Journal of Experimental Marine Biology and Ecology 361 (2008) 49–57

Contents lists available at ScienceDirect

Journal of Experimental Marine Biology and Ecology

j ourna l homepage: www.e lsev ie r.com/ locate / jembe

Effects of drill cuttings on biogeochemical fluxes and macrobenthos ofmarine sediments

Morten Thorne Schaanning a,⁎, Hilde Cecilie Trannum a, Sigurd Øxnevad a, JoLynn Carroll b, Torgeir Bakke a

a Norwegian Institute for Water Research, Gaustadalleen 21, NO-0349 Oslob Akvaplan-niva AS, NO-9296 Tromsø, Norway

⁎ Corresponding author. Tel.: +47 99230782.E-mail address: morten.schaanning@niva.no (M.T. Sc

0022-0981/$ – see front matter © 2008 Elsevier B.V. Aldoi:10.1016/j.jembe.2008.04.014

A B S T R A C T

A R T I C L E I N F O

Article history:

Experimental work was per Received 2 July 2007Received in revised form 4 April 2008Accepted 25 April 2008

Keywords:MacrofaunaNutrient fluxOlefin-based drill cuttingsOxygen consumptionWater-based drill cuttings

formed on drill cuttings sampled from off-shore drilling operations. The cuttingscontained remnants of two different types of drilling muds: a water-ilmenite based mud and an olefin-baritebased mud. In a pilot experiment, a gradient of up to 65 mm thick layers of water-ilmenite based cuttingswere added to 78 cm2 core samples. In another set-up, 3 mm layers of water-ilmenite and olefin-barite basedcuttings were added to replicate 1000 cm2 box-core samples with natural benthic communities transferredfrom the Oslofjord, S.E. Norway. Boxes with no addition and addition of 3 mm “clean” sediment were used forcontrol. Increased consumption of oxygen and nitrate indicated the presence of degradable organic phases inboth mud systems. The release of silicate showed a general decrease with increasing thickness of the cuttingslayer, but maximum rates in the 3.1 mm treatment indicated increased bioturbation at low and moderatedoses. The initial (field) composition of the macrobenthic communities was maintained throughout the3 months experimental period, and at community level, no significant difference was observed between thefour treatments at the end of the exposure period. However, after grouping the treatments into “clean”(untreated control and 3 mm clean sediment) and “cuttings” (3 mm water-ilmenite and 3 mm olefin-baritebased cuttings), multivariate statistical analyses revealed a significant difference in community compositionbetween clean and cuttings treatments, and three taxa showed significantly reduced abundances in thecuttings treatments. Chemical toxicity of mud components is assumed to be small, and the observed effectwas more likely a result of physical properties such as the size or shape of cuttings particles.

© 2008 Elsevier B.V. All rights reserved.

1. Introduction

Drilling muds are used in large quantities by the oil and gasindustry to optimise on- and off-shore drilling operations (Neff, 2005).The mud is continuously pumped into the inner pipe of the bore holeand returns through the outer hole together with the rock cuttingsproduced by the drill bit. When drilling is performed from off-shoreplatforms, the drill cuttings are usually treated to reuse mud beforetransportation to land deposits, re-injection into seabed deposits ordischarge to the water column. When drilling is performed from sub-sea platforms, cuttings are discharged close to the bottom and henceless exposed in the water column than cuttings discharged near thesea surface (Rye et al., 2006).

Drilling muds are typically composed of a high density mineralsuch as barite or ilmenite and various additives suspended inwater oran organic phase fluid (OPF). The OPF may be petrogenic (oil-basedmud; OBM) or synthetic (synthetic-based mud; SBM). SBMs arefrequently based on esters derived from plant or fish oils or linear C14-

haanning).

l rights reserved.

C16 olefins (Schaanning and Bakke, 2006). Due to strict regulations ondischarge of OPF-contaminated cuttings (Anon, 2000), most off-shorewells are currently drilled with water based muds (WBM) (Neff,2005). In addition to heavy metal contaminants in the weightminerals, most WBMs contain approximately 20 different additives(Neff, 2005 and references therein), most of which are considered topose little or no risk (PLONOR) to the environment (Anon, 2004).

Discharges of contaminated drill cuttings (mainly OBM) have inthe past caused appreciable change of the benthos adjacent to manyoil and gas platforms in the North Sea (Davies et al., 1981; Gray et al.,1990; Kingston, 1992; Olsgard and Gray, 1995). In the most stronglyaffected areas, the fauna is of low diversity and dominated byopportunistic species. Further away from the platform, faunaldiversity may be similar to that of the surrounding area, but with adetectable difference in species composition. At some sites, thesechanges in faunal composition were detectable as far as 6000 m fromthe platform (Olsgard and Gray, 1995). A toxicity test of sedimentsfrom drill-cuttings around a platform in the North Sea concluded thathydrocarbons were the most significant cause of toxicity of thesediments contaminated with OBM cuttings (Grant and Briggs, 2002).

As with OBM, the major environmental concern with SBM isrelated to the organic phase, either by toxicity of the phase itself or its

Table 1Overview of samples and treatments in core and box-core experiments

Samplereference

WBM SBM CSED ELT MLTg wet sed. cm−2 mm

Core experimenta WBM-0 0 0 0 0.0 -WBM-0.4 0.038 0 0 0.4 1WBM-0.8 0.076 0 0 0.8 1WBM-1.5 0.152 0 0 1.5 2WBM-3.1 0.305 0 0 3.1 5WBM-6.1 0.617 0 0 6.1 10WBM-9.2 0.918 0 0 9.2 12WBM-12 1.222 0 0 12 14WBM-15 1.527 0 0 15 26WBM-23 2.292 0 0 23 26WBM-31 3.057 0 0 31 45WBM-38 3.822 0 0 38 53WBM-46 4.586 0 0 46 65

Box-core experiment F1b - - - - -F2b - - - - -C3 0 0 0 0 -C7 0 0 0 0 -C10 0 0 0 0 -S2 0 0 0.300 3.1 2–5S5 0 0 0.300 3.1 2–5S8 0 0 0.300 3.1 2–5W4 0.300 0 0 3.1 2–5W6 0.300 0 0 3.1 2–5W12 0.300 0 0 3.1 2–5O1 0 0.150 0.150 3.1 2–5O9 0 0.150 0.150 3.1 2–5O11 0 0.150 0.150 3.1 2–5

WBM = water-ilmenite based cuttings. SBM = olefin-barite based cuttings. CSED =control sediment from field location. ELT = estimated layer thickness. MLT = measuredlayer thickness.

a four replicate control cores were included in the setup.b zero samples sieved for analyses of macrofauna during sediment transfer from field

to mesocosm.

50 M.T. Schaanning et al. / Journal of Experimental Marine Biology and Ecology 361 (2008) 49–57

degradation products, or the sulphide toxicity generated duringbiodegradation by sulphate reducing bacteria in the sediments(Schaanning and Bakke, 1997). Data from around platforms whereonly SBM have been used, have indicated that the effects on thebenthic fauna are less pronounced than around platforms where OBMhas been used (Jensen et al., 1999).

