Amphipods are Good Bioindicators of the Impact of Oil Spills on Soft-Bottom Macrobenthic Communities

PII:

Marine Pollution Bulletin Vol. 40, No. 11, pp. 1017±1027, 2000 Ó 2000 Elsevier Science Ltd. All rights reserved Printed in Great Britain S0025-326X(00)00046-1 0025-326X/00 $ - see front matter

Amphipods are Good Bioindicators of the Impact of Oil Spills on Soft-Bottom Macrobenthic Communities  J. L. GOMEZ GESTEIRA * and J.-C. DAUVINà  Facultade de Bioloxia, Departamento de Bioloxõa Animal, Universidade de Santiago de Compostela, 15706 Santiago de Compostela, Spain àStation Marine de Wimereux, Universit e des Sciences et Technologies de Lille 1, CNRS-UPRES-A 8013 ELICO, B.P. 80, 62930 Wimereux, France

The Amoco Cadiz oil spill in 1978, and the Aegean Sea oil spill in 1992, a€ected soft-bottom communities, respectively from the Bay of Morlaix (western English Channel) and from the Rõa de Ares and Betanzos in the northwestern Iberian peninsula. These infralittoral communities on muddy ®ne sand showed similar species composition and structure and occurred in similar hydro-climatic conditions. The e€ects of the spills were identical in both areas with the disappearance of the amphipods especially those from the amphipod genus Ampelisca with a very low colonization of these species during the four years after the spill. The recovery rate of the amphipods was slow but progressive. In such communities no proliferation of opportunistics was observed after the stress. In the sites, where polychaetes dominated before the spill, they remained dominant, whereas other sites showed very low total abundances during the two years after the spill due to the absence of compensation for the disappearance of these crustaceans. In fact, there was a very low impact of the spill on polychaetes, but a high one on amphipods. In the future, it is suggested to focus monitoring after a spill only on a single amphipod group proposed as a bioindicator for detecting the impact of pollution. A polychaete/ amphipod ratio is proposed to re¯ect temporal change of soft-bottom communities analogous to the nematode/copepod previously suggested for the meiobenthos. Detailed knowledge of the qualitative and quantitative structure of a benthic community is still needed in order to identify very precisely the e€ect of a pollution event. Ó 2000 Elsevier Science Ltd. All rights reserved. Keywords: Amoco Cadiz; Aegean Sea; oil; bioindicators; amphipods; polychaetes. Since the end of the 1980s, the number of oil spills have dramatically decreased due to the reduction in the *Corresponding author.

quantity of oil carried at sea, 431 million t less in 1986 than in 1977 (GESAMP, 1991), and high levels of security of navigation. So 1995 was the best year to date with only 9000 t spilled at sea (ITOPF, 1996). Nevertheless there has been a considerable annual variation although the majority of oil spills are small (less than 7 t). Some catastrophic releases have occurred in recent years, e.g. Aegean Sea 1992, Braer 1993, Sea Empress 1996 and Erika in 1999. By contrast, the preceding years 1960±1980 were characterized by numerous major oil spills (more than 700 t) with some of them being enormous judging by the volume of oil entering in the marine environment as well as the impact of the pollution on marine communities. Among the more important ones, there were the catastrophes of the Torrey Canyon in 1967 (Smith, 1968), Urquiola in 1976 (Gundlach and Hayes, 1977), the Amoco Cadiz in 1978 (Laubier, 1991), the Mexican Ixtoc I in 1979 (Lee et al., 1980), and the Exxon Valdez in 1989 (Holloway and Horgan, 1991; Feder and Blanchard, 1998; Jewett et al., 1999). The impact of some other smaller spills has been very well studied in terms of short-and long-term changes on marine communities, see Sanders et al. (1980) for the oil spill of the barge ÔFloridaÕ in 1977, and Elmgren et al. (1983), Linden et al. (1979) for the ÔTsesisÕ oil spill also in 1977. The e€ects of very small accidents like the Antonio Gramsci in 1979 and Nella Dan in 1987 on the littoral benthic communities have also been studied (Bonsdor€, 1981; Smith and Simpson, 1998). Some general features on the impact of the spills on macrobenthic species and communities have resulted in a few key observations: (i) species sensitive to hydrocarbons, especially crustaceans, and especially amphipods, disappear rapidly and show very high initial mortalities, (ii) the initial impact is correlated with the importance of sensitive species in natural conditions, (iii) in some cases no sensitive species or opportunistic species, especially polychaetes which usually proliferate after an increase of organic matter, show important increases of abundance 1±3 years after 1017

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and Betanzos of the Aegean Sea in Galicia (Spain) in 1992s were monitored for four years (1992±1996) to reveal the main features of this impact. This work showed a very high similarity with the impact of the Amoco Cadiz oil spill on the infralittoral communities from the Bay of Morlaix (western English Channel). The comparison of these two oil spills reveals general patterns of the e€ects of oil on soft-bottom macrobenthic species and populations. The objectives of this paper are: (i) to describe the e€ects of oil pollution over four years such a spill, (ii) to compare the impact of the Amoco Cadiz and the Aegean oil spill on two infralittoral bays, and (iii) to propose a selection of species suitable for use in monitoring the biological e€ects of oil pollution on macrobenthic communities.

the stress, and (iv) the duration of colonization of affected species after an oil spill generally surpasses 10 years (Smith, 1968; Laubier, 1991; Holloway and Horgan, 1991; Dauvin, 1998). At the end of the 1970s and the beginning of the 1980s, many studies emerged on bioindicators of pollution or pollution indices to represent the structure and spatio-temporal changes of the marine benthic communities (e.g. Pearson and Rosenberg, 1978; Glemarec and Hily, 1981; Bellan, 1980, 1984; Ra€aelli and Mason, 1981). These works underlined the potential to group macrobenthic species into categories according to sensitivity, resistance or proliferation along a pollution gradient. The e€ects of the wreck on the infralittoral muddysand macrobenthic communities from the Ria de Ares

