Comparison of benthic foraminifera and macrofaunal indicators of the impact of oil-based drill mud disposal

Marine Pollution Bulletin 60 (2010) 2007–2021

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Marine Pollution Bulletin journal homepage: www.elsevier.com/locate/marpolbul

Comparison of benthic foraminifera and macrofaunal indicators of the impact of oil-based drill mud disposal Mariéva Denoyelle a,b,c,⇑, Frans J. Jorissen a,b, Daniel Martin d, François Galgani e, Jacques Miné c a

Laboratory of Recent and Fossil Bio-Indicators, UPRES EA 2644 BIAF, Angers University, 2 Bd Lavoisier, 49045 Angers, France LEBIM, Ile d’Yeu, France c TOTAL S.A., DGEP/HSE-ENV, 2 place Jean Millier, 92078 Paris la Défense Cedex, France d Centre d’Estudis Avançats de Blanes (CEAB–CSIC), Carrer d’accés a la Cala Sant Francesc 14, 17300 Blanes (Girona), Catalunya, Spain e IFREMER Corse, Imm Agostini, ZI Furiani, 20600 Bastia, France b

a r t i c l e Keywords: Bio-indicators Biotic index Drilling mud Foraminifera Macrofauna

i n f o

a b s t r a c t We compare foraminifera and macrofauna as bio-indicators of oil-based drill mud disposal site off Congo. The most polluted sites are characterized by poor faunas, dominated by some very tolerant taxa. Slightly further from the disposal site, there is an area with strongly increased densities, heavily dominated by opportunistic taxa. Still further, macrofauna appears to be similar to that at the reference area, but the foraminiferal meiofauna still suggests a slight environmental perturbation. The foraminiferal FIEI index, based on the species distribution in the study area, appears to be more discriminative than the macrofaunal ITI index, based on a priori definitions of the trophic guilds of the various taxa. Our comparative approach allows us to point out the benefits of (1) the use of macrofauna and foraminifera together and (2) the definition of the species groups used in biotic indices on the basis of observations made directly in the study area. Ó 2010 Elsevier Ltd. All rights reserved.

1. Introduction Offshore oil drilling activities may cause environmental perturbation on the sea floor, due to the construction of platforms, to accidental oil spills, or to the disposal of drill cuttings with associated oil- or water-based drill mud. The process of drilling for oil and gas produces a large quantity of cuttings, rock fragments surrounded by drilling fluids. These drilling fluids are necessary to lubricate the drilling bit, to maintain the pressure of the well, and to transport the cuttings upward, to the platform. Once on the platform, the cuttings are treated with special devices (shale shakers, centrifugation, etc.) aiming to separate the cuttings from the surrounding drilling mud, which is recovered and, as much as possible used again. Next, in accordance with the local regulations, the cuttings are discharged into the sea, reinjected in the well or recycled on land (Dalmazzone et al., 2004). Different bio-indicators are used to assess the impact of drill cutting disposal on the organisms inhabiting the sea floor ecosystems. These bio-indicators do not reveal the presence or impact

⇑ Corresponding author at: Address: BIAF, Université d’Angers, Laboratoire de Géologie, 2 Bd Lavoisier, 49045 Angers, France. Tel.: +33 2 41 73 54 08; fax: +33 2 41 73 53 52. E-mail addresses: [email protected] (M. Denoyelle), frans. [email protected] (F.J. Jorissen), [email protected] (D. Martin), francois.galgani @ifremer.fr (F. Galgani), [email protected] (J. Min&eacu. 0025-326X/$ - see front matter Ó 2010 Elsevier Ltd. All rights reserved. doi:10.1016/j.marpolbul.2010.07.024

of specific pollutants, but rather give an integrated picture of the impact of all pollutants and physical disturbance on the ecosystem. They can be used to describe the geographical extent and the severity of environmental impact, and to track ecosystem recovery after cessation of drilling activities. Usually, benthic macrofauna and/or meiofauna are used to monitor drill mud disposal (e.g. Davies et al., 1984; Dicks et al., 1988; Gray et al., 1990; Daan et al., 1994; Olsgard and Gray, 1995; Shimmield et al., 2000; Gage, 2001; Grant and Briggs, 2002; Borja et al., 2003; Breuer et al., 2004; Dalmazzone et al., 2004; Durrieu and Bouzet, 2004; Muxika et al., 2005; Durrieu et al., 2006; Gass and Roberts, 2006; Flaten et al., 2007; Olsen et al., 2007). Macrofaunal and meiofaunal patterns around oil drilling platforms resemble those found around other point sources of pollution (Dalmazzone et al., 2004; Parr et al., 2007; Schaanning et al., 2008; Venturini et al., 2008). Generally, a very typical succession of tolerant, opportunistic and sensitive species mirrors the pollution gradient. In cases of severe pollution, the most impacted area may even be devoid of benthic life. Less severely polluted areas are dominated by a small number of tolerant and/or opportunistic taxa, often with high densities. Farther away from the source of pollution, these indicator taxa tend to become less prominent, being gradually replaced by intermediate and sensitive species (Pearson, 1985; Pearson and Rosenberg, 1978; Warwick, 1986; Weston, 1990). Benthic foraminifera were first applied to assess the impact of oil exploration activities on the sea floor by Locklin and Maddocks

