a Marine Biotic Index To Establish The Ecological - ECASA · A Marine Biotic Index to Establish the...

A Marine Biotic Index to Establish theEcological Quality of Soft-BottomBenthos Within European Estuarine andCoastal EnvironmentsA. BORJA*, J. FRANCO and V. P�EREZDepartment of Oceanography and Marine Environment, Technological Institute for Fisheries and Food (AZTI),Av. Satr�ustegui 8, 20008 San Sebasti�an, Spain

In this paper, a marine Biotic Index (BI) for soft-bottombenthos of European estuarine and coastal environments isproposed. This is derived from the proportions of indi-vidual abundance in ®ve ecological groups, which are re-lated to the degree of sensitivity/tolerance to anenvironmental stress gradient. The main di�erence withpreviously published indices is the use of a simple formulathat produces a continuous Biotic Coe�cient (BC) ±which makes it more suitable for statistical analysis, inopposition with previous discreet biotic indices ± not af-fected by subjectivity. Relationships between this coe�-cient and a complementary BI with several environmentalvariables are discussed. Finally, a validation of the pro-posed index is made with data from systems a�ected byrecent human disturbances, showing that di�erent an-thropogenic changes in the environment can be detectedthrough the use of this BI. Ó 2000 Elsevier Science Ltd.All rights reserved.

Keywords: biotic index; ecological quality; diversity;benthos; soft-bottom; European coastal environments.

Introduction

Marine environmental quality control is undertakenusually by means of monitoring di�erent parameters inwater, sediment and sentinel organisms (i.e. MusselWatch), as in the USA (OÕConnor, 1992), France (RNO,1998) or Great Britain (Franklin and Jones, 1994). Thiscontrol is centred on physico-chemical and ecotoxico-logical variables and, less usually, on biological vari-ables. Dauer (1993) stated that biological criteria areconsidered important components of water quality be-cause: (i) they are direct measures of the condition of the

biota, (ii) they may uncover problems undetected orunderestimated by other methods; and (iii) such criteriaprovide measurements of the progress of restoratione�orts.

New European rules (see Directive Proposal 1999/C343/01, O�cial Journal of the European Communities30/11/1999) emphasize the importance of biological in-dicators, in order to establish the ecological quality ofEuropean coasts and estuaries. Benthic invertebrates areused frequently as bio-indicators of marine monitoring,because various studies have demonstrated that macro-benthos responds relatively rapidly to anthropic andnatural stress (Pearson and Rosenberg, 1978; Dauer,1993).

River ecology has an established long tradition inapplying macrobenthos as bio-indicators; likewise somebiotic indices have been proposed (Woodiwiss, 1964;Cairns et al., 1968; Chandler, 1970; ISO-BMWP, 1979,etc.). On the other hand, some attempts to provideuseful `tools' to measure ecological quality in the marineenvironment have been developed in Europe and NorthAmerica (Hily, 1984; Majeed, 1987; Dauer, 1993; Gralland Gl�emarec, 1997; Weisberg et al., 1997).

All the aforementioned studies utilize soft-bottomcommunities to construct the indices, because macro-benthic animals are relatively sedentary (and cannotavoid deteriorating water/sediment quality conditions),have relatively long life-spans (thus, indicate and inte-grate water/sediment quality conditions, with time),consist of di�erent species that exhibit di�erent toler-ances to stress and have an important role in cyclingnutrients and materials between the underlying sedi-ments and the overlying water column (Hily, 1984;Dauer, 1993).

In this contribution, a marine Biotic Index (BI) isdesigned to establish the ecological quality of Europeancoasts. This explores the response of soft-bottom com-munities to natural and man-induced changes in waterquality, integrating long-term environmental conditions.

Marine Pollution Bulletin Vol. 40, No. 12, pp. 1100±1114, 2000

Ó 2000 Elsevier Science Ltd. All rights reserved

Printed in Great Britain

0025-326X/00 $ - see front matterPII: S0025-326X(00)00061-8

*Corresponding author.E-mail address: [email protected] (A. Borja).

1100

Methods

SamplingThe Department of Land Action, Housing and

Environment of the Basque Government has establisheda network of monitoring stations along the Basquecoast-line (North of Spain). This provides water, sedi-ment and biological quality information from 30 sam-pling stations (Fig. 1). The benthic sampling has beencarried out every February, from 1995 to 1998 using theresearch vessel `Ortze'.

At each of these stations, three replicates of benthoswere collected with a Van Veen grab (1215 cm2). Thesamples were ®ltered immediately, using a sieve of meshsize of 1 mm and ®xed in a solution of 4% formalin(Holme and McIntyre, 1971).

Sediment dataAt each station, a sediment sample was obtained to

determine redox potential, organic matter content andcontaminant levels (heavy metals and organic com-pounds). The redox potential was measured, on board,by means of an Orion 977800 platinum electrode whichwas connected to a Crison 501 pH-meter-milivoltimeter.

A 200 g sediment sample was dried at 80°C for 24 h,then it was washed with freshwater on a mesh of 63 lm.The dried residue was sieved on a column of eight sieves(size 31 lm to 4 mm). The percentages of gravel, sandand mud were calculated as: >2 mm fraction, 63 lm ± 2mm and <63 lm, respectively (Holme and McIntyre,1971).

The organic matter content was calculated by the losson ignition method: drying at 105°C, 24 h; then com-busting at 520°C, 6 h (Kristensen and Anderson, 1993).

Metal concentrations (As, Cd, Cu, Cr, Hg, Ni, Pb andZn) were analysed on the <63 lm fraction. Extractionwas made ®rst with nitric acid, during 15 h, at ambienttemperature; and second, with nitric and hydrochloricacids (1:3 in volume), using a microwave oven (130 W,4 min; 0 W, 1.5 min; 250 W, 5 min; 0 W, 2 min; 400 W,4 min). Detection was made by atomic absorption, using¯ame, graphite furnace and cold vapour techniques. Theanalytical procedure was checked with reference mate-rial (BCR marine sediment-harbour PACS-1); di�er-ences with this material were lower than 10%.

For PCB (eight congeners), DDT and HCH deter-mination a portion of the original sample was desiccatedwith anhydrous sodium sulphate and extraction wasmade with iso-octane, after conditioning and clean-up ofthe extract the analysis was made with an HP-5890 gaschromatograph. On the other hand, for PAH (10 com-pounds) determination, the extraction was made withether, and the analysis was made by means of HPLC.

Water quality dataThe mean bottom oxygen concentration was mea-

sured with a CTD Sea-Bird 25, or with a portable YSI-

55 oxymeter. Salinity was measured with the same CTD,or with a Kahlsico SR10 induction salinometer.

Biological dataThe identi®cation was undertaken in the laboratory

by means of a binocular microscope (4±40�). Aftercomputing the mean abundance of each taxon, at eachsampling station, the macrobenthic community struc-ture was described calculating the following descriptors(Washington, 1984): richness (number of identi®edtaxa); abundance (N: ind mÿ2); numerical diversity(Shannon Wiener H0n: bits indÿ1); biomass (Dry Weight,B: g mÿ2); and biomass diversity (Shannon Wiener H0b:bits gÿ1).

BI modelThe model here developed is based on that ®rst used

by Gl�emarec and Hily (1981) and then by Hily (1984),which utilizes soft-bottom benthos to construct a BI.

Soft-bottom macrobenthic communities respond toenvironmental stress (i.e. the introduction of organicmatter in the system) by means of di�erent adaptivestrategies. Gray (1979) summarizes these strategies intothree ecological groups: r (r-selected: species with shortlife-span, fast growth, early sexual maturation and lar-vae throughout the year); k (k-selected: species withrelatively long life, slow growth and high biomass); andT (stress tolerant: species not a�ected by alterations).

Salen-Picard (1983) has proposed four progressivesteps relating to stressed environments: (i) initial state(in an unpolluted situation, there is a rich biocenosis inindividuals and species, with exclusive species and highdiversity); (ii) slight unbalance (regression of exclusivespecies, proliferation of tolerant species, the appearanceof pioneering species, decrease of diversity); (iii) pro-nounced unbalance (population dominated by pollutionindicators, very low diversity); and (iv) azoic substrata.

Following these four steps, Hily (1984) and Gl�emarec(1986) have stated that the soft-bottom macrofaunacould be ordered in ®ve groups, according to their sen-sitivity to an increasing stress gradient (i.e. increasingorganic matter enrichment). Their concept is similar tothat developed for the Infaunal Index for SouthernCalifornia, described by Mearns and Word (1982) andFerraro et al. (1991). These groups have been summa-rized by Grall and Gl�emarec (1997), as outlined below.

Group I. Species very sensitive to organic enrichmentand present under unpolluted conditions (initial state).They include the specialist carnivores and some deposit-feeding tubicolous polychaetes.

Group II. Species indi�erent to enrichment, alwayspresent in low densities with non-signi®cant variationswith time (from initial state, to slight unbalance). Theseinclude suspension feeders, less selective carnivores andscavengers.

Group III. Species tolerant to excess organic matterenrichment. These species may occur under normalconditions, but their populations are stimulated by

1101

Volume 40/Number 12/December 2000

Fig.1

Positionofthe30stationsmonitoredalongtheBasquecoast-

line(N

orthofSpain),from

1995to

1998.Thestationsusedto

validate

themodel

are

shownin

black.