Materials and Methods Study area Bay of Morlaix (Fig. 1). The Pierre Noire (PN) site, in the Abra alba±Hyalinoecia bilineata ®ne sand macrobenthic community, is located in the eastern part of the Bay of Morlaix, France (48°42.500 N; 3°51.960 W). The sediment is ®ne sand and shows low temporal changes (Table 1). Hydrological characteristics present few seasonal or multi-annual ¯uctuations; the bottom temperatures ranged from 8°C in March to 15°C in September, and the salinity varied between 34.5 P.S.U. in winter and 35.3 PSU at the beginning of October (Dauvin, 1984). The Riviere de Morlaix (RM) site, in the A. alba± Melinna palmata muddy ®ne sand macrobenthic community, is located in the middle of the navigational channel at the eastern border of the Morlaix Estuary (48°39.270 N; 3°52.070 W). The sediment is a mixture of ®ne sand and mud (about 30% of the sediment consists of particles between 63 and 125 lm) (Dauvin, 1984; Ibanez and Dauvin, 1988). Ordinarily salinity ranges from 34.00 P.S.U. in winter to 35.10 P.S.U. at the end of the summer. Because the station is located near the mouth of the estuary, the bottom waters show dilution during the maximum river discharge in winter (< 32:2 P.S.U.). Bottom temperatures range from 8°C in winter

Fig. 1 Location of the PN and RM sites in the Bay of Morlaix.

TABLE 1 Main characteristics of the sampling sites in the bay of Morlaix and Ria de Ares and Betanzos.a Area Sites Depth (m) Median grain size (lm) % of ®ne particles < 63lm Grab Number of replicates Sieve mesh (mm) Total surface sampled Date of sampling Numbers of samples a b

Bay of Morlaix PN RM 17 10 148±184  90 <1 13.5 SMI SMIb 10 10 1 1 1 m2 1 m2 April 78±March 82 48 20

Rõa de Ares and Betanzos K 5 27 66.5 BC 6 1 0.1 m2 28

BC: Box Corer. SMI: Smith McIntyre grab. Except in August 1978 when a Hamon gab was used (1.2 m2 sampled).

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T W X 8.5 13 11 67 174 138 45.4 15.2 16.7 BC BC BC 6 6 6 1 1 1 0.1 m2 0.1 m2 0.1 m2 December 92±November 96 28 28 28

Z 14 95 19 BC 6 1 0.1 m2 28

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to 16°C in summer, but during severe winters the temperature is <6°C as in 1986. Ria de Ares and Betanzos (Fig. 2). The ®ve sites located in the Ria de Ares and Betanzos, Spain, come from two di€erent sectors. Two were located in the inner part of the ria, each one near a di€erent estuarine area. Site T (43°25.70 N; 8°12.80 W) and site K (43°21.920 N; 8°13.920 W), with bottoms less than 10 m deep, belonged to the same infralittoral A. alba community. The sediment there is characterized by ®ne particles, more than 50% silt and clay (Table 1), and the percentage of organic matter ranged from 2.38% to 3.28% in T and from 3.62% to 4.91% in K. The community is slightly a€ected by continental water supply, reaching salinity values below 32 P.S.U. and also receives untreated industrial and urban sewage. The three remaining sites were located in the central zone of the ria, site X (43°23.900 N; 8°14.150 W), site W (43°24.750 N; 8°15.000 W) and site Z (43° 23.850 N; 8°15.750 W). The depths ranged from 10 to 15 m and sediments were dominated by medium, ®ne and very ®ne sands (Table 1) with moderate organic matter content (between 0.91% and 2.63%). Salinity levels ranged from 34.5 to 36.5 P.S.U. These sites were located in an ecotone between the A. alba and Venus gallina communities (S anchez Mata et al., 1999).

the PN site and in the other occasions at RM site. Sampling was done four to six times per year from August 1977 to March 1982 at RM and was monthly from April 1978 to March 1982 at PN (Table 1). After collection, the sediment was sieved (1 mm circular mesh) and the retained material was ®xed with 10% neutralized formalin. In the Rõa de Ares and Betanzos, macrobenthic samples were collected using a 0.017 m2 box corer. At each site six replicate samples were taken (total area of 0.1 m2 ). The grab penetrated approximately 16 cm into the bottom. A sediment sub-sample, for particle-size determination and for other sediment analyses was taken from the grab by means of a corer tube. Samples for fauna were sieved through 1 mm mesh sieve and the residue preserved in 6% neutralized formalin. The temperature, salinity and oxygen concentration was also assessed to obtain some additional information about each site. The sampling was carried out monthly during the ®rst thirteen months after the oil spill (from December 1992 to November 1993), at three occasions in 1994 (March, June and September 1994), and eight occasions in 1995 (January, April, June, July, August, September, October and November 1995) and seasonally during the last year (January, April, July and November 1996).

Sampling For the Bay of Morlaix, except the samples of August 1978 when a Hamon grab was used at RM (four replicates covering a surface area of 1.2 m2 ), 10 replicate samples (Smith McIntyre grab, 0.10 m2 ) were taken at

Results

Fig. 2 Location of the K, W, X, T, and Z sites in the Rõa de Ares and Betanzos.