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(1982). More recently, a monitoring method based on foraminiferal meiofauna has been tested in continental shelf and slope environments off Africa (Durrieu et al., 2006; Mojtahid et al., 2006; Jorissen et al., 2009). For several reasons, benthic foraminifera are particularly useful for environmental monitoring. They occur in all marine environments, and have much higher densities than macrofauna, from tens up to several thousands of ind/10 cm3 (Murray, 2006). These high densities allow producing large quantitative data with only small sediment volumes. Furthermore, foraminiferal diversity is almost comparable to that of the entire macrofauna; with up to hundred different species occurring at a single site (Murray, 2006). Because of their high diversity, and the fact that they occupy a wide range of ecological niches (Murray, 2006), foraminifera potentially offer a large range of indicator species. Finally, many foraminiferal species are protected by calcareous shells, which are preserved in the sediment after the death of the organism. The study of the assemblage of dead foraminiferal shells at some centimeters depth in the sediment can therefore inform us about the composition of the foraminiferal meiofauna which lived in the area before the start of oil production activities. Lacking baseline studies, this particular feature represent a major advantage with respect to macrofauna. Although their use to assess the impact of oil production activities is relatively new, foraminifera have been used for several decades as bio-indicators of other types of anthropogenic impact, mainly in coastal areas (e.g. Watkins, 1961; Seiglie, 1968, 1971; Setty, 1976; Rao and Rao, 1979; Schafer, 1982; Setty and Nigam, 1984; Bhalla and Nigam, 1986; Nagy and Alve, 1987; Schafer et al., 1991; Alve, 1995; Coccioni, 2000; Bergin et al., 2006). Their response to various toxic substances has been tested, such as Trin-Butyltin (Gustafson et al., 2000), heavy metals (de Nooijer et al., 2007; Le Cadre et al., 2003; Saraswat et al., 2004) and oil (Ernst et al., 2006). These studies suggest that foraminifera are suitable for monitoring open marine environments, but do not prove whether they are as sensitive to pollution as macrofauna. Therefore, it is not yet clear whether foraminifera have the same reliability as environmental perturbation indicators as the more commonly used macrofauna. To our knowledge, there is a single study comparing the use of foraminifera and macrofauna as pollution indicators in open marine environments. This study focused on the distribution of both groups around a sewage sludge disposal site at 80 m depth in the Firth of Clyde, off Western Scotland (Mojtahid et al., 2008). Very comparable patterns were found for both groups, with poor macrofauna and foraminiferal assemblages just at the disposal site, surrounded by an aureole of opportunistic species, which tended to disappear farther away. At about 3 km from the disposal site, faunas were comparable to those found at the reference station. However, some minor differences existed, with foraminifera appearing to be more impacted at the disposal site, and still showing a slight environmental impact at the outer edge of the studied area, where the macrofauna was already similar to that at the reference station. Such a comparable study between foraminifera and macrofauna has never been made for the impact of oil drill mud. Therefore, in this paper, we compare the results of two monitoring studies of the same drill mud disposal site off Congo, one based on the macrofauna, and one on benthic foraminifera. We have investigated whether both groups respond in the same way to drill mud disposal, and whether their distributional patterns are comparable. This allowed us to compare the relative extent of environmental impact, as indicated by the two methods, and to detect potential differences in sensitivity. The results of our comparative study will reveal whether foraminifera are as adequate as bio-indicators of drill mud disposal as macrofauna, and will inform us whether either of the two groups can be used independently, or whether there is a bonus in studying both groups together.

2. Materials and methods 2.1. Study area The study area is located in the vicinity of two operating offshore oil platforms off Congo, at a water depth of about 180 m (Fig. 1). Oil production was active from November 1993 to April 1999. Mostly oil-based drilling mud was used, and the treated cuttings were directly discharged in sea, to accumulate at the sea floor. After the cessation of oil drilling activities in 1999, the benthic macrofauna was sampled in November 2000 (11 stations), March 2002 (7 stations) and April 2003 (7 stations), with four samples in common for the three surveys (Table 1). In April 2003, six stations of the 2002 macrofauna survey, from 70 to 2 km of the disposal site, were revisited to study the foraminiferal meiofauna, together with a seventh station at 450 m WNW of the drilling platform. Since bottom and surface currents both have a NNWSSE direction, the sampling stations were predominantly chosen South of the platform. In this study, we compared the standing stocks, diversity and biotic indices of the 2003 foraminiferal survey with the 2000, 2002 and 2003 macrofaunal data. Comparisons of individual taxa were limited to the 2003 survey, when the same samples were studied for both groups. 2.2. Sample collection Sediment samples were collected with a Van Veen grab (surface area 0.1 m2). An aliquot of the upper cm of each station was used for grain size analysis, as well as for water quality analysis and, total organic matter and organic carbon contents, total nitrogen and phosphorous, total hydrocarbons, and several heavy metals contents (Cd, Pb, Hg, Al, Ba). The methods and results of these analyses are presented in Dalmazzone et al. (2004). Three replicate grab samples were used for macrofaunal analyses (0.1 m2, 15 cm deep) On board, each sample was gently mixed in a barrel with seawater until a homogeneous mixture was obtained, which was sieved through a 1 mm mesh size stainless steel sieve. The sieve residues (>1 mm) were transferred into hermetic plastic bags, fixed with a solution of buffered formaldehyde and stained with Rose Bengal. In the laboratory, all macrofaunal organisms were identified at the lowest possible taxonomic level to determine the species richness (number of species per station). 2.3. Faunal analyses and comparisons After counting all specimens, densities were calculated for all species, which were expressed as ind/m2 (averaging the three replicates of each station). The Shannon diversity index (Shannon, 1948) was estimated for all sampling stations, using the expression:

H0 ¼ 

S X ni ni log2 N N i¼1

ð1Þ

where S is the number of species, N the total number of individuals and ni the number of individuals for each species. The H0 result is given as a numerical value between 0 and 5 bits (Frontier, 1983). It is minimal if the individuals mainly belong to a single species and maximal if the individuals are equally distributed among many species. The taxa have been divided into four trophic groups according to Word (1979):  Group 1: suspension feeders, feeding in the water column,  Group 2: deposit feeders, feeding at the sediment–water interface,  Group 3: surface deposit feeders, foraging in the oxic upper part of the sediment, and

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Fig. 1. Geographical location of the study site and map of the oil field, the two platforms and the 12 sampling stations used in this study.

