Ecological Analysis in a Polluted Area of Algeciras Bay (Southern

Pergamon
PII: S0025-326X(97)00046-5
Marine Pollution Bulletin, Vol. 34, No. 10, pp. 780-793, 1997
© 1997 Elsevier Science Ltd
All rights reserved. Printed in Great Britain
0025-326X/97 $17.00 + 0.00
Ecological Analysis in a Polluted Area
of Algeciras Bay (Southern Spain):
External 'Versus' Internal Outfalls and
Environmental Implications
F. J. ESTACIO*, E. M. GARCIA-ADIEGO*, D. A. FAt, J. C. GARCIA-G6MEZ*, J. L. DAZA*, F. HORTAS*
and J. L. GtMEZ-ARIZA:~
*Laboratorio de Biologla Marina, Departamento de Fisiologla y Biologia Animal, Facultad de Biologla, Universidad de
Sevilla. Apdo. 1095, E-41080 Sevilla, Espada
tDepartment of Oceanography, University of Southampton, Highfield, Southampton S017 1BJ, U.K.
~Departamento de Quimica y Ciencias de los Materiales, Universidad de Huelva, 2189 La Rdbida, Huelva, Espada
The effects of organic effluents both inside and outside the
Saladillo Harbour (Algeciras, southern Spain) are
investigated. Although the external outfall has a greater
rate of discharge, the low levels of hydrodynamism inside
the harbour create an area of relatively stagnant water,
with markedly different environmental conditions. A clear
gradient of decreasing pollution levels was observed from
the interior to the exterior of the harbour. This was
reflected both in the physieochemical water and sediment
parameters and in their respective microbiological
parameters. Macrobenthic species also mirrored the
pollution gradients as did the applied analysis. The effects
of the external outfall are seen to dissipate and clear
much closer to the external pollution source than in the
internal, enclosed harbour area. © 1997 Elsevier Science
Ltd
Keywords: macrobenthos; sediment; pollution; outfalls;
southern Spain.
The Saladillo Harbour in the Bay of Algeciras (southern
Spain) has suffered a series of transformations due to
the growth of the port of Algeciras. These have created
conditions of reduced water movement and renewal in
its interior. This situation is worsened by the existence
of two raw sewage disposal points (one internal, one
external) that originate from the City of Algeciras and
the Saladillo River that transport a great quantity of
organic waste. The internal outfall has a flow capacity
of 3251 x 106 1 d a y - l and the external a flow capacity of
22580x106 1 day - l . The latter also has a subsidiary
outflow into the harbour that is only used when outfall
levels are higher than the norm. There are also two
present small ship repair yards and mooring facilities
for small fishing boats on its northern side. Via physical,
780
chemical and microbiological analysis of the waters and
sediments undertaken in this study the presence of
organic contamination in the Harbour and in the
immediate vicinity of the exterior outfall has become
evident.
An extensive literature has described the close
relationship between the macroinfauna in the sediment
and the effect of contaminants on the medium (Reish,
1959, 1971, 1986; Pearson, 1975; Pearson and Rosenberg, 1976, 1978; Dauvin, 1982; Gray and Pearson,
1982; Bilyard, 1987; Warwick et al., 1990; Krtncke et
al., 1992; Warwick, 1993; Simboura et al., 1995).
Physical, chemical and microbiological analysis of the
surface water and sediment characteristics were undertaken together with the application of univariate and
multivariate techniques to the biotic data in order to
measure changes caused to the community by pollution
(Field, 1971; Gray, 1981; Ibafiez and Dauvin, 1988;
Gray et al., 1988; Warwick et al., 1990). Through their
relationship with physical and chemical variables in the
sediments, it has been possible to show the existence of
a gradient from the interior of the Harbour as the zone
most affected by effluents to the less perturbed exterior
(Gray and Pearson, 1982; Reish, 1986; Ltpez-Jamar
and Cal, 1990; Krtncke et al., 1992). It has also been
possible to compare the differing effects of the effluents
both in the interior and the exterior of the Harbour due
to different hydrodynamic conditions.
M a t e r i a l s and M e t h o d s
The study was conducted in June of 1993 in the
Saladillo Harbour in the western side of the Bay of
Algeciras (Fig. l(a and b)). Half of the Harbour bottom
is formed by a rocky substratum and the remainder by
sediments. A breakwater parallel to the coastline acts as
a physical barrier between the interior and exterior of
Volume M/Number 10/October 1997
A
EXTERNAL
j~..
OUTFALL~
~/~
SALADILLO
B
Fig. 1 (a) Locationof SaladilloHarbour. (b) Locationof ettluentsand
sampling areas.
the Harbour. The sea bottom on the exterior is mainly
composed of rocks. On the exterior side towards the
northern end of the breakwater there exists a further
urban effluent outfall which also originates from the
City of Algeciras. Due to the morphology of the
Harbour and its location it is well protected from the
actions of the winds and waves. Only easterly (due to
refraction by the Rock of Gibraltar) and south-easterly
winds with a frequency equal to or greater than 3 5 0
affect the interior of the Harbour to any degree. Data
supplied by Autoridad Portuaria de la Bahia de Algeciras (1993) on the range of values obtained for the coefficient of agitation (H/Ho where H is the mean height of the
upper third of maximal wave sizes, and Ho is the wave
height over indefinite depths, calculated using the
MIKE21 matematical model) were averaged to obtain
mean values for each station and show how even in conditions of predominant easterly and south-easterly wind,
the area contained within stations 2, 3, 6 and 7 show
lower values of agitation and consequently hydrodinamism. Figure 2 shows the distribution of the mean values
obtained for all the stations. These values were also ineluded as abiotie parameters in the statistical analysis.
