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Marine Micropaleontology 101 (2013) 1–9
Contents lists available at SciVerse ScienceDirect
Marine Micropaleontology
journal homepage: www.elsevier.com/locate/marmicro
Benthic foraminiferal responses to water-based drill cuttings and natural sediment
burial: Results from a mesocosm experiment
Silvia Hess a,⁎, Elisabeth Alve a, Hilde Cecilie Trannum b, Karl Norling b, c
a
b
c
Department of Geosciences, University of Oslo, P.O. Box 1047, Blindern, 0316 Oslo, Norway
Norwegian Institute for Water Research, Gaustadalléen 21, 0349 Oslo, Norway
Department of Biosciences, University of Oslo, P.O. Box 1066, Blindern, 0316 Oslo, Norway
a r t i c l e
i n f o
Article history:
Received 4 September 2012
Received in revised form 6 March 2013
Accepted 13 March 2013
Available online 26 March 2013
Keywords:
Drill cuttings
Benthic ecosystem
Foraminifera vs macrofauna
Foraminiferal vertical migration
Recovery following disturbance
a b s t r a c t
Effects of burial by water-based drill cuttings and natural test sediment on living (stained) benthic foraminifera
were investigated in a mesocosm experiment. After 193 days, the foraminiferal response in sediment covered
with drill cuttings was compared to the response in sediment covered with defaunated natural test sediment.
Increasing thickness of added material, independent of type of material, significantly reduced the benthic
foraminiferal abundance and species richness. While most species managed to migrate through added sediments
of up to 12 mm thickness, results indicate that a burial depth of 24 mm severely limits the migration capability of
the foraminifera. Textularia earlandi and Bulimina marginata dominated the 0–1 cm of sediment (including
added material) in most mesocosms but the former was most resistant to maximum burial (24 mm). The
physical disturbance caused by the burial triggered reproduction in surviving populations of B. marginata and
Nonionellina labradorica. Addition of water-based drill cuttings and defaunated natural test sediments impacted
the microhabitat of N. labradorica differently. Stainforthia fusiformis seems to be the species most tolerant to the
water-based drill cuttings. Results indicate that the foraminiferal faunal composition respond differently to the
two different materials added, even if only agglutinated forms are considered. This agrees with earlier
macrofaunal results from the same experiment which indicate that the water-based drill cuttings represent an
additional stress factor for the benthic community.
© 2013 Elsevier B.V. All rights reserved.
1. Introduction
Offshore petroleum activities affect the local marine environment in
various ways. During drilling processes, large quantities of drill
cuttings, i.e., a mixture of fragments of reservoir rocks, chemicals, and
drilling mud, are produced. In some regions, these drill cuttings are
partly discharged to the sea floor. Their impact on the marine benthic
ecosystem depends on the amount, rate and type of waste products
discharged which in turn influence e.g., the degree of burial, oxygen
depletion, and toxicity of the drilling fluids used in the drilling mud
(Singsaas et al., 2008). Drilling mud is a suspension of solids (e.g.,
clay, barite, ilmenite) in liquids (e.g., water, oil) containing chemical
additives as required to modify its properties (Neff, 2005). Three
main types of drilling mud have been used in exploration and production including oil-, synthetic- and water-based drilling mud. Of these,
the water-based drilling mud, with relatively low hydrocarbon concentration and low toxicity, has been regarded as having the least environmental impact on marine ecosystems (Olsgard and Gray, 1995; Neff,
⁎ Corresponding author. Fax: +47 22854215.
E-mail addresses: silvia.hess@geo.uio.no (S. Hess), ealve@geo.uio.no (E. Alve),
hilde.trannum@niva.no (H.C. Trannum), karl.norling@niva.no (K. Norling).
0377-8398/$ – see front matter © 2013 Elsevier B.V. All rights reserved.
http://dx.doi.org/10.1016/j.marmicro.2013.03.004
2005). Consequently, the use of water-based drilling mud has increased in offshore production areas and water-based cuttings, which
are produced when using this mud, are considered to affect the marine
benthic community mainly through physical disturbance (burial)
(Neff, 2005). However, recent impact-studies using water-based drill
cuttings (Schaanning et al., 2008; Trannum et al., 2010, 2011) indicate
that factors other than just sedimentation influence the macrofaunal
community structure.
Foraminifera are an important component of marine benthic communities. The usefulness of these heterotrophic protists in environmental monitoring has been shown for a wide range of environments
over the past half century (summaries in Alve, 1995; Nigam et al.,
2006; Martínez-Colón et al., 2009). Compared to macrofaunal organisms, which are traditionally used in environmental monitoring, most
benthic foraminifera occur in high densities, respond fast to environmental changes (high population turnover rate), and mineral-walled
forms commonly produce a fossil record. This fossil record provides information about the in situ pre-impacted ecological status of an environment (Alve et al., 2009; Dolven et al., 2013). A few studies have
focused on the impact of oil drilling activities on benthic foraminifera
(e.g., Locklin and Maddocks, 1982; Morvan et al., 2004; Ernst et al.,
2006; Denoyelle et al., 2012) and only recently benthic foraminifera
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S. Hess et al. / Marine Micropaleontology 101 (2013) 1–9
have been used to evaluate effects of drill cutting disposals on benthic
environments (Durrieu et al., 2006; Mojtahid et al., 2006; Jorissen et al.,
2009; Denoyelle et al., 2010).
