with
depth for each collection at
DSH08 with reference to the
surface interval (0-10 mm). Y-
axes are depth in millimeters.
Note: for the S,E,andHplots, the
blue circles are raw data, the
green circles are a 3-point runnin g
mean. Black lines represent the
down-core (10-50 mm) mean
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cause significant reduction in new chamber production
(100 μgg
1
) and pseudopodal activity (500 μgg
1
). From cul-
ture studies of estuarine Ammonia tepida, Morvan et al. (2004)
Tabl e 2 Total benthic foraminiferal density for each increment (median depth) as well as mean (μ) and standard deviation (1σ) for the surface interval
(010 mm) and the down-core interval (>10 mm) for each collection
Dec 2010 Feb 2011 Sep 2011 Aug 2012
Depth (mm) indiv./cm
3
Depth (mm) indiv./cm
3
Depth (mm) Indiv./cm
3
Depth (mm) indiv./cm
3
PCB06
1 33 1 1 1 48 1 89
5 56 5 1 5 58 3 73
9 75 9 10 9 48 5 93
13 53 13 42 13 57 9 136
17 24 17 44 17 37 13 64
21 40 21 38 21 34 17 95
25 41 25 43 25 49 21 82
29 44 29 38 29 42 25 122
33 62 33 63 33 36 29 70
37 32 37 73 37 55 33 114
41 58 42.5 82 41 43 37 96
49 11347.572455141141
45 115
49 86
μ(010 mm) 55 4 51 98
1σ21 5 6 27
μ(>10mm)52554598
1σ26 17 8 24
μ(total)53424698
1σ24 27 8 25
DSH08
1 41184184176
5 6 5 69 3 153 5 84
9 39 9 72 7 92 9 99
13 67 13 89 11 118 13 85
17 44 17 53 15 81 17 175
22.5 57 21 96 19 95 21 135
32.5 199 25 72 23 93 25 166
42.5 97 29 70 27 103 29 126
52.5 99 33 83 31 140 33 176
37 72 35 118 37 161
41 148 39 124 41 152
45 50 43 144 45 187
49 75 47 178 49 176
μ(010 mm) 16 108 110 86
1σ20 66 38 11
μ(>10 mm) 94 81 119 154
1σ56 27 29 31
μ(total) 68 87 117 138
1σ60 38 30 40
Fig. 4 Plots of the surface (010 mm) total benthic foraminiferal density
(plots a,b), S(plots c,d), E(plots e,f), and H(plots g, h) for each date of
collection at PCB06 and DSH08. Standard deviations (1σ)arerepresent-
ed by error bars.Horizontal black lines and gray bars represent the
down-core (1050 mm) mean and standard deviation, respectively
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Tabl e 3 Fishersalpha(S), equitability (E), and Shannon-Wiener (H) for each increment as well as mean (μ) and standard deviation (1σ) for the surface
interval (010 mm) and the down-core interval (>10 mm) for each collection
PCB06
Dec 2010 Depth (mm) SEHFeb 2011 Depth (mm) SEH
1 12 0.8 2.7 1 3 0.6 1.3
5 11 0.8 2.7 5 3 0.7 1.3
9 12 0.8 2.9 9 4 0.6 1.5
13 11 0.8 2.8 13 11 0.7 2.6
17 9 0.7 2.4 17 8 0.7 2.3
21 10 0.8 2.6 21 9 0.8 2.5
25 10 0.8 2.6 25 7 0.8 2.5
29 11 0.8 2.7 29 11 0.8 2.7
33 11 0.8 2.6 33 11 0.7 2.6
37 11 0.7 2.4 37 10 0.8 2.7
41 11 0.8 2.6 43 9 0.8 2.5
45 9 0.7 2.3 48 11 0.7 2.3
49 12 0.8 2.9
μ(010 mm) 11 0.7 2.6 μ(010 mm) 3 0.6 1.4
1σ0 0.0 0.1 1σ1 0.1 0.1
μ(>10 mm) 10 0.7 2.4 μ(>10 mm) 9 0.7 2.4
1σ1 0.0 0.1 1σ1 0.0 0.2
Sep 2011 Depth (mm) SEHAug 2012 Depth (mm) SEH
1 11 0.7 2.5 1 9 0.8 2.8
5 11 0.7 2.5 3 9 0.8 2.6
9 11 0.7 2.5 5 8 0.8 2.5
13 10 0.7 2.4 9 8 0.8 2.5
17 9 0.7 2.4 13 9 0.7 2.5
21 10 0.7 2.5 17 10 0.7 2.5
25 9 0.7 2.6 21 10 0.7 2.5
29 9 0.7 2.6 25 10 0.7 2.4
33 9 0.7 2.5 29 10 0.7 2.4
37 8 0.7 2.3 33 10 0.7 2.3
41 8 0.7 2.2 37 9 0.7 2.4
45 8 0.7 2.2 41 10 0.7 2.3
49 8 0.7 2.1 45 8 0.7 2.1
49 8 0.6 1.9
μ(010 mm) 11 0.7 2.5 μ(010 mm) 8 0.8 2.6
1σ0 0.0 0.0 1σ0 0.0 0.1
μ(>10 mm) 9 0.7 2.4 μ(>10 mm) 9 0.7 2.4
1σ0 0.0 0.2 1σ0 0.0 0.1
DSH08
Dec 2010 Depth (mm) SEHFeb 2011 Depth (mm) SEH
1 12 0.8 2.6 1 20 0.8 3.4
5 13 0.8 2.7 5 22 0.8 3.4
9 16 0.8 2.9 9 23 0.8 3.3
13 19 0.8 3.2 13 23 0.8 3.3
17 19 0.8 3.1 17 23 0.8 3.3
22.5 19 0.8 3.2 21 22 0.8 3.3
32.5 18 0.8 3.2 25 22 0.8 3.3
42.5 19 0.8 3.3 29 19 0.8 3.2
52.5 18 0.8 3.2 33 20 0.8 3.2
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found that inhibition of reproduction was caused by total petro-
leum hydrocarbon concentrations between 150 and 300 μgg
1
.
