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. P

EREZ
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 indi-
vidual abundance in ve ecological groups, which are re-
lated 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 af-
fected by subjectivity. Relationships between this coe-
cient and a complementary BI with several environmental
variables are discussed. Finally, a validation of the pro-
posed index is made with data from systems aected by
recent human disturbances, showing that dierent an-
thropogenic changes in the environment can be detected
through the use of this BI. 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 (OConnor, 1992), France (RNO,
1998) or Great Britain (Franklin and Jones, 1994). This
control is centred on physico-chemical and ecotoxico-
logical variables and, less usually, on biological vari-
ables. Dauer (1993) stated that biological criteria are
considered important components of water quality be-
cause: (i) they are direct measures of the condition of the
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 in-
dicators, 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 macro-
benthos 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 macro-
benthic animals are relatively sedentary (and cannot
avoid deteriorating water/sediment quality conditions),
have relatively long life-spans (thus, indicate and inte-
grate water/sediment quality conditions, with time),
consist of dierent species that exhibit dierent toler-
ances to stress and have an important role in cycling
nutrients and materials between the underlying sedi-
ments 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 com-
munities to natural and man-induced changes in water
quality, integrating long-term environmental conditions.
Marine Pollution Bulletin Vol. 40, No. 12, pp. 11001114, 2000
2000 Elsevier Science Ltd. All rights reserved
Printed in Great Britain
0025-326X/00 $ - see front matter PII: S0025-326X(00)00061-8
*Corresponding author.
E-mail address: aborja@azti.es (A. Borja).
1100
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, sedi-
ment and biological quality information from 30 sam-
pling 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 cm
2
). 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 com-
pounds). 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 80C 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 105C, 24 h; then com-
busting at 520C, 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 mate-
rial (BCR marine sediment-harbour PACS-1); dier-
ences with this material were lower than 10%.
For PCB (eight congeners), DDT and HCH deter-
mination 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 com-
pounds) 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 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 data
The identication was undertaken in the laboratory
by means of a binocular microscope (440). After
computing the mean abundance of each taxon, at each
sampling station, the macrobenthic community struc-
ture was described calculating the following descriptors
(Washington, 1984): richness (number of identied
taxa); abundance (N: ind m
2
); numerical diversity
(Shannon Wiener H
/
n
: bits ind
1
); biomass (Dry Weight,
B: g m
2
); and biomass diversity (Shannon Wiener H
/
b
:
bits g
1
).
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 lar-
vae 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) pro-
nounced 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 sen-
sitivity 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 summa-
rized 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 deposit-
feeding tubicolous polychaetes.
Group II. Species indierent to enrichment, always
present in low densities with non-signicant 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
Volume 40/Number 12/December 2000
F
i
g
.
1
P
o
s
i
t
i
o
n
o
f
t
h
e
3
0
s
t
a
t
i
o
n
s
m
o
n
i
t
o
r
e
d
a
l
o
n
g
t
h
e
B
a
s
q
u
e
c
o
a
s
t
-
l
i
n
e
(
N
o
r
t
h
o
f
S
p
a
i
n
)
,
f
r
o
m
1
9
9
5
t
o
1
9
9
8
.
T
h
e
s
t
a
t
i
o
n
s
u
s
e
d
t
o
v
a
l
i
d
a
t
e
t
h
e
m
o
d
e
l
a
r
e
s
h
o
w
n
i
n
b
l
a
c
k
.
1102
Marine Pollution Bulletin
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 (pro-
nounced unbalanced situations). These are deposit-
feeders, 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 sam-
pling 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 identied. These species are representative of
the most important soft-bottom communities present at
European estuarine and coastal systems. The taxa have
been classied (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 Hilys 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 calcu-
lation 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 = (0 % GI) (1X5 % GII)
(3 % GIII) (4X5 % GIV)
(6 % GV)a100X
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 sedi-
ment 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
classication' 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 and
physical characteristic associated with each of the sam-
pling 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 3035 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 (35.335.5).
The range in the percentage of oxygen saturation is
very high within the estuaries (43119%), but ranges in
the littoral stations from 92% to 97%. The organic
Fig. 2 Theoretical model, modied from Hily (1984), Hily et al. (1986)
and Majeed (1987), which provides the ordination of soft-
bottom 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 (07) and an equivalent
continuous BC (values between 0 and 6).
TABLE 1
Summary of the BC and BI (modied from Grall and Glemarec, 1997).
Site pollution classication Biotic Coecient Biotic index Dominating ecological group Benthic community health
Unpolluted 0X0 ` BC _ 0X2 0 I Normal
Unpolluted 0X2 ` BC _ 1X2 1 Impoverished
Slightly polluted 1X2 ` BC _ 3X3 2 III Unbalanced
Meanly polluted 3X3 ` BC _ 4X3 3 Transitional to pollution
Meanly polluted 4X5 ` BC _ 5X0 4 IVV Polluted
Heavily polluted 5X0 ` BC _ 5X5 5 Transitional to heavy pollution
Heavily polluted 5X5 ` BC _ 6X0 6 V Heavy polluted
Extremely polluted Azoic 7 Azoic Azoic
1103
Volume 40/Number 12/December 2000
matter content in the sediments is higher in the estuaries
(2.328.2%) than in littoral zone (3.46.8%). This cor-
responds to a higher range of the mud content within the
sediments (0.380.1% and 0.117.3%, 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 oversat-
uration in the bottom waters, poor organic matter
proportion and enrichment, etc.).
After the application of the BC, considering its cor-
respondence 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 dif-
ferent 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.
The mean abundance increases from 36.7 ind m
2
(BI =0) to 2 559 ind m
2
(BI =6), with the exception of
BI =5, with a value of 456 ind m
2
(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-para-
metric Spearman rank correlation between the abun-
dance and the BC is not statistically signicant
(p b 0X05).
On the other hand, biomass (Fig. 3(b)) increases from
0.1 g m
2
(BI =0) to 14.3 g m
2
(BI =4). However for
Biotic Indices 5 and 6, dominated by small opportunistic
species, the biomass is lower than 4 g m
2
. There is no a
statistically signicant 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 pro-
gressively from 26 to 27 species (BI =1 and 2) to 0
species (BI =7). Richness and BC are highly correlated
(p ` 0X001, Spearman rank correlation).
TABLE 2
Physico-chemical characterisation of sampling stations, showing mean and standard error (SE) values of some sedimentological and water
parameters.
a
Station
number
Station
type
Depth
(m)
Salinity Dissolved
oxygen (ml l
1
)
% Oxygen
saturation
% Sand % Mud % Organic
matter
Redox
potential (mV)
Mean Mean SE Mean SE Mean SE Mean SE Mean SE Mean SE Mean SE
1 E I 23X5 2X3 6X1 0X2 101 3X8 95X1 3X8 4X6 4X0 5X2 0X2 296 41X7
2 E 3 16X2 2X0 3X1 0X5 43 6X0 38X5 6X3 47X7 6X2 8X7 1X0 101 38X2
3 E 14 35X1 0X1 5X0 0X1 87 1X7 19X6 2X1 80X1 2X1 13X0 0X3 53 37X7
4 E 24 35X3 0X1 5X4 0X1 94 1X3 80X7 4X6 18X3 4X8 6X0 0X4 153 45X2
5 L 34 35X3 0X1 5X6 0X1 96 1X7 96X3 0X8 3X3 0X9 3X9 0X3 248 45X5
6 L 32 35X3 0X1 5X5 0X1 95 1X7 94X8 3X2 0X4 0X2 6X8 1X7 405 18X2
7 E I 29X5 1X6 6X1 0X2 105 3X3 85X3 2X4 0X5 0X2 2X3 0X1 388 18X7
8 L 34 35X4 0X0 5X5 0X1 95 1X5 81X5 6X7 0X7 0X5 3X8 0X8 389 7X2
9 L 33 35X4 0X0 5X5 0X1 96 2X0 98X4 0X2 1X1 0X2 3X4 0X4 322 26X9
10 E I 25X7 2X5 6X1 0X2 102 3X3 27X4 2X9 64X8 4X2 7X7 0X4 25 20X2
11 E I 34X8 0X1 6X6 0X2 119 3X3 97X6 1X3 0X3 0X3 3X4 0X5 410 45X0
12 L 31 35X5 0X0 5X6 0X1 97 1X8 95X6 0X8 3X6 0X8 3X6 0X7 268 43X8
13 E I 26X3 3X0 6X5 0X2 111 3X1 82X4 4X8 12X5 3X9 4X6 0X7 167 50X4
14 L 34 35X5 0X0 5X6 0X1 96 2X0 93X8 2X3 5X4 2X3 3X7 0X3 299 34X5
15 E I 28X9 1X6 5X0 0X3 87 3X9 38X6 3X1 16X7 2X6 6X1 0X5 0 32X3
16 L 34 35X4 0X1 5X3 0X3 94 3X4 94X3 3X5 0X1 0X1 3X7 0X6 336 11X5
17 E I 17X5 2X7 5X9 0X2 89 3X7 55X8 5X8 40X3 6X8 6X7 0X6 63 48X9
18 L 32 35X4 0X1 5X4 0X1 94 1X8 95X1 1X0 3X3 1X0 4X2 0X1 264 37X2
19 E I 23X3 2X2 5X8 0X2 96 2X9 40X1 5X2 51X3 5X6 9X0 0X7 24 21X3
20 L 32 35X4 0X0 5X3 0X1 93 2X0 84X8 6X5 8X7 6X7 5X5 1X2 286 39X0
21 E I 21X1 2X2 6X0 0X2 97 3X0 85X3 5X0 7X4 4X8 4X0 0X6 313 38X0
22 L 32 35X4 0X1 5X4 0X1 95 2X0 86X2 2X9 11X0 2X7 3X8 0X2 83 18X1
23 E I 21X1 3X1 5X7 0X3 92 5X2 84X2 5X8 5X4 4X1 4X2 1X3 210 49X3
24 L 34 35X4 0X0 5X5 0X1 95 2X3 81X6 4X2 17X3 4X3 5X0 0X6 84 45X4
25 E 9 34X0 0X2 3X2 0X3 55 4X9 36X7 7X6 59X9 8X8 28X2 2X8 185 8X0
26 E 8 33X3 0X4 5X0 0X2 88 3X7 46X8 6X7 36X0 7X6 9X4 1X0 71 21X9
27 L 32 35X4 0X0 5X3 0X1 92 2X2 89X1 4X7 3X4 2X2 3X4 0X5 240 53X0
28 E I 19X3 2X3 5X2 0X3 83 4X4 80X8 5X0 13X7 5X2 5X0 1X0 102 35X1
29 E I 26X2 1X6 5X6 0X2 91 4X6 91X9 2X2 0X7 0X3 2X7 0X1 285 32X0
30 L 33 35X3 0X1 5X5 0X1 97 2X1 89X0 5X7 6X4 5X5 5X8 1X8 232 61X4
a
E: estuarine site; L: littoral site; I: intertidal site.
1104
Marine Pollution Bulletin
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 ind
1
(BI =1) to 0 bits ind
1
(BI =7), with the exception of BI =0 which is associated
with a low value (0.6 bits ind
1
). Biomass diversity has
values of about 1.6 bits g
1
, between BI =1 to 4; then, it
decreases to 0 (BI =7). Both variables are correlated
with BC (p ` 0X001 and p ` 0X05 for numerical and
biomass diversities, respectively), using Spearman rank
correlation.
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 highest
mean redox potential (Fig. 4(a): 360 mV). This param-
eter becomes progressively lower, with BI =7 having a
mean potential which is very reduced (125 mV). Sam-
ples 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 1020% of mud. The or-
ganic matter content has a similar pattern of distribu-
tion 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.
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).
1105
Volume 40/Number 12/December 2000
(6.5 ml l
1
), decreasing to 2.6 ml l
1
at BI =7. The
Spearman rank correlations between these variables and
BC are highly signicant (p ` 0X001).
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 specic
peaks (BI =3, for chromium and nickel; and BI =6, for
lead and copper) and troughs (BI =4 and 5, for cad-
mium, nickel and zinc). Except arsenic and mercury all
the metals are positively correlated with BC (p ` 0X01,
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
signicant correlation is found between BC and PCB
(p ` 0X05, Spearman rank correlation).
Comparing the percentage of samples of each BI that
goes beyond the ER-L (or Eects Range-Low, repre-
senting 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.
1106
Marine Pollution Bulletin
increase progressively in the percentage of samples sur-
passing 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 Ro-
senberg (1978), as stated by Weisberg et al. (1997) in
developing their own index. The paradigm states that
benthic communities respond to improvements in hab-
itat quality in three progressive steps: the abundance
increases; species diversity increases; and dominant
species change from pollution-tolerant to pollution-
sensitive 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 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 reected 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 unpol-
luted samples (BI =0) which correspond to a `normal'
community (sensu Grall and Glemarec, 1997). The di-
versity results do not correspond to those expected from
the aforementioned paradigm, because the richness is
very low. Conversely, samples with BI =1 (also unpol-
luted in the present proposal, corresponding to an
impoverished community) or higher, BI =26 (corre-
sponding to slightly to heavily polluted sites) have
well-dened 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 pol-
lution 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 compari-
son with unpolluted areas. This is because faunal
abundance will increase under slight to moderate pol-
lution, 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 ap-
proach has a high sensitivity at these levels, with well-
dened 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 =57).
Diaz and Rosenberg (1995) have suggested that benthic
infaunal mortality could be initiated when the oxygen
concentration falls below 2 ml l
1
. Ritter and Montagna
(1999) have recently proposed that 3 mg l
1
( =2.14 ml
l
1
) denes the breakpoint between normoxic and hy-
poxic benthic communities. The mean oxygen concen-
tration obtained for BI =7 indicates that life could be
very limited in those sites. However, within BI =6, there
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.
1107
Volume 40/Number 12/December 2000
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 clas-
sied 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 Saiz-Salinas
(1997) and Gonzalez-Oreja and Saiz-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 or-
ganic 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 deposit-
feeders. 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 inverte-
brates modify the grain size of the surcial 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 evo-
lution 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 lo-
cated 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) pro-
vides a classication of the site as `slightly polluted'. In
1995 and 1996, some channelling works were under-
Fig. 8 Evolution of the percentage of ecological groups (IV), 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
Marine Pollution Bulletin
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 eco-
logical 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 pol-
lution, 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 classied as an unpolluted site.
Finally, within the coastal area of Mompas, 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
56 (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 wa-
ters, derived from nearby areas such as Pasajes or
Tximistarri, were diverted to Mompas. The waste in-
cludes contaminants (heavy metals and organic com-
pounds) 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 eco-
logical 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 bot-
tom 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 bio-
logical criteria may complement toxicity and chemical
assessment methods, to serve as independent evaluations
of the ecological quality of marine and estuarine eco-
systems.
Validation of the model developed shows that dier-
ent anthropogenically changes in the environment can
be detected through the use of the BI, including altera-
tions 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 partic-
ular 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 repre-
sentative 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 South-
ampton, UK) and an anonymous referee for kindly advising us on
some details of this paper.
Appendix A
See Table 3.
1109
Volume 40/Number 12/December 2000
T
A
B
L
E
3
L
i
s
t
o
f
s
p
e
c
i
e
s
a
n
d
t
a
x
a
(
i
n
a
l
p
h
a
b
e
t
i
c
a
l
o
r
d
e
r
)
t
h
a
t
h
a
v
e
b
e
e
n
f
o
u
n
d
i
n
a
l
l
t
h
e
s
t
a
t
i
o
n
s
a
l
o
n
g
t
h
e
w
h
o
l
e
s
t
u
d
i
e
d
p
e
r
i
o
d
(
t
h
e
a
s
s
i
g
n
e
d
e
c
o
l
o
g
i
c
a
l
g
r
o
u
p
s
(
s
e
e
t
e
x
t
)
a
r
e
a
l
s
o
s
h
o
w
n
)
.
a
S
p
e
c
i
e
s
G
r
o
u
p
S
p
e
c
i
e
s
G
r
o
u
p
S
p
e
c
i
e
s
G
r
o
u
p
S
p
e
c
i
e
s
G
r
o
u
p
S
p
e
c
i
e
s
G
r
o
u
p
A
b
a
r
e
n
i
c
o
l
a
c
l
a
p
a
r
e
d
i
I
A
n
g
u
l
u
s
t
e
n
u
i
s
I
B
e
l
a
p
o
w
i
s
i
a
n
a
I
C
h
o
n
e
i
n
f
u
n
d
i
b
u
l
i
f
o
r
m
i
s
I
I
D
i
a
s
t
y
l
i
s
r
u
g
o
s
a
I
A
b
a
r
e
n
i
c
o
l
a
s
p
.
I
A
n
o
m
i
a
e
p
h
i
p
p
i
u
m
I
B
e
l
a
s
p
.
I
C
h
o
n
e
s
p
.
I
I
D
i
a
s
t
y
l
i
s
s
p
.
I
A
b
i
s
s
o
n
i
n
o
e
h
i
b
e
r
n
i
c
a
I
I
A
n
o
p
l
o
d
a
c
t
y
l
u
s
p
e
t
i
o
l
a
t
u
s
N
.
A
B
i
t
t
i
u
m
r
e
t
i
c
u
l
a
t
u
m
I
C
h
t
h
a
m
a
l
u
s
s
t
e
l
l
a
t
u
s
I
D
i
a
s
t
y
l
i
s
t
u
m
i
d
a
I
A
b
r
a
a
l
b
a
I
I
I
A
n
o
p
l
o
d
a
c
t
y
l
u
s
p
y
g
m
a
e
u
s
N
.
A
B
o
c
c
a
r
d
i
a
c
h
i
l
e
n
s
i
s
I
C
i
r
c
e
m
i
n
i
m
a
I
D
i
o
d
o
r
a
a
p
e
r
t
u
r
a
I
A
b
r
a
n
i
t
i
d
a
I
I
I
A
n
t
e
n
e
l
l
a
s
p
.
I
B
o
c
c
a
r
d
i
a
p
o
l
y
b
r
a
n
c
h
i
a
I
C
i
r
c
u
l
u
s
s
t
r
i
a
t
u
s
I
D
i
o
g
e
n
e
s
p
u
g
i
l
a
t
o
r
I
I
A
b
r
a
p
r
i
s
m
a
t
i
c
a
I
I
I
A
n
t
h
o
z
o
a
s
p
.
I
B
o
c
c
a
r
d
i
a
s
p
.
I
C
i
r
r
a
t
u
l
u
s
c
h
r
y
s
o
d
e
r
m
a
I
V
D
i
o
p
a
t
r
a
n
e
a
p
o
l
i
t
a
n
a
I
A
b
r
a
s
p
.
I
I
I
A
n
t
h
u
r
a
g
r
a
c
i
l
i
s
I
B
o
d
o
t
r
i
a
a
r
e
n
o
s
a
I
I
C
i
r
r
a
t
u
l
u
s
c
i
r
r
a
t
u
s
I
V
D
i
p
l
o
c
i
r
r
u
s
g
l
a
u
c
u
s
I
A
b
r
a
t
e
n
u
i
s
I
I
I
A
o
n
i
d
e
s
o
x
y
c
e
p
h
a
l
a
I
I
I
B
o
d
o
t
r
i
a
s
c
o
r
p
i
o
i
d
e
s
I
I
C
i
r
r
i
f
o
r
m
i
a
t
e
n
t
a
c
u
l
a
t
a
I
V
D
i
s
p
i
o
u
n
c
i
n
a
t
a
I
I
I
A
c
a
n
t
h
o
c
a
r
d
i
a
a
c
u
l
e
a
t
a
I
A
o
r
a
g
r
a
c
i
l
i
s
I
B
r
a
d
a
v
i
l
l
o
s
a
N
.
A
C
i
r
r
i
p
e
d
o
s
p
.
I
D
i
v
a
r
i
c
e
l
l
a
d
i
v
a
r
i
c
a
t
a
I
A
c
a
n
t
h
o
c
a
r
d
i
a
e
c
h
i
n
a
t
a
I
A
o
r
a
t
y
p
i
c
a
I
B
r
a
n
c
h
i
o
m
m
a
v
e
s
i
c
u
l
o
s
u
m
I
C
l
a
u
s
i
n
e
l
l
a
f
a
s
c
i
a
t
a
I
D
o
n
a
x
t
r
u
n
c
u
l
u
s
I
A
c
a
n
t
h
o
c
a
r
d
i
a
p
a
u
c
i
c
o
s
t
a
t
a
I
A
p
h
e
l
o
c
h
a
t
e
a
m
u
l
t
i
b
r
a
n
c
h
i
i
s
N
.
A
B
r
a
n
c
h
i
o
s
t
o
m
a
l
a
n
c
e
o
l
a
t
a
I
C
l
a
v
i
d
a
e
I
D
o
r
i
s
s
p
.
I
A
c
a
n
t
h
o
c
a
r
d
i
a
s
p
.
I
A
p
h
e
r
u
s
a
c
i
r
r
u
s
I
B
r
a
n
i
a
o
c
u
l
a
t
a
I
I
C
l
y
m
e
n
e
c
f
.
p
r
a
e
t
e
r
m
i
s
a
I
D
o
s
i
n
i
a
e
x
o
l
e
t
a
I
A
c
a
n
t
h
o
c
a
r
d
i
a
t
u
b
e
r
c
u
l
a
t
a
I
A
p
h
e
r
u
s
a
o
v
a
l
i
p
e
s
I
B
r
a
n
i
a
p
u
s
i
l
l
a
I
I
C
l
y
m
e
n
e
l
u
m
b
r
i
c
o
i
d
e
s
I
D
o
s
i
n
i
a
j
u
v
.
i
n
d
e
t
.
I
A
c
a
n
t
h
o
c
h
i
t
o
n
a
c
r
i
t
i
n
u
s
I
A
p
h
o
n
u
p
i
s
g
r
u
b
e
i
I
B
u
g
u
l
a
s
p
.
I
C
l
y
m
e
n
e
m
o
d
e
s
t
a
I
D
o
s
i
n
i
a
l
u
p
i
n
u
s
I
A
c
a
n
t
h
o
c
h
i
t
o
n
a
f
a
s
c
i
c
u
l
a
r
i
s
I
A
p
h
r
o
d
i
t
e
a
c
u
l
e
a
t
a
N
.
A
C
a
l
l
i
a
n
a
s
s
a
s
p
.
I
I
I
C
l
y
m
e
n
e
o
e
r
s
t
e
d
i
i
I
D
o
s
i
n
i
a
s
p
.
I
A
c
h
e
l
i
a
h
i
s
p
i
d
a
I
A
p
i
c
u
l
a
r
i
a
g
u
e
r
i
n
i
I
C
a
l
l
i
a
n
a
s
s
a
s
u
b
t
e
r
r
a
n
e
a
I
I
I
C
l
y
t
i
a
s
p
.
I
D
r
i
l
o
n
e
r
e
i
s