The main aim of this study is to investigate possible impacts that
burial by Water-Based drill cuttings (WB) may have on benthic foraminifera and compare the results with the effects of burial by natural
Test Sediments (TS). Furthermore, the results of the foraminiferal
study are used for comparison with macrofaunal community responses from the same experiment as described and discussed in
Trannum et al. (2010).
2. Materials and methods
2.1. Mesocosm set-up
Twenty-four box-core samples (inner liner surface area 0.09 m 2)
with benthic communities were collected 3rd March 2006 at 41 m
water depth in the Bjørnhodebukta, Oslofjord, Norway (58°42.78′N,
10°33.19′E). The box-core liners were transferred to a mesocosm
set-up at the Norwegian Institute for Water Research's (NIVA) Marine
Research Station Solbergstrand. All box-core liners were carefully
placed in two basins filled with seawater, and during the experiment
continuously supplied with Oslofjord seawater from 60 m water
depth. The temperature was kept at ambient level of about 10 °C
throughout the experiment. After 8 weeks (18th May 2006), WB
and TS were added to the mesocosms. The WB, taken from a
land-based deposition plant, originated from a drilling operation in
the Barents Sea and contained, in addition to rock fragments
(cuttings), remnants of ilmenite (FeTiO3) as weighting material and
polyalkylene glycol as lubricant. The TS, collected at the same location
as the box-core sediments, was sieved through a 1 mm sieve and the
smaller fraction was defaunated by freezing prior to addition to the
mesocosms. Both kinds of material, WB and TS, were mixed with seawater into a slurry and gently poured into the overlying water of the
mesocosms with minimal disturbance of the sediment surface.
Water-based drill cuttings were added to obtain thicknesses of 3, 6,
12, and 24 mm (WB3, WB6, WB12 and WB24) and TS was added to
obtain thicknesses of 6, 12, and 24 mm (TS6, TS12 and TS24), with
3 replicate mesocosms per treatment. Three box-core liners were
left untreated and used as controls (C). For further information
concerning the experimental design, see Trannum et al. (2010). Limitations of the experimental design are discussed in Section 4.5.
2.2. Measurements and data analyses
After 193 days (5th December 2006), the experiment was terminated and the mesocosms were sampled for faunal analyses. A short
sediment core (5.5 cm diameter; 23.8 cm2 surface area) was collected
from each mesocosm for benthic foraminiferal examination. In order to
sample the majority of the assemblages in each sediment core and to
investigate preferred living depths after burial, the upper 4 cm of
each core (including added sediment layers) were sliced as follows:
0–1, 1–2, and 2–4 cm. Most samples were preserved in 3% buffered
formalin (Natriumtetraborat-10-hydrate) in seawater whereas six 1–
2 cm-samples were preserved in 70% ethanol (due to logistical
problems; samples are marked in Appendix Table 1), all stained with
rose Bengal (1 g L −1) to distinguish between live and dead individuals
(Walton, 1952; Murray and Bowser, 2000). The remaining sediment in
each mesocosm was washed through a 0.5 mm sieve for retrieval of
macrofauna (see Trannum et al., 2010).
The foraminiferal samples were washed through 500 and
63 μm-sieves. The residues were dried at 40 °C. All rose Bengal stained
benthic foraminifera >63 μm in the 0–1 and 1–2 cm of each core were
picked with a wet brush, mounted on micro-sample slides, identified
and counted. A previous field-study in the same area showed very
low foraminiferal abundances at 2–4 cm sediment depth in this
environment (Alve and Bernhard, 1995). In the present study, 10
samples from this sediment level representing different treatments
were analyzed in order to check the foraminiferal abundance. Counting
results were standardized to individuals per 10 cm3 sediment. Maximum abundance of benthic foraminifera commonly occurs in the surface 0–1 cm of the sediment (Murray, 2006). Therefore, although
deeper layers were examined to consider burial/migration effects;
most analyses focused on the top 0–1 cm.
Response in abundance (N) and species richness (S) were tested
using t-test and 2-way ANOVA analyses. Prior to analyses the homoscedasticity was tested by Levene's test (Levene, 1960). Univariate statistical analyses were performed using the statistical language R version
2.13.2. To analyze similarities in the community structure, non-metric
multidimensional scaling (MDS)-ordinations were performed. These
analyses were based on Bray–Curtis similarity (Bray and Curtis,
1957). Before calculating the Bray–Curtis similarity, the raw abundance
data were transformed to square root in order to equalize the potential
contribution of each species. PERMANOVA was conducted to test the
multivariate patterns. However, due to low number of permutations
(b 60), analyses of difference between each set of treatments were
not performed (Anderson et al., 2008). Planned comparisons were
performed for differences between WB and TS in the top 0–1 cm sediment. The C and WB3 cores were excluded, and the 6, 12 and 24 mm
cores were treated together (i.e. WB consists of WB6(0–1), WB12(0–1)
and WB24(0–1) and TS consists of TS6(0–1), TS12(0–1) and TS24(0–1)).
Prior to PERMANOVA, the PERMDISP test was used to check the homogeneity of variances. The multivariate statistics were conducted using
PRIMER version 6.1.6 and PERMANOVA + version 1.0.3.
During the course of the experiment, biogeochemical variables in
the mesocosms, including total organic carbon (TOC) and oxygen
penetration depth were measured as discussed by Trannum et al.
(2010).