The study zone, both inside and outside the Harbour,
was divided into 200x200 m square areas. This was
selected as the area for study as it is the same as the area
formed by the ship repair yard at the northern end of
the Harbour (Station 7, see Fig. 1(b)). Only 9 of the 30
quadrats sampled in the study were selected for the
study of the benthic communities (Fig. 1(b)) and for the
physical and chemical analysis of the sediments (depth
between 2 and 9 m) due to the presence of rocky
781
Marine Pollution Bulletin
:: ~:i
:::
s 8~:::8:X:~:z,
: : : : : :::.:".¢;;;:
. >,-:,:,;.
ii!
i ;i!i!~
Fig. 2 Graphical representation of the mean valuescalculated for the
agitation coeltieient (H/I-lo)for all the stations (Data s o u r c e :
Autoridad Portuaria de la Bahiade Algeciras,1993).
outcrops in the others. These were selected based on
their varying distances from the pollution foci in both
the interior and exterior of the Harbour. At the centre
of all the quadrats water samples were taken for
physical, chemical and microbiological analysis. At the
same point in each of the nine selected quadrats,
samples were taken for community data analysis using a
van Veen grab (0.05 m 2) as the sampling tool. Five
replicates were found to be sufficient to estimate the
total diversity. The samples were sieved using a 0.5 mm
mesh and specimens found were preserved in 4%
formaldehyde, stained with bengal rose and were
determined to species level almost in their totality.
Water samples were taken in all 30 stations in the
study area for physical and chemical analysis. For these,
salinity, density, mean temperature, chlorophyll a, b
and c, dissolved oxygen (DO), biological oxygen
demand (BOD), total hydrocarbons, total fats, turbidity, nitrites, nitrates, ammonia and phosphates were
measured. For the sediment, percentage of organic
material, total nitrogen, phosphate, fats, hydrocarbons,
granulometry and percentage water content were
measured.
Measurements of dissolved oxygen (ppm) were done
in situ using an oxygen electrode. BOD (ppm) was
ascertained after incubating the samples over 5 days at
20°C. Ammonia (ppm) was measured using a selective
electrode. Nitrite (ppb), nitrate (ppm), chlorophyll
(ppm) and phosphates (ppb) were measured using UV
visible spectrophotometry. Fats and hydrocarbons
(ppm) were measured by extraction and F T - I R spectrophotometry. Total nitrogen (ppm) in the sediment was
assessed via Kjeldahl digestion and further determination with an ammonia selective electrode. Organic
material (%) was analysed by ashing to 500°C (mean
value for 3 replicates per sample) of subsamples of
sediment previously dried at 100°C during 24h.
Granulometry was determined by Buchanan and
Kain's method (Buchanan and Kain, 1984) for
782
sediments with a percentage of silt less than 5 and
with Bouyoucos method (Bouyoucos, 1934) for samples
with a percentage higher than 5.
In turn, and in the same way as for the earlier
analysis, water samples were taken at the centre of the
30 quadrats and also at the outfall points for
microbiological analysis. These samples were conserved
in sterile containers and kept in cork and gelatine packs
until their arrival at the laboratory where they were
frozen. With these the quantity of total aerobes (gram
positive and gram negative bacteria with growth in
aerobic conditions) were obtained, as were total
coliforms (bacilli gram negative or facultative anaerobes
oxidases that ferment lactose with production of acids
and gas at 307°C in a maximum time of 48 h) and faecal
coliforms (total coliforms that ferment lactose with
production of acid and gas at 35°C in a maximum time
of 24 h). These last two are indicators of levels of recent
faecal pollution such as stated in Directive 75/440/EEC
for bathing waters. Results in all 3 cases were expressed
as number of bacteria per 100 ml of sample and these
were contrasted to the guide values (values beyond
which remedial action is suggested) and imperative
values (values beyond which remedial action is
obligatory) that are prescribed by the normative for
total and faecal coliforms.
As only one sampling was undertaken, results
obtained using the biotic and abiotic water parameter
information will have a limited value as it was not
possible to establish whether these readings were
temporally representative. Nevertheless, it was considered that due to the conditions of reduced water
movement found (particularly in the interior), their
inclusion could still generate relevant results. The
sediment parameters were also sampled on only one
occasion but as these have a greater temporal stability
they were considered as representative of overall
conditions.
To correctly examine the results obtained for the
communities of the infaunal macrobenthos a number of
diverse techniques and models were employed. Univariate analyses provided the total number of species,
total abundance, total biomass, Shannon-Wiener and
Pielou's equitativity index (Shannon and Weaver, 1963;
Pielou, 1966) for each of the stations (calculated on the
datasets generated by aggregating all five samples). The
differences between all of these population parameters
for all samples at each of the stations with the exception
of the biomass were tested with one-tailed ANOVAs
using Tuokey's test for statistical significance after the
data was tested for normality using the KolmogorovSmirnov test and Bartlett's test for homogeneity of
variances.
Using the Plymouth Routines In Multivariate
Ecological Analysis (PRIMER) package, the data
were analysed using the Bray-Curtis index of similarity
(Bray and Curtis, 1957) and a dendrogram created using
the UPGMA method (Romesburg, 1984) with which
Volume 34/Number 10/October 1997
the existence of groupings between stations based on
their similarities was obtained. The data for this were
previously transformed using a root-root transformation, given the high dominance levels of some species
(Clarke and Warwick, 1994).
Graphical representation of cumulative percentage of
abundances and the cumulative percentage of biomass
can be compared as ABC (abundance biomass
comparison) curves, proposed by Warwick (1986) and
based on the K-dominance curves of Lambshead et al.
(1983). This technique has been employed in some
studies to detect community perturbation (Warwick et
al., 1987; Gray et al., 1988; Ibafiez and Dauvin, 1988;
Austen et al., 1989; Ritz et al., 1989; Simboura et al.,
1995). In order to quantify the interpretations deriving
from this model the SEP index proposed by McManus
and Pauly (1990) was used. This index is based on the
relationship between the calculated Shannon diversity
values (H') of the abundances and biomasses.
