You are on page 1of 12

Short-term responses to sewage discharge and storms of subtidal

sand-bottom macrozoobenthic assemblages off Mar del Plata City,


Argentina (SW Atlantic)
R. El as
*
, J.R. Palacios, M.S. Rivero, E.A. Vallarino
Departamento de Ciencias Marinas, Universidad Nacional de Mar del Plata, Dea n Funes 3350, B 7602 AYL, Mar del Plata, Argentina
Received 23 April 2004; accepted 12 August 2004
Available online 25 February 2005
Abstract
This work describes short-term responses of sandy-bottom infaunal macrobenthic communities to environmental
disturbances, such as episodic storms and the intertidal sewage discharge of the Mar del Plata City (388 S, 578 W, Argentina).
Sewage discharge increases by up to 60% every summer due to tourism pressure. Episodic storms affect the area during
autumn-winter and arguably have a cleaning effect on the water and sediment quality. Quantitative data on benthic communities
(based on Van Veen grab samples), water and sediment variables were obtained in November 1999 and March 2000. During
March the sampling was carried out before and after a storm. Parametric and non- parametric tests showed highly significant
differences in both environmental (pH, dissolved oxygen, salinity, temperature, grain size and total organic carbon of sediments)
and biological data (species distribution and abundances, density, species number, diversity and evenness), reflecting changes
that might be related to increasing sewage discharge between November and March, and to storm effects of March. High values
of pH and dissolved oxygen, including a slight stratification in the water column, as well as high values of mean grain size and
total organic carbon were observed in March with the increasing sewage volume. Nevertheless, diversity and evenness showed
low values, but higher density. The ratio crustacean/polychaetes + molluscs also showed low values compared to November
data. Maldanid polychaetes (indicator of low content of organic matter in sediments) dominated in November, but they were
replaced by the polychaete Prionospio spp. (indicator of organic enrichment in subtidal areas) and the tanaidacean
Kalliapseudes schubarti in March. Before the storm event, values of both environmental and biological data returned to
relatively normal conditions, but without reaching the November values, reflecting the disturbance produced by a moderate
northern storm. In spite of an inappropriate replication in time, the present results strongly suggest that these changes were
related to both sewage disturbance and storm effects. These data are in agreement with and explain the pattern observed in
shallow-shelf benthic communities of the SW Atlantic. Implications for environmental management and decision making are
1385-1101/$ - see front matter D 2004 Elsevier B.V. All rights reserved.
doi:10.1016/j.seares.2004.08.001
* Corresponding author.
E-mail address: roelias@mdp.edu.ar (R. El as).
Journal of Sea Research 53 (2005) 231242
www.elsevier.com/locate/seares
discussed, because a pulse disturbance (storms) becomes a press disturbance, keeping the environment healthy in spite of strong
pressure and pulse sewage-disturbances.
D 2004 Elsevier B.V. All rights reserved.
Keywords: Macrozoobenthos resilience; Subtidal sandy bottoms; Sewage and storm disturbance; SW Atlantic; Argentina
1. Introduction
Sewage discharge is the oldest form of marine
pollution (Pearson and Rosenberg, 1978). Most
coastal countries discharge domestic wastes into the
ocean, but there is a current tendency to increase the
length of discharge pipes, in an attempt to keep
plumes away from the shore. Some countries have
also adopted various types of treatment, but ocean
disposal is still considered to be a cost-effective
method for urban wastes due to the dilution effect (but
see Otway et al., 1996). On the other hand, coastal
dynamics, in particular periodical storms, affect
marine benthic communities (Probert, 1984; Sousa,
1984). In gulfs and coasts of North America, period-
ical storms have significant effects on bottom com-
munities to depths of N35 m, affecting the relative
abundance and dominance of benthic fauna and
favouring opportunistic taxa when disturbances occur
at a certain frequency (Posey et al., 1996; Posey and
Alphin, 2002). If a heavy input of organic matter
(such as sewage discharge) exceeds the capacity of
heterotrophic assimilation, storms can partially or
totally clean the bottom, by removing the superficial
layer with organic matter and other pollutants. A
benthic mesocosm experiment has shown that phys-
ical disturbance and organic enrichment of sediments
interact, but it remains to be tested in field conditions
(Widdicombe and Austen, 2001).
Biological indicators have been used to detect
changes related to organic pollution. In particular,
macrobenthic organisms, either the whole community
structure or variables related to particular taxa (such as
polychaetes) are considered powerful tools to assess
environmental quality (Reish, 1987; Warwick, 1993;
Belan, 2003). Assessment of patterns in structure of
marine benthic assemblages has several advantages
over other experimental or field methods for detection
of anthropogenic disturbance. The benthos can
integrate conditions over a period of time rather than
reflecting conditions just at the time of sampling, so
benthic organisms are more useful in assessing local
effects in monitoring programs (UNESCO, 1986).
Few studies are available regarding the effect of
pollution on macrobenthic assemblages in coastal
waters of Argentina (Lo pez Gappa et al., 1990, 1993;
El as, 1992; El as and Bremec, 1994; Vallarino et al.,
2002; El as et al., 2003). Previous data on the relative
abundance of macroinfaunal benthic communities in
subtidal areas of Mar del Plata (388 S, 578 W) showed