Field studies on water-based mud are relatively scarce, but a fewspecially designed surveys indicate that effects are restricted to adistance of less than 100 m from the platforms (Neff, 1987; Daan andMulder, 1996; Trannum et al., 2004; Currie and Isaacs, 2005; Trannumet al., 2006). The major concern with regard to discharge of WBMappears to be the potential toxic effects from trace metal impurities inthe weight material and physical stress related to smothering anddifferent size or shape of the cuttings particles compared to the actualsediment habitat (Hyland et al., 1994; Cranford et al., 1999; Holdway,2002). Water-based muds contain low concentrations of biodegrad-able organic matter and do not support large populations of bacteria(Dow et al., 1990). Experimental work has shown that the addition ofbarite (Tagatz and Tobia, 1978) and water based mud with barite(Bakke et al., 1989) may affect species composition in marinesediments. In both studies the observed effects were concludedmost likely to result from physical factors such as altered grain sizedistribution. Hyland et al. (1994) concluded that significant reductionsin abundances of hard-bottom species in the vicinity of an off-shoredrilling operation were primarily related to physical effects ofincreased particle loading.

Thus, it appears well documented that the effects of WBM onbenthic communities are less severe than the effects from OBM andSBM. However, WBM-cuttings is by far the most common dischargefrom drilling operations and effects of WBM have been observedboth in field and experimental studies. At the same time experi-mental studies are scarce and field data from around platforms arefrequently biased from multiple anthropogenic discharges making itdifficult to establish accurate causal relationships between environ-mental factors and the effects observed. Through several experi-ments performed in the benthic mesocosm at NIVAs MarineResearch Station at Solbergstrand, a test procedure often referredto as Simulated Seabed Studies have been developed and proven tobe both sensitive and accurate with regard to prediction of the ratesof biodegradation of the organic phase and biological effects of thinlayers of cuttings contaminated with OBM or SBM (Schaanning, 1994,1995; Schaanning and Bakke, 1997, 2006; Schaanning and Rygg,2002; Schaanning et al., 1996, 1997) (all reports available at www.niva.no). The objective of this studywas to perform a similar study onthe effects of WBMs on biogeochemical fluxes and the benthicmacrofauna community.

2. Material and Methods

2.1. Outline of core- and boxcore-experiment

In the first experiment conducted in March-April 2004, variousamounts of WBM cuttings were added to 78 cm2 core samples fordetermination of sediment oxygen consumption and nutrient fluxes.Treatments are specified in Table 1. In the second experiment,conducted in August-October 2005, a constant dose (i.e. layerthickness) of WBM- and SBM-cuttings was added to 0.1 m2 box-coresamples for determination of potential effects on benthic commu-nities. Both no addition and addition of silty clay sediment from thefield location were used as controls.

2.2. Sampling and maintenance of test communities

The core samples were collected at 35 m depth in Bjørnhodebuktain the Oslofjord, S.E.Norway, using a Bowers and Connolly multicorer(10 cm diameter, 60 cm high). The box core samples were collected

08.08.05 at about 200 m depth in the Oslofjord near the mesocosmfacility using a 0.1 m2 KC-Denmark™ box corer with a transparentpolycarbonate liner. On deck, the overlying water was removedthrough a siphon to reduce erosion of the sediment surface duringtransportation and handling. Black plastic cover and ice was used toavoid direct sun-light and heating.

In themesocosm (Berge et al.,1986), inwhich all samples arrived lessthan 12 hours after retrieval from the seabed, artificial light and acontinuous supply of fjordwater from 60mdepthwas used tomaintainan experimental environment resembling the conditions at the fjordsampling locations, i.e. dim light, temperatures of 6–10 °C and salinitiesof 34–35 PSU. The head-space water was continuously exchanged withthe fjord water at constant rates of about 0.01 cm min−1 (water flow/sediment area). Stirring was performed to eliminate concentrationgradients in the water without resuspension of sediments.

2.3. Addition of test substances

WBM- and SBM-cuttings were collected from off-shore drillingoperations in the Barents and North Sea, respectively. The mud in theWBM-cuttings sample was based on the weight material ilmenite(mainly TiO2). The mud in the SBM-cuttings sample was based onbarite (mainly BaSO4) and a linear C14-C16 olefin (Schaanning, 1995;Schaanning et al., 1997) for organic phase. The clean particles were amixed batch of silty clay sediments from the top 0–30 cm layer at thefjord sampling location.

Aliquots of cuttings or particle samples (Table 1) were mixed (1:1)with seawater using a high-speed stainless steel mixer. The slurrieswere sprinkled into the head-space water and stirred gently to ensureeven sedimentation onto the sediment surface. The overlying waterwas then left undisturbed for 24 hours before restart of the water flowand wash-out of remnant suspended particles.

Fig. 1. Excess sediment oxygen consumption (treated-control) in core-experiment.Legend shows estimated thickness (mm) of wet cuttings layers.

51M.T. Schaanning et al. / Journal of Experimental Marine Biology and Ecology 361 (2008) 49–57

2.4. Fluxes of oxygen and nutrient species

Fluxes (F) of oxygen (O2) and nutrient species (SiO4 and NO3 incl.NO2) were determined from the concentration difference between theinlet water (Ci) and the headspace water (Co) in each core: F=(Ci−Co)Q/A, in which A is the sediment area in the core and Q is the flow rateof seawater through each core. The O2 difference was measured with aprecision of b0.05 mg O2 l−1 using a Clark-type oxygen electrode withan internal reference electrode. Nutrient concentrations were deter-mined in water samples drawn from the header tank and core headspace using a 50ml syringe. The syringewas rinsedwith samplewaterbefore transfer of subsamples to separate vials for each nutrient andpreserved using 1 ml 4 M H2SO4 per 100 ml sample for NO3, and 2drops of chloroform per 20 ml sample for SiO4. All samples werestored in the dark at −20°C until analyses at the NIVA-laboratory usingautomated spectrophotometric methods for nutrient analyses in seawater following the principles described in Grasshoff et al. (1985),modified in accordance with acid preservation procedure. Oxygenconsumption was measured 1–3 times per week in both experiments.Nutrient fluxes were measured on day 12, 18 and 25 in the coreexperiment, only.

2.5. Oxic layer thickness

In the box-core experiment, the oxygen saturation profile acrossthe sediment-water interface was recorded on day 8, 22 and 89using a Unisense™ Clark-type microelectrode (OX-50) with aninternal reference and a guard cathode (Revsbech, 1989). Themeasurements were performed in 10 mm (ID) core sub-samplesdrawn from each box. Readings were taken at 1 mm depth intervalsfrom 5 mm above the sediment-water interface down to zero O2.The oxic layer was taken to be the distance between zero depth andthe depth at which the interpolated oxygen saturation decreasedbelow 10%. Thus occasional long tails with near zero O2 were nottaken to be part of the oxic layer determined in this study.