Table 1 Geographical position with respect to the discharge point of the 12 sampled stations. Station

10 9 17 8 7 6 13 5 4 3 16 2

Position with respect to the discharge point

Macrofauna 2000

2 km N 500 m WNW 450 m WNW 300 m WNW 150 m WNW 70 m W 100 m S 175 m SSE 230 m S 470 m S 730 m SSE 2 km SSE

X X

Macrofauna 2002

Macrofauna and Foraminifera 2003

The overall assessment of the state of the environment, expressed as a function of the macrofaunal response to organic matter enrichment, is given by the Infaunal Trophic Index (ITI, Word, 1979):

 ITI ¼ 100 

X X X X X X X X

X X

X X

X X X X

X X X X

 Group 4: subsurface deposit feeders, foraging in deeper sediment layers, often in dysaerobic ecosystems.

33; 33ð0n1 þ 1n2 þ 2n3 þ 3n4 Þ n1 þ n2 þ n3 þ n4

 ð2Þ

where n1, n2, n3, n4 are the relative densities of the four trophic groups. ITI has been successfully used in previous ecological studies (e.g. Word, 1979, 1980; Maurer et al., 1999; Grall and Hily, 2003), and has later been formalized by Bascom et al. (1979), who distinguished three ITI intervals to define various degrees of disturbance: ITI > 60: normal faunas typical of non organically enriched sediments, 30 > ITI > 60: faunas typical of sediments moderately enriched in organic matter, ITI < 30: faunas typical of severely organically enriched areas. The foraminiferal meiofauna was studied in subsamples from the Van Veen grabs, taken with a Plexiglas core (4 cm inner diam-

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eter, surface area 12.56 cm2). Each core was sliced into 0.5 cm layers down to 1 cm and then in 1 cm layers down to 3 cm depth. All layers were immediately packed in sealed plastic bags with 95% Ethanol with 1 g/L Rose Bengal. About one month later, the sediment samples were sieved over 63 and 150 lm meshes in the laboratory. Living foraminifera from the >150 lm fraction were sampled down to 3 cm depth; the 63–150 lm fraction was studied in the upper 2 cm. Foraminifera from the >150 lm fraction of the surface (0–0.5 cm) and 2–3 cm level were sorted out wet (in 50% ethanol), without preliminary treatment. Those from the 0.5–1 and 1–2 cm layers, as well as all samples of the 63–150 lm fraction, were separated by density using trichloroethylene (D = 1.46), in order to distinguish them from the numerous sediment grains, and so to accelerate picking. Living (Rose-Bengal stained) foraminifera were then picked from the floating portion, while the deposited sediment was checked for the absence of live individuals. All foraminifera were determined at the lowest possible taxonomic level, using common taxonomic references, and their densities were expressed as ind/10 cm2. To allow a comparison with the ITI, the Foraminiferal Index of Environmental Impact (FIEI, Mojtahid et al., 2006) was calculated and defined as the cumulative percentage of all pollution-tolerant and/or opportunistic taxa. Species were defined as ‘‘opportunistic” or ‘‘pollution-tolerant” on the basis of their distribution patterns in the study area, and comparison of the living foraminiferal meiofauna with the subfossil foraminiferal meiofauna found in the 2–3 cm sediment layer, which is for the more distal stations considered to represent pre-impacted conditions. Only species that show a clear trend of increased densities from the reference station to the discharge site were considered as opportunistic and/or pollution-tolerant. Their maximum density was generally not found at the station closest to the discharge site, but slightly farther away. The various opportunistic taxa did not all have their maximal density at the same station. Species that did not show a density decrease from the reference site towards the discharge site have been considered as pollution-tolerant. A comparison of living and subfossil foraminiferal meiofauna was used to confirm the selection of tolerant/opportunistic taxa. At the stations close to the disposal site, such tolerant/opportunistic taxa have a higher relative abundance in the living than in the subfossil foraminiferal meiofauna. See Mojtahid

et al. (2006) for more detailed information on the selection of foraminiferal indicator species. In order to compare macrofauna and foraminifera, the FIEI procedure was also applied to the macrofaunal datasets. Unfortunately, for macrofauna, it is impossible to compare recent and dead faunas. Therefore, our selection of opportunistic and/or tolerant macrofaunal indicator species was exclusively based on the observed spatial patterns. 3. Results 3.1. Geochemical data In 2000, 2002 and 2003, the hydrocarbon concentrations around the disposal site showed similar patterns (Fig. 2). A conspicuous maximum at station 6, 70 m W of the disposal site, was higher in 2000 (170 g/kg dry weight) than in 2002 and 2003 (65 and 110 g/kg, respectively, see Dalmazzone et al., 2004; Durrieu and Bouzet, 2004). Away from the disposal site, hydrocarbon concentrations rapidly decreased, until only trace amounts were detectable at 500 m distance. Maximum barium concentrations (150 g/kg dw in 2000 and 2002; 95 g/kg dw in 2003) occurred also at 70 m W of the disposal site, with values decreasing rapidly, until becoming insignificant at 500 m (Dalmazzone et al., 2004; Durrieu and Bouzet, 2004). 3.2. Macrofauna: density and diversity patterns, ITI With the exception of some minor differences, the macrofauna showed similar trends in the three surveys, allowing to present all them together (Fig. 3A–C). In 2003, the macrofaunal density (an average of three samples studied for each station) ranged from 100 to 250 ind/m2 from 2 km to 500 m from the discharge point (Fig. 3A). From 500 m towards the platform, the macrofaunal density strongly increased to maximum values of 8600 ind/m2 100 m S, and 5000 ind/m2 70 m W of the disposal site. In 2002, the macrofaunal density showed the same pattern with about 500 ind/m2 from 2 km to 500 m, followed by a progressive increase to a maximum of 6800 ind/m2 100 m S of the platform.

Fig. 2. Distribution of total hydrocarbon and barium contents in the sediment (g/kg dry weight) as a function of the distance from the discharge point in 2000, 2002 and 2003 (after Dalmazzone et al., 2004; Durrieu and Bouzet, 2004).

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Fig. 3. Distribution of macrofaunal assemblage descriptors as a function of the distance from the discharge point. (A) Total density (ind/m2). (B) Species richness (number of species per sample). (C) ITI (%).