Main characteristics of the oil spills Of the 220 000 t of oil spilled into the sea from the Amoco Cadiz wreck, between 10 000 and 92 000 t according to di€erent authors had been trapped in subtidal sediments (Dauvin, 1984). The presence of hydrocarbons in the subtidal bottom sediments of the Morlaix bay was evident at the beginning of April 1978 just two weeks after the wreck (Cabioch et al., 1978). At the Pierre Noire site, the concentration of hydrocarbons (in part 10ÿ6 , i.e. mg kgÿ1 dry sediment) in the sediments measured by infrared spectrophotometry reached 200 ppm in the summers of 1978 and 1979, and did not exceed 50 ppm after the winter of 1981 (Dauvin, 1984). At the RM site, the content of hydrocarbons remained higher than 50 ppm from the spill to April 1980. They reached very high values in August 1978 (1443 ppm), May 1979 (3152 ppm), and later in February 1981 (540 ppm), and did not exceed 50 ppm after the winter of 1981 (Dauvin, 1982, 1984). The oil tanker `Aegean Sea' crashed on 3 December 1992, and spilled nearly 80 000 t of light `brent blend' crude along 200 km of coastline. A high portion of oil was lost by evaporation after the explosion and the resulting ®re. Because the low speci®c gravity of the oil and weather conditions the crude was emulsi®ed and spread rapidly. High concentrations of aromatic hydrocarbons in the water column were found two months after the oil spill (mean 79.1 lg/l and maximum 257 lg/ l), with a sharp decrease in May 1993 (mean 3.2 lg/l) 1019

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and an important `peak' in September 1993 (mean 18.8 lg/l) (Gonzalez et al., 1997) as a result of physical disturbances of the contaminated sediment by di€erent dredging operations and by materials dumped from beach cleaning operations. Some oil went down reaching the subtidal bottom forming oil sandy layers, in March 1993 these oily layers were 10 cm deep within sediments (S anchez Mata, 1996). Two years after the spill the composition and spatial distribution of the hydrocarbons in sediment samples showed values typical of medium-contaminated environments. The analysis was performed by gas chromatography (aliphatics) and HPLC-UV (PAHs). High values were found at the mouth of the rõa (4000 ng/ g aliphatics and 10 174 ng/g PAHs), and concentrations of PAH in a small area in the middle part of the ria reached 34228 ng/g; nevertheless, the levels decreased in the innermost part of the ria (Neira et al., 1997). Total abundance of macrobenthos The total densities of macrobenthos were in the same order of magnitude in the seven sites (Fig. 3) with a minimum including between 500 and 1000 ind. mÿ2 , and

maximum varying between 5000 and 8000 ind. mÿ2 . Three patterns were observed over the four years after the oil spill: (i) three sites Z, RM, and K, showed regular seasonal variations with minima at the end of winter or at the beginning of spring and maxima at the end of summer or at the beginning of the autumn. Nevertheless, at station K, the polychaete Chaetozone setosa dominated and the changes in the total abundance at the site were a€ected by this opportunistic species. The spill seemed to have little e€ect on the macrobenthic communities which continued to show annual cyclical changes. (ii) two sites (T and X) both in the rõa, showed a decrease of density from the beginning of the spill (month 1, t1) until 6±9 months after the spill, where the abundance remained very low until t30, after it rapidly increased during spring±summer 1995 (months, t32±34). (iii) two sites (PN and W), showed low density from the beginning of the survey (month 1, t1) to the ®rst 24± 30 months after the spill. After this abundances showed, as the second group of sites (T and X), of important recruitment three and four years respectively after the pollution. Crustacea abundance Fig. 4 shows the temporal changes of the Crustacea, the Amphipoda and the amphipod genus Ampelisca, which was one of the most abundant amphipod groups in the soft-bottom communities from both areas. Except in the RM site, where some amphipods and some other crustaceans (mainly decapods) remained after the spill, it was evident that this group was particularly a€ected by the spill, especially Ampelisca which is very sensitive to oil. In fact, three main steps of temporal change can be identi®ed: (i) the mortality a€ecting the crustacean populations until t1±2 after the pollution. Some individuals resisted the spill and died in the ®rst months after the spill. High concentrations of hydrocarbons were present in the sediment. The high sensitivity of crustaceans to toxic aromatic hydrocarbons which affected the communities in the ®rst weeks after the spill; (ii) very low abundances of crustaceans, amphipods and Ampelisca until t24±28 after the spill, and (iii) large increases of crustaceans when the sediment was decontaminated t30±48 within seasonal changes in abundance. It is clear that for all sites, the increase of Ampelisca occurred only two years after the spill, respectively between t28±32 and t40±44, during the spring and summer periods of recruitment.

Fig. 3 Temporal changes in total abundance of the seven sites from t1 to t48 (t in months) after the spill.

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Polychaete abundance In some sites, polychaetes were the dominant group. In sites RM and K, they formed >90% of the total abundance (Table 2). At site Z the polychaetes represented >50% of the total abundance. In these three sites the total abundance re¯ected the seasonal variation of

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Spiochaetopterus costarum. Nevertheless, these species seemed una€ected by oil concentrations in the sediment. D. glaucus showed higher densities at the end of the study. However S. costarum showed the opposite pattern with maximal abundance at the beginning of the survey. Mollusc abundance Molluscs, particularly represented by bivalves, were a secondary group and formed <10% of the total abundance in the seven sites (not ®gured in this paper). Except in the Bay of Morlaix (PN, RM), where the bivalves (A. alba, A. prismatica, Thyasira ¯exuosa and Venus ovata) showed high levels of recruitment the second and the third years after the spill (t12±18, t24±30, see Dauvin, 1984), molluscs showed more erratic ¯uctuations in the other sites, with an increasing trend until t30 to the end of the survey in the three sites K, X, and W in the rias. At sites W and Z the bivalve Fabulina fabula reached higher abundance values during the two ®rst years of the survey (Table 2), this species was constant on these bottoms with a small increase over some months (t10±29).