2.6. Macrofauana

During field sampling at the 200 m location (08.08.05) and ontermination of the sub-sequent 3-months experiment, sedimentsfrom box core samples were washed through a sieve with 1 mm(ID) circular holes for retrieval of the macrofauna. The sieveresidues were fixed in 10% buffered formalin, and stored inappropriate containers. The macrofauna was sorted into maintaxonomic groups (mollusca, polychaeta, crustacea, echinodermataand “others”) and preserved in 75–80% ethanol. The organismswere identified to the nearest taxon possible. Biomass (g wetweight) was determined for the main taxonomic groups. Univariatemeasures included total number of taxa (S), total abundance (N),Shannon-Wiener diversity index calculated with log2 as the base,Pielou's evenness (J') and ES50, i.e. the number of species expectedfrom 50 randomly selected individuals. To analyse for similarities inthe community structure, a MDS was performed, based on Bray-Curtis similarity measure. Similarity was calculated based onfourth-root transformed data. To test for significant differences infaunal composition between treatments, an ANOSIM analysis wasperformed. The calculation of the univariate parameters and themultivariate analyses was performed with the PRIMER softwarepackage (Clarke and Gorley, 2002). ANOVA was used to test forsignificant differences between univariate parameters, incl.selected taxa, and was performed with the software package JMPversion 5.01 (SAS Institute Inc.). Prior to ANOVA, a Levene's test wasperformed to check for homogeneity of variances. When theANOVA indicated that there were significant differences withinthe dataset, Tukey's HSD test was used as a post hoc test betweenpairs of treatments.

3. Results

3.1. Visual change in core samples

Initially, the silty clay sediment appeared grey with only weakshades of different layers down the core. The sediments in controlcores and the added cuttingsmaintained their initial light, grey colour,whereas black spots developed in the sediment below the cuttings. Incores with cuttings layers of 10 mm and more, homogenous black-ening was observed from the cuttings-sediment interface down toseveral centimetres below. In marine sediments, the development ofblack spots is known to occur after natural or anthropogenic input ofdegradable organic matter as result of precipitation of ferroussulphide (FeS) produced by carbon oxidation by sulphate reducingbacteria (Fenchel and Riedl, 1970; Lyle, 1983).

3.2. Oxygen and nutrient fluxes in core experiment

In the four control samples with no addition of cuttings, theweighted average sediment oxygen consumption (SOC) for the25 days experimental period was 1.14–1.20mmolem−2 h−1. MaximumSOC was 3.6 mmole m−2 h−1 observed in WBM-23 nine days afteraddition of the cuttings. Therewas a positive correlation between SOCand cuttings layer thickness (p=0.0016, R2=0.47). In most of themoderately dosed cores (0.4–12 mm), SOC was observed to cross overfrom higher to lower than control at about day 10 day (Fig. 1). At thesame time, large peaks of SOC were observed in 4 of the 5 high dosecores with cuttings layers of 15–46 mm. This remarkable differencesuggested that doses exceeding 12–15 mm represent a critical loadeither in terms of total amount of labile carbon or layer thickness or acombination of both factors.

Nitrate was consumed in all cores and the fluxes were positivelycorrelated with SOC (FNO3=22.7+0.026.SOC, R2=0.55, pb0.0001, n=38)(Fig. 2). Silicate was released from all cores. The rate of release showed ageneral decrease with increasing layer thickness (FSiO4=−323+7.3 ELT,R2=0.17, p=0.0088, n=38), but no correlationwith SOC (p=0.83) or thefluxof NO3 (p=0.43). Anomalous high release of silicatewas observed inthe two cores treated with 1.5 and 3.1 mm layers (Fig. 2). Omitting theobservations in these two cores andone outlier value (WBM-23, day 12),

Fig. 2. Fluxes of nutrients and oxygen (µmole m−2 h−1) vs estimated thickness of cuttings layer (ELT). The lower right diagram shows a log-log plot of fluxes of NO3 vs O2. Data fromcore-experiment day 12 (open circles), day 18 (crosses) and day 25 (closed squares). Control cores are plotted at ELT=0.2 mm.

Fig. 3. Cumulative excess sediment oxygen consumption in box-core experiment. Eachpoint represent mean of three replicate boxes. W (triangles) = water-ilmenite basedcuttings. O (squares) = olefin-barite based cuttings. S (circles) = clean sediment particles.C = untreated control.

52 M.T. Schaanning et al. / Journal of Experimental Marine Biology and Ecology 361 (2008) 49–57

the flux of SiO4 was found to correlate well with the log of the layerthickness: F'SiO4=−185+36.1.Log(ELT) (R2=0.856, pb0.0001, n=32,ELT=0.1 mm assigned to control cores).

3.3. Oxygen consumption in box-core experiment

In thewater-based cuttings (W) and clean sediment (S) treatments,oxygen consumption was very similar to control boxes with noadditions (Fig. 3). Considering the low dose of 3.1 mm (ELT) applied inthis set-up, the absence of increased SOC in the WBM box cores wasconsistent with the absence of large SOC peaks in all cores with lessthan 12 mm added in the first experiment (Fig. 1).

In the olefin based cuttings (O), however, oxygen consumptionincreased after a lag phase of 2–3 weeks. Similar results have beenobserved in previous experiments and occur simultaneously with adecrease of olefin concentration in the sediment (Schaanning, 1995;Schaanning et al., 1996, 1997; Schaanning and Rygg, 2002). Based on areview of cross-test data from these experiments, a halflife of 75 dayshas been estimated for the C14-C16 olefins, when present in thin(b8 mm) cuttings layers (Schaanning and Bakke, 2006).

O2 layer thickness was less than 10 mm in all experimental boxes(Fig. 4). Diaz and Trefry (2006) observed similar O2 penetration incores collected at drilling sites in Gulf of Mexico. However, opposite toour study, they found thicker oxic layers in control cores. As shown inFig. 4, O2 penetrated deeper into the sediment during the first surveyas compared to the second and third survey. This was consistent witha concurrent decrease of O2 in the source water observed both in thefjord water, in the header tank and in the head space water in theboxes (Table 2). During all surveys the oxic layer was thinner in theolefin boxes (1.66–2.13 mm) than in the other treatments (2.26–5.83 mm). Statistical analyses (ANOVA, Tukey HSD) showed a

significant difference between water- and olefin-based cuttings, butneither water- nor olefin-based cuttings were significantly differentfrom control or clean particle treatments.

Fig. 4. Depth of oxic layer (N10% O2 saturation) determined with microelectrodes 8, 21and 89 days after treatment with water-ilmenite (W) or olefin-barite (O) based cuttingsor clean sediment particles (S). C represents control boxes with no addition of particles.Vertical bars = one standard deviation.