At station 6, 70 m W, the density was somewhat lower than in 2003 (2300 ind/m2). In 2000, about 300 ind/m2 were found between 500 and 2 km from the platform and there were a maximum of 3000 ind/m2 at station 5 (175 m SSE of the platform), which was less prominent than in 2003 and 2002. In 2003, species richness ranged from 20 to 40 between 2 km and 250 m (Fig. 3B.), decreasing until a minimum of 20 species 70 m W of the disposal site. In 2002, species richness was generally higher, but the pattern was similar, with 45–60 species between 2 km and 250 m, decreasing until a minimum of 15 species 70 m W of the discharge point. In 2000, the pattern was the same, but species richness was generally lower, with about 40 species at 2 km SSW of the platform, there was a gradual decrease towards the disposal site. NNW of the platform, on the contrary, species richness remained elevated until station 8, at 500 m, where a maximum of 45 species was observed. Closer to the disposal site, spe-

cies richness decreased rapidly to a minimum of only 15 species 70 m W (station 6). In turn, the diversity showed a similar pattern for the three years (Fig. 4). Maxima of 4.1–5.0 bits were observed between 2 km and 380 m. In 2002 and 2003, a clear minimum, of about 0.5 bits was found 70 m W of the discharge point. In 2000, minima of about 1.8 bits were found at 70 m W and 175 m SSE. Also ITI showed very similar patterns in the three surveys (Fig. 3C). In 2003, ITI ranged from 55% to 60% between 2 km and 500 m, decreasing until a minimum of 5% at 70 m W. At station 17, about 450 m WNW of the platform, the ITI was about 35%. In 2002, the ITI was about 60% from 2 km to 500 m of the discharge point, rapidly decreasing to a minimum of only 3% at 70 m W. In 2000, minima of 7% and 8% were observed 70 m W and 175 m SSE, respectively. Farther SSE, ITI values were almost identical to those of 2002. To the NNW, the ITI varied between 60% and 70% at distances larger than 150 m from the disposal site.

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Fig. 4. Distribution of the diversity for macrofauna (2000, 2002 and 2003) and foraminifera (2003) as a function of the distance from the discharge point.

Fig. 5. Distribution of foraminiferal assemblage descriptors as a function of the distance from the discharge point. (A) Density of living benthic foraminifera (ind/10 cm2). (B) Species richness (number of species per sample). (C) FIEI (%).

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3.3. Foraminifera: Density and species richness patterns, FIEI Foraminiferal meiofauna was only sampled in 2003. A detailed description of the data is given by Mojtahid et al. (2006). In Fig. 5A, the foraminiferal data are presented separately for the two investigated size fractions: all data for the >150 lm fraction are based on an inventory of the topmost 3 cm, whereas the data for the 63–150 lm fraction pertain to the topmost 2 cm. The foraminiferal densities showed a marked spatial pattern (Fig. 5A). Between 2 km and 500 m, they varied from 5 to 30 ind/10 cm2 (>150 lm fraction) and from 25 to 40 ind/10 cm2 (63–150 lm fraction). From 500 m to the disposal point, densities increased until reaching a maximum at 230 m South (170 and 250 ind/10 cm2 in the >150 lm and 63–150 lm fractions, respectively). Still closer to the platform, densities decreased until 15 and 60 ind/10 cm2 70 m W. Also, at station 17 (450 m NNW of the discharge site), the foraminiferal assemblages were poor, with 10 and 20 ind/ 10cm2 in the >150 lm and 63–150 lm fraction, respectively. The species richness showed a rather irregular pattern (Fig. 5B). SSE of the disposal site, the species number increased from five for each of the two fractions at 2 km, to maxima of 30 (>150 lm) and 25 (63–150 lm) at 230 m. However, this trend was interrupted by a minimum at 470 m S. At 500 m NNW, species richness was only 9 (>150 lm) and 1 (63–150 lm). Also, at the two stations closest to the disposal site, species richness was fairly low (9 and 12 for >150 lm and five and 16 for 63–150 lm, at 70 m W and 100 m S, respectively). In turn, the diversity ranged between 2.0 and 3.0 bits, without showing a clear tendency (Fig. 4). The FIEI, which were exclusively based on an inventory of the >150 lm fraction (Fig. 5C), showed an increase from a minimum of 15% at 2 km to a maximum of 85% 100 m South of the platform. To the NNW, the FIEI decreased again until reaching 50% at 450 m. 3.4. Macrofaunal and foraminiferal indicator species Eighteen macrofaunal indicator species have been selected according to their sensitivity/tolerance to environmental stress due to oil-based drill mud disposal. Among them, there were 15 annelid polychaetes, two bivalves and one nemertean. Since we only have foraminiferal data for 2003, we will base our comparison of macrofaunal and foraminiferal patterns mainly on the 2003 data set (Fig. 6). Sigambra sp. (polychaete) and Capitella sp. (polychaete) were dominant around the disposal site, the former reaching maximal densities of about 4500 ind/m2 at 70 m W, the latter reaching a maximum of about 3500 ind/m2 at 100 m S of the disposal site, decreasing to 600 ind/m2 at 250 SSE. The densities of both taxa drastically decreased farther away from the disposal site, with only a few specimens remaining at 500 m, and being totally absent from all more distant stations. In spite of the different absolute densities, the overall patterns were very similar in 2003, 2002 and 2000 (Fig. 7). Four other taxa, Ampharetidae genus A (polychaete), Anodontia cf. edentula (bivalve), Loripes cf. contrarius (bivalve) and Paramphinome cf. tryonix (polychaete) showed high densities at 100 m and 230 m S. The first three all had a clear maximum of 500–600 ind/ m2, at 100 m, while at 230 m their densities were significantly lower, with about 400 ind/m2 for A. edentula and 150–200 ind/m2 for Ampharetidae genus A and L. cf. contrarius. P. cf. tryonix showed similar densities, but a slightly different pattern, with about 500 ind/m2 at 100 m and a maximum of about 650 ind/m2 at 230 m S. Farther away from the discharge point, there was a rapid density decrease to a near absence at 470 SSE. Glycera sp. 1 (polychaete), Prionospio cf. multibranchiata (polychaete) and Spiophanes sp. (polychaete) were less numerous, and their maximum densities occurred at 230 m S (70, 140 and

Fig. 6. Distribution of the average densities of the 18 macrofaunal indicator species (ind/m2) as a function of the distance from the discharge point in 2003.

