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Benthos response following petroleum exploration in the southern
Caspian Sea: Relating effects of nonaqueous drilling fluid, water depth,
and dissolved oxygen
R.D. Tait
a
,C.L.Maxon
b,
⁎,T.D.Parr
c
, F.C. Newton III
b
a
Exxon Mobil Corporation, 22777 Springwoods Village Parkway, Spring, TX 77389, USA
b
Maxon Consulting, 2546 San Clemente Terrace, San Diego, CA 92122, USA
c
Terry Parr Environmental Consulting Services, 7924 Grape Street, La Mesa, CA 91924, USA
abstractarticle info
Article history:
Received 16 January 2016
Received in revised form 25 February 2016
Accepted 26 February 2016
Available online 11 July 2016
The effects of linear alpha olefin (LAO) nonaqueous drilling fluid on benthic macrofauna were assessed over a six
year period at a southern CaspianSea petroleum exploration site. A wide-ranging, pre-drilling survey identified a
relatively diverse shelf-depth macrofauna numerically dominated by amphipods, cumaceans, and gastropods
that transitioned to a less diverse assemblage dominated by hypoxia-tolerant annelid worms and motile ostra-
cods with increasing depth. After drilling, a similar transition in macrofauna assemblage was observed with in-
creasing concentration of LAO proximate to the shelf-depth well site. Post-drilling results were consistent with
a hypothesis of hypoxia from microbial degradation of LAO, supported by the presence of bacterial mats and
lack of oxygen penetration in surface sediment. Chemical and biological recoveries at ≥200 m distance from
the well site were evident 33 months after drilling ceased. Our findings show the importance of monitoring re-
covery over time and understanding macrofauna community structure prior to drilling.
© 2016 The Authors. Published by Elsevier Ltd. This is an open access article under the CC BY-NC-ND license
(http://creativecommons.org/licenses/by-nc-nd/4.0/).
Keywords:
Hypoxia
Benthic macrofauna
Nonaqueous drilling fluid (NADF)
Linear alpha olefin(LAO)
Caspian Sea
Drill cuttings
1. Introduction
Studies on impacts to aquatic environments associated with oil and
gas exploration and production have been conducted over the past few
decades, with many focusing on benthic community effects from
discharge and accumulation of drill cuttings and nonaqueous drilling
fluid (NADF) on the seafloor (Kingston, 1992; Neff et al., 2000;
Schaanning et al., 2008). Effects include physical smothering and acute
toxicity, as well as habitat alteration, such as organic enrichment,
changes to sediment particle size, and increased oxygen demand. The
most widely used synthetic NADFs are esters, poly alpha olefins, and
olefin isomers, including linear alpha olefin (LAO). These fluids tend to
be less toxic and degrade faster in aquatic environments than their
petroleum-based predecessors and hence, should present less risk to
the receiving environment. The short-term toxicity of synthetic drilling
fluids is well characterized in laboratory studies using standard test or-
ganisms (Still et al., 2000; Munro et al., 1998), as are in situ effects of
ester-based drilling fluid discharged in offshore environments
(Roberts and Nguyen, 2006). However, information is lacking on the
effect mechanism and subsequent recovery over time of benthic macro-
fauna from LAO-based fluids and their associated drill cuttings.
This study assesses effects on macrofauna associated with discharged
cuttings with adhered LAO at a single well site located at 145 m water
depth, approximately 45 km off the Azerbaijan coastline in the southern
Caspian Sea. Exploration drilling commenced in July 2001 and ended in
January 2002. The well was drilled to a target sub-seafloor depth of ap-
proximately 6700 m using water-based drilling fluid in the top sections
and LAO fluid for the deeper well sections. Barium, in the form of barite,
was used in both sections as the weighting agent. Results are examined
from an August 1998 regional pre-drilling survey and two focused post-
drilling surveys conducted in September 2002 and November 2004
(Fig. 1).
The pre-drilling macrofauna community is described in Parr et al.
(2007) as a relatively diverse macrofauna, numerically dominated by
amphipods, cumaceans, annelid worms, and gastropods at shelf depths
(b150 m), compared with increasingly hypoxic habitats dominated by a
few species of annelid worms and crustaceans at deeper depths. Results
for the 2002 post-drilling survey, conducted eight months after well
completion, are reported in Tait etal. (2004). The presentstudy expands
on the 1998 regional pre-drilling and 2002 post-drilling studies by in-
cluding 2004 results to examine LAO degradation and macrofauna re-
covery 33 months after drilling ceased, and to propose and evaluate
the hypothesis that the primary effect mechanism on macrofauna at
the well site was hypoxia from the microbial degradation of LAO.
Marine Pollution Bulletin 110 (2016) 520–527
⁎Corresponding author.