Fig. 4 Temporal changes in the relative frequency of the crustacea, amphipoda and Ampelisca abundances in the seven sites from t1 to t48 (t in months) after the spill (100% corresponds to the maximum of crustacea abundance, and the other values correspond to the ratio between the observed abundances of each group at each date and the maximum abundance of crustacea 100).

polychaete abundance, as this group was dominant. At the other sites T, X, PN, and W, the polychaetes formed the dominant group of the communities from the beginning of the surveys (t1) until t30, then their dominance decreased until the end of the observation (t48) (Fig. 5). In the Rõa de Ares and Betanzos, important peaks of density were due to opportunistic polychaetes. At site W, the increase in total density between t30 and t35 was due to Diplocirrus glaucus, as at site K where a single species C. setosa formed about 60% of the total abundance at t16. The muddy sites (K and T) were dominated by two polychaetes D. glaucus and

Polychaete/amphipod ratio According to Pearson and Rosenberg (1978) and Glemarec and Hily (1981) opportunistic polychaetes species are selected in relation to their ability to proliferate after an increase in organic matter. Typically, these are, Capitellidae: Capitella capitata, Mediomastus fragilis, Heteromastus ®liformis, and other unidenti®ed Capitellidae; Cirratulidae, C. setosa, Cirriformia tentaculata, Cirratulus ®liformis, Tharyx marioni, and other unidenti®ed Cirratulidae; Spionidae, Polydora ¯ava and Malacorecos fuliginosus, Eunicidae, Nematonereis unicornis, (groups IV and V in Glemarec and HilyÕs classi®cation and, species indicators of pollution or species indicators of sub-normal area Bellan (1984) and Lechapt et al. (1993)), and the Spiochaetopteridae: S. costarum (this genus was considered by Wass (1967) as an organic pollution indicator, and S. costarum described in Galician coasts as an opportunistic species typical in muddy bottoms enriched by organic matter L opez-Jamar (1981) and Rodrõguez Rey and Mora (1984)), was present only in the Iberian sites. The temporal changes of the ratio log10 (polychaetes/amphipods + 1) (Fig. 6) showed three main patterns within the sites during the four years after the oil spill: (i) the ratio at sites RM and K remained very stable along the survey with very high values: log10 (polychaetes/amphipods + 1)>1(polychaetes/amphipods+1, between 20 and 140) showing a very strong dominance of opportunistic polychaetes. The spill had negligible e€ects on the ratio in these communities. (ii) four sites Z, T, X,W, showed a stable ratio from the beginning of the spill t1 until t32±36 after the spill with high values, after this the ratio decreased until 1021

Marine Pollution Bulletin TABLE 2 List and dominance (%) in abundance of the ®ve dominant species in each sites over the four years following the spill. Site

Z

1 2 3 4 5 R

Year 1

Year 2

Year 3

Year 4

t1±t12

t13±t24

t25±t36

t37±t48

Edwardsia claparedii Fabulina fabula Spio decorata Chamelea gallina Magelona mirabilis

13.6 9.0 6.9 6.5 6.2 41.8

Spiophanes bombyx Fabulina fabula Edwardsia claparedii Diplocirrus glaucus Magelona mirabilis

17.2 14.7 8.0 7.3 4.9 52.1

Edwardsia claparedii Tubulanus polymorphus Phoronis muelleri Spiophanes bombyx Hyalinoecia bilineata

9.9 5.7 5.3 5.2 4.3 30.3

Spio decorata Spiophanes bombyx Hyalinoecia bilineata Edwardsia claparedii Phoronis muelleri

9.3 9.3 6.5 3.8 3.6 32.5

RM 1 2 3 4 5 R

Chaetozone setosa Melinna palmata Mediomastus fragilis Notomastus latericeus Euclymene oestedii

64.6 11.2 9.2 2.2 2.0 89.2

Chaetozone setosa Mediomastus fragilis Melinna palmata Polydora pulchra Lanice conchilega

54.5 7.9 7.0 3.3 2.9 75.6

Chaetozone setosa Mediomastus fragilis Lanice conchilega Melinna palmata Tharyx marioni

41.7 8.8 7.4 7.1 5.9 70.9

Chaetozone setosa Melinna palmata Polydora pulchra Tharyx marioni Lanice conchilega

52.7 9.6 7.4 5.4 4.8 79.9

K

1 2 3 4 5 R

Spiochaetopterus costarum Diplocirrus glaucus Chaetozone setosa Phoronis muelleri Polydora ¯ava

49.8 11.1 9.3 2.6 2.4 75.2

Chaetozone setosa Spiochaetopterus costarum Diplocirrus glaucus Phoronis muelleri Paradoneis armata

48.1 21.3 13.7 1.5 1.2 85.9

Diplocirrus glaucus Spiochaetopterus costarum Edwardsia claparedii Tubulanus polymorphus Paradoneis armata

31.6 19.0 7.2 5.9 5.2 68.9

Diplocirrus glaucus 40.6 Spiochaetopterus costarum 18.6 Paradoneis armata 8.1 Tubulanus polymorphus 3.5 Chaetozone setosa 2.7 73.6

T

1 2 3 4 5 R

Spiochaetopterus costarum Diplocirrus glaucus Paradoneis armata Chaetozone setosa Phoronis muelleri

40.8 18.2 6.9 3.3 3.0 72.3

Spiochaetopterus costarum Diplocirrus glaucus Chaetozone setosa Paradoneis armata Phoronis muelleri