Table 3Number of species (S), number of individuals (N), Shannon-Wiener diversity (H'), ES50and Pielou's evenness (J') in the fjord zero samples (F, n=2) and experimental samples(C, S, W and O, n=3) 3 months after treatment ± one standard deviation

Field zero(F)

Untreatedcontrol (C)

Sedimentparticles (S)

Water-basedcuttings (W)

Olefin-basedcuttings (O)

S 19.5±0.7 21.3±8.4 19.7±3.8 15.0±8.1 18.7±8.1N 90±16 125±84 172±95 96±44 92±44H' 3.35±0.08 3.34±0.47 2.97±0.54 2.83±0.25 2.93±0.25ES50 15.5±0.7 15.0±1.7 12.7±3.8 11.7±0.6 13.3±0.6J' 0.8±0.0 0.8±0.0 0.7±0.1 0.7±0.0 0.7±0.0

53M.T. Schaanning et al. / Journal of Experimental Marine Biology and Ecology 361 (2008) 49–57

3.4. Macrofauna

In total, 63 species and 1612 individuals were recorded in thetwelve experimental and two field samples. The individual samplesranged from 13 (W2 and O2) to 31 species (O3) and from 55 (O2) to281 individuals (S3). The Shannon-Wiener diversity ranged from 2.65(S3) to 3.89 (C1), ES50 from 10 (S3 and W2) to 17 (C1 and S1) and theevenness from 0.64 (S2) to 0.80 (F1). Statistical comparison (ANOVA,Tukey HSD) of the experimental treatments (field excluded) showedno significant difference between the treatments with regard to any ofthe univariate parameters shown in Table 3 (pN0.38). Furthermore,the control samples were not statistically different from the fjordsamples with regard to the univariate parameters. Thus, no evidencewas found for any severe disturbance of the macrobenthic communitydue to transfer from sea to mesocosm and maintenance in themesocosm for the three months experiment.

The total biomass ranged from 5 to 53 g box−1 and large variationwas found within all treatments, field samples included (Fig. 5). Thesea urchin Brissopsis lyrifera made up a large part of the biomass andtogether with the bivalves, this species accounted for 74–98% of thetotal biomass. For biomass and community structure parameters(Table 3), statistical analyses (ANOVA) showed no significant differ-ence (pN0.05) between field and control samples and no significantdifference between any of the experimental groups (C, S, W, O).

Similarities in faunal structure between the samples are shown asMDS-plot in Fig. 6. ANOSIM (Analysis of Similarities) confirmed thatthere were no statistically significant differences between the varioustreatments regarding species composition (p=0.086). However, theplot revealed two interesting features. First, the fjord samples showeda large degree of similarity with the experimental samples. As for theunivariate analyses this confirmed that the experimental setup had nosignificant effects on the community composition throughout thisexperiment. Secondly, the cuttings treatments (W and O) all occur onthe right-hand side of the plot, whereas the sediment treatment,untreated control (except C3) and field samples tend to occur on the

Table 2Oxygen determined in fjord water sampled nearby the 60 m depth water inlet for theresearch station at Solbergstrand (Magnusson et al., 2006), in the mesocosm headertank and in the overlying water in control boxes

Fjord water Mesocosm water

Date 50 m 60 m 80 m Date Inlet Control box

15.08.05 7.80 7.94 7.83 15.08.05 7.95 5.6317.10.05 6.65 6.80 7.22 11.10.05 7.26 5.2712.12.05 6.56 6.64 6.70 15.11.05 6.20 4.77

Unit = mg O2 L−1.

left-hand side. A separate ANOSIM-analysis showed that the twogroups “clean” (C+S) (fjord samples excluded) vs. “cuttings”, (W+O)were significantly different (p=0.048).

Many species were present at mean densities lower than twoindividuals/box in all treatments and field samples. Disregarding theserare species, the total number was reduced from 63 to the 21 specieslisted in Table 4. Comparison of the two groups “clean” (n=6) and“cuttings” (n=6) showed a general decrease of number of individualsin cuttings treatments (Table 4). This applied to total number ofindividuals as well as to each of the five most abundant species. One-way ANOVA showed that this effect was significant for Abra nitida(p=0.006), Onchnesoma steenstrupi (p=0.019) and Nemertinea indet.(p=0.049) (Fig. 7). In addition, the number of species (S) whichremained after omitting the rare species was significantly (p=0.002)less in cuttings treatments (11.7 species) than in the clean sediment(15.3 species).

Oxygen conditions at the sediment water interface is a major factoraffecting benthic communities. Therefore, linear regression analyseswas performed on benthic diversity (H') vs oxygen consumption andoxic layer thickness, respectively. However, no significant relation-ships were found (slope pN0.05). Thus, although the oxic layerbecame thinner throughout the experiment, it did not seem to haveany measurable effect on the diversity.

Fig. 5. Biomass in field and experimental samples (g wet weight/sample). F=field zerosamples, C=untreated control, W=water-ilmenite cuttings, O=olefin-barite cuttings,S=clean sediment particles. Vertical bars = one standard deviation.

54 M.T. Schaanning et al. / Journal of Experimental Marine Biology and Ecology 361 (2008) 49–57

4. Discussion

4.1. Oxygen consumption

The characteristic sequence with two successive peaks of SOCduring the initial phase of an organic enrichment event (Fig. 1), hasbeen observed in previous experiments with biodegradable SBMs(Schaanning, 1994; Schaanning et al., 1996) and is most probably ageneral feature which reflects successive events triggered by theaddition of cuttings. The formation of black precipitates beneath, butnot within, the cuttings layer showed that the {Fe2+}{S2−} ion activityproduct in the pore water must have been lower in the cuttings layerthan in the sediment below (Berner, 1967; Wolthers et al., 2005). Thecap effect of the added cuttings may have reduced oxygen availabilityand thereby favoured a shift from oxic to anoxic degradation ofinherent organic carbon in the sediment, but both oxygen consump-tion from the overlying water and the extent of the blackening in theunderlying sediment was clearly related to the dose of cuttings added.Therefore, the precipitation was most likely driven by downwardsdiffusion of S2− produced within the cuttings layer by sulphatereducing bacteria, which utilised a source of organic carbon addedwith the cuttings. High S2− activity in the under-saturated pore waterof the cuttings layer implies a correspondingly low Fe2+ activity. Thisseemed reasonable for two reasons: 1) the set-up procedure impliesintially oxic pore waters of the cuttings layer which will favour Fe2+

oxidation to Fe3+ and precipitation of Fe(III)oxides with low solubility(Rickard, 1969) and 2) chemical analyses have shown a much lowercontent of acid-extractable iron in ilmenite than in control sedimentsfrom the Oslofjord area (Schaanning et al., 2002).