that the organic enrichment produced by sewage
discharge affected the shallowest sites and those
closest to the outfall (El as et al., 2001). However,
later quantitative data covering the whole area have
shown that sewage-induced changes in benthos were
present only in patches and without relation to
distance from the effluent (El as et al., 2004).
Mar del Plata City has about 550 000 inhabitants. It
is the most important seaside resort in Argentina,
receiving more than 2 million people during the
summer months (DecemberMarch). Domestic sew-
age is discharged through an untreated intertidal
effluent, with a mean flow of 2.5 m
3
s
-1
, but reaching
4 m
3
s
1
during summer. The City Council of Water
Management (Obras Sanitarias Sociedad de Estado,
OSSE) decided to build a new submarine outflow
facility 3.3 km long with 500 m of diffusers,
discharging at a depth of 11 m. Since 1996, and as
a requirement of the City Council authorities, several
studies have been conducted in the area, including the
first spatial quantitative macroinfaunal benthic survey
(El as et al., 2004). However, a temporal study of the
area was needed to assess differences due to the yearly
variations in fauna and those caused by domestic
wastes. Before the constructional phase, a series of
short-term studies (NovemberMarch) were carried
out in the intertidal areas to test differences due to
increased sewage discharges. Afterwards, the com-
pany supported a program (a Beyond BACI design,
Underwood, 1991, 1992) aimed at monitoring the
R. El as et al. / Journal of Sea Research 53 (2005) 231242 232
two-year construction period and the sewage effect on
the subtidal areas after the new submarine effluent had
become operational. However, no short-term sam-
plings have been carried out again, because of the
operational costs and the economic fault of the
country. The present short-term study is the first to
show results on subtidal sand-bottoms affected by
intertidal sewage discharge and storms. It analyses the
short-term response of macrobenthic infaunal com-
munities off Mar del Plata, before and after the
summer season (November March), testing two
hypotheses: (i) the increase in sewage volumes
produces an acute impact on bottom quality, and
sand-bottom macrobenthic communities show symp-
toms of this stress, and (ii) storms have a cleaning
effect on these shallow subtidal bottoms, causing a
reversal in the impact produced by the sewage
disposal.
2. Material and methods
2.1. Study area
The inner shelf of Mar del Plata City contains
continental shelf waters, with water temperatures
ranging between 8 and 21 8C and salinity between
33.5 and 33.8 psu (Guerrero and Piola, 1997; Lucas et
al., 2000). Tides are semi-diurnal, and waves have
mean heights of 0.91 m (Lanfredi et al., 1992; Isla et
al., 1998). A longshore current flows from south to
north (with a mean velocity of 15 cm s
1
). Seasonal
autumn-winter (mainly in April September) storms
from S-SE affect the region (Manolidis and Alvarez,
1994; Isla and Ferrante, 1997). Sand ridges dominate
to the north of the sewage discharge, while sand
ribbons characterise the southern part. Ridges are
composed of fine sand with coarse material (mainly
shell debris) in the swales, while sand ribbons are fine
sand bodies. Rocky outcrops have been recorded near
the coast (Isla and Schnack, 1986; Isla et al., 1997;
Isla and Aliotta, 1999).
2.2. Methods
In November 1999, 13 stations were sampled, and
randomly re-sampled in March-2000 (Fig. 1) on board
the dARA LuisitoT (National School of Fisheries).
During March, the sampling was carried out before a
moderate storm (with variable winds from NNE
NNW between 2236 km h
1
) named March-1 (9
stations), and after the storm (two weeks later) named
March-2 (8 stations). At each station, four replicated
Van Veen grab samples of 0.05 m
2
were taken for
biological analyses. The sediment was sieved (0.5 mm
mesh) on board, and the retained macrobenthos was
preserved in 10% neutralised formaldehyde. One extra
grab was obtained for analyses of grain size and
organic-matter content. Dry sieving was performed
and a mean size (phi=-log of particle diameter in mm)
was calculated for each station. Total Organic Carbon
(TOC) was calculated after the Walkley and Black
(1965) method. Water quality data (pH, turbidity,
dissolved oxygen, temperature and salinity) were
collected at the surface (1 m depth) and close to the
bottom (1 m above the bottom) with Horiba U-10
equipment.
Variations in water parameters in November (undis-
turbed situation), March-1 and March-2 (before and
after the storm, respectively), and depth were analysed
by a two-way Analysis of Variance (ANOVA). Data of
mean grain size and TOC were compared with one-
way ANOVA. In most cases, variances of environ-
mental (or biological) data proved to be heterogeneous
and could not be stabilised. Nevertheless, analysis of
Fig. 1. Sampling area and location of sampling stations.
R. El as et al. / Journal of Sea Research 53 (2005) 231242 233
variance is considered sufficiently robust to the
departures from the assumption (if the design is
balanced and has many independent estimates of
sample variance, as in this case). Thus, the raw data
were interpreted with the more conservative proba-
bility level of 0.01 (Underwood, 1997). Whenever a
difference between variables and samplings was
established in the ANOVA Student-Newman-Keuls
(SNK) method, multiple comparisons were done at the
appropriate alpha level (p b0.01) to determine differ-
ences between means.
Ordination with non-metric Multi-dimensional
Scaling (MDS) was used to investigate quantitative
data on species abundance and distribution. Biological
and environmental data were analysed without trans-
formation since coding tends to downplay the species
dominance (Clarke and Warwick, 1994). Due to the
