Using biotic indices to estimate macrobenthic community perturbations in the Bay of Brest

Estuarine, Coastal and Shelf Science (1997) 44 (Supplement A), 43-53

Using Biotic Indices to Estimate Macrobenthic Community Perturbations in the Bay of Brest J. Grall and M. Glemarec Uniuersite de Bretagne Occidentale, URA CNRS 1513, Oceanographic Biologique, Faculte des Sciences, 6 Avenue Victor Le Gorgeu, BP 809, 29285 Brest Cedex, France Shallow-water macrofaunaI communities have been studied in the Bay of Brest in order to estimate the impact of the main sources of urban, industrial, harbour and agricultural perturbations. Sampling stations were located on the shallow muddy grounds, between 0 and 5 m depth and in the estuaries. The analytic method of evaluation was based on the recognition of ecological groups of different sensitivity to organic matter overload. Their relative abundances allowed identification of stages of perturbation including eutrophication. The heavily polluted areas were easily identified in the northern basin, along Brest city and its harbour complex. With respect to the latter, opposite situations were shown for the northern and southern basins (the northern being eutrophicated). The double statistical analysis revealed that the first factor structuring the communities was anthropogenic perturbations, the second was the edaphic factor. © 1997 Academic Press Limited Keywords: marine eutrophication; biotic indices; benthic macrofauna

Introduction In a synthesis, largely inspired by the review of Pearson and Rosenberg (1978), Gray (1992) hierarchized the four main consequences of eutrophication on benthic organisms. The effects range from an increase in the growth rate of the organisms (Hily, 1984) to extreme symptoms of eutrophication with the disappearance of organisms due to anoxia. The two other consequences are: (1) a change in the composition of the communities, and (2) a reduction in the number of species following repeated hypoxia. In fact, the major goal of monitoring the health of an area is the early detection of effects of stress (Gray, 1989; Atkins & Jones, 1990). The Pearson and Rosenberg model (1978) used the synthetic parameters, species richness (S), abundance (A), and biomass (B), and identified a group of opportunistic species of universal character. Going beyond this work, and following Bellan (1967) in the Marseille area, the present authors' laboratory (Glemarec & Hily, 1981, Hily, 1984, Hily et al., 1986; Majeed, 1987) put in place a bioindicator model based on recognition, inside the spectrum of fauna in each kind of community, of groups of benthic invertebrates which give identifical responses with regard to the degree of enrichment by organic matter. The respective dominance of different groups along the declining oxygen gradient conditions defines the stages of degradation of the communities. Coupling this with the model of Pearson and Rosenberg (1978) permits 0272-7714/97/44A043+ 11 $25.0010

detection of initial signs of benthic communities perturbations. This multiple approach was developed in the Bay of Brest, a semi-enclosed environment with several potential sources of pollution. The first diagnosis of benthic system health readily obtained by this coupled method (biotic indices and synthetic parameters) may be used as the starting point of subsequent research on the identification and the quantification of sources of perturbation in the benthic ecosystem.

The site The semi-enclosed study area (Figure 1) is 180 km 2 • It is supplied by the Elom and Aulne rivers, which have a catchment of 2800 km 2 inhabited by 358 600 habitants. In these catchments, intensive pig, cattle and poultry breeding involves high amounts of some elements such as minerals and metals (phosphorus, copper, zinc). Nitrogen and phosphorus are used in large quantities to increase agriculture and production, particularly on intensive corn agriculture, and large amounts of herbicides are applied (Cann, 1995). Since the 1970s, a two-fold increase in nitrate loading is entering this ecosystem but phytoplankton stocks have not increased (Le Pape et al., 1995). In addition, water pollution comes from urban stormwater discharges and combined sewer outflows (Patris et al., 1995). So on a mass basis, heavy metals, oxygen demand, suspended solids and bacteria in urban

©

1997 Academic Press Limited

44

J. Grall & M. Glernarec

FIGURE 1.

Location of sampling stations in the Bay of Brest.

inputs are significant. Industrial activines, naval, commercial and leisure harbours are major sources of large amounts of hydrocarbons and heavy metals, including tributyl (Huet et al., 1995) .

Materials and methods

cu ssed further. The samples were filtered immediately on a sieve of mesh size 1 mm and fixed in a solution of 4 % formalin. The identifications were done in the laboratory after staining with Rose Bengal. The majority of the benthic invertebrates were identified to species, with the exceptions of Nemertea, Nematoda and Oligochaeta.