25 ind/m2, respectively). At 100 m S, Glycera sp. 1 (120 ind/m2) and Spiophanes sp. (20 ind/m2) had still fairly high densities, whereas P. cf. multibranchiata was almost absent. All three species showed a rapid density decrease towards the stations at 470 m SSE and 60 m W. Spiochaetopterus sp. (polychaete), Monticellina dorsobranchialis (polychaete) and Marphysa sp. (polychaete) had lower densities,

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Fig. 7. Average densities of the indicator species Sigambra sp. (A) and Capitella sp. (B) (ind/ m2) at the 12 stations sampled in 2000, 2002 and 2003.

but showed a similar pattern, with maxima of 15–25 ind/m2 at 470 m SSE. They were all absent at less than 250 m from the disposal site. To the NNW, they re-appeared at 500 m, with densities of about 10 ind/m2. Aphelochaeta sp. (polychaete), Anobothrus gracilis (polychaete) and an unidentified Nemertean (referred to as sp. 1) reached all maxima of 10–40 ind/m2 at 730 m SSE and 500 m NNW. They tended to disappear farther away from the platform, with only A. gracilis being present at 2 km SSE. Except for a punctual presence of Aphelochaeta sp. at 230 m S, these three taxa were absent at all stations closer to the disposal point. Aricidea assimilis (polychaete), Sternaspis scutata (polychaete) and Cossura cf. coasta (polychaete) reached maxima of about 10 ind/m2) at 2 km SSE. They were all rare closer to the platform, but A. assimilis re-appeared at 500 m NNW. In the case of foraminifera, 13 indicator taxa have been selected (Figs. 8 and 9). In the 150 lm fraction, Bulimina marginata, Bulimina costata, Trifarina bradyi and Uvigerina peregrina all had maximum densities at 100 m S, ranging from 20 ind/10 cm2 for B. marginata to 10–15 ind/10 cm2 for the other three species. Their densities progressively decreased farther away, although U. peregrina was still present in fair numbers at 730 m SSE. Bulimina aculeata and Textularia sagittula attained maximum densities (of 25 and 7 ind/10 cm2, respectively) at 230 m S, and were still present 100 m S of the platform. With increasing distance, their densities rapidly decreased. Also Amphicoryna scalaris and Eggerella sp. 1 both had a maximum density, of about 35 ind/10 cm2, at 230 m S. This was the only station where these taxa appeared with significant numbers. In the 63–150 lm fraction, Valvulineria bradyana and Bolivina dilatata showed maxima of about 5 ind/10 cm2 at 100 m S.

Farther away, their densities rapidly decreased in all directions. B. marginata and Gyroidina sp. 1 showed maxima at 230 and 100 m S, of about 35 and 25 ind/10 cm2, respectively. Both species were present with about 10 ind/10cm2 at 70 m W, and decreased very rapidly towards all more distanced stations. Finally, Bolivina striatula, Bolivina seminuda and B. aculeata showed conspicuous maxima at 230 m S (about 70, 25 and 20 ind/10 cm2, respectively), and minimal densities at all other stations. 4. Discussion 4.1. Sediment chemistry The benthic environment around the investigated oil platforms was modified by the disposal of oily drill cuttings, which finished in 1999, 1 year before the start of the benthic surveys discussed in this paper. The spatial distribution of hydrocarbon concentrations suggests that environmental perturbation was maximal 70 m W of the platform, where a maximum hydrocarbon concentration (of about 160 g/kg) was observed. Oily drill cuttings usually contain large quantities of barium, a relatively inert, non-toxic metal in marine environments often used as a tracer of the dispersion of drill cuttings on the sea floor (Chow, 1976; Zemel, 1995; Kennicutt et al., 2006). At our study area, barium concentrations indicated the presence of drill cuttings until 230 m S of the platform. Both hydrocarbons and barium concentrations fall to zero at about 500 m from the platform, suggesting the absence of drill cuttings. In the affected area, the presence of an important quantity of hydrocarbon likely caused a strong increase in oxygen demand at the sediment–water interface and in the uppermost sediment layer, as a consequence of the aerobic degradation of the oil components. Unfortunately, no oxygen measurements were performed during

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the sampling surveys, but negative sediment redox potentials until 500 m distance indicate the presence of hypoxic conditions (Dalmazzone et al., 2004). Therefore, the benthic environment in the most affected area was probably subject to eutrophication phenomena comparable to those observed in areas impacted by waste disposals (e.g. Parr et al., 2007; Schaanning et al., 2008; Venturini et al., 2008). Since the oily drill mud used in the study area has a low toxicity, toxic and/or lethal effects on the associated benthic faunas were probably very limited (Neff, 1987, 2005; Dalmazzone et al., 2004). 4.2. Macrofauna On the basis of our macrofaunal descriptors, we recognised four groups of stations: (1) Reference stations 2 and 10, with a low macrofaunal density (<1000 ind/m2, Fig. 3A) and high species richness (>30), diversity (5 bits) and ITI (>60%), suggesting a natural, unimpacted environment. In 2003, polychaete species, such

2015

as S. scutata were dominant. These taxa tend to have a large body size, a low growth rate and long reproductive periods, typical of animals with a slow turnover rate, occurring in well oxygenated outer shelf environments. They are highly sensitive to disturbance, particularly to those involving an organic enrichment (Salen-Picard and Arlhac, 2002). (2) An area between 300 and 700 m distance (stations 3 and 16, 500 and 730 m SSE, and stations 9, 17 and 8, 500–300 m NNW), with macrofauna very similar to the reference stations, characterized by low macrofaunal densities (<1000 ind/m2), high species richness (>30) and diversity (3.5–5 bits) and ITI above 60%. In 2003 A. assimilis, S. scutata and C. cf. coasta had lower densities in this group than at station 2, and Aphelochaeta sp., A. gracilis and Nemertean sp. 1 showed higher densities (particularly at stations 16 and 17). At station 3, Spiochaetopterus sp., M. dorsobranchialis and Marphysa sp. showed increased densities. Barium and hydrocarbons concentrations were close to zero, and the nine taxa most resistant to environmental disturbance

Fig. 8. Distribution of the total densities of the eight foraminiferal indicator species from the fraction >150 lm (ind/10 cm2) as a function of the distance from the discharge point.