l
u
m
I
I
A
c
h
e
l
i
a
s
i
m
p
l
e
x
I
A
p
i
s
t
o
b
r
a
n
c
h
u
s
t
u
l
l
b
e
r
g
i
I
C
a
l
l
i
a
n
a
s
s
a
t
r
u
n
c
a
t
a
I
I
I
C
n
i
d
a
r
i
a
s
p
.
I
E
b
a
l
i
a
s
p
.
N
.
A
A
c
l
i
s
g
u
l
s
o
n
a
e
N
.
A
A
p
o
n
u
p
h
i
s
b
i
l
i
n
e
a
t
a
I
I
C
a
l
l
i
o
s
t
o
m
a
p
a
p
i
l
l
o
s
u
m
I
C
o
c
h
l
o
d
e
s
m
a
p
r
a
e
t
e
n
u
e
N
.
A
E
b
a
l
i
a
t
u
b
e
r
o
s
a
N
.
A
A
c
r
o
n
i
d
a
b
r
a
c
h
i
a
t
a
I
A
p
o
r
r
h
a
i
s
p
e
s
p
e
l
e
c
a
n
i
I
C
a
l
l
i
o
s
t
o
m
a
z
i
z
y
p
h
i
n
u
m
I
C
o
p
e
p
o
d
a
i
n
d
e
t
.
N
.
A
E
c
h
i
n
o
c
a
r
d
i
u
m
c
o
r
d
a
t
u
m
I
A
c
t
e
o
n
s
p
.
I
A
p
o
r
r
h
a
i
s
s
p
.
I
C
a
l
y
p
t
r
a
e
a
s
i
n
e
n
s
i
s
I
C
o
p
e
p
o
d
o
s
p
.
N
.
A
E
c
h
i
n
o
c
y
a
m
u
s
p
u
s
i
l
l
u
s
I
A
c
t
i
n
i
a
e
q
u
i
n
a
I
A
p
s
e
u
d
e
s
l
a
t
r
e
i
l
l
e
i
I
I
I
C
a
m
p
y
l
a
s
p
i
s
g
l
a
b
r
a
N
.
A
C
o
r
b
u
l
a
g
i
b
b
a
I
I
I
E
c
h
i
n
o
i
d
e
a
s
p
.
I
A
g
l
a
o
p
h
a
m
u
s
r
u
b
e
l
l
a
N
.
A
A
r
c
t
u
r
e
l
l
a
s
p
.
N
.
A
C
a
p
i
t
e
l
l
a
c
a
p
i
t
a
t
a
V
C
o
r
o
p
h
i
u
m
a
c
h
e
r
u
s
i
c
u
m
I
I
I
E
c
h
i
u
r
o
i
d
e
a
s
p
.
I
A
g
l
a
o
p
h
a
m
u
s
s
p
.
N
.
A
A
r
e
n
i
c
o
l
a
m
a
r
i
n
a
N
.
A
C
a
p
i
t
e
l
l
a
s
p
.
V
C
o
r
o
p
h
i
u
m
a
c
u
t
u
m
I
I
I
E
c
h
i
u
r
u
s
e
c
h
i
u
r
u
s
I
A
i
p
t
a
s
i
a
m
u
t
a
b
i
l
i
s
N
.
A
A
r
i
c
i
a
l
a
t
r
e
i
l
l
i
I
C
a
p
i
t
e
l
l
i
d
e
s
g
i
a
r
d
i
V
C
o
r
o
p
h
i
u
m
a
r
e
n
a
r
i
u
m
I
I
I
E
d
w
a
r
d
s
i
a
s
p
.
I
I
A
l
c
y
o
n
a
c
e
a
i
n
d
e
t
N
.
A
A
r
i
c
i
d
e
a
c
a
t
h
e
r
i
n
a
e
I
C
a
p
i
t
o
m
a
s
t
u
s
m
i
n
i
m
u
s
I
V
C
o
r
o
p
h
i
u
m
i
n
s
i
d
i
o
s
u
m
I
I
I
E
h
l
e
r
s
i
a
f
e
r
r
u
g
i
n
a
N
.
A
A
l
k
m
a
r
i
a
r
o
m
i
j
n
i
I
I
I
A
r
i
c
i
d
e
a
c
e
r
r
u
t
i
I
C
a
p
r
e
l
l
a
f
r
e
t
e
n
s
i
s
N
.
A
C
o
r
o
p
h
i
u
m
m
u
l
t
i
s
e
t
o
s
u
m
I
I
I
E
n
s
i
s
s
p
.
I
A
l
p
h
e
u
s
g
l
a
b
e
r
N
.
A
A
r
i
c
i
d
e
a
c
f
.
a
s
s
i
m
i
l
i
s
I
C
a
p
r
e
l
l
a
l
i
n
e
a
r
i
s
N
.
A
C
o
r
o
p
h
i
u
m
s
p
.
I
I
I
E
o
c
u
m
a
d
i
m
o
r
p
h
a
I
I
A
l
v
a
n
i
a
c
r
a
s
s
a
I
A
r
i
c
i
d
e
a
f
r
a
g
i
l
i
s
I
C
a
p
r
e
l
l
a
p
e
n
a
n
t
i
s
N
.
A
C
o
r
o
p
h
i
u
m
v
o
l
u
t
a
t
o
r
I
I
I
E
o
c
u
m
a
d
o
l
l
f
u
s
i
I
I
A
l
v
a
n
i
a
s
e
m
i
s
t
r
i
a
t
a
I
A
r
i
c
i
d
e
a
j
e