An alternative method that attempts to elucidate the
main factors affecting distributions was proposed by
Clarke and Ainsworth (1993) and involves the comparison of the (rank) similarity matrices which underlie the
resulting PCA ordinations of all possible permutations
of the environmental data and correlating these with the
similarity matrix obtained for an MDS of species
abundances. The subset of environmental factors that
best explains the observed patterns is then obtained by
choosing the combination that gives the highest
correlations using Spearman's test for non-parametric
ranges. This was achieved using the BIOENV extension
to the P R I M E R package.
Results
Physicochemical parameters and microbiological
variables
Table 1 shows the main results obtained. It will be
seen that density does not show significant differences
between sites and neither does the mean water
temperature. In contrast, turbidity is higher (low
Secchi disk values) and salinity lower in the internal
stations most closely located to the effluents (1, 2 and 3),
stabilizing as one approaches the harbour entrance.
Decreased values for pH were also obtained at these
sites. With respect to the chlorophyll values, it is
interesting to note the high values obtained at stations
9 and 15. Low levels of DO were also found in the
interior of the harbour, particularly so at station 3 and
were also low close to the external outfall. Stations 4, 5,
6 and 7 showed intermediate DO values. Again, BOD is
very high in stations close to effluents (including the
exterior effluent), falling towards the harbour mouth,
and this result is also found for levels of ammonia.
Perhaps surprisingly, fats and hydrocarbon levels in the
water are low; moreover, levels of nitrates, nitrites and
phosphates can be considered normal, although these
are higher at stations 1, 2, 3 and 21, especially the
nitrites and phosphates. In general, 'exterior' values
show an improvement in environmental conditions as
one moves away from the harbour's sphere of influence.
With regard to the sediments (Table 2), stations 2 and
3 show an increased level of organic material, higher
even than that obtained for station 1. This may be due
to the greater content of fine fractions in the first two.
Nevertheless stations 6 and 7 stand out with even higher
values of fine fractions than the aforementioned
stations. To these must be added the highest levels of
total nitrogen found and elevated hydrocarbon readings. Particularly high levels of hydrocarbons in station
3 should also be noted. In the same manner, phosphate
levels are also high in stations 1, 2 and 3 and diminish in
the same way as other sediment parameters towards the
external stations. Granulometry is predominantly fine in
the internal stations, again becoming more coarse as
one moves out of the harbour. Values for all sediment
quality parameters obtained for station 13 (next to
external outfall) are similar in all respects to those
obtained for the internal stations (1, 2 and 3), although
probably due to a greater turnover of water, these
conditions improve more rapidly as one moves away
from this pollution source.
Following the 'Guide' and 'Imperative' values
proposed by Directive 75/440/EEC for bathing waters,
Fig. 3 shows the levels of the different microbiological
parameters found at each station. A simple scaled rank
is used to show whether a particular sample proves
higher (or not) than that required by law. High values
are found close to the internal effluent points with a
progressive decrease as one moves away towards the
exterior where values can be considered as normal.
Normal values are reached very close to the external
station.
Dendrograms based on the euclidean distance have
been created from previously log (x+ 1) transformed
and standardized water physicochemical data (abiotic)
and the Bray-Curtis index of similarity from root-root
transformed microbiological data. The resulting groupings are shown in Figs 4 and 5 in order to show
similarities between methods. Some differences can be
seen but a clear internal/external gradient is evident,
approaching normal conditions in the stations farthest
away from the harbour. The strong dilution of the
exterior effluent is also clearly visible especially in a
northerly direction.
Macrobenthos
The species found in the interior stations are
characteristic of disturbed environments due to a high
content of organic material. Highly dominant in this
area is the polychaete Capitella capitata which drops in
abundance towards the harbour mouth (98.5% to
16.8%). Accompanying polychaete species Cirratulus
cirratus, Cirriformia tentaculata, Capitomastus minimus
and Notomastus latericius have also been associated
with high levels of organic enrichment (Theede et al.,
783
Marine Pollution Bulletin
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784
Volume M/Number 10/Oetober 1997
TABLE 2
Values obtained for sediments variables.
Site
1
2
3
6
7
9
11
13
17
Depth (m)
Hydrocarbons
(ppm)
Fats (ppm)
Phosphate
(P,ppm)
Nitrogen
(N,ppm)
Organic
matter (%)
Sand (%)
Water
content (%)
2
3
3
4
4
4
7
8
9
332
863
4415
891
1179
106
20
25
13
38
97
229
82
0
11
31
38
8
933
800
1537
719
789
484
356
450
388
463
863
1028
1574
2011
223
120
79
120
2.9
6.8
6.3
8.1
13.2
3.7
2.9
2
3.3
74
33
40
25
20
98
99
99
98
32.58
40.12
56.38
54.65
61.04
30.77
26.87
23.99
27.68
Tailnledfurms I./100 NO
O
•
>!0.000
10.000..500
•
<500
Fueal ulfuu'iu (/!001
0
>2.000
•
2.ram
'~
<100
N
Fig. 3 Total values for total and faecal coliforms in the samples taken:
the space internal of the spheres shown is directly related to the
'guide' and 'imperative' values for water quality (Directive 75/
440/EEC).
1969; Pearson and Rosenberg, 1978). The only bivalves
present in the interior stations, Abra alba and Mysella
bidentata appear in the stations closest to the open sea.
In Station 9 and for the exterior stations other bivalve
species such as Digitaria digitaria, Gouldia minima,
Dosinia lupinus and Clausinella fasciata indicate the
presence of substratum composed of high levels of
coarse material (Glemarec, 1969) in the form of
bioclasts derived f r o m the proximal rocky substrata.
Even though the proportion of polychaete abundance
remains high, (72.72%), the proportion of mollusc
abundance (3.07%) and crustaceans (22.84%) especially
gammarids, increases in the external stations (Table 3).
Univariate analysis
Species richness, total n u m b e r of individuals, total
biomass, diversity and equitability in each station
consistently show a gradual increase f r o m the interior
to the exterior of the h a r b o u r (Fig. 6). The results of
a one-way test of variances between samples in each
station using Tuckeys Test are also shown in Table 4.