3. Results
In total, 72 living (stained) foraminiferal species were determined
to species level: 40 agglutinated and 32 calcareous ones. All identified
species are listed with taxonomic references in Appendix A. Living
(stained) foraminifera were present in all 0–1 and 1–2 cm samples
(Fig. 1, Appendix Table 1). In samples strongly dominated (> 75%)
by agglutinated species, some calcareous tests were thin and etched
indicating carbonate dissolution (Ca(0–1, 1–2), TS6b(0–1), TS6c(0–1),
TS24b(1–2), TS24c(0–1), WB6b(1–2), WB12b(1–2)). These samples are
marked in Fig. 1 and in Appendix Table 1. Of all samples from the
1–2 cm level which either had been preserved in ethanol or in formalin, individuals with calcareous tests made up 81% in the former and
78% in the latter.
Substantial variability of species richness (S) and abundance (N)
occurred between replicates in all treatments. The species richness in
the 0–1 and 1–2 cm was 10–40 and 4–32, respectively (Fig. 1). Overall,
species richness decreased with increasing thickness of added material
(Fig. 2). WB24 and TS24 had significantly fewer (p b 0.001) species in
the 0–1 cm (10–20 and 16–19, respectively) than the other treatments
(17–40 species), C included (Fig. 2, Table 1). The same pattern (but
with a weaker significance, p b 0.05) was observed if the WB + TS
12 + 24 mm treatments or if only agglutinated species (i.e., excluding
all calcareous species) were considered (Fig. 3). There was no significant difference in species richness between the C + TS and WB
samples (all treatments considered) (Table 1).
Highest abundances (N > 500 individuals ∗ 10 cm−3) in the top
0–1 cm were recorded in cores treated with 3–12 mm WB and in control core Ca (Fig. 1). The lowest values (N b 30 individuals ∗ 10 cm−3)
occurred in two of the WB24 cores. The overall abundance in the
0–1 cm was significantly higher than in the 1–2 cm (t-test, p b 0.005;
Fig. 4). The abundance in the 0–1 cm in the WB24 and TS24 cores was
significantly lower than in the remaining cores (p b 0.001, Table 1).
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0 - 1 cm
800
40
600
30
400
20
200
0
10
a* b
c
a
C
b* c*
a
TS 6
b
c
a
TS 12
c*
b
a
TS 24
b
c
a
WB 3
b
c
WB 6
a
b
c
WB 12
a
0
b
c
WB 24
1- 2 cm
800
40
600
30
400
20
200
10
0
number of species
stained individuals/10 cm3
3
number of species
stained individuals/10 cm3
S. Hess et al. / Marine Micropaleontology 101 (2013) 1–9
0
a* b
c
C
a
b
c
a
TS 6
b
TS 12
c
a
b* c
TS 24
a
b
c
WB 3
a
b* c
WB 6
a
b* c
WB 12
a
b
c
WB 24
Fig. 1. Foraminiferal abundance (stained individuals/10 cm3) of agglutinated (dark color) and calcareous (light color) taxa and species richness (• = number of species) in 0–1 cm
and 1–2 cm. * = samples influenced by carbonate dissolution. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this
article.)
T-test analyses and 2-way ANOVA indicate that the thickness of added
material influenced the complete foraminiferal assemblages significantly, independent of the material used (Tables 1, 2). The agglutinated assemblages (i.e., excluding all calcareous species) were impacted by the
added material and showed a significant interaction between the 2
factors “type of added material” and “thickness”, whereas the complete
Species richness (0-1cm)
number of species
40
30
20
10
0
stained individuals/10 cm3
0
5
10
15
20
25
20
25
Abundance (0-1 cm)
800
600
400
200
0
5
10
15
thickness of added material (mm)
control sediment (C)
test sediment (TS)
water-based
drill cuttings (WB)
Fig. 2. Species richness (number of species) and foraminiferal abundance (stained individuals/10 cm3) in the 0–1 cm sediment layer.
assemblage did not (Table 2). The abundance in the 2–4 cm level was
highest in WB3 − 6 and TS6 cores (0–42 individuals ∗ 10 cm−3) and
lowest (0–4 individuals ∗ 10 cm−3) below the added 24 mm layer in
both the TS24 and WB24 treatments (Appendix Table 1). The absolute
abundance was significantly lower (p b 0.001) in the 0–4 cm (i.e.,
added layer plus original surface sediment) of WB24 and TS24 than in
the 0–2 cm of C and WB3. This relationship was equally significant if
the WB12 and TS12 treatments were included (together with WB24
and TS24).
The most abundant species (> 10% in at least 2 cores) were
Textularia earlandi, Bulimina marginata, Stainforthia fusiformis, and
Nonionellina labradorica, accompanied by less abundant species such
as Adercotryma wrighti (Fig. 4). The foraminiferal assemblages in the
0–1 cm were mainly dominated by T. earlandi and B. marginata
irrespective of treatment. Both species had a significantly higher
abundance in the 0–1 cm than in 1–2 cm (p b 0.05). Textularia
earlandi occurred in all 0–1 cm samples and it was the dominant species in WB24. The absolute abundance of S. fusiformis was about twice
as high in the WB as in the TS samples, and its maximum abundance
occurred in the 1–2 cm irrespective of treatment. In the TS samples,
the maximum abundance of N. labradorica occurred in the 1–2 cm,
whereas in the WB samples, the maximum abundance was in the
0–1 cm layer. Adercotryma wrighti occurred regularly, with maximum
abundances at 0–1 cm, and with slightly higher abundances in the TS
than in the WB samples. Small individuals (b about 130 μm) of
B. marginata and N. labradorica were common in both TS and WB
cores.