Morvan et al. (2004) also found uncommonly low densities (1
indiv./cm
3
) of benthic foraminifera in field studies following the
Erika oil spill for up to 21 months. Despite the difference be-
tween environments (estuarine vs. continental slope), this was
consistent with the low densities found in the surface interval of
the February 2011 PCB06 (1 indiv./cm
3
) and December 2010
DSH08 records (4 indiv./cm
3
). Romero et al. (2015) found sed-
imentary total petroleum hydrocarbon (aliphatic) concentrations
at DSH08 ranging from 46 to 332 μgg
1
and PCB06 ranging
from20to36μgg
1
in the December 2010 and February 2011
records. Despite lower total petroleum hydrocarbon (TPH) con-
centrations at PCB06, the type (primarily LMW PAH) and form
(primarily dissolved species) of the hydrocarbons (Romero et al.
2015) likely played a role in their control of benthic foraminiferal
variability. The fact that the TPH values from DSH08 and
PCB06 were similar and in some cases in excess (DSH08) of
those found to cause low densities and inhibition of reproduction
(Denoyelle et al. 2012; Morvan et al. 2004) strongly suggested
that hydrocarbon concentrations were driving the benthic fora-
miniferal variability in the surface interval during the December
2010 and February 2011 collections from both sites.
There was evidence that subtle increases in rhenium concen-
tration in the surface interval of the December 2010 DSH08
and February 2011 PCB06 records were controlling benthic
foraminiferal density and diversity (Figs. 2and 3). According
to Hastings et al. (2016), these increases in rhenium concentra-
tion indicated shoaling of the redoxcline (reducing surface
sediments). However, rhenium does not group strongly with
the surface benthic foraminifera intervals (Fig. 5). So, redox
variability was likely a secondary environmental driver of ben-
thic foraminiferal density and diversity in the December 2010
DSH08 and February 2011 PCB06 records.
Overall, a significant impact was assessed in the surface in-
terval of the December 2010 collection from DSH08 and the
February 2011 collection from PCB06. This impact was charac-
terized by a significant decline in total benthic foraminiferal
density and diversity relative to down-core intervals.
Considering the timing of the impact, the strong grouping of
PAH concentrations with samples in the surface interval, and
the previously documented effects of petroleum on benthic fo-
raminifera at low concentrations, it was likely that petroleum
hydrocarbon concentrations were the driver of benthic forami-
niferal variability.