With the exception of stations 1 and 2 for diversity
and 13 and 17 for number of species we can
generalise that the stations closest to the interior
effluents are not significantly different but are
different with respect to stations 6 and 7 which are
themselves very similar to each other. In turn, these
show clear differences to the external stations which
again show high levels of similarity between
themselves. I f we compare the values obtained with
these parameters at station 13, close to the external
effluent to those obtained for stations 1, 2 and 3 we
will find significant differences exist (Table 5). A oneway analysis of variance on each of the parameters
785
Marine Pollution Bulletin
4
EUCLIDEAN DISTANCES
3.53 2 . 5 2 1.5 1 0.5 0
,
i
,.-i
1,-4
~ ,
1
ul,
•
Fig. 4 Cluster analysis of physicochemical water variables: the
different groups are shown via differential shading in the
above diagram.
1
2
3
4
9
II
7
~17
'i
18
t'i
BRAY-CURTIS SIMILARITY
Fig. 5 Cluster analysis of the observed microbiologicalvariables: the
different groups are shown via differential shading in the above
diagram.
indicates significant differences between the stations
(Table 6).
Similarity analysis
Species abundance data was root-root transformed
and a similarity matrix was calculated using the Bray786
Curtis index. The resulting dendrogram was obtained
using the U P G M A method (Fig. 7). This cluster
analysis clearly shows three groups which in turn
integrate most internal stations, the intermediate
stations close to the harbour m o u t h and the external
stations including station 9.
Volume 34/Number 10/October 1997
~
B Diversity I
2.5 -
•
External outfall
[ ] Evenness
-
2 "Internal outfall
1.5
0
1
2
3
6
7
9
Station
1.6
11
13
0.5 ~o
17
3000
Ex~
2500
~. 1
Biomass
2000
!°fl
•
n]
0.6
0.4
nternal outfall
1
1500
500
I I II
2
3
6
7
11
9
13
17"
Station
External outfaU
80
60
20
0
_ Internal ouffall
1
2
3
6
7
9
11
1
13
17
Station
Fig. 6 Graphical representation of the total species, number o f
individuals, biomass (grs-station 17 is not included-), diversity
(Shannon-Wiener) and evenness (Pielou) for each of the
stations (calculated on the datasets generated by aggregating
all five samples).
TABLE 3
TABLE 4
Percentages for each taxonomic group found at the internal and
external stations.
One-way ANOVA (F-ratio values) o f values obtained for inter-station
univariate analysis along the internal-external gradient (1 and 8
degrees of freedom).
MoUusca
Crustacea
Polychaeta
Echinodermata
Sipunculida
Ascidiacea
Int.
Ext.
1.22
0.52
98.25
0.00
0.00
0.00
3.07
22.84
72.72
0.07
1.27
0.02
Sites
H'
J'
Total ind.
Total spp.
1-2
2-3
3-6
6--7
7-9
9-11
11-13
13-17
12.62'*
n.s.
32.58**
10.49"
n.s.
n.s.
n.s.
n.s.
7.23*
n.s.
6.42*
n.s.
32.75**
6.95*
n.s.
n.s.
n.s.
n.s.
n.s.
n.s.
46.53***
n.s.
n.s.
n.s.
n.s.
n.s.
26.45**
n.s.
339.97***
n.s.
n.s.
7.51"
*p < 0.05; **p < 0.0 !; ***p < 0.001; n.s., not significant.
787
Marine Pollution Bulletin
TABLE 5
One-way ANOVA of values obtained from the various univariate
analysis of the stations closest to the internal effluents(1, 2 and 3) and
closest to the external effluent (13).
d.f.
Sites 1-13
Total spp.
Total ind.
H'
J'
Total spp.
Total ind.
H'
J'
Total spp.
Total ind.
H'
J'
Sites 2-13
Sites 3-13
F
1, 8
1, 8
1, 8
1, 8
1, 8
1, 8
1, 8
1, 8
p
504.131
31.392
95.04
31.549
657.509
2.988
141.057
19.976
786.178
23.198
273.769
73.053
1, 8
1, 8
1, 8
1, 8
<0.0001
< 0.0005
< 0.0001
<0.0005
< 0.0001
n.s.
< 0.0001
<0.01
< 0.0001
<0.01
< 0.0001
< 0.001
TABLE 6
One-way ANOVA of values obtained from the various univariate
analysis applied.
d.f.
Tot. sp.
Tot. ind
H'
8
8
8
J'
8
M.S.
F
1255.95
221035.89
4.7122
79.101'***
9.544****
79.657****
0.1412
10
I
/
7°tl
80+1
100-~
17
11
13"
P
q
External stations
7
]
6
v
3
I
2
*
Internal stations
Fig. 7 Dendrogram of similarities of root-root transformed abundances using the Bray-Curtis index (Asterisks * indicate the
stations closest to the internal and external effluents).
Model for detecting pollution effects on communities
Abundance biomass curves (ABC curves) show a
gradient from the interior to the exterior (Fig. 8).
Stations 1, 2, 3 and 13 are shown to be perturbed.
Stations 6, 7 and 9 moderately perturbed and station 11
shows no perturbation. Values obtained for the SEP
index (Fig. 9) again highlight a similar scenario. As the
sampling was undertaken in June, there is the possibilty
that juvenile settlement may affect the ABC curves
(Warwick and Clarke, 1993). Although the observed
gradient between stations would remain unchanged (as
788
Relationships between biotic and abiotic variables
In order to achieve this the BIOENV programme was
used which contrasts the station similarity matrix
obtained for species abundance data via cluster analysis
to the resulting matrix o f Euclidean distances obtained
following PCA ordination of all the possible combinations of selected environmental variables. This has
allowed us to extract those variables that show greatest
correlations using a Spearman's test. Firstly, an analysis
was undertaken which incorporated only the sediment
variables. The subset of variables that gave the highest
correlation were percentage of sand, phosphates and
depth (0.88) (Table 7a). A further analysis incorporating
the physicochemical water parameters give even higher
correlation values (0.969 and 0.967) for two environmental subsets of percentage of sand, phosphates, depth
and total nitrogen as sediment variables and DO, pH,
nitrites and agitation as water parameters (Table 7b).