The MDS analyses based on all living (stained) foraminifera in the
surface 0–1 cm separated all WB24 and two WB12 assemblages from
the others (Fig. 5a). The stress value of 0.11 shows that the MDS plot
gives a representative picture of the similarities or dissimilarities between the various treatments and replicates. Analyses based solely on
agglutinated species showed comparable groupings (Fig. 5b). At the
same time, the PERMANOVA on WB vs. TS (Table 3) indicates that
the communities in these two sample sets differ, even if only agglutinated forms are considered (p = 0.009 and p = 0.004, respectively),
i.e. that the response to the capping materials is different.
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S. Hess et al. / Marine Micropaleontology 101 (2013) 1–9
Table 1
Results of two-tailed t-tests. The possible effects of selected treatments on the species richness (S) and abundance (N) are calculated to identify significant (p ≤ 0.05) changes in the
0–1 cm sediment layer. Agglut. = agglutinated. C, TS and WB include all replicates.
t-Test
Species richness (S): all
taxa
Ho
df
t-Value
p-Value
df
t-Value
p-Value
df
t-Value
p-Value
df
t-Value
p-Value
C + TS6–24 = WB3-24
C + TS6 + WB3 + WB6 = TS12 + TS24 + WB12 + WB24
C + TS6 + TS12+ WB3 + WB6 + WB12 = TS24 + WB24
19
18
12
−0.05
3.11
5.86
0.96
b0.01
b0.001
21
21
9
1.57
3.66
3.14
0.13
b0.01
0.01
21
22
20
−0.09
3.09
5.48
0.93
b0.01
b0.001
16
13
21
1.29
2.7
2.91
0.22
0.02
b0.01
4. Discussion
4.1. Foraminiferal response to sediment thickness and material added
Some foraminiferal species are well known to be able to migrate
through the sediment (e.g., Severin, 1987; Gross, 2000; Ernst et al.,
2002). In the present study, the maximum benthic foraminiferal abundance mainly occurred in the upper 0–1 cm (Fig. 1) and the assemblages were dominated by small, shallow infaunal species b0.5 mm
in size. After addition of the new 3–24 mm thick sediment layers, the
pre-treatment “sediment surface” was suddenly situated at subsurface depths equal to the thickness of the added layer (e.g., below
12 or 24 mm), i.e., at least 6–48 times the size of the individuals. The
assemblages in these buried sediments could respond either by migrating up to the new sediment surface, by staying at the buried depth
level, or by dying. It is reasonable to assume that before addition of
the new material, the foraminiferal abundance in all cores was comparable to that of the C and the 3 mm (WB3) cores (Fig. 2). Consequently,
the significantly lower foraminiferal abundance in the top 0–4 cm
(i.e., added layer plus the original 0–2 cm) of the WB24 and TS24
cores compared to the 0–2 cm in the C and WB3 cores shows that
the vast majority of individuals had died rather than migrated during
Species richness
(0-1 cm; only agglutinated taxa)
number of aggl. species
40
30
20
10
0
stained individuals/10 cm3
5
10
15
20
25
Abundance
(0-1 cm; only agglutinated taxa)
800
600
400
Species richness (S):
only agglut. taxa
Abundance (N): all taxa
Abundance (N): only
agglut. taxa
the 193 days of the experiment. The facts that the abundance below
the thickest added layer was extremely low in both the TS and WB
cores, and that the redox boundary was mainly situated at 1–10 mm
sediment depth (see Trannum et al., 2010), also shows that the foraminiferal cytoplasm must have decayed in the anoxic pore waters during
the course of the experiment (otherwise it would have been stained by
the rose Bengal). On the other hand, Ernst et al. (2006) explained a
higher infaunal compared to epifaunal abundance after a 112 day
exposure to oil pollution as being due to staining of dead infaunal individuals during slow protoplasm degradation. The significantly lower
foraminiferal abundance in the 2–4 cm of the 24 mm treatments
than the abundance in those which had received no or b6 mm sediment, indicates that the physical component of the burial (i.e., not
only the anoxia) at least was co-responsible for the death of the
foraminifera.
In our experiment, most of the common species managed to
migrate through sediments up to 12 mm thickness, but a severe
reduction in species richness as well as abundance was recorded
when the sediment layer had increased to 24 mm, independent of
added material. A burial thickness of about 2 cm was also observed
as a limiting migration boundary for some foraminiferal species
after the Mt. Pinatubo ash layer deposit in the South China Sea
(Hess and Kuhnt, 1996; Hess et al., 2001; Kuhnt et al., 2005). In
concert, these findings indicate that 2 cm is a layer thickness which
severely limits the migration of benthic foraminifera. It appears that,
due to the small test size and the relatively slow migration speeds
(e.g., b 10 μm/min, Gross, 2000) of benthic foraminifera, there is a
critical burial thickness, beyond which the migration of the foraminifera back to the sediment surface is not possible. Laboratory experiments by Severin (1987) investigated the vertical movement of
the miliolid Quinqueloculina impressa after burial under a 4 cm thick
sand layer. After 3.5 days the author found very few (b5) individuals
of this rather fast moving species in the upper sediment centimeter.