From the site of production within the cuttings layer, hydrogensulphide will diffuse not only downwards to precipitate as FeS in thesediment layer, but also upwards into the benthic boundary layerwithin which the diffusion resistance decreases rapidly (Hall et al.,1989). When this occurs, the rate of oxygen consumption will changefrom being controlled by downwards diffusion through the boundarylayer and chemical or biological consumption within the sediment, toprimarily chemical consumption within or above the boundary layer.This event is thought to have triggered the peaks of oxygenconsumption at about day 12 (Fig. 1). The high intensity and shortduration of the peaks indicated a low, but highly degradable pool ofcarbon in the water based mud. Glycol is a common additive to waterbased muds and available to degradation by anaerobic bacteria. Thusglycol may have been the organic compound which triggered theanoxic event observed in this experiment. Glycol is more water-soluble than the organic phase used in SBMs and cuttings discharged

Fig. 6. MDS-ordination of macrofauna communities, shown as a 2-D plot. F=field zerosamples, C=untreated control, W=water-ilmenite cuttings, O=olefin-barite cuttings,S=clean sediment particles.

at the sea surface may be stripped with this compound before settlingon the seabed (Rye et al., 2006).

4.2. Nutrient fluxes

Like O2, nitrate is an important electron acceptor in biological andchemical processes in the sediments. The correlation between thefluxesof O2 and NO3 (R2=0.55) and the co-occurrence of exceptionally highrates of consumption in high dose treatments on day 12 and 18 (Fig. 2)substantiates this similarity. Apparently, production of hydrogensulphide in the cuttings layer triggered rapid chemical consumption ofboth NO3 and O2 at the sediment water interface. Silicate will not reactwith sulphide and the flux of this nutrient decreased with increasingdose in treatments exceeding 3.1 mm (Fig. 2).

Silicate is released to the pore water by dissolution of silicaminerals and biogenous silica skeletons (Devol and Christensen, 1993;Hall et al., 1996) and increased efflux to the overlying water has beenpositively correlatedwith increasing number of bioturbator organismspresent in the sediment (Olsgard et al., submitted for publication). Ifsilicate is less abundant or more slowly dissolved in drill cuttings thanin fjord sediments, the release of silicate should decrease withincreasing layer thickness, merely as result of increased path ofdiffusion between the fjord sediment and the overlying water.Omitting all fluxes observed in the two cores with intermediatedoses (1.5 and 3.1 mm) and the flux on day 12 in the core treated with23 mm cuttings (i.e. 7 of 39 measurements) the correlation betweenthe silicate flux and layer thickness improved from R2=0.17 toR2=0.85. Provided that the omitted values can be reasonablyexplained, the correlation tended to confirm that the flux wasprimarily controlled by layer thickness.

When present in small cores, single individuals of large bioturbat-ing organisms may occasionally show up to provide anomalous ratesof all nutrient fluxes and a large increase of the release of silicate(Olsgard et al., submitted for publication). In the core-experiment, theaddition of cuttings may have stressed the benthic organisms both byphysical smothering and the proliferation of toxic hydrogen sulphide.How the organisms may respond to such stress is not obvious. It ispossible that at low or moderate doses, increased bioturbation isassociated with escape reactions and increased ventilation rates oftubes and burrows. Beyond a certain dose level, however, inhibition ofthese activities may occur. Thus, the decrease to normal levels of theflux of silicate in the 23 mm core after day 12 (Fig. 2), may haveresulted from the inactivation of one large (or several smaller)organism due to burial or the release of toxic hydrogen sulphide to thepore water. In the two other cores omitted from the regressionanalyses (1.5 and 3.1 mm), anomalous high rates of release of silicatepersisted throughout the experimental period. These enhanced fluxrates are difficult to explain as other than increased bioturbation andsurvival of the bioturbators throughout the experimental period. Thusthe nutrient flux observations suggest a critical layer thicknessbetween 3.1 and 6.1 mm, above which benthic community functionswere severely disturbed by decreased bioturbation and occasionalhigh rates of consumption of oxygen and nitrate by hydrogen sulphidepresent at the sediment surface.

4.3. Macrofauna

The box-core communities were dominated by the small bivalvesNucula tumidula and Thyasira equalis (Table 4). Both are subsurfacedeposit feeders. The suspension/surface deposit feeder Abra nitidawas quite abundant in field and some of the experimental samples,and the anthozoa Paraedwardsia arenaria was abundant, in particularin the experimental samples. The latter is a sessile burrower, livingmainly as a carnivore/omnivore. Of polychaetes, the tube-buildingsurface deposit feeder Melinna cristata and the subsurface depositfeeder Heteromastus filiformis were the most abundant. The large

Table 4Numbers of individuals of the most abundant (see text) species in fjord (F) and experimental (C, S, W, O) samples. The right-hand columns show mean numbers for the twoexperimental groups “clean” (=C+S) and “cuttings” (=O+W), and the probability (p) that “cuttings” were not different from “clean” (ANOVA t-test)

F1 F2 C1 C2 C3 S1 S2 S3 O1 O2 O3 W1 W2 W3 Clean Cuttings p

Nucula tumidula 26 27 52 29 14 26 57 97 34 4 36 31 45 32 45.8 30.3 0.276Thyasira equalis 10 26 39 13 28 25 26 92 18 23 45 25 24 18 37.2 25.5 0.361Paraedwardsia arenaria 0 4 13 9 2 5 4 17 3 7 9 9 10 10 8.3 8.0 0.901Abra nitida 8 9 17 5 0 8 10 12 0 0 0 0 2 0 8.7 0.3 0.006Thyasira ferruginea 5 2 10 0 0 4 7 19 1 2 0 1 6 0 6.7 1.7 0.136Thyasira pygmaea 1 3 6 5 2 4 1 3 4 2 13 0 7 0 3.5 4.3 0.711Kelliella miliaris 1 1 14 0 6 11 2 0 1 0 7 0 2 1 5.5 1.8 0.196Montacuta tenella 0 0 1 0 2 3 0 6 4 8 0 5 1 4 2.0 3.7 0.292Brissopsis lyrifera 2 2 0 1 2 1 3 12 2 2 0 2 1 1 3.2 1.3 0.344Onchnesoma steenstrupi 4 1 4 3 3 1 3 4 2 0 1 1 3 0 3.0 1.2 0.019Heteromastus filiformis 4 1 7 3 0 3 1 5 0 0 1 2 0 2 3.2 0.8 0.064Melinna cristata 0 6 6 1 1 1 1 1 0 1 1 3 5 1 1.8 1.8 1.000Yoldiella lucida 5 7 5 0 0 2 0 0 0 0 0 3 0 0 1.2 0.5 0.508Thyasira obsolete 0 2 1 0 1 0 3 8 0 1 1 2 0 0 2.2 0.7 0.273Neoleanira tetragona 0 3 6 3 0 2 0 0 3 0 0 0 0 0 1.8 0.5 0.254Nucula sulcata 0 1 0 0 1 1 1 1 0 2 5 0 0 3 0.7 1.7 0.277Eriopisa elongate 1 0 1 0 1 0 1 1 0 0 0 5 1 4 0.7 1.7 0.314Nemertinea indet 0 1 3 1 2 3 0 1 0 0 2 0 0 0 1.7 0.3 0.049Yoldiella tomlini 3 0 6 0 2 0 1 0 0 0 0 0 0 1 1.5 0.2 0.200Parvicardium minimum 1 0 9 1 0 2 0 0 0 0 0 0 0 0 2.0 0.0 0.194Nereimyra punctata 0 0 0 0 4 0 0 0 3 1 2 1 0 0 0.7 1.2 0.556Nos. species S' 13 16 18 12 15 17 15 15 11 11 12 13 12 11 15.3 11.7 0.002Nos. individuals N' 71 96 200 74 71 102 121 279 75 53 123 90 107 77 141.2 87.5 0.157