8.068****
****/7<.0001.
00 l r
settlement could be considered a constant) there may be
difficulties when comparing results to established ABC
distributions. A temporal extension would be required
to establish to what extent, if any, this is affecting the
results.
Discussion
Following the results obtained a clear gradient of
environmental perturbation can be shown to exist from
the internal stations to the outside of the Saladillo
harbour, primarily correlated to DO, pH, nitrites,
agitation, total nitrogen, phosphates, percentage of
sand and water depth (which may be related to differing
levels of sedimentation between the interior and exterior
of the harbour). All these are indicative of high levels of
organic matter stemming from the aforementioned
effluents and a reduced level of hydrodynamism within
the harbour itself.
On the one hand, high levels of bacterial contamination, particularly faecal coliforms in the internal zones,
indicate high levels of organic enrichment. These results
are supported by those obtained from the chemical
variables, either directly or indirectly related to the
aforementioned microbiological parameters, such as
low values of DO (Theede et al., 1969; Tenore, 1972;
Driscoll, 1975; Thiel, 1978; Pearson and Rosenberg,
1978), high BOD (Frankenberg and Westerfield, 1968;
L6pez-Jamar, 1978; Pearson and Rosenberg, 1978),
high turbidity close to the effluents (Rhoads and Young,
1970) and also variables that show high correlations
with the sampled bacterial flora and high values of
reduced forms of nitrogen (Theede et al., 1969; Tenore,
1972). Also correlated with these variables are high
levels of hydrocarbons (Reish, 1971) and fats in
sediments together with increased values o f organic
material in sediments (Tenore, 1972; Driscoll, 1975;
Pearson, 1975; Reish, 1980; Tenore et al., 1984; L6pezJamar and Cal, 1990). On the other hand, the sheltered
location of the harbour reduces both exposure to wind
Volume 34/Number 10/October 1997
Station 2
Station 1
,~
P
==
--=
100
90
8O
7o
60
50
40
3O
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ABUNDANCE
BIOMASS
I
Fig. 8 Warwick's ABC model applied to each of the stations sampled
(station 17 was omitted due to some biomass values not being
available for some species).
789
M a r i n e P o l l u t i o n Bulletin
3.5
SEP= H' biomass / H'abundance
3
2.5
W 1.5
1
0
1
2
3
6
7
STATION
9
11
13
Fig. 9 Graphical representation of the SEP values for each station.
and waves and may have created conditions of reduced
water renewal within the harbour, favouring sedimentation processes (L6pez-Jamar, 1978; Parker, 1982; Sola
and Ibafiez, 1986). This would have encouraged the
formation of substrata with high levels of fine particles
many of which emanate from the effluents. A different
granulometry is found towards the harbour exit as
greater exposure to wave and wind action increases the
degree of water movement (Carballo et al., 1995;
Conradi and Cervera, 1995), together with a greater
proportion of rocky substrata. Levels of the measured
variables soon return to normal in the exterior stations,
even those close to the exterior effluent particularly
towards the North.
Concerning the substratum, dominance of opportunistic species such as C. capitata in the interior of the
harbour are indicative of environmental perturbations.
The decrease in its abundance towards the exterior
stations reflects the effect of the effluents on the
communities. The proximity of organic effluents, the
results obtained from the different environmental
variables measured in the surrounding sediments, and
the presence of this species within them coincides with
the zone described by Bellan (1967a,b) as a 'polluted'
site. Numerous studies highlight that reproductive
strategy based on lecitrophic and planktotrophic
larvae (McCall, 1977) short life cycles (Grassle and
Grassle, 1974) coupled with various annual cycles of
reproduction (Warren, 1976), higher resistance to low
oxygen levels (Glemarec, 1969; Theede et aL, 1969;
Driscoll, 1975) and high resistance to hydrocarbon
levels (Dauvin, 1982), a detrivorous habit (Fauchald
and Jumars, 1979) and conditions of low interspecific
competition (Warwick, 1986; L6pez-Jamar and Mejuto,
1988) go towards explaining the high level of dominance
of this species.
Stations 6 and 7 show differences when compared to
the more internal stations. The first bivalves appear in
these stations even though there are high levels of
organic materials present which create unfavourable
conditions (Tenore et aL, 1968). Crustaceans are poorly
represented due to their being a taxonomic group which
in general shows a high sensitivity to environmental
790
pollution (Pearson and Rosenberg, 1978; Parker, 1982).
Based on the ABC curves and on the values obtained
for the SEP index, these stations exhibit intermediate
levels of environmental perturbation when compared to
the more polluted internal and effectively normalized
external stations. Similar results were obtained for the
physical and chemical variables together with the
microbiological parameters measured at these sites,
although some of the sediment variables such as organic
material give readings that would classify these sites as
polluted.
Station 9 is located at the mouth of the harbour and
its environmental qualities are consequently improved
as shown by the values of the measured physical,
chemical and microbiological parameters. This is
probably due to increased levels of hydrodynamism.
Moreover, given the increased organic food resource it
receives from the interior of the harbour it may also
undergo 'biostimulation' for some species (Pearson and
Rosenberg, 1978). The presence in this station of species
such as Corbula gibba and Myrthea spinifera, characteristic of muddy habitats (note that percentage of
sand= 98%) although not dominant, may be indicative
of increased levels of organic enrichment (Gray et al.,
1988). This station would be categorized as 'subnormal'
by Bellan and Bourcier (1984). Population parameters
show moderate values, similar to those encountered for
the other external stations, and these similarities are
confirmed by the multivariate analyses performed. The
ABC curves also classify this station as 'moderately
polluted'.
Station 11 appears to be generally regarded by most
methods of analysis as having the best environmental
characteristics of all the stations in the study.