30.4 19.3 8.5 6.2 3.1 67.5

Diplocirrus glaucus Edwardsia claparedii Tubulanus polymorphus Spiochaetopterus costarum Paradoneis armata

38.2 14.6 5.7 5.2 4.8 68.6

Diplocirrus glaucus 44.5 Paradoneis armata 6.9 Tubulanus polymorphus 6.7 Spiochaetopterus costarum 5.0 Edwardsia claparedii 4.1 67.2

X

1 2 3 4 5 R

Edwardsia claparedii Chamelea gallina Paradoneis armata Phoronis muelleri Spio decorata

12.6 12.4 6.6 2.6 2.4 40.6

Edwardsia claparedii Chamelea gallina Hyalinoecia bilineata Diplocirrus glaucus Fabulina fabula

22.6 8.9 4.5 4.2 4.2 44.3

Paradoneis armata Edwardsia claparedii Tubulanus polymorphus Lanice conchilega Thracia phaseolina

10.0 7.4 7.4 6.6 4.5 35.9

Paradoneis armata Spio decorata Tubulanus polymorphus Chamelea gallina Thracia phaseolina

20.6 7.5 5.3 5.3 4.7 43.5

PN

1 2 3 4 5 R

Paradoneis armata Spio decorata Chaetozone setosa Heterocirrus alatus Aricidea fragilis

26.6 16.3 7.8 6.8 6.1 63.6

Spio decoratus Paradoneis armata Chaetozone setosa Abra alba Scoloplos armiger

27.1 13.9 10.7 7.2 4.5 63.4

Spio decorata Paradoneis armata Chaetozone setos Marphysa bellii Abra alba

11.3 10.9 9.6 8.7 7.5 48

Ampelisca sarsi Paradoneis armata Polydora pulchra Spio decorata Chaetozone setosa

17.8 10.6 9.4 7.1 6.2 51.1

W

1 2 3 4 5 R

Paradoneis armata Fabulina fabula Diplocirrus glaucus Glycera tridactyla Chamelea gallina

8.9 7.7 6.8 6.4 5.6 35.4

Glycera trydactyla Fabulina fabula Nematoda Nephtys hombergi Nephtys cirrosa

12.1 12.1 8.4 7.3 6.1 46.1

Diplocirrus glaucus Mediomastus fragilis Tubulanus polymorphus Edwardsia claparedii Phoronis muelleri

32.1 6.3 6.3 5.2 4.3 30.5

Spio decorata 17.7 Diplocirrus glaucus 15.2 Pseudopolydora antennata 8.1 Spiophanes bombyx 6.5 Ampelisca spinimana 5.2 52.8

the end of the survey due to colonization by the amphipods. Nevertheless, at site X, there was a rapid increase of the ratio between t1 and t2. However, at these sites, there is great variability of the ratio values from one date to another related to polychaete recruitment especially in species such as Spio decorata or S. costarum. (iii) the PN site, where the ratio showed a rapid increase between t1 and t2, two main periods followed: t2± t28 with high values of the ratio in relation to the low abundance of amphipods, and t29±48, with decreasing values in relation to the increase of amphipods in decontaminated sediments. At the end of the survey, the ratio log10 (polychaetes/amphipods +1) was 1 showing that the abundances of amphipods was higher than those of the polychaetes. 1022

Discussion Benthic community structure can be altered by concentrations of petroleum hydrocarbons in the sediment <50 ppm, and some species may be excluded by concentrations <10 ppm (Kingston, 1992). In the Bay of Morlaix, hydrocarbon concentrations remained >50 ppm at RM site three years after the spill. A useful measure of the potential for toxic e€ects is the ER-L (E€ects Range-Low) sediment toxicity threshold of 4000 ng/g per total resolved PAH (Lee and Page, 1997). Two years after the Aegean spill, some areas of Rõa of Ares and Betanzos showed PAH concentration values >4000 ng/g. Concentrations of hydrocarbons in subtidal sediments of both sites were suciently high to a€ect macrobenthic communities: Amoco Cadiz (see Cabioch et al.,

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Fig. 5 Temporal changes in relative frequency of the total polychaetes abundance and the opportunistic polychaete abundances in the seven sites from t1 to t48 (t in months) after the spill (100% corresponds to the maximum, and the other values correspond the ratio between the observed abundances at each date and the maximum abundance 100).

1978; Dauvin, 1982, 1984, 1987, 1998, 2000), and Aegean Sea (see Mora et al., 1996a,b; Parra and L opez-Jamar, 1997; Gonzalez et al., 1997; Neira et al., 1997). Crustaceans The spill markedly a€ected the crustaceans. Some of them have been employed as indicator species, especially amphipods which have served as targets of biological and chemical monitoring. Among them, the genus Ampelisca showed a high sensitivity to toxins in the sediment (especially PCBs, pesticides, metals and PAHs) and has been chosen for di€erent toxicity testing meth-

Fig. 6 Temporal changes from t1 to t48 (t in months) in the ratio between the opportunistic polychaete abundance and the amphipod abundance ‡1, log10 scale for the ratio (each value is indicated by a bar, the line for each site is the mobile mean).

ods in estuarine and marine sediments (e.g., Ampelisca abdita, Ho et al. (1997); Carr et al. (1996)). Several papers have showed experimentally that amphipods are very sensitive to oil especially to aromatic components which have a high toxicity (e.g. Lee et al., 1977; Percy, 1977). Weathered oil appeared much less toxic than fresh oil. The most toxic components such as benzenes and naphthalenes must have already evaporated to the extent that the residual concentrations are not able to induce any signi®cant acute toxicity to the amphipod 1023