Most individuals were still present at 4 cm sediment depth. A foraminiferal recolonization monitoring after a rapid ash layer deposit of
about 6 cm in the South China Sea resulted in a community composition on top of the new substrate which differed from the pre-ashfall
communities. This indicates that recruitment to the new substrate
happened from external sources (i.e., not a result of upward migration through the sediment) (Hess and Kuhnt, 1996). Comparable
observations were made after a rapid turbidite deposition with a
thickness varying between 8 and 18 cm in the Cap Breton Canyon in
the Bay of Biscay (Hess et al., 2005). These two field observations
show that a sediment cover of > 6 cm is a physical barrier for benthic
foraminifera which they are unable to overcome and burrow through.
200
4.2. Species response to stressed conditions
0
5
10
15
20
25
thickness of added material (mm)
control sediment (C)
test sediment (TS)
water-based
drill cuttings (WB)
Fig. 3. Species richness (number of species) and foraminiferal abundance (stained
individuals/10 cm3) in 0–1 cm. Based on agglutinated taxa only.
At the beginning of the experiment, the organic carbon content
was the same in the C and TS sediments (TOC 2.13%, Trannum et al.,
2010). The WB consisted primarily of inorganic particles and presumably some unknown organic compounds in addition to the polyglycol
resulting in a TOC of 0.84% (Trannum et al., 2010). Since no food was
added during the experiment, most labile food particles were probably exhausted by the end of the experiment leaving more refractory
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S. Hess et al. / Marine Micropaleontology 101 (2013) 1–9
All stained individuals 140
400
Individuals/10cm3
5
Adercotryma wrighti
120
300
100
80
200
60
40
100
20
0
0
0
5
10
20
5
10
140
120
120
100
100
80
80
60
60
40
40
20
20
15
20
25
Bulimina marginata
0
0
0
5
10
140
Individuals/10cm3
0
25
Textularia earlandi
140
Individuals/10cm3
15
15
20
0
25
Stainforthia fusiformis
5
140
120
120
100
100
80
80
60
60
40
40
20
20
10
15
20
25
Nonionellina labradorica
0
0
0
5
10
15
20
0
25
Thickness of added sediment (mm)
5
10
15
20
25
Thickness of added sediment (mm)
Fig. 4. Abundance (stained individuals/10 cm3, pooled replicates) of all and of the most common species in the 0–1 cm (filled symbols) and 1–2 cm (open symbols) sediment
layers. Blue circle = control (C), green triangle = natural test sediment (TS) treatment, and red square = water-based (WB) drill cutting treatment. (For interpretation of the
references to color in this figure legend, the reader is referred to the web version of this article.)
material behind as food for organisms which are not dependant on
fresh organic material (e.g., Alve, 2010). This might result in starvation and reduced abundance of the foraminiferal species which are
dependent on fresh organic material. The degradable phase in the
WB may also be used for bacterial growth which again may serve as
food for the surviving organisms in the WB mesocosms (Trannum
et al., 2010).
Most of the species abundant in the experimental sediments are well
known as opportunistic or stress-tolerant species (e.g., Barmawidjaja et
al., 1992; Alve and Bernhard, 1995). Opportunistic behavior mainly becomes evident after environmental disturbances and is characterized
by e.g., rapid reproduction. In the present study, T. earlandi represents
such an example. Additionally, the fact that B. marginata and
N. labradorica showed their maximum abundance in the WB and TS
cores (relative to controls) and appeared with high abundance of
young (small) specimens in both WB and TS cores, suggests that the
physical disturbance had triggered reproduction. These species had
probably reproduced following migration up to the new sediment
Table 2
Two-way ANOVA results testing the effects of added material (TS vs WB) and added sediment thickness on foraminiferal species richness (S) and abundance (N) in the 0–1 cm
sediment layer. Agglut. = agglutinated.
2-Way ANOVA
Species richness (S): All spp.
Species richness (S): Only
agglut. species
Abundance (N): All species
Abundance (N): Only
agglut. species
Factors
df
MS
F
p-Value
df
MS
F
p-Value
df
MS
F
p-Value
df
MS
F
p-Value
Added material (WB6−24, TS6 −24)
Thickness⁎ (6, 12, 24 mm)
Interaction (material × thickness)
Residual
Total
1
2
2
12
17
0.889
310.222
14.222
50.389
0.018
6.157
0.282
0.897
0.014
0.759
1
2
2
12
17
68.056
88.222
17.556
24.39
2.790
3.617
0.720
0.121
0.059
0.507
1
2
2
12
17
56.889
###
88067.056
###
b 0.001
5.065
0.761
0.983
0.025
0.488
1
2
2
12
17
110763.556
130011.500
92311.722
23299.833
4.754
5.580
3.962
0.050
0.019
0.148
⁎ Thickness of added material.
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S. Hess et al. / Marine Micropaleontology 101 (2013) 1–9
a) All living foraminifera
(0-1 cm; 23.8
cm2)
Transform: Square root
Resemblance: S17 Bray Curtis similarity
2D Stress: 0.11
TS24a
TS24c
PERMANOVA
TS12b
WB24a
TS24b
Ca
TS6c
WB6a
WB3c
WB24c
Table 3
PERMANOVA results a) based on all living (stained) foraminifera (calcareous and agglutinated) in 0–1 cm for WB6, 12, 24 vs TS6, 12, 24 and b) base on agglutinated living
(stained) foraminifera in 0–1 cm or WB6, 12, 24 vs TS6, 12, 24. Significant levels in
PERMANOVA were obtained from p-values calculated by permutations of residuals
under a reduced model. No. of unique permutations were 8148.