E-mail addresses: russell.d.tait@exxonmobil.com (R.D. Tait),
maxonc@maxonconsulting.com (C.L. Maxon), terparr@cox.net (T.D. Parr),
newtonf@maxonconsulting.com (F.C. Newton).
http://dx.doi.org/10.1016/j.marpolbul.2016.02.079
0025-326X/© 2016 The Authors. Published by Elsevier Ltd. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
Contents lists available at ScienceDirect
Marine Pollution Bulletin
journal homepage: www.elsevier.com/locate/marpolbul
2. Study design and methods
2.1. Study design
The 1998 pre-drilling survey sampled sediments 30 months before
the start of drilling in the northern half of the Nakhchivan contract
area, which included the future well site location (Fig. 1). Fifty-six
sediment samples were collected over a depth range of 67–692 m at
36 stations, including six stations with 3–5field replicates to establish
small-scale (within-station) estimates of variance to aid post-drilling
sampling design. The well site location, which was designated later,
was not sampled.
Post-drilling studies were designed to quantify spatial changes in
macrofauna, sediment chemistry, and sediment particle size in relation
to drilling operations and discharged cuttings. The post-drilling design
was based on the spatial variability of macrofauna estimated from the
1998 regional dataset and hydrodynamic modeling (Nedwed et al.,
2004), which predicted that LAO retained on drill cuttings would settle
within 400–600 m of the well site, without strong directionalbias due to
persistently weak subsurface circulation. Comparison of pre-drilling
mean results for nine key macrofauna variables showed no statistical
differences (one-way ANOVA, pN0.05) and homogeneity of variance
(Levene, 1960)(pN0.05) between tightly grouped station replicates
and more distant non-replicated stations sampled within the same
depth range as the well site (data not shown). Therefore, stations locat-
ed at 800–1000 m from the well site at depths of 120–170 m could be
used as a within-survey reference group to evaluate effects from the
drilling-related discharge.
Twenty-five post-drilling sediment samples were collected in 2002,
and 15 of those stations were re-sampled in 2004 (Fig. 1, right). In 2002,
five stations each were located along five transects (N, NE, SE, SW and
NW) at distances of 50 m (well site), 200 m, 400 m, 600 m, and 800 m
(reference) from the well site. In 2004, only the N, SE, and SW transects
were re-sampled, following 2002 results indicating near omnidirection-
al settling of discharged cuttings. The design was modified slightly in
the 2004 post-drilling survey, resulting in the replacement of an 800-
m station located at a depth of 192 m (station 17), with a 1000-m sta-
tion located at a depth of 135 m (station 24), similar to the well site
depth. Station 17 results were excluded from the 2002 dataset.
In 2000, 2002, and 2004 dissolved oxygen (DO) measurements from
the water surface to within 5–10 m above the seafloor were profiled at
29 locations, ranging from 0 to 80 km of the well site. Near-bottom
water DO at the 145-m deep well site was above the hypoxia upper
limit of 2 ml l
−1
(Diaz and Rosenberg, 1995), ranging from 4 to
6.5 ml l
−1
. Concentrations at or below 1 ml l
−1
, the lower limit of hyp-
oxia (Levin, 2003), were measured in near-bottom waters N600 m.
Combined results showed stable near-bottom concentrations ranging
from N7mll
−1
DO at shallow stations, grading into hypoxic conditions
at stations deeper than 400 m (Fig. 2).
Regional pre-drilling and focused post-drilling sediments were ana-
lyzed for grain size, sedimentorganic carbon, macrofauna,41 polycyclic
aromatic hydrocarbons (PAH), nC
9
–nC
44
saturated hydrocarbons (SHC),
and 14 metals.Sediment profile imaging (SPI) photographs and analysis
of LAO were conducted on post-drilling sediments only. SPI provided in-
formation on the horizontal and vertical extent of settled cuttings, evi-
dence of bacterial mats, and estimates of reduction–oxidation
potential discontinuity (RPD), a surrogate for the depth of oxygen pen-
etration in surface sediment (Rosenberg et al., 2001). Except for total
PAH, post-drilling chemical results, including sediment organic carbon,
Fig. 1. Regional and survey area maps showing location of Nakhchivan contract area (left), 1998 pre-drilling stations (middle), and 2002 and 2004 post-drilling station locations (right).
Shallow (120–170 m) pre-drilling stations used in post-drilling comparisons are identified (□,middle).
Fig. 2. Dissolved oxygen concentrations in near-bottom water measured in the southern
Caspian Sea over a four year period. Hypoxia upper limit (2 ml l
−1
) predicted at ~400 m
bottom depth.