Marine Pollution Bulletin

population (Lee et al., 1980). Low molecular weight aromatics (one and two-ringed aromatics such as benzenes and naphthalenes) constituted the most volatile and water soluble fraction of crude oil and many petroleum products. These components have also been shown to be the more toxic fractions, so that after an accident, changes in chemical composition of oil take place rapidly and the weathered oil which reaches the bottom appears much less toxic than fresh oil. Another factor that can explain the high mortality of crustaceans (especially amphipods) is their placement on the sea bottom: `we suggest that the hydrocarbon material present in the ®ne ¯oc at the sediment±water interface is dicult to sample even with careful grabs or core sampling. Indeed as an example of the importance of surface ¯occulant material; and this fact may also account for the elimination of the benthic crustacean' (Boehm et al., 1982). High mortality of amphipods after an oil spill has been observed by several authors (e.g. Sanders et al., 1980; Elmgren et al., 1983; Dauvin, 1987). Lee et al. (1977) and Sanders et al. (1980) suggested that ampeliscid amphipods could be excellent indicators of oil pollution. Nevertheless, ampeliscids were not present in all soft-bottom communities, so all amphipods living in such communities could be considered as indicators of oil pollution (Swartz et al., 1982). For the hard bottom from the French Mediterranean coast, Bellan-Santini (1980) found an inverse relationship between the species richness and abundance of amphipods and the degree of pollution showing that C. acutifrons, Podocerus variegatus and Jassa falcata prefer more or less polluted water. Certain species were excluded by severe pollution whereas the abundance of some other species increased. For the soft-bottom communities, an inverse relationship appeared between species richness and abundance of amphipods, but observations proved that some species are favoured by organic, metallic or oil pollution (Bellan, 1980). The low colonization of the amphipods after the spill was due to their weak capacity for dispersion and their low fecundity (Dauvin, 1987). At the Pierre Noire site, the duration of colonization of a€ected populations after the spill reached 15 years. It was not until 1993 that Ampelisca showed similar high densities to those found before the pollution incident (Dauvin, 1998). In several cases, the duration of colonization of a€ected species after an oil spill surpassed 10 years (Smith, 1968; Laubier, 1991; Holloway and Horgan, 1991). The recovery rate of amphipods is slow but progressive. Polychaetes By contrast, polychaetes appeared to be resistant to high levels of hydrocarbons in sediment. In fact, after various disturbances, several changes were observed: (i) an increase in abundance of opportunistic taxa such as opportunistic polychaetes, oligochetes and nematodes and, (ii) a decrease and low abundance of the species 1024

considered to be sensitive to the pollution. A proliferation of opportunistic taxa has been documented after di€erent catastrophic releases, for instance (Sanders, 1980), found that the Florida oil spill resulted in a massive and immediate death of subtidal fauna of some sites, and after this total eradication of the benthic fauna these bottoms were occupied by the opportunistic polychaete C. capitata. Some months afterwards this species was replaced by a fewer less opportunistic species. Steichen et al. (1996) found that at natural oil seeps there was a negative relationship between most taxa and oil exposure, infaunal densities were very low in the most contaminated sites due to toxic e€ects, but higher abundances were found in surrounding sediments where bacterial decomposition of the oil took place providing a supply of organic carbon, these areas are typically dominated by deposit-feeding taxa. Glemarec and Hussenot (1981) also described a pattern of succession along gradients of organic material after the Amoco Cadiz oil spill, the recolonization time being dependent on initial hydrocarbon concentrations. At our sites where polychaetes dominated (RM, K), the e€ects of the spill were minimal because the number of sensitive species in natural conditions was low (Dauvin, 1982, 2000). At no sites was major proliferation of polychaete opportunists observed which compensated for the disappearance of the amphipods during the four ®rst years after the spill. Nevertheless, for the Bay of Morlaix, at the PN site, a temporary autumn increase in abundance of the Cirratulidae Heterocirrus alatus was observed in 1978 (Dauvin, 1984) and, at the RM site an increase in abundance of two opportunistic polychaetes: M. fragilis and T. marioni was also recorded (Dauvin, 1982). These responses of the macrobenthos are similar to those reported for the Braer oil spill, where Kingston et al. (1995) found that the e€ects of the oil spill were delayed [see also the Florida oil spill Sanders (1980) when a capitellid worm M. ambiseta bloom occurred 11 months after the spill]. A certain delay was observed with C. setosa in K site or D. glaucus in W site. On muddy stations (K an T), an `unbalanced stability A. alba community' described by Sanchez-Mata (1996) was found as an e€ect of perturbations by organic and minerals with the control in both estuaries (e.g., K and T sites) by two polychaetes D. glaucus and S. costarum (>50% of the macrobenthic individuals) This phenomenon occurred with and without pollution. Nevertheless, these results are not in accord with those of Parra and L opez-Jamar (1997) working in an area near the Aegean Sea wreck where they found an alteration in temporal cycles of several opportunistic species, mainly polychaetes such as C. capitata and Pseudopolydora cf. paucibranchiata, which proliferated just after the spill. Polychaete/amphipod ratio For macrobenthic polychaetes, Bellan (1980) suggested to use an Annelid Index of Pollution (or Pollu-