WB12b
TS12a
WB6b
Cb
Cc
TS6b
TS6a
WB3b
TS12c
WB3a
WB24b
SS
MS
Pseudo-F
P (perm)
⁎⁎ p b 0.01.
WB12c
WB12a
df
a) Based on all living (stained) foraminifera (calcareous and agglutinated) in 0–1 cm
1
4023
4023
2.91
0.009⁎⁎
WB6, 12, 24 vs TS6, 12, 24
Residual
16
22,118
1382
Total
17
26,140
b) Base on agglutinated living (stained) foraminifera in 0–1 cm
WB6, 12, 24 vs TS6, 12, 24
1
5345
5346
3.84
0.004⁎⁎
Residual
16
22,263
1392
Total
17
27,609
WB6c
b) Living agglutinated foraminifera
(0-1 cm; 23.8 cm2)
Transform: Square root
Resemblance: S17 Bray Curtis similarity
2D Stress: 0.1
TS12b
TS24a
WB6b
TS24b
WB24a
Cb
TS12a
TS24c
WB3c
WB12c
Cc
WB6a
WB3b
WB6c
WB12b
WB24c
TS6a
TS12c
Ca
TS6b
WB3a
WB12a
TS6c
WB24b
c) Macrofauna
(90 cm2)
Transform: Square root
Resemblance: S17 Bray Curtis similarity
2D Stress: 0.15
TS24-1
WB12-1
TS24-2
C-3
WB24-3
TS6-1
WB12-2
WB3-3
WB6-1
WB6-3
TS24-3
TS12-3
TS6-2
WB24-1
WB12-3
C-1
TS6-3
TS12-2
WB6-2
C-2
WB24-2
TS12-1
WB3-2
WB3-1
Control
test sediment
drill cuttings
Fig. 5. Plot of MDS-ordination of (a) all living foraminifera in 0–1 cm; (b) living agglutinated foraminifera in 0–1 cm; and (c) macrofauna (reprinted from the Journal of
Experimental Marine Biology and Ecology, 383, Trannum et al., 2010: Effects of sedimentation from water-based drill cuttings and natural sediment on benthic macrofaunal
community structure and ecosystem processes, with permission from Elsevier).
surface. Reproduction in response to physical stress has been observed
by e.g., Ernst et al. (2006). These authors also found a sudden appearance
of T. earlandi in high numbers as a response to oil pollution. Other species, such as A. wrighti showed slightly higher abundance in the TS compared to the WB cores and maintained their low population size in most
cores. This suggests that they survived the burial and that they seem to
respond more negatively to WB than to TS. Surprisingly, S. fusiformis, a
species well known for its opportunistic lifestyle (Alve, 2003), showed
relatively low abundances in most TS cores compared to WB and C
(Figs. 4). As S. fusiformis is known to reproduce within weeks in response
to phytoplankton blooms (Gustafsson and Nordberg, 2001), this low
abundance may be a response to the lack of labile organic matter input
that could serve as food for this species. In most WB treatments, S.
fusiformis was an important component of the foraminiferal assemblage
suggesting that the WB contained food source(s) not present in TS.
Nonionellina labradorica, which in natural environments often shows a
preference for levels below about 1 cm, seemed to migrate to the sediment surface in the WB mesocosms after the sediment input while it
had its maximum abundance in the 1–2 cm layer in the TS cores
(Fig. 4). This might reflect a special food preference of this species.
Pucci et al. (2009) described a trophic dependency of another infaunal
species, Nonionella turgida, on bacteria involved in anaerobic degradation
of organic matter. All living organisms in the TS material were killed by
deep-freezing prior to the addition of the sediment to the mesocosms.
The decay of this dead fauna might have been associated with bacteria
preferred by infaunal species like N. labradorica.
The foraminiferal assemblage composition, as reflected by the
MDS- and PERMANOVA analyses, also indicates that burial by WB initiated a different effect on the benthic foraminiferal community than
burial by TS. These observations suggest that the WB is associated
with other, additional stressors influencing the foraminiferal community. It has been observed that the presence of an organic phase
(polyalkylene glycol) in the WB cuttings leads to increased oxygen
consumption and eventually hypoxia in the sediments (Schaanning
et al., 2008; Trannum et al., 2010, 2011). Possibly, the WB cuttings
also lead to a toxic response (Trannum et al., 2011).
4.3. Agglutinated foraminiferal assemblages: How much of the story can
they tell?
One advantage by using benthic foraminifera in environmental
monitoring is their ability to leave a fossil record. If deposited in sediment accumulation basins, this allows comparison between the
present-day and in situ pre-impact assemblages, the latter representing
reference conditions (Alve et al., 2009; Dolven et al., 2013). However,
some taphonomic processes will always modify the original faunal
composition. Faunal components that most likely get destroyed are
soft-shelled monothalamids. Furthermore, syn- and post-depositional
dissolution of calcareous tests occurs in some environments, for example in Long Island Sound (Green et al., 1993) and in some marginal
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S. Hess et al. / Marine Micropaleontology 101 (2013) 1–9
marine areas along the coasts of the Skagerrak, E North Sea (Murray and
Alve, 1999). In such areas, it is useful to know if the preserved assemblages that remain after taphonomic loss of calcareous components
still record useful ecological information. Indeed, in the present experiment the species richness and community structure showed
similar responses to type of material added whether all fossilizable
species or only agglutinated species were considered (Table 1, Fig. 5).
As far as abundance is concerned, the agglutinated forms seem to be
more negatively affected by the WB than the complete assemblage
(Figs. 2, 3, Table 2). Consequently, our results show that even if assemblages have been impacted by carbonate dissolution, the agglutinated
assemblage alone reflects differences in effects of TS and WB cover.
Hence, the present study supports previous findings that agglutinated
assemblages are useful to detect ecological responses to environmental
variables (Murray and Alve, 2011 and references therein).
4.4. Macrofauna vs. foraminifera responses
The distribution pattern of macrofauna and foraminifera in our
mesocosm experiment indicates that both organism groups respond
to the addition of WB cuttings (Fig. 5). Trannum et al. (2010)
described a significant reduction in abundance and diversity of the
macrofauna with increasing thickness of the WB layer. Since no
macrobenthic response was observed to the addition of TS up to
24 mm thickness, Trannum et al. (2010) concluded that the impact
of WB on the macrofauna is not related to the burial proper and
must be triggered by a particular mechanism associated with the
WB, like hypoxia or toxicity. The benthic foraminiferal assemblages
also showed a reduction in abundance and species richness with
increasing thickness of the WB layer. However, as opposed to the
macrofauna, the foraminifera also responded negatively to the addition of TS, indicating that the burial overprinted a possible impact
caused by the WB treatment. We observed that most common species
in the mesocosms were able to migrate through sediment layers up to
12 mm thickness, but a highly significant decrease in abundance and
species richness was recorded when the thickness was 24 mm, independent of the added material. This finding indicates that, as opposed
to what is the case for the macrofauna, a sediment layer of about 2 cm
thickness severely limits the migration of benthic foraminifera and
represents a physical barrier for these meiofaunal organisms. In addition, the assemblage composition responded differently to the TS and
WB treatments as shown by the MDS and PERMANOVA analyses.
Consequently, as for the macrofauna, the foraminiferal WB assemblages seem to be influenced by a stress factor related to the WB
(i.e., not only by the burial).
4.5. Limitations of the experiment and dataset
A comparison of the three replicates per treatment showed considerable variability in foraminiferal abundance and species richness
(Fig. 1). These differences may be due to patchiness in macrofaunal
distribution within and between the mesocosms. The design of the
experiment implied that organisms that physically disturb the sediments (e.g., polychaetes) or prey on foraminifera could not escape.
Consequently, the influence the macrofauna had on the foraminiferal
distribution might have varied between mesocosms and therefore
was more pronounced than under natural conditions. On the other
hand, considerable variability among replicates are described in a
number of benthic foraminiferal studies from both shallow and
deep-sea environments (e.g. Murray and Alve, 2000; Fontanier et
al., 2003; Murray, 2003; Cornelius and Gooday, 2004), and natural
patchiness seems to be higher in stressed compared to stable environments (Warwick and Clarke, 1993; Gustafsson and Nordberg,
2000).
Even though efforts were made to spread the added sediment
evenly out over the sediment surface in the mesocosms, there is no
7
guarantee that it was distributed at a 1 mm level accuracy all over
the surfaces. Additionally, faunal activity during the experimental period probably caused some heterogeneity. Due to the small test size of
benthic foraminifera, it is reasonable to assume that they are more
influenced by possible inconsistencies in the thickness of the added
layers than the macrofauna.
The foraminiferal composition of the C samples reflect the assemblages of untreated, unfed mesocosms at the end of the experiment
i.e., they do not reflect the assemblage in the natural situation or at
time ‘0’ of the experiment. Nevertheless, some important differences
between the C and some of the TS and WB treated samples were
recorded regarding the foraminiferal abundance- and composition
patterns after sediment disturbance.
The Oslofjord, from which the sediments used in the experiment
were collected, has served as a major recipient for nutrients, organic
material and contaminants for more than a century. Consequently,
the assemblages used in the present study were already before the
onset of the experiment adapted to some degree of disturbance. Therefore, the response signal may have been stronger if the initial assemblages had consisted of more sensitive species. Owing to lack of
information about the original drilling mud composition (e.g., concentration of glycol, trace metal concentration), we can only speculate
about the agent having the strongest disturbing effect on the benthic
community.
Most of the samples were initially stored in 3% buffered formalin in
sea-water. Buffering the formalin is essential to prevent dissolution of
calcareous shells. The observed carbonate dissolution in some samples
indicates that the storage time in formalin was probably too long. We
still consider the results to be reliable because the difference in abundance of calcareous forms between formalin and ethanol samples is
trivial (78 vs 81%) and they show meaningful patterns.
5. Conclusions
The present experiment aimed to investigate which effects WaterBased drill cuttings (WB) may have on benthic foraminifera and to
compare the results with simple burial effects caused by natural Test
Sediments (TS). The burial had a severely negative effect on the benthic
foraminiferal abundance and species richness when the sediment
cover reached a thickness of 24 mm, irrespective of added material.
Of the species dominating the surface 0–1 cm (including added material), T. earlandi seems to be more resistant to maximum burial
(24 mm) than B. marginata. N. labradorica showed a negative response
to WB by changing its microhabitat, while S. fusiformis seems to be the
species most tolerant to WB. At community level, there are indications
that the WB represents an additional stress factor affecting the foraminiferal faunal composition. The latter agrees with the macrofauna
results from the same experiment (Trannum et al., 2010).
Supplementary data to this article can be found online at http://
dx.doi.org/10.1016/j.marmicro.2013.03.004.
Acknowledgments
We thank the captain and the crew of RV Trygve Braarud and the
staff at the Marine Research Station at Solbergstrand for their assistance and help during field sampling and experimental performance.
Jane K. Dolven kindly helped with sub-sampling for foraminiferal
analyses. The late Frode Olsgard initiated the project and kindly
suggested to include benthic foraminiferal studies in the mesocosm
experiment. We express our thanks to Statoil for providing the drill
cutting material. We also thank the two anonymous reviewers and
the editor, Frans Jorissen, for their constructive comments. Hilde
C. Trannum thanks the Norwegian Research Council for funding her
doctoral grant (NFR projects 17333/S40 and 164410/S40).
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S. Hess et al. / Marine Micropaleontology 101 (2013) 1–9
Appendix A. Taxonomical reference list
All foraminiferal species identified in this study are listed alphabetically. Generic classification follows Loeblich and Tappan (1987).
Original descriptions can be found in the Ellis and Messina foraminiferal species catalog (www.micropress.org).
1.1. Agglutinated species
Adercotryma wrighti Brönnimann & Whittaker 1987
Ammodiscus gullmarensis Höglund 1948
Ammoscalaria pseudospiralis (Williamson) = Proteonina pseudospiralis
Williamson 1858
Ammoscalaria tenuimargo (Brady) = Haplophragmium tenuimargo
Brady 1882
Cribrostomoides
jeffreysii
(Williamson) = Nonionina
jeffreysii
Williamson 1858
Cribrostomoides subglobosus (Sars) = Lituola subglobosa Sars 1868
Cuneata arctica (Brady) = Reophax arctica Brady 1881
Eggerella
europeum
(Christiansen) = Verneuilina
europeum
Christiansen 1958
Eggerelloides medius (Höglund) = Verneuilina media Höglund 1947
Eggerelloides scaber (Williamson) = Bulimina scabra Williamson
1858
Haplophragmoides bradyi (Robertson) = Trochammina bradyi Robertson 1891
Haplophragmoides membranaceum Höglund 1947
Hippocrepina pusilla Heron-Allen & Earland 1930
Hippocrepinella alba Heron-Allen & Earland 1932
Leptohalysis catenata (Höglund) = Reophax catenata Höglund 1947
Leptohalysis gracilis (Kiaer) = Reophax gracilis Kiaer 1900
Leptohalysis scottii (Chaster) = Reophax scottii Chaster 1892
Liebusella goesi Höglund 1947
Morulaeplecta bulbosa Höglund 1947
Psammosphaera bowmani Heron-Allen & Earland 1912
Recurvoides trochamminiforme Höglund 1947
Reophax dentaliniformis Brady 1881
Reophax fusiformis (Williamson) = Proteonina fusiformis Williamson
1858
Reophax rostrata Höglund 1947
Reophax scorpiurus Montfort 1808
Spiroplectammina biformis (Parker & Jones) = Textularia agglutinans
d'Orbigny var. biformis Parker & Jones 1865
Textularia contorta Höglund 1947
Textularia earlandi Parker 1952 = new name for Textularia tenuissima
Earland 1933
Textularia kattegatensis (Höglund) = Textularia gracillima Höglund
1947
Textularia skagerakensis Höglund 1947
Textularia bigenerinoides Lacroix 1932
Trochamminopsis quadriloba Höglund 1948 = new name for
Trochamminopsis pusilla Höglund 1947
1.2. Calcareous species
Astrononion gallowayi Loeblich & Tappan 1953
Bolivina difformis (Williamson) = Textularia variabilis Williamson
var. difformis Williamson 1858
Bolivina pseudoplicata Heron-Allen & Earland 1930
Bolivinellina pseudopunctata (Höglund) = Bolivina pseudopunctata
Höglund 1947
Brizalina spathulata (Williamson) = Textularia variabilis Williamson
var. spathulata Williamson 1858
Bulimina marginata d'Orbigny 1826
Buliminella elegantissima (d'Orbigny) = Bulimina elegantissima
d'Orbigny 1839
Cassidulina laevigata d'Orbigny 1826
Cornuloculina inconstans (Brady) = Hauerina inconstans Brady 1879
Cornuspira involvens (Reuss) = Operculina involvens Reuss 1850
Elphidium albiumbilicatum (Weiss) = Nonion pauciloculum (Cushman)
subsp. albiumbilicatum Weiss 1954
Elphidium excavatum (Terquem) = Polystomella excavata Terquem
1875
Epistominella vitrea Parker 1953
Globobulimina auriculata (Bailey) = Bulimina auriculata Bailey 1851
Hyalinea balthica (Schröter) = Nautilus balthicus Schröter 1783
Miliolinella subrotunda (Montagu) = Quinqueloculina subrotunda
Montagu 1803
Nonionella auricula Heron-Allen & Earland 1930
Nonionella turgida (Williamson) = Rotalina turgida 1858
Nonionellina labradorica (Dawson) = Nonionina labradorica Dawson
1860
Pyrgo williamsoni (Silvestri) = Biloculina williamsoni Silvestri 1923
Stainforthia fusiformis (Williamson) = Bulimina pupoides d'Orbigny
var. fusiformis Williamson 1858
Stainforthia loeblichi (Feyling-Hanssen) = Virgulina loeblichi
Feyling-Hanssen 1954
Uvigerina peregrina Cushman 1923
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