Field sampling To evaluate the ' health' of macrobenthic communities, the stations chosen were those adjacent to potential sources of pollution, i.e. the estuaries, urban outflows and industrial and port structures. Sampling was limited to tile shallow banks situated between o and 5 m. These banks represent one-third of the total surface of this bay. A first survey onboard the N /O Pluteus in October 1992 sampled 24 stations. With the same ship, five stations were re- visited in October 1993 (cf. 11 band 26 b), and six complementary stations were added in the northern basin (Stations 7-12). At each of these 33 stations, six samples of 0·1 m - 2 were taken with a Smith-Maclntyre grab. The 14 other stations concerned the estuarine parts and port zones (Penfeld, Elorn and Daoulas rivers). These were sampled in May 1993 onboard the N /O Palangrin with a smaller grab (Shipeck model) of 0·04 m - 2. So the sampling was biased by seasonal variation, grab size and configuration. This introduced variability will be dis-

Sediment data At each station, a sediment sample was taken to determine the granulometry. The 100 g sediment sample was dried at 80 °C for 24 h maximum, then it was washed with freshwater on a mesh of 63)lm (AFNOR). The dried residue was sieved on a column of 14 sieves (size 63-10000 urn) . The proportion of fine particles (the fraction smaller than 63 urn lost by washing) was taken as equal to the difference between the 100 g sample and the total weight of the sediment retained on the 14 sieves . Taking into account the three fractions [fine particles, sand grains (fine and coarse) and gravel] larger than 10000 urn, each sample was placed on a Shepard (1954) diagram (Figure 2). The sands are grouped in the upper part of this diagram, the muds in th e left inferior part and the mixed sediments in the centre. Different groups of stations on this diagram are classed in reference to the biosedimentary entities defined by Chasse and Glernarec (1976).

Biotic indices and macrobenthic community perturbations

45

are readily available in software developed at the laboratory by Le Bris (1988). Station specific richness was evaluated on the basis of the six grabs from each site, abundances expressed per m 2 and biomass as dry weight per m 2 •

Bio-indicator model

\

Gravels FIGURE 2. Triangular diagram of Shepard allows grouping of the stations in five large sedimentary units. FS, fine and silty; SM, sandy mud; MM, fine mud; HM, heterogeneous mud; MX, mixed sediments.

Data analysis Although benthic communrnes are distributed in a continuum along environmental gradients, it remains common practice to recognize discrete faunal assemblages and clustering techniques have been widely employed in benthic studies in order to delimit zones of faunal similarity. For these techniques, some species were deliberately excluded from the statistical analysis. From the list of identified species (n= 272), it was possible to narrow down the list of analysed species to 104, using two criteria conjointly. Firstly (Lebart et al., 1982), if the number of stations where a species was found was less than five, the species was eliminated. Secondly, species represented by less than 100 individuals were omitted from the whole sampling programme. For the hierarchical ascending classification (HAC) and the factorial correspondence analysis (FCA), the number of stations used was 49 and the number of species was 104. The HAC allows the identification of the groups of samples which are biologically similar. For that, it is necessary to calculate the coefficient of association based on the mean of the six samples obtained at each station. The average distance of Chi-square is the coefficient of association most suitable for quantitive data (Le Bris, 1988). This is the same distance that is used in the FCA. The calculations were carried out on logarithmic transformed data. These two techniques are complimentary, and

The model used here was first used close to the outlets and in the port of Concarneau (Glemarec & Hily, 1981), and subsequently applied in the northern basin of the Bay of Brest, close to the city and in the ports (Hily, 1984). Then this model was amended to different situations, notably for the beach communities after the Amoco-Cadiz oil spill (Majeed, 1987). The model is based on the recognition of five groups of species which present similar abundance profiles along the enrichment gradient by organic matter of the environment. These groups are defined below and their specific composition is given in Appendix A: Group I: Species very sensitive to organic enrichment and present in normal conditions. They include the specialist carnivores and some depositfeeding tubicolous polychaetes. Group II: Species indifferent to enrichment, always present in low densities with non-significant variations in time. These include suspension feeders, less selective carnivores and scavengers. Group III: Species tolerant of excess organic matter enrichment. These species may occur in normal conditions but their populations are stimulated by organic enrichment. These are only some of the surface-deposit-feeding species, for example tubicolo us spionids, which ingest the superficial film of organic matter deposited at the surface. Group IV: Second-order opportunistic species. These are the small species with a short life cycle, adapted to a life in reduced sediment where they can proliferate. They are the subsurface deposit feeders essentially related to the cirratulids. Group V: First-order opportunistic species. These are the deposit feeders that proliferate in sediments reduced up to the surface. Two species of polychaetes of universal distribution are typical of this group, Capitella capitata and Scolelepis (lvIalacoceros) juliginosa. Some nematodes and oligochaetes are also present. The distribution of these ecological groups according to their sensitivity to an excess of the organic matter provides for seven biotic indices (BI), which define different stages of community degradation. Previous

46

J.