2016

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Fig. 9. Distribution of the total densities of the seven foraminiferal indicator species from the fraction 63–150 lm (ind/10 cm2) as a function of the distance from the discharge point.

(Fig. 6) were almost completely absent. However, the slightly different macrofaunal composition suggests that the environmental conditions in this area (especially at stations 3 and 16) were somewhat modified in comparison to the reference stations. (3) An area represented by stations 4 and 7 (230 m SSE and 150 m WNW, respectively), showing a marked increase in macrofaunal density, but still a fairly high species richness and diversity (2.5–3 bits). In 2002, species richness was even maximal at station 4. The ITI was intermediate (20–30%) at station 4, but still very high (>60%) at station 7, which was only sampled in 2000. At station 4 (but not at station 7), high barium contents, and traces of hydrocarbon (found in 2000) indicated the presence of drill mud. The associated benthic macrofauna apparently responded to a moderately modified environment due to drill mud disposal. Unfortunately, station 7 was not sampled in 2003, when station 4 was strongly dominated by Capitella sp. and Sigambra sp., and P. cf. tryonix, and A. cf. edentula were also very abundant. The first species is a well known indicator of organic enrichment, just like the lucinid bivalve A. edentula (Lebata, 2001) and some Paramphinome species (such as P. jeffreysi in Rosenberg, 1995). In fact, P. cf. tryonix, P. cf. multibranchiata, Spiophanes

sp. (all deposit feeders), and Glycera sp. 1 (possibly a carnivorous species feeding on the other highly abundant polychaete species) all attained maximum densities at this station. The dominant taxa of area two were still present, but much less abundant. (4) A strongly modified area (stations 5, 13 and 6, at 175 m SSE, 100 m S, and 70 m W, respectively), showing maximal macrofaunal densities together with minimal species richness and diversity (0.5–2 bits). This decreased diversity was the result of an almost total disappearance of all sensitive taxa. The ITI was always below 20% and the hydrocarbon and barium concentrations were very high, all these data pointing to a substantial ecosystem modification due to oil drilling activities. In 2003, the macrofauna of stations of the fourth group was strongly dominated by Sigambra sp. and Capitella sp., two polychaete worms commonly found in sediments characterized by organic enrichment (Warwick, 1986; Weston, 1990). Especially the sibling species of the Capitella capitata group show in many studies a proliferation in the immediate vicinity of a disposal point of organic waste, followed by sharp decrease in density together with the increasing distance from the waste disposal source (e.g. Rosen-

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berg, 1976; McCall, 1977; Pearson and Rosenberg, 1978; Kikuchi, 1979; Gray, 1981; Tsutsumi and Kikuchi, 1984; Martin and Grémare, 1997). The genus Sigambra, in turn, is commonly considered as carnivorous (Fauchald and Jumars, 1979) but, more recently, some species of the genus have been reported as opportunistic species likely associated to organic enrichment from different origins (Mackie et al., 1993; Brooks et al., 2004), which may be the case in our study area. In 2003, station 5 was not sampled and a difference was observed between stations 13 and 6. At station 6 (70 m W), Sigambra sp. was strongly dominant and Capitella sp. occurred with a low density. At station 13 (100 m S), both species were dominant, with equal densities, but also Ampharetidae genus A, A. cf. edentula, L. cf. contrarius and P. cf. tryonix were very abundant. At station 6, the latter four taxa were almost absent. This suggests that station 6 was more strongly modified than station 13 in 2003, which agrees with the observed maximum in hydrocarbon contents. A comparable macrofaunal pattern was observed in 2002, while in 2000 both species occurred with high densities at station 6, suggesting that this station was slightly less perturbed that year. The macrofaunal distribution in our study area showed a very typical pattern, commonly associated with point sources of organic matter input (e.g. Mackay et al., 1972; Pearson and Rosenberg, 1978). The changes in macrofaunal density, diversity and composition seem to be caused by different responses of the various taxa to an environmental stress gradient. The more sensitive species progressively disappeared when the sediment quality deteriorated, being replaced by more tolerant taxa, which were rare or absent at the non-impacted sites (e.g. Chandler, 1970; Washington, 1984; Hellawell, 1986). In the vicinity of the disposal site, where environmental changes were maximal, species richness was minimal, macrofaunal density was maximal, the most sensitive species were absent, and only the most resistant, often opportunistic, taxa were capable to survive and proliferate. With an increasing distance from the disposal site, the environmental perturbation diminished, and the diversity progressively increased due to a proportional increase of more sensitive taxa. In turn, the reduction in organic matter contents prevented the proliferation of opportunistic/resistant species, resulting in an overall density decrease. Station 4 (250 m S of the discharge point) showed the high density and elevated species richness typical of a transitional area, where opportunistic species (related to the still elevated organic matter availability) coexisted with sensitive taxa. Farther than 250 m, the conditions became progressively similar to those found at the reference stations.

