Caracterização Ambiental

Marine Pollution Bulletin 60 (2010) 536553
Contents lists available at ScienceDirect
Marine Pollution Bulletin

journal homepage: www.elsevier.com/locate/marpolbul
Analysis of foraminifera assemblages and sediment geochemical properties

to characterise the environment near Ara and Saco da Capela domestic
sewage submarine outfalls of So Sebastio Channel, So Paulo State, Brazil
A.C. Teodoro a,*, W. Duleba a, S. Gubitoso a, S.M. Prada b, C.C. Lamparelli c, J.E. Bevilacqua c
a
b
c
Institute of Geoscience, University of So Paulo, Rua do Lago, 562, So Paulo State, Brazil
Unieo, Av. Franz Voegeli, 1743, Osasco, So Paulo State, Brazil
Cetesb Companhia de Tecnologia de Saneamento Ambiental, Av. Prof. Frederico Hermann Jr., 345, So Paulo State, Brazil
a r t i c l e
i n f o
Keywords:
So Sebastio Channel
Benthic foraminifera
Submarine outfalls
Domestic sewage
Geochemical
a b s t r a c t
Supercial bottom samples were collected near diffusers of domestic sewage submarine outfalls at Ara
and Saco da Capela, So Sebastio Channel, Brazil. The goal of this study was to investigate the distribution and composition of live benthic foraminifera assemblages and integrate the results obtained with
geochemical analyses to assess human-induced changes. According to the results obtained no environmental stress was observed near the Saco da Capela submarine outfall diffusers. The foraminifera assemblage is characterised by species typical of highly hydrodynamic environments, with well-oxygenated
bottom waters and low nutrient contents. In contrast, near Ara submarine outfall, organic enrichment
was denoted by high phosphorus, sulphur and, to a lesser extent, total organic carbon content. Harmful
inuences on foraminifera could be identied by low richness and specic diversity, as well as the predominance of detritivore feeder species, which are associated with higher organic matter ux and low
oxygen in the interstitial pore water.
2009 Elsevier Ltd. All rights reserved.
1. Introduction
Due to exponential urban growth in coastal zones, domestic
sewage has become one of the main causes of pollution in marine
environments. Input of sewage to the environment can occur indirectly, either by means of river systems or from point sources, such
as submarine outfalls (Lamparelli, 2007).
When associated with secondary and tertiary treatments,
domestic sewage submarine outfalls represent safe removal of
contaminants in coastal regions (Werme and Hunt, 2004). However, when the sewage receives only a pre-conditioning treatment,
a large amount of organic and inorganic compounds are deposited
on the oceans bottom sediment, changing the region under direct
inuence of the disposal in source of contamination.
Discharges of sewage to natural waterways can result in a range
environmental impacts including: (i) poor recreational water quality due mainly to pathogen loading, (ii) eutrophication due to
nutrient loading, (iii) toxicity to humans and ecosystems due to a
range of chemicals in sewage and (iv) accumulation of contaminants in organisms and sediments due to chemicals in sewage
(Scanes, 2007).
* Corresponding author. Tel.: +55 11 30911988.

E-mail addresses: andreia.teodoro@usp.br (A.C. Teodoro), wduleba@usp.br
(W. Duleba).
0025-326X/$ - see front matter 2009 Elsevier Ltd. All rights reserved.
doi:10.1016/j.marpolbul.2009.11.011
These harmful effects on the environment may occur immediately or gradually. Therefore, it becomes important to assess not only
water and sediment quality, but also their impact on living beings.
Among all the benthic microfauna, foraminifera are one of the
most abundant protists in marine environments (Murray, 1991).
Due to their high sensitivity to rapid physicochemical variation
in the environment, short life cycles and high biodiversity, foraminifera have been increasingly used to assess anthropogenic pollution. The responses in foraminifera can include local extinctions,
resulting in a barren zone where polluted levels are high (Alve,
1995), as well as assemblage modications with increased density
and low diversity (Yanko et al., 1994; Alve, 1995; Cearreta et al.,
2002; McGann et al., 2003; Frontalini and Coccioni, 2008).
The goal of this study was to investigate the distribution and
composition of live benthic foraminifera assemblages and to integrate the results obtained with geochemical analyses to assess
environmental changes near diffusers of domestic sewage submarine outfalls at Ara and Saco da Capela, both located in the So
Sebastio Channel, So Paulo State, Brazil.
2. Study area
The So Sebastio Channel (SSC; Fig. 1) is located in the northern coast of So Paulo State, Brazil (23410 2353.50 S; 45190
45300 W).
A.C. Teodoro et al. / Marine Pollution Bulletin 60 (2010) 536553
537
Fig. 1. Studies area and sampling grid.
The SSC is about 25 km long with two large entrances, 67 km

wide in the southern and northern portions, respectively. The
water depths are 2025 m at the entrances, and up to 40 m deep
in the central region.
The channel outline, more specically its lateral curvature,
resembles a river channel with depositional (mainland) and erosional (island) sides.
The circulation inside the channel is characterised by water
movements to the north and south, with the direction alternating
within the days (Miranda and Castro Filho, 1995). There appears to
be no direct relationship with tidal currents; rather, the direction
of circulation seems to be related to changes in wind patterns.
The wind-driven surface circulation is intense, with average currents between 0.7 and 1.0 m s1, SW to NE (Furtado et al., 2008).
The thermohaline patterns of the channel are controlled by
movement of water masses from the continental shelf, generated
mostly by wind and pressure gradient forces.
The main water masses in the SSC are Coastal water (CW),
South Atlantic central water (SACW) and Tropical water (TW). In
the summer, CW occurs in the surface water and sub-surface layers
are dominated by SACW. In the winter, SACW remains far from
SSC, and the channel is dominated entirely by CW or by CW with
intrusions from TW.
The bottom sediment distributions are heterogeneous (i.e.,
granules to clay) and are related to the coastline, bathymetry and
local circulation.
The SSC area is under intensive anthropic activities, such as a
port (Porto de So Sebastio), an oil terminal (Dutos e Terminais
Centro Sul DTCS) and oceanic disposal of domestic sewage by

Ara and Saco da Capela submarine outfalls.
The Ara submarine outfall is located on the continental side of
the SSC. Its operation started in 1990. The underwater pipeline
length is 1090 m (Cetesb, 2007). The diffusers, with 17 openings,
are located in the last 10 m of the pipeline. Daily, 104 L s1 of
domestic sewage (liquid part) are disposed of through this outfall.
The Saco da Capela submarine outfall, which started to operate
in 1997, is located in the city of Ilhabela, on the west coast of So
Sebastio Island. The underwater pipeline is 220 m long. Diffusers,
with 24 openings, are distributed in the last 2.5 m of the pipeline
(24 m water depth) (Cetesb, 2007). Every day, 30 L s1 of domestic
sewage (liquid part) are disposed of through this outfall.
The oceanic disposal system used in Ara and Saco da Capela is
composed of a pre-conditioning plant and their respective sewage
outfall. The pre-conditioning consists of a process in which the
efuent is chlorinated, double screened and sieved before being
carried out into the outfall. There is not any further treatment (primary, secondary or tertiary), such that the sewage is discharged
effectively untreated.
3. Materials and methods

Twenty supercial bottom sediment samples were collected in
2005, 10 in July near the Ara outfall diffusers, and 10 in September in the vicinity of Saco da Capela outfall diffusers. The sampling
grids were positioned in an area of 500 m2 surrounding the
538
submarine outfall diffusers (Fig. 1). Another ve samples were collected far from of main disposal sites (Fig. 1).
In each station, hydrographic data (water depth, temperature
and salinity) and sediment samples were taken. The hydrographic
data were obtained by CTD Seacat, and sediment samples were collected with a stainless steel Petersen grab sampler.
The sediment samples were divided into three sub-samples for
different analysis: (i) grain size, (ii) geochemical analysis of calcium carbonate, total organic carbon, total nitrogen, total sulphur
and phosphorus speciation (total, organic and inorganic phosphorus) and (iii) determination of live benthic foraminifera.
3.1. Grain size and geochemical analysis
The grain size analysis was performed using standard sieve and
pipette methods described in Suguio (1973). Textural typology was
determined using the Wentworth classication (Wentworth,
1922).
Calcium carbonate (CaCO3) contents were determined by
weight loss after dissolution in hydrochloric acid (Gross, 1971).
The classication of carbonate calcium content was performed
according to Larssoneur et al. (1982).
The determination of total organic carbon (TOC) and total nitrogen (N) was carried out on a LECO CHN-1000 analyzer. For TOC
analysis, the carbonatic fraction was eliminated through hydrochloric acid (HCl 10%) treatment. Total sulphur (S) was determined
on a LECO SC-432 analyzer.
Organic P (Porg) was estimated from the difference between
HCl-extractable P of ignited (240 C) and unignited samples (Legg
and Black, 1955). The fractionation of inorganic P (Pinorg) was
determined by following Legg and Black (1955).
The ratios of TOC/N (elemental) and TOC/Porg (molar) were calculated to determine the origin of organic matter in the sediments.
The ratio of TOC/S was calculated to distinguish normal marine
(oxygenated) depositional environments from anoxic or semi-anoxic marine sediments.
3.2. Live benthic foraminifera
Sometimes the use of grab sampler can mix deeper and supercial sediments together, and foraminifera may be lost due to the
bow wave generated by the impact of the sampling engine at the
sea oor (Mojtahid et al., 2008). To minimize this problem, grab
sampling was carefully operated, and only the uppermost (rst
5 cm) of the undisturbed bottom sediments were taken at each station. Mixtures of black (anoxic) and brown (oxic) sediments were
specically avoided.
Immediately after sampling, the sediment was preserved with
alcohol 70 GL and stained with Rose Bengal to distinguish between
living (stained) and dead (unstained) benthic foraminifera (Walton, 1952).
In the laboratory, the sediment aliquots were washed and
sieved over 62 lm and 500 lm mesh sizes (Boltovskoy et al.,
1980). The foraminifera were separated from the sediment by otation in trichloroethylene (CCl4). The residue was also checked for
foraminifera.
To detect submarine inuence upon foraminifera assemblages,
only live individuals were studied. Living benthic foraminifera
indicate the autochthonous origin of their species (Armynot du
Chtelet et al., 2004), which is thus under the inuence of local
environmental parameters (Murray, 1991). Aliquots of 10 cm3 of
sediment were analysed until 100 live specimens were handpicked, a number considered feasible for statistical analysis (Murray, 1991).
The abundance of live benthic foraminifera has been standardized to 10 cm3 of sediment in common practice; however, because
of the low individual numbers, in this study their abundance is expressed as foraminifera per cm3 of sediment (Murray, 2003). The
mean density in relation to 10 cm3 of sediment was also calculated
from each of the stations.
Taxonomic identication was done under a binocular magnier
(ZEISS-Stemi SV6), following the classication Atlas of Benthic
Shelf Foraminifera of the Southwestern Atlantic (Boltovskoy
et al., 1980).
Morphometric analysis was performed on all foraminifera shells
with the Analysis Imaging Program. After the morphometric analysis, the foraminifera were divided into four size classes: small
(<125 lm), medium (125250 lm), large (250500 lm) and very
large (>500 lm). The size classes of foraminifera shells were based
on Wentworth (1922) grain-size scale, respectively: ne, medium,
coarse and very coarse sand.
Considering that live benthic foraminifera respond sensitively
to sediment changes (e.g., in organic matter ux, oxygenation
and bottom hydrodynamics), the species with a relative abundance
higher than 5% in all sampling grids were divided in two groups:
species bioindicators of organic-enriched environments and species bioindicators of well-oxygenated environments (see Appendix
1 for references). The use of live benthic foraminifera as a qualitative proxy to analyse organic enrichment and oxygenation level
was mainly based on Kaiho (1994) and Martins et al. (2007), with
modications.
3.2.1. Statistical analysis of data
Specic diversity was determined using the Shannon index
(Shannon and Weaver, 1948):
H0
pi ln pi
and equitability (J) was calculated according to the Pielou index

(Pielou, 1969):
H0
ln S
where (i) pi is the proportion of each species, (ii) S is the total number of species identied at each station and (iii) ln = loge.
Richness was dened as the total number of species at each
station.
Canonical correspondence analysis (CCA) and Pearsons correlation coefcients were used to verify the relationship between species and environmental variables. CCA was performed using the
CANOCO program, version 4.5 (ter Braak and Smilauer, 2002).
The model achieved was tested by the Monte-Carlo Permutation
test (ter Braak, 1994). The matrix of biotic data was elaborated
using the absolute abundance of live benthic foraminifera species
with density higher than 40 specimens according to what was suggested by Horton et al. (1999). Rare species do not interfere with
the results (Duleba and Debenay, 2003); however, they can make
interpretation of the analysis difcult (Gauch, 1982). Data were
transformed using the log (x + 1) to increase the importance of
smaller values, leading to a more normalized distribution. The
choice of environmental variables occurred based on a signicant
statistical level in the forward selection (p < 0.05).
4. Results
4.1. Ara sewage submarine outfall
4.1.1. Hydrographic data, grain size and geochemical analysis
Geographical positions, hydrographic data, grain size and geochemical results for Ara are summarized in Appendix 2.
The salinity and temperature values in the bottom water ranged
from 34.7 to 35.1 and from 22.1 C to 22.6 C, respectively.
Sediment mean grain ranged from 1.81U to 4.12U, and grain

sorting ranged from 1r to 4r. Sandy sediments (Fig. 2) were prominent with percentage ranging from 46.4% to 82.7% (average
70.45%), mainly in ne and very ne sand. High muddy concentrations (silt plus clay) were observed only at station Ar10 (53.24%)
(Fig. 2).
Granules, sedimentary fraction >2 mm, occurred in almost all
stations, with percentages ranging from 0.36% to 12.59%. In this
study, the granule fractions were exclusively composed of shells
and mollusc fragments.
Station 4 was not sampled due to the high bioclastic contents.
The background station (Bck1) and stations Ar11 and Ar12 were
sampled approximately 10 km, 2 km and 2.5 km away from the
main disposal site (i.e., Ar1), respectively. According to textural
composition, the sediments at the Ar12 station are classied as
sand and for Bck1 and Ar13 as clayey sand.
Based on CaCO3 content, three different sub-environments
could be identied: (i) litoclastic (<30% CaCO3) stations Ar1,
Ar5Ar7, Ar10; (ii) litobioclastic (3050% CaCO3) stations Ar2,
Ar3, Ar9 and (iii) biolitoclastic (5070% CaCO3) station Ar8.
TOC content ranged from 0.10% to 3.37% (average 1.10 1.34%).
The highest concentrations were observed at stations Ar8 (3.31%)
and Ar9 (3.37%), which presented contents 330 times higher than
the other ones.
N content ranged from 0.01% to 0.10% (average 0.03 0.03%).
For P speciation, the following values were obtained: P = 0.1
Porg = 0.0020.053%
(23.8
0.19%
(688.81922 lg g1),
528.3 lg g1) and Pinorg = 0.0580.159% (809.61591.3 lg g1).
The sulphur content oscillated from 0.09% to 0.46% (average
0.18 0.11%). The highest value was observed at station Ar10,
whose percentage was 25 times higher than the percentage observed in other stations.
For the Bck1, Ar12 and Ar13 stations, the following values of
nutrients and sulphur were obtained, respectively: TOC 1%, 1.1%
and 0.51%; N 0.1%, 0.11% and 0.05%; S 0.23%, 0.46% and 0.07.
The C/N and C/P ratios ranged from 2.4 to 337.0 and 10.74 to
266.7, respectively.
539
The C/S ratios oscillated from 0.8 to 19.9.

4.1.2. Live benthic foraminifera
A total of 40 species of live benthic foraminifera were identied
belonging to the suborders Rotaliina (27 species), Textulariina (8
species) and Miliolina (5 species) (Appendix 3). Some of the main
species are illustrated in Plates 1 and 2.
The benthic foraminifera density ranged from 3 to 10 specimens
per cm3 of sediment; with mean density in relation to 10 cm3 ranging from 28 to 96 foraminifera. The sediment volumes analysed
oscillated between 10 and 40 cm3.
The highest density was observed at station Ar1, from which 96
benthic foraminifera in 10 cm3 of sediment were obtained. Station
Ar10 presented the lowest values of density and richness. At station Ar10, 111 foraminifera were handpicked from 40 cm3 of sediment and 11 species were identied.
The species richness ranged from 11 to 25 species per sample.
The specic diversity (H0 ) and equitability (J) values ranged
from 1.77 to 2.86 and from 0.72 to 0.92, respectively.
The most abundant species is Ammonia tepida (24.747.7%), followed by Pararotalia cananeiansis (1.817.1%).
The foraminifera shells have a mean size of 148.4 6 lm, with
minimum and maximum sizes of 80 lm and 366 lm, respectively.
Morphometric results indicate a predominance of medium-sized
shells (4376%, average 59%; Fig. 3). However, a signicant percentage of small-sized shells was also observed; the values ranged
from 21% to 54% (average 37.0%), with small shells predominating
(54%) at stations Ar3 and Ar8. Large-sized shells were observed in
all stations, but their concentrations were lower than 8% (average
3.66%).
4.2. Saco da Capela sewage submarine outfall
4.2.1. Hydrographic data, grain size and geochemical analysis
The geographical positions, hydrographic data, grain size and
geochemical results for Saco da Capela are described in Appendix
2.
Fig. 2. Grain size distribution of the sampled sediments near the Ara submarine outfall. Size terms according to Wentworth (1922).
540
Plate 1. (A) Ammotium salsum, 30 lm; (B) A. tepida, spiral side, 20 lm; (C) A. tepida, umbilical side, 30 lm; (D) B. marginata, 30 lm; (E) B. ordinaria, 10 lm; (F) B. striatula,
20 lm; (G) Buliminella elgantissima, 30 lm; (H) Cancris sagra, umbilical side, 30 lm; (I) C. crassa, 10 lm; (J) Cibicides sp., spiral side, 30 lm; (K) C. involvens, 10 lm; (L)
Cribroelphidium poyeanum, 100 lm; (M) G. praegeri, umbilical side, 20 lm; (N) G. praegeri, spiral side, 20 lm; (O) F. pontoni, 20 lm; (P) H. boueana, spiral side, 30 lm.
The temperature and salinity values in the bottom water ranged

from 20.5 C to 20.8 C and 31.7 to 31.9, respectively.
Sediment mean grain ranged from 0.39U to 3.94U, and grain

sorting ranged from 0.35r to 4r.
541
Plate 2. (A) Haynesina germanica, 30 lm; (B) Hopkinsina pacica, 10 lm; (C) Gaudryina exilis, 30 lm; (D) Lagena laevis f. tenuis, 30 lm; (E) Lenticulina sp., 100 lm; (F) L.
lobatula, spiral side, 30 lm; (G) N. terquemi, ventral side, 30 lm; (H) P. cananeiaensis, spiral side, 20 lm; (I) P. cananeiaensis, ventral side, 20 lm; (J) Poroeponides lateralis,
umbilical side, 100 lm; (K) P. atlanticum, umbilical side, 20 lm; (L) Pseudononion opima, spiral side, 30 lm; (M) Quinqueloculina lamarckiana, 20 lm; (N) R. oridana, spiral
side, 30 lm; (O) R. oridana, umbilical side, 20 lm; (P) Trochammina inata, spiral side, 30 lm.
Near Saco da Capela submarine outfall diffusers, sandy sediments are predominant (Fig. 4), mainly in coarse and very coarse
sand. The percentages of sandy sediments ranged from 53.2% to

95.67% (average 82.5%), and the ne fraction ranged from 1.37%
542
Fig. 3. Morphometric analysis performed on foraminifera shells sampled near the Ara submarine outfall.
Fig. 4. Grain size distribution of the sampled sediments near the Saco da Capela submarine outfall. Size terms according to Wentworth (1922).
to 25.28% (average 14.5%). Granules occurred only at stations Sc2,

Sc6 and Sc8. The granule fractions were exclusively composed of
shell and mollusc fragments.
Stations Sc1 and Sc4 were not sampled due to high bioclastic
content.
The background station (Bck1) and stations Sc13 and Sc14 were
sampled about 15 km, 0.3 km and 1.0 km from the main disposal
site (Sc1). According to textural composition, the sediments of all
stations are classied as clayey sand.
The CaCO3 content indicates a litoclastic environment. The values obtained ranged from 5.93% to 23.87%.
TOC content ranged from 0.15% to 2.27% (average 1.11 0.62%).
The highest TOC value was observed at station Sc5, located in the
north area of the sampling grid.
N content ranged from 0.01% to 0.1% (average 0.029 0.03%).
The P speciation values were (i) P = 0.03340.0926% (334.07
925.84 lg g1), (ii) Porg = 0.0030.0111% (3.43111.24 lg g1)
and (iii) Pinorg = 0.03090.0885% (308.57849.3 lg g1).
The S content ranged from 0.003% to 0.163% (average

0.064 0.05%). The highest values were observed at stations Sc9
and Sc10, located in the west and northwest area of the sampling
grid.
For the Bck1, Sc13 and Sc14 stations, the following values of
nutrients and sulphur were obtained: TOC 1%, 0.83% and 0.0.95%;
N 0.1%, 0.85% and 0.12%; S 0.23%, 0.19% and 0.16%, respectively.
The values obtained for TOC/N and TOC/P ratios ranged from 3.0
to 168.0 and from 128.9 to 5853.8, respectively. Anomalous TOC/P
ratios were observed at stations Sc5 (C/P = 5853.8) and Sc9 (C/
P = 4332.3).
The C/S ratios values ranged from 4.3 to 236.7.
4.2.2. Live benthic foraminifera
A total of 54 species of live benthic foraminifera were identied
throughout the study area (Appendix 3). The species are distributed among the Suborders Rotaliina (41 species), Miliolina (8 species) and Textulariina (5 species). Some of main species are
illustrated in Plates 1 and 2.
The benthic foraminifera density oscillated from 1 to 9 specimens per cm3, with mean density in relation to 10 cm3 varying between 7 and 19 individuals. The sediment volumes analysed varied
from 20 to 160 cm3.
The lowest density was observed at station Sc9, from which
160 cm3 of sediment were analysed to handpick 107 live benthic
foraminifera. In contrast, station Sc12 presented the highest density and richness. One hundred and sixty seven (167) foraminifera
were handpicked in 20 cm3 of sediment and 33 species were
identied.
The H0 and J values ranged from 2.49 to 2.94 and from 0.78 to
0.96, respectively.
A. tepida and Gavelinopsis praegeri were the most abundant species. The relative abundance of A. tepida ranged from 4.72% to
28.74% (average 18.37%). The relative abundance of G. praegeri ranged from 7.2% to 33.02% (average 14.75%).
The foraminifera shells have mean size of 179.5 17.0 lm; with
minimum and maximum sizes of 85 lm and 1225.0 lm, respectively. Morphometric analysis results indicated four size classes
543
of foraminifera shells (Fig. 5). The percentage of small shells ranged

from 15% to 31% (average 20.3%). The highest percentage was observed at station Sc10, to the northwest of the disposal site. Medium-sized shells were dominant, ranging from 60% to 71% (average
67.52%). Large-sized shells were observed in all stations in percentages ranging from 7% to 19% (average 11.09%). Very large shells
(>500 lm) occurred only at stations Sc2, Sc3, Sc7, Sc8 and Sc11
in percentages ranging from 1% to 4% (average 1.08%).
4.3. Canonical correspondence analysis (CCA) and Pearsons
correlation index
The ordination diagram obtained from the CCA shows a significant correlation among live benthic foraminifera and environmental variables. According to vector size, in decreasing order of
importance, the variables selected by CANOCO program are depth,
mean grain and sulphur (Fig. 6).
Mean grain and sulphur are associated with axis 1, and depth is
associated with axis 2. Together, axes 1 and 2 explained 95.2% of
the relationship between species and environment; 81.3% is explained by the rst axis alone (Table 1; Fig. 6).
Bolivina ordinaria, Buliminella elegantissima, Cassidulina crassa f.
media, Pararotalia cananeiaensis, Ammonia parkinsoniana, Pseudononion atlanticum, Rosalina oridensis are positively associated with
axis 1, being more frequent in environments with low bottom
hydrodynamics, a predominance of the ne sedimentary fraction
and high S content. Hanzawaia boueana, Neocornobina terquemi,
Bolivina cf. sphatula and G. praegeri are negatively associated with
axis 1, and are thus more frequent in environmental conditions
opposite to those listed above.
Lobatula lobatula and Discorbis williamsoni are negatively associated with axis 2.
The position of Brizalina striatula and A. tepida near the diagram
ordination origin showed the complexity of its distribution. A. tepida has a broad ecological distribution due to its capacity to adapt
to environments with high variation in physicochemical parameters. On the other hand, B. striatula is a detritivorous species (Murray, 1991) observed in poor-oxygen and organic rich environments
Fig. 5. Morphometric analysis performed in foraminifera shells sampled near the Saco da Capela submarine outfall.
544
Fig. 6. Ordination diagram of species-environment relation.
Table 1
Canonical correspondence analysis results.
Axes
Total inertia
Eigenvalues
Speciesenvironment correlations
0.213
0.873
0.037
0.702
0.013
0.657
0.103
0.000
0.623
Cumulative percentage variance

Of species data
Of speciesenvironment relation
34.3
81.3
40.1
95.2
42.2
100.0
58.7
0.0
(Lutze and Coulbourn, 1984; Martins et al., 2006). The distributions

of both species related to axes 1 and 2, infer that yours density may
also be inuenced by other abiotic parameters not selected by the
CANOCO analysis.
The ordination diagram for samples and environmental variables (Fig. 7) characterises the study areas.
The samples collected nearby to Ara are indicated by black
dots. Exception station Ar11, the stations were sampled in a shallow environment. The station Ar11 was sampled in deepest environment. In all stations coarser and ne sediments coexist,
inferring moderate to low bottom circulation, which permitted
the preservation of sulphur.
Samples collected near Saco da Capela, indicated by white dots,
were sampled at deep (stations Sc3, Sc5, Sc8, Sc9, Sc10, and Sc11)
and intermediate (stations Sc2, Sc6, Sc7, and Sc12) water depths,
with high hydrodynamic and low sulphur contents and where sandy sediments predominate. Sc13 and Sc14 are positioned in intermediate and deep water depth, with signicant S contents. Coarser
and ne fractions coexist.
Corroborating the CCA, near the Ara submarine outfall the
same negative relationship among live benthic foraminifera
assemblages and ne particles, mainly the silt fraction, and sulphur
was denoted by Pearson correlation index (Table 2). In less extension, a negative inuence on foraminifera parameters was also observed in relation to organic phosphorus contents (Table 2).
In relation the samples collected near the Saco da Capela submarine outfall, Pearson correlation index indicated that the grain
size and salinity are the most important environmental variables

inuencing the foraminifera assemblage (Table 3). According with
results the foraminifera parameters are positively linked by ne
particles, mainly silt fraction, and negatively linked with salinity
values.
5. Discussion
5.1. Ara sewage submarine outfall
5.1.1. Sedimentological analysis: grain size and geochemical
The Ara diffuser sewage submarine outfall is positioned in a
shallow environment, with an average 10 m water depth. During
the sampling period, thermohaline stratication was not observed;
however, CW mass water (temperature > 20 C and salinity < 35)
was observed.
The grain size composition shows very heterogeneous surface
bottom sediments (granule to clay). The same result was observed
in other studies (Furtado et al., 2008). According to the authors, the
SSC has a complex sedimentary system related to coastline,
bathymetry and local circulation. In the study area, as well as in
all of the SSC, the constant alternation in velocity and direction
of the bottom current and bathymetry induces grain size heterogeneity, with patchy distribution of sediments.
The distribution pattern of grain size shows that the western
and central regions of the sampling grid are probably under direct
inuence of bottom circulation and of the efuent disposed, which
545
Fig. 7. Ordination diagram for samples and environment variables. Grey dot background station; black dots Ara stations; white dots Saco da Capela stations.
ows at a rate of 140 L s1. These regions presented the highest

sand concentrations, as well as better grain sorting, which indicates reworking of the sediments by bottom currents. In contrast,
ne sediments with low grain sorting have been deposited to the
southeast and northeast of the disposal site, indicating a diminishing of bottom current energy to these regions.
In this study, the distribution of the geochemical compounds
analysed in supercial bottom sediments was similar to grain size
disposition. In general, the distribution of nutrients and sulphur is
associated with the texture of sediments. Their concentrations increase as the particle size of the sediments decreases. For this reason, in this study the lowest percentages occurred in the central
region, close to station Ar1, the main disposal site, where coarser
sediments are preeminent.
The organic enrichment at the study area was evaluated by
nutrient and sulphur content. At the majority of the stations,
TOC contents are considerate moderate (stations Ar1Ar7; <1%);
substantial values are observed at stations Ar8 (3.31%), Ar9
(3.37%) and Ar10 (1.49%). Comparatively, the TOC contents obtained in these stations are similar to the contents obtained in
recognized impacted sites. Aston and Hewitt (1977) obtained concentrations of TOC ranging from 0.07% to 1.97% in Walton Backwater (Essex, England). The region studied by Aston and Hewitt
(1977) is impacted due to the presence of commercial ports,
drainage from agricultural land and domestic sewage disposal.
Carreira and Wagener (1998), in an area located near the Ipanema
submarine outfall (Rio de Janeiro, Brazil), found TOC concentrations ranging from 0.79% to 3.18%. The Ipanema submarine outfall
discharges on average 8 m3 s1 of untreated sewage derived from
a population of 2 106 inhabitants (Carreira and Wagener, 1998).
Abessa et al. (2005), close to the Santos submarine outfall diffusers (Santos, Brazil), obtained 0.092.91% of TOC. Daily, 0.6
1.6 m3 s1 of untreated sewage is disposed of into Santos Bay
(Abessa et al., 2005). In the Gulf of Izmir (Easter Aegean Sea), an
area that is intensely industrialized, Bergin et al. (2006) obtained
TOC contents ranging from 0.40% to 3.12%. Cesar et al. (2007)
found levels of TOC from 0.85% to 3.75% in the Santos and So
Vicente estuarine system (Brazil), a region that comprises a densely urbanized area, the biggest Brazilian industrial complex, predominantly with the petrochemical, siderurgy, and fertilizer
industries, and also the major Latin American port Port of
Santos.
The TOC content at the background stations is higher than the
values obtained at station Ar1; however, Ar1 is located in an environment with high bottom hydrodynamics, inhibiting organic
enrichment. In contrast, the background station Bck1 (1.00%) and
stations Ar11 (1.10%