r
e
y
s
i
i
I
C
a
r
c
i
n
u
s
m
a
e
n
a
s
I
I
I
C
o
r
y
n
e
p
u
s
i
l
l
a
I
E
p
i
l
e
p
t
o
n
c
l
a
r
k
i
a
e
I
A
l
v
a
n
i
a
s
p
.
I
A
r
i
c
i
d
e
a
m
i
n
u
t
a
I
C
a
r
y
o
p
h
y
l
l
i
a
s
m
i
t
h
i
I
C
o
r
y
s
t
e
s
c
a
s
s
i
v
e
l
a
u
n
u
s
I
E
p
i
t
h
o
n
i
u
m
c
l
a
t
h
r
u
s
I
A
m
a
t
e
a
t
r
i
l
o
b
a
t
a
I
A
r
i
c
i
d
e
a
s
p
.
I
C
a
u
l
l
e
r
i
e
l
l
a
a
l
a
t
a
I
I
I
C
o
s
s
u
r
a
l
o
n
g
o
c
i
r
r
a
t
a
N
.
A
E
p
i
t
o
n
i
u
m
t
u
r
t
o
n
i
I
A
m
a
t
h
i
a
p
r
u
v
o
t
I
A
r
m
a
n
d
i
a
c
i
r
r
o
s
a
I
C
a
u
l
l
e
r
i
e
l
l
a
b
i
o
c
u
l
a
t
a
I
I
I
C
o
s
s
u
r
a
p
y
g
o
d
a
c
t
y
l
a
t
a
N
.
A
E
r
i
c
t
h
o
n
i
u
s
b
r
a
s
i
l
e
n
s
i
s
N
.
A
A
m
p
e
l
i
s
c
a
b
r
e
v
i
c
o
r
n
i
s
I
A
r
m
a
n
d
i
a
s
p
p
I
C
a
u
l
l
e
r
i
e
l
l
a
s
p
.
I
I
I
C
o
s
s
u
r
a
s
p
.
N
.
A
E
t
e
o
n
e
l
o
n
g
a
I
I
A
m
p
e
l
i
s
c
a
c
f
.
s
p
o
o
n
e
r
i
I
A
s
p
i
d
o
s
i
p
h
o
n
m
u
e
l
l
e
r
i
I
C
a
u
l
l
e
r
i
e
l
l
a
z
e
t
l
a
n
d
i
c
a
I
I
I
C
r
a
n
g
o
n
a
l
l
m
a
n
i
I
E
t
e
o
n
e
p
i
c
t
a
I
I
A
m
p
e
l
i
s
c
a
h
e
t
e
r
o
d
a
c
t
y
l
a
I
A
s
t
a
c
i
l
l
a
l
o
n
g
i
c
o
r
n
i
s
I
C
a
v
e
r
n
u
l
a
r
i
a
p
u
s
i
l
l
a
I
C
r
a
n
g
o
n
c
r
a
n
g
o
n
I
E
u
c
l
y
m
e
d
e
p
r
a
e
t
e
r
m
i
s
s
a
I
A
m
p
e
l
i
s
c
a
j
u
v
.
i
n
d
e
t
.
I
A
s
t
a
r
t
e
s
p
.
I
C
e
r
a
d
o
c
u
s
s
e
m
i
s
e
r
r
a
t
u
s
I
C
r
a
s
s
o
s
t
r
e
a
a
n
g
u
l
a
t
a
I
I
I
E
u
c
l
y
m
e
n
e
a

n
i
s
I
A
m
p
e
l
i
s
c
a
s
a
r
s
i
I
A
s
t
a
r
t
e
s
u
l
c
a
t
a
I
C
e
r
a
s
t
o
d
e
r
m
a
e
d
u
l
e
I
I
I
C
r
e
p
i
d
u
l
a
f
o
r
n
i
c
a
t
a
I
I
I
E
u
c
l
y
m
e
n
e
o
e
r
s
t
e
d
i
i
I
A
m
p
e
l
i
s
c
a
s
p
.
I
A
s
t
a
r
t
e
t
r
i
a
n
g
u
l
a
r
i
s
I
C
e
r
a
s
t
o
d
e
r
m
a
l
a
m
a
r
c
k
i
I
I
I
C
u
c
u
m
a
r
i
a
e
l
o
n
g
a
t
a
I
E
u
c
l
y
m
e
n
e
s
p
.
I
A
m
p
e
l
i
s
c
a
s
p
i
n
i
f
e
r
I
A
s
t
e
r
i
n
a
g
i
b
o
s
a
I
C
e
r
a
t
o
s
t
o
m
a
e
r
i
n
a
c
e
u
m
I
C
u
c
u
m
a
r
i
a
s
p
.
I
E
u
c
l
y
m
e
n
i
d
a
e
i
n
d
e
t
.
I
A
m
p
e
l
i
s
c
a
s
p
i
n
i
m
a
n
a
I
A
s
t
r
o
p
e
c
t
e
n
i
r
r
e
g
u
l
a
r
i
s
I
C
e
r
e
b
r
a
t
u
l
u
s
m
a
r
g
i
n
a
t
u
s
I
I
I
C
u
l
t
e
l
l
u
s
p
e
l
l
u
c
i
d
u
s
I
E
u
d
o
r
e
l
l
a
t
r
u
n
c
a
t
u
l
a
N
.
A
A
m
p
e
l
i
s
c
a
t
e
n
u
i
c
o
r
n
i
s
I
A
s
t
r
o
p
e
c
t
e
n
i
r
r
e
g
u
l
a
r
i
s
t
y
p
i
c
u
s
I
C
e
r
e
b
r
a
t
u
l
u
s
s
p
.
I
I
I
C
u
m
o
p
s
i
s
f
a
g
e
i
I
I
E
u
l
a
l
i
a
b
i
l
i
n
e
a
t
a
I
I
A
m
p
e
l
i
s
c
a
t
o
u
l
e
m
o
n
t
i
I
A
t
h
a
n
a
s
n
i
t
e
s
c
e
n
s
I
C
e
r
e
u
s
p
e
d
u
n
c
u
l
a
t
u
s
I
C
u
m
o
p
s
i
s
s
p
.
I
I
E
u
l
a
l
i
a
m
u
s
t
e
l
a
I
I
A
m
p
h
a
r
e
t
e

n
m
a
r
c
h
i
c
a
I
A
t
h
e
c
a
t
a
s
p
.
I
C
e
r
i
a
n
t
a
r
i
o
s
p
.
I
C
y
a
t
h
u
r
a
c
a
r
i
n
a
t
a
I
I
I
E
u
l
a
l
i
a
s
a
n
g
u
i
n
e
a
I
I
A
m
p
h
a
r
e
t
e
g
r
u
b
e
i
I
A
t
y
l
u
s
f
a
l
c
a
t
u
s
I
C
e
r
i
a
n
t
h
u
s
l
l
o
y
d
i
i
I
C
y
c
l
o
p
e
n
e
r
i
t
e
a
I
E
u
l
a
l
i
a
s
p
.
I
I
A
m
p
h
a
r
e
t
e
j
u
v
.
i
n
d
e
t
.
I
A
t
y
l
u
s
g
u
t
t
a
t
u
s
I
C
e
r
i
a
n
t
h
u
s
m
e
m
b
r
a
n
a
c
e
u
s
I
C
y
l
i
c
h
n
a
c
y
l
i
n
d
r
a
c
e
a
I
E
u
l
a
l
i
a
t
r
i
p
u
n
c
t
a
t
a
I
I
A
m
p
h
a
r
e
t
e
l
i
n
d
s
t
r
o
e
m
i
I
A
t
y
l
u
s
s
p
.
I
C
e
r
i
a
n
t
h
u
s
s
p
.
I
C
y
l
i
c
h
n
a
s
p
.
I
E
u
l
a
l
i
a
v
i
r
i
d
i
s
I
I
A
m
p
h
a
r
e
t
e
s
p
.
I
A
t
y
l
u
s
s
w
a
m
m
e
r
d
a
m
i
I
C
e
s
t
o
p
a
g
u
r
u
s
t
i
m
i
d
u
s
I
C
y
l
i
c
h
n
i
n
a
s
u
b
c
y
l
i
n
d
r
i
c
a
I
E
u
l
i
m
e
l
l
a
a
c
i
c
u
t
a
I
A
m
p
h
i
c
t
e
i
s
g
u
n
n
e
r
i
I
I
I
A
t
y
l
u
s
v
e
d
l
o
m
e
n
s
i
s
I
C
h
a
e
t
o
p
t
e
r
u
s
v
a
r
i
o
p
e
d
a
t
u
s
I
C
y
m
o
d
o
c
e
t
r
u
n
c
a
t
a
I
E
u
l
i
m
e
l
l
a
s
p
.
I
A
m
p
h
i
p
h
o
l
i
s
s
q
u
a
m
a
t
a
I
A
u
d
o
u
i
n
i
a
t
e
n
t
a
c
u
l
a
t
a
I
V
C
h
a
e
t
o
z
o
n
e
B
s
p
p
I
V
C
y
t
h
a
r
a
a
t
t
e
n
u
a
t
a
I
E
u
m
i
d
a
b
a
h
u
s
i
e
n
s
i
s
I
I
A
m
p
h
i
t
r
i
t
e
j
o
h
n
s
t
o
n
i
I
A
u
t
o
l
y
t
u
s
l
o
n
g
e
f
e
r
i
e
n
s
N
.
A
C
h
a
e
t
o
z
o
n
e
c
f
.
g
i
b
b
e
r
I
V
C
y
t
h
a
r
a
c
o
s
t
a
t
a
I
E
u
m
i
d
a
s
a
n
g
u
i
n
e
a
I
I
A
m
p
h
i
u
r
a
b
r
a
c
h
i
a
t
a
I
A
u
t
o
l
y
t
u
s
s
p
.
N
.
A
C
h
a
e
t
o
z
o
n
e
g
i
b
b
e
r
I
V
D
a
r
d
a
n
u
s
a
r
r
o
s
o
r
N
.
A
E
u
m
i
d
a
s
p
.
I
I
1110
Marine Pollution Bulletin
A
m
p
h
i
u
r
a
c
h
i
a
j
e
i
I
A
x
i
o
n
i
c
e
m
a
c
u
l
a
t
a
N
.
A
C
h
a
e
t
o
z
o
n
e
s
e
t
o
s
a
I
V
D
e
m
o
n
a
x
s
p
.
N
.
A
E
u
n
i
c
e
h
a
r
a
s
s
i
i
I
I
A
m
p
h
i
u
r
a

l
i
f
o
r
m
i
s
I
B
a
c
h
y
c
u
m
a
b
r
e
v
i
c
o
r
n
i
s
N
.
A
C
h
a
e
t
o
z
o
n
e
s
p
.
I
V
D
e
m
o
s
p
o
n
g
i
a
s
p
.
I
E
u
n
i
c
e
s
p
.
I
I
A
m
p
h
i
u
r
a
j
u
v
.
i
n
d
e
t
.
I
B
a
l
c
i
s
a
l
b
a
I
C
h
a
m
e
l
e
a
g
a
l
l
i
n
a
I
D
e
n
t
a
l
i
u
m
n
o
v
e
m
c
o
s
t
a
t
u
m
I
E
u
n
i
c
e
v
i
t
t
a
t
a
I
I
A
m
p
h
i
u
r
a
s
p
.
I
B
a
r
l
e
e
i
a
r
u
b
r
a
I
I
C
h
a
m
e
l
e
a
g
a
l
l
i
n
a
s
t
r
i
a
t
u
l
a
I
D
e
n
t
a
l
i
u
m
s
p
.
I
E
u
p
h
r
o
s
y
n
e
f
o
l
i
o
s
a
I
A
n
a
i
t
i
d
e
s
l
i
n
e
a
t
a
I
I
B
a
t
h
y
p
o
r
e
i
a
e
l
e
g
a
n
s
I
C
h
a
m
e
l
e
a
s
t
r
i
a
t
u
l
a
I
D
e
s
d
e
m
o
n
a
c
f
.
o
r
n
a
t
a
I
I
E
u
r
y
d
i
c
e
a

n
i
s
I
A
n
a
i
t
i
d
e
s
m
a
c
u
l
a
t
a
I
I
B
a
t
h
y
p
o
r
e
i
a
n
a
n
a
I
C
h
a
u
v
e
t
i
a
b
r
u
n
n
e
a
I
D
e
s
d
e
m
o
n
a
o
r
n
a
t
a
I
I
E
u
r
y
d
i
c
e
p
u
l
c
h
r
a
I
A
n
a
i
t
i
d
e
s
m
u
c
o
s
a
I
I
B
a
t
h
y
p
o
r
e
i
a
p
e
l
a
g
i
c
a
I
C
h
e
i
r
o
c
r
a
t
u
s
s
u
n
d
e
v
a
l
l
i
i
I
D
e
v
o
n
i
a
p
e
r
r
i
e
r
i
I
E
u
r
y
d
i
c
e
s
p
.
I
A
n
a
i
t
i
d
e
s
s
p
.
I
I
B
a
t
h
y
p
o
r
e
i
a
p
i
l
o
s
a
I
C
h
e
r
i
o
c
r
a
t
u
s
s
p
.
I
D
i
a
s
t
y
l
i
s
b
r
a
d
y
i
I
E
u
r
y
d
i
c
e
s
p
i
n
i
g
e
r
a
I
A
n
a
p
a
g
u
r
u
s
h
y
n
d
m
a
n
i
I
B
a
t
h
y
p
o
r
e
i
a
s
a
r
s
i
I
C
h
i
r
o
n
o
m
i
d
a
I
V
D
i
a
s
t
y
l
i
s
c
f
.
t
u
m
i
d
a
I
E
u
r
y
n
o
m
e
a
s
p
e
r
a
I
A
n
a
p
a
g
u
r
u
s
l
a
e
v
i
s
I
B
a
t
h
y
p
o
r
e
i
a
s
p
.
I
C
h
l
a
m
y
s
v
a
r
i
a
I
D
i
a
s
t
y
l
i
s
c
o
r
n
u
t
a
I
E
u
r
y
n
o
m
e
s
p
i
n
o
s
a
I
A
n
a
p
a
g
u
r
u
s
s
p
.
I
B
a
t
h
y
p
o
r
e
i
a
t
e
n
u
i
p
e
s
I
C
h
o
n
e
c
o
l
l
a
r
i
s
I
I
D
i
a
s
t
y
l
i
s
l
a
e
v
i
s
I
E
u
r
y
s
y
l
l
i
s
t
u
b
e
r
c
u
l
a
t
a
I
I
A
n
g
u
i
l
l
a
a
n
g
u
i
l
l
a
I
I
B
e
l
a
n
e
b
u
l
a
I
C
h
o
n
e

l
i
c
a
u
d
a
t
a
I
I
D
i
a
s
t
y
l
i
s
l
u
c
i
f
e
r
a
I
E
x
o
g
o
n
e
n
a
i
d
i
n
a
I
I
E
x
o
g
o
n
e
s
p
.
I
I
H
e
s
i
o
n
u
r
a
e
l
o
n
g
a
t
a
I
I
L
e
u
c
o
t
h
o
e
s
p
i
n
i
c
a
r
p
a
I
M
a
r
p
h
y
s
a
f
a
l
l
a
x
I
I
N
e
p
h
t
y
s
c
i
r
r
o
s
a
I
I
F
a
b
r
i
c
i
a
s
a
b
e
l
l
a
N
.
A
H
e
t
e
r
o
c
i
r
r
u
s
b
i
o
c
u
l
a
t
u
s
I
V
L
e
v
i
n
s
e
n
i
a
g
r
a
c
i
l
i
s
N
.
A
M
a
r
p
h
y
s
a
s
a
n
g
i
n
e
a
I
I
N
e
p
h
t
y
s
h
o
m
b
e
r
g
i
I
I
F
a
b
u
l
i
n
a
f
a
b
u
l
a
I
H
e
t
e
r
o
c
i
r
r
u
s
s
p
p
I
V
L
i
l
l
e
b
o
r
j
i
a
p
a
l
l
i
d
a
I
M
a
r
p
h
y
s
a
s
p
.
I
I
N
e
p
h
t
y
s
h
y
s
t
r
i
c
i
s
I
I
F
i
l
o
g
r
a
n
a
i
m
p
l
e
x
a
N
.
A
H
e
t
e
r
o
m
a
s
t
u
s

l
i
f
o
r
m
i
s
I
I
I
L
i
o
c
a
r
c
i
n
u
s
a
r
c
u
a
t
u
s
I
M
a
r
p
h
y
s
a
s
p
.
(
b
e
l
l
i
?
)
I
I
N
e
p
h
t
y
s
i
n
c
i
s
a
I
I
G
a
l
a
t
h
e
a
i
n
t
e
r
m
e
d
i
a
I
H
e
x
a
c
o
r
a
l
l
i
a
s
p
.
I
L
i
o
c
a
r
c
i
n
u
s
a
r
c
u
a
t
u
s
I
M
a
r
t
a
s
t
h
e
r
i
a
s
g
l
a
c
i
a
l
i
s
I
N
e
p
h
t
y
s
j
u
v
.
s
p
p
I
I
G
a
l
a
t
h
e
a
s
p
.
I
H
i
a
t
e
l
l
a
a
r
t
i
c
a
I
L
i
o
c
a
r
c
i
n
u
s
d
e
p
u
r
a
t
o
r
I
M
e
d
i
o
m
a
s
t
u
s
f
r
a
g
i
l
i
s
I
I
I
N
e
p
h
t
y
s
k
e
r
s
i
v
a
l
e
n
s
i
s
I
I
G
a
l
a
t
h
e
a
s
q
u
a
m
i
f
e
r
a
I
H
i
n
i
a
i
n
c
r
a
s
s
a
t
a
I
I
L
i
o
c
a
r
c
i
n
u
s
h
o
l
s
a
t
u
s
I
M
e
g
a
l
u
r
o
p
u
s
a
g
i
l
i
s
I
N
e
p
h
t
y
s
p
a
r
a
d
o
x
a
I
I
G
a
l
a
t
h
o
w
e
n
i
a
o
c
u
l
a
t
a
I
H
i
n
i
a
j
u
v
.
i
n
d
e
t
.
I
I
L
i
o
c
a
r
c
i
n
u
s
m
a
r
m
o
r
e
u
s
I
M
e
g
a
m
p
h
o
p
u
s
c
o
r
n
u
t
u
s
I
N
e
p
h
t
y
s
s
p
.
I
I
G
a
l
e
o
m
n
a
t
u
r
t
o
n
i
I
H
i
n
i
a
p
y
g
m
a
e
a
I
I
L
i
o
c
a
r
c
i
n
u
s
p
u
s
i
l
l
u
s
I
M
e
l
i
n
n
a
c
r
i
s
t
a
t
a
I
I
I
N
e
p
h
t
y
s
s
p
.
j
u
v
.
I
I
G
a
m
m
a
r
e
l
l
a
f
u
c
i
c
o
l
a
I
I
I
H
i
n
i
a
r
e
t
i
c
u
l
a
t
a
I
I
L
i
o
c
a
r
c
i
n
u
s
s
p
.
I
M
e
l
i
n
n
a
p
a
l
m
a
t
a
I
I
I
N
e
p
h
t
y
s
s
p
p
I
I
G
a
m
m
a
r
i
d
e
a
I
H
i
p
p
o
l
y
t
e
v
a
r
i
a
n
s
I
L
i
o
c
a
r
c
i
n
u
s
v
e
r
n
a
l
i
s
I
M
e
l
i
n
n
a
s
p
.
I
I
I
N
e
r
e
i
m
y
r
a
p
u
n
c
t
a
t
a
I
I
I
G
a
m
m
a
r
o
p
s
i
s
p
a
l
m
a
t
a
I
H
i
p
p
o
m
e
d
o
n
d
e
n
t
i
c
u
l
a
t
u
s
I
L
i
o
c
a
r
c
i
n
u
s
z
a
r
i
q
u
i
e
y
i
I
M
e
l
i
t
a
g
l
a
d
i
o
s
a
I
N
e
r
e
i
p
h
y
l
l
a
r
u
b
i
g
i
n
o
s
a
N
.
A
G
a
m
m
a
r
o
p
s
i
s
s
h
o
p
h
i
a
e
I
H
y
a
l
a
v
i
t
r
e
a
I
L
i
s
t
r
i
e
l
l
a
p
i
c
t
a
I
M
e
l
i
t
a
p
a
l
m
a
t
a
I
I
I
N
e
r
e
i
s
c
a
u
d
a
t
a
I
V
G
a
m
m
a
r
o
p
s
i
s
s
p
.
I
H
y
a
l
e
n
i
l
s
s
o
n
i
I
L
o
r
i
p
e
s
l
u
c
i
n
a
l
i
s
I
M
e
r
c
e
r
i
e
l
l
a
e
n
i
g
m
a
t
i
c
a
I
I
N
e
r
e
i
s
c
f
.
l
a
m
e
l
l
o
s
a
I
I
I
G
a
m
m
a
r
u
s
i
n
s
e
n
s
i
b
i
l
i
s
I
H
y
a
l
i
n
o
e
c
i
a
b
i
l
i
n
e
a
t
a
N
.
A
L
u
c
i
n
o
m
a
b
o
r
e
a
l
i
s
I
M
e
t
a
p
h
o
x
u
s
f
u
l
t
o
n
i
I
N
e
r
e
i
s
d
i
v
e
r
s
i
c
o
l
o
r
I
I
I
G
a
m
m
a
r
u
s
s
p
.
I
H
y
a
l
i
n
o
e
c
i
a
f
a
u
v
e
l
i
N
.
A
L
u
c
i
n
o
m
a
b
o
r
e
a
l
i
s
I
M
e
t
a
p
h
o
x
u
s
p
e
c
t
i
n
a
t
u
s
I
N
e
r
e
i
s
l
o
n
g
i
s
s
i
m
a
I
I
I
G
a
r
i
c
o
s
t
u
l
a
t
a
I
H
y
a
l
i
n
o
e
c
i
a
s
p
.
N
.
A
L
u
m
b
r
i
n
e
r
i
d
e
s
s
p
.
I
I
M
e
t
a
z
o
e
a
d
e
p
o
r
c
e
l
l
a
n
i
d
a
e
N
.
A
N
e
r
e
i
s
s
p
.
I
I
I
G
a
r
i
d
e
p
r
e
s
s
a
I
H
y
d
r
o
b
i
a
u
l
v
a
e
I
I
I
L
u
m
b
r
i
n
e
r
i
o
p
s
i
s
p
a
r
a
d
o
x
a
I
I
M
i
c
r
o
d
e
u
t
o
p
u
s
a
n
o
m
a
l
u
s
I
N
o
t
h
r
i
a
g
e
o

l
i
f
o
r
m
i
s
I
I
G
a
r
i
f
e
r
v
e
n
s
i
s
I
H
y
d
r
o
i
d
e
s
n
o
r
v
e
g
i
c
a
N
.
A
L
u
m
b
r
i
n
e
r
i
s
c
f
.
g
r
a
c
i
l
i
s
I
I
M
i
c
r
o
d
e
u
t
o
p
u
s
d
a
m
n
o
n
i
e
n
s
i
s
I
N
o
t
h
r
i
a
l
e
p
t
a
I
I
G
a
r
i
t
e
l
l
i
n
e
l
l
a
I
I
d
o
t
e
a
l
i
n
e
a
r
i
s
N
.
A
L
u
m
b
r
i
n
e
r
i
s
e
m
a
n
d
i
b
u
l
a
t
a
I
I
M
i
c
r
o
d
e
u
t
o
p
u
s
s
p
.
I
N
o
t
h
r
i
a
s
p
.
I
I
G
a
r
i
i
d
a
e
i
n
d
e
t
.
I
I
d
u
n
e
l
l
a
p
i
c
t
a
N
.
A
L
u
m
b
r
i
n
e
r
i
s
e
m
a
n
d
i
b
u
l
a
t
a
m
a
b
i
t
i
I
I
M
i
c
r
o
d
e
u
t
o
p
u
s
s
t
a
t
i
o
n
i
s
I
N
o
t
i
r
u
s
i
r
u
s
I
G
a
t
t
y
a
n
a
c
i
r
r
o
s
a
N
.
A
I
n
a
c
h
u
s
d
o
r
s
e
t
t
e
n
s
i
s
I
L
u
m
b
r
i
n
e
r
i
s
g
r
a
c
i
l
i
s
I
I
M
i
c
r
o
d
e
u
t
o
p
u
s
v
e
r
s
i
c
u
l
a
t
u
s
I
N
o
t
o
c
i
r
r
u
s
s
p
.
N
.
A
G
i
b
b
u
l
a
m
a
g
u
s
I
I
n
a
c
h
u
s
s
p
.
l
a
r
v
a
I
L
u
m
b
r
i
n
e
r
i
s
i
m
p
a
t
i
e
n
s
I
I
M
i
c
r
o
p
h
t
h
a
l
m
u
s
s
c
z
e
l
k
o
w
i
i
N
.
A
N
o
t
o
m
a
s
t
u
s
l
a
t
e
r
i
c
e
u
s
I
I
I
G
l
y
c
e
r
a
a
l
b
a
I
I
I
p
h
i
m
e
d
i
a
o
b
e
s
a
I
L
u
m
b
r
i
n
e
r
i
s
l
a
t
r
e
i
l
l
i
I
I
M
i
c
r
o
s
p
i
o
s
p
.
N
.
A
N
o
t
o
m
a
s
t
u
s
l
i
n
e
a
t
u
s
I
I
I
G
l
y
c
e
r
a
c
a
p
i
t
a
t
a
I
I
I
p
h
i
n
o
 e
s
e
r
r
a
t
a
I
L
u
m
b
r
i
n
e
r
i
s
l
a
t
r
e
i
l
l
i
I
I
M
i
c
r
u
r
a
s
p
.
N
.
A
N
o
t
o
m
a
s
t
u
s
s
p
.
I
I
I
G
l
y
c
e
r
a
c
o
n
v
o
l
u
t
a
I
I
I
p
h
i
n
o
e
s
p
.
I
L
u
m
b
r
i
n
e
r
i
s
s
p
.
I
I
M
o
d
i
o
l
u
l
a
p
h
a
s
e
o
l
i
n
a
I
N
u
c
u
l
a
n
i
t
i
d
a
I
G
l
y
c
e
r
a
l
a
p
i
d
u
m
I
I
J
a
e
r
a
a
l
b
i
f
r
o
n
s
I
L
u
n
a
t
i
a
a
l
d
e
r
i
I
I
M
o
d
i
o
l
u
s
b
a
r
b
a
t
u
s
I
N
u
c
u
l
a
n
i
t
i
d
o
s
a
I
G
l
y
c
e
r
a
r
o
u
x
i
i
I
I
J
a
e
r
a
s
p
.
I
L
u
t
r
a
r
i
a
a
n
g
u
s
t
i
o
r
I
M
o
d
i
o
l
u
s
g
a
l
l
i
c
u
s
I
N
u
c
u
l
a
n
u
c
l
e
u
s
I
G
l
y
c
e
r
a
s
p
.
I
I
J
a
n
i
r
a
m
a
c
u
l
o
s
a
N
.
A
L
u
t
r
a
r
i
a
l
u
t
r
a
r
i
a
I
M
o
d
i
o
l
u
s
m
o
d
i
o
l
u
s
I
N
u
c
u
l
a
s
p
.
I
G
l
y
c
e
r
a
t
e
s
s
e
l
a
t
a
I
I
J
a
s
m
i
n
e
i
r
a
e
l
e
g
a
n
s
N
.
A
L
u
t
r
a
r
i
a
l
u
t
r
a
r
i
a
I
M
o
n
o
c
u
l
o
d
e
s
c
a
r
i
n
a
t
u
s
I
N
u
c
u
l
a
s
u
l
c
a
t
a
I
G
l
y
c
e
r
a
t
r
i
d
a
c
t
y
l
a
I
I
J
u
p
i
t
e
r
i
a
m
i
n
u
t
a
N
.
A
L
u
t
r
a
r
i
a
s
p
.
I
M
o
n
o
p
y
l
e
p
h
o
r
u
s
i
r
r
o
r
a
t
u
s
V
N
u
c
u
l
a
t
u
r
g
i
d
a
I
G
l
y
c
e
r
a
u
n
i
c
o
r
n
i
s
I
I
K
e
f
e
r
s
t
e
i
n
i
a
c
i
r
r
a
t
a
N
.
A
L
y
o
n
s
i
a
n
o
r
v
e
g
i
c
u
m
I
M
o
n
t
a
c
u
t
a
f
e
r
r
u
g
i
n
o
s
a
I
I
O
c
e
n
e
b
r
a
e
r
i
n
a
c
e
a
I
I
G
l
y
c
i
n
d
e
n
o
r
d
m
a
n
i
I
I
K
e
l
l
i
a
s
u
b
o
r
b
i
c
u
l
a
r
i
s
I
L
y
s
i
a
n
a
s
s
a
c
e
r
a
t
i
n
a
I
M
u
s
c
u
l
u
s
d
i
s
c
o
r
s
I
O
d
o
s
t
o
m
i
a
s
p
.
I
I
G
l
y
c
i
n
d
e
n
o
r
d
m
a
n
n
i
I
I
L
a
b
i
d
o
p
l
a
x
c
f
.
t
h
o
m
s
o
n
i
I
L
y
s
i
a
n
a
s
s
a
i
n
s
p
e
r
a
t
a
I
M
y
a
a
r
e
n
a
r
i
a
I
I
O
l
i
g
o
c
h
a
e
t
a
V
G
n
a
t
h
i
a
o
x
y
u
r
e
a
I
L
a
b
i
d
o
p
l
a
x
d
i
g
i
t
a
t
a
I
L
y
s
i
d
i
c
e
n
i
n
e
t
t
a
I
I
M
y
r
t
e
a
s
p
i
n
i
f
e
r
a
I
O
n
u
p
h
i
d
a
e
j
u
v
e
n
i
l
I
I
G
o
b
i
u
s
n
i
g
e
r
I
I
I
L
a
b
i
d
o
p
l
a
x
s
p
p
I
L
y
s
i
p
p
e
l
a
b
i
a
t
a
N
.
A
M
y
s
e
l
l
a
b
i
d
e
n
t
a
t
a
I
O
n
u
p
h
i
s
c
f
.
g
e
o
p
h
i
l
i
f
o
r
m
i
s
I
I
G
o
n
i
a
d
a
m
a
c
u
l
a
t
a
I
I
L
a
c
y
d
o
n
i
a
m
i
r
a
n
d
a
N
.
A
M
a
c
o
m
a
b
a
l
t
i
c
a
I
M
y
s
i
a
u
n
d
a
t
a
I
O
n
u
p
h
i
s
c
o
n
c
h
y
l
e
g
a
I
I
G
o
n
i
a
d
a
s
p
.
I
I
L
a
g
i
s
c
a
e
x
t
e
n
u
a
t
a
I
I
M
a
c
r
o
p
o
d
i
a
r
o
s
t
r
a
t
a
I
M
y
s
i
d
a
c
e
a
I
I
O
n
u
p
h
i
s
e
r
e
m
i
t
a
I
I
G
o
o
d
a
l
l
i
a
t
r
i
a
n
g
u
l
a
r
i
s
I
L
a
n
i
c
e
c
i
r
r
a
t
a
I
I
I
M
a
c
t
r
a
c
o
r
a
l
l
i
n
a
I
M
y
s
t
i
d
e
s
e
l
o
n
g
a
t
a
I
I
O
p
h
e
l
i
a
b
i
c
o
r
n
i
s
I
G
o
u
l
d
i
a
m
i
n
i
m
a
I
L
a
n
i
c
e
c
i
r
r
a
t
a
I
I
I
M
a
c
t
r
a
s
t
u
l
t
o
r
u
m
I
M
y
s
t
i
d
e
s
l
i
m
b
a
t
a
I
I
O
p
h
e
l
i
n
a
a
c
u
m
i
n
a
t
a
N
.
A
G
r
e
g
a
r
i
e
l
l
a
b
a
r
b
a
t
e
l
l
a
I
L
a
n
i
c
e
c
o
n
c
h
i
l
e
g
a
I
I
M
a
c
t
r
a
c
e
a
i
n
d
e
t
.
I
M
y
t
i
l
a
s
t
e
r
m
i
n
i
m
u
n
I
O
p
h
i
o
c
e
n
t
r
u
s
b
r
a
c
h
i
a
t
u
s
I
G
u
e
r
n
e
a
c
o
a
l
i
t
a
N
.
A
L
a
n
i
c
e
c
o
n
c
h
i
l
e
g
a
I
I
M
a
e
r
a
g
r
o
s
s
i
m
a
n
a
I
M
y
t
i
l
u
s
e
d
u
l
i
s
I
I
I
O
p
h
i
o
c
o
m
i
n
a
n
i
g
r
a
I
G
y
m
n
a
m
m
o
d
y
t
e
s
s
e
m
i
s
q
u
a
m
a
t
u
s
N
.
A
L
a
n
i
c
e
s
p
p
I
I
M
a
e
r
a
o
t
h
o
n
i
s
I
N
a
s
s
a
r
i
u
s
i
n
c
r
a
s
s
a
t
u
s
I
I
O
p
h
i
o
d
r
o
m
u
s

e
x
u
o
s
u
s
I
I
G
y
p
t
i
s
c
a
p
e
n
s
i
s
I
I
L
a
o
n
i
c
e
s
p
.
N
.
A
M
a
e
r
a
s
p
.
I
N
a
s
s
a
r
i
u
s
r
e
t
i
c
u
l
a
t
u
s
I
I
O
p
h
i
o
p
s
i
l
a
a
r
a
n
e
a
I
1111
Volume 40/Number 12/December 2000
T
A
B
L
E
3
(
C
O
N
T
I
N
U
E
D
)
S
p
e
c
i
e
s
G
r
o
u
p
S
p
e
c
i
e
s
G
r
o
u
p
S
p
e
c
i
e
s
G
r
o
u
p
S
p
e
c
i
e
s
G
r
o
u
p
S
p
e
c
i
e
s
G
r
o
u
p
G
y
p
t
i
s
r
o
s
e
a
I
I
L
e
a
n
i
r
a
y
h
l
e
n
i
N
.
A
M
a
g
e
l
o
n
a
a
l
l
e
n
i
I
N
a
t
a
n
t
i
a
s
p
.
N
.
A
O
p
h
i
o
t
r
i
x
f
r
a
g
i
l
i
s
I
H
a
l
c
a
m
p
a
s
p
.
I
L
e
m
b
o
s
s
p
.
N
.
A
M
a
g
e
l
o
n
a

l
i
f
o
r
m
i
s
I
N
a
t
i
c
a
a
l
d
e
r
i
I
I
O
p
h
i
u
r
a
a
l
b
i
d
a
I
I
H
a
m
i
n
o
e
a
n
a
v
i
c
u
l
a
I
I
L
e
p
i
d
o
n
o
t
u
s
c
l
a
v
a
I
I
M
a
g
e
l
o
n
a
m
i
n
u
t
a
I
N
a
t
i
c
a
c
a
t
e
n
a
I
I
O
p
h
i
u
r
a
o
p
h
i
u
r
a
I
I
H
a
r
m
o
t
h
o
e
a
n
t
i
l
o
p
e
s
I
I
L
e
p
i
d
o
n
o
t
u
s
s
q
u
a
m
a
t
u
s
I
I
M
a
g
e
l
o
n
a
m
i
r
a
b
i
l
i
s
I
N
e
a
n
t
h
e
s
c
a
u
d
a
t
a
I
I
I
O
p
h
i
u
r
a
s
p
.
I
I
H
a
r
m
o
t
h
o
e
c
f
.
l
u
n
u
l
a
t
a
I
I
L
e
p
t
o
c
h
e
i
r
u
s
p
e
c
t
i
n
a
t
u
s
I
I
I
M
a
g
e
l
o
n
a
p
a
p
i
l
l
i
c
o
r
n
i
s
I
N
e
a
n
t
h
e
s
i
r
r
o
r
a
t
a
I
I
I
O
p
h
i
u
r
a
t
e
x
t
u
r
a
t
a
I
I
H
a
r
m
o
t
h
o
e
g
l
a
b
r
a
I
I
L
e
p
t
o
c
h
e
i
r
u
s
p
i
l
o
s
u
s
I
I
I
M
a
g
e
l
o
n
a
s
p
.
I
N
e
a
n
t
h
e
s
j
u
v
.
i
n
d
e
t
.
I
I
I
O
p
h
i
u
r
a
t
e
x
t
u
r
a
t
a
(
j
u
v
.
)
I
I
H
a
r
m
o
t
h
o
e
i
m
b
r
i
c
a
t
a
I
I
L
e
p
t
o
c
h
e
l
i
a
s
a
v
i
g
n
y
i
N
.
A
M
a
g
e
l
o
n
a
w
i
l
s
o
n
i
I
N
e
a
n
t
h
e
s
s
p
.
I
I
I
O
p
h
r
y
o
t
r
o
c
h
a
l
a
b
r
o
n
i
c
a
I
I
H
a
r
m
o
t
h
o
e
i
m
p
a
r
I
I
L
e
p
t
o
c
h
i
t
o
n
a
s
e
l
l
u
s
I
M
a
l
a
c
o
c
e
r
o
s
c
i
l
i
a
t
a
I
I
I
N
e
b
a
l
i
a
b
i
p
e
s
V
O
p
h
r
y
o
t
r
o
c
h
a
p
u
e
r
i
l
i
s
I
I
H
a
r
m
o
t
h
o
e
l
u
n
u
l
a
t
a
I
I
L
e
p
t
o
c
h
i
t
o
n
c
a
n
c
e
l
l
a
t
u
s
I
M
a
l
a
c
o
c
e
r
o
s
f
u
l
i
g
i
n
o
s
u
s
V
N
e
b
a
l
i
a
s
p
.
i
n
d
e
t
.
V
O
p
h
r
y
o
t
r
o
c
h
a
s
p
.
I
I
H
a
r
m
o
t
h
o
e
s
p
.
I
I
L
e
p
t
o
c
h
i
t
o
n
i
n
h
a
e
r
e
n
s
I
M
a
l
a
c
o
c
e
r
o
s
g
i
r
a
r
d
i
I
I
I
N
e
b
a
l
i
a
t
h
y
p
h
l
o
p
s
I
I
O
p
i
s
t
o
d
o
n
t
a
p
t
e
r
o
c
h
a
e
t
a
N
.
A
H
a
r
m
o
t
h
o
e
s
p
.
(
a
n
t
i
l
o
p
e
s
?
)
I
I
L
e
p
t
o
n
e
r
i
s
g
l
a
u
c
a
I
I
I
M
a
l
a
c
o
c
e
r
o
s
s
p
.
I
I
I
N
e
m
a
t
o
d
a
I
I
I
O
r
b
i
n
i
a
c
u
v
i
e
r
i
N
.
A
H
a
r
m
o
t
h
o
e
s
p
i
n
i
f
e
r
a
I
I
L
e
p
t
o
s
y
n
a
p
t
a
c
f
.
g
a
l
l
i
e
n
e
i
I
M
a
l
a
c
o
c
e
r
o
s
v
u
l
g
a
r
i
s
I
I
I
N
e
m
a
t
o
n
e
r
e
i
s
u
n
i
c
o
r
n
i
s
I
I
O
r
c
h
o
m
e
n
e
n
a
n
a
N
.
A
H
a
r
p
i
n
i
a
a
n
t
e
n
n
a
r
i
a
I
L
e
p
t
o
s
y
n
a
p
t
a
g
a
l
l
i
e
n
e
i
I
M
a
l
d
a
n
e
g
l
e
b
i
f
e
x
I
N
e
m
e
r
t
e
a
I
I
I
O
r
c
h
o
m
e
n
e
s
i
m
i
l
i
s
N
.
A
H
a
r
p
i
n
i
a
p
e
c
t
i
n
a
t
a
I
L
e
p
t
o
s
y
n
a
p
t
a
i
n
h
a
e
r
e
n
s
I
M
a
n
a
y
u
n
k
i
a
a
e
s
t
u
a
r
i
n
a
I
I
N
e
o
a
m
p
h
i
t
r
i
t
e
a

n
i
s
N
.
A
O
r
i
o
p
s
i
s
a
r
m
a
n
d
i
N
.
A
H
a
r
p
i
n
i
a
s
p
.
I
L
e
u
c
o
t
h
o
e
i
n
c
i
s
a
I
M
a
n
g
e
l
i
a
a
t
t
e
n
u
a
t
a
I
N
e
o
a
m
p
h
i
t
r
i
t
e
c
f
.
a

n
i
s
N
.
A
O
r
i
o
p
s
i
s
s
p
.
N
.
A
H
a
u
s
t
o
r
i
u
s
a
r
e
n
a
r
i
u
s
I
L
e
u
c
o
t
h
o
e
i
n
c
i
s
a
I
M
a
n
g
e
l
i
a
n
e
b
u
l
a
I
N
e
o
a
m
p
h
i
t
r
i
t
e
s
p
.
N
.
A
O
s
t
r
e
a
e
d
u
l
i
s
I
H
e
d
i
s
t
e
d
i
v
e
r
s
i
c
o
l
o
r
I
I
I
L
e
u
c
o
t
h
o
e
l
i
l
l
j
e
b
o
r
g
i
I
M
a
n
g
e
l
i
a
s
m
i
t
h
i
I
N
e
p
h
t
y
s
a
s
s
i
m
i
l
i
s
I
I
O
v
a
t
e
l
l
a
m
y
o
s
o
t
i
s
N
.
A
H
e
r
m
i
o
n
e
h
y
s
t
r
i
x
I
I
L
e
u
c
o
t
h
o
e
r
i
c
h
i
a
r
d
i
i
I
M
a
n
g
e
l
i
a
s
p
.
I
N
e
p
h
t
y
s
c
a
e
c
a
I
I
O
w
e
n
i
a

l
i
f
o
r
m
i
s
I
H
e
s
i
o
n
e
p
a
n
t
h
e
r
i
n
a
I
I
L
e
u
c
o
t
h
o
e
s
p
.
I
M
a
r
p
h
y
s
a
b
e
l
l
i
i
I
I
N
e
p
h
t
y
s
c
f
.
p
a
r
a
d
o
x
a
I
I
O
w
e
n
i
a
f
u
s
i
f
o
r
m
i
s
I
P
a
c
h
y
g
r
a
p
s
u
s
m
a
r
m
o
r
a
t
u
s
I
I
P
h
y
l
l
o
d
o
c
e
r
o
s
e
a
I
I
P
r
o
t
o
d
r
i
l
u
s
s
p
.
N
.
A
S
p
h
a
e
r
o
s
y
l
l
i
s
h
y
s
t
r
i
x
I
I
T
h
o
l
a
r
u
s
c
r
a
n
c
h
i
i
I
P
a
g
u
r
o
i
d
e
a
i
n
d
e
t
.
I
P
h
y
l
l
o
d
o
c
e
s
p
.
I
I
P
s
a
m
e
c
h
i
n
u
s
m
i
l
i
a
r
i
s
I
S
p
h
a
e
r
o
s
y
l
l
i
s
p
y
r
i
f
e
r
a
I
I
T
h
r
a
c
i
a
p
h
a
s
e
o
l
i
n
a
I
P
a
g
u
r
u
s
b
e
r
n
h
a
r
d
u
s
I
P
h
y
l
o
c
h
e
r
a
s
b
i
s
p
i
n
o
s
u
s
I
P
s
a
m
m
o
b
i
a
c
o
s
t
u
l
a
t
a
I
S
p
h
a
e
r
o
s
y
l
l
i
s
s
p
.
I
I
T
h
r
a
c
i
a
v
i
l
l
o
s
i
u
s
c
u
l
a
I
P
a
g
u
r
u
s
p
r
i
d
e
a
u
x
i
I
P
h
y
l
o
c
h
e
r
a
s
m
o
n
a
c
a
n
t
u
s
I
P
s
a
m
m
o
l
y
c
e
a
r
e
n
o
s
a
I
I
S
p
h
a
e
r
o
s
y
l
l
i
s
t
a
y
l
o
r
i
I
I
T
h
y
a
s
i
r
a

e
x
u
o
s
a
I
I
I
P
a
g
u
r
u
s
s
p
.
l
a
r
v
a
I
P
h
y
l
o
c
h
e
r
a
s
t
r
i
s
p
i
n
o
s
u
s
I
P
s
e
u
d
o
b
r
a
n
i
a
s
p
.
I
I
S
p
h
e
n
i
a
b
i
n
g
h
a
m
i
I
T
h
y
o
n
e
f
u
s
u
s
I
P
a
l
a
e
m
o
n
s
e
r
r
a
t
u
s
I
P
i
l
a
r
g
i
s
v
e
r
r
u
c
o
s
a
I
P
s
e
u
d
o
c
u
m
a
l
o
n
g
i
c
o
r
n
i
s
I
I
S
p
i
o
a
r
m
a
t
a
I
I
I
T
i
m
o
c
l
e
a
o
v
a
t
a
I
P
a
n
d
o
r
a
a
l
b
i
d
a
I
P
i
l
u
m
n
u
s
h
i
r
t
e
l
l
u
s
I
P
s
e
u
d
o
c
u
m
a
s
i
m
i
l
i
s
I
I
S
p
i
o
d
e
c
o
r
a
t
u
s
I
I
I
T
o
n
i
c
e
l
l
a
m
a
r
m
o
r
e
a
I
P
a
n
d
o
r
a
i
n
a
e
q
u
i
v
a
l
v
i
s
I
P
i
n
n
o
t
h
e
r
e
s
p
i
s
u
m
N
.
A
P
s
e
u
d
o
c
u
m
a
s
p
.
I
I
S
p
i
o

l
i
c
o
r
n
i
s
I
I
I
T
r
i
c
o
l
i
a
p
u
l
l
u
s
I
P
a
n
d
o
r
a
p
i
n
n
a
I
P
i
o
n
o
s
y
l
l
i
s
s
e
r
r
a
t
a
I
I
P
s
e
u
d
o
p
o
l
y
d
o
r
a
a
n
t
e
n
n
a
t
a
I
V
S
p
i
o
m
a
r
t
i
n
e
n
s
i
s
I
I
I
T
r
i
p
h
o
r
a
a
d
v
e
r
s
a
I
P
a
n
o
p
l
o
e
a
m
i
n
u
t
a
I
P
i
s
i
d
i
a
l
o
n
g
i
c
o
r
n
i
s
I
P
s
e
u
d
o
p
o
l
y
d
o
r
a
p
a
u
c
i
b
r
a
n
c
h
i
a
t
a
I
V
S
p
i
o
s
p
.
I
I
I
T
r
i
p
h
o
r
a
a
s
p
e
r
a
I
P
a
r
a
d
o
n
e
i
s
a
r
m
a
t
a
I
I
I
P
i
s
i
d
i
u
m
s
p
.
i
n
d
e
t
.
I
P
s
e
u
d
o
p
o
l
y
d
o
r
a
p
u
l
c
h
r
a
I
V
S
p
i
o
c
h
a
e
t
o
p
t
e
r
u
s
c
o
s
t
a
r
u
m
I
I
I
T
r
i
p
h
o
r
a
p
e
r
v
e
r
s
a
I
P
a
r
a
d
o
n
e
i
s
l
y
r
a
I
I
I
P
i
s
i
o
n
e
r
e
m
o
t
a
I
I
P
s
e
u
d
o
p
o
l
y
d
o
r
a
s
p
.
I
V
S
p
i
o
c
h
a
e
t
o
p
t
e
r
u
s
s
p
.
I
I
I
T
r
i
v
i
a
m
o
n
a
c
h
a
I
P
a
r
a
g
n
a
t
h
i
a
f
o
r
m
i
c
a
I
I
I
P
i
s
t
a
c
r
i
s
t
a
t
a
I
P
s
e
u
d
o
p
r
o
t
e
l
l
a
p
h
a
s
m
a
N
.
A
S
p
i
o
c
h
a
e
t
o
p
t
e
r
u
s
t
y
p
i
c
u
s
I
I
I
T
r
o
p
h
o
n
o
p
s
i
s
m
u
r
i
c
a
t
u
s
I
P
a
r
a
m
p
h
i
t
r
i
t
e
t
e
t
r
a
b
r
a
n
c
h
i
a
N
.
A
P
l
a
k
o
s
y
l
l
i
s
b
r
e
v
i
p
e
s
I
I
P
s
e
u
d
o
s
y
l
l
i
s
b
r
e
v
i
p
e
n
n
i
s
I
I
S
p
i
o
p
h
a
n
e
s
b
o
m
b
y
x
I
I
I
T
r
y
p
h
o
s
e
l
l
a
n
a
n
o
i
d
e
s
I
P
a
r
a
o
n
i
s
f
u
l
g
e
n
s
N
.
A
P
l
a
t
h
e
l
m
i
n
t
e
s
I
I
P
s
e
u
d
o
s
y
l
l
i
s
s
p
.
I
I
S
p
i
o
p
h
a
n
e
s
k
r
o
y
e
r
i
I
I
I
T
r
y
p
h
o
s
e
l
l
a
s
a
r
s
i
I
P
a
r
a
o
n
i
s
g
r
a
c
i
l
i
s
N
.
A
P
l
a
t
y
n
e
r
e
i
s
d
u
m
e
r
i
l
i
i
I
I
I
P
y
g
o
s
p
i
o
e
l
e
g
a
n
s
I
I
I
S
p
i
r
o
b
r
a
n
c
h
u
s
p
o
l
y
t
r
e
m
a
N
.
A
T
r
y
p
h
o
s
i
t
e
s
l
o
n
g
i
p
e
s
I
I
P
a
r
a
o
n
i
s
l
y
r
a
N
.
A
P
l
e
u
r
o
n
e
c
t
i
d
a
e
s
p
.
I
I
Q
u
a
d
r
a
n
s
s
e
r
r
a
t
u
s
I
S
p
i
s
u
l
a
e
l
l
i
p
t
i
c
a
I
T
u
b
i

c
o
i
d
e
s
b
e
n
e
d
i
i
V
P
a
r
a
p
i
o
n
o
s
y
l
l
i
s
c
f
.
g
e
s
t
a
n
s
I
I
P
o
d
o
c
e
u
s
v
a
r
i
e
g
a
t
u
s
N
.
A
R
a
p
h
i
t
o
m
a
p
u
r
p
u
r
e
a
I
S
p
i
s
u
l
a
s
o
l
i
d
a
I
T
u
b
i

c
o
i
d
e
s
p
s
e
u
d
o
g
a
s
t
e
r
V
P
a
r
a
p
i
o
n
o
s
y
l
l
i
s
g
e
s
t
a
n
s
I
I
P
o
e
c
i
l
o
c
h
a
e
t
u
s
s
e
r
p
e
n
s
I
R
a
p
h
i
t
o
m
a
s
p
.
I
S
p
i
s
u
l
a
s
u
b
t
r
u
n
c
a
t
a
I
T
u
b
u
l
a
n
u
s
p
o
l
y
m
o
r
p
h
u
s
I
I
P
a
r
a
p
i
o
n
o
s
y
l
l
i
s
l
a
b
r
o
n
i
c
a
I
I
P
o
e
c
i
l
o
c
h
a
e
t
u
s
s
e
r
p
e
n
s
I
R
e
t
u
s
a
t
r
u
n
c
a
t
u
l
a
I
S
t
a
u
r
o
c
e
p
h
a
l
u
s
r
u
d
o
l
p
h
i
i
I
V
T
u
b
u
l
a
n
u
s
s
p
p
I
I
P
a
r
a
p
i
o
n
o
s
y
l
l
i
s
m
i
n
u
t
a
I
I
P
o
l
y
c
i
r
r
u
s
a
u
r
a
n
t
i
a
c
u
s
I
V
R
e
t
u
s
a
u
m
b
i
l
i
c
a
t
a
I
S
t
e
n
o
t
h
o
e
m
o
n
o
c
u
l
o
i
d
e
s
I
I
T
u
r
b
e
l
a
r
i
o
s
p
.
N
.
A
P
a
r
a
p
i
o
n
o
s
y
l
l
i
s
s
p
.
I
I
P
o
l
y
c
i
r
r
u
s
c
f
.
m
e
d
u
s
a
I
V
R
h
i
z
o
r
u
s
a
c
u
m
i
n
a
t
u
s
N
.
A
S
t
e
n
o
t
h
o
i
d
a
e
I
I
T
u
r
b
o
e
l
l
a
p
a
r
v
a
I
P
a
r
a
t
h
e
l
e
p
u
s
s
p
.
I
P
o
l
y
c
i
r
r
u
s
m
e
d
u
s
a
I
V
R
i
n
g
i
c
u
l
a
a
u
r
i
c
u
l
a
t
a
I
S
t
e
r
n
a
s
p
i
s
s
c
u
t
a
t
a
I
I
I
T
u
r
b
o
n
i
l
l
a
a
c
u
t
a
I
P
a
r
i
a
m
b
u
s
t
y
p
i
c
u
s
I
I
I
P
o
l
y
c
i
r
r
u
s
s
p
.
I
V
R
i
n
g
i
c
u
l
a
c
o
n
f
o
r
m
i
s
I
S
t
h
e
n
e
l
a
i
s
b
o
a
I
I
T
u
r
b
o
n
i
l
l
a
e
l
e
g
a
n
t
i
s
s
i
m
a
I
P
a
r
i
a
m
b
u
s
t
y
p
i
c
u
s
v
a
r
i
n
e
r
m
i
s
I
I
I
P
o
l
y
c
i
r
r
u
s
t
e
n
u
i
s
e
t
i
s
I
V
R
i
n
g
i
c
u
l
a
s
p
.
I
S
t
h
e
n
e
l
a
i
s
c
f
.
m
i
n
o
r
I
I
T
u
r
b
o
n
i
l
l
a
l
a
c
t
e
a
I
1112
Marine Pollution Bulletin
P
a
r
v
i
c
a
r
d
i
u
m
e
x
i
g
u
u
m
I
P
o
l
y
d
o
r
a
a
n
t
e
n
n
a
t
a
I
V
S
a
b
e
l
l
a
p
a
v
o
n
i
n
a
I
S
t
h
e
n
e
l
a
i
s
l
i
m
i
c
o
l
a
I
I
T
u
r
b
o
n
i
l
l
a
r
u
f
a
I
P
a
r
v
i
c
a
r
d
i
u
m
m
i
n
i
m
u
m
I
P
o
l
y
d
o
r
a
c
a
e
c
a
I
V
S
a
b
e
l
l
a
s
p
.
I
S
t
h
e
n
e
l
a
i
s
m
i
n
o
r
I
I
T
u
r
b
o
n
i
l
l
a
s
p
p
I
P
a
r
v
i
c
a
r
d
i
u
m
o
v
a
l
e
I
P
o
l
y
d
o
r
a
c
i
l
i
a
t
a
I
V
S
a
b
e
l
l
a
r
i
a
a
l
v
e
o
l
a
t
a
I
S
t
h
e
n
e
l
a
i
s
s
p
.
I
I
T
u
r
r
i
t
e
l
l
a
c
o
m
m
u
n
i
s
I
P
a
r
v
i
c
a
r
d
i
u
m
p
a
p
i
l
l
o
s
u
m
I
P
o
l
y
d
o
r
a

a
v
a
I
V
S
a
b
e
l
l
a
r
i
a
s
p
i
n
u
l
o
s
a
I
S
t
r
e
b
l
o
s
o
m
a
b
a
i
r
d
i
N
.
A
T
u
r
r
i
t
e
l
l
a
t
r
i
p
l
i
c
a
t
a
I
P
a
r
v
i
c
a
r
d
i
u
m
s
c
a
b
r
u
m
I
P
o
l
y
d
o
r
a
j
u
v
.
s
p
p
I
V
S
c
a
l
i
b
r
e
g
m
a
i
n

a
t
u
m
I
I
I
S
t
r
e
b
l
o
s
p
i
o
d
e
k
h
u
y
z
e
n
i
I
I
I
U
n
c
i
o
l
a
c
r
e
n
a
t
i
p
a
l
m
a
N
.
A
P
e
c
t
i
n
a
r
i
a
a
u
r
i
c
o
m
a
I
P
o
l
y
d
o
r
a
l
i
g
e
r
i
c
a
I
V
S
c
a
p
h
a
n
d
e
r
l
i
g
n
a
r
i
u
s
I
S
t
r
e
b
l
o
s
p
i
o
s
h
r
u
b
s
o
l
i
i
I
I
I
U
p
o
g
e
b
i
a
c
f
.
t
i
p
i
c
a
I
P
e
c
t
i
n
a
r
i
a
k
o
r
e
n
i
I
P
o
l
y
d
o
r
a
l
i
g
n
i
I
V
S
c
h
i
s
t
o
m
e
r
i
n
g
o
s
c
a
e
c
a
I
I
S
t
r
e
m
b
l
o
s
o
m
a
i
n
t
e
s
t
i
n
a
l
i
s
N
.
A
U
p
o
g
e
b
i
a
d
e
l
t
a
u
r
a
I
P
e
c
t
i
n
a
r
i
a
s
p
.
I
P
o
l
y
d
o
r
a
p
o
l
y
b
r
a
n
c
h
i
a
I
V
S
c
h
i
s
t
o
m
e
r
i
n
g
o
s
r
u
d
o
l
p
h
i
I
V
S
t
r
i
a
r
c
a
l
a
c
t
e
a
I
U
p
o
g
e
b
i
a
p
u
s
i
l
l
a
I
P
e
r
i
n
e
r
e
i
s
c
u
l
t
r
i
f
e
r
a
I
I
I
P
o
l
y
d
o
r
a
p
u
l
c
h
r
a
I
V
S
c
i
o
n
e
l
l
a
l
o
r
n
e
n
s
i
s
N
.
A
S
y
c
o
n
c
i
l
i
a
t
u
m
I
U
p
o
g
e
b
i
a
s
p
.
I
P
e
r
i
o
c
u
l
o
d
e
s
l
o
n
g
i
m
a
n
u
s
I
P
o
l
y
d
o
r
a
s
p
.
I
V
S
c
l
e
r
o
c
h
e
i
l
u
s
m
i
n
u
t
u
s
N
.
A
S
y
c
o
n
r
a
p
h
a
n
u
s
I
U
p
o
g
e
b
i
a
s
t
e
l
l
a
t
a
I
P
h
a
r
u
s
l
e
g
u
m
e
n
I
P
o
l
y
g
o
r
d
i
u
s
a
p
e
n
d
i
c
u
l
a
t
u
s
I
S
c
o
l
a
r
i
c
i
a
s
p
.
I
S
y
l
l
i
s
c
o
r
n
u
t
a
I
I
U
p
o
g
e
b
i
a
t
y
p
i
c
a
I
P
h
a
s
c
o
l
i
o
n
s
t
r
o
m
b
i
I
P
o
l
y
m
n
i
a
n
e
b
u
l
o
s
a
I
I
I
S
c
o
l
a
r
i
c
i
a
t
y
p
i
c
a
I
S
y
l
l
i
s
g
e
r
l
a
c
h
i
I
I
U
r
o
t
h
o
e
b
r
e
v
i
c
o
r
n
i
s
I
P
h
a
s
c
o
l
i
o
n
s
t
r
o
m
b
u
s
I
P
o
l
y
n
o
e
s
c
o
l
o
p
e
n
d
r
i
n
a
I
I
S
c
o
l
e
l
e
p
i
s
f
u
l
i
g
i
n
o
s
a
V
S
y
l
l
i
s
g
r
a
c
i
l
i
s
I
I
U
r
o
t
h
o
e
e
l
e
g
a
n
s
I
P
h
a
s
c
o
l
o
s
o
m
a
e
l
o
n
g
a
t
u
m
I
P
o
l
y
o
p
h
t
h
a
l
m
u
s
p
i
c
t
u
s
I
S
c
o
l
e
l
e
p
i
s
s
p
.
I
I
I
S
y
l
l
i
s
p
r
o
l
i
f
e
r
a
I
I
U
r
o
t
h
o
e
p
o
s
e
i
d
o
n
i
s
I
P
h
a
s
c
o
l
o
s
o
m
a
g
r
a
n
u
l
a
t
u
m
I
I
P
o
m
a
t
o
c
e
r
o
s
l
a
m
a
r
c
k
i
i
N
.
A
S
c
o
l
e
l
e
p
i
s
s
q
u
a
m
a
t
a
I
I
I
S
y
l
l
i
s
s
p
.
I
I
U
r
o
t
h
o
e
p
u
l
c
h
e
l
l
a
I
P
h
a
s
c
o
l
o
s
o
m
a
v
u
l
g
a
r
e
I
P
o
m
a
t
o
c
e
r
o
s
t
r
i
q
u
e
t
e
r
N
.
A
S
c
o
l
o
p
l
o
s
a
r
m
i
g
e
r
I
S
y
l
l
i
s
v
a
r
i
e
g
a
t
a
I
I
V
a
u
t
h
o
m
p
s
o
n
i
a
c
r
i
s
t
a
t
a
N
.
A
P
h
a
x
a
s
p
e
l
l
u
c
i
d
u
s
I
P
o
n
t
o
c
r
a
t
e
s
a
l
t
a
m
a
r
i
n
u
s
I
S
c
r
o
b
i
c
u
l
a
r
i
a
p
l
a
n
a
I
I
I
S
y
n
c
h
e
l
i
d
i
u
m
h
a
p
l
o
c
h
e
l
e
s
I
V
e
n
e
r
a
c
e
a
I
P
h
e
r
u
s
a
m
o
n
i
l
i
f
e
r
a
I
P
o
n
t
o
c
r
a
t
e
s
a
r
e
n
a
r
i
u
s
I
S
c
r
u
p
o
c
e
l
l
a
r
i
a
s
c
r
u
p
e
a
N
.
A
S
y
n
c
h
e
l
i
d
i
u
m
m
a
c
u
l
a
t
u
m
I
V
e
n
e
r
u
p
i
s
a
u
r
e
a
I
P
h
e
r
u
s
a
p
l
u
m
o
s
a
I
P
o
r
t
u
m
n
u
s
l
a
t
i
p
e
s
I
S
e
m
i
v
e
r
m
i
l
i
a
s
p
.
N
.
A
T
a
n
a
i
s
d
u
l
o
n
g
i
i
N
.
A
V
e
n
e
r
u
p
i
s
p
u
l
l
a
s
t
r
a
I
P
h
e
r
u
s
a
s
p
.
I
P
o
t
a
m
i
l
l
a
r
e
n
i
f
o
r
m
i
s
N
.
A
S
e
r
t
u
l
a
r
i
i
d
a
e
I
T
a
p
e
s
d
e
c
u
s
s
a
t
a
I
V
e
n
e
r
u
p
i
s
r
h
o
m
b
o
i
d
e
s
I
P
h
i
l
i
n
e
a
p
e
r
t
a
I
I
P
o
t
a
m
i
l
l
a
s
p
.
N
.
A
S
e
x
t
o
n
i
a
l
o
n
g
i
r
o
s
t
r
i
s
I
I
T
e
l
e
p
s
a
v
u
s
c
o
s
t
a
r
u
m
I
V
e
n
e
r
u
p
i
s
s
e
n
e
g
a
l
e
n
s
i
s
I
P
h
i
l
i
n
e
l
o
w
e
n
i
I
I
P
o
t
a
m
i
l
l
a
t
o
r
e
l
l
i
N
.
A
S
i
g
a
l
i
o
n
c
f
.
m
a
t
h
i
l
d
a
e
I
I
T
e
l
i
n
a
t
e
n
u
i
s
I
V
e
n
u
s
c
a
s
i
n
a
I
P
h
i
l
i
n
e
s
p
p
I
I
P
o
t
a
m
o
p
y
r
g
u
s
j
e
n
k
i
n
s
i
I
I
S
i
g
a
l
i
o
n
m
a
t
h
i
l
d
a
e
I
I
T
e
l
l
i
m
y
a
f
e
r
r
u
g
i
n
o
s
a
I
I
V
e
n
u
s
f
a
s
c
i
a
t
a
I
P
h
o
l
o
e
m
i
n
u
t
a
I
I
P
r
a
x
i
l
l
e
a
o
e
r
s
t
e
d
i
N
.
A
S
i
g
a
l
i
o
n
s
q
u
a
m
a
t
u
m
I
I
T
e
l
l
i
n
a
c
o
m
p
r
e
s
s
a
I
V
e
n
u
s
g
a
l
l
i
n
a
I
P
h
o
l
o
e
s
y
n
o
p
t
h
a
l
m
i
c
a
I
I
P
r
i
o
n
o
s
p
i
o
c
a
s
p
e
r
s
i
I
V
S
i
p
h
o
n
o
e
c
e
t
e
s
k
r
o
y
e
r
a
n
u
s
I
T
e
l
l
i
n
a
d
o
n
a
c
i
n
a
I
V
e
n
u
s
j
u
v
.
s
p
.
I
P
h
o
r
o
n
i
s
p
s
a
m
m
o
p
h
i
l
a
I
P
r
i
o
n
o
s
p
i
o
c
i
r
r
i
f
e
r
a
I
V
S
i
p
h
o
n
o
e
c
e
t
e
s
s
p
.
I
T
e
l
l
i
n
a
f
a
b
u
l
a
I
V
e
n
u
s
o
v
a
t
a
I
P
h
o
t
i
s
l
o
n
g
i
c
a
u
d
a
t
a
I
P
r
i
o
n
o
s
p
i
o
e
h
l
e
r
s
i
I
V
S
i
p
h
o
n
o
e
c
e
t
e
s
s
t
r
i
a
t
u
s
I
T
e
l
l
i
n
a
p
u
s
i
l
l
a
I
V
e
n
u
s
s
t
r
i
a
t
u
l
a
I
P
h
o
x
o
c
e
p
h
a
l
u
s
r
u
d
o
l
p
h
i
i
I
P
r
i
o
n
o
s
p
i
o
f
a
l
l
a
x
I
V
S
i
p
u
n
c
u
l
a
I
T
e
l
l
i
n
a
p
y
g
m
a
e
a
I
V
e
n
u
s
v
e
r
r
u
c
o
s
a
I
P
h
t
h
i
s
i
c
a
m
a
r
i
n
a
I
P
r
i
o
n
o
s
p
i
o
m
a
l
m
g
r
e
n
i
I
V
S
k
e
n
e
a
s
p
.
I
I
I
T
e
l
l
i
n
a
s
p
.
I
V
e
r
e
t
i
l
l
u
m
c
y
n
o
m
o
r
i
u
m
I
P
h
y
l
l
o
c
h
a
e
t
o
p
t
e
r
u
s
s
p
.
N
.
A
P
r
i
o
n
o
s
p
i
o
m
u
l
t
i
b
r
a
n
c
h
i
a
t
a
I
V
S
k
e
n
i
a
s
e
r
p
u
l
o
i
d
e
s
N
.
A
T
e
l
l
i
n
a
s
q
u
a
l
i
d
a
I
V
e
r
e
t
i
l
l
u
m
s
p
.
I
P
h
y
l
l
o
d
o
c
e
g
r
o
e
l
a
n
d
i
c
a
I
I
P
r
i
o
n
o
s
p
i
o
s
p
.
I
V
S
o
c
a
r
n
e
s
e
r
y
t
h
r
o
p
h
t
h
a
l
m
u
s
N
.
A
T
e
l
l
i
n
a
t
e
n
u
i
s
I
V
e
r
r
u
c
a
s
t
r
o
m
i
a
I
P
h
y
l
l
o
d
o
c
e
l
a
m
e
l
l
i
g
e
r
a
I
I
P
r
i
o
n
o
s
p
i
o
s
t
e
e
n
s
t
r
u
p
i
I
V
S
o
l
e
n
m
a
r
g
i
n
a
t
u
s
I
T
e
r
e
b
e
l
l
a
l
a
p
i
d
a
r
i
a
I
V
i
t
u
p
e
r
i
s
e
s
r
i
b
o
s
a
V
P
h
y
l
l
o
d
o
c
e
l
a
m
i
n
o
s
a
I
I
P
r
o
c
e
s
s
a
c
a
n
a
l
i
c
u
l
a
t
a
I
S
o
l
e
n
a
c
e
a
I
T
e
r
e
b
e
l
l
i
d
e
s
s
t
r
o
e
m
i
I
X
a
n
t
h
o
p
i
l
i
p
e
s
N
.
A
P
h
y
l
l
o
d
o
c
e
l
i
n
e
a
t
a
I
I
P
r
o
c
e
s
s
a
m
o
d
i
c
a
I
S
p
h
a
e
r
o
d
o
r
o
p
s
i
s
s
p
.
N
.
A
T
e
r
e
b
e
l
l
o
m
o
r
p
h
a
s
p
.
i
n
d
e
t
I
I
X
e
n
o
s
y
l
l
i
s
s
c
a
b
r
a
I
I
P
h
y
l
l
o
d
o
c
e
l
o
n
g
i
p
e
s
I
I
P
r
o
c
e
s
s
a
n
o
u
v
e
l
i
I
S
p
h
a
e
r
o
m
a
m
o
n
o
d
i
I
I
T
h
a
l
a
s
s
e
m
a
n
e
p
t
u
n
i
I
Z
e
n
o
b
i
a
n
a
p
r
i
s
m
a
t
i
c
a
I
I
P
h
y
l
l
o
d
o
c
e
m
a
c
u
l
a
t
a
I
I
P
r
o
c
e
s
s
a
p
a
r
v
a
I
S
p
h
a
e
r
o
m
a
r
u
g
i
c
a
u
d
a
t
a
I
I
T
h
a
r
y
x
m
a
r
i
o
n
i
N
.
A
Z
o
a
n
t
h
a
r
i
a
s
p
.
I
P
h
y
l
l
o
d
o
c
e
m
u
c
o
s
a
I
I
I
P
r
o
c
e
s
s
a
s
p
.
I
S
p
h
a
e
r
o
m
a
s
e
r
r
a
t
u
m
I
I
T
h
e
l
e
p
u
s
s
e
t
o
s
u
s
N
.
A
P
h
y
l
l
o
d
o
c
e
p
a
r
e
t
t
i
I
I
P
r
o
t
o
d
o
r
v
i
l
l
e
a
k
e
f
e
r
s
t
e
i
n
i
I
I
S
p
h
a
e
r
o
s
y
l
l
i
s
b
u
l
b
o
s
a
I
I
T
h
i
a
s
c
u
t
e
l
l
a
t
a
I
I
a
N
.
A
.

n
o
t
a
s
s
i
g
n
e
d
.
1113
Volume 40/Number 12/December 2000
Bogdanos, C. and Satsmadjis, J. (1985) Quantitative eect of sediment
coarseness and depth on the macrobenthos of an unpolluted and
closed Mediterranean Gulf. Revue Internationale d' Oceanographie
medicale 77/78, 7485.
Borja, A., Valencia, V., Garca, L. and Arresti, A. (1995) Las
comunidades bent onicas intermareales y submareales en San
Sebastian-Pasajes (Guip uzcoa, N de Espa~ na). Actas IV Coloquio
Internacional de Oceanografa del Golfo de Vizcaya (Santander)
165181.
Borja, A., Franco, J., Belzunce, M. J. and Valencia, V. (1999a) Red de
Vigilancia y Control de la calidad de las aguas litorales del Pas
Vasco (oto~ no 1997verano 1998). Departamento de Ordenaci on del
Territorio, Vivienda y Medio Ambiente, Gobierno Vasco, 333
pp+appendices.
Borja, A., Belzunce, M. J., Franco J. and Castro, R. (1999b)
Seguimiento ambiental de los estuarios del Nervi on, Barbad un y
Butr on durante 1998. Consorcio de Aguas Bilbao-Bizkaia, 228
pp+appendices.
Cairns, J., Douglas, W. A., Busey, F. and Chaney, M. D. (1968) The
sequential comparison index a simplied method for non-
biologists to estimate relative dierences in biological diversity in
stream pollution studies. Journal of Water Pollution Control. Fed 40,
16071613.
Chandler, J. R. (1970) A biological approach to water quality
management. Water Pollution Control 69, 415422.
Clements, W. H., Cherry, D. S. and Van Hassel, J. H. (1992)
Assessment of the impact of heavy metals on benthic communities
at the Clinch River (Virginia): evaluation of an index of community
sensitivity. Canadian Journal of Fisheries and Aquatic Sciences 49,
16861894.
Dauer, D. M. (1993) Biological criteria, environmental health and
estuarine macrobenthic community structure. Marine Pollution
Bulletin 26 (5), 249257.
Diaz, R. J. and Rosenberg, R. (1995) Marine benthic hypoxia: a review
of its ecological eects and the behavioural responses of benthic
macrofauna. Oceanography and Marine Biology Annual Review 33,
245303.
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 eects of natural phenomena from sewage-
industrial wastewater eects. Estuarine, Coastal and Shelf Science
33, 383407.
Franco, J., Borja, A., Belzunce, M. J. Valencia, V. (1999) Campa~ na de
medici on de variables biol ogicas y fsico-qumicas en el estuario del ro
Oiartzun y area costera pr oxima a cala Murgita. Departamento de
Obras Hidraulicas y Urbanismo de la Diputaci on Foral de
Gipuzkoa, 197 p. +appendices.
Franklin, A. and Jones, J. (1994) Monitoring and surveillance of non-
radiactive contaminants in the aquatic environment and activities
regulating the disposal of wastes at sea, 1992. Aquatic Environment
Monitoring Report, MAFF 40, 183.
Glemarec, M. (1986) Ecological impact of an oil-spill: utilisation of
biological indicators. IAWPRC-NERC Conference, July 1985.
IAWPRC Journal 18, 203211.
Glemarec, M. and Hily, C. (1981) Perturbations apportees a la
macrofaune benthique de la baie de Concarneau par les euents
urbains et portuaires. Acta Oecologica Oecologia Applicata 2, 139
150.
Gonzalez-Oreja, J. A. and Saiz-Salinas, J. I. (1998) Exploring the
relationships between abiotic variables and benthic community
structure in a polluted estuarine system. Water Research 32 (12),
37993807.
Grall, J. and Glemarec, M. (1997) Using biotic indices to estimate
macrobenthic community perturbations in the Bay of Brest.
Estuarine, Coastal and Shelf Science 44 (suppl. A), 4353.
Gray, J. S. (1979) Pollution-induced changes in populations. Philo-
sophycal Transactions of the Royal Society of London. Series B, 286,
545561.
Hall, S. J. (1994) Physical disturbance and marine benthic communi-
ties: life in unconsolidated sediments. Oceanography and Marine
Biology Annual Review 32, 179239.
Hily, C. (1984) Variabilit e de la macrofaune benthique dans les milieux
hypertrophiques de la Rade de Brest. These de Doctorat dEtat,
Univ. Bretagne Occidentale. Vol. 1, 359 pp; Vol. 2, 337 pp.
Hily, C., Le Bris, H. and Glemarec, M. (1986) Impacts biologiques des
emissaires urbains sur les ecosystemes benthiques. Oceanis 12, 419
426.
Holme, N. A. and McIntyre, A.D. (1971) Methods for the Study of
Marine Benthos, p. 387. Blackwell, Oxford.
ISO-BMWP (1979) Assessment of the Biological Quality of Rivers by a
Macroinvertebrate Score. ISO/TC147/SC5/WG6/N5, International
Standards Organisation, p. 18.
Kristensen, E. and Andersen, F. O. (1993) Determination of organic
carbon in marine sediments: a comparison of two CHN-analyzer
methods. Journal of Experimental Marine Biology and Ecology 109,
1523.
Long, E. R., MacDonald, D. D., Smith, S. L. and Calder, F. D. (1995)
Incidence of adverse biological eects within ranges of chemical
concentrations in marine and estuarine sediments. Environmental
Management 19, 8197.
MAFF (1993) Analysis and interpretation of benthic community data
at sewage-sludge disposal sites. Aquatic Environmental Monitoring
Report, MAFF Directorate of Fisheries Research, Lowestoft, Vol. 37,
80 pp.
Majeed, S. A. (1987) Organic matter and biotic indices on the beaches
of North Brittany. Marine Pollution Bulletin 18 (9), 490495.
Mearns, A. J. and Word, J. Q. (1982) Forecasting eects of
sewage solids on marine benthic communities. In Ecological Stress
and the New York Bight: Science and management ed. G. F. Mayer,
pp. 495512. Estuarine Research Federation, Columbia, South
Carolina.
Mouthon, J. (1993) Un indice biologique lacustre base sur lexamen
des peuplements de mollusques. Bulletin Francaise de la P eche et la
Piscicul 331, 397406.
OConnor, 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 in
relation to organic enrichment and pollution of the marine
environment. Oceanography and Marine Biology Annual Review
16, 229311.
Ritter, C. and Montagna, P. A. (1999) Seasonal hypoxia and model of
benthic response in a Texas bay. Estuaries 22 (1), 720.
Roberts, R. D., Gregory, M. R. and Fosters, B. A. (1998) Developing
an ecient macrofauna monitoring index from an impact study A
dredge spoil example. Marine Pollution Bulletin 36 (3), 231235.
R.N.O. (1998) Surveillance du Milieu Marin. Travaux du Reseau
National d'Observation de la Qualite du Milieu Marin. Edition
1998. Ifremer et Ministere de lAmenagement du Territoire et de
lEnvironnement, 52 pp.
Saiz-Salinas, J. I. (1997) Evaluation of adverse biological eects
induced by pollution in the Bilbao estuary. Environmental Pollution
96 (3), 351359.
Salen-Picard, C. (1983) Schemas devolution dune biocenose macro-
benthique du substrat meuble. Comptes Rendus de l9Academie des
Sciencies de Paris 296, 587590.
Snelgrove, P. V. R. and Butman, C. A. (1994) Animal-sediment
relationships revisited: cause versus eect. Oceanography and
Marine Biology Annual Review 32, 111177.
Stark, J. D. (1993) Performance of the macroinvertebrate community
index: eects of sampling method, sample replication, water depth,
current velocity and substratum on index values. New Zealand
Journal of Marine and Freshwater Research 27, 463478.
Washington, H. G. (1984) Diversity, biotic and similarity indices. A
review with special relevance to aquatic ecosystems. Water Research
18, 653694.
Weisberg, S. B., Ranasinghe, J. A., Dauer, D. M., Schaner, L. C.,
Diaz, R. J. and Frithsen, J. B. (1997) An estuarine benthic index
of biotic integrity (B-IBI) for Chesapeake Bay. Estuaries 20 (1),
149158.
Woodiwiss, F. S. (1964). The biological system of stream classication
used by the Trent River Board. Chemistry Industries. 11, 443447.
1114
Marine Pollution Bulletin