2017

degree of environmental stress, as reflected by an increased density of stress-resistant and opportunistic taxa such as U. peregrina and B. dilatata (Figs. 8 and 9) at station 16. These species have often been described as indicators of increased food availability in marine benthic ecosystems. (e.g. Lutze and Coulbourn, 1984; Lutze, 1986; Barmawidjaja et al., 1995; Mackensen et al., 1995;Kuhnt et al., 1999; De Rijk et al., 2000; Huang et al., 2002). In view of the first traces of eutrophication found at station 16 (as suggested by the FIEI), which should intensify towards the disposal site, the very low density at station 3 was surprising, particularly in contrast with the relatively high FIEI. A possible explanation could be an inadequate sampling of the sediment surface, leading to an under-estimation of the foraminiferal densities (Mojtahid et al., 2006). (3) Stations 4 and 13 (230 m SSW and 100 m S), with very high foraminiferal density and diversity, particularly at station 4. The FIEI above 60% suggested a strong environmental impact for both stations, although the composition of the foraminiferal meiofauna indicated slight differences. While B. marginata and Gyroidina sp. 1 showed comparable densities at both stations, B. striatula, B. aculeata, A. scalaris and Eggerella sp. 1 dominated at station 4, whereas B. costata, U. peregrina, V. bradyana and B. dilatata were very abundant at station 13. These differences may correspond to a succession in dominance from more opportunistic taxa at station 4 to more stress-tolerant and less opportunistic taxa at station 13. Accordingly, the dominant taxa at station 13 had lower standing stocks than those at station 4. The distribution of A. scalaris and Eggerella sp., which were dominant at station 4, but are almost absent at station 13, was particularly remarkable. Since environmental stress appeared to be higher at station 13 than at station 4 (FIEI = 85% and 65%, respectively), we suggest that these two taxa were still capable to profit from the eutrophic conditions at station 4, but did not tolerate the increased stress at station 13. (4) A highly modified area (station 6, 70 m W), with a density comparable to that of the reference area (station 2), but much lower than in area three (stations 4 and 13). FIEI was very high (70%) and B. marginata, B. costata, B. aculeata and B. striatula were dominant. Although the foraminiferal meiofauna was poor and dominated by opportunistic taxa, the environmental conditions were probably too adverse to allow them to attain high standing stocks. 4.4. Comparison macrofauna/foraminifera

4.3. Foraminifera The foraminiferal distribution patterns, which are only available for 2003 (Mojtahid et al., 2006) showed evident similarities with the macrofaunal ones, but also some remarkable differences. The overall characteristics of the foraminiferal meiofauna also allow us to distinguish four groups of stations. (1) The reference area (station 2, 2 km SSW), showing low foraminiferal density, species richness and FIEI (15%), indicative of a low relative proportion of perturbation-resistant taxa, and a dominance of a foraminiferal meiofauna typical of natural, non-impacted conditions. According to Mojtahid et al. (2008) the low foraminiferal densities could be related to the presence of strong bottom currents, that gave rise to relatively coarse (i.e. silty to fine sandy) sediments, less favorable for mud-dwelling foraminifera. (2) An area between 450 and 730 m from the disposal site (stations 16, 3 and 17), with low foraminiferal density and diversity, but a relatively elevated FIEI (40–55%) suggesting a low

In spite of the overall similarity of the macrofaunal and foraminiferal distribution patterns, some key differences existed, which were particularly evident in the density and diversity trends:  Both macrobenthos and foraminifera showed perspicuous density maxima at some distance from the disposal site, and decreasing densities both towards the disposal site and towards sites farther away. For macrofauna, maximal densities, 15–20 times higher than at the reference station, were found 100 m S of the disposal site. For foraminifera, maximal densities, 30 (>150 lm fraction) to 10 times higher (63–150 lm fraction), were found 250 m S.  The macrofaunal density at station 6 (closest to the disposal site), was still one order of magnitude higher than at the reference area, whereas the foraminiferal standing stocks were very low, and comparable to those of the reference station.  For both groups, diversity was maximal at station 4, which appears to be in a transitional area, with a mixture of species with different ecological strategies.

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 For macrofauna, this density pattern was confirmed by that of diversity, while, rather surprisingly, the diversity of benthic foraminifera did not show a decreasing trend towards the disposal site.  The macrofaunal densities appeared to show an inverse tendency with respect to the species number, while these two parameters showed the same tendency in the case of foraminifera. This difference could be due to the fact that many macrofaunal taxa were very stress-sensitive, leading to their absence from the immediate vicinity of the disposal site. Conversely, such sensitive species may not exist in foraminifera. Alternatively, due to their small size, and in the hypothetical presence of strong bottom currents, foraminifera may easily be transported. The foraminifera found at the most severely impacted area may not live there permanently, but may have been transported there. Finally, the fact that density and diversity showed same tendency could indicate that a larger sediment volume should have been sampled to obtain a more correct picture of the foraminiferal diversity, which was surprisingly similar at all stations. However, the fact that FIEI gradually decreases with increasing distance from the disposal site, indicates that in spite of the small sample volumes, the composition of the foraminiferal faunas shows a clear response to the degree of environmental stress. Summarising, macrofaunal and foraminiferal assemblages appear to respond in a slightly different way to environmental stress related to drill mud disposal, the former appearing to be less heavily impacted than the latter at the disposal site. In fact, the low foraminiferal densities suggest nearly azoic conditions, which seem typical for the most impacted sites (e.g. Schafer, 1970; Alve, 1995; Burone et al., 2006; Mojtahid et al., 2008). In turn, the high macrofaunal densities suggest a stronger tolerance to stressed conditions. Moreover, the peak of opportunistic species was positioned S of the disposal site in both cases, but 100 m closer for macrofauna than for foraminifera. Macrofaunal and foraminiferal assemblages also differed at a species level. First, some macrofaunal taxa (sensitive to pollution) showed a maximum density at the reference area and rapidly disappeared when approaching the drilling platform. Rather surprisingly, none of the dominant foraminiferal taxa showed such a pattern. Although we cannot exclude that some rare taxa were sensitive to disturbance, the total density of such taxa was very low, also in the reference area. Furthermore, there was a succession of first and second order opportunistic macrofaunal species, strongly increasing their standing stocks from station 16 (730 m SSE) to station 6, and then decreasing towards the disposal site. However, even if total macrofaunal densities were lower at the most impacted area (stations 6 and 13), the two dominant macrofaunal taxa showed higher densities there, pointing to their opportunistic mode of life. Although a similar succession of opportunistic foraminiferal species was observed, maximum densities at stations 4 and 13 were followed by a strong reduction at station 6, including the most resistant taxa. This suggests that unlike some macrofaunal species, the corresponding foraminiferal taxa no longer had an opportunistic response to stress. As a consequence, quantitative methods using biotic indexes to assess environmental impact cannot be constructed exactly in the same way. For macrofauna, Word’s (1979) ITI, which has previously been successfully used (e.g., Wildish, 1984; Gaston, 1987; Gaston and Nasci, 1988; Karakassis and Eleftheriou, 1997; Gaston et al., 1998), also gave satisfactory results in our study. ITI estimates the level of environmental impact according to the differential response of each trophic group to the changing environmental conditions. In comparison to other biotic indices, such as AMBI (Borja