55M.T. Schaanning et al. / Journal of Experimental Marine Biology and Ecology 361 (2008) 49–57

heart urchin Brissopsis lyrifera was also represented in most boxes,mainly with 1–2 individuals. Although this species only made up avery small part of the total abundance, its size (Fig. 6) and bulldozingactivity as a non-selective subsurface deposit feeder makes it animportant structuring member of the communities in which it ispresent (Widdicombe and Austen, 1998; Widdicombe et al., 2004).

Even though no overall faunal effects were observed as a result ofthe treatments in this experiment, the ANOSIM analyses showed asignificant difference in faunal composition between the two groups“clean” (control and boxes treated with uncontaminated sediment)and “cuttings” (water- and olefin-based cuttings). The number ofspecies which remained after omitting the rare species, wassignificantly less in cuttings treatments than in the clean sediments,and so was the number of individuals of the bivalve Abra nitida, the

Fig. 7. Average abundance and one standard deviation of the bivalve Abra nitida, the sipexperimental boxes. C=untreated control, W=water-ilmenite cuttings, O=olefin-barite cuttin

sipunculid Onchnesoma steenstrupi and the nemertineas. Abra nitida isgenerally a quite tolerant species (Rygg, 2002). Based on the OLF-database (Anon, 2005) containing all benthic offshoremonitoring datafor the Norwegian sector of the North Sea since 1990, Bjørgesæter(pers. comm.) found that A. nitidawas positively correlated to severalcomponents associated with cuttings, including barium. However, inthe present experiment it clearly responded negatively to somechemical or property of the drilling mud. Onchnesoma steenstrupi livesas a surface deposit feeder, and is generally considered a sensitivespecies (Rygg, 2002). According to Bjørgesæter (pers. comm.) thisspecies is sensitive to several drill cuttings components, although notto barium. Nemertinea indet. was the third taxon which showed aresponse to the cuttings deposition. Nemertineans live as carnivores/omnivores, and the group is generally considered tolerant to

unculid Onchnesoma steenstrupi and Nemertinea indet. in field zero samples (F) andgs, S=clean sediment particles.

56 M.T. Schaanning et al. / Journal of Experimental Marine Biology and Ecology 361 (2008) 49–57

disturbances (e.g. Rygg, 2002). Based on somewhat sparse data on thisgroup Bjørgesæter (pers. com.) found that Nemertineans weresensitive towards high concentrations of barium.

The different response towards deposition of cuttings compared todeposition of clean sediment in the three “sensitive” taxa, seemed toreveal a harmful effect of some property present in both types ofcuttings. There was no indication that oxygen depletion affected thecommunities, despite the fact that the olefin-boxes gradually showeda reduced thickness of the oxygenated layer. Toxic effects of waterbased muds have not previously been reported, but there areindications that physical properties such as the shape and size ofparticles may affect proper functioning of certain organs, throughphysical interactions with gill, the gastrointestinal tract and integu-ment (Neff, 2005). Both weight materials are characterised by smallgrain size and high specific gravity. The properties of bore holecuttings themselves will depend on the local geology, but sharp edgesof machined stone are likely to represent at least one common factorof all cuttings whether they contain ilmenite, barite or water- orolefin-based muds. Barite and bentonite has been characterised astoxicologically inert (Neff, 1987). Nevertheles, Cranford et al. (1999)found that they had the potential to affect growth, reproductivesuccess and survival of sea scallops (Placopectenmagellanicus) throughphysical interactions with ciliary processes in the feeding structureand gill membranes. Similarly, Barlow and Kingston (2001) found thatbarite damaged the gill tissues of the suspension feeding bivalveCerastoderma edule and the deposit feeding bivalve Macoma balthica.Thus, it is likely that such mechanisms contributed to the responses ofthe single taxa that were observed in the present experiment.

Efforts have been made by the oil industry to develop a “zeroharmful discharge” strategy based on the assessment of Environ-mental Impact Factors (EIF) for drilling discharges (Johnsen et al.,2000). The EIF is an integrated measure of the overall probability ofdamage caused by the different stressors present in a discharge. Basedon threshold levels defined for each stressor, Smit et al. (2008) deriveda layer thickness of 6.3mm, belowwhich 95% of the species should notbe affected by burial. The nominal layer thickness in the presentexperiment was 3.1 mm, which means that one should expect lessthan 5% of the species affected by burial only. There were no signs ofeffects on the fauna in the treatment with clean sediment, which is inaccordance with the threshold level of 6.3 mm. However, as cuttingsparticles have different properties than the original sediment, e.g. theyare more sharp-edged, one may expect a lower threshold level forburial by cuttings particles than by clean sediment.

From the present experiment, it is not clear which property of themud that was responsible for the difference between cuttings andclean particles, and further documentation is needed before conclu-sions can be drawn on the actual risk. In a follow-up experiment weare currently investigating effects of different layer thicknesses ofwater-based cuttings and clean sediment, from which we hope to getmore information on threshold level for effects.

The communities were dominated by subsurface deposit feeders.Compared to other groups, this group is generally tolerant todisturbances (e.g. Pearson and Rosenberg, 1978), such as burial (e.g.Holte and Gulliksen,1998) and contamination (e.g. Gaston et al., 1998).Suspension feeders, on the other hand, which were not very abundantin the present study, have been shown to be more sensitive towardsincreased sedimentation (e.g. Hyland et al., 1994; Holte and Gulliksen,1998). This corresponds well with the finding that the bivalve Abranitida appeared to be negatively affected by cuttings deposition in thepresent experiment. Suspension feeders are generally more repre-sented at exposed habitats with coarser sediments and more particlesavailable for capture from the overlying water. New potentialexploration sites, e.g. in the Barents Sea, as well as at many of theold exploration sites in the northern North Sea, will often becharacterised by coarser sediments than those used in the presentexperiment. Future studies should also address whether such

communities are more sensitive than the communities from theOslofjord sampling site.

5. Conclusions

Increased consumption of oxygen and nitrate and formation ofblack precipitates in sediments treated with drill cuttings sampledfrom an off-shore drilling operation was related to biodegradation ofan organic phase added with thewater-basedmud used in the drillingoperation. However, the total amount of oxygen consumed by thewater-based cuttings was negligible compared to the amount ofoxygen consumed by cuttings from a different drilling operation inwhich olefin based mud had been used. Silicate fluxes indicated thatbioturbation was stimulated by addition of thin layers of water basedcuttings, but inhibited by addition of layers exceeding 3.1 mmnominalthickness.