Volume 40/Number 11/November 2000

tion Index) based on the ratio of Ôpollution sentinel speciesÕ to that of the Ôpure water sentinel speciesÕ. This Pollution Index was tested for the French Mediterranean coast in unpolluted or moderately polluted zones (Bellan et al., 1988) and it was shown later (Lechapt et al., 1993) that the method can be usefully extended much further a®eld, e.g. the western Channel (Saint Malo Bay). Nevertheless, the selection of these species was made on annelids from hard bottoms, and these ratios could not be used eciently in muddy ®ne sand communities. So, we have tested di€erent ratios (polychaetes/crustaceans + 1, opportunistic polychaetes/ crustaceans + 1, and polychaetes/amphipods + 1) to identify the more ecient ratio for identifying oil impacts on soft-bottom communities. It appears that, for the more a€ected communities, the ratio opportunistic polychaetes/amphipods reveal temporal changes varying between low values (log10 (polychaetes/amphipods + 1) 61 in the absence of pollution) to high values >1 in stations when the amphipods disappeared completely (as at Pierre Noire site). Then the ratio decreases related to amphipod colonization. At the sites which were always dominated by polychaetes the ratio shows no change and remains stable after a pollution event (log10 (polychaetes/amphipods + 1) >1). The ratio can also be used to compare stations as PN, and RM in the English Channel and Galician sites. Similar thinking has been behind attempts to identify the e€ects of pollution on the meiobenthos. Ra€aelli and Mason (1981) suggested the usage of a nematode/ copepod ratio (N/C ratio). At PN site Boucher (1985) showed extremely high values of the ratio (45±65) just after the pollution event (April±May 1978) which demonstrated mortality for copepods (as amphipods) during the acute phase of toxicity with fast recovery. On beaches near the Amoco Cadiz wreck, Bodin (1988) showed that just after the Amoco Cadiz oil spill a drastic fall in densities occurred, particularly among the harpacticoid Copepoda, and an increase of the N/C ratio, con®rming that copepods are more sensitive than nematodes both to hydrocarbon toxicity and anoxia. This author suggested that for an ecological survey of the meiobenthos, it may be sucient to study only harparcticoid copepods. But, a warning was given against the use of the N/C which did not appear to be very useful for this long-term study. Moore and Stevenson (1997) reported that harpacticoid and amphipod abundances showed similar responses to pollution from gas platforms in the Gulf of Mexico. However, the N/C ratio is directly in¯uenced by granulometry which a€ects nematodes and copepods in di€erent manners, nematodes prefering mud and copepods sand. Warwick (1981) suggested that an indication of pollution might be given by ratios around 40 for mud and 10 for sand. These values are considerably lower than the values >100 suggested by Ra€aelli and Mason to be characteristic of polluted intertidal sites. Carman et al. (1997) examined the direct and indirect e€ects of

diesel-contaminated sediments on microalgae, meiofauna and meiofauna-microalgae trophic interactions. Microalgal activity was stimulated in high diesel concentration treatments. By contrast, high PAH concentrations eliminated copepods, and N/C ratios increased signi®cantly. The N/C ratio has provoked much discussion and controversy in recent literature. Lambshead (1984) raised the possibility that nematode and copepod populations may be in¯uenced independently by various ecological factors, perhaps including pollution, and that the simple ratio is inadequate and dicult to relate to environmental parameters. It will always be dicult to use a single index to identify the impact of oil pollution on soft-bottom communities, it was often necessary to have to administer complementary approaches. The presence or absence of amphipods, especially ampeliscids, should be an excellent test revealing the appearance of a disturbance in a community, and should be added to the repertoire of the existing techniques. The Bay of Morlaix study was carried out in the frame of the Programme GDR Manche, CNRS supported by IFREMER (RNO) contracts. The authors thank the captain and the crew of ÔNO MysisÕ, and sta€ of Marine Biological Station of Rosco€ in the ®eld work. Research of the Rõa de Ares and Betanzos was part of the projects: `Seguimiento de la macro y meiofauna bent onica intermareal y submareal de las rõas afectadas por el siniestro del petrolero Aegean Sea', supported by M.O.P.T.M.A. (Direcci on General de Polõtica Ambiental) and `Seguimento do estado dos fondos bent onicos submareais da Rõa de Ares e Betanzos a medio e longo prazo: estudio de series temporais 1988±1996' XUGA20008B95. The authors thank K. GHERTSOS for the English proof reading. Bellan, G. (1980) Relationship of pollution to rocky substatum polychaetes on the French Mediterranean coast. Marine Pollution Bulletin 11, 318±321. Bellan, G. (1984) Indicateurs et indices biologiques dans le domaine marin. Bulletin of the Ecology 15, 13±20. Bellan, G., Desrosiers, G. and Willsie, A. (1988) Use of an annelid pollution index for monitoring a moderately polluted littoral zone. Marine Pollution Bulletin 19, 662±665. Bellan-Santini, D. (1980) Relationship between populations of amphipods and pollution. Marine Pollution Bulletin 11, 224±227. Bodin, P. (1988) Results of ecological monitoring of three beaches polluted by the ÔAmoco CadizÕ oil spill: development of meiofauna from 1978 to 1984. Marine Ecology and Progressive Series 42, 105±123. Boehm, P. D. Judith, E., Barak, Fiest, L. D. and Elskus, A. A. (1982) A chemical investigation of the transport and fate of petroleum hydrocarbons in littoral and benthic environments: The Tsesis oil spill. Marine Environmental Research 6, 157±188. Bonsdor€, E. (1981) The Antonio Gramsci oil spill impact on the littoral and benthic ecosystems. Marine Pollution Bulletin 12, 301±305. Boucher, G. (1985) Long term monitoring of meiofauna densities after the Amoco Cadiz oil spill. Marine Pollution Bulletin 16, 328±333. Cabioch, L., Dauvin, J. C. and Gentil, F. (1978) Preliminary observations on pollution of the sea bed and disturbance of sublittoral communities in northern Brittany by oil from the ÔAmoco CadizÕ. Marine Pollution Bulletin 9, 303±307. Carman, R. K., Fleeger, J. W. and Pomarico, S. M. (1997) Response of a benthic food web to hydrocarbon contamination. Limnology and Oceanography 42, 561±571. Carr, R. S., Long, E. R., Herbert, L. W., Chapman, D. C., Thursby, G., Sloane, G. M and Wolfe, A. W. (1996) Sediment quality assessment studies of Tampa bay. Florida Environmental Toxicology and Chemistry 15, 1218±1231.