Establishing time of recovery: surface interval time series
variability
Following the impact in December 2010 and February 2011 at
DSH08 and PCB06, respectively, the density at each site re-
covered heterogeneously in the surface interval. At PCB06,
there was a protracted recovery from February 2011 to August
2012 (Fig. 4a, Table 2). At DSH08, the density increased
dramatically from December 2010 to February 2011 and
remained consistent in the September 2011 and August 2012
records. The relatively high densities of B. aculeata in 2010,
which thrive in areas of high organic carbon deposition and in
Tabl e 3 (continued)
37 19 0.8 3.2
41 23 0.8 3.3
45 22 0.8 3.2
49 24 0.8 3.3
μ(010 mm) 14 0.8 2.7 μ(010 mm) 22 0.8 3.4
1σ2 0.0 0.2 1σ1 0.0 0.0
μ(>10 mm) 19 0.8 3.2 μ(>10 mm) 22 0.8 3.3
1σ0 0.0 0.0 1σ2 0.0 0.1
Sep 2011 Depth (mm) SEHAug 2012 Depth (mm) SEH
1 25 0.8 3.5 1 34 0.9 3.7
3 24 0.8 3.4 5 35 0.9 3.8
7 25 0.8 3.4 9 36 0.9 3.9
11 22 0.8 3.3 13 37 0.9 3.8
15 21 0.8 3.2 17 35 0.9 3.7
19 19 0.8 3.2 21 34 0.9 3.7
23 21 0.8 3.3 25 32 0.9 3.6
27 21 0.8 3.3 29 30 0.8 3.5
31 22 0.8 3.3 33 29 0.8 3.4
35 21 0.8 3.2 37 29 0.8 3.4
39 19 0.8 3.2 41 28 0.8 3.5
43 22 0.8 3.2 45 26 0.8 3.5
47 22 0.8 3.3 49 24 0.8 3.4
μ(010 mm) 24 0.8 3.4 μ(010 mm) 35 0.9 3.8
1σ0 0.0 0.0 1σ1 0.0 0.1
μ(>10 mm) 21 0.8 3.3 μ(>10 mm) 30 0.8 3.6
1σ1 0.0 0.1 1σ4 0.0 0.1
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Fig. 5 Non-metric
multidimensional scaling plots of
each collection. Black dots
represent each increment with
depth (distance is relative to
similarity of benthic foraminiferal
fauna), green vectors represent
the magnitude and orientation of
environmental parameters
[polycyclic aromatic hydrocarbon
concentrations (LMW PAH,
HMW PAH), redox metal
concentrations (Re, Mn), grain
size (CFM(g))], gray ellipses
represent the surficial (010 mm)
interval which groups with PAH
concentration and, in some cases,
Mn concentration, green ellipses
represent the intermediate interval
(1030 mm) which groups
solely with Mn concentration, and
blue ellipses are the deep interval
(>30 mm) which group solely
with Re. The numbers associated
with each cluster represent the
Bray-Curtis similarity (%)
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areas of increased petroleum concentration (total petroleum
hydrocarbons 16111 mg g
1
,Mojtahidetal.2006), and sub-
sequent decrease (through August 2012) supported the hy-
pothesis of initial impact of the DWH event and subsequent
recovery (Table 1).
One of the most important metrics following an impact such
as the one documented in the records of December 2010 and
February 2011 at DSH08 and PCB06 was the time needed for a
complete benthic foraminiferal recovery. As discussed previous-
ly, there was a protracted recovery in density at PCB06 from
February 2011 until August 2012, which suggested that some
areas take as much as a year and a half to recover. However, all of
the densities measured at PCB06 were significantly lower than
those previously reported from other surveys in the nGoM.
Therefore, further collections are necessary to establish whether
the benthic foraminifera have fully recovered as of August 2012.
There was also a protracted recovery in diversity at DSH08 from
December 2010 to August 2012. This evidence supports a re-
covery time on the order of between 1 and 2 years, which is
consistent with the findings of Morvan et al. (2004) following
the Erika oil spill.
Conclusions
1. An impact, characterized by decreases in benthic forami-
niferal density and diversity, as well as strong grouping
with PAH concentrations, was documented in the surface
interval (010 mm) of the sedimentary records collected
in December 2010 at DSH08 and February 2011 at
PCB06.
2. The subsequent recovery was characterized by a hetero-
geneous response at both sites. At PCB06, there was a
protracted recovery in density and a rapid recovery in
diversity. However, at DSH08, there was a rapid recovery
in density and a protracted recovery in diversity. The rapid
recovery in density and gradual recovery in diversity were
likely caused by a dominance of opportunistic taxa that
are able to thrive in areas with high organic carbon depo-
sition and petroleum concentration.
3. The records of impact and recovery of benthic foraminif-
era suggested that the benthic recovery time, following an
event such as the DWH, was on the order of 12years.
However, future collections will be necessary to deter-
mine if these sites have fully recovered as early as
August 2012, considering that some of the metrics (e.g.,
density at PCB06) continue to be significantly below the
densities found in previous studies conducted in the
nGoM before the DWH event. Future work is also neces-
sary to document the connectivity of benthic foraminifera
with higher trophic levels in order to determine any
longer-term impacts from the DWH event in the nGoM.
Acknowledgments This research was made possible in part by a grant
from the Gulf of Mexico Research Initiative, C-IMAGE, and DEEP-C
and in part by the British Petroleum/Florida Institute of Oceanography
(BP/FIO)-Gulf Oil Spill Prevention, Response, and Recovery Grants
Program. The authors also thank the crew of the R/V Weatherbird II for
their help during the field program. Data are publicly available through
the Gulf of Mexico Research Initiative Information & Data Cooperative
(GRIIDC) at https://data.gulfresearchinitiative.org/R1.x135.120:0004.
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Environ Sci Pollut Res
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... These changes in oxygen concentrations at the sedimentwater interface and their morphological characteristics are reflected in the size, wall thickness, porosity, and taxa (genera and species) of presented foraminifera. Some morphological and taxonomic differences have been quantified as a dissolved oxygen index (FBOI) (Kaiho, 1994), which, together, with the change in the abundance, diversity, density, and dominance of this group provides information on oil release events or spills in marine reservoirs (Schwing et al., 2017;Pan et al., 2017;Panieri, 2005). ...
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