After three months exposure in the mesocosm, the macrobenthiccommunities in control samples had maintained their high similarityto zero samples taken from the fjord. After dividing the samples intothe two groups “clean” (no addition or addition of 3.1 mm cleansediment) and “cuttings” (addition of 3.1 mm water- or olefin-basedcuttings), multivariate analyses showed a significant difference incommunity composition. In particular, three taxa (Abra nitida, Onch-nesoma steenstrupi and Nemertinea indet.) showed significantlyreduced abundances (pb0.05) in sediments treated with cuttings.The fauna did not seem to be affected by increased oxygenconsumption and reduced thickness of the oxygenated layer in thesediments treated with olefin-based cuttings. Thus the effects weremost likely related to physical properties such as shape and size ofcuttings particles. In this respect, this study has not revealed anydifference between the alternative weight materials ilmenite andbarite.

Acknowledgements

The crew on RF Tryggve Braarud and the staff at Marine ResearchStation at Solbergstrand are acknowledged for skilled assistanceduring field sampling and experimental performance. The study wasfunded by the Norwegian Research Council; PROOF project 159016/S40 and doctoral grand 164410/S40 to Hilde C. Trannum. [ST]

References

Anon, 2000. OSPAR Decision 2000/3 on the use of Organic-Phase Drilling Fluids (OPF)and the discharge of OPF-Contaminated Cuttings. http://www.ospar.org.

Anon, 2004. OSPAR List of Substances/Preparations Used and Discharged Offshorewhich Are Considered to Pose Little or No Risk to the Environment (PLONOR).Revision 2004 (Reference Number 2004-10). http://www.ospar.org.

Anon, 2005. Environmental report 2005. The Norwegian Oil Industry Association http://www.olf.no.

Bakke, T., Berge, J.A., Næs, K., Oreld, F., Reiersen, L.O., Bryne, K., 1989. Long termrecolonization and chemical change in sediments contaminated with oil based drillcuttings. In: Engelhardt, F.R., Ray, J.P., Gillam, A.H. (Eds.), Drilling Wastes. ElsevierApplied Science, pp. 521–544. 867 pp. (Proceeding of the International Conferenceon Drilling wastes, Calgary 1988).

Barlow, M.J., Kingston, P.F., 2001. Observation on the effects of barite on the gill tissues ofthe suspension feeder Cerastoderma edule (Linné) and the deposit feeder Macomabalthica (Linné). Mar. Poll. Bull. 42, 71–76.

Berge, J.A., Schaanning, M., Bakke, T., Sandøy, K.A., Skeie, G.M., Ambrose Jr., W.G., 1986. ASoft-bottom Sublittoral Mesocosm by the Oslofjord: Description, Performance andExamples of Application. Ophelia 26, 37–54.

Berner, R.A., 1967. Diagenesis of iron sulfide in recent marine sediments. In: Lauff, G.H.(Ed.), Estuaries. American Association for the Advancement of Science, pp. 268–272.

Clarke, K.R., Gorley, R.N., 2002. PRIMER v5.2. PRIMER-E Ltd., Plymouth, U.K.Cranford, P.J., Gordon Jr., D.C., Lee, K., Armsworthy, S.L., Tremblay, G.-H., 1999. Chronic

toxicity and physical disturbance effects of water- and oil-based drilling fluids andsome major constituents on adult sea scallops (Placopecten magellanicus). Mar.Environ. Res. 48, 225–256.

Currie, D.R., Isaacs, L.R., 2005. Impact of exploratory offshore drilling on benthiccommunities in the Minerva gas field, port Campbell, Australia. Mar. Environ. Res. 59,217–233.

Daan, R., Mulder, M., 1996. On the short-term and long-term impact of drilling activitiesin the Dutch sector of the North Sea. ICES J. Mar. Sci. 53, 1036–1044.

57M.T. Schaanning et al. / Journal of Experimental Marine Biology and Ecology 361 (2008) 49–57

Davies, J.M., Hardy, R., McIntyre, A.D., 1981. Environmental effects of North Sea oiloperations. Mar. Pollut. Bull. 12, 412–416.

Devol, A.H., Christensen, J.P., 1993. Benthic fluxes and nitrogen cycling in sediments ofthe continental margin of the eastern North Pacific. J. Mar. Res. 51, 345–372.

Diaz, R.J., Trefry, J.H., 2006. Comparison of sediment profile image data with profiles ofoxygen and Eh from sediment cores. J. Mar. Syst. 62, 164–172.

Dow, F.K., Davies, J.M., Raffaeli, D., 1990. The effect of drilling cuttings on amodel marinesediment system. Mar. Environ. Res. 29, 103–124.

Fenchel, T.M., Riedl, R.J., 1970. The sulfide system: a new biotic community underneaththe oxidised layer of marine sand bottoms. Mar. Biol. 7, 255–268.

Gaston, G.R., Rakocinski, C.F., Brown, S.S., Clevland, C.M., 1998. Trophic function inestuaries: response of macrobenthos to natural and contamination gradients. Mar.Freshwater Res. 49, 833–846.

Grant, A., Briggs, A.D., 2002. Toxicity of sediment from around a North Sea oil platform: aremetals or hydrocarbons responsible for ecological impacts? Mar. Environ. Res. 53,95–116.

Grasshoff, K., Erhardt, M.P., Kremling, K., 1985. Methods of seawater analysis.Gray, J., Clarke, K.R., Warwick, R.M., Hobbs, G., 1990. Detection of initial effects of

pollution on marine benthos: an example from the Ekofisk and Eldfisk oilfields,North Sea. Mar. Ecol. Progr. Ser. 66, 285–299.

Hall, P.O.J., Anderson, L.G., Vanderloefff, M.M.R., Sundby, B., Westerlund, S.F.G., 1989.Oxygen-uptake kinetics in the benthic boundary layer. Limnol. Oceanogr. 34 (4),734–746.

Hall, P.O.J., Hulth, S., Hulthe, G., Landen, A., Tengberg, A., 1996. Benthic nutrient fluxes ona basin-wide scale in the Skagerrak (North-Eastern North Sea). J. Sea Res. 35,123–137.

Holdway, D.A., 2002. The acute and chronic effects of wastes associatedwith offshore oiland gas production on temperate and tropical marine ecological processes. Mar.Pollut. Bull. 44, 185–203.

Holte, B., Gulliksen, B., 1998. Common macrofaunal dominant species in the sedimentsof some north Norwegian and Svalbard glacial fjords. Polar Biol. 19, 375–382.

Hyland, J., Hardin, D., Steinhauer, M., Coats, D., Green, R., Neff, J., 1994. EnvironmentalImpact of Offshore Oil Development on the Outer Continental Shelf and Slope offPoint Arguello, California. Mar. Environ. Res. 37, 195–229.