Even though it would initially appear that station
13, which is located next to the external outfall,
should be very similar to its apparent homologues in
the interior of the harbour, this turns out not to be
the case. Environmental parameters all show an
improvement relative to the internal stations, although
a slight deterioration is present when compared to the
external stations. A less optimistic result is obtained
from the ABC curves, and the SEP index wich
highlight the presence of environmental perturbation
at this location.
Although subject to various climatic and physical
factors such as wave action, wind, currents and rain, the
various physical, chemical and microbiological variables
of the water all appear to show a clear gradient of
conditions which can be divided into three zones: the
first would include the innermost (internal) stations, the
second intermediate zone covering the area surrounding
and including the mouth of the harbour, and the final
zone encompassing the external stations. Sediment
quality characteristics also break up the stations into
three broad groups, although the degree of apparent
environmental remediation is decreased; the intermediate sites are still classed as being moderately polluted
Volume 34/Number 10/October 1997
TABLE7
(Best combinationsof variables selectedby the BIOENVprogramme.)
(a) For sediment parameters only;
k
Best combinations of variables (p=)
1 PO43" % SAND HYDROC. WAT.CONT NITROGEN
(.775) (.541)
(.782)
(.517)
(.752)
FATS
.202
ORG.MAT. DEPTH
(.332)
(.667)
2 PO4Z',%SAND DEPTH.,PO43" HYDROC,PO43" HYDROC,DEPTH HYDROC,NITROGEN DEPTH',NITROGEN
(.843)
(.830)
3
4
(.816)
(.807)
PO4~',NITROGEN,DEPTH HIDROC.,NITROG.,PO4="
(.869)
(.843)
PO43",NITROGENO,HYDROC.,DEPTH
PO43",HYDROC.,%
SAND,DEPTH
(.872)
5
6
7
(.806)
(790)
PO~,HYDROC,DEPTH
(.840)
PO~,NITROGENO,MAT.ORG.,DEPTH
(.858)
HYDROC.,PO4Z',NITROGENO,%
SAND,DEPTH
(.846)
(.850)
HIDROC,,PO4~',NITROGENO,ORG.MAT.,DEPTH
(.841)
HYDROC.,PO43",NITROGEN,%SAND,WAT.CONT.,DEPTH
(.833)
HYDROC,
FATS,PO+=', NITROGEN,% SAND, DEPTH
(.827)
HYDROC.,FATS,PO4a-, NITROGEN,%SAND,WAT.CONT., DEPTH
(.814)
8 HYDROC.,FATS,PO43",NITROG.,ORGMAT.,%SAND,WAT.CONT.,DEPTH
(.739)
(b) For all environmental variables measured.
k
1
2
Bestcombinations of variables (p,)
NO="
(.832)
DO
(.808)
DO, NITROG.
(.945)
PO4Z'(s) pH SAND FATS NITROG. DEPTH ORG.MAT. AGIT.
(.775) (.708) (.541) (.202) (.752) (.667) (.332)
(.306)
NO2", NITROG.
(.939)
NOz',PO4Z'(s)
(.901)
pH, NITROG. NO2",Sand NO=',AGIT. DO, NO2"
(.898)
(.883)
NO=', DO,NITROG. NO2-,PO43"(s),NITROG. DO,NITROG,DEPTH NO=-,PO4='(s),S A N D
(957)
(.951)
(.939)
(.937)
(.877)
(.851)
NO=-,DEPTH,AGIT.
(.935)
4 pH,NITROG.,po43-(s),DEPTH pH,NITROG.,DEPTH,AGIT, pH, PO4~(s),SAND, DEPTH
(.958*)
(.954)
(.951)
5
pH, DO,NITROG.,DEPTH,AGIT. DO,NO=',NITROG.,DEPTH,AGIT. pH,DO,NITROG.,SAND,DEPTH
(.960)
(.960)
(.956)
8 DO, NO2,,PO4Z'(s),NITROG.,DEPTH,AGIT. pH,DO,PO4a'(s),NITROG.,DEPTH,AGIT.
(.987)
(.966)
8
pH,DO,NO=', PO43"(w),NITROG.,PO43"(s),DEPTH,AGIT.
(.959)
9
pH,DO,NO=', pO+3"(w),NITROG.,pO,3"(s),SAND, DEPTH,AGIT.
(.953)
10
pH,DO,NO=',PO43"(w),pO43"(s),NITROG.,ORG.MAT.,SAND,DEPHT,AGIT.
(927)
and the external stations only show a generally
moderate environmental improvement. Taking these
together, a generalized internal-external gradient of
conditions is evident determined mainly by physical
factors such as substratum type, hydrodynamism, depth
and by chemical factors related to the organic content
of the surrounding water such as DO and nitrites and
the sediments, for example total nitrogen and phosphate, these being the overriding chemical factors in the
sediment.
Overall, the results of all the analysis help to
distinguish between the effects of the effluents within
791
Marine Pollution Bulletin
an almost enclosed system such as the Saladillo
Harbour and their effects in open coastal waters.
Environmental implications
Poorly treated urban effluents that discharge into
areas with reduced hydrodynamism affect much larger
areas, both with regard to water quality and sediment
parameters (biotic and abiotic) than outfalls that
discharge in hydrodynamically energetic zones, where
their effects are much more rapidly dispersed.
Needless to say, this type of situation should be
avoided wherever possible. Although the ideal solution
would be a total treatment of the effluent before
discharge, a transitional solution may be the channelling
of these effluents to areas of higher water movement
(making maximal use of the breakwaters and other
structures that accentuate these effects) and/or constructing open-water channels under the breakwater
that would allow a greater degree of water movement
and renewal within the harbour itself. It must be borne
in mind, however, that these remedial actions are only
suggestions. It may even be the case that (although
spatially more constrained) a greater impact on the
existing biota in the surrounding area may occur due to
the increased external outfall load. In order to establish
what the possible outcome(s) could be, specific studies
would be required for each proposed option.