Grall & M. Glernarec Biotic index 100%

6

o

2

4

90% 80% 70%

60 % 50% 40%

30% 20% 10%

Ecological groups

10 Group I

0 Group II

Group III • Group IV • Group

Vi

FIGURE 3. Degradation model of the benthic structures. For each station, the percentages of the respective five ecological groups are represented. The stations are regrouped according to these percentages and in function of the increasing Group I from left to right. Groups of stations are defined by a biotic index.

work has coupled the BI with organic carbon (Hily et al., 1986; Majeed, 1987). The biotic index reflects the dominance of the ecological groups: BlOis dominated by Group I; BI 2 by Group 3; BI 4 by Group 4; and BI 6 by Group 3. BI 1, 3 and 5 are transitional stages (ecotones as defined by Glernarec & Hily, 1981) and BI 7 corresponds to maximal pollution without macrofauna on the grounds.

Results Using the Shepard diagram (Figure 2), the stations were grouped as: (1) mixed sediments (MX) covered by maerl (Lithothamnium corallioides) overlying fine particles, sands and gravel in equal proportions; (2) sandy muds (SM) with less than 10% maerl and found mainly in the area of Lanveoc at Roscanvel or in l'Auberlac'h; (3) muds (MM) with more than 70% fine particles at river outflows, town effluents and inside the port structures; (4) heterogeneous muds (EM), a hybrid category contaminating the maerl bottoms and found in the area of the Bay of Daoulas;

and (5) fine muddy sands (FS) characterized by sand with fine particles « 30 %) in the external part of the northern basin facing the western swell, i.e, at Sainte-Anne, at the Caro or to the north of the Pointe de l' Armorique. Each station was characterized by a profile showing the relative proportions of the five ecological groups. The juxtaposition side by side of the 37 profiles with progressive permutation station by station will allow the establishment of the model of degradation of benthic communities. The progressive importance of Group I (sensitive species) is chosen as a guide for establishment of this model (Figure 3). This way, the model of Hily (1984) was rebuilt and enlarged to the whole Bay of Brest. Stations (Figure 4) in normal condition (BI 0) only existed in the Aulne basin. They were essentially the maerl bottoms (MX) on silt banks (Figure 4) where the sensitive species (Group I) dominate the population (>30%), followed by Group III (~25%), while Group IV is less than 10%. The other types of muddy habitats (FS, SM) and HM in this Aulne basin are characterized by the same index BI O.

Biotic indices and macrobenthic community perturbations

47

FIGURE 4. Map of the degradation of the benthic structures in the Bay of Brest. Each station is represented by its biotic index. Areas I, 1', II and II' are derived from the hierarchical ascending classification.

The stations where disturbance was indicated (BI 2=unbalanced) were found in the northern basin, notably the fine muddy sands where the hydrodynamic mixing limits the effect of the organic enrichment. Group III represented more than 40% of the community, whereas Group I was between 10 and 30% and Group N was less than 20%. The estuarine stations (Elorn and the River of Daoulas) were found in that grouping. They included the brackish fauna that is characteristic of the variable salinity but tolerant of the organic overload. When Group N dominated the community (4080%), the stations were considered to be polluted (BI 4). They were confined to the port areas of the northern basin, notably the mouth of the River Penfeld. It was also here that significant pollution, probably due to heavy metals in the harbour, was found (El 6). In the Bay of Brest, a characteristic group consisting of a mixture of Group I with the second-order opportunist group (Group N) was found. These two groups have equal abundance and therefore the double index 0-4 has been chosen for these stations. These were localized in the marine environment within the confines of the brackish water of the Aulne and the Elorn estuaries. The outflow of freshwater or sewage effluents, like those of the Quatre-Pompes (Station 20), can be identified by the double index.