Jensen, T., Palerud, R., Olsgard, F., Bakke, S.M., 1999. Spredning og effekter av syntetiskeborevæsker i miljøet. (Dispersion and effects of synthetic drilling muds in theenvironment.) for the Norwegian Ministry of Petroleum and Industry. Rapport 99–3507, rev. 1. 49 pp. (In Norwegian).

Johnsen, S., Frost, T.K., Hjelsvold, M., Røe Utvik, T., 2000. The Environmental ImpactFactor-a proposed tool for produced water impact reduction, management andregulation. Society of Petroleum Engineers SPE 61178.

Kingston, P.F., 1992. Impact of offshore oil production installations on the benthos of theNorth Sea. ICES J. Mar. Sci. 49, 45–53.

Lyle, M., 1983. The brown-green color in marine sediments: a marker of the Fe(III)-Fe(II)redox boundary. Limnol. Oceanogr. 28, 1026–1033.

Magnusson, J., Andersen, T., Amundsen, R., Berge, J., Bjerkeng, B., Gjøsæter, J., Hylland, K.,Johnsen, T., Lømsland, E., Paulsen, Ø., Ruus, A., Schøyen, M., Walday, M., 2006.Overvåking av forurensningsitusjonen i indre Oslofjord 2005NIVA report 5242.102 pp.

Neff, J.M., 1987. Biological effects of drilling fluids, drilling cuttings and producedwaters. In: Boesch, D.F., Rabalais, N.N. (Eds.), Long term environmental effect ofoffshore oil and gas development. Elsevier Applied Science Publishers, London, pp.469–538.

Neff, J.M., 2005. Composition, environmental fates and biological effects of water baseddrilling muds and cuttings discharged to the marine environment: A Synthesis andAnnotated Bibliography. Battelle report to Petroleum Environmental ResearchForum (PERF) and American Petroleum Institute. 73 pp.

Olsgard, F., Gray, J.S., 1995. A comprehensive analysis of the effects of offshore oil and gasexploration and production on the benthic communities of the Norwegiancontinental shelf. Mar. Ecol. Prog. Ser. 122, 277–306.

Olsgard, F., Schaanning, M.T., Widdicombe, S., Kendall, M.A., Austen, M.C., submitted forpublication. Effects of bottom trawling on ecosystem functioning. J. Exp. Mar. Biol.Ecol.

Pearson, T., Rosenberg, R., 1978. Macrobenthic succession in relation to organicenrichment and pollution of the marine environment. Oceanogr. Mar. Biol. Ann.Rev. 16, 229–311.

Revsbech, N.P., 1989. An oxygen microelectrode with a guard cathode. Limnol.Oceanogr. 34, 472–476.

Rickard, D.T., 1969. The chemistry of iron sulfide formation at low temperatures.Stockholm Contribution Geol. 20, 67–95.

Rye, H., Reed, M., Durgut, I., Ditlevsen, M.K., 2006. Documentation report for the revisedDREAM model ERMS Report No. 18. ISBN 82-14-03769-7. 85 pp.

Rygg, B., 2002. Indicator species index for assessing benthic ecological quality in marinewaters of Norway NIVA report 4548-2002. ISBN 82-577-4202-3. 22 pp.+appendix.

Schaanning, M.T., 1994. Test on Degradation of AQUAMUL BII Drill Mud on Cuttingsunder Simulated Seabed Conditions NIVA report 3092. 81 pp.

Schaanning, M.,1995. Biodegradation of Ultidril Base Fluid and Drilling Mud on CuttingsDeposited in Benthic Chambers NIVA report 3321. 64 pp+appendix.

Schaanning, M., Bakke, T., 1997. Environmental fate of drill cuttings in mesocosm andfield. SEBA, UK National Workshop on Drilling Fluids, Aberdeen 11–14.November1997 WDF97/3/6, 10 pp.

Schaanning, M., Bakke, T., 2006. Remediation of sediments contaminated with drillcuttings-A review of field monitoring and experimental data for validation of theERMS sediment module NIVA report 5188. 36 pp.

Schaanning, M., Hylland, K., Lichtenthaler, R., Rygg, B., 1996. Biodegradation of AncoGreen and Novaplus Drilling Muds on Cuttings Deposited in Benthic ChambersNIVA report 3475. 77pp + appendix.

Schaanning, M., Lichtenthaler, R., Rygg, B., 1997. Biodegradation of Esters and Olefins inDrilling Mud Deposited on Arctic Soft-bottom Communities in a Low-temperatureMesocosm NIVA report 3760. 57pp+appendix.

Schaanning, M.T., Ruus, A., Bakke, T., Hylland, K., Olsgard, F., 2002. Bioavailability ofmetals in weight materials for drilling muds NIVA report 4597, 36 pp.

Schaanning, M.T., Rygg, B., 2002. Environmental benefits of drilling muds based oncalcium nitrate? NIVA report 4735. 51 pp.

Smit, M.G.D., Holthaus, K.I.E., Trannum, H.C., Neff, J.M., Kjeilen-Eilertsen, G., Jak, R.G.,Singsaas, I., Huijbregts, M.A.J., Hendriks, A.J., 2008. Species sensitivity distributionsfor suspended clays, burial and grain size change in the marine environment.Environ. Toxicol. Chem. 27, 1006–1012.

Tagatz, M.E., Tobia, M., 1978. Effect of Barite (BaSO4) on Development of EstuarineCommunities. Est. Cstl. Mar. Sci. 7, 401–407.

Trannum, H.C., Pettersen, A., Oug, E., Bjørnbom, E., 2004. Environmental surveyaround well 7122/7-1 and well 7122/7-2 at Goliat Akvaplan-niva report 411.2803.62 pp.+ appendix.

Trannum, H.C., Pettersen, A., Brakstad, F., 2006. Field trial at Sleipner Vest Alfa Nord:Effects of drilling activities on benthic communities ERMS report no. 16. Akvaplan-niva report 411.3041. 49 pp.+appendix.

Widdicombe, S., Austen, M.C., 1998. Experimental evidence for the role of Brissopsislyrifera (Forbes, 1841) as a critical species in the maintenance of benthic diversityand the modification of sediment chemistry. J. Exp. Mar. Biol. Ecol. 228, 241–255.

Widdicombe, S., Austen, M.C., Kendall, M.A., Olsgard, F., Schaanning, M.T., Dashfield, S.L.,Needham, H.R., 2004. Importance of bioturbators for biodiversity maintenance:indirect effects of fishing disturbance. Mar. Ecol. Prog. Ser. 275, 1–10.

Wolthers, M., Charlet, L., Linde, P.R.v.D., Rickard, D., Weijden, C.H.v.D., 2005. Surfacechemistry of disordered mackinawite (FeS). Geochim. Cosmochim. Acta 69 (14),3469–3481.