We would like to thank D. E. Morfin and D. F. del Castillo for having
undertaken the microbiological analyses, and Dr M. Conradi for her
help in the identification of gammarid species. We would also like to
thank Mr A. Menez for his help regarding EEC legislation, and to the
Autoridad Portuaria de la Bahia de Algeciras by have provided the agitation data and by their contribution, together with CEPSA (Compafiia
Espafiola de Petrrleos, S.A.), Fundacibn Sevillana de Electricidad,
Excmo. Ayuntamiento de los Barrios y Mancomunidad de Municipios
del Campo de Gibraltar, in the financial support of this work.
Austen, M. C., Warwick, R. M. and Rosado, M. C. (1989)
Meiobenthic and macrobenthic community structure along a
putative pollution gradient in southern Portugal. Marine Pollution
Bulletin 20, 398-405.
Autoridad Portuaria de la Bahia de Algeciras (1993) Proyecto de D~trsena de embarcaciones menores en el Saladillo. Autoridad Portuaria
de la Bahia de Algeciras, Algeciras (unpublished).
Bellan, G. (1967a) Pollution et peuplements benthiques de substrat
meuble dans la rrgion de Marseille. I-Le secteur de Cortiou. Revue
Internationale d'Oceanographie Medicale 6/7, 53-87.
Bellan, G. (1967b) Pollution et peuplements benthiques de substrat
meuble dans la rrgion de Marseille. II-L'ensemble portuaire
marsellais. Revue lnternationale d'Oceanographie Medicale 8, 51-95.
Bellan, G. and Bourcier, M. (1984) Bilan 6cologique du d&ournement
permanent d'un petit fleuve crtier dans l'rmissaire d'eaux usres
d'une grande ville. Marine Environmental Research 12, 11-83.
Bilyard, G. R. (1987) The value of benthic infauna in marine pollution
monitoring studies. Marine Pollution Bulletin 18, 581-585.
Bouyoucos, G. J. (1934) The hydrometer method for making
mechanical analysis of soils. Soil Science 38, 335--343.
Bray, J. R. and Curtis, J. T. (1957) An ordination of the upland forest
communities of Southern Wisconsin. Ecological Monographs 27,
325-349.
Buchannan, J. D. and Kain, J. M. (1984) Measurement of the physical
and chemical environment. In Methods for the Study of Marine
792
Benthos, eds N. L. Holme and A. D. Mclntyre, pp. 30-50. Blackwell
Scientific Publications, Oxford.
Carbalto, J. L., Naranjo, S. and Garcia-Gbmez, J. C. (1995) Use of
marine spongies as stress indicators in marine ecosystem at Algeciras
Bay (southern Iberian Peninsula). Marine Ecology Progress Series
135, 109-122.
Clarke, K. R. and Ainsworth, M. (1993) A method of linking
multivariate community structure to environmental variables.
Marine Ecology Progress Series 92, 205-219.
Clarke, K. R. and Warwick, R. M. (1994) Change in Marine
Communities: an Approach to Statistical Analysis and Interpretation,
pp. 144. Natural Environment Research Council, UK.
Conradi, M. and Cervera, J. L. (1995) Variability in trophic
dominance of Amphipod associated with the hidrozoa Bugula
neritina (Linneo, 1758) in Algeciras Bay (Southern Iberia
Peninsula). Polish Archives of Hydrobiology 42(4), 483-494.
Dauvin, J. C. (1982) Impact of the Amoco Cadiz oil spill on the
muddy fine sand Abra alba and Melinna palmata community from
the Bay of Morlaix. Estuarine and Coastal Shelf Science 14, 517531.
Driscoll, E. G. (1975) Sediment-animal-water interaction, Buzzards
Bay, Massachusetts. Journal of Marine Research 33(3), 275-302.
Fauchald, K. and Jumars, P. A. (1979) The diet of worms: a study of
polycbaete feeding guilds. Oceanography and Marine Biology Annual
Review 17, 193-284.
Field, J. G. (1971) A numerical analysis of changes in the soft-bottom
fauna along a transect across False Bay, South Africa. Journal of
Experimental Marine Biology and Ecology 7, 215-253.
Frankenberg, D. and Westerfield, C. W. Jr. (1968) Oxygen demand
and oxygen depletion capacity of sediments from Wassaw Saound,
Georgia. Bulletin of the Georgia Academy of Science 26, 160-172.
Glemarec, M. (1969) Les peuplements benthiques du plateau
continental Nord Gascogne. PhD Thesis, University of Paris.
Grassle, J. F. and Grassle, J. P. (1974) Opportunistic life histories and
genetic systems in marine benthic polychaetes. Journal of Marine
Research 32, 253-284.
Gray, J. S. (198 i) Detecting pollution induced changes in communities
using the log-normal distribution of individuals among species.
Marine Pollution Bulletin 12, 173-176.
Gray, J. S., Aschan, M., Carr, M. R., Clarke, K. R., Green, R. H.,
Pearson, T. H., Rosenberg, R. and Warwick, R. M. (1988) Analysis
of community attributes of the benthic macrofauna of Frierljord/
Langesundljord and in a mesocosm experiment. Marine Ecology
Progress Series 46, 151-165.
Gray, J. S. and Pearson, T. H. (1982) Objective selection of sensitive
species indicative of pollution-induced change in benthic communities. I-Comparative methodology. Marine Ecology Progress Series
9, 111-119.
Ibafiez, F. and Dauvin, J. C. (1988) Long-term changes (1977-1987) in
a muddy fine sand Abra alba-Melinna palmata community from the
Western English Channel: multivariate time-series analysis. Marine
Ecology Progress Series 49, 65-81.
Krfncke, I., Duineveld, G. C. A., Raak, S., Rachor, E. and Daan, R.
(1992) Effects of a former discharge of drill cutting on the
macrofauna community. Marine Ecology Progress Series 91, 277287.
Lambshead, P. J. D., Platt, H. M. and Shaw, K. M. (1983) The
detection of differences among assemblages of marine benthic
species based on an assessment of dominance and diversity. Journal
of Natural History 17, 859-874.
Lrpez-Jamar, E. (1978) Primeros datos sobre la biomasa y la
composicirn del bentos infaunal de la Ria de Pontevedra, en relacirn con el contenido en materia org~mica del sedimento. Boletin de
lnstituto EspaJqol d'Oceanograph6 240(4), 57-65.
Lrpez-Jamar, E. and Cal, R. M. (1990) El sistema bentrnico de la
zona submareal de la ria de Vlgo. Macroinfauna y microbiologia del
sedimento. Boletin de Instituto Espa~qol d'Oceanograph6 6(2), 49-60.
Lrpez-Jamar, E. and Mejuto, J. (1988) Infaunal benthic recolonization after dredging operations in La Corufia Bay, NW Spain.
Cahiers de Biologie Marine 29, 37-49.
McCall, P. L. (1977) Community patterns and adaptative strategies of
the infaunal benthos of Long Island Sound. Journal of Marine
Research 35(2), 221-265.
McManus, J. W. and Pauly, D. (1990) Measuring ecological stress:
variations on a theme by RM Warwick. Marine Biology 106, 305-308.
Volume 34/Number 10/October 1997
Parker, J. G. (1982) Effects of pollutants upon the benthic ecology of
Belfast Lough. Analytical Proceedings, 429-432.
Pearson, T. H. (1975) The benthic ecology of Loeb Linnbe and Loch
Eil, a sea-Itch system on the west coast of Scotland. IV. Changes in
the benthic fauna attributable to organic enrichment. Journal of
Experimental Marine Biology and Ecology 20, 1-41.
Pearson, T. H. and Rosenberg, R. (1976) A comparative study of the
effects on the marine environment of wastes from cellulose
industries in Scotland and Sweden. Ambio 5, 77-79.
Pearson, T. H. and Rosenberg, R. (1978) Macrobenthic succession in
relation to organic enrichment and pollution of the marine
environment. Oceanography and Marine Biology Annual Review
16, 229-311.
Pielou, E. C. (1966) The measurement of diversity in different types of
biological collections. Journal of Theoretical Biology 13, 131-144.
Reish, D. J. (1959) An ecological study of pollution in Los AngelesLong Beach harbors, California. Allan Hancock Foundation
Publication Occasional 22, 119.
Reish, D. J. (1971) Effect of pollution abatement in Los Angeles
Harbours. Marine Pollution Bulletin 2, 71-74.
Reish, D. J. (1980) Effect of domestic wastes on the benthic marine
communities of southern California. Helgoldnder Meeresunterschun.
gen 38, 377-383.
Reish, D. J. (1986) Benthic invertebrates as indicators of marine
pollution: 35 years of study. Proceed IEEE Oceans '86 Conference,
pp. 885-888. Washington.
Rhoads, D. C. and Young, D. K. (1970) The influence of depositfeeding organisms on sediment stability and community trophic
structure. Journal of Marine Research 28, 150-178.
Ritz, D. A., Lewis, M. E. and Shen, M. (1989) Response to organic
enrichment of infaunal macrobenthic communities under salmonid
seacages. Marine Biology 103, 211-214.
Romesburg, C. H. (1984) Cluster Analysis for Researchers. Wadsworth, Belmont.
Shannon, C. E. and Weaver, W. (1963) The Matematical Theory of
Communication, pp. 117. University of Illinois Press, Urbana,
Illinois.
Simboura, N., Zenetos, A., Panayotidis, P. and Makra, A. (1995)
Changes in benthic community structure along an environmental
pollution gradient. Marine Pollution Bulletin 30(7), 470-474.
Sola, J. C. and Ibafiez, M. (1986) Estudio de la fauna de antlidos
poliquetos de los fondos blandos del estuario del Bidasoa. Larralde
Investigaci6n y Espacio 9, 165-181.
Tenore, K. R. (1972) Maerobenthos of the Pamlico River Estuary,
North Carolina. Ecological Monographs 42, 51-69.
Tenore, K. R., Horton, D. B. and Duke, T. W. (1968) Effects of
bottom substrate on the brackish water bivalve Rangia caneata.
Chesapeake Science 9, 238-248.
Tenore, K. R., Cal, R. M., Hanson, R. B., L6pez-Jamar, E., Santiago,
G. and Tietgen, J. H. (1984) Coastal upwelling off the Rias Bajas,
Galicia, Nortwest Spain. II Benthic studies. Rhunion Conseil
Internationale Exploration Met 183, 91-100.
Theede, H., Ponat, A., Hiroki, K. and Sehlieper, C. (1969) Studies on
the resistance of marine bottom invertebrates to oxygen-deficiency
and hydrogen sulphide. Marine Biology 2(4), 325-337.
Thiei, H. (1978) Benthos in upwelling regions. In Upwelling
Ecosystems, eds R. Boje and M. Tomczak, pp. 124-138. Springer,
Berlin.
Warren, L. M. (1976) A population study of the polychaete Capitella
capitata at Plymouth. Marine Biology 180, 209-216.
Warwick, R. M. (1986) A new method for detecting pollution effects
on marine macrobenthic communities. Marine Biology 92, 557-562.
Warwick, R. M. (1993) Environmental impact studies on marine
communities: pragmatical considerations. Australian Journal of
Ecology 18, 63--80.
Warwick, R. M. and Clarke, K. R. (1993) Comparing the severity of
disturbance: a meta-analysis of marine macrobenthic community
data. Marine Ecology Progress Series 92, 221-231.
Warwick, R. M., Pearson, T. H. and Ruswahyuni (1987) Detection of
pollution effects on marine macrobenthos: further evaluation of the
species abundanceflaiomass method. Marine Biology 95, 193-200.
Warwick, R. M., Platt, H. M., Clarke, K. R., Agard, J. and Gobin, J.
(1990) Analysis of macrobenthic and meiobenthic community
structure in relation to pollution and disturbance in Hamilton
Harbour, Bermuda. Journal of Experimental Marine Biology and
Ecology 138, 119-142.
793