In the establishment of this model, Ecotones 1, 3 and 5 were not taken into account as the low abundance did not allow the establishment of the relative proportions of the different groups in an acceptable manner. In the southern basin, Ecotone 1 was indicated by an abundance of less than 1000 individuals m - 2. Athough Ecotone 3 is rare, it was found at the Iroise bridge in the cove of Camfrout at the mouth of the estuary. Ecotone 5 was well represented and illustrates the action of the outfalls in the port zones of the northern basin; the Stang Alar stream, the outfalls at Moulin Blanc and close to Cale de Radoub and Cabliers port. Macrofauna were totally absent upstream in the Penfeld river (BI 7). The HAC (Figure 5) used on the density matrix gave rise to the two large groups (Groups I and II) identified by a similarity level defined by the average distance of Chi square less than 2230. A certain number of stations (Figure 4) did not belong to these two major groups but corresponded to the polluted muds of the port area with a BI 6 or BI 5 (Stations 5, 6, 11, 12 and 18). In the same way, the muds of Moulin Blanc were defined by Ecotone 5 (Stations 5 and 6). The muds of Rade Abri were characterized by BI 4. The muds in estuarine conditions (River Elorn) were characterized by Ecotone 3. In all these stations, the communities were unstructured, characterized by

48

J.

Grall & M. Glernarec 2

BI SENO.

16.57%

6W18:=============~=1=J 6 2 5 5 "

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VV E 2 - - - - - - - - '

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6---------,

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20-------.l

8M 2 6 B - - - - - - - - , VH29D------, VB 14 8M 10

2

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8M 7 0-48M 8 0-4VH27B 2 VH29C 0-48M29B 0-48M 9 0-48M 4A 0-4SM 4B 2 VH28B 2 VV 2 0-4 vrl 1 - - . . . r -- n 2 VV E l - - - - - '

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FIGURE 6. Correspondance analysis of the log transformed data. The station groups (---) and significant species (---) were taken into account for the relative and absolute contributions; with reference to the first two axes. The abbreviated names are given in Appendix A.

34

25

V8 2 4 - - - - ' FV FV FV

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FIGURE 5. Hierarchical ascending classification performed on the stations. The similarity dendrogram is based on the transformed log data. Two large groups (Groups I and II) are separated by the hierarchical ascending classification and two sub-groups can be identified. For each station, the biotic index (Bl) and the grouping is specified to a sedimentary entity (SE). a very low abundance (ecotonal situation) or dominated by opportunistic species; but without the appearance of any real similarities in terms of quality or quantity. All these stations revealed stressed communities. These samples were taken in a different season and with a different grab, but this double source of variation did not affect the statistical analysis, firstly because data were log-transformed and secondly because the seasonality was not important in these unstructured communities (Hily, 1984; Ros & Cardell; 1992). Isolation of Station 26B can be explained by its different epifauna community (abundant Pisidia longicomis), and isolation of Station 29 D was

due to the presence of brackish water species at this site. Group I was composed of the stations situated in the northern basin of the bay, and in the cove of Daoulas, Despite the sedimentological variability in this group, the degradation of the communities has to be recognized (BI 0-4; 2 or even 4 in the port complex). Group II is made up of all stations of the southern basin and by the external part of the cove of Daoulas (Stations 27 A, 28 A). The biotic indices revealed that the communities are in normal condition BI 0 or just a little affected in abundance (Ecotone 1). However, within Group II, Sub-group II' has been isolated, composed of stations localized at the outside of northern basin with unbalanced communities (BI2). To better quantify these apparent differences in the community health between northern and southern basins, seen by the individualization of Groups I and II, it is possible to subject stations belonging to these two groups to FCA. In order to minimize the influence of the sedimentological factors as much as possible; Sub-groups I' and II' and the Elorn muds

Biotic indices and macrobenthic community perturbations

49

TABLE 1. Summary of the bio-indicator model Biotic index 0 1 2 3 4 5 6 7

Dominating group I

III IV V No macrofauna

Benthic community health Normal Impoverished community (low abundance) Unbalanced community Transitional stage to pollution Polluted community Transitional stage to heavy pollution Heavy polluted community

were removed from this complementary statistical analysis. In the FCA, the first two axes (Figure 6) were the principal contributors to the total inertia (21'94% for Axis 1, 16·57% for Axis 2). The third, fourth and fifth axes contributed 10'61, 7·14 and 6,89%, respectively. Relative and absolute contributions with reference to these two first axes allowed the isolation of the station groups and significant species. Axis 1 isolated in positive values all the southern basin stations, i.e. Group II of the HAC, characterized by biotic indexes 0 and 1. The stations of the northern basin and of the Daoulas river (BI 0-4 and 2) fall in the negative values of this axis. The analysis of the significant species in the stations of the southern basin gives a range of sand/mud-dwelling polychaetes such as Terebellides stroemi, Glycera unicornis, Nematonereis unicomis, Scalibregma infimum, Phascolosoma vulgare, and the amphipods Amphithoe rubricata and Lysianassa ceratina, which indicates a healthy community. In the negative values of Axis 1, the second-order opportunists appear as well as tolerant species: Polydora ciliata, Polydora antennata, Prionospio malmgreni, Spio filicornis, Amphicteis gunneri, Polymnia nebulosa as sensitive species, or indifferent Ampharete grubei, Ophiodromus flexuosus, Phyllodoce maculata. Three species of amphipods: Ampelisca sp., Harpinia pectinata and Leucothoe incisa characterized the disturbed communities of the northern basin. Axis 2 isolated the stations of Group II of the HAC. Three groups of stations and species were distinguished. In the negative values of this axis, two maerl stations (26 and 23) were associated with the gravel-dwelling polychaetes: Eunice harassi, Hesione pantherina, Styarioides eruca, Staurocephalus rudolphii, and also the crustaceans: Maera grossimana, Melita gladiosa, Leucothoe spinicarpa, Lysianassa carinata, Jaera albijrons and Pisidia longicornis. Stations of mixed sediments or muds were grouped at intermediate values. In the positive values of Axis 2