521R.D. Tait et al. / Marine Pollution Bulletin 110 (2016) 520–527
were commensurate with pre-drilling results at similar depths, and
therefore, excluded from the present study. Summed results (e.g., total
PAH = sum of 43 analytes, LAO = sum of 6 analytes) were evaluated,
reducingthe original data set from over 400 variables to ten macrofauna
and two chemical variables (Fig. 4). Statistical analyses of macrofauna
were limited to general community indicators of total abundance, spe-
cies richness (no. of taxa per 0.1 m
2
grab sample), dominance (total
no. of taxa with the highest abundances that comprise N50% of total
abundance per 0.1 m
2
grab sample), and abundances of higher taxo-
nomic groups, rather than genus or species.
2.2. Field and laboratory methods
Sediment collection methods were consistent across surveys, and
are described in Parr et al. (2007), which presents results for macrofau-
na (0.1 m
2
grab, 500 μm sieve), sediment particle size, and organic car-
bon from the 1998 pre-drilling study.
Laboratory methods are described in Tait et al. (2004) for all param-
eters except LAO, which was quantified as C
14
–C
18
parent compounds
and the sum of corresponding isomers by GC with a flame ionization de-
tector using a modification of the SHC method described in Douglas
et al. (1994). Benthic macrofauna were identified to the lowest practical
taxonomic level (usually genus or species) and enumerated. Species
vouchers (preserved in 70% ethanol) are held by the Benthic
Invertebrate Collection, Scripps Institution of Oceanography, University
of California, San Diego.
3. Results
3.1. SPI photographs
Estimated RPD depths were absent or extremely shallow (≤0.5 cm)
in well site sediments, reaching reference depths (2.5–3.4 cm) at dis-
tances of 400 m in 2002, and generally at 200 m in 2004. Colonies of a
dense white bacterium, resembling Beggiatoa sp., observed in all 2002
well site images and three 200 m images, were completely absent in
2004. Differences between 2002 and 2004 sediment conditions at
≤200 m from the well site are represented in photos taken at post-
drilling station 4 (Fig. 3). White mats covering black, refractive cuttings
and adhered muds in 2002 transitioned to 1–4 cm deep deposits of light
brown sediment in 2004. The majority of 2004 SPI photographs at
≥200 m from the well site displayed evidence of active bioturbation in
the top 4–5 cm, with burrows extending beyond a depth of 5 cmin sev-
eral images, most likely from the polychaete Nereis diversicolor, a rela-
tively large deeper burrowing organism.
3.2. Sediment LAO and PAH
Mean LAO (log-transformed) was significantly elevated at the well
site and at the 200 m station group compared to reference stations in
2002 and 2004 (Table 1). LAO concentrations ranging from 3740 to
25,200 μgg
−1
decreased exponentially from the well site to
b15 μgg
−1
at 600–800 m in 2002 and to b2μgg
−1
(the limit of
Table 1
Comparison of post-drilling data grouped by distance from the well site. Only significant (pb0.05) ANOVA results shown. Groups with different letters are significantly different from
Duncan's test (Duncan, 1955). No significant difference in homogeneity of variance (Levene, 1960) indicated by ‘ns’.
Key
parameter
50 m 200 m 400 m 600 m 800 m
reference
ANOVA
F-ratio
ANOVA
p
Levene
p
2002 post-drilling
RPD depth
a
C BC AB A A 9.77 b0.01 b0.01
Total PAH
b
A AB B B B 9.66 b0.01 ns
LAO
b
A A B B B 18.1 b0.01 ns
Amphipod
a
B A A A A 9.97 b0.01 b0.01
Cumacea B A A A A 0.23 0.04 ns
Oligochaete
a
C BC AB A AB 9.00 b0.01 b0.01
Polychaete
a
B AB AB A A 8.97 b0.01 b0.01
Total abundance B A A A A 0.41 0.02 ns
Species richness
a
B A A A A 18.7 b0.01 b0.01
2004 post-drilling
RPD depth B AB AB A A 6.84 0.01 ns
Total LAO
a,b
A B BC BC C 17.7 0.01 b0.01
Total PAH
a,b
A B B B B 8.29 b0.01 0.03
Species richness B AB AB A A 4.44 0.03 ns
a
Welch (1951) ANOVA for unequal variances.
b
Log-transformed data.
Fig. 3. SPI photos of representative 2004 reference sediment (left)and post-drillingsediment at 200 m from thewell site in 2002 (middle) and in 2004 (right).Dashed lines represent the
average apparent RPD layer. White bacterial mats on surface of settled cuttings are visible in 2002 photo.