high number of samplings, the four replicates from
each station were averaged prior to MDS analysis. A
matrix of similarities between each pair of samples
was calculated using the Bray-Curtis similarity index.
This coefficient was adopted since it was not affected
by joint absence and was considered sufficiently
robust for marine data (Field et al., 1982). The
significance of the groups outlined a priori (Novem-
ber, March-1 and March-2) was tested by the
ANOSIM (dAnalysis of SimilaritiesT) method; the
organisms that contributed most to the differences
observed among groups were found by the SIMPER
(dSimilarity PercentagesT) test. The relationships
between the faunal patterns and the environmental
variables were analysed using the multivariate BIO-
ENV procedure. All these subroutines were performed
using the PRIMER computer program package (Ply-
mouth Marine Laboratory, 1994).
For each sampling, the species number (S), total
abundance (N), the Shannon-Wiener index (H), and
the evenness (J) were calculated using the subroutine
DIVERSE of the PRIMER program. Differences
between sampling dates (considered as treatments)
of these variables were tested using one-way ANOVA.
One-way ANOVA was also performed to analyse
variations in abundance of infaunal organisms dis-
criminated by the SIMPER analysis of the three
samplings dates. After a significant result in the
ANOVA, differences between variables and sam-
plings were analysed by a posteriori SNK test to the
appropriate alpha level (p b0.01). Prior to the
analyses, data from November were tested against
spatial baseline from autumn-winter data (El as et al.,
2004). As differences in main species abundance,
density and species number were not significant,
November was used as a control (undisturbed)
situation. Finally, a Redundancy Analysis (RDA)
was performed to relate environmental and biological
variables as well as sampling sites (a tri-plot),
reducing the dimensionality using the subroutine bi-
plot of the EXCEL worksheet. The analysis is based
on a Singular Value Decomposition of the centred Y*
regressed on columns of the centred X* matrix. Y
contains sites in rows and abundance of species
(transformed as log
10
X+1) in columns, and X
contains site environmental data (not transformed).
Graphical displays of both environmental and bio-
logical data were carried out with raw data.
3. Results
3.1. Water quality
Turbidity was excluded from the analysis because
it had a constant value throughout samplings and
depths (possibly due to a sensor failure). The variables
analysed (Fig. 2) showed highly significant differ-
ences for sampling, depth and interactions (Table 1).
Although the results could not be interpreted directly
(because of the significant interactions), they showed
differences between depth (mainly in March-1
because there was a slight stratification in the water
column) and sampling dates.
3.2. Sediment patterns
Grain-size distribution showed a heterogeneous
pattern during November, with patches of well-sorted
fine sand and poorly sorted coarse sand throughout
the area. In March, fine sand dominated before the
storm (March-1), but the sediment was coarser after
the storm (March-2). This difference was highly
significant (F
2,26
=4.43; pb0.01) only for November
vs March-1, and March-1 vs March-2 (Fig. 3a). Mean
Total Organic Carbon (TOC) also increased between
November and March, whereas it decreased between
March-1 and March-2 (Fig. 3b), showing no signifi-
cant differences (F
2, 26
=3.04; ns).
R. El as et al. / Journal of Sea Research 53 (2005) 231242 234
3.3. Faunal results
In total, 114 species were identified. Crustaceans
had the highest species number (44.95%), and
polychaetes were sub-dominant (38.53%). Poly-
chaetes were numerically dominant (59.26% of the
total fauna), followed by crustaceans (38.36%).
However, dominance differed between sampling
dates: crustacean proportions were higher in Novem-
ber than in March-1 and March-2 (46.2, 36.9 and
34%, respectively). Polychaetes showed higher pro-
portions in March-1 and March-2 (63.8 and 64.3%,
respectively) and were relatively low in November
(47.6%). Molluscs occurred in low proportions in
November (0.6%) and also in March (0.1 before and
0.4% after the storm).
The MDS plot (Fig. 4) showed the sampling sites
segregated along the horizontal axis, with the
November stations on the left, March-1 at the top
and March-2 intermediate. The analysis of similarity
showed a global value of R= 0.372 (999 permuta-
tions) and the highest significance level (pb0.1%).
The Pairwise test (Table 2) showed highly significant
differences in all possible pairs of comparisons. The
BIO-ENV procedure between fauna and environ-
mental variables (pH, dissolved oxygen, temperature,
salinity, phi and total organic carbon) showed better
discrimination among groups (Fig. 5).
Mean Density (Fig. 6a) increased from November
to March, and decreased after the storm; differences
were highly significant (pb0.01). Species number
increased from November to March-1, and also after
the storm (Fig. 6b); differences were highly signifi-
cant (pb0.01). Diversity and evenness (Fig. 6c and d)
showed opposite trends, with values lower in March-1
(after the summer enrichment) and increasing in
March-2 (after the storm). Differences in the Shan-
non-Wiener index and evenness values were highly
significant for all comparisons (pb0.01).
According to the SIMPER analysis (Table 3), six
species contributed most to the differences between
November, March-1 and March-2. Differences in
these species between samplings were tested with
one-way ANOVA, showing highly significant differ-
ences (pb0. 01) in species distribution and abundances
(Table 4, Fig. 7).
p
H
7,6
7,8
8,0
8,2
8,4
8,6
8,8
9,0
November March 1 March 2
Bottom
Surface
D
i
s
s
o
l
v
e
d

o
x
y
g
e
n

(
m
g
*
l
-
1
)
4
5
6
7
8
9
10
11
12
13
November March 1 March 2
S
a
l
i
n
i
t
y

(
u
p
s
)
33,2
33,7
34,2
34,7
35,2
November March 1 March 2
T
e
m
p
e
r
a
t
u
r
e

(

C
)
17
18
19
20
21
22
November March 1 March 2
Fig. 2. Trend in environmental variables (Mean FSD) according to depth (1 m depth and 1 m above the bottom) in samplings of November,
March-1 and March-2.
R. El as et al. / Journal of Sea Research 53 (2005) 231242 235
The post-hoc test demonstrated that Prionospio
spp. showed highly significant differences between all
possible pairs of comparisons, being more abundant in
March-1 (as were Armandia hossfeldti and A. loboi).
The abundance of Kalliapseudes schubarti was highly
different between November and March-1, and
between March-1 and March-2, but not between
November and March-2. Melita sp., as well as
Polygordius lacteus and Sabellidae, were significantly
less abundant in March-2 than in November and
March-1. Maldanidae and Jassa falcata (and also
Amphelisca sp., Dyastilis sp., Amphiura eugeniae and
three unidentified amphipods) showed no differences
between samplings.
The Redundancy Analysis (RDA), performed to
establish a relationship between biotic and abiotic
variables (Fig. 8), showed a very similar pattern to n-
MDS. November samples were located in the negative
values of Axis 1, while March samples were in the
positive values. Axis 1 can be considered to represent
the shift between undisturbed benthic communities
and unbalanced communities dominated by the
polychaete Prionospio spp. and the tanaidacean
Kalliapseudes schubarti. High values of dissolved
oxygen (and high pH, omitted from the representation
Table 1
Summary of all effects in the two-way ANOVA on environmental
water column variables
df Effect MS Effect F p-level
pH
Sampling date 2 4.15 588.81 0.000000**
Depth 1 0.05 8.04 0.006862**
Interaction 2 0.02 3.47 0.039633**
Error 44 0.00
Dissolved oxygen
Sampling date 2 76.39 274.40 0.000000**
Depth 1 8.37 30.07 0.000002**
Interaction 2 13.17 47.32 0.000000**
Error 44 0.27
Temperature
Sampling date 2 37.20 211.27 0.000000**
Depth 1 3.06 17.39 0.000140**
Interaction 2 1.03 5.89 0.005405**
Error 44 0.17
Salinity
Sampling date 2 5.70 209.39 0.000000**
Depth 1 0.98 36.08 0.000000**
Interaction 2 0.39 14.54 0.000014**
Error 44 0.02
Sampling date: November, March-1, March-2; Depth: surface (at 1
m depth), and bottom (1 m below the bottom).
** pb0.01.
T
O
C

(
%
)
0,06
0,12
0,18
November March 1 March 2
p
h
i

u
n
i
t
s
1,4
2,2
3,0
3,8
(a)
(b)
Fig. 3. Mean (FSD) of (a) phi units, and (b) Total Organic Carbon
(%) of sandy sediments in the three samplings performed in a
subtidal area exposed to sewage discharge.
November March 1 March 2
Stress: 0,11
Fig. 4. Non-metric Multi-dimensional Scaling for the samples of
November, March-1, and March-2 of subtidal sand-bottom macro-
benthos of a shallow shelf area in the SW Atlantic affected by an
intertidal sewage discharge.
Table 2
Pairwise tests
Groups Statistic
value
Significance
level
Permutations
used
Permutations
actual
November
March-1
0.475 0.1 293930 999
November
March-2
0.361 0.2 125970 999
March-1
March-2
0.265 0.8 24310 999
R. El as et al. / Journal of Sea Research 53 (2005) 231242 236
due to the strong correlation between them) were
related to normal conditions prevailing in November.
Salinity (with high TOC and temperature values, not
shown) showed the opposite trend, associated with
March-1 conditions, as well as finer mean grain size
values, representing the high loading of fine organic
and inorganic particles from the increased sewage
volume. March-2 data represented the return to the
previous situation, but with intermediate values.
Along Axis 2, March-1 and March-2 samplings were
different, representing the conditions before and after
the storm event. Axis 1 explained 66.04% of the
variance, and Axis 2 the remaining 31.46%.
4. Discussion
The observed temporal variation in water data had a
seasonal component (end of spring end of summer in
the Southern Hemisphere), but was also affected by
changes in water quality. Relatively high values of pH
and dissolved oxygen were measured in November,
but decreased in March-1 (more evident in dissolved
oxygen at the bottom). Water oxygen deficiency was
detected as the main ecological factor causing severe
stress to the macrofauna (Sainz Salinas, 1997; Gonza-
lez-Oreja and Sainz Salinas, 1999; UNESCO, 2000).
November March 1 March 2
Stress: 0,01
Fig. 5. MDS plot of environmental variables (Euclidean distance).
Maximum correlation was obtained with two variables, Dissolved
Oxygen (DO) and phi (0.993), but correlation was perfect (1.00)
considering pH, DO, temperature, salinity and phi, or DO, temper-
ature, salinity, phi and TOC.
S
p
e
c
i
e
s

N
u
m
b
e
r

(
S
)
20
25
30
35
40
45
50
55
60
November March 1 March 2
S
h
a
n
n
o
n

i
n
d
e
x

(
H
'
)
1,0
1,4
1,8
2,2
2,6
3,0
3,4
3,8
November March 1 March 2
E
v
e
n
n
e
s
s

(
J
'
)

0,25
0,35
0,45
0,55
0,65
0,75
0,85
November March 1 March 2
D
e
n
s
i
t
y

(
i
n
d
*
m
-
2
)
0
10000
20000
30000
40000
50000
November March 1 March 2
(a) (b)
(c) (d)
Fig. 6. Means (FSD) of (a) density of total infauna, (b) species number, (c) diversity (Shannon index), and (d) evenness in the three samplings
in an area exposed to sewage discharge.
R. El as et al. / Journal of Sea Research 53 (2005) 231242 237
After the storm, pH and dissolved oxygen increased,
but both values were lower than in November. In
March-1 (before the storm), a slight stratification of the
water column was recorded, which was reflected by
both salinity and temperature values. Water stratifica-
tion patterns have previously been recorded for the
area, but only in water deeper than 50 m, and only
during summer (Isla and Ferrante, 1997; Guerrero and
Piola, 1997; Lucas et al., 2000). The present paper is
the first to show a slight stratification in local shallow
waters, at least during summer; the stratification
disappeared before the storm.
The community structure also showed the shift from
a non-disturbed benthic community to a post-impact
situation. Although these changes could be due to
several interacting factors (including unknown season-
ality of faunas and environmental factors that could
work simultaneously), the evidence suggests that they
were related to sewage and storm effects. Diversity and
evenness were relatively high in November (when
sewage flowwas 2.5 m
3
s
-1
), but lowin March-1 (when
sewage flow was 4 m
3
s
-1
), in response to high
dominance. Faunal density showed the opposite
situation (increasing from 5000 to 35 000 ind m
-2
).
Although the SAB models (Pearson and Rosenberg,
1978) cannot be applied to open shores (Maurer et al.,
1993), a rapid response of dopportunistic speciesT (in
terms of organic enrichment, as suggested by Pearson
and Rosenberg, 1978) seems to take place when large
amounts of organic matter are available. Mean total
organic carbon increased from November to March
(0.11 to 0.13%) and decreased slightly after the storm
(0.12%), but these differences were not significant.
Organic carbon content in shallow shelf sediments is
usually low (underestimated by the titration method,
Leong and Tanner, 1999), ranging from 0.12 to 0.48%
(Isla and Ferrante, 1997), with the greatest value
recorded 900 m from the effluent (El as et al., 2001).
Values observed in the present study are slightly lower,
but correspond to a slightly more seaward area.
It is clear that changes in grain size on the sea bottom
were due to the increasing input of both organic and
inorganic fine particles in March-1 after the increase of
sewage discharge (see Fig. 3a). The storm effect was
also evident in March-2, when there was a change in the
grain size after the storm (although differences were
only significant between November March-1).
The March-2 situation (after the storm) was a return
to relatively normal values in the benthic community.
During March-1, mean density of infaunal organisms
reached their maximum value (up to 35 000 ind m
2
),
but decreased in March-2 (15 000 ind m
2
). Variability
Table 3
Percentage of similarities (SIMPER)
Species November March-1
av.abund av.abund av. diss diss/sd cum %
Average dissimilarity=89.72
Prionospio spp. 6.3 389.9 47.5 2.1 52.9
K. schubarti 12.5 118.8 13.1 1.4 67.5
Jassa falcata 1.7 40.3 5.1 0.3 73.2
Maldanidae 28.7 10.6 4.7 0.4 78.5
November March-2
Average dissimilarity=86.90
Prionospio spp. 6.3 159.4 29.4 1.14 33.8
Jassa falcata 1.7 47.1 10.8 0.6 46.3
Polygordius 1.9 12.6 6.4 0.4 53.6
Maldanidae 28.7 12.2 6.2 0.4 60.8
Melita sp. 15.6 6.1 3.8 0.7 65.2
March-1 March-2
Average dissimilarity=67.54
Prionospio spp. 389.9 159.4 30.5 1.5 45.2
K. schubarti 118.8 11.5 10.8 1.4 61.2
Jassa falcata 40.3 47.1 7.7 0.7 72.6
Average abundance between each pair of samplings, average
dissimilarity and standard deviation, and cumulative percentage
for each species.
Table 4
Analysis of Variance (one-way ANOVA) considering the three
samplings (November, March-1 and March-2) and the 6 species
discriminated as important in differences among samplings outlined
by the SIMPER analysis
df Effect MS effect F p-level
Kalliapseudes schubarti 2 47790776 33.66 0.000000**
Error 97 1419794
Prionospio spp. 2 517464416 46.52 0.000000**
Error 97 11121920
Maldanidae 2 1316388 0.51 0.602154ns
Error 97 2581642
Polygordius lacteus 2 353504 3.34 0.039300**
Error 97 105619
Melita sp. 2 380163 3.56 0.032037**
Error 97 106612
Jassa falcata 2 8108155 2.04 0.135058ns
Error 97 3966912
** pb0.01.
R. El as et al. / Journal of Sea Research 53 (2005) 231242 238
Prionospio spp.
D
e
n
s
i
t
y

(
i
n
d
*
m
-
2
)
0
6000
12000
18000
Kalliapseudes schubartii
D
e
n
s
i
t
y

(
i
n
d
*
m
-
2
)
0
1500
3000
4500
Maldanidae
D
e
n
s
i
t
y

(
i
n
d
*
m
-
2
)
D
e
n
s
i
t
y

(
i
n
d
*
m
-
2
)
D
e
n
s
i
t
y

(
i
n
d
*
m
-
2
)
D
e
n
s
i
t
y

(
i
n
d
*
m
-
2
)
0
200
400
600
800
November March 1 March 2
Melita sp.
0
200
400
600
800
1000
Polygordius lacteus
0
10
20
30
40
50
Jassa falcata
0
1000
2000
3000
November March 1 March 2
Fig. 7. Densities (FSD) on three sampling occasions of main species in subtidal sand-bottoms exposed to an intertidal sewage discharge.
Kalliapseudes
Prionospio spp.
Spionidae
Maldanidae
Polygordius
Melita sp.
Jassa falcata
D.Oxygen
Salinity
phi
50 N
51 N
52 N
53 N
54 N
55 N
56 N
57 N
58 N
59 N
60 N
61 N
50 M1
51 M1
52 M1
53 M1
54 M1
55 M1
56 M1
57 M1
58 M1
50 M2
55 M2
57 M2
58 M2
59 M2
60 M2 61 M2
62 M2
-1,5
-1
-0,5
0
0,5
1
1,5
-1,5
-1 -0,5 0 0,5
1
1,5
2
2,5
Fig. 8. Redundancy analysis showing the plot of sites (stations) in November (N), March-1 (M1) and March-2 (M2), with main environmental
variables and macrobenthic species (abundances transformed as Log
10
X+1) in a subtidal sand bottom exposed to intertidal sewage discharge in
the SW Atlantic.
R. El as et al. / Journal of Sea Research 53 (2005) 231242 239
was greater in March-1 in response to the sewage
disturbance, and intermediate in March-2 after the
storm disturbance (see Figs. 5 and 6). Increasing
variability is common in locally disturbed environ-
ments (Warwick and Clarke, 1993; Chapman et al.,
1995). In the present study, high variability was found
in response to both organic matter enrichment and
storm disturbance.
Increasing values of diversity and evenness also
reflected the response to dnormalT conditions by
lowering dominance after the storm. In November,
unidentified species of Maldanidae and Spionidae,
including Melita sp., were dominant. Conveyor-belt
feeding bamboo worms, maldanid polychaetes, often
indicate low organic content in sediments (Gallagher
and Keay, 1998). In the present study, these species
almost disappeared in March-1, when they were
replaced by Kalliapseudes schubarti, and the indica-
tor of organic enrichment in subtidal areas Prionospio
spp. (Levin, 2000). The dominance of these species
decreased after the storm, reflecting an abrupt change
in the bottom quality. In contrast, the crustaceans
Jassa falcata, Dyastilis sp. and other amphipods
showed an increasing dominance after the storm. This
can be due to the higher mobility of crustaceans and
their capacity to change faster after environmental
disturbance. Another potential indicator of benthic
stress is the ratio between the percentage of crusta-
ceans and polychaetes + molluscs (UNESCO, 2000),
which also showed a normal condition in November
(0.96) and a low value (0.56) in March-1, when
sewage increased up to 60%. After the storm, this
ratio remained low (0.53), possibly as a post-impact
response.
In 1999, an unidentified species of the polychaete
genus Caulleriella (Cirratulidae) dominated at some
stations (up to 90%), and was considered to be an
indicator of organic enrichment (El as et al., 2004).
However, in the present study, this species was only
present in low density (3%) during November and
disappeared in March. In the same way, Owenia
fusiformis was dominant near the sewage discharge
in 1996 (El as et al., 2001), but was almost absent in
the present study. This confirmed the great variability
of benthic associations in the shallow shelf which
several authors have assumed to be a consequence of
high-energy conditions (Olivier et al., 1968; Roux et
al., 1993; Bremec and Roux, 1997; El as et al., 2001).
Storms in the inner shelf also affect the beaches.
Mean breaker height (usually 0.6 0.8 m) can reach 1.2
m during storms (Isla and Aliotta, 1999), but in a
similar situation waves can reach 2.3 m offshore (at 11
m depth; see Lanfredi et al., 1992). Manolidis and
Alvarez (1994) state that the stormperiods extend from
April to September, while moderate storms can occur
the year round, including the summer season. As
pointed out by Underwood (1992) it is difficult in some
cases to distinguish between dpulseT (short-term) and
dpressT (continuous) disturbances (Bender et al., 1984).
In this inner shelf of the SWAtlantic, the frequency of
pulse disturbance due to storms becomes a press
disturbance, affecting both sediment quality and
benthic assemblage stability by removing the surface
sediment layer (decreasing both organic matter and
heavy-metals content), and forcing benthic commun-
ities to start re-colonisation processes. Flocks fromMar
del Platas sewage could be observed up to 5 km
offshore (Isla et al., 1998), but bottom sediments
remained relatively healthy. Heavy metals in sediments
showed low values (Scagliola, 1993). Small-sized
organisms are common in organically enriched envi-
ronments (Pearson and Rosenberg, 1978; Oyarzu n et
al., 1987; Beukema, 1988). Nevertheless, shallow shelf
communities of the SW Atlantic respond to sediment
disturbances rather than to organic enrichment (El as et
al., 2001, 2004). The present study agrees with this
statement. Moreover, the observed changes were
related to a moderate storm from the north, while most
storms come from the southeast (dsudestadasT), and are
generally stronger and last longer. Although the data
set here presented had an inadequate replication of
sampling over time, the results strongly suggest that the
observed changes are related to both sewage-disturb-
ance and storm effects.
Benthic responses to dredging disturbances have
been reported to last as long as four years around
England and Wales, but relatively rapid recovery

in
two to three years has occurred in European coastal
gravel areas (Boyd et al., 2003). However, high-energy
storm events have been shown to affect directly both
the geological and biological characteristics in the
short-term (Posey et al., 1996; Renaud et al., 1997;
Posey and Alphin, 2002, and references therein). As
the literature suggests, subtidal macrobenthic com-
munities in the SWAtlantic show short-term responses
to both sewage discharges and storm disturbances. The
R. El as et al. / Journal of Sea Research 53 (2005) 231242 240
present paper is the first discussion of a possible effect
of both pulse disturbances caused by storms and the
seasonal increase of sewage discharge on benthic
communities along the SW Atlantic coast. The con-
sequences are important for managers and decision
makers, because bottom quality remains relatively
healthy due to these periodical storms, in spite of the
continuous seasonal peaks of organic-matter load.
Acknowledgements
The INTA soil laboratory performed organic matter
analyses. Lic. Rau l Guerrero (INIDEP) supplied
information about mass waters of the Southwestern
Atlantic. Dr. Paulo Lana (Universidade Federal do
Parana, Brazil) and J. M. dLoboT Orensanz (Centro
Nacional Patago nico) improved the original manu-
script. Dr. F. Isla (Centro de Geolog a de Costas y el
Cuaternario, CGCyC) revised the English and made
suggestions that improved the manuscript. Four anon-
ymous reviewers provided comments that helped to
clarify the manuscript. Susana Serra performed the
grain size analyses (CGCyC). Nilda Manolidis pro-
vided data about winds and storms. This study is part of
the evaluation carried out by Obras Sanitarias Sociedad
de Estado (OSSE) of the Mar del Plata City Hall in the
environment, in order to measure baseline data for an
ongoing monitoring program supported by the authors.
References
Bender, E.A., Case, T.J., Gilpin, M.E., 1984. Perturbation
experiments in community ecology: theory and practice.
Ecology 65, 113.
Belan, T.A., 2003. Benthos abundance pattern and species
composition in conditions of pollution in Amursky Bay (the
Peter the Great Bay, the Sea of Japan). Mar. Pollut. Bull. 46,
11111119.
Beukema, J.J., 1988. An evaluation of the ABC-method (abundance/
biomass comparison) as applied to macrobenthic communities
living on tidal flats in the Dutch Wadden Sea. Mar. Biol. 99,
425433.
Boyd, S.E., Limpenny, D.S., Rees, H.L., Cooper, K.M., Campbell,
S., 2003. Preliminary observations of the effects of dredging
intensity on the re-colonization of dredged sediments off the
southeast coast of England (Area 222). Estuar. Coast. Shelf Sci.
56, 115.
Bremec, C.S., Roux, A., 1997. Resultados del analisis de una
campan a de investigacio n pesquera sobre comunidades
bento nicas asociadas a bancos de mejillo n (Mytilus edulis
platensis DOrb.) en costas de Buenos Aires. Argentina. Rev.
Invest. Des. Pesq. 11, 153166.
Chapman, M.G., Underwood, A.J., Skilleter, G.A., 1995. Variability
at different spatial scales between a subtidal assemblage exposed
to the discharge of sewage and two control assemblages. J. Exp.
Mar. Biol. Ecol. 189, 103122.
Clarke, K.R., Warwick, R.M., 1994. Similarity-based testing for
community pattern: the two-way layout with no replication.
Mar. Biol. 118, 167176.
El as, R., 1992. Quantitative benthic structure in Blanca Bay and
their relationship with organic enrichment. P.S.Z.N. Mar. Ecol.
13, 189201.
El as, R., Bremec, C.S., 1994. Biomonitoring of water quality using
benthic communities in Blanca Bay (Argentina). Sci. Tot.
Environ. 158, 4549.
El as, R., Bremec, C.S., Vallarino, E.A., 2001. Polychaetes
assemblages in a southern shallow shelf affected by sewage
discharge. Rev. Chil. Hist. Nat. 74, 523531.
El as, R., Rivero, M.S., Vallarino, E.A., 2003. Sewage impact on the
composition and distribution of Polychaeta associated to
intertidal mussel beds of the Mar del Plata rocky shore.
Argentina. Iheringia, Ser. Zool. 93, 309318.
El as, R., Vallarino, E.A., Scagliola, M., Isla, F.I., 2004.
Macrobenthic distribution patterns at a sewage disposal site
in the inner shelf off Mar del Plata (SW Atlantic). J. Coast.
Res. 20 (3) (in press).
Field, J.G., Clarke, K.R., Warwick, R.M., 1982. A practical strategy
for analyzing multispecies distribution patterns. Mar. Ecol. Prog.
Ser. 8, 3752.
Gallagher, E.D., Keay, K.E., 1998. Organism-sediment-contaminant
interactions in Boston Harbor. In: Stolzenbach, K.D., Adams,
E.E. (Eds.), Contaminated Sediments in Boston Harbor. MIT
Sea Grant Publication 98-1, Boston, pp. 89132.
Guerrero, R.A., Piola, A.R., 1997. Masas de agua en la plataforma
continental. In: Boschi, E.E. (Ed.), El Mar y sus Recursos
Pesqueros. Instituto Nacional de Investigacio n y Desarrollo
Pesquero (INIDEP), Mar del Plata, pp. 107118.
Gonzales-Oreja, J.A., Sainz Salinas, J.I., 1999. Fitting response
models of benthic community structure to abiotic variables in a
pollued estuarine system. Acta Oecol. 20, 471477.
Isla, F.I., Schnack, E.J., 1986. Gradacio n bribbonsQ/dorsales de
arena en la plataforma costera entre Mar Chiquita y Mar del
Plata. Extended Abstracts from 1
a
Reunio n Argentina de
Sedimentolog a, La Plata, 4548.
Isla, F.I., Ferrante, A., 1997. Corrientes. In: Isla, F.I. (Ed.), Estudio
del Sector de Plataforma Receptor de la Descarga Cloacal de
Camet, Mar del Plata. Unpublished report to Obras Sanitarias
Sociedad del Estado (OSSE), Facultad de Ciencias Exactas y
Naturales (UNMdP), Mar del Plata, pp. 83116.
Isla, F.I., Aliotta, S., 1999. Storm Dispersal of Volcanogenic Sands
fromBuenos Aires, where heavy-metal concentrations are heavy-
mineral segregations. Mar. Geores. Geotech. 17, 357370.
Isla, F.I., Serra, S., Farenga, M., 1997. Sedimentos del Fondo. In:
Isla, F.I. (Ed.), Estudio del Sector de Plataforma Receptor de la
Descarga Cloacal de Camet, Mar del Plata. Unpublished
Report to Obras Sanitarias Sociedad del Estado (OSSE),
R. El as et al. / Journal of Sea Research 53 (2005) 231242 241
Facultad de Ciencias Exactas y Naturales (UNMdP), Mar del
Plata, pp. 7077.
Isla, F.I., Perez Guzzi, J., Zamora, A., Folabella, A., 1998. Aportes
de coliformes a la costa de Mar del Plata (Argentina) por v as
naturales e inducidas. Thalassas 14, 6370.
Lanfredi, N.W., Pousa, J.L., Mazio, C.A., Dragani, W.C., 1992.
Wave-power potential along the coast of the Province of Buenos
Aires, Argentina. Energy 17, 9971006.
Levin, L.A., 2000. Polychaetes as environmental indicators:
response to low oxygen and organic enrichment. Abstract from
the 6th International Polychaete Conference, 317 August 1998,
Curitiba, Brasil. Bull. Mar. Sci., vol. 67, pp. 668.
Leong, L.E., Tanner, P.A., 1999. Comparison of methods for
determination of organic carbon in marine sediments. Mar.
Pollut. Bull. 38, 875879.
Lo pez Gappa, J.J., Tablado, A., Magaldi, N.H., 1990. Influence of
sewage pollution on a rocky intertidal community dominated by
the mytilid Brachydontes rodriguezi. Mar. Ecol. Prog. Ser. 63,
63175.
Lo pez Gappa, J.J., Tablado, A., Magaldi, N.H., 1993. Seasonal
changes in an intertidal community affected by sewage
pollution. Environ. Pollut. 82, 157165.
Lucas, A., Guerrero, R., Mianzan, H.W., Acha, M.E., Lasta, C.,
2000. On the coastal oceanographic regimes of northern
Argentine continental shelf. Abstracts of the IVs Jornadas de
Ciencias del Mar, Puerto Madryn, 84. September.
Manolidis, N., Alvarez, J.A., 1994. Grandes tormentas en la zona
costera marplatense entre 19801992. Centro Oceanografico
Buenos Aires, Serie Ciencia y Tecnica 5, 133.
Maurer, D., Robertson, G., Gerlinger, T., 1993. San Pedro shelf
California: testing the Pearson-Rosenberg model (PRM). Mar.
Environ. Res. 35, 303321.
Olivier, S.R., Bastida, R., Torti, M.R., 1968. Resultados de las
campan as oceanograficas Mar del Plata I-V. Contribucio n al
trazado de una carta biono mica del area de Mar del Plata. Las
asociaciones del sistema litoral entre 12 y 70 m de profundidad.
Bol. Inst. Biol. Mar. 16, 185.
Otway, N.M., Gray, C.A., Craig, J.R., Mcvea, T.A., Ling, J.E.,
1996. Assessing the impacts of deepwater sewage outfalls on
spatially- and temporally-variable marine communities. Mar.
Environ. Res. 41, 4571.
Oyarzu n, C., Carrasco, F.D., Gallardo, V.A., 1987. Some character-
istics of the macrobenthic fauna from the organic-enriched
sediments at Talcahuano. Chile. Cahiers Biol. Mar. 28, 429446.
Pearson, T.H., Rosenberg, R., 1978. Macrobenthic succession in
relation to organic enrichment and pollution of the marine
environment. Oceanogr. Mar. Biol. Ann. Rev. 16, 229311.
Plymouth Marine Laboratory, 1994. Primer Plymouth Routines in
Multivariate Ecological Research. Plymouth U.K. Version
prepared for training workshop at Laboratorio Costero San
Jose, Callao, Peru , April 1997, 151.
Posey, M., Alphin, T., 2002. Resilience and stability in an offshore
benthic community: response to sediment borrow activities and
hurricane disturbance. J. Coast. Res. 18, 685697.
Posey, M., Lindberg, W., Alphin, T., Vose, F., 1996. Influence of
storm disturbance on an offshore benthic community. Bull. Mar.
Sci. 59, 523529.
Probert, P.K., 1984. Disturbance, sediment stability, and trophic
structure of soft-bottom communities. J. Mar. Res. 42, 893921.
Reish, D.J., 1987. The use of benthic communities in marine
environmental assessment. In: Malagrino, G., Santoyo, H.
(Eds.), Mem. V Simp. Biol.. Mar. Univ. Auton. Baja Calif.
Sur, La Paz, Mexico, pp. 123126.
Renaud, P.E., Riggs, S.R., Ambrose Jr., W.G., Snyder, S.W.,
1997. Biological-geological interactions: storm effects on
macroalgal communities mediated by sediment characteristics
and distribution. Cont. Shelf Res. 17, 3756.
Roux, A., Bastida, R., Bremec, C.S., 1993. Comunidades bento nicas
de la plataforma continental Argentina. Campan as Transeccio n
BIP bOca BaldaQ 1987/88/89. Bolm. Inst. Oceanogr. Sao Paulo
41, 8194.
Sainz Salinas, J.I., 1997. Evaluation of adverse biological effects
induced by pollution in the Bilbao Estuary (Spain). Environ.
Pollut. 96, 351359.
Scagliola, M.O., 1993. Metales pesados en sedimentos, material
particulado y organismos bento nicos del medio marino receptor
del efluente cloacal de Mar del Plata. Unpublished Thesis,
Facultad de Ciencias Exactas y Naturales. Univ. Nac. Mar del
Plata, 129.
Sousa, W.P., 1984. The role of disturbance in natural communities.
Ann. Rev. Ecol. Syst. 15, 353391.
UNECSO, 1986. IOC Workshop on the biological effects of
pollutants. Workshop Report No. 53. Oslo, Norway. 48 pp. + app.
UNESCO, 2000. Ad hoc Benthic Indicator Group Results of
initial planning meeting. IOC Technical Series No. 57, Paris,
France. 74 pp.
Underwood, A.J., 1991. Beyond BACI: experimental designs for
detecting human environmental impacts on temporal variations
in natural populations. Aust. J. Mar. Freshw. Res. 42, 569587.
Underwood, A.J., 1992. Beyond BACI: the detection of environ-
mental impacts on populations in the real, but variable world. J.
Exp. Mar. Biol. Ecol. 161, 145178.
Underwood, A.J., 1997. Experiments in Ecology: Their Logical
Design and Interpretation Using Analysis of Variances. Cam-
bridge University Press, Cambridge. 504 pp.
Vallarino, E.A., Rivero, M.S., Gravina, M.C., El as, R., 2002. The
community-level response to sewage impact in intertidal mussel
beds of the Southwestern Atlantic, and the use of the Shannon
index to assess pollution. Rev. Biol. Mar. Oceanogr. 37, 2533.
Warwick, R.M., 1993. Environmental impact studies on marine
communities: pragmatical considerations. Aust. J. Ecol. 18,
6380.
Warwick, R.M., Clarke, K.R., 1993. Increased variability as a
symptom of stress in marine communities. J. Exp. Mar. Biol.
Ecol. 172, 215226.
Walkley, A., Black, A., 1965. Organic carbon. In: Black, A., Evans,
J. (Eds.), Methods of Soil Analysis. Am. Soc. Agron., Madison,
USA, p. 219.
Widdicombe, S., Austen, M.C., 2001. The interaction between
physical disturbance and organic enrichment: an important
element in structuring benthic communities. Limnol. Oceanogr.
46, 17201733.
R. El as et al. / Journal of Sea Research 53 (2005) 231242 242