it was possible to isolate cornmumnes found in the sandy and heterogeneous muds (24,27 B, 31 and 36). The characteristic species linked to this group were fine-particle-loving species which were intolerant of coarse material «20% of gravels), i.e. Thyasira flexuosa, Abra alba, Marphysa bellii, Notomastus latericeus, Poecilochaetus serpens. Axis 2 distinguished, among little affected communities, the muddy sediments from the mixed sediments, i.e. it illustrated the edaphic gradient from coarse to fine sediments. The FCA showed that the communities were first structured by the organic matter overload. Secondly, in the stations in good health, the edaphic factors remainded the major force structuring the communities. Table 2 summarizes the values of the synthetic descriptors S, A and B characterizing each stage of degradation. The unpolluted stations BI 0 have the maximum specific richness with an abundance of less than 2000 individuals m - 2. Degradation steps 2 and 0-4 were almost comparable. These first stages of disturbance due to the enrichment by organic matter were marked by an increasing abundance and biomass, and a reducing species richness compared to the , normal' situation. The polluted communities (Steps 4 and 6) see a rise in the abundance and a massive drop in the number of species and biomass. Index 4 is characterized by a still important biomass, partly explained by the 'heavy' cirratulids. The biomass data confirm the obvious affinities between Steps 2 and 0-4 shown by the two other descriptors. So, the first sign of degradation (imbalance) was clearly marked by biomass and abundance increases. Discussion

In terms of the community, stress is reflected by a change in qualitative and quantitative community composition. With opportunistic species, heavy

50

J.

Grall & M. Glemarec

2. Average values of synthetic descriptors and standard deviation (SD),established over the stations of the same biotic index

TABLE

6 Biotic index Abundance (ind m - 2) Species riches (by six grabs) Biomass (g dry weight m - 2)

0-4

4

2

0

Average

SD

Average

SD

Average

SD

Average

SD

Average

SD

17564

± 12065

4319

± 1357

2787

± 918

2581

±969

1874

± 586

15

±5

47

± 14

64

± 15

68

± 18

79

± 13

14

3

20

8

22

2

24

5

18

3

A, abundance m -2; S, specific richness established by six grabs station - '; B, biomass m - 2.

pollution is relatively easy to detect and many studies are related to highly enriched or polluted situations (see Reish, 1959; Bellan, 1967; Pearson & Rosenberg, 1978). Ros and Cardell (1992) have shown that it was possible to identify two groups of opportunistic species characterizing two different steps of altered structures of communities. This study has identified those groups as 'Groups V and IV', which include the leading species in the heavy polluted and polluted areas, respectively. In these areas of hypertrophy, microbial degradation of organic. matter can create permanent or transitory anoxic conditions. Concurrently, heavy metal concentrations can be responsible for toxicity. Groups IV and V can be considered relatively tolerant of both anoxic and toxic conditions. In the beginning of the 1980s, the detection of the initial effects of pollution on communities was a major goal of ecological research. Gray (1982) and Gray and Pearson (1982) compared the rank of abundance among species to find a distinction between the pattern obtained in unpolluted and polluted conditions. Plots of numbers of individuals per species against number of species (using geometric classes) showed clear trends. Warwick (1986) compared the rank of abundance and biomass among species with the ABC curves. These methods all suggest that the first phase of response to a stressor is that some species decrease in abundance and are eliminated; these can be considered as 'sensitive species'. In contrast, some moderately common species increase in abundance; these are the ' tolerant species'. With the sensitivity of multivariate techniques and ordination developed in the 1990s, detection of initial effects of eutrophication (for example) was easier. In response to chronic oil pollution, Gray et al. (1990) showed increased abundance patterns of species and changes in the presence and absence patterns of rare species. In this work, the recognition of tolerant