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Marine Pollution Bulletin Dauvin, J. C. (1982) Impact of Amoco Cadiz oil spill on the muddy ®ne sand Abra alba and Melinna palmata community from the Bay of Morlaix. Estuarine of the Coastal Shelf Science 14, 517±531. Dauvin, J. C. (1984) Dynamique dÕecosystemes macrobenthiques des fonds sedimentaires de la baie de Morlaix et leur perturbation par les hydrocarbures de lÕAmoco CadizÕ. These de doctorat Etat, es sciences, Universite de Paris VI, 456 pp+ annexes 192 pp. Dauvin, J. C. (1987) Evolution  a long terme (1978±1986) des populations dÕamphipodes des sables ®ns de la Pierre Noire (Baie de Morlaix, Manche Occidentale) apres la catastrophe de lÕAmoco Cadiz. Marine Environmental Research 21, 247±273. Dauvin, J. C. (1998) The ®ne sand Abra alba community of the Bay of Morlaix twenty years after the Amoco Cadiz oil spill. Marine Pollution Bulletin 36, 669±676. Dauvin, J. C. (2000) The muddy ®ne sand Abra alba±Melinna palmata community of the Bay of Morlaix twenty years after the Amoco Cadiz oil spill. Marine Pollution Bulletin. Elmgren, E., Hansson, S., Larsson, U., Sundelin, B. and Boehm, P. D. (1983) The ÔThesisÕ oil spill: acute and long term impact on the benthos. Marine Biology 73, 51±65. Feder, H. M. and Blanchard, A. (1998) The deep benthos of Prince William Sound, Alaska, 16 months after the Exxon Valdez oil spill. Marine Pollution Bulletin 36, 118±130. GESAMP (1991) The State of the Marine Environment. Oxford. Glemarec, M. and Hily, C. (1981) Perturbations apportees  a la macrofaune benthique de la baie de Concarneau par les e‚uents urbains et portuaires. Acta Oecologica, Acta Applicata 2, 139±150. Glemarec, M. and Hussenot, E. (1981) De®nition dÕune succession ecologique en milieu meuble anormalement enrichi en matieres organiques a la suite de la catastrophe de lÕAmoco Cadiz. In Amoco Cadiz: Cons equences d'une Pollution Accidentelle par les Hydrocarbures; Fates and E€ects of the Oil Spill, pp. 499±525. Centre National Pour LÕExploitation des Oceans, Paris. Gonz alez, J. J., Schultze, F., Esc anez, J. and Cerqueira, E. M. (1997) Distribuci on espacial y evoluci on anual en el agua submareal de los hidrocarburos poliarom aticos vertidos por el `Mar Egeo'. In Procesos biogeoquõmicos en sitemas coseros Hipano-Lusos, eds. R. Prego y J. M. Fernandez, pp. 137±141. Gundlach, E. R. and Hayes, M. O. (1977) The Urquiola Oil Spill, La Coru~ na, Spain: case history and discussion of methods of control and clean-up. Marine Pollution Bulletin 8, 132±136. Ho, K. T., Mckinney, R. A., Khun, A., Pelletier, M. C. and Burgess, R. M. (1997) Identi®cation of acute toxicants in New Bedford Harbor Sediments. Environmental Toxicology and Chemistry 16, 551±557. Holloway, M. and Horgan, J. (1991) Les marees noires. Pour la Science 170, 78±88. International Tanker Owners Pollution Federation (1996) Ocean Orbit. Ibanez, F. and Dauvin, J. C. (1988) Long term changes (1977±1987) in a muddy ®ne sand Abra alba±Melinna palmata community from the Western English Channel: multivariate time-series analysis. Marine Ecology and Progressive Series 49, 65±81. Jewett, S. C., Dean, T. A., Smith, R. O. and Blanchard, A. (1999) ÔExxon ValdezÕ oil spill: impacts and recovery in the soft-bottom benthic community in and adjacent to eelgrass beds. Marine Ecology and Progressive Series 185, 59±83. Kingston, P. F. (1992) Impact of o€shore oil production installations on the benthos of the North Sea. Journal of Marine Science 49, 45±53. Kingston, P. F., Dixon, I. M. T., Hamilton, S. and Moore, D. C. (1995) The Impact of the Braer oil spill on the macrobenthic infauna of the sediments o€ the Shetland Islands. Marine Pollution Bulletin 30, 445±459. Lambshead, P. J. D. (1984) The Nematode/Copepod ratio some anomalous results from the Firth of Clyde. Marine Pollution Bulletin 7, 256±259. Laubier, L. (1991) Les marees noires. Consequences  a long terme. La Recherche 22, 814±823. Lechapt, J. P., Bellan, G. and Retiere, C. (1993) Transposition en regime megatidal dÕune methode dÕevaluation des e€ets de perturbations anthropiques sur des peuplements annelidiens. Annales de Institut Oc eanographique 69, 225±237. Lee, W. Y., Welch, M. F. and Nicol, J. A. C. (1977) Survival of two species of amphipods in aqueous extracts of petroleum oils. Marine Pollution Bulletin 8, 92±94.

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