522 R.D. Tait et al. / Marine Pollution Bulletin 110 (2016) 520–527
Fig. 4. Mean results (+std. dev.) for LAO, PAH, and key macrofauna parameters for 1998 shallow pre-drilling (SP) stations (120–170 m depth), 1998 deep pre-drilling (DP) stations
(≥600 m depth), and 2002 and 2004 post-drilling stations grouped by distance (m) from the well site. NM = not measured.
523R.D. Tait et al. / Marine Pollution Bulletin 110 (2016) 520–527
detection) at 400–800 m in 2004 (Fig. 4). The post-drilling spatial distri-
bution of LAO in surfacesediment around the well site is shown in Fig. 5.
Total PAH (log-transformed) was significantly elevated at the well
site compared to all other post-drilling station groups (Table 1). Con-
centrations of total PAH based on 41 analytes ranged from 78 to
9000 ng g
−1
across post-drilling surveys (Fig. 4), with lower concentra-
tions reported at all but a single well site station (4W). Sediment from
all post-drilling stations, except for 4W, had relatively uniform distribu-
tions of individual PAH analytes, with near equal concentrations of low
(2–3 ring) and high (4–6 ring) molecular weight compounds. Other
than at the well site, analyte distributions were similar to those found
in the majority of 1998 pre-drilling sediment, indicating combustion-
related sources from the prominence of 4- and 5-ring non-alkylated
PAH (LaFlamme and Hites, 1978). Sediment at station 4W had a much
higher proportion of 2- and 3-ring PAH, dominated by alkylated naph-
thalenes (i.e., nC
2
-tonC
4
-naphthalenes), alkylated phenanthrene/an-
thracenes, and to a lesser extent alkylated fluorenes, possibly from
degraded petroleum (Steinhauer and Boehm, 1992) or leached natural
gas condensate. Although the LAO formulation used at Nakhchivan
was 0.0005% total PAH by weight, it was comprised mainly of
acenaphthene (76%), which was low (b2% of total PAH) in post-
drilling well site samples, indicating a PAH source to sediment other
than drilling fluid. For this reason, and because concentrations were el-
evated only at one well site station and a single 200 m station in 2002,
total PAH was removed from further analysis.
3.3. Benthic macrofauna
In general, abundances of major taxonomic groups and community
indicators of total abundance, species richness, and dominance were re-
duced at the well site compared to shallow (120–170 m depth) pre-
drilling stations (n= 22) and 800-m reference stations (n=9)
(Fig. 4). In 2002, amphipod and cumaceanabundance, species richness,
and dominance were significantly lower at the well site compared with
the 800-m reference group (Table 1). In 2004, only well site species
richness remained significantly depressed compared to reference.
In 2002, ostracod crustaceans comprised 51% of total abundance at
50–400 m from the well site compared with only 1.6% in 2004.Ostracod
colonization of sediments has been reported from natural saline envi-
ronments where periodic or episodic hypoxia occurs (Gamenick et al.,
1996; Modig and Olafsson, 1998), and may be an effective sentinel of
eutrophication, organic loading, and anthropogenic impact (Ruiz et al.,
2005). The post-drilling dominance of ostracods was limited in space
and time to a 400 m radius around the well site in 2002. Numbers
were dramatically reduced in 2004, trending toward shallow pre-
drilling abundances. The pelecypod Didacna profundicola, which was
found at relatively low abundance in shallow pre-drilling sediment
(avg. 27 m
−2
), was the only other post-drilling taxa with abundance
≥600 m
−2
at the well site (2002 only).
Excludingwell site stations, average abundances of polychaetes and
cumaceans generally were higher in 2002 compared with both 2004
and shallow pre-drilling abundances (Fig. 4). In contrast, average abun-
dances of amphipods and gastropods were lower in most 2002 groups.
Differences tended to be greatest between 2002 and 2004 reference sta-
tions, indicating naturally high temporal variability in the four afore-
mentioned groups. Only three of ten macrofauna parameters differed
statistically between shallow pre-drilling and post-drilling reference
groups (Table 2).
Hypania invalida, a highly eurytopic species, was the dominant poly-
chaete in all surveys, with the highest relative abundance recorded in
2002 (74% of all polychaetes). It is present in freshwater rivers, reser-
voirs, and brackish habitats throughout Europe, having been introduced
into the Caspian in the last 50 years through its canal connection with
the Black Sea (Karpinsky, 1992).
Whereas amphipods were completely absent at the well site in
2002, four species were recorded in 2004, with a collective average
abundance of 130 m
−2
. Extendingout to 200 m from the well site, aver-
age amphipod abundance increased to 1713 m
−2
, similar to 800 m ref-
erence sites. Molluscan gastropod (snail) species, mainly from a single
genus, Turricaspia displayed significant increases in average abundance
between post-drilling surveys; however, there were no significant
within-survey differences.
4. Discussion
Several lines of evidence indicate hypoxia from microbial degrada-
tion of LAO drilling fluid as a probable factor in observed changes in
post-drilling benthic community structure. Lines of evidence fall into
three major categories: 1) dense white bacterial mats coupled with ab-
sence of a discernible RPD layer in well site surface sediments, 2) degra-
dation of the LAO chemical signature over time, and 3) changesin post-
drilling macrofauna community structure with increased LAO that
paralleled depth/DO related changes in the pre-drilling community.
4.1. Hydrocarbon-degrading bacteria
Beggiatoa sp. is found in Caspian Sea sediments (Salmanov, 2006)
and is an effective petroleum hydrocarbon degrader under aerobic
and anaerobic pathways (Atlas, 1981). In 2002, dense white filamen-
tous bacterial mats, resembling Beggiatoa sp., were observed at all but
Fig. 5. Spatial distribution of LAO in surface sediment around the well site in 2002 (left) and 2004 (right) post-drilling surveys.
524 R.D. Tait et al. / Marine Pollution Bulletin 110 (2016) 520–527
two stations located within 200 m of the well site. The densest mats
were observed at four well site stations with the highest LAO (11,513–
23,230 μgg
−1
) measured in 2002. Stations with LAO ranging from
1024 to 7130 μgg
−1
had patchy occurrences of less dense mats. In
2004, well site sediments had no visible mats, and LAO concentrations
at ≤200 m from the well site were lower (3.17–3740 μgg
−1
) at all but
well site station 4W, wh ich was 2000 μgg
−1
higher than in 2002, noting
an 18 m offset in station location between surveys.
4.2. Degradation of LAO in post-drilling sediment
Fresh LAO consists primarily of normal straight-chain alkanes with a
terminal olefin, with minor contributions of alkylated (branched-chain)
isomers for each C
14
to C
18
constituent. As LAO degrades, relative concen-
trations of alkylated isomers (e.g., C
14
isomers) increase, and the corre-
sponding parent compound (e.g., C
14
) decreases under aerobic or
anaerobic bacterial pathways (Atlas, 1981; Sauer et al., 1993). This pat-
tern was observed between 2002 and 2004 post-drilling sediments
with N50 μgg
−1
LAO (Fig. 6).
Between post-drilling surveys (ca. 8 months), there was a 42% aver-
age decrease in sediment LAO at five stations (avg. distance = 78 m)
with the highest initial concentrations. This result is fairly consistent
with an average decrease of 48% over 7 months reported for stations lo-
cated at 75 m distance from a North Sea well site drilled using ester-
based fluid (Daan et al., 1996).TherateofdecreaseinLAOissomewhat
unexpected, because slower microbial degradation rates for olefinversus
ester-based drilling fluid formulations in fine-grained sediment are re-
ported from both laboratory (Mille et al., 1988) and field studies
(Roberts and Nguyen, 2006), which cite relative field degradation rates
of synthetic NADFs as: ester NLAO Nacetal Nether ≫mineral oil. High
populations of indigenous hydrocarbon-degrading bacteria (Salmanov,
2006) aided by hypoxia tolerant, bioturbating tubificid worms (Parr
et al., 2007; Karpinsky, 1992) may have contributed to the relatively
rapid LAO degradation rate observed at the Caspian Sea well site.
4.3. Evidence of LAO-induced hypoxia
There were statistically demonstrable declines in species richness
and dominance with increased bottom depth (decreased DO) in the
pre-drilling survey, and with increased LAO in combined post-drilling
surveys. These relationships were strongest with species richness
(Fig. 7), and insignificant with total abundance (pN0.05). The dimin-
ished response of post-drilling totalabundance was partially due tocon-
flicting trends between fauna, in which abundance of most groups
decreased significantly with increasing LAO, but several actually
flourished. Ostracod crustaceans, the pelecypod D. profundicola,and
two species of polychaete worms (N. diversicolor,H. invalida)werethe
only fauna with abundances greater than 600 m
−2
(the highest average
abundance for any shallow pre-drilling species) found in sediment with
N5000 μgg
−1
LAO; and ostracods were the only enriched fauna
(N2000 m
−2
) in sediment with N15,000 μgg
−1
LAO. The decline in av-
erage ostracod abundance from 2002 to 2004 (1046 to 88.6 m
−2
)was
accompanied by an approximate 70% decline in LAO from the well site
out to 400 m distance.
Dominance of certain fauna in sediment with high concentrations of
LAO mimics the response of hypoxia-tolerant polychaetes (Woulds
et al., 2007) and motile ostracods (Noguera and Hendrickx, 1997)toor-
ganically enriched sediment. The enhanced number of ostracods at a
mud-volcano site sampled in the Nakhchivan Contract Area in 1998,
and their overwhelming numerical dominance at post-drilling well
site stations, indicate a strong chemo-sensory capability as opportunist
foragers. Didacna sp. also tolerates moderate levels of organic loading
Fig. 6. Percent distribution of LAO analytes measured in the initialLAO drilling fluid (prior
to discharge) and in 2002 and 2004 post-drilling sediment samples collected from well
site station 1W. The relative increase in alkylated isomers and corresponding decrease
in the associated parent compound over time denotes a typical hydrocarbon microbial
degradation pattern.
Fig. 7. Regression results (±95th conf. interval) for post-drilling log LAO ( ) vs. species
richness, using only sediment samples N2μgg
−1
total LAO (n= 22). Results for pre-
drilling station bottom depth ( ) vs. species richness plotted for comparison. Upper and
lower hypoxia limits predicted using Fig. 2 regression results.
Table 2
Comparison of shallowpre-drilling and post-drillingreference data. Only significant (pb0.05) ANOVA results shown. Groupswith different lettersare significantly different from Tukey's
HSD test. No significant difference in homogeneity of variance (Levene, 1960) indicated by ‘ns’.
Key parameter Shallow predrilling n= 7 2002 reference n= 4 2004 reference n= 4 ANOVA F-ratio ANOVA pLevene p
Cumacea
a
A B A 23.3 b0.01 .04
Total abundance A B AB 5.08 0.02 ns
Species richness A A B 6.83 0.01 ns
a
Welch (1951) ANOVA for unequal variances.
525R.D. Tait et al. / Marine Pollution Bulletin 110 (2016) 520–527
and low oxygen, and was the only genus of pelecypod molluscs from
pre-drilling sediment at depths greater than 600 m, while also com-
monly occurring at shallower depths.
The normal shallow water (120–170 m) pre- and post-drilling
benthos resides in a stable environment of sufficient bottom water DO
(N4–7.5 ml l
−1
), with the highest values of species richness (17–41
taxa 0.1 m
−2
grab) and dominance (8–19 species) reported across sur-
veys. In general, the shallow benthos was distinguished by a relatively
abundant and diverse pericarid crustacean fauna, dominated by amphi-
pod families Gammaridae, Corophiidae and Haustoriidae. Abundance of
gastropods (snails) and molluscan pelecypods (clams) also were
highest in this depth range. This community structure was observed in
all post-drilling sediments with ≤100 μgg
−1
LAO.
The benthiccommunity found at depths of 400–600 m (with bottom
water DO predicted at 1–2mll
−1
) in the pre-drilling survey andat post-
drilling stations with LAO N100–500 μgg
−1
was less diverse (≤15 taxa
0.1 m
−2
grab) than the normal shallow water community. This transi-
tional community was increasingly dominated by the hypoxia tolerant
ampharetid polychaete H. invalida,afewspeciesoftubificids (an oligo-
chaete family that is also tolerant of hypoxia), 2–8 cumacean groups
(most capable of leaving the sediment to enter the water column),
and 4–7 groups each of amphipods, gastropods, and pelecypods.
Post-drilling stations located within 50 m of the well site and at a
single 200 m station with high LAO (2000–10,000 μgg
−1
) in general,
had community characteristics s imilar to those found a t pre-drilling sta-
tions sampled at ≥600–692 m depth, where hypoxic conditions
prevailed. This oxygen deprived community was dominated by
H. invalida, with patchy occurrences of several motile cumaceans, and
the bivalve D. profundicola.
Other than relatively high abundances (N850 m
−2
) of an unidentified
ostracod species within 50–200 m of the well site, post-drilling sediments
with N10,000 μgg
−1
LAO had low individual abundances (10–150 m
−2
)
of only a few hypoxia-tolerant annelid worms (H. invalida,N. diversicolor,
Psammoryctides deserticola) and two species of Cumacea (Schizorhynchus
eudorelloides,Stenocuma diastyloides). A similarly depauperate communi-
ty was not found in the pre-drilling survey that had a maximum sampling
depth of 692 m with a predicted bottom water DO of 0.72 ml l
−1
(below
the lower limit of hypoxia) (Fig. 7).
5. Conclusions
Our findings show the importance of monitoring recovery over time
and understanding natural changes in macrofauna community structure
related to water depth and oxygen availability prior to drilling. Although
direct causal relationships were not established, the independent, parallel
relationship between LAO and bottom depth (as a surrogate for dissolved
oxygen) with species richness indicate hypoxia as the most likely cause of
the observed taxonomic shift from a relatively diverse macrofauna to a
less diverse assemblage dominated by a few fauna. At the shelf-depth
well site in 2002, eight months after drilling ceased, dense bacterial
mats and dominance by an unidentified ostracod lead us to hypothesize
that LAO is a strong attractor of certain chemo-sensory fauna.
In 2004, recolonization around the wellsite was well underway with
recruitment cues approaching normal at a threshold of approximately
100 μgg
−1
LAO. Abundances of six out of seven taxonomic groups at
200–600 m from the well site were commensurate with shallow pre-
drilling and 2004 post-drilling reference results, as were the more con-
servative indictors of total abundance, species richness, and dominance.
Thus, the area of maximum observable effects, 33 months after well
completion, was contained to a relatively uniform area less than
0.12 km
2
, centered near the well site.
Our results have implications for predicting impacts to macrofauna
from drilling discharges containing low-toxicity, biodegradable syn-
thetic NADF. These discharges should have relatively little impact on a
macrofauna that resides beyond shelf depths and is naturally
impoverished due to oxygen deficiency. In contrast, oxygen-sensitive,
shelf depth macrofauna may be acutely impacted, but should recover
relatively quickly with the coincident degradation of NADF.
Acknowledgments
We thank the State Oil Company of the Azerbaijan Republic for
supporting the environmental assessments and granting permission to
publish these results, and in particular, Dr. Iffat Afandiyeva. Appreciation
also is due to a large staff of scientists who performed a variety of field,
laboratory, and administrative tasks. We are grateful to the Benthic Inver-
tebrate Collection laboratory at Scripps Institution of Oceanography
(UC San Diego), La Jolla, California for archiving the taxonomic voucher
collection of Caspian Sea macrofauna produced from this study. This
research and its associated field surveys were funded by Exxon
Azerbaijan Operating Company.
References
Atlas, R.M., 1981. Microbial degradation of petroleum hydrocarbons: an environmental
perspective. Microbiol. Rev. 45, 180–209.
Daan, R., Booij, K., Mulder, M., Van Weerlee, E.M., 1996. Environmental effects of dis-
charge of drilling cuttings contaminated with ester-based drilling muds in the
North Sea. Environ. Toxicol. Chem. 15, 1709–1722.
Diaz, R.J., Rosenberg, R., 1995. Marine benthic hypoxia: a review of its ecological effects
and the behavioral resp onses of benthic macrof auna. Oceanogr. Mar. Bio l. Annu.
Rev. 33, 245–303.
Douglas, G.S., Prince, R.C., Butler, E.L., Steinhauer, W.G., 1994. In: Hinchee, R.E., Alleman,
B.C., Hoeppel, R.E., Miller, R.N. (Eds.), Hydrocarbon Bioremediation. Lewis Publishers,
Ann Arbor, MI, pp. 219–236.
Duncan, D.B., 1955. Multiple range and multiple F tests. Biometrics 11, 1–42.
Gamenick, I., Jahn, A., Vopel, K., Giere, O., 1996. Hypoxia and sulfide as structuring factors
in a macrobenthic community on the Baltic Sea shore: colonisation studies and toler-
ance experiments. Mar. Ecol. Prog. Ser. 144, 73–85.
Karpinsky, M.G., 1992. Aspects of the Caspian Sea benthicecosystem. Mar. Pollut. Bull. 24,
384–389.
Kingston, P.F., 1992. Impact of offshore oil production installations on the benthos of the
North Sea. ICES J . Mar. Sci. 49, 45.
LaFlamme, R.E., Hites, R.A., 1978. The global distribution of polycyclic aromatic hydrocar-
bons in recent sediments. Geochim. Cosmochim. Acta 42, 289–303.
Levene, H., 1960. Robust tests for the equality of variance. In: Olkin, I. (Ed.), Contributions
to Probability and Statistics. Stanford University Press, Palo Alto, CA, pp. 278–292.
Levin, L.A., 2003. Oxygen minimum zone benthos: adaptation and community response
to hypoxia. In: Gibson, R.N., Atkinson, R.J.A. (Ed s.), Oceanograp hy and Marine
Biology: An Annual Review Vol. 41. Taylor and Francis, NY, NY, pp. 1–45.
Mille, G.,Mulyono, M., El Jammal, T., Bertrand, J.C., 1988. Effects of oxygenon hydrocarbon
degradation studies in vitro in surficial sediments. Est uar. Coast. Shelf Sci. 27,
283–295.
Modig, H., Olafsson, E., 1998. Responses of Baltic benthic invertebrates to hypoxic events.
J. Exp. Mar. Biol. Ecol. 229, 133–148.
Munro, P.D., Bronwen, C., Moffat, C.F., Brown, N.A., McIntosh, A.D., Hird, S.J., Stagg, R.M.,
1998. Solid-phase test for comparison of degradation rates of synthetic mud base
fluids used in the off-shore drilling industry. Environ. Toxicol. Chem. 17, 1951–1959.
Nedwed, T.J., Smith,J.P., Brandsma, M.G., 2004. Verification of the OOC mud and prod uced
water discharge model using lab-scale plume behavior experiments. Environ. Model.
Softw. 19, 655–670.
Neff, J.M.,McKelvie, S., Ayers Jr., R.C.,2000. Environmentalimpacts of syntheticbased dril-
ling fluids. Report Prepared for MMS by Robert Ayers & Associates, Inc. August 2000.
U.S. Department of the Interior, Minerals Management Service, Gulf of Mexico OCS
Region, New Orleans, LA (OCS Study MMS 2000-064. 118 pp).
Noguera,S.E.G., Hendrickx,M.E., 1997. Distribution and abundance of meiofaunain a sub-
tropical coastal lagoon in the south-eastern Gulf of California, Mexico. Mar. Pollut.
Bull. 34, 582–587.
Parr, T.D.,Tait, R.D., Maxon,C.L., Newton III, F.C.,Hardin, J.L., 2007.A descriptive account of
benthic macrofauna and sediment from an area of planned petroleum exploration in
the southern Caspian Sea. Estuar. Coast. Shelf Sci. 71, 170–180.
Roberts, D.J., Nguyen, A.H., 2006. Degradation of Synthetic-basedDrilling Mud Base Fluids
by Gulf of Mexico Sediments: Final Report. U.S. Dept. of the Interior, Minerals Man-
agement Service, Gulf of Mexico O CS Region, New Or leans, LA (OCS Stu dy MMS
2006-028. 122 pp).
Rosenberg, R., Nilsson, H.C., Diaz, R.J., 2001. Response of benthic fauna and changing sed-
iment redox profiles over a hypoxic gradient. Estuar. Coast. Shelf Sci. 53, 343–350.
Ruiz, F., Abad, M., Bodergat, A.M., Carbonel, P., Rodriguez-Lazaro, J., Yasuhara, M., 2005.
Marine and brackish water ostracods as sentinels of anthropogenic impacts. Earth-
Sci. Rev. 72, 89–111.
Salmanov, M.A., 2006. Mic robiological studies in th e deepwater area of the southern
Caspian Sea. Microbiology 75, 206–212.
Sauer, T.C., Brown, J.S., Boehm, P.D., Aurand, D.V., Michel, J., Hayes, M.O., 1993. Hydrocar-
bon source identification and weathering characterization of intertidal and subtidal
sediments along the Saudi Arabian coast after the Gulf War Oil Spill. Mar. Pollut.
Bull. 27, 117–134.
526 R.D. Tait et al. / Marine Pollution Bulletin 110 (2016) 520–527
Schaanning, M., Trannum, H., Øxnevad, S., Carroll, J., Bakke, T., 2008. Effects of drill cut-
tings on biogeochemical fluxes and macrobenthos of marine sediments. J. Exp. Mar.
Biol. Ecol. 361, 49–57.
Steinhauer, M.S., Boehm, P.D.,1992. The compositionand distribution of saturated and ar-
omatic hydrocarbons in nearshore sediments, riversediments, and coastal peat of the
Alaskan Beaufort Sea: implications for detecting anthropogenic inputs. Mar. Environ.
Res. 33, 223–253.
Still, I., Rabke, S., Candler, J., 2000. Development of a standardized reference sediment to
improve the usefulness of marine benthic toxicity testing as a regulatory tool. Envi-
ron. Toxicol. 15, 406–416.
Tait, R.D., Maxon, C.L., Parr, T.D., Newton III, F.C., Hardin, J.L., 2004. Impact assessment and
benthic recruitment following exploration drilling in the south Caspian Sea. Proc.
Seventh International Conference on Heal th, Safety, and Environment in Oil and
Gas Exploration and Production, Calgary, Alberta, Canada. Society of Petroleum Engi-
neers, Richardson, Texas, USA, p. SPE86709 (12 pp).
Welch, B.L., 1951. On the comparison of several mean values: an alternative approach.
Biometrika 38, 330–336.
Woulds, C., Cowie, G.L., Levin, L.A., Andersson, J.H., Middleburg, J.J. , Vandewiele, S.,
Lamont, P.A., Larkin, K.E., Gooday, A.J., Schumacher, S., Whitcraft, C., Jeffreys, R.M.,
Schwarz, M., 2007 . Oxygen as a cont rol on seafloor bi ological communities and
their roles in sedimentary carbon cycling. Limnol. Oceanogr. 52, 1698–1709.
527R.D. Tait et al. / Marine Pollution Bulletin 110 (2016) 520–527