(Group III) and sensitive species (Group I) is implicit. The effects of low levels of organic enrichment are easy to detect and appreciate if Groups I and II are identified independently of the local sedimentary entities. The SAB method confirms that the first step of perturbation is clearly marked by biomass and abundance increases, and notably the development of Group III. Conversely, specific richness decreases. The coupling of two methods, BI and SAB, allows detection of the first sign of perturbation (BI 2 or 0-4). The statistical analyses are essential in validation of stations and species grouping, so they confirm the sensitivity of the BI method. With this method, it was possible to establish a relatively precise diagnosis of degradation and its distribution to discover local effects. This is not so evident with statistical methods. This global and structural method of biotic indices was analysed by Blandin (1988) who concluded that the empirical method, based on the recognition of ecological groups, was not always invalid. Indeed, empiricism disappeared progressively with time and more developed research. This global approach using groups is the only possibility when so little is known about the lifestyles of the numerous macrobenthic species in the marine coastal environment (close to 300 species in the present case). This method used in the Bay of Brest is evidence of significant degradation of the harbour complex where domestic and industrial effluents are added to the general eutrophication. When the communities were polluted to different degrees (BI 4 and 6), it was not possible to distinguish pollution by chemical products, heavy metals or hydrocarbons from eutrophication. However, when the communities were not greatly perturbed, the BI method revealed the first sign of eutrophication, due essentially to the agricultural inputs. These indices also differentiated the two basins. Oceanographic factors probably prevent the eutrophication effects in the southern basin.

Biotic indices and macrobenthic community perturbations

Acknowledgements This work was supported finacially by the Communaute Urbaine de Brest. The authors wish to thank J. Peron, G. Cohat, R. Marc and S. Dao for technical assistance and preparing the manuscript. Several colleagues are gratefully acknowledged for helpful discussions: L. Chauvaud, F. Jean, G. Thouzeau. Thanks to M. J. Costello and J. Wilson for critical review and language correction. References Atkins, M. S. & Jones, M. A. 1990 Studies on natural and anthropogenic influences on macrofauna of sandy shores at four sites in Orkney over a IS-year period. In Estuaries and Coasts: Spatial and Temporal Comparisons (Elliott, M. & Ducroroy, J. P., eds). ECSA Symposium, Olsen & Olsen, Fredensborg, pp. 139143. Bellan, G. 1967 Pollution et peuplements benthiques des substrats meubles de la region de Marseille. Revue Intemationale d'Oceanographie Medicale 6-7, 53-87. Blandin, P. 1988 Bioindicateurs et diagnostic des systernes ecologiques. Bulletin d'Ecologie 17, 257-272. Cann, C. 1995 Flux de nutriments d'origine agricole vers la rade de Brest. Ingenieries CEMAGREF Hors serie, 37-44. Chasse, C. & Glemarec, M. 1976 Principes generaux des cartes biosedimenraires. Journal de Recherche Oceanographique 1 No.3, 1-18. Glemarec, M. 1986 Ecological impact of an oil-spill: utilisation of biological indicators. IAWPRC-NERC Conference, July 1985. IA WPRC Journal 18, 203-211. Glemarec, M. & Hily, C. 1981 Perturbations apportees a la macrofaune benthique de la baie de Concameau par les effluents urbains et portuaires. Acra Oecologica, Oecologica Applicata 2, 139-150. Gray, J. S. 1982 Effects of polluants on marine ecosystems. Netherlands Journal of Sea Research 16, 424-443. Gray, J. S. 1989 Effects of environmental stress on species rich assemblages. Biological Journal of the Linnean Society 37,19-32. Gray, J. S. 1992 Eutrophication in the sea. In Marine Eutrophication and Population Dynamics (Colombo, G., Ferrari, I., Ceccherelli, V. & Rossi, R, eds). Olsen & Olsen, Fredensborg, 25th EMBS, pp.3-15. Gray, J. S. & Pearson, T. H. 1982 Objective selection of sensitive species indicative of pollution-induced changed in benthic communities. Marine Ecology Progress Series 9, 11-21.

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Gray, J. S., Clarke, K. R., Warwick, R. M. & Hobbs, G. 1990 Detection of initial effects of pollution on marine benthos: an example from the Ekofisk and Eldfisk oilfields, North Sea. Marine Ecological Progress Series 66, 285-299. Hily, C. 1984 Variabilite de la Macrofaune Benthique dans les Milieux Hypertrophiques de la Rade de Brest. These de Doctorat d'Etat, Universite de Bretagne Occidentale, Vol. 1, 359 pp., Vol. 2, 337 pp. Hily, C., Le Bris, H. & Glemarec, M. 1986 Impacts biologiques des emissaires urbains sur les ecosystemes benthiques. Oceanis 12, 419-426. Huet, M., Paulet, Y. M. & Glemarec, M. 1995 Tributyl (TBT) pollution in the coastal waters of west Brittany as indicated by imposex in Nucella lapillus. Marine Enuironmental Research 41, 157-167. Le Bris, H. 1988 Fonctionnement des Ecosystemes Benthiques au Contact des Estuaires la Rade de Lorient et la Baie de Vilaine. These de Doctorat de l'Universite de Bretagne Occidentale, Specialite: Oceanologie Biologique, Brest, 273 pp Le Pape, 0., Delarno, Y., Cann, C., Menesguen, A., Aminot, A., Queguiner, B. & Treguer, P. 1995 Reponse de la rade de Brest a l'augmentation des apports de sels nutritifs. Ingenieries CEMAGREF Hors serie, 103-110. Majeed, S. A. 1987 Organic matter and biotic indices on the beaches of North Brittany. Marine Pollution Bulletin 18, 490-495. Patris, T., Lefebvre, M., Troadec, L. & Laplanche, A. 1995 Pollution chimique et bacterienne dans les eaux de ruisselement pluvial sur Ie bassin versant du Stang Alar. Ingenieries CEMAGREF Hors serie, 51-58. Pearson, T. & Rosenberg, R 1978 Macrobenthic sucession in relation to organic enrichment and pollution of the marine environment. Oceanography and Marine Biology, Annual Review 16, 229-311. Reish, D. J, 1959 An ecological study of pollution in Los Angeles, Long Beach Harbors, California. Allan Hancock Foundation Public, Occasional Paper 22, 117 pp, Ros, J. & Cardell, M. J. 1992 Seasonal distribution of Polychaetes from a heavily polluted coastal area (Barcelona, NE Spain, NW Mediterranean). In Marine Eutrophication and Population Dynamics (Colombo, G., Ferrari, I., Ceccherelli, V. & Rossi, R, eds), Olsen & Olsen, Fredensberg, 25th EMBS, pp. 101-110. Shepard, F. P. 1954 Nomenclature based on sand-silt-clay ratios. Journal of Sedimentology and Petrology 24, 151-158. Warwick, R. M. 1986 A new method for detecting pollution effects on marine macrobenthic communities. Marine Biology 92, 557-562.

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J. Grall

& M. Glemnrec

Appendix A List of the species in the different ecological groups. Ecological Group I Acanthocardia echinata Acanthocardia paucicostata A canthochitona crinitus Acanthochitona fascicularis Achelia simplex Acrocnida brachiata Amaea trilobata Ampelisca breuicornis Ampelisca tou lem onti Ampharete grubei Amphipholis squamata Amphitrite johnstoni Ampithoe rubricate Anapagurus hyndmani Anomia ephippium Amhura gracilis Aora gracilis Apherusa cirrus Apherusa ovalipes Aponuphis grubei Aporrhais pespelicany Aricia latreilli Astacilia longicomis Athanas nitescens B alcis alba Bathyporeia sarsi B ranchiomma uesiculosum Calliostoma papillosum Calyptrea sinensis Ceradococus semiserratus Cereus pedunculatus Cerianthus membranaceus Chaetap terus uariopedatus Oheirocratus sp , Chlamys varia Circe minima Clymene lumbricoides Clymene modesta Clymene oerstedii Crangon crangon Cucumaria elongata Cultellus pellucidus Cyliehna cylindraeea Cymodoce truncata D en talium nouemcostatum

amg amr

aph

cas cep

do

Deuoniaperrieri Diodora apertura D iplocirrus glaucus Divarieella diuaricata Doris sp, Dosinia exolata Dosinia lupina Echinocardium cordatum Ensis sp . Euphrosyne foliosa Eurynome spinosa Galathea intermedia Galathea squamifera

eys

Gammaropsis sp , Gammarus insensibilis Gari depressa Gari feruensis Gari teilinella OJ'bbula magus Gnathia oxyurea Halcampa sp . H arpinia pectinata Helcion pellucidus Hippolyte varians Hyale nilsoni Hyatella artica Inachus dorsettensis Iphimedia obesa Iphinoe serrata Jaera albifrons Labidoplax digitata L ep tochiton asellus Leptochiton cancellatus Leptochiton squabridus Leptosynapta inhaerens Leucothoe incisa Leucothoe lilljeborgi Leucothoe richiardii Leucothoe spinicarpa Lilleborjia pallida Liocarcinus arcuatus Liocarcinus depurator Liocarcinus pusillus Listriella picta Loripes lucinalis Lucinoma borealis Lutraria lutraria Ly onsia noruegicum Lysianassa ceratina Lysianassa insperata Macoma baltica Macropodia rostrata Mactra corallina Maera grossimana Maera othon is Magelona alleni Maldane glebifex Melita gladiosa Metaphoxus pectinatus Microdeutopus anomalus Microdeutopus damnoniensis Microdeutopus uersiculatus Modiolus barbatus Modiolus gallicus Musculus discors Mysella bideniata Nucula nucleus Nucula turgida Ophelia bicornis Ophiocentru s brachiatus Op hiocomina nigra

gap

hap

Ophiotrix jragilis Ostrea edulis Palaemon serratus Pandora albida Panoploea minuta Parathelepus sp . Parvicardium exiguum Parvicardium ovale Parvicardium papillosum Pectinaria auricoma Pectinaria koreni

Phascolion strombi

jaa

lei leu

luI lyc mcs mae maa meg

Phascolosoma elongatum Phascolosoma v ulgare Phoronis psammophila Photis longicaudata Phoxocephalus rudolphii Phtisica marina Pilargis verrucosa Pilumnus hirtellus Pisidia longicornis Pista cristata Poecilochaetus serpens Processa canaliculata Proc/ea grajfii Quadrans serratus Sabella paoonina Sabellaria alueolata Scoloplos armiger Sipunculus nudus Solen marginatus Sphenia binghami Stylarioides eruca

phe phv

poe

ste

Telepsauus costarum Tellina donacina Tellina fabula Terebella lapidaria Terebellides stroemi Thalassema neptuni Tholarus cranch ii Thracia phaseolin a Thyone fusus

Tonicella marmorea Trivia monacha Tryphosella nanoides Tryphosella sarsi Upogebia deltaura

Urothoe poseidonis Urothoe puleh ella Venerupis aurea Venerupis pullastra

Venerupis rhomboides Venu s Venus Venus Venus

gallina ovata striatula verrucosa

tel tes

Biotic indices and macrobenthic community perturbations

53

Appendix A Continued Ecological groups Group II Drilonereis fi lum Eteone longa Eulalia sanguinea Eulalia sp. Eunice harassii Eunice oittata Glycera conooluta Glycera rouxii Glycera sp. Glycera unicomis Goniada maculata Haminoea navicula Harmothoe sp. Harmothoe spinijera Hermione hystrix Hesione pantherina Lagisca extenuata Lanice chonchylega Lepidonotus clava Lepidonotus squamatus Lumbrineris gracilis Lumbrineris impatiens Lumbrineris latreillei Lumbrineris sp. Lysidice ninetta Mangilia sp, Marphysa bellii Marphysa fallax Marphysa sanguinea Mystides limbata Nassarius incrassatus Nassarius reticulatus Natica alderi Natica catena Nematonereis unicornis Nephtys hombergii Nephtys hystricis Ocenebra erinacea Ophiodromusflexuosus Ophiura albida Philine aperta Pholoe minuta Pholoe synophtalmica Phyllodoce lamelligera Phyllodoce laminosa Phyllodoce maculata Polynoe scolopendrina

Psammolyce arenosa Sigalion mathildae Sthenelias boa Sthenelias minor Syllis prolifera

eus euh

gls

heh hep

Group III Abra alba Abra tenuis Amphicteis gunneri Aonides oxycephala Apseudes latreillei Carcinus maenas Cerastoderma edule Cerastoderma lamarcki Corophium sp, Crepidula[ornicata Cyathura carinata Dexamine spinosa Gammarella fucicola Laonice cirrata Leptocheirus pectinatus

aba amu

erf

Group IV Audouinia tentaculata Chaetozone serosa Cirratulus cirratus Heterocirrus bioculatus Nerds caudata Polycirrus aurantiacus Polydara antennata Polydora caeca Polydora ciliata Polydora polybranchia Prionospio malmgreni Staurocephalus rudolphii

Leptonereis glauca

Melinna palmata Nereis diuersicolor

mep

Nereis longissima

Ius mab

neu

phy pym

syl

Notomastus latericeus Paradoneis armata Perinereis cultrifera Platynereis dumerilii Polymnia nebulosa Pygospio elegans Scalibregma infimum Spio filicornis Spiophanes bombyx Spiophanes kroyeri Sternaspis scutata Thyasira flexuosa

nol

pon pyl sci spf

thf

Group V Capitella capitate Nebalia bipes Scolelepisfuliginosa

poa poi prm