PII:
Marine Pollution Bulletin Vol. 40, No. 12, pp. 1100±1114, 2000
Ó 2000 Elsevier Science Ltd. All rights reserved
Printed in Great Britain
S0025-326X(00)00061-8
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A Marine Biotic Index to Establish the
Ecological Quality of Soft-Bottom
Benthos Within European Estuarine and
Coastal Environments
A. BORJA*, J. FRANCO and V. PEREZ
Department 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-bottom
benthos of European estuarine and coastal environments is
proposed. This is derived from the proportions of individual abundance in ®ve ecological groups, which are related to the degree of sensitivity/tolerance to an
environmental stress gradient. The main dierence with
previously published indices is the use of a simple formula
that produces a continuous Biotic Coecient (BC) ±
which makes it more suitable for statistical analysis, in
opposition with previous discreet biotic indices ± not affected by subjectivity. Relationships between this coecient and a complementary BI with several environmental
variables are discussed. Finally, a validation of the proposed index is made with data from systems aected by
recent human disturbances, showing that dierent anthropogenic changes in the environment can be detected
through 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 undertaken
usually by means of monitoring dierent parameters in
water, sediment and sentinel organisms (i.e. Mussel
Watch), as in the USA (OÕConnor, 1992), France (RNO,
1998) or Great Britain (Franklin and Jones, 1994). This
control is centred on physico-chemical and ecotoxicological variables and, less usually, on biological variables. Dauer (1993) stated that biological criteria are
considered important components of water quality because: (i) they are direct measures of the condition of the
*Corresponding author.
E-mail address: aborja@azti.es (A. Borja).
1100
biota, (ii) they may uncover problems undetected or
underestimated by other methods; and (iii) such criteria
provide measurements of the progress of restoration
eorts.
New European rules (see Directive Proposal 1999/C
343/01, Ocial Journal of the European Communities
30/11/1999) emphasize the importance of biological indicators, in order to establish the ecological quality of
European coasts and estuaries. Benthic invertebrates are
used frequently as bio-indicators of marine monitoring,
because various studies have demonstrated that macrobenthos responds relatively rapidly to anthropic and
natural stress (Pearson and Rosenberg, 1978; Dauer,
1993).
River ecology has an established long tradition in
applying macrobenthos as bio-indicators; likewise some
biotic indices have been proposed (Woodiwiss, 1964;
Cairns et al., 1968; Chandler, 1970; ISO-BMWP, 1979,
etc.). On the other hand, some attempts to provide
useful `tools' to measure ecological quality in the marine
environment have been developed in Europe and North
America (Hily, 1984; Majeed, 1987; Dauer, 1993; Grall
and Glemarec, 1997; Weisberg et al., 1997).
All the aforementioned studies utilize soft-bottom
communities to construct the indices, because macrobenthic animals are relatively sedentary (and cannot
avoid deteriorating water/sediment quality conditions),
have relatively long life-spans (thus, indicate and integrate water/sediment quality conditions, with time),
consist of dierent species that exhibit dierent tolerances to stress and have an important role in cycling
nutrients and materials between the underlying sediments and the overlying water column (Hily, 1984;
Dauer, 1993).
In this contribution, a marine Biotic Index (BI) is
designed to establish the ecological quality of European
coasts. This explores the response of soft-bottom communities to natural and man-induced changes in water
quality, integrating long-term environmental conditions.
Volume 40/Number 12/December 2000
Methods
Sampling
The Department of Land Action, Housing and
Environment of the Basque Government has established
a network of monitoring stations along the Basque
coast-line (North of Spain). This provides water, sediment and biological quality information from 30 sampling stations (Fig. 1). The benthic sampling has been
carried out every February, from 1995 to 1998 using the
research vessel `Ortze'.
At each of these stations, three replicates of benthos
were collected with a Van Veen grab (1215 cm2 ). The
samples were ®ltered immediately, using a sieve of mesh
size of 1 mm and ®xed in a solution of 4% formalin
(Holme and McIntyre, 1971).
Sediment data
At each station, a sediment sample was obtained to
determine redox potential, organic matter content and
contaminant levels (heavy metals and organic compounds). The redox potential was measured, on board,
by means of an Orion 977800 platinum electrode which
was 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, sand
and mud were calculated as: >2 mm fraction, 63 lm ± 2
mm and <63 lm, respectively (Holme and McIntyre,
1971).
The organic matter content was calculated by the loss
on ignition method: drying at 105°C, 24 h; then combusting at 520°C, 6 h (Kristensen and Anderson, 1993).
Metal concentrations (As, Cd, Cu, Cr, Hg, Ni, Pb and
Zn) were analysed on the <63 lm fraction. Extraction
was made ®rst with nitric acid, during 15 h, at ambient
temperature; and second, with nitric and hydrochloric
acids (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. The
analytical procedure was checked with reference material (BCR marine sediment-harbour PACS-1); dierences with this material were lower than 10%.
For PCB (eight congeners), DDT and HCH determination a portion of the original sample was desiccated
with anhydrous sodium sulphate and extraction was
made with iso-octane, after conditioning and clean-up of
the extract the analysis was made with an HP-5890 gas
chromatograph. On the other hand, for PAH (10 compounds) determination, the extraction was made with
ether, and the analysis was made by means of HPLC.
Water quality data
The mean bottom oxygen concentration was measured 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 data
The identi®cation was undertaken in the laboratory
by means of a binocular microscope (4±40). After
computing the mean abundance of each taxon, at each
sampling station, the macrobenthic community structure was described calculating the following descriptors
(Washington, 1984): richness (number of identi®ed
taxa); abundance (N: ind mÿ2 ); numerical diversity
(Shannon Wiener H0 n : bits indÿ1 ); biomass (Dry Weight,
B: g mÿ2 ); and biomass diversity (Shannon Wiener H0 b :
bits gÿ1 ).
BI model
The model here developed is based on that ®rst used
by Glemarec and Hily (1981) and then by Hily (1984),
which utilizes soft-bottom benthos to construct a BI.
Soft-bottom macrobenthic communities respond to
environmental stress (i.e. the introduction of organic
matter in the system) by means of dierent adaptive
strategies. Gray (1979) summarizes these strategies into
three ecological groups: r (r-selected: species with short
life-span, fast growth, early sexual maturation and larvae throughout the year); k (k-selected: species with
relatively long life, slow growth and high biomass); and
T (stress tolerant: species not aected by alterations).
Salen-Picard (1983) has proposed four progressive
steps relating to stressed environments: (i) initial state
(in an unpolluted situation, there is a rich biocenosis in
individuals and species, with exclusive species and high
diversity); (ii) slight unbalance (regression of exclusive
species, proliferation of tolerant species, the appearance
of pioneering species, decrease of diversity); (iii) pronounced unbalance (population dominated by pollution
indicators, very low diversity); and (iv) azoic substrata.
Following these four steps, Hily (1984) and Glemarec
(1986) have stated that the soft-bottom macrofauna
could be ordered in ®ve groups, according to their sensitivity to an increasing stress gradient (i.e. increasing
organic matter enrichment). Their concept is similar to
that developed for the Infaunal Index for Southern
California, described by Mearns and Word (1982) and
Ferraro et al. (1991). These groups have been summarized by Grall and Glemarec (1997), as outlined below.
Group I. Species very sensitive to organic enrichment
and present under unpolluted conditions (initial state).
They include the specialist carnivores and some depositfeeding tubicolous polychaetes.
Group II. Species indierent to enrichment, always
present in low densities with non-signi®cant variations
with time (from initial state, to slight unbalance). These
include suspension feeders, less selective carnivores and
scavengers.
Group III. Species tolerant to excess organic matter
enrichment. These species may occur under normal
conditions, but their populations are stimulated by
1101
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Marine Pollution Bulletin
Fig. 1 Position of the 30 stations monitored along the Basque coastline (North of Spain), from 1995 to 1998. The stations used to
validate the model are shown in black.
Volume 40/Number 12/December 2000
organic richment (slight unbalance situations). They are
surface deposit-feeding species, as tubicolous spionids.
Group IV. Second-order opportunistic species (slight
to pronounced unbalanced situations). Mainly small
sized polychaetes: subsurface deposit-feeders, such as
cirratulids.
Group V. First-order opportunistic species (pronounced unbalanced situations). These are depositfeeders, which proliferate in reduced sediments.
The distribution of these ecological groups, according
to their sensitivity to pollution stress, provides a BI with
eight levels, from 0 to 7 (Hily, 1984; Hily et al., 1986;
Majeed, 1987).
In the aforementioned monitoring network of sampling stations, together with other studies developed by
AZTI along the Basque coastline within the last ®ve
years (Borja et al., 1995, 1999a,b), more than 900 taxa
have been identi®ed. These species are representative of
the most important soft-bottom communities present at
European estuarine and coastal systems. The taxa have
been classi®ed (list in Appendix A) according to the
above ecological groups, following Majeed (1987),
Dauer (1993), Weisberg et al. (1997), Grall and
Glemarec (1997) and Roberts et al. (1998). Only about
12% of the taxa have not been possible to be assigned to
an ecological group.
Based upon HilyÕs model (Hily, 1984; Hily et al., 1986;
Majeed, 1987), Fig. 2 shows the theoretical distribution
of relative abundance of each ecological group, along a
pollution gradient.
A possible limitation in the utilisation of the model of
Hily is that each BI has a discreet value and its calculation is not systematized. In order to improve the index,
a single formula is proposed here. This is based upon the
percentages of abundance of each ecological group,
within each sample, to obtain a continuous index (the
Biotic Coecient (BC)), where
Biotic Coefficient f 0 % GI 1:5 % GII
3 % GIII 4:5 % GIV
6 % GVg=100:
The above-mentioned ecological groups (GI, GII,
GIII, GIV and GV) are summarized in Table 1. Species
not 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 of
continuous values, from 0 to 6, being 7 when the sediment is azoic. Nonetheless, the BC can be compared to
the Grall and Glemarec (1997) BI, as adapted in this
paper (Table 1). The result obtained is a `pollution
classi®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
Fig. 2 Theoretical model, modi®ed from Hily (1984), Hily et al. (1986)
and Majeed (1987), which provides the ordination of softbottom macrofauna species into ®ve ecological groups (Group
I: species very sensitive; Group II: species indierent; Group
III: species tolerant; Group IV: second-order opportunistic
species; Group V: ®rst-order opportunistic species), according
to their sensitivity to an increasing pollution gradient. The
relative proportion of abundance of each group in a sample
provides a discreet BI with eight levels (0±7) and an equivalent
continuous BC (values between 0 and 6).
The mean and standard error values of grain size and
physical characteristic associated with each of the sampling stations (17 estuarine and 13 littoral) are listed in
Table 2. The water depth range is very large at each of
the stations (under Mean High Water Neap to 24 m in
the estuaries and 30±35 m associated with the littoral
samples). Mean salinity, at bottom water, ranges from
16.2 to 35.3 in estuaries, but is restricted within the
coastal areas (35.3±35.5).
The range in the percentage of oxygen saturation is
very high within the estuaries (43±119%), but ranges in
the littoral stations from 92% to 97%. The organic
TABLE 1
Summary of the BC and BI (modi®ed from Grall and Glemarec, 1997).
Site pollution classi®cation
Unpolluted
Unpolluted
Slightly polluted
Meanly polluted
Meanly polluted
Heavily polluted
Heavily polluted
Extremely polluted
Biotic Coecient
Biotic index
Dominating ecological group
Benthic community health
0:0 < BC 0:2
0:2 < BC 1:2
1:2 < BC 3:3
3:3 < BC 4:3
4:5 < BC 5:0
5:0 < BC 5:5
5:5 < BC 6:0
Azoic
0
1
2
3
4
5
6
7
I
Normal
Impoverished
Unbalanced
Transitional to pollution
Polluted
Transitional to heavy pollution
Heavy polluted
Azoic
III
IV±V
V
Azoic
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Marine Pollution Bulletin
TABLE 2
Physico-chemical characterisation of sampling stations, showing mean and standard error (SE) values of some sedimentological and water
parameters.a
Station
number
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
a
Station
type
E
E
E
E
L
L
E
L
L
E
E
L
E
L
E
L
E
L
E
L
E
L
E
L
E
E
L
E
E
L
Depth
(m)
Salinity
Dissolved
oxygen (ml lÿ1 )
% Oxygen
saturation
% Sand
% Mud
% Organic
matter
Redox
potential (mV)
Mean
Mean SE
Mean SE
Mean SE
Mean SE
Mean SE
Mean SE
Mean SE
I
3
14
24
34
32
I
34
33
I
I
31
I
34
I
34
I
32
I
32
I
32
I
34
9
8
32
I
I
33
23:5 2:3
16:2 2:0
35:1 0:1
35:3 0:1
35:3 0:1
35:3 0:1
29:5 1:6
35:4 0:0
35:4 0:0
25:7 2:5
34:8 0:1
35:5 0:0
26:3 3:0
35:5 0:0
28:9 1:6
35:4 0:1
17:5 2:7
35:4 0:1
23:3 2:2
35:4 0:0
21:1 2:2
35:4 0:1
21:1 3:1
35:4 0:0
34:0 0:2
33:3 0:4
35:4 0:0
19:3 2:3
26:2 1:6
35:3 0:1
6:1 0:2
3:1 0:5
5:0 0:1
5:4 0:1
5:6 0:1
5:5 0:1
6:1 0:2
5:5 0:1
5:5 0:1
6:1 0:2
6:6 0:2
5:6 0:1
6:5 0:2
5:6 0:1
5:0 0:3
5:3 0:3
5:9 0:2
5:4 0:1
5:8 0:2
5:3 0:1
6:0 0:2
5:4 0:1
5:7 0:3
5:5 0:1
3:2 0:3
5:0 0:2
5:3 0:1
5:2 0:3
5:6 0:2
5:5 0:1
101 3:8
43 6:0
87 1:7
94 1:3
96 1:7
95 1:7
105 3:3
95 1:5
96 2:0
102 3:3
119 3:3
97 1:8
111 3:1
96 2:0
87 3:9
94 3:4
89 3:7
94 1:8
96 2:9
93 2:0
97 3:0
95 2:0
92 5:2
95 2:3
55 4:9
88 3:7
92 2:2
83 4:4
91 4:6
97 2:1
95:1 3:8
38:5 6:3
19:6 2:1
80:7 4:6
96:3 0:8
94:8 3:2
85:3 2:4
81:5 6:7
98:4 0:2
27:4 2:9
97:6 1:3
95:6 0:8
82:4 4:8
93:8 2:3
38:6 3:1
94:3 3:5
55:8 5:8
95:1 1:0
40:1 5:2
84:8 6:5
85:3 5:0
86:2 2:9
84:2 5:8
81:6 4:2
36:7 7:6
46:8 6:7
89:1 4:7
80:8 5:0
91:9 2:2
89:0 5:7
4:6 4:0
47:7 6:2
80:1 2:1
18:3 4:8
3:3 0:9
0:4 0:2
0:5 0:2
0:7 0:5
1:1 0:2
64:8 4:2
0:3 0:3
3:6 0:8
12:5 3:9
5:4 2:3
16:7 2:6
0:1 0:1
40:3 6:8
3:3 1:0
51:3 5:6
8:7 6:7
7:4 4:8
11:0 2:7
5:4 4:1
17:3 4:3
59:9 8:8
36:0 7:6
3:4 2:2
13:7 5:2
0:7 0:3
6:4 5:5
5:2 0:2
8:7 1:0
13:0 0:3
6:0 0:4
3:9 0:3
6:8 1:7
2:3 0:1
3:8 0:8
3:4 0:4
7:7 0:4
3:4 0:5
3:6 0:7
4:6 0:7
3:7 0:3
6:1 0:5
3:7 0:6
6:7 0:6
4:2 0:1
9:0 0:7
5:5 1:2
4:0 0:6
3:8 0:2
4:2 1:3
5:0 0:6
28:2 2:8
9:4 1:0
3:4 0:5
5:0 1:0
2:7 0:1
5:8 1:8
296 41:7
ÿ101 38:2
ÿ53 37:7
153 45:2
248 45:5
405 18:2
388 18:7
389 7:2
322 26:9
25 20:2
410 45:0
268 43:8
167 50:4
299 34:5
0 32:3
336 11:5
63 48:9
264 37:2
24 21:3
286 39:0
313 38:0
83 18:1
210 49:3
ÿ84 45:4
ÿ185 8:0
ÿ71 21:9
240 53:0
102 35:1
285 32:0
232 61:4
E: estuarine site; L: littoral site; I: intertidal site.
matter content in the sediments is higher in the estuaries
(2.3±28.2%) than in littoral zone (3.4±6.8%). This corresponds to a higher range of the mud content within the
sediments (0.3±80.1% and 0.1±17.3%, respectively). The
redox potential ranges from )185 to 410 mV within the
estuaries, and from )84 to 405 mV within the littoral
samples.
From 30 stations, some 114 samples of benthos have
been obtained over a 4 year period. These samples
correspond to dierent environments (estuarine, littoral,
intertidal, subtidal) and physico-chemical characteristics
(reduced and oxidized sediments, hypoxia and oversaturation in the bottom waters, poor organic matter
proportion and enrichment, etc.).
After the application of the BC, considering its correspondence with the BI (Table 1), the results were: 2
samples with a BI 0; 23 samples of BI 1; 48 samples
of BI 2; 15 samples of BI 3; 7 samples of BI 4; 6
samples of BI 5; 6 samples of BI 6; and 7 samples of
BI 7.
Fig. 3 shows the results obtained by comparing different biological parameters, on samples having the
same biotic indices. The BI 7 is equivalent to an azoic
site, so all the biological parameters are equal to 0 in
these particular samples.
1104
The mean abundance increases from 36.7 ind mÿ2
(BI 0) to 2 559 ind mÿ2 (BI 6), with the exception of
BI 5, with a value of 456 ind mÿ2 (Fig. 3(a)). Within
the lowest of the Biotic Indices (0, 1 and 2), the standard
error of the mean is very small; it is progressively larger
in the highest.
Statistical analyses were made considering the BC
because, as this coecient can derive continuous values,
it is more suitable for this purpose than the BI. Taking
into account all the samples analysed, the non-parametric Spearman rank correlation between the abundance and the BC is not statistically signi®cant
(p > 0:05).
On the other hand, biomass (Fig. 3(b)) increases from
0.1 g mÿ2 (BI 0) to 14.3 g mÿ2 (BI 4). However for
Biotic Indices 5 and 6, dominated by small opportunistic
species, the biomass is lower than 4 g mÿ2 . There is no a
statistically signi®cant correlation between biomass and
BC (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 progressively from 26 to 27 species (BI 1 and 2) to 0
species (BI 7). Richness and BC are highly correlated
(p < 0:001, Spearman rank correlation).
Volume 40/Number 12/December 2000
Fig. 3 Mean and standard error values of dierent biological
parameters 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).
Numerical diversity (Fig. 3(d)) shows a similar pattern
to that of richness. There is a progressive decrease in the
mean values, from 3.5 bits indÿ1 (BI 1) to 0 bits indÿ1
(BI 7), with the exception of BI 0 which is associated
with a low value (0.6 bits indÿ1 ). Biomass diversity has
values of about 1.6 bits gÿ1 , between BI 1 to 4; then, it
decreases to 0 (BI 7). Both variables are correlated
with BC (p < 0:001 and p < 0:05 for numerical and
biomass diversities, respectively), using Spearman rank
correlation.
The relationships between some of the sedimentological and water quality parameters and biotic indices
are shown in Fig. 4. BI 0 is associated with the highest
mean redox potential (Fig. 4(a): 360 mV). This parameter becomes progressively lower, with BI 7 having a
mean potential which is very reduced (±125 mV). Samples with low biotic indices (0 and 1) are associated with
less than 2% of mud (Fig. 4(b)) and the values increase
to 63% (BI 7). Some anomalies were detected in
BI 5 and 6, which present 10±20% of mud. The organic matter content has a similar pattern of distribution to that of granulometry (Fig. 4(c)). Data on the
mean bottom dissolved oxygen content are presented in
Fig. 4(d). The highest value corresponds to BI 0
Fig. 4 Mean and standard error values of dierent sedimentological
and water quality parameters obtained on samples having the
same biotic indices. (a) redox potential; (b) percentage of mud;
(c) organic matter content; and (d) bottom dissolved oxygen
content.
1105
Marine Pollution Bulletin
(6.5 ml lÿ1 ), decreasing to 2.6 ml lÿ1 at BI 7. The
Spearman rank correlations between these variables and
BC are highly signi®cant (p < 0:001).
The mean concentrations relating to some of the
heavy metals in the sediments associated to each BI are
shown in Fig. 5. Arsenic and mercury contents do not
reveal any clear pattern of distribution with the BI.
Other metals present increasing concentrations from
BI 0 to BI 7, with the exception of some speci®c
peaks (BI 3, for chromium and nickel; and BI 6, for
lead and copper) and troughs (BI 4 and 5, for cadmium, nickel and zinc). Except arsenic and mercury all
the metals are positively correlated with BC (p < 0:01,
Spearman rank correlations).
On the other hand, the organic compounds (Fig. 6) do
not show a similar pattern to that of the metals. Only
PCB increase in their concentrations from BI 0 to
BI 7; however the dierences are very small. PAH is at
their smallest concentrations in BI 5 and 6. The only
signi®cant correlation is found between BC and PCB
(p < 0:05, Spearman rank correlation).
Comparing the percentage of samples of each BI that
goes beyond the ER-L (or Eects Range-Low, representing concentrations below which adverse eects to
fauna are expected to occur rarely (Long et al., 1995)),
the data presented in Fig. 7 shows that BI 0 does not
include samples that surpass these limits for metals and
organic compounds. Normally, the other biotic indices
Fig. 5 Mean and standard error values of eight heavy metal contents
in sediments obtained on samples having the same biotic
indices.
Fig. 6 Mean and standard error values of four organic compound
contents in sediments obtained on samples having the same
biotic indices.
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Volume 40/Number 12/December 2000
Fig. 7 Percentage of samples of each biotic index that goes beyond the
ER-L (or Eects Range-Low, representing concentrations
below which adverse eects are expected to occur rarely), for
seven heavy metals and three organic compounds.
increase progressively in the percentage of samples surpassing these limits (see data presented for arsenic,
mercury, nickel, lead, copper, chromium, PCB and
DDT).
Discussion
Many of the biotic indices developed in the literature
(Clements et al., 1992; Mouthon, 1993; Stark, 1993;
Grall and Glemarec, 1997; Roberts et al., 1998, etc.)
have been based on the paradigm of Pearson and Rosenberg (1978), as stated by Weisberg et al. (1997) in
developing their own index. The paradigm states that
benthic communities respond to improvements in habitat quality in three progressive steps: the abundance
increases; species diversity increases; and dominant
species change from pollution-tolerant to pollutionsensitive species.
This generally accepted paradigm has been adapted
from Grall and Glemarec (1997) in this contribution, in
order to obtain an European BI. This should be able to
distinguish easily estuaries and coastal reference sites
from polluted sites, with dierent levels of anthropogenic or natural degradation.
The index derived provides a semi-quantitative measurement of the degree of impact on soft-bottom macrofauna, which is re¯ected by changes in the qualitative
and quantitative community composition.
As the BI has been established on the basis of analysis
of samples obtained from a monitoring network, with a
prevalence of polluted sites, there are only two unpolluted samples (BI 0) which correspond to a `normal'
community (sensu Grall and Glemarec, 1997). The diversity results do not correspond to those expected from
the aforementioned paradigm, because the richness is
very low. Conversely, samples with BI 1 (also unpolluted in the present proposal, corresponding to an
impoverished community) or higher, BI 2±6 (corresponding to slightly to heavily polluted sites) have
well-de®ned values of biological parameters; this is as
might be expected from the results of Pearson and
Rosenberg (1978).
Some biotic indices, or Coecients of Pollution (i.e.
Bogdanos and Satsmadjis, 1985) do not appear to be
suitable for application in some cases. This is due to the
lack of sensitivity of these indices to intermediate pollution levels (MAFF, 1993), corresponding with slightly
polluted areas. Hily (1984) and Grall and Glemarec
(1997) have described similar diculties.
The above limitation appears to be due to a general
under-estimation of the faunal abundance in comparison with unpolluted areas. This is because faunal
abundance will increase under slight to moderate pollution, but numbers of species can either stay constant
or show only a slight increase. In the present proposal,
this problem appears to be eliminated because the approach has a high sensitivity at these levels, with wellde®ned values in the biological parameters.
Organic enrichment and muddy bottoms, associated
with subsequent low redox potential and hypoxia, are
related with opportunistic species (Majeed, 1987) in
`heavily polluted' levels, according to the BI (BI 5±7).
Diaz and Rosenberg (1995) have suggested that benthic
infaunal mortality could be initiated when the oxygen
concentration falls below 2 ml lÿ1 . Ritter and Montagna
(1999) have recently proposed that 3 mg lÿ1 ( 2.14 ml
lÿ1 ) de®nes the breakpoint between normoxic and hypoxic benthic communities. The mean oxygen concentration obtained for BI 7 indicates that life could be
very limited in those sites. However, within BI 6, there
1107
Marine Pollution Bulletin
are some situations of very low oxygen concentration
which explain the presence of species which are resistant
to severe or moderate hypoxia. These species are classi®ed within ecological Groups IV and V.
Samples with BI 6 and 7 are associated with sites
that experience periodic hypoxia, consisting of repeated
brief periods (days or weeks, in the case of BI 6) or
seasonal hypoxia (months, in the case of BI 7), that
generate mass mortality or complete elimination of the
macrofauna. Some of the samples with BI 7 are
located within the Bilbao estuary, for which S
aiz-Salinas
(1997) and Gonzalez-Oreja and S
aiz-Salinas (1998) have
demonstrated that the oxygen limitation represents the
key factor in the estuarine defaunation of sampling
stations within the estuary.
Physico-chemical results related to the BI (see Fig. 4)
have some unexpected results at the level of BI 5 and
6. The trend of increasing percentages of mud and organic matter, together with decreasing redox potential,
break-down at these particular levels. BI 5 and 6
correspond to high percentages of ecological Group V
(with a mean of 77.5% of species in BI 5, together with
92.7% in BI 6). These species are mainly depositfeeders. As such, they could modify the proportion of
organic matter in the sediments on which they feed and,
subsequently, modify the grain size composition of the
sediments. The optimal grain size may be dierent for
the settling larvae, juveniles and adults of a variety of
deposit-feeders (Snelgrove and Butman, 1994), changing
their physico-chemical properties. For example, Hall
(1994) has stated that faecal pellets of benthic invertebrates modify the grain size of the sur®cial sediments.
In spite of the fact that hypoxia seems to control the
presence of the groupings with BI 7 and that organic
matter content is very important in ascribing samples to
the BI, ecotoxicological eects appear to play only a
secondary role in the analyses; however it may have had
an eect in the longer time, as cited by Saiz-Salinas
(1997) for the Bilbao Estuary.
In order to validate the derived BI, for more general
application, four stations from the 30 stations sampled
have been selected for more detailed analysis. The evolution of the percentage of ecological grouping, the BI
and the BC, derived for between 1995 and 1998, at these
stations is shown in Fig. 8.
Within the Urdaibai estuary (Figs. 1 and 8(a)) the
results obtained from a single station, in the inner part
of the estuary, shows a dominance of ecological Group
III. This is characteristic of estuarine communities located at sites with organic matter inputs. The derived BI
shows that, in 1995 and 1996, the site is slightly polluted
(BI 2) due mainly to the aforementioned organic
matter enrichment. In 1997 and 1998, the BI increases
progressively (BI 3 and 4); as such classifying this
station as `meanly polluted'. Such a trend is caused by
the increasing dominance of ecological Group V, which
indicates the presence of opportunistic species. On the
other hand, the BC increases gradually with time, which
indicates a rising contamination in this site during the
last years.
The increase in the BI could be the result of dredging
activities undertaken along this particular estuary,
within the last few years. At the same time, there are
changes in the sediment composition, the abundance of
suspended matter, etc. These provide the basis for an
increase in the opportunistic species at this particular
location.
In February 1995, the station in the Oria estuary
(Figs. 1 and 8(b)), was located some 500 m landward of
the mouth. Group I was dominant and the BI (2) provides a classi®cation of the site as `slightly polluted'. In
1995 and 1996, some channelling works were under-
Fig. 8 Evolution of the percentage of ecological groups (I±V), the BI
and the BC, derived for between 1995 and 1998, for the stations
showed in Fig. 1: Station 10; Station 21; Station 13; and Station
24.
1108
Volume 40/Number 12/December 2000
taken in this estuary, extending the mouth of the estuary
some 500 m oshore. This development has led to an
increase in the distance from the mouth of the estuary to
the sampling station, with a subsequent change in the
physico-chemical conditions (Borja et al., 1999a). This
change resulted in an increase in the mud and organic
matter content, together with a decrease in dissolved
oxygen. This change in the physical setting provides an
explanation for the increase in the dominance of ecological Groups III and V (more characteristic at the
inner part of the estuary), modifying the BI to `meanly
polluted' (3). The BC increased during this period, from
1.4 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 been
subjected to a sewerage plan, eliminating urban and
industrial euent discharges into the estuarine waters.
The estuary was dominated by the opportunistic Group
V in 1995, with a BI of 3 (meanly polluted). Following
the introduction of the sewerage scheme, the ecological
Group I, composed of species that are sensitive to pollution, increased in its dominance. This represented, in
1997 and 1998, nearly 100% of the community.
Throughout these two last years, the BI is 0. The BC
decreases from 4.2 in 1995 to 0.4 in 1996 and near 0 in
1997 and 1998. So, in the last two years this station can
be classi®ed as an unpolluted site.
Finally, within the coastal area of Momp
as, near San
Sebastian (Figs. 1 and 8(d)), there is an important
change in the ecological group composition between
1995 and 1996. At the beginning of this period, there is a
co-dominance of Groups V, I and II. However, there is a
clear dominance of Group V from 1996 to 1998. At the
same time, the BI changes from 2 (slightly polluted) to
5±6 (heavily polluted). The BC, which was 3.0 in 1995,
increased to values between 5.3 and 5.9 during the last
three years. This particular coastal area has received
large amounts of domestic and industrial waste from the
San Sebastian area since the 1970s. Further, in 1995 and
1996, some sewerage works were constructed and an
important volume of urban and industrial polluted waters, derived from nearby areas such as Pasajes or
Tximistarri, were diverted to Momp
as. The waste includes contaminants (heavy metals and organic compounds) and a high amount of organic matter
originating from the paper manufacturers (Franco et al.,
1999).
Conclusions
The BC, proposed here as a BI to establish the ecological quality of the soft-bottom benthos within the
European coastal environments, takes into account the
faunal composition. As such, it ascribes each species to
an ecological grouping, according to their sensitivity to
an increasing stress gradient.
The dierent composition, in terms of the abundance
of 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 bottom conditions in a discreet range from 0 (unpolluted)
to 7 (extremely polluted). This composition is governed
by the physico-chemical factors within the sediments
and the overlying water column in terms of: organic
matter content; percentage of mud within the sediments;
dissolved oxygen content within the bottom waters; and
the concentration of pollutants.
Biological parameters (such abundance, richness,
biomass or diversity) provide a useful (and more
broadly applicable) description of each level of the BI. It
is considered (as described by Dauer, 1993) that biological criteria may complement toxicity and chemical
assessment methods, to serve as independent evaluations
of the ecological quality of marine and estuarine ecosystems.
Validation of the model developed shows that dierent anthropogenically changes in the environment can
be detected through the use of the BI, including alterations to the natural system such as dredging, engineering
works, sewerage plans and the dumping of polluted
waters. On the other hand, the BC provides a more
accurate view of the evolution of the ecological status of
a particular location. Further, the fact that this particular coecient can derive continuous values makes it
more suitable for application to statistical analysis than
the BI (i.e. temporal trend analysis).
The BI proposed here is relatively simple and can,
meaningfully, be applied when attempting to determine
the ecological status of European coastlines. Although
this index has been developed in the Bay of Biscay, the
methodology can be applied for other European coastal
areas, only conditioned by the assignation of the species
to the ecological groups described here. In fact, many of
the species compiled in the Appendix A are present in
North Sea and Mediterranean. So, the index may be
improved with the contributions of newly assigned
species from these seas and further examples of its more
general application and validation.
Finally, this index facilitates the understanding of
complex benthic data, summarizing a considerable
amount of ecological information into a single representative value.
This study was supported by dierent contracts undertaken between
the Department of Land Action, Housing and Environment of the
Basque Government and AZTI. One of the authors (V. Perez) was
supported by a grant from the Department of Agriculture and Fishing
of the Basque Government. We thank the sta of the Department of
Oceanography of AZTI for their assistance during the ®eld sampling
and laboratory analyses and the INSUB Group that was charged of
the taxonomical analysis. We wish to thank also Professor Michael
Collins (School of Ocean and Earth Science, University of Southampton, UK) and an anonymous referee for kindly advising us on
some details of this paper.
Appendix A
See Table 3.
1109
1110
TABLE 3
List of species and taxa (in alphabetical order) that have been found in all the stations along the whole studied period (the assigned ecological groups (see text) are also shown).a
Species
Species
Group
Species
Group
Species
Group
Species
Group
I
I
II
III
III
III
III
III
I
I
I
I
I
I
I
I
I
N.A
I
I
I
N.A
N.A
N.A
N.A
III
N.A
I
I
I
I
I
I
I
I
I
I
I
I
I
I
I
I
I
I
I
I
III
I
I
I
Angulus tenuis
Anomia ephippium
Anoplodactylus petiolatus
Anoplodactylus pygmaeus
Antenella sp.
Anthozoa sp.
Anthura gracilis
Aonides oxycephala
Aora gracilis
Aora typica
Aphelochatea multibranchiis
Apherusa cirrus
Apherusa ovalipes
Aphonupis grubei
Aphrodite aculeata
Apicularia guerini
Apistobranchus tullbergi
Aponuphis bilineata
Aporrhais pespelecani
Aporrhais sp.
Apseudes latreillei
Arcturella sp.
Arenicola marina
Aricia latreilli
Aricidea catherinae
Aricidea cerruti
Aricidea cf. assimilis
Aricidea fragilis
Aricidea jereysii
Aricidea minuta
Aricidea sp.
Armandia cirrosa
Armandia spp
Aspidosiphon muelleri
Astacilla longicornis
Astarte sp.
Astarte sulcata
Astarte triangularis
Asterina gibosa
Astropecten irregularis
Astropecten irregularis typicus
Athanas nitescens
Athecata sp.
Atylus falcatus
Atylus guttatus
Atylus sp.
Atylus swammerdami
Atylus vedlomensis
Audouinia tentaculata
Autolytus longeferiens
Autolytus sp.
I
I
N.A
N.A
I
I
I
III
I
I
N.A
I
I
I
N.A
I
I
II
I
I
III
N.A
N.A
I
I
I
I
I
I
I
I
I
I
I
I
I
I
I
I
I
I
I
I
I
I
I
I
I
IV
N.A
N.A
Bela powisiana
Bela sp.
Bittium reticulatum
Boccardia chilensis
Boccardia polybranchia
Boccardia sp.
Bodotria arenosa
Bodotria scorpioides
Brada villosa
Branchiomma vesiculosum
Branchiostoma lanceolata
Brania oculata
Brania pusilla
Bugula sp.
Callianassa sp.
Callianassa subterranea
Callianassa truncata
Calliostoma papillosum
Calliostoma zizyphinum
Calyptraea sinensis
Campylaspis glabra
Capitella capitata
Capitella sp.
Capitellides giardi
Capitomastus minimus
Caprella fretensis
Caprella linearis
Caprella penantis
Carcinus maenas
Caryophyllia smithi
Caulleriella alata
Caulleriella bioculata
Caulleriella sp.
Caulleriella zetlandica
Cavernularia pusilla
Ceradocus semiserratus
Cerastoderma edule
Cerastoderma lamarcki
Ceratostoma erinaceum
Cerebratulus marginatus
Cerebratulus sp.
Cereus pedunculatus
Ceriantario sp.
Cerianthus lloydii
Cerianthus membranaceus
Cerianthus sp.
Cestopagurus timidus
Chaetopterus variopedatus
Chaetozone B spp
Chaetozone cf. gibber
Chaetozone gibber
I
I
I
I
I
I
II
II
N.A
I
I
II
II
I
III
III
III
I
I
I
N.A
V
V
V
IV
N.A
N.A
N.A
III
I
III
III
III
III
I
I
III
III
I
III
III
I
I
I
I
I
I
I
IV
IV
IV
Chone infundibuliformis
Chone sp.
Chthamalus stellatus
Circe minima
Circulus striatus
Cirratulus chrysoderma
Cirratulus cirratus
Cirriformia tentaculata
Cirripedo sp.
Clausinella fasciata
Clavidae
Clymene cf. praetermisa
Clymene lumbricoides
Clymene modesta
Clymene oerstedii
Clytia sp.
Cnidaria sp.
Cochlodesma praetenue
Copepoda indet.
Cop
epodo sp.
Corbula gibba
Corophium acherusicum
Corophium acutum
Corophium arenarium
Corophium insidiosum
Corophium multisetosum
Corophium sp.
Corophium volutator
Coryne pusilla
Corystes cassivelaunus
Cossura longocirrata
Cossura pygodactylata
Cossura sp.
Crangon allmani
Crangon crangon
Crassostrea angulata
Crepidula fornicata
Cucumaria elongata
Cucumaria sp.
Cultellus pellucidus
Cumopsis fagei
Cumopsis sp.
Cyathura carinata
Cyclope neritea
Cylichna cylindracea
Cylichna sp.
Cylichnina subcylindrica
Cymodoce truncata
Cythara attenuata
Cythara costata
Dardanus arrosor
II
II
I
I
I
IV
IV
IV
I
I
I
I
I
I
I
I
I
N.A
N.A
N.A
III
III
III
III
III
III
III
III
I
I
N.A
N.A
N.A
I
I
III
III
I
I
I
II
II
III
I
I
I
I
I
I
I
N.A
Diastylis rugosa
Diastylis sp.
Diastylis tumida
Diodora apertura
Diogenes pugilator
Diopatra neapolitana
Diplocirrus glaucus
Dispio uncinata
Divaricella divaricata
Donax trunculus
Doris sp.
Dosinia exoleta
Dosinia juv. indet.
Dosinia lupinus
Dosinia sp.
Drilonereis ®lum
Ebalia sp.
Ebalia tuberosa
Echinocardium cordatum
Echinocyamus pusillus
Echinoidea sp.
Echiuroidea sp.
Echiurus echiurus
Edwardsia sp.
Ehlersia ferrugina
Ensis sp.
Eocuma dimorpha
Eocuma dollfusi
Epilepton clarkiae
Epithonium clathrus
Epitonium turtoni
Ericthonius brasilensis
Eteone longa
Eteone picta
Euclymede praetermissa
Euclymene anis
Euclymene oerstedii
Euclymene sp.
Euclymenidae indet.
Eudorella truncatula
Eulalia bilineata
Eulalia mustela
Eulalia sanguinea
Eulalia sp.
Eulalia tripunctata
Eulalia viridis
Eulimella acicuta
Eulimella sp.
Eumida bahusiensis
Eumida sanguinea
Eumida sp.
I
I
I
I
II
I
I
III
I
I
I
I
I
I
I
II
N.A
N.A
I
I
I
I
I
II
N.A
I
II
II
I
I
I
N.A
II
II
I
I
I
I
I
N.A
II
II
II
II
II
II
I
I
II
II
II
Marine Pollution Bulletin
Abarenicola claparedi
Abarenicola sp.
Abissoninoe hibernica
Abra alba
Abra nitida
Abra prismatica
Abra sp.
Abra tenuis
Acanthocardia aculeata
Acanthocardia echinata
Acanthocardia paucicostata
Acanthocardia sp.
Acanthocardia tuberculata
Acanthochitona critinus
Acanthochitona fascicularis
Achelia hispida
Achelia simplex
Aclis gulsonae
Acronida brachiata
Acteon sp.
Actinia equina
Aglaophamus rubella
Aglaophamus sp.
Aiptasia mutabilis
Alcyonacea indet
Alkmaria romijni
Alpheus glaber
Alvania crassa
Alvania semistriata
Alvania sp.
Amatea trilobata
Amathia pruvot
Ampelisca brevicornis
Ampelisca cf. spooneri
Ampelisca heterodactyla
Ampelisca juv. indet.
Ampelisca sarsi
Ampelisca sp.
Ampelisca spinifer
Ampelisca spinimana
Ampelisca tenuicornis
Ampelisca toulemonti
Ampharete ®nmarchica
Ampharete grubei
Ampharete juv. indet.
Ampharete lindstroemi
Ampharete sp.
Amphicteis gunneri
Amphipholis squamata
Amphitrite johnstoni
Amphiura brachiata
Group
I
I
I
I
II
II
II
II
I
I
I
II
II
N.A
I
N.A
I
I
I
I
I
III
I
I
I
I
I
I
I
I
I
I
I
N.A
I
II
II
II
II
II
II
II
II
II
II
II
I
III
II
II
I
I
I
N.A
N.A
II
Axionice maculata
Bachycuma brevicornis
Balcis alba
Barleeia rubra
Bathyporeia elegans
Bathyporeia nana
Bathyporeia pelagica
Bathyporeia pilosa
Bathyporeia sarsi
Bathyporeia sp.
Bathyporeia tenuipes
Bela nebula
Hesionura elongata
Heterocirrus bioculatus
Heterocirrus spp
Heteromastus ®liformis
Hexacorallia sp.
Hiatella artica
Hinia incrassata
Hinia juv. indet.
Hinia pygmaea
Hinia reticulata
Hippolyte varians
Hippomedon denticulatus
Hyala vitrea
Hyale nilssoni
Hyalinoecia bilineata
Hyalinoecia fauveli
Hyalinoecia sp.
Hydrobia ulvae
Hydroides norvegica
Idotea linearis
Idunella picta
Inachus dorsettensis
Inachus sp. larva
Iphimedia obesa
Iphinoe serrata
Iphinoe sp.
Jaera albifrons
Jaera sp.
Janira maculosa
Jasmineira elegans
Jupiteria minuta
Kefersteinia cirrata
Kellia suborbicularis
Labidoplax cf. thomsoni
Labidoplax digitata
Labidoplax spp
Lacydonia miranda
Lagisca extenuata
Lanice cirrata
Lanice cirrata
Lanice conchilega
Lanice conchilega
Lanice spp
Laonice sp.
N.A
N.A
I
II
I
I
I
I
I
I
I
I
II
IV
IV
III
I
I
II
II
II
II
I
I
I
I
N.A
N.A
N.A
III
N.A
N.A
N.A
I
I
I
I
I
I
I
N.A
N.A
N.A
N.A
I
I
I
I
N.A
II
III
III
II
II
II
N.A
Chaetozone setosa
Chaetozone sp.
Chamelea gallina
Chamelea gallina striatula
Chamelea striatula
Chauvetia brunnea
Cheirocratus sundevallii
Cheriocratus sp.
Chironomida
Chlamys varia
Chone collaris
Chone ®licaudata
Leucothoe spinicarpa
Levinsenia gracilis
Lilleborjia pallida
Liocarcinus arcuatus
Liocarcinus arcuatus
Liocarcinus depurator
Liocarcinus holsatus
Liocarcinus marmoreus
Liocarcinus pusillus
Liocarcinus sp.
Liocarcinus vernalis
Liocarcinus zariquieyi
Listriella picta
Loripes lucinalis
Lucinoma borealis
Lucinoma borealis
Lumbrinerides sp.
Lumbrineriopsis paradoxa
Lumbrineris cf. gracilis
Lumbrineris emandibulata
Lumbrineris emandibulata mabiti
Lumbrineris gracilis
Lumbrineris impatiens
Lumbrineris latreilli
Lumbrineris latreilli
Lumbrineris sp.
Lunatia alderi
Lutraria angustior
Lutraria lutraria
Lutraria lutraria
Lutraria sp.
Lyonsia norvegicum
Lysianassa ceratina
Lysianassa insperata
Lysidice ninetta
Lysippe labiata
Macoma baltica
Macropodia rostrata
Mactra corallina
Mactra stultorum
Mactracea indet.
Maera grossimana
Maera othonis
Maera sp.
IV
IV
I
I
I
I
I
I
IV
I
II
II
I
N.A
I
I
I
I
I
I
I
I
I
I
I
I
I
I
II
II
II
II
II
II
II
II
II
II
II
I
I
I
I
I
I
I
II
N.A
I
I
I
I
I
I
I
I
Demonax sp.
Demospongia sp.
Dentalium novemcostatum
Dentalium sp.
Desdemona cf. ornata
Desdemona ornata
Devonia perrieri
Diastylis bradyi
Diastylis cf. tumida
Diastylis cornuta
Diastylis laevis
Diastylis lucifera
Marphysa fallax
Marphysa sanginea
Marphysa sp.
Marphysa sp. (belli?)
Martastherias glacialis
Mediomastus fragilis
Megaluropus agilis
Megamphopus cornutus
Melinna cristata
Melinna palmata
Melinna sp.
Melita gladiosa
Melita palmata
Merceriella enigmatica
Metaphoxus fultoni
Metaphoxus pectinatus
Metazoea de porcellanidae
Microdeutopus anomalus
Microdeutopus damnoniensis
Microdeutopus sp.
Microdeutopus stationis
Microdeutopus versiculatus
Microphthalmus sczelkowii
Microspio sp.
Micrura sp.
Modiolula phaseolina
Modiolus barbatus
Modiolus gallicus
Modiolus modiolus
Monoculodes carinatus
Monopylephorus irroratus
Montacuta ferruginosa
Musculus discors
Mya arenaria
Myrtea spinifera
Mysella bidentata
Mysia undata
Mysidacea
Mystides elongata
Mystides limbata
Mytilaster minimun
Mytilus edulis
Nassarius incrassatus
Nassarius reticulatus
N.A
I
I
I
II
II
I
I
I
I
I
I
II
II
II
II
I
III
I
I
III
III
III
I
III
II
I
I
N.A
I
I
I
I
I
N.A
N.A
N.A
I
I
I
I
I
V
II
I
II
I
I
I
II
II
II
I
III
II
II
Eunice harassii
Eunice sp.
Eunice vittata
Euphrosyne foliosa
Eurydice anis
Eurydice pulchra
Eurydice sp.
Eurydice spinigera
Eurynome aspera
Eurynome spinosa
Eurysyllis tuberculata
Exogone naidina
Nephtys cirrosa
Nephtys hombergi
Nephtys hystricis
Nephtys incisa
Nephtys juv. spp
Nephtys kersivalensis
Nephtys paradoxa
Nephtys sp.
Nephtys sp. juv.
Nephtys spp
Nereimyra punctata
Nereiphylla rubiginosa
Nereis caudata
Nereis cf. lamellosa
Nereis diversicolor
Nereis longissima
Nereis sp.
Nothria geo®liformis
Nothria lepta
Nothria sp.
Notirus irus
Notocirrus sp.
Notomastus latericeus
Notomastus lineatus
Notomastus sp.
Nucula nitida
Nucula nitidosa
Nucula nucleus
Nucula sp.
Nucula sulcata
Nucula turgida
Ocenebra erinacea
Odostomia sp.
Oligochaeta
Onuphidae juvenil
Onuphis cf. geophiliformis
Onuphis conchylega
Onuphis eremita
Ophelia bicornis
Ophelina acuminata
Ophiocentrus brachiatus
Ophiocomina nigra
Ophiodromus ¯exuosus
Ophiopsila aranea
II
II
II
I
I
I
I
I
I
I
II
II
II
II
II
II
II
II
II
II
II
II
III
N.A
IV
III
III
III
III
II
II
II
I
N.A
III
III
III
I
I
I
I
I
I
II
II
V
II
II
II
II
I
N.A
I
I
II
I
Volume 40/Number 12/December 2000
1111
Amphiura chiajei
Amphiura ®liformis
Amphiura juv. indet.
Amphiura sp.
Anaitides lineata
Anaitides maculata
Anaitides mucosa
Anaitides sp.
Anapagurus hyndmani
Anapagurus laevis
Anapagurus sp.
Anguilla anguilla
Exogone sp.
Fabricia sabella
Fabulina fabula
Filograna implexa
Galathea intermedia
Galathea sp.
Galathea squamifera
Galathowenia oculata
Galeomna turtoni
Gammarella fucicola
Gammaridea
Gammaropsis palmata
Gammaropsis shophiae
Gammaropsis sp.
Gammarus insensibilis
Gammarus sp.
Gari costulata
Gari depressa
Gari fervensis
Gari tellinella
Gariidae indet.
Gattyana cirrosa
Gibbula magus
Glycera alba
Glycera capitata
Glycera convoluta
Glycera lapidum
Glycera rouxii
Glycera sp.
Glycera tesselata
Glycera tridactyla
Glycera unicornis
Glycinde nordmani
Glycinde nordmanni
Gnathia oxyurea
Gobius niger
Goniada maculata
Goniada sp.
Goodallia triangularis
Gouldia minima
Gregariella barbatella
Guernea coalita
Gymnammodytes semisquamatus
Gyptis capensis
1112
TABLE 3 (CONTINUED)
Species
Species
Group
Species
Group
Species
Group
Species
Group
II
I
II
II
II
II
II
II
II
II
II
II
I
I
I
I
III
II
II
II
I
I
I
I
I
I
I
I
I
III
III
III
N.A
N.A
N.A
N.A
II
II
II
II
II
I
III
III
Leanira yhleni
Lembos sp.
Lepidonotus clava
Lepidonotus squamatus
Leptocheirus pectinatus
Leptocheirus pilosus
Leptochelia savignyi
Leptochiton asellus
Leptochiton cancellatus
Leptochiton inhaerens
Leptoneris glauca
Leptosynapta cf. gallienei
Leptosynapta gallienei
Leptosynapta inhaerens
Leucothoe incisa
Leucothoe incisa
Leucothoe lilljeborgi
Leucothoe richiardii
Leucothoe sp.
Phyllodoce rosea
Phyllodoce sp.
Phylocheras bispinosus
Phylocheras monacantus
Phylocheras trispinosus
Pilargis verrucosa
Pilumnus hirtellus
Pinnotheres pisum
Pionosyllis serrata
Pisidia longicornis
Pisidium sp. indet.
Pisione remota
Pista cristata
Plakosyllis brevipes
Plathelmintes
Platynereis dumerilii
Pleuronectidae sp.
Podoceus variegatus
Poecilochaetus serpens
Poecilochaetus serpens
Polycirrus aurantiacus
Polycirrus cf. medusa
Polycirrus medusa
Polycirrus sp.
Polycirrus tenuisetis
N.A
N.A
II
II
III
III
N.A
I
I
I
III
I
I
I
I
I
I
I
I
II
II
I
I
I
I
I
N.A
II
I
I
II
I
II
II
III
II
N.A
I
I
IV
IV
IV
IV
IV
Magelona alleni
Magelona ®liformis
Magelona minuta
Magelona mirabilis
Magelona papillicornis
Magelona sp.
Magelona wilsoni
Malacoceros ciliata
Malacoceros fuliginosus
Malacoceros girardi
Malacoceros sp.
Malacoceros vulgaris
Maldane glebifex
Manayunkia aestuarina
Mangelia attenuata
Mangelia nebula
Mangelia smithi
Mangelia sp.
Marphysa bellii
Protodrilus sp.
Psamechinus miliaris
Psammobia costulata
Psammolyce arenosa
Pseudobrania sp.
Pseudocuma longicornis
Pseudocuma similis
Pseudocuma sp.
Pseudopolydora antennata
Pseudopolydora paucibranchiata
Pseudopolydora pulchra
Pseudopolydora sp.
Pseudoprotella phasma
Pseudosyllis brevipennis
Pseudosyllis sp.
Pygospio elegans
Quadrans serratus
Raphitoma purpurea
Raphitoma sp.
Retusa truncatula
Retusa umbilicata
Rhizorus acuminatus
Ringicula auriculata
Ringicula conformis
Ringicula sp.
I
I
I
I
I
I
I
III
V
III
III
III
I
II
I
I
I
I
II
N.A
I
I
II
II
II
II
II
IV
IV
IV
IV
N.A
II
II
III
I
I
I
I
I
N.A
I
I
I
Natantia sp.
Natica alderi
Natica catena
Neanthes caudata
Neanthes irrorata
Neanthes juv. indet.
Neanthes sp.
Nebalia bipes
Nebalia sp. indet.
Nebalia thyphlops
Nematoda
Nematonereis unicornis
Nemertea
Neoamphitrite anis
Neoamphitrite cf. anis
Neoamphitrite sp.
Nephtys assimilis
Nephtys caeca
Nephtys cf. paradoxa
Sphaerosyllis hystrix
Sphaerosyllis pyrifera
Sphaerosyllis sp.
Sphaerosyllis taylori
Sphenia binghami
Spio armata
Spio decoratus
Spio ®licornis
Spio martinensis
Spio sp.
Spiochaetopterus costarum
Spiochaetopterus sp.
Spiochaetopterus typicus
Spiophanes bombyx
Spiophanes kroyeri
Spirobranchus polytrema
Spisula elliptica
Spisula solida
Spisula subtruncata
Staurocephalus rudolphii
Stenothoe monoculoides
Stenothoidae
Sternaspis scutata
Sthenelais boa
Sthenelais cf. minor
N.A
II
II
III
III
III
III
V
V
II
III
II
III
N.A
N.A
N.A
II
II
II
II
II
II
II
I
III
III
III
III
III
III
III
III
III
III
N.A
I
I
I
IV
II
II
III
II
II
Ophiotrix fragilis
Ophiura albida
Ophiura ophiura
Ophiura sp.
Ophiura texturata
Ophiura texturata (juv.)
Ophryotrocha labronica
Ophryotrocha puerilis
Ophryotrocha sp.
Opistodonta pterochaeta
Orbinia cuvieri
Orchomene nana
Orchomene similis
Oriopsis armandi
Oriopsis sp.
Ostrea edulis
Ovatella myosotis
Owenia ®liformis
Owenia fusiformis
Tholarus cranchii
Thracia phaseolina
Thracia villosiuscula
Thyasira ¯exuosa
Thyone fusus
Timoclea ovata
Tonicella marmorea
Tricolia pullus
Triphora adversa
Triphora aspera
Triphora perversa
Trivia monacha
Trophonopsis muricatus
Tryphosella nanoides
Tryphosella sarsi
Tryphosites longipes
Tubi®coides benedii
Tubi®coides pseudogaster
Tubulanus polymorphus
Tubulanus spp
Turbelario sp.
Turboella parva
Turbonilla acuta
Turbonilla elegantissima
Turbonilla lactea
I
II
II
II
II
II
II
II
II
N.A
N.A
N.A
N.A
N.A
N.A
I
N.A
I
I
I
I
I
III
I
I
I
I
I
I
I
I
I
I
I
II
V
V
II
II
N.A
I
I
I
I
Marine Pollution Bulletin
Gyptis rosea
Halcampa sp.
Haminoea navicula
Harmothoe antilopes
Harmothoe cf. lunulata
Harmothoe glabra
Harmothoe imbricata
Harmothoe impar
Harmothoe lunulata
Harmothoe sp.
Harmothoe sp.(antilopes?)
Harmothoe spinifera
Harpinia antennaria
Harpinia pectinata
Harpinia sp.
Haustorius arenarius
Hediste diversicolor
Hermione hystrix
Hesione pantherina
Pachygrapsus marmoratus
Paguroidea indet.
Pagurus bernhardus
Pagurus prideauxi
Pagurus sp. larva
Palaemon serratus
Pandora albida
Pandora inaequivalvis
Pandora pinna
Panoploea minuta
Paradoneis armata
Paradoneis lyra
Paragnathia formica
Paramphitrite tetrabranchia
Paraonis fulgens
Paraonis gracilis
Paraonis lyra
Parapionosyllis cf. gestans
Parapionosyllis gestans
Parapionosyllis labronica
Parapionosyllis minuta
Parapionosyllis sp.
Parathelepus sp.
Pariambus typicus
Pariambus typicus varinermis
Group
a
N.A. ± not assigned.
I
I
I
I
I
I
I
I
III
I
I
I
I
I
II
I
I
I
I
I
II
II
II
II
II
I
I
I
I
N.A
II
II
II
II
II
II
III
II
Polydora antennata
Polydora caeca
Polydora ciliata
Polydora ¯ava
Polydora juv. spp
Polydora ligerica
Polydora ligni
Polydora polybranchia
Polydora pulchra
Polydora sp.
Polygordius apendiculatus
Polymnia nebulosa
Polynoe scolopendrina
Polyophthalmus pictus
Pomatoceros lamarckii
Pomatoceros triqueter
Pontocrates altamarinus
Pontocrates arenarius
Portumnus latipes
Potamilla reniformis
Potamilla sp.
Potamilla torelli
Potamopyrgus jenkinsi
Praxillea oerstedi
Prionospio caspersi
Prionospio cirrifera
Prionospio ehlersi
Prionospio fallax
Prionospio malmgreni
Prionospio multibranchiata
Prionospio sp.
Prionospio steenstrupi
Processa canaliculata
Processa modica
Processa nouveli
Processa parva
Processa sp.
Protodorvillea kefersteini
IV
IV
IV
IV
IV
IV
IV
IV
IV
IV
I
III
II
I
N.A
N.A
I
I
I
N.A
N.A
N.A
II
N.A
IV
IV
IV
IV
IV
IV
IV
IV
I
I
I
I
I
II
Sabella pavonina
Sabella sp.
Sabellaria alveolata
Sabellaria spinulosa
Scalibregma in¯atum
Scaphander lignarius
Schistomeringos caeca
Schistomeringos rudolphi
Scionella lornensis
Sclerocheilus minutus
Scolaricia sp.
Scolaricia typica
Scolelepis fuliginosa
Scolelepis sp.
Scolelepis squamata
Scoloplos armiger
Scrobicularia plana
Scrupocellaria scrupea
Semivermilia sp.
Sertulariidae
Sextonia longirostris
Sigalion cf. mathildae
Sigalion mathildae
Sigalion squamatum
Siphonoecetes kroyeranus
Siphonoecetes sp.
Siphonoecetes striatus
Sipuncula
Skenea sp.
Skenia serpuloides
Socarnes erythrophthalmus
Solen marginatus
Solenacea
Sphaerodoropsis sp.
Sphaeroma monodi
Sphaeroma rugicaudata
Sphaeroma serratum
Sphaerosyllis bulbosa
I
I
I
I
III
I
II
IV
N.A
N.A
I
I
V
III
III
I
III
N.A
N.A
I
II
II
II
II
I
I
I
I
III
N.A
N.A
I
I
N.A
II
II
II
II
Sthenelais limicola
Sthenelais minor
Sthenelais sp.
Streblosoma bairdi
Streblospio dekhuyzeni
Streblospio shrubsolii
Stremblosoma intestinalis
Striarca lactea
Sycon ciliatum
Sycon raphanus
Syllis cornuta
Syllis gerlachi
Syllis gracilis
Syllis prolifera
Syllis sp.
Syllis variegata
Synchelidium haplocheles
Synchelidium maculatum
Tanais dulongii
Tapes decussata
Telepsavus costarum
Telina tenuis
Tellimya ferruginosa
Tellina compressa
Tellina donacina
Tellina fabula
Tellina pusilla
Tellina pygmaea
Tellina sp.
Tellina squalida
Tellina tenuis
Terebella lapidaria
Terebellides stroemi
Terebellomorpha sp. indet
Thalassema neptuni
Tharyx marioni
Thelepus setosus
Thia scutellata
II
II
II
N.A
III
III
N.A
I
I
I
II
II
II
II
II
II
I
I
N.A
I
I
I
II
I
I
I
I
I
I
I
I
I
I
II
I
N.A
N.A
II
Turbonilla rufa
Turbonilla spp
Turritella communis
Turritella triplicata
Unciola crenatipalma
Upogebia cf. tipica
Upogebia deltaura
Upogebia pusilla
Upogebia sp.
Upogebia stellata
Upogebia typica
Urothoe brevicornis
Urothoe elegans
Urothoe poseidonis
Urothoe pulchella
Vauthompsonia cristata
Veneracea
Venerupis aurea
Venerupis pullastra
Venerupis rhomboides
Venerupis senegalensis
Venus casina
Venus fasciata
Venus gallina
Venus juv. sp.
Venus ovata
Venus striatula
Venus verrucosa
Veretillum cynomorium
Veretillum sp.
Verruca stromia
Vituperis esribosa
Xantho pilipes
Xenosyllis scabra
Zenobiana prismatica
Zoantharia sp.
I
I
I
I
N.A
I
I
I
I
I
I
I
I
I
I
N.A
I
I
I
I
I
I
I
I
I
I
I
I
I
I
I
V
N.A
II
II
I
Volume 40/Number 12/December 2000
Parvicardium exiguum
Parvicardium minimum
Parvicardium ovale
Parvicardium papillosum
Parvicardium scabrum
Pectinaria auricoma
Pectinaria koreni
Pectinaria sp.
Perinereis cultrifera
Perioculodes longimanus
Pharus legumen
Phascolion strombi
Phascolion strombus
Phascolosoma elongatum
Phascolosoma granulatum
Phascolosoma vulgare
Phaxas pellucidus
Pherusa monilifera
Pherusa plumosa
Pherusa sp.
Philine aperta
Philine loweni
Philine spp
Pholoe minuta
Pholoe synopthalmica
Phoronis psammophila
Photis longicaudata
Phoxocephalus rudolphii
Phthisica marina
Phyllochaetopterus sp.
Phyllodoce groelandica
Phyllodoce lamelligera
Phyllodoce laminosa
Phyllodoce lineata
Phyllodoce longipes
Phyllodoce maculata
Phyllodoce mucosa
Phyllodoce paretti
1113
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