1102

Marine Pollution Bulletin

organic richment (slight unbalance situations). They aresurface deposit-feeding species, as tubicolous spionids.

Group IV. Second-order opportunistic species (slightto pronounced unbalanced situations). Mainly smallsized polychaetes: subsurface deposit-feeders, such ascirratulids.

Group V. First-order opportunistic species (pro-nounced unbalanced situations). These are deposit-feeders, which proliferate in reduced sediments.

The distribution of these ecological groups, accordingto their sensitivity to pollution stress, provides a BI witheight levels, from 0 to 7 (Hily, 1984; Hily et al., 1986;Majeed, 1987).

In the aforementioned monitoring network of sam-pling stations, together with other studies developed byAZTI along the Basque coastline within the last ®veyears (Borja et al., 1995, 1999a,b), more than 900 taxahave been identi®ed. These species are representative ofthe most important soft-bottom communities present atEuropean estuarine and coastal systems. The taxa havebeen classi®ed (list in Appendix A) according to theabove ecological groups, following Majeed (1987),Dauer (1993), Weisberg et al. (1997), Grall andGl�emarec (1997) and Roberts et al. (1998). Only about

12% of the taxa have not been possible to be assigned toan ecological group.

Based upon HilyÕs model (Hily, 1984; Hily et al., 1986;Majeed, 1987), Fig. 2 shows the theoretical distributionof relative abundance of each ecological group, along apollution gradient.

A possible limitation in the utilisation of the model ofHily is that each BI has a discreet value and its calcu-lation is not systematized. In order to improve the index,a single formula is proposed here. This is based upon thepercentages of abundance of each ecological group,within each sample, to obtain a continuous index (theBiotic Coe�cient (BC)), where

Biotic Coefficient � f�0�% GI� � �1:5�% GII�� 3�% GIII� � �4:5�% GIV�� 6�% GV�g=100:

The above-mentioned ecological groups (GI, GII,GIII, GIV and GV) are summarized in Table 1. Speciesnot assigned to a group were not taken into account.These species represent only a mean abundance of 1.4%,for the total number of samples.

In this way, use of the BC can derive a series ofcontinuous values, from 0 to 6, being 7 when the sedi-ment is azoic. Nonetheless, the BC can be compared tothe Grall and Gl�emarec (1997) BI, as adapted in thispaper (Table 1). The result obtained is a `pollutionclassi®cation' of a site which is a function of the BC.Consequently, this represents the benthic community`health', represented by the entire numbers of the BI.

Results

The mean and standard error values of grain size andphysical characteristic associated with each of the sam-pling stations (17 estuarine and 13 littoral) are listed inTable 2. The water depth range is very large at each ofthe stations (under Mean High Water Neap to 24 m inthe estuaries and 30±35 m associated with the littoralsamples). Mean salinity, at bottom water, ranges from16.2 to 35.3 in estuaries, but is restricted within thecoastal areas (35.3±35.5).

The range in the percentage of oxygen saturation isvery high within the estuaries (43±119%), but ranges inthe littoral stations from 92% to 97%. The organic

Fig. 2 Theoretical model, modi®ed from Hily (1984), Hily et al. (1986)and Majeed (1987), which provides the ordination of soft-bottom macrofauna species into ®ve ecological groups (GroupI: species very sensitive; Group II: species indi�erent; GroupIII: species tolerant; Group IV: second-order opportunisticspecies; Group V: ®rst-order opportunistic species), accordingto their sensitivity to an increasing pollution gradient. Therelative proportion of abundance of each group in a sampleprovides a discreet BI with eight levels (0±7) and an equivalentcontinuous BC (values between 0 and 6).

TABLE 1

Summary of the BC and BI (modi®ed from Grall and Gl�emarec, 1997).

Site pollution classi®cation Biotic Coe�cient Biotic index Dominating ecological group Benthic community health

Unpolluted 0:0 < BC � 0:2 0 I NormalUnpolluted 0:2 < BC � 1:2 1 ImpoverishedSlightly polluted 1:2 < BC � 3:3 2 III UnbalancedMeanly polluted 3:3 < BC � 4:3 3 Transitional to pollutionMeanly polluted 4:5 < BC � 5:0 4 IV±V PollutedHeavily polluted 5:0 < BC � 5:5 5 Transitional to heavy pollutionHeavily polluted 5:5 < BC � 6:0 6 V Heavy pollutedExtremely polluted Azoic 7 Azoic Azoic

1103


matter content in the sediments is higher in the estuaries(2.3±28.2%) than in littoral zone (3.4±6.8%). This cor-responds to a higher range of the mud content within thesediments (0.3±80.1% and 0.1±17.3%, respectively). Theredox potential ranges from )185 to 410 mV within theestuaries, and from )84 to 405 mV within the littoralsamples.

From 30 stations, some 114 samples of benthos havebeen obtained over a 4 year period. These samplescorrespond to di�erent environments (estuarine, littoral,intertidal, subtidal) and physico-chemical characteristics(reduced and oxidized sediments, hypoxia and oversat-uration in the bottom waters, poor organic matterproportion and enrichment, etc.).

After the application of the BC, considering its cor-respondence with the BI (Table 1), the results were: 2samples with a BI� 0; 23 samples of BI� 1; 48 samplesof BI� 2; 15 samples of BI� 3; 7 samples of BI� 4; 6samples of BI� 5; 6 samples of BI� 6; and 7 samples ofBI� 7.

Fig. 3 shows the results obtained by comparing dif-ferent biological parameters, on samples having thesame biotic indices. The BI� 7 is equivalent to an azoicsite, so all the biological parameters are equal to 0 inthese particular samples.

The mean abundance increases from 36.7 ind mÿ2

(BI� 0) to 2 559 ind mÿ2 (BI� 6), with the exception ofBI� 5, with a value of 456 ind mÿ2 (Fig. 3(a)). Withinthe lowest of the Biotic Indices (0, 1 and 2), the standarderror of the mean is very small; it is progressively largerin the highest.

Statistical analyses were made considering the BCbecause, as this coe�cient can derive continuous values,it is more suitable for this purpose than the BI. Takinginto account all the samples analysed, the non-para-metric Spearman rank correlation between the abun-dance and the BC is not statistically signi®cant(p > 0:05).

On the other hand, biomass (Fig. 3(b)) increases from0.1 g mÿ2 (BI� 0) to 14.3 g mÿ2 (BI� 4). However forBiotic Indices 5 and 6, dominated by small opportunisticspecies, the biomass is lower than 4 g mÿ2. There is no astatistically signi®cant correlation between biomass andBC (Spearman rank correlation).

Fig. 3(c) shows the mean richness of the samples.Except in the case of BI� 0, with a mean richness of 2,in the other biotic indices the richness decreases pro-gressively from 26 to 27 species (BI� 1 and 2) to 0species (BI� 7). Richness and BC are highly correlated(p < 0:001, Spearman rank correlation).

TABLE 2

Physico-chemical characterisation of sampling stations, showing mean and standard error (SE) values of some sedimentological and waterparameters.a

Stationnumber

Stationtype

Depth(m)

Salinity Dissolvedoxygen (ml lÿ1)

% Oxygensaturation

% Sand % Mud % Organicmatter

Redoxpotential (mV)

Mean Mean� SE Mean� SE Mean� SE Mean� SE Mean� SE Mean� SE Mean� SE

1 E I 23:5� 2:3 6:1� 0:2 101� 3:8 95:1� 3:8 4:6� 4:0 5:2� 0:2 296� 41:72 E 3 16:2� 2:0 3:1� 0:5 43� 6:0 38:5� 6:3 47:7� 6:2 8:7� 1:0 ÿ101� 38:23 E 14 35:1� 0:1 5:0� 0:1 87� 1:7 19:6� 2:1 80:1� 2:1 13:0� 0:3 ÿ53� 37:74 E 24 35:3� 0:1 5:4� 0:1 94� 1:3 80:7� 4:6 18:3� 4:8 6:0� 0:4 153� 45:25 L 34 35:3� 0:1 5:6� 0:1 96� 1:7 96:3� 0:8 3:3� 0:9 3:9� 0:3 248� 45:56 L 32 35:3� 0:1 5:5� 0:1 95� 1:7 94:8� 3:2 0:4� 0:2 6:8� 1:7 405� 18:27 E I 29:5� 1:6 6:1� 0:2 105� 3:3 85:3� 2:4 0:5� 0:2 2:3� 0:1 388� 18:78 L 34 35:4� 0:0 5:5� 0:1 95� 1:5 81:5� 6:7 0:7� 0:5 3:8� 0:8 389� 7:29 L 33 35:4� 0:0 5:5� 0:1 96� 2:0 98:4� 0:2 1:1� 0:2 3:4� 0:4 322� 26:910 E I 25:7� 2:5 6:1� 0:2 102� 3:3 27:4� 2:9 64:8� 4:2 7:7� 0:4 25� 20:211 E I 34:8� 0:1 6:6� 0:2 119� 3:3 97:6� 1:3 0:3� 0:3 3:4� 0:5 410� 45:012 L 31 35:5� 0:0 5:6� 0:1 97� 1:8 95:6� 0:8 3:6� 0:8 3:6� 0:7 268� 43:813 E I 26:3� 3:0 6:5� 0:2 111� 3:1 82:4� 4:8 12:5� 3:9 4:6� 0:7 167� 50:414 L 34 35:5� 0:0 5:6� 0:1 96� 2:0 93:8� 2:3 5:4� 2:3 3:7� 0:3 299� 34:515 E I 28:9� 1:6 5:0� 0:3 87� 3:9 38:6� 3:1 16:7� 2:6 6:1� 0:5 0� 32:316 L 34 35:4� 0:1 5:3� 0:3 94� 3:4 94:3� 3:5 0:1� 0:1 3:7� 0:6 336� 11:517 E I 17:5� 2:7 5:9� 0:2 89� 3:7 55:8� 5:8 40:3� 6:8 6:7� 0:6 63� 48:918 L 32 35:4� 0:1 5:4� 0:1 94� 1:8 95:1� 1:0 3:3� 1:0 4:2� 0:1 264� 37:219 E I 23:3� 2:2 5:8� 0:2 96� 2:9 40:1� 5:2 51:3� 5:6 9:0� 0:7 24� 21:320 L 32 35:4� 0:0 5:3� 0:1 93� 2:0 84:8� 6:5 8:7� 6:7 5:5� 1:2 286� 39:021 E I 21:1� 2:2 6:0� 0:2 97� 3:0 85:3� 5:0 7:4� 4:8 4:0� 0:6 313� 38:022 L 32 35:4� 0:1 5:4� 0:1 95� 2:0 86:2� 2:9 11:0� 2:7 3:8� 0:2 83� 18:123 E I 21:1� 3:1 5:7� 0:3 92� 5:2 84:2� 5:8 5:4� 4:1 4:2� 1:3 210� 49:324 L 34 35:4� 0:0 5:5� 0:1 95� 2:3 81:6� 4:2 17:3� 4:3 5:0� 0:6 ÿ84� 45:425 E 9 34:0� 0:2 3:2� 0:3 55� 4:9 36:7� 7:6 59:9� 8:8 28:2� 2:8 ÿ185� 8:026 E 8 33:3� 0:4 5:0� 0:2 88� 3:7 46:8� 6:7 36:0� 7:6 9:4� 1:0 ÿ71� 21:927 L 32 35:4� 0:0 5:3� 0:1 92� 2:2 89:1� 4:7 3:4� 2:2 3:4� 0:5 240� 53:028 E I 19:3� 2:3 5:2� 0:3 83� 4:4 80:8� 5:0 13:7� 5:2 5:0� 1:0 102� 35:129 E I 26:2� 1:6 5:6� 0:2 91� 4:6 91:9� 2:2 0:7� 0:3 2:7� 0:1 285� 32:030 L 33 35:3� 0:1 5:5� 0:1 97� 2:1 89:0� 5:7 6:4� 5:5 5:8� 1:8 232� 61:4

a E: estuarine site; L: littoral site; I: intertidal site.

1104


Numerical diversity (Fig. 3(d)) shows a similar patternto that of richness. There is a progressive decrease in themean values, from 3.5 bits indÿ1 (BI� 1) to 0 bits indÿ1

(BI� 7), with the exception of BI� 0 which is associatedwith a low value (0.6 bits indÿ1). Biomass diversity hasvalues of about 1.6 bits gÿ1, between BI� 1 to 4; then, itdecreases to 0 (BI� 7). Both variables are correlatedwith BC (p < 0:001 and p < 0:05 for numerical andbiomass diversities, respectively), using Spearman rankcorrelation.

The relationships between some of the sedimento-logical and water quality parameters and biotic indices

are shown in Fig. 4. BI� 0 is associated with the highestmean redox potential (Fig. 4(a): 360 mV). This param-eter becomes progressively lower, with BI� 7 having amean potential which is very reduced (±125 mV). Sam-ples with low biotic indices (0 and 1) are associated withless than 2% of mud (Fig. 4(b)) and the values increaseto 63% (BI� 7). Some anomalies were detected inBI� 5 and 6, which present 10±20% of mud. The or-ganic matter content has a similar pattern of distribu-tion to that of granulometry (Fig. 4(c)). Data on themean bottom dissolved oxygen content are presented inFig. 4(d). The highest value corresponds to BI� 0

Fig. 4 Mean and standard error values of di�erent sedimentologicaland water quality parameters obtained on samples having thesame biotic indices. (a) redox potential; (b) percentage of mud;(c) organic matter content; and (d) bottom dissolved oxygencontent.

Fig. 3 Mean and standard error values of di�erent biologicalparameters obtained on samples having the same biotic indices.(a) abundance; (b) biomass; (c) richness; and (d) diversity(derived from number of individuals N and biomass B).

1105


(6.5 ml lÿ1), decreasing to 2.6 ml lÿ1 at BI� 7. TheSpearman rank correlations between these variables andBC are highly signi®cant (p < 0:001).

The mean concentrations relating to some of theheavy metals in the sediments associated to each BI areshown in Fig. 5. Arsenic and mercury contents do notreveal any clear pattern of distribution with the BI.Other metals present increasing concentrations fromBI� 0 to BI� 7, with the exception of some speci®cpeaks (BI� 3, for chromium and nickel; and BI� 6, forlead and copper) and troughs (BI� 4 and 5, for cad-mium, nickel and zinc). Except arsenic and mercury allthe metals are positively correlated with BC (p < 0:01,Spearman rank correlations).

On the other hand, the organic compounds (Fig. 6) donot show a similar pattern to that of the metals. OnlyPCB increase in their concentrations from BI� 0 toBI� 7; however the di�erences are very small. PAH is attheir smallest concentrations in BI� 5 and 6. The onlysigni®cant correlation is found between BC and PCB(p < 0:05, Spearman rank correlation).

Comparing the percentage of samples of each BI thatgoes beyond the ER-L (or E�ects Range-Low, repre-senting concentrations below which adverse e�ects tofauna are expected to occur rarely (Long et al., 1995)),the data presented in Fig. 7 shows that BI� 0 does notinclude samples that surpass these limits for metals andorganic compounds. Normally, the other biotic indices

Fig. 5 Mean and standard error values of eight heavy metal contentsin sediments obtained on samples having the same bioticindices.

Fig. 6 Mean and standard error values of four organic compoundcontents in sediments obtained on samples having the samebiotic indices.

1106


increase progressively in the percentage of samples sur-passing these limits (see data presented for arsenic,mercury, nickel, lead, copper, chromium, PCB andDDT).

Discussion

Many of the biotic indices developed in the literature(Clements et al., 1992; Mouthon, 1993; Stark, 1993;Grall and Gl�emarec, 1997; Roberts et al., 1998, etc.)have been based on the paradigm of Pearson and Ro-senberg (1978), as stated by Weisberg et al. (1997) indeveloping their own index. The paradigm states thatbenthic communities respond to improvements in hab-itat quality in three progressive steps: the abundanceincreases; species diversity increases; and dominantspecies change from pollution-tolerant to pollution-sensitive species.

This generally accepted paradigm has been adaptedfrom Grall and Gl�emarec (1997) in this contribution, inorder to obtain an European BI. This should be able todistinguish easily estuaries and coastal reference sitesfrom polluted sites, with di�erent levels of anthropo-genic or natural degradation.

The index derived provides a semi-quantitative mea-surement of the degree of impact on soft-bottom mac-rofauna, which is re¯ected by changes in the qualitativeand quantitative community composition.

As the BI has been established on the basis of analysisof samples obtained from a monitoring network, with aprevalence of polluted sites, there are only two unpol-luted samples (BI� 0) which correspond to a `normal'community (sensu Grall and Gl�emarec, 1997). The di-versity results do not correspond to those expected fromthe aforementioned paradigm, because the richness is

very low. Conversely, samples with BI� 1 (also unpol-luted in the present proposal, corresponding to animpoverished community) or higher, BI� 2±6 (corre-sponding to slightly to heavily polluted sites) havewell-de®ned values of biological parameters; this is asmight be expected from the results of Pearson andRosenberg (1978).

Some biotic indices, or Coe�cients of Pollution (i.e.Bogdanos and Satsmadjis, 1985) do not appear to besuitable for application in some cases. This is due to thelack of sensitivity of these indices to intermediate pol-lution levels (MAFF, 1993), corresponding with slightlypolluted areas. Hily (1984) and Grall and Gl�emarec(1997) have described similar di�culties.

The above limitation appears to be due to a generalunder-estimation of the faunal abundance in compari-son with unpolluted areas. This is because faunalabundance will increase under slight to moderate pol-lution, but numbers of species can either stay constantor show only a slight increase. In the present proposal,this problem appears to be eliminated because the ap-proach has a high sensitivity at these levels, with well-de®ned values in the biological parameters.

Organic enrichment and muddy bottoms, associatedwith subsequent low redox potential and hypoxia, arerelated with opportunistic species (Majeed, 1987) in`heavily polluted' levels, according to the BI (BI� 5±7).Diaz and Rosenberg (1995) have suggested that benthicinfaunal mortality could be initiated when the oxygenconcentration falls below 2 ml lÿ1. Ritter and Montagna(1999) have recently proposed that 3 mg lÿ1 (� 2.14 mllÿ1) de®nes the breakpoint between normoxic and hy-poxic benthic communities. The mean oxygen concen-tration obtained for BI� 7 indicates that life could bevery limited in those sites. However, within BI� 6, there

Fig. 7 Percentage of samples of each biotic index that goes beyond theER-L (or E�ects Range-Low, representing concentrationsbelow which adverse e�ects are expected to occur rarely), forseven heavy metals and three organic compounds.

1107


are some situations of very low oxygen concentrationwhich explain the presence of species which are resistantto severe or moderate hypoxia. These species are clas-si®ed within ecological Groups IV and V.

Samples with BI� 6 and 7 are associated with sitesthat experience periodic hypoxia, consisting of repeatedbrief periods (days or weeks, in the case of BI� 6) orseasonal hypoxia (months, in the case of BI� 7), thatgenerate mass mortality or complete elimination of themacrofauna. Some of the samples with BI� 7 arelocated within the Bilbao estuary, for which S�aiz-Salinas(1997) and Gonz�alez-Oreja and S�aiz-Salinas (1998) havedemonstrated that the oxygen limitation represents thekey factor in the estuarine defaunation of samplingstations within the estuary.

Physico-chemical results related to the BI (see Fig. 4)have some unexpected results at the level of BI� 5 and6. The trend of increasing percentages of mud and or-ganic matter, together with decreasing redox potential,break-down at these particular levels. BI� 5 and 6correspond to high percentages of ecological Group V(with a mean of 77.5% of species in BI� 5, together with92.7% in BI� 6). These species are mainly deposit-feeders. As such, they could modify the proportion oforganic matter in the sediments on which they feed and,subsequently, modify the grain size composition of thesediments. The optimal grain size may be di�erent forthe settling larvae, juveniles and adults of a variety ofdeposit-feeders (Snelgrove and Butman, 1994), changingtheir physico-chemical properties. For example, Hall(1994) has stated that faecal pellets of benthic inverte-brates modify the grain size of the sur®cial sediments.

In spite of the fact that hypoxia seems to control thepresence of the groupings with BI� 7 and that organicmatter content is very important in ascribing samples tothe BI, ecotoxicological e�ects appear to play only a

secondary role in the analyses; however it may have hadan e�ect in the longer time, as cited by S�aiz-Salinas(1997) for the Bilbao Estuary.

In order to validate the derived BI, for more generalapplication, four stations from the 30 stations sampledhave been selected for more detailed analysis. The evo-lution of the percentage of ecological grouping, the BIand the BC, derived for between 1995 and 1998, at thesestations is shown in Fig. 8.

Within the Urdaibai estuary (Figs. 1 and 8(a)) theresults obtained from a single station, in the inner partof the estuary, shows a dominance of ecological GroupIII. This is characteristic of estuarine communities lo-cated at sites with organic matter inputs. The derived BIshows that, in 1995 and 1996, the site is slightly polluted(BI� 2) due mainly to the aforementioned organicmatter enrichment. In 1997 and 1998, the BI increasesprogressively (BI� 3 and 4); as such classifying thisstation as `meanly polluted'. Such a trend is caused bythe increasing dominance of ecological Group V, whichindicates the presence of opportunistic species. On theother hand, the BC increases gradually with time, whichindicates a rising contamination in this site during thelast years.

The increase in the BI could be the result of dredgingactivities undertaken along this particular estuary,within the last few years. At the same time, there arechanges in the sediment composition, the abundance ofsuspended matter, etc. These provide the basis for anincrease in the opportunistic species at this particularlocation.

In February 1995, the station in the Oria estuary(Figs. 1 and 8(b)), was located some 500 m landward ofthe mouth. Group I was dominant and the BI (2) pro-vides a classi®cation of the site as `slightly polluted'. In1995 and 1996, some channelling works were under-

Fig. 8 Evolution of the percentage of ecological groups (I±V), the BIand the BC, derived for between 1995 and 1998, for the stationsshowed in Fig. 1: Station 10; Station 21; Station 13; and Station24.

1108


taken in this estuary, extending the mouth of the estuarysome 500 m o�shore. This development has led to anincrease in the distance from the mouth of the estuary tothe sampling station, with a subsequent change in thephysico-chemical conditions (Borja et al., 1999a). Thischange resulted in an increase in the mud and organicmatter content, together with a decrease in dissolvedoxygen. This change in the physical setting provides anexplanation for the increase in the dominance of eco-logical Groups III and V (more characteristic at theinner part of the estuary), modifying the BI to `meanlypolluted' (3). The BC increased during this period, from1.4 to 3.5.

The Lea is a small estuary within the Basque Country(Figs. 1 and 8(c)) which, in the past 4 years, has beensubjected to a sewerage plan, eliminating urban andindustrial e�uent discharges into the estuarine waters.The estuary was dominated by the opportunistic GroupV in 1995, with a BI of 3 (meanly polluted). Followingthe introduction of the sewerage scheme, the ecologicalGroup I, composed of species that are sensitive to pol-lution, increased in its dominance. This represented, in1997 and 1998, nearly 100% of the community.Throughout these two last years, the BI is 0. The BCdecreases from 4.2 in 1995 to 0.4 in 1996 and near 0 in1997 and 1998. So, in the last two years this station canbe classi®ed as an unpolluted site.

Finally, within the coastal area of Momp�as, near SanSebasti�an (Figs. 1 and 8(d)), there is an importantchange in the ecological group composition between1995 and 1996. At the beginning of this period, there is aco-dominance of Groups V, I and II. However, there is aclear dominance of Group V from 1996 to 1998. At thesame time, the BI changes from 2 (slightly polluted) to5±6 (heavily polluted). The BC, which was 3.0 in 1995,increased to values between 5.3 and 5.9 during the lastthree years. This particular coastal area has receivedlarge amounts of domestic and industrial waste from theSan Sebasti�an area since the 1970s. Further, in 1995 and1996, some sewerage works were constructed and animportant volume of urban and industrial polluted wa-ters, derived from nearby areas such as Pasajes orTximistarri, were diverted to Momp�as. The waste in-cludes contaminants (heavy metals and organic com-pounds) and a high amount of organic matteroriginating from the paper manufacturers (Franco et al.,1999).

Conclusions

The BC, proposed here as a BI to establish the eco-logical quality of the soft-bottom benthos within theEuropean coastal environments, takes into account thefaunal composition. As such, it ascribes each species toan ecological grouping, according to their sensitivity toan increasing stress gradient.

The di�erent composition, in terms of the abundanceof the various ecological groups in these samples pro-

vides a continuous BC (with values between 0 and 6).This is referenced to a BI, representing quality of bot-tom conditions in a discreet range from 0 (unpolluted)to 7 (extremely polluted). This composition is governedby the physico-chemical factors within the sedimentsand the overlying water column in terms of: organicmatter content; percentage of mud within the sediments;dissolved oxygen content within the bottom waters; andthe concentration of pollutants.

Biological parameters (such abundance, richness,biomass or diversity) provide a useful (and morebroadly applicable) description of each level of the BI. Itis considered (as described by Dauer, 1993) that bio-logical criteria may complement toxicity and chemicalassessment methods, to serve as independent evaluationsof the ecological quality of marine and estuarine eco-systems.

Validation of the model developed shows that di�er-ent anthropogenically changes in the environment canbe detected through the use of the BI, including altera-tions to the natural system such as dredging, engineeringworks, sewerage plans and the dumping of pollutedwaters. On the other hand, the BC provides a moreaccurate view of the evolution of the ecological status ofa particular location. Further, the fact that this partic-ular coe�cient can derive continuous values makes itmore suitable for application to statistical analysis thanthe BI (i.e. temporal trend analysis).

The BI proposed here is relatively simple and can,meaningfully, be applied when attempting to determinethe ecological status of European coastlines. Althoughthis index has been developed in the Bay of Biscay, themethodology can be applied for other European coastalareas, only conditioned by the assignation of the speciesto the ecological groups described here. In fact, many ofthe species compiled in the Appendix A are present inNorth Sea and Mediterranean. So, the index may beimproved with the contributions of newly assignedspecies from these seas and further examples of its moregeneral application and validation.

Finally, this index facilitates the understanding ofcomplex benthic data, summarizing a considerableamount of ecological information into a single repre-sentative value.

This study was supported by di�erent contracts undertaken betweenthe Department of Land Action, Housing and Environment of theBasque Government and AZTI. One of the authors (V. P�erez) wassupported by a grant from the Department of Agriculture and Fishingof the Basque Government. We thank the sta� of the Department ofOceanography of AZTI for their assistance during the ®eld samplingand laboratory analyses and the INSUB Group that was charged ofthe taxonomical analysis. We wish to thank also Professor MichaelCollins (School of Ocean and Earth Science, University of South-ampton, UK) and an anonymous referee for kindly advising us onsome details of this paper.

Appendix A

See Table 3.

1109


TABLE

3

Listofspeciesandtaxa(inalphabeticalorder)thathavebeenfoundin

allthestationsalongthewhole

studiedperiod(theassigned

ecologicalgroups(see

text)are

alsoshown).

a

Species

Group

Species

Group

Species

Group

Species

Group

Species

Group

Abarenicola

claparedi

IAngulustenuis

IBelapowisiana

IChoneinfundibuliform

isII

Diastylisrugosa

IAbarenicola

sp.

IAnomia

ephippium

IBelasp.

IChonesp.

IIDiastylissp.

IAbissoninoehibernica

IIAnoplodactyluspetiolatus

N.A

Bittium

reticulatum

IChthamalusstellatus

IDiastylistumida

IAbra

alba

III

Anoplodactyluspygmaeus

N.A

Boccardia

chilensis

ICirce

minim

aI

Diodora

apertura

IAbra

nitida

III

Antenella

sp.

IBoccardia

polybranchia

ICirculusstriatus

IDiogenes

pugilator

IIAbra

prism

atica

III

Anthozoasp.

IBoccardia

sp.

ICirratuluschrysoderma

IVDiopatraneapolitana

IAbra

sp.

III

Anthura

gracilis

IBodotria

arenosa

IICirratuluscirratus

IVDiplocirrusglaucus

IAbra

tenuis

III

Aonides

oxycephala

III

Bodotria

scorpioides

IICirriform

iatentaculata

IVDispio

uncinata

III

Acanthocardia

aculeata

IAora

gracilis

IBradavillosa

N.A

Cirripedosp.

IDivaricelladivaricata

IAcanthocardia

echinata

IAora

typica

IBranchiommavesiculosum

IClausinella

fasciata

IDonaxtrunculus

IAcanthocardia

paucicostata

IAphelochateamultibranchiis

N.A

Branchiostomalanceolata

IClavidae

IDorissp.

IAcanthocardia

sp.

IApherusa

cirrus

IBrania

oculata

IIClymenecf.praetermisa

IDosinia

exoleta

IAcanthocardia

tuberculata

IApherusa

ovalipes

IBrania

pusilla

IIClymenelumbricoides

IDosinia

juv.

indet.

IAcanthochitonacritinus

IAphonupisgrubei

IBugula

sp.

IClymenemodesta

IDosinia

lupinus

IAcanthochitonafascicularis

IAphroditeaculeata

N.A

Callianassasp.

III

Clymeneoerstedii

IDosinia

sp.

IAchelia

hispida

IApiculariaguerini

ICallianassasubterranea

III

Clytiasp.

IDrilonereis®lum

IIAchelia

simplex

IApistobranchustullbergi

ICallianassatruncata

III

Cnidariasp.

IEbaliasp.

N.A

Aclisgulsonae

N.A

Aponuphisbilineata

IICalliostomapapillosum

ICochlodesmapraetenue

N.A

Ebaliatuberosa

N.A

Acronidabrachiata

IAporrhaispespelecani

ICalliostomazizyphinum

ICopepodaindet.

N.A

Echinocardium

cordatum

IActeonsp.

IAporrhaissp.

ICalyptraea

sinensis

ICop� epodosp.

N.A

Echinocyamuspusillus

IActinia

equina

IApseudes

latreillei

III

Campylaspisglabra

N.A

Corbula

gibba

III

Echinoidea

sp.

IAglaophamusrubella

N.A

Arcturellasp.

N.A

Capitella

capitata

VCorophium

acherusicum

III

Echiuroidea

sp.

IAglaophamussp.

N.A

Arenicola

marina

N.A

Capitella

sp.

VCorophium

acutum

III

Echiurusechiurus

IAiptasiamutabilis

N.A

Aricialatreilli

ICapitellides

giardi

VCorophium

arenarium

III

Edwardsiasp.

IIAlcyonaceaindet

N.A

Aricidea

catherinae

ICapitomastusminim

us

IVCorophium

insidiosum

III

Ehlersia

ferrugina

N.A

Alkmariaromijni

III

Aricidea

cerruti

ICaprellafretensis

N.A

Corophium

multisetosum

III

Ensissp.

IAlpheusglaber

N.A

Aricidea

cf.assim

ilis

ICaprellalinearis

N.A

Corophium

sp.

III

Eocumadim

orpha

IIAlvania

crassa

IAricidea

fragilis

ICaprellapenantis

N.A

Corophium

volutator

III

Eocumadollfusi

IIAlvania

semistriata

IAricidea

je�reysii

ICarcinusmaenas

III

Corynepusilla

IEpileptonclarkiae

IAlvania

sp.

IAricidea

minuta

ICaryophyllia

smithi

ICorystes

cassivelaunus

IEpithonium

clathrus

IAmateatrilobata

IAricidea

sp.

ICaulleriellaalata

III

Cossura

longocirrata

N.A

Epitonium

turtoni

IAmathia

pruvot

IArm

andia

cirrosa

ICaulleriellabioculata

III

Cossura

pygodactylata

N.A

Ericthoniusbrasilensis

N.A

Ampelisca

brevicornis

IArm

andia

spp

ICaulleriellasp.

III

Cossura

sp.

N.A

Eteonelonga

IIAmpelisca

cf.spooneri

IAspidosiphonmuelleri

ICaulleriellazetlandica

III

Crangonallmani

IEteonepicta

IIAmpelisca

heterodactyla

IAstacillalongicornis

ICavernulariapusilla

ICrangoncrangon

IEuclymedepraetermissa

IAmpelisca

juv.

indet.

IAstartesp.

ICeradocussemiserratus

ICrassostreaangulata

III

Euclymenea�nis

IAmpelisca

sarsi

IAstartesulcata

ICerastodermaedule

III

Crepidula

fornicata

III

Euclymeneoerstedii

IAmpelisca

sp.

IAstartetriangularis

ICerastodermalamarcki

III

Cucumariaelongata

IEuclymenesp.

IAmpelisca

spinifer

IAsterinagibosa

ICeratostomaerinaceum

ICucumariasp.

IEuclymenidaeindet.

IAmpelisca

spinim

ana

IAstropectenirregularis

ICerebratulusmarginatus

III

Cultelluspellucidus

IEudorellatruncatula

N.A

Ampelisca

tenuicornis

IAstropectenirregularistypicus

ICerebratulussp.

III

Cumopsisfagei

IIEulaliabilineata

IIAmpelisca

toulemonti

IAthanasnitescens

ICereuspedunculatus

ICumopsissp.

IIEulaliamustela

IIAmpharete

®nmarchica

IAthecata

sp.

ICeriantariosp.

ICyathura

carinata

III

Eulaliasanguinea

IIAmpharete

grubei

IAtylusfalcatus

ICerianthuslloydii

ICyclopeneritea

IEulaliasp.

IIAmpharete

juv.

indet.

IAtylusguttatus

ICerianthusmem

branaceus

ICylichnacylindracea

IEulaliatripunctata

IIAmpharete

lindstroem

iI

Atylussp.

ICerianthussp.

ICylichnasp.

IEulaliaviridis

IIAmpharete

sp.

IAtylussw

ammerdami

ICestopagurustimidus

ICylichninasubcylindrica

IEulimella

acicuta

IAmphicteisgunneri

III

Atylusvedlomensis

IChaetopterusvariopedatus

ICymodoce

truncata

IEulimella

sp.

IAmphipholissquamata

IAudouinia

tentaculata

IVChaetozoneBspp

IVCythara

attenuata

IEumidabahusiensis

IIAmphitrite

johnstoni

IAutolytuslongeferiens

N.A

Chaetozonecf.gibber

IVCythara

costata

IEumidasanguinea

IIAmphiura

brachiata

IAutolytussp.

N.A

Chaetozonegibber

IVDardanusarrosor

N.A

Eumidasp.

II

1110


Amphiura

chiajei

IAxionicemaculata

N.A

Chaetozonesetosa

IVDem

onaxsp.

N.A

Euniceharassii

IIAmphiura

®liform

isI

Bachycumabrevicornis

N.A

Chaetozonesp.

IVDem

ospongia

sp.

IEunicesp.

IIAmphiura

juv.

indet.

IBalcisalba

IChamelea

gallina

IDentalium

novemcostatum

IEunicevittata

IIAmphiura

sp.

IBarleeia

rubra

IIChamelea

gallinastriatula

IDentalium

sp.

IEuphrosynefoliosa

IAnaitides

lineata

IIBathyporeia

elegans

IChamelea

striatula

IDesdem

onacf.ornata

IIEurydicea�nis

IAnaitides

maculata

IIBathyporeia

nana

IChauvetiabrunnea

IDesdem

onaornata

IIEurydicepulchra

IAnaitides

mucosa

IIBathyporeia

pelagica

ICheirocratussundevallii

IDevonia

perrieri

IEurydicesp.

IAnaitides

sp.

IIBathyporeia

pilosa

ICheriocratussp.

IDiastylisbradyi

IEurydicespinigera

IAnapagurushyndmani

IBathyporeia

sarsi

IChironomida

IVDiastyliscf.tumida

IEurynomeaspera

IAnapaguruslaevis

IBathyporeia

sp.

IChlamysvaria

IDiastyliscornuta

IEurynomespinosa

IAnapagurussp.

IBathyporeia

tenuipes

IChonecollaris

IIDiastylislaevis

IEurysyllistuberculata

IIAnguilla

anguilla

IIBelanebula

IChone®licaudata

IIDiastylislucifera

IExogonenaidina

IIExogonesp.

IIHesionura

elongata

IILeucothoespinicarpa

IMarphysa

fallax

IINephtyscirrosa

IIFabriciasabella

N.A

Heterocirrusbioculatus

IVLevinsenia

gracilis

N.A

Marphysa

sanginea

IINephtyshombergi

IIFabulinafabula

IHeterocirrusspp

IVLilleborjia

pallida

IMarphysa

sp.

IINephtyshystricis

IIFilogranaim

plexa

N.A

Heteromastus®liform

isIII

Liocarcinusarcuatus

IMarphysa

sp.(belli?)

IINephtysincisa

IIGalathea

interm

edia

IHexacorallia

sp.

ILiocarcinusarcuatus

IMartastheriasglacialis

INephtysjuv.

spp

IIGalathea

sp.

IHiatellaartica

ILiocarcinusdepurator

IMediomastusfragilis

III

Nephtyskersivalensis

IIGalathea

squamifera

IHinia

incrassata

IILiocarcinusholsatus

IMegaluropusagilis

INephtysparadoxa

IIGalathowenia

oculata

IHinia

juv.

indet.

IILiocarcinusmarm

oreus

IMegamphopuscornutus

INephtyssp.

IIGaleomnaturtoni

IHinia

pygmaea

IILiocarcinuspusillus

IMelinnacristata

III

Nephtyssp.juv.

IIGammarellafucicola

III

Hinia

reticulata

IILiocarcinussp.

IMelinnapalm

ata

III

Nephtysspp

IIGammaridea

IHippolyte

varians

ILiocarcinusvernalis

IMelinnasp.

III

Nereimyra

punctata

III

Gammaropsispalm

ata

IHippomedondenticulatus

ILiocarcinuszariquieyi

IMelitagladiosa

INereiphyllarubiginosa

N.A

Gammaropsisshophiae

IHyala

vitrea

IListriellapicta

IMelitapalm

ata

III

Nereiscaudata

IVGammaropsissp.

IHyale

nilssoni

ILoripes

lucinalis

IMerceriella

enigmatica

IINereiscf.lamellosa

III

Gammarusinsensibilis

IHyalinoecia

bilineata

N.A

Lucinomaborealis

IMetaphoxusfultoni

INereisdiversicolor

III

Gammarussp.

IHyalinoecia

fauveli

N.A

Lucinomaborealis

IMetaphoxuspectinatus

INereislongissima

III

Garicostulata

IHyalinoecia

sp.

N.A

Lumbrinerides

sp.

IIMetazoea

deporcellanidae

N.A

Nereissp.

III

Garidepressa

IHydrobia

ulvae

III

Lumbrineriopsisparadoxa

IIMicrodeutopusanomalus

INothriageo®liform

isII

Garifervensis

IHydroides

norvegica

N.A

Lumbrineriscf.gracilis

IIMicrodeutopusdamnoniensis

INothrialepta

IIGaritellinella

IIdotealinearis

N.A

Lumbrinerisem

andibulata

IIMicrodeutopussp.

INothriasp.

IIGariidaeindet.

IIdunella

picta

N.A

Lumbrinerisem

andibulata

mabiti

IIMicrodeutopusstationis

INotirusirus

IGattyanacirrosa

N.A

Inachusdorsettensis

ILumbrinerisgracilis

IIMicrodeutopusversiculatus

INotocirrussp.

N.A

Gibbula

magus

IInachussp.larva

ILumbrinerisim

patiens

IIMicrophthalm

ussczelkowii

N.A

Notomastuslatericeus

III

Glycera

alba

IIIphim

edia

obesa

ILumbrinerislatreilli

IIMicrospio

sp.

N.A

Notomastuslineatus

III

Glycera

capitata

IIIphino� e

serrata

ILumbrinerislatreilli

IIMicrura

sp.

N.A

Notomastussp.

III

Glycera

convoluta

IIIphinoesp.

ILumbrinerissp.

IIModiolula

phaseolina

INucula

nitida

IGlycera

lapidum

IIJaeraalbifrons

ILunatiaalderi

IIModiolusbarbatus

INucula

nitidosa

IGlycera

rouxii

IIJaerasp.

ILutrariaangustior

IModiolusgallicus

INucula

nucleus

IGlycera

sp.

IIJaniramaculosa

N.A

Lutrarialutraria

IModiolusmodiolus

INucula

sp.

IGlycera

tesselata

IIJasm

ineira

elegans

N.A

Lutrarialutraria

IMonoculodes

carinatus

INucula

sulcata

IGlycera

tridactyla

IIJupiteria

minuta

N.A

Lutrariasp.

IMonopylephorusirroratus

VNucula

turgida

IGlycera

unicornis

IIKefersteinia

cirrata

N.A

Lyonsianorvegicum

IMontacuta

ferruginosa

IIOcenebra

erinacea

IIGlycindenordmani

IIKelliasuborbicularis

ILysianassaceratina

IMusculusdiscors

IOdostomia

sp.

IIGlycindenordmanni

IILabidoplaxcf.thomsoni

ILysianassainsperata

IMyaarenaria

IIOligochaeta

VGnathia

oxyurea

ILabidoplaxdigitata

ILysidiceninetta

IIMyrtea

spinifera

IOnuphidaejuvenil

IIGobiusniger

III

Labidoplaxspp

ILysippelabiata

N.A

Mysellabidentata

IOnuphiscf.geophiliform

isII

Goniadamaculata

IILacydonia

miranda

N.A

Macomabaltica

IMysiaundata

IOnuphisconchylega

IIGoniadasp.

IILagisca

extenuata

IIMacropodia

rostrata

IMysidacea

IIOnuphiserem

ita

IIGoodallia

triangularis

ILanicecirrata

III

Mactra

corallina

IMystides

elongata

IIOphelia

bicornis

IGouldia

minim

aI

Lanicecirrata

III

Mactra

stultorum

IMystides

limbata

IIOphelinaacuminata

N.A

Gregariella

barbatella

ILaniceconchilega

IIMactraceaindet.

IMytilaster

minim

un

IOphiocentrusbrachiatus

IGuernea

coalita

N.A

Laniceconchilega

IIMaeragrossim

ana

IMytilusedulis

III

Ophiocominanigra

IGymnammodytessemisquamatus

N.A

Lanicespp

IIMaeraothonis

INassariusincrassatus

IIOphiodromus¯exuosus

IIGyptiscapensis

IILaonicesp.

N.A

Maerasp.

INassariusreticulatus

IIOphiopsila

aranea

I

1111


TABLE

3(C

ONTIN

UED)

Species

Group

Species

Group

Species

Group

Species

Group

Species

Group

Gyptisrosea

IILeanirayhleni

N.A

Magelonaalleni

INatantiasp.

N.A

Ophiotrix

fragilis

IHalcampasp.

ILem

bossp.

N.A

Magelona®liform

isI

Natica

alderi

IIOphiura

albida

IIHaminoea

navicula

IILepidonotusclava

IIMagelonaminuta

INatica

catena

IIOphiura

ophiura

IIHarm

othoeantilopes

IILepidonotussquamatus

IIMagelonamirabilis

INeanthes

caudata

III

Ophiura

sp.

IIHarm

othoecf.lunulata

IILeptocheiruspectinatus

III

Magelonapapillicornis

INeanthes

irrorata

III

Ophiura

texturata

IIHarm

othoeglabra

IILeptocheiruspilosus

III

Magelonasp.

INeanthes

juv.

indet.

III

Ophiura

texturata

(juv.)

IIHarm

othoeim

bricata

IILeptochelia

savignyi

N.A

Magelonawilsoni

INeanthes

sp.

III

Ophryotrochalabronica

IIHarm

othoeim

par

IILeptochitonasellus

IMalacocerosciliata

III

Nebaliabipes

VOphryotrochapuerilis

IIHarm

othoelunulata

IILeptochitoncancellatus

IMalacocerosfuliginosus

VNebaliasp.indet.

VOphryotrochasp.

IIHarm

othoesp.

IILeptochitoninhaerens

IMalacocerosgirardi

III

Nebaliathyphlops

IIOpistodonta

pterochaeta

N.A

Harm

othoesp.(antilopes?)

IILeptonerisglauca

III

Malacocerossp.

III

Nem

atoda

III

Orbinia

cuvieri

N.A

Harm

othoespinifera

IILeptosynapta

cf.gallienei

IMalacocerosvulgaris

III

Nem

atonereisunicornis

IIOrchomenenana

N.A

Harpinia

antennaria

ILeptosynapta

gallienei

IMaldaneglebifex

INem

ertea

III

Orchomenesimilis

N.A

Harpinia

pectinata

ILeptosynapta

inhaerens

IManayunkia

aestuarina

IINeoamphitrite

a�nis

N.A

Oriopsisarm

andi

N.A

Harpinia

sp.

ILeucothoeincisa

IMangelia

attenuata

INeoamphitrite

cf.a�nis

N.A

Oriopsissp.

N.A

Haustoriusarenarius

ILeucothoeincisa

IMangelia

nebula

INeoamphitrite

sp.

N.A

Ostreaedulis

IHediste

diversicolor

III

Leucothoelilljeborgi

IMangelia

smithi

INephtysassim

ilis

IIOvatellamyosotis

N.A

Hermionehystrix

IILeucothoerichiardii

IMangelia

sp.

INephtyscaeca

IIOwenia

®liform

isI

Hesionepantherina

IILeucothoesp.

IMarphysa

bellii

IINephtyscf.paradoxa

IIOwenia

fusiform

isI

Pachygrapsusmarm

oratus

IIPhyllodoce

rosea

IIProtodrilussp.

N.A

Sphaerosyllishystrix

IITholaruscranchii

IPaguroidea

indet.

IPhyllodoce

sp.

IIPsamechinusmiliaris

ISphaerosyllispyrifera

IIThraciaphaseolina

IPagurusbernhardus

IPhylocherasbispinosus

IPsammobia

costulata

ISphaerosyllissp.

IIThraciavillosiuscula

IPagurusprideauxi

IPhylocherasmonacantus

IPsammolyce

arenosa

IISphaerosyllistaylori

IIThyasira

¯exuosa

III

Pagurussp.larva

IPhylocherastrispinosus

IPseudobrania

sp.

IISphenia

binghami

IThyonefusus

IPalaem

onserratus

IPilargisverrucosa

IPseudocumalongicornis

IISpio

arm

ata

III

Tim

oclea

ovata

IPandora

albida

IPilumnushirtellus

IPseudocumasimilis

IISpio

decoratus

III

Tonicella

marm

orea

IPandora

inaequivalvis

IPinnotheres

pisum

N.A

Pseudocumasp.

IISpio

®licornis

III

Tricoliapullus

IPandora

pinna

IPionosyllisserrata

IIPseudopolydora

antennata

IVSpio

martinensis

III

Triphora

adversa

IPanoploea

minuta

IPisidia

longicornis

IPseudopolydora

paucibranchiata

IVSpio

sp.

III

Triphora

aspera

IParadoneisarm

ata

III

Pisidium

sp.indet.

IPseudopolydora

pulchra

IVSpiochaetopteruscostarum

III

Triphora

perversa

IParadoneislyra

III

Pisioneremota

IIPseudopolydora

sp.

IVSpiochaetopterussp.

III

Triviamonacha

IParagnathia

form

ica

III

Pista

cristata

IPseudoprotellaphasm

aN.A

Spiochaetopterustypicus

III

Trophonopsismuricatus

IParamphitrite

tetrabranchia

N.A

Plakosyllisbrevipes

IIPseudosyllisbrevipennis

IISpiophanes

bombyx

III

Tryphosellananoides

IParaonisfulgens

N.A

Plathelmintes

IIPseudosyllissp.

IISpiophanes

kroyeri

III

Tryphosellasarsi

IParaonisgracilis

N.A

Platynereisdumerilii

III

Pygospio

elegans

III

Spirobranchuspolytrem

aN.A

Tryphositeslongipes

IIParaonislyra

N.A

Pleuronectidaesp.

IIQuadransserratus

ISpisula

elliptica

ITubi®coides

benedii

VParapionosylliscf.gestans

IIPodoceusvariegatus

N.A

Raphitomapurpurea

ISpisula

solida

ITubi®coides

pseudogaster

VParapionosyllisgestans

IIPoecilochaetusserpens

IRaphitomasp.

ISpisula

subtruncata

ITubulanuspolymorphus

IIParapionosyllislabronica

IIPoecilochaetusserpens

IRetusa

truncatula

IStaurocephalusrudolphii

IVTubulanusspp

IIParapionosyllisminuta

IIPolycirrusaurantiacus

IVRetusa

umbilicata

IStenothoemonoculoides

IITurbelariosp.

N.A

Parapionosyllissp.

IIPolycirruscf.medusa

IVRhizorusacuminatus

N.A

Stenothoidae

IITurboella

parva

IParathelepussp.

IPolycirrusmedusa

IVRingicula

auriculata

ISternaspisscutata

III

Turbonilla

acuta

IPariambustypicus

III

Polycirrussp.

IVRingicula

conform

isI

Sthenelaisboa

IITurbonilla

elegantissim

aI

Pariambustypicusvarinermis

III

Polycirrustenuisetis

IVRingicula

sp.

ISthenelaiscf.minor

IITurbonilla

lactea

I

1112


Parvicardium

exiguum

IPolydora

antennata

IVSabella

pavonina

ISthenelaislimicola

IITurbonilla

rufa

IParvicardium

minim

um

IPolydora

caeca

IVSabella

sp.

ISthenelaisminor

IITurbonilla

spp

IParvicardium

ovale

IPolydora

ciliata

IVSabellariaalveolata

ISthenelaissp.

IITurritella

communis

IParvicardium

papillosum

IPolydora

¯ava

IVSabellariaspinulosa

IStreblosomabairdi

N.A

Turritella

triplicata

IParvicardium

scabrum

IPolydora

juv.

spp

IVScalibregmain¯atum

III

Streblospio

dekhuyzeni

III

Unciola

crenatipalm

aN.A

Pectinariaauricoma

IPolydora

ligerica

IVScaphander

lignarius

IStreblospio

shrubsolii

III

Upogebia

cf.tipica

IPectinariakoreni

IPolydora

ligni

IVSchistomeringoscaeca

IIStrem

blosomaintestinalis

N.A

Upogebia

deltaura

IPectinariasp.

IPolydora

polybranchia

IVSchistomeringosrudolphi

IVStriarcalactea

IUpogebia

pusilla

IPerinereiscultrifera

III

Polydora

pulchra

IVScionella

lornensis

N.A

Syconciliatum

IUpogebia

sp.

IPerioculodes

longim

anus

IPolydora

sp.

IVSclerocheilusminutus

N.A

Syconraphanus

IUpogebia

stellata

IPharuslegumen

IPolygordiusapendiculatus

IScolariciasp.

ISylliscornuta

IIUpogebia

typica

IPhascolionstrombi

IPolymnia

nebulosa

III

Scolariciatypica

ISyllisgerlachi

IIUrothoebrevicornis

IPhascolionstrombus

IPolynoescolopendrina

IIScolelepisfuliginosa

VSyllisgracilis

IIUrothoeelegans

IPhascolosomaelongatum

IPolyophthalm

uspictus

IScolelepissp.

III

Syllisprolifera

IIUrothoeposeidonis

IPhascolosomagranulatum

IIPomatoceroslamarckii

N.A

Scolelepissquamata

III

Syllissp.

IIUrothoepulchella

IPhascolosomavulgare

IPomatocerostriqueter

N.A

Scoloplosarm

iger

ISyllisvariegata

IIVauthompsonia

cristata

N.A

Phaxaspellucidus

IPontocratesaltamarinus

IScrobiculariaplana

III

Synchelidium

haplocheles

IVeneracea

IPherusa

monilifera

IPontocratesarenarius

IScrupocellariascrupea

N.A

Synchelidium

maculatum

IVenerupisaurea

IPherusa

plumosa

IPortumnuslatipes

ISem

ivermilia

sp.

N.A

Tanaisdulongii

N.A

Venerupispullastra

IPherusa

sp.

IPotamilla

reniform

isN.A

Sertulariidae

ITapes

decussata

IVenerupisrhomboides

IPhilineaperta

IIPotamilla

sp.

N.A

Sextonia

longirostris

IITelepsavuscostarum

IVenerupissenegalensis

IPhilineloweni

IIPotamilla

torelli

N.A

Sigalioncf.mathildae

IITelinatenuis

IVenuscasina

IPhilinespp

IIPotamopyrgusjenkinsi

IISigalionmathildae

IITellimyaferruginosa

IIVenusfasciata

IPholoeminuta

IIPraxilleaoerstedi

N.A

Sigalionsquamatum

IITellinacompressa

IVenusgallina

IPholoesynopthalm

ica

IIPrionospio

caspersi

IVSiphonoecetes

kroyeranus

ITellinadonacina

IVenusjuv.

sp.

IPhoronispsammophila

IPrionospio

cirrifera

IVSiphonoecetes

sp.

ITellinafabula

IVenusovata

IPhotislongicaudata

IPrionospio

ehlersi

IVSiphonoecetes

striatus

ITellinapusilla

IVenusstriatula

IPhoxocephalusrudolphii

IPrionospio

fallax

IVSipuncula

ITellinapygmaea

IVenusverrucosa

IPhthisicamarina

IPrionospio

malm

greni

IVSkenea

sp.

III

Tellinasp.

IVeretillum

cynomorium

IPhyllochaetopterussp.

N.A

Prionospio

multibranchiata

IVSkenia

serpuloides

N.A

Tellinasqualida

IVeretillum

sp.

IPhyllodoce

groelandica

IIPrionospio

sp.

IVSocarnes

erythrophthalm

us

N.A

Tellinatenuis

IVerruca

stromia

IPhyllodoce

lamelligera

IIPrionospio

steenstrupi

IVSolenmarginatus

ITerebella

lapidaria

IVituperisesribosa

VPhyllodoce

laminosa

IIProcessacanaliculata

ISolenacea

ITerebellides

stroem

iI

Xanthopilipes

N.A

Phyllodoce

lineata

IIProcessamodica

ISphaerodoropsissp.

N.A

Terebellomorphasp.indet

IIXenosyllisscabra

IIPhyllodoce

longipes

IIProcessanouveli

ISphaeromamonodi

IIThalassem

aneptuni

IZenobianaprism

atica

IIPhyllodoce

maculata

IIProcessaparva

ISphaeromarugicaudata

IITharyxmarioni

N.A

Zoanthariasp.

IPhyllodoce

mucosa

III

Processasp.

ISphaeromaserratum

IIThelepussetosus

N.A

Phyllodoce

paretti

IIProtodorvilleakefersteini

IISphaerosyllisbulbosa

IIThia

scutellata

II

aN.A

.±notassigned.

1113


Bogdanos, C. and Satsmadjis, J. (1985) Quantitative e�ect of sedimentcoarseness and depth on the macrobenthos of an unpolluted andclosed Mediterranean Gulf. Revue Internationale d' Oceanographiemedicale 77/78, 74±85.

Borja, A., Valencia, V., Garc�õa, L. and Arresti, A. (1995) Lascomunidades bent�onicas intermareales y submareales en SanSebasti�an-Pasajes (Guip�uzcoa, N de Espa~na). Actas IV ColoquioInternacional de Oceanograf�õa del Golfo de Vizcaya (Santander)165±181.

Borja, A., Franco, J., Belzunce, M. J. and Valencia, V. (1999a) Red deVigilancia y Control de la calidad de las aguas litorales del Pa�õsVasco (oto~no 1997±verano 1998). Departamento de Ordenaci�on delTerritorio, Vivienda y Medio Ambiente, Gobierno Vasco, 333pp+appendices.

Borja, A., Belzunce, M. J., Franco J. and Castro, R. (1999b)Seguimiento ambiental de los estuarios del Nervi�on, Barbad�un yButr�on durante 1998. Consorcio de Aguas Bilbao-Bizkaia, 228pp+appendices.

Cairns, J., Douglas, W. A., Busey, F. and Chaney, M. D. (1968) Thesequential comparison index ± a simpli®ed method for non-biologists to estimate relative di�erences in biological diversity instream pollution studies. Journal of Water Pollution Control. Fed 40,1607±1613.

Chandler, J. R. (1970) A biological approach to water qualitymanagement. Water Pollution Control 69, 415±422.

Clements, W. H., Cherry, D. S. and Van Hassel, J. H. (1992)Assessment of the impact of heavy metals on benthic communitiesat the Clinch River (Virginia): evaluation of an index of communitysensitivity. Canadian Journal of Fisheries and Aquatic Sciences 49,1686±1894.

Dauer, D. M. (1993) Biological criteria, environmental health andestuarine macrobenthic community structure. Marine PollutionBulletin 26 (5), 249±257.

Diaz, R. J. and Rosenberg, R. (1995) Marine benthic hypoxia: a reviewof its ecological e�ects and the behavioural responses of benthicmacrofauna. Oceanography and Marine Biology Annual Review 33,245±303.

Ferraro, S. P., Swartz, R. C., Cole, F. A. and Schults, D. W. (1991)Temporal changes in the benthos along a pollution gradient:discriminating the e�ects of natural phenomena from sewage-industrial wastewater e�ects. Estuarine, Coastal and Shelf Science33, 383±407.

Franco, J., Borja, A., Belzunce, M. J. Valencia, V. (1999) Campa~na demedici�on de variables biol�ogicas y f�õsico-qu�õmicas en el estuario del r�õoOiartzun y �area costera pr�oxima a cala Murgita. Departamento deObras Hidr�aulicas y Urbanismo de la Diputaci�on Foral deGipuzkoa, 197 p.+appendices.

Franklin, A. and Jones, J. (1994) Monitoring and surveillance of non-radiactive contaminants in the aquatic environment and activitiesregulating the disposal of wastes at sea, 1992. Aquatic EnvironmentMonitoring Report, MAFF 40, 1±83.

Gl�emarec, M. (1986) Ecological impact of an oil-spill: utilisation ofbiological indicators. IAWPRC-NERC Conference, July 1985.IAWPRC Journal 18, 203±211.

Gl�emarec, M. and Hily, C. (1981) Perturbations apport�ees �a lamacrofaune benthique de la baie de Concarneau par les e�uentsurbains et portuaires. Acta Oecologica Oecologia Applicata 2, 139±150.

Gonz�alez-Oreja, J. A. and S�aiz-Salinas, J. I. (1998) Exploring therelationships between abiotic variables and benthic communitystructure in a polluted estuarine system. Water Research 32 (12),3799±3807.

Grall, J. and Gl�emarec, M. (1997) Using biotic indices to estimatemacrobenthic community perturbations in the Bay of Brest.Estuarine, Coastal and Shelf Science 44 (suppl. A), 43±53.

Gray, J. S. (1979) Pollution-induced changes in populations. Philo-sophycal Transactions of the Royal Society of London. Series B, 286,545±561.

Hall, S. J. (1994) Physical disturbance and marine benthic communi-ties: life in unconsolidated sediments. Oceanography and MarineBiology Annual Review 32, 179±239.

Hily, C. (1984) Variabilit�e de la macrofaune benthique dans les milieuxhypertrophiques de la Rade de Brest. Th�ese de Doctorat dÕEtat,Univ. Bretagne Occidentale. Vol. 1, 359 pp; Vol. 2, 337 pp.

Hily, C., Le Bris, H. and Gl�emarec, M. (1986) Impacts biologiques des�emissaires urbains sur les �ecosyst�emes benthiques. Oceanis 12, 419±426.

Holme, N. A. and McIntyre, A.D. (1971) Methods for the Study ofMarine Benthos, p. 387. Blackwell, Oxford.

ISO-BMWP (1979) Assessment of the Biological Quality of Rivers by aMacroinvertebrate Score. ISO/TC147/SC5/WG6/N5, InternationalStandards Organisation, p. 18.

Kristensen, E. and Andersen, F. O. (1993) Determination of organiccarbon in marine sediments: a comparison of two CHN-analyzermethods. Journal of Experimental Marine Biology and Ecology 109,15±23.

Long, E. R., MacDonald, D. D., Smith, S. L. and Calder, F. D. (1995)Incidence of adverse biological e�ects within ranges of chemicalconcentrations in marine and estuarine sediments. EnvironmentalManagement 19, 81±97.

MAFF (1993) Analysis and interpretation of benthic community dataat sewage-sludge disposal sites. Aquatic Environmental MonitoringReport,MAFF Directorate of Fisheries Research, Lowestoft, Vol. 37,80 pp.

Majeed, S. A. (1987) Organic matter and biotic indices on the beachesof North Brittany. Marine Pollution Bulletin 18 (9), 490±495.

Mearns, A. J. and Word, J. Q. (1982) Forecasting e�ects ofsewage solids on marine benthic communities. In Ecological Stressand the New York Bight: Science and management ed. G. F. Mayer,pp. 495±512. Estuarine Research Federation, Columbia, SouthCarolina.

Mouthon, J. (1993) Un indice biologique lacustre bas�e sur lÕexamendes peuplements de mollusques. Bulletin Francßaise de la Peche et laPiscicul 331, 397±406.

OÕConnor, T. P. (1992) Recent trends in coastal environmental quality:results from the ®rst ®ve years of the NOAA Mussel Watch project.US Department of Commerce, NOAA, Rockville, 45 pp.

Pearson, T. and Rosenberg, R. (1978) Macrobenthic succession inrelation to organic enrichment and pollution of the marineenvironment. Oceanography and Marine Biology Annual Review16, 229±311.

Ritter, C. and Montagna, P. A. (1999) Seasonal hypoxia and model ofbenthic response in a Texas bay. Estuaries 22 (1), 7±20.

Roberts, R. D., Gregory, M. R. and Fosters, B. A. (1998) Developingan e�cient macrofauna monitoring index from an impact study ± Adredge spoil example. Marine Pollution Bulletin 36 (3), 231±235.

R.N.O. (1998) Surveillance du Milieu Marin. Travaux du R�eseauNational d'Observation de la Qualit�e du Milieu Marin. Edition1998. Ifremer et Minist�ere de lÕAm�enagement du Territoire et delÕEnvironnement, 52 pp.

S�aiz-Salinas, J. I. (1997) Evaluation of adverse biological e�ectsinduced by pollution in the Bilbao estuary. Environmental Pollution96 (3), 351±359.

Salen-Picard, C. (1983) Sch�emas dÕ�evolution dÕune bioc�enose macro-benthique du substrat meuble. Comptes Rendus de l'Academie desSciencies de Paris 296, 587±590.

Snelgrove, P. V. R. and Butman, C. A. (1994) Animal-sedimentrelationships revisited: cause versus e�ect. Oceanography andMarine Biology Annual Review 32, 111±177.

Stark, J. D. (1993) Performance of the macroinvertebrate communityindex: e�ects of sampling method, sample replication, water depth,current velocity and substratum on index values. New ZealandJournal of Marine and Freshwater Research 27, 463±478.

Washington, H. G. (1984) Diversity, biotic and similarity indices. Areview with special relevance to aquatic ecosystems.Water Research18, 653±694.

Weisberg, S. B., Ranasinghe, J. A., Dauer, D. M., Scha�ner, L. C.,Diaz, R. J. and Frithsen, J. B. (1997) An estuarine benthic indexof biotic integrity (B-IBI) for Chesapeake Bay. Estuaries 20 (1),149±158.

Woodiwiss, F. S. (1964). The biological system of stream classi®cationused by the Trent River Board. Chemistry Industries. 11, 443±447.

1114


a Marine Biotic Index To Establish The Ecological - ECASA · A Marine Biotic Index to Establish the...

Documents

Transcript of a Marine Biotic Index To Establish The Ecological - ECASA · A Marine Biotic Index to Establish the...