et al., 2003), which uses rather subjective ecological characterizations of the various species (sensitive, intermediate, 1st and 2nd order opportunist, etc.), the advantage of the ITI is that for many species, the feeding strategy is well known, and has been observed objectively (Grall and Hily, 2003). For foraminifera, an approach comparable to the ITI is not possible. Most taxa found in our study area are shallow infaunal deposit feeders (Murray, 2006), whereas suspension feeders and sediment surface dwellers were very rare. Consequently, the FIEI was necessarily based on the differential response of the various taxa to environmental perturbation. This response was estimated on the basis of (1) their respective distributional patterns in this study area and (2) a comparison of living and subrecent foraminiferal meiofauna, the latter supposed to represent the pre-impact, natural conditions (Mojtahid et al., 2006). Although this method could eventually lead to a certain circularity, it has the evident advantage that the selection of indicator species is based on the local conditions. This is particularly important, because a foraminiferal (or macrofaunal) species will not always respond in the same way to ecosystem enrichment. Opportunistic responses to ecosystem enrichment only appear when the original (natural) trophic level is below their preferred range for a given species. In case the trophic level of the natural environment coincides with the preferred trophic range of a species, further ecosystem enrichment can only lead to a reduction of the standing stocks, and ultimately, to its disappearance from the ecosystem. This dichotomy seems to be the underlying reason for the succession of opportunistic species along our sample transect. It strongly suggests that single species will not systematically show an opportunistic response to ecosystem enrichment. Therefore, generalisations in this sense are necessarily too simplistic. The comparison between ITI and FIEI for 2003 (Fig. 10) reveals a very similar overall pattern, but with two clear differences. First, ITI indicates maximal impact at station 6, whereas FIEI suggested maximal environmental stress at station 13. However, the slightly lower FIEI value at station 6 was mainly caused by the extremely low foraminiferal density at this station, which in itself indicates a severe stress. Second, ITI suggests a very sharp boundary between the still clearly impacted station 4 (230 m S) and the apparently unimpacted stations 3 and 16 (470 and 730 m, respectively). On the contrary, FIEI shows a gradual decrease until the reference station 2, with stations 3 and 16 still being moderately impacted. These differences could be explained by a higher sensitivity of foraminifera than of macrofauna to low stress levels (Mojtahid et al., 2008). However, the difference between the groups could also be due to the different approaches used in the ITI and FIEI methods. The ITI is based on an ‘‘a priori” grouping of macrofaunal taxa in four categories, which may be problematic because of a lack of information for some species and contradictory literature evidence for others, as suggested by Wildish (1984) and Grall and Hily (2003). Also some macrofaunal taxa (e.g. polychaetes, bivalves) may change their feeding behavior in function of the environmental conditions (e.g. Levinton, 1982; Gambi, 1989; Shimeta, 1996; Pinedo et al., 1997), and a different, additional trophic group (i.e. mixed group) has often been used for such species (Dauvin and Ibanez, 1986; Pinedo et al., 1997; Martin et al., 2000). As explained before, the selection of tolerant and/or opportunistic indicator species used in the FIEI is based on the distributional patterns in the study area, which has the evident advantage of better taking into account the species adaptations to local environmental conditions. In order to find out whether these different strategies may be the origin of the difference between ITI and FIEI at stations S3 and S16, we applied our FIEI approach to the macrofaunal data of 2003. The resulting macrofaunal curve (Fig. 10) was very similar to the FIEI curve, suggesting that macrofauna had a sensitivity similar to foraminifera, and that stations 3 and 16 were still moder-

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2019

Fig. 10. Distribution of ITI (%), FIEI (%) and FIEI (%) based on macrofaunal data as a function of the distance from the discharge point in 2003.

ately impacted. Nevertheless, a difference occurred at the most impacted sites, where the macrofaunal FIEI rose above 90%, whereas the foraminiferal FIEI ranged between 70% and 90%. According to our data, this difference was probably caused by the fact that sensitive macrofaunal taxa had completely disappeared from these sites, whereas sensitive foraminiferal taxa were still present, albeit in lower numbers. 5. Conclusions (1) Both macrofauna and foraminifera can be used as bio-indicators of environmental impact due to offshore oil drilling activities. (2) The wide spectrum of sensitive to opportunistic/tolerant taxa allowed the macrofauna to show important differences in spatial distribution. There were also tolerant and/or opportunistic foraminiferal taxa, but species being very sensitive to drill mud disposal were not very prominent. If existing, such species did not dominate the macrofauna of the native, unimpacted areas. (3) There are evident differences between macrofaunal and foraminiferal indices of environmental impact. The former are mainly based on a priori groupings of indicator species (either according to their tolerance levels or their feeding behavior), while for the foraminiferal index, indicator species were selected on the basis of both the observed spatial patterns in the study area, and the comparison of recent and subfossil foraminiferal meiofauna. (4) The foraminiferal index (i.e. FIEI) appeared to be more discriminative than the macrofaunal one (i.e. ITI), since the area between 500 and 750 m from the disposal site was nonimpacted according to ITI, but still moderately disturbed according to FIEI. (5) Our tentative use of the FIEI approach applied to macrofaunal data showed a similar sensitivity to that of the index based on foraminifera. Unfortunately, since most macrofauna remains are not preserved in the sediment record, it is not possible to use the comparison of recent and subfossil macrofauna to confirm the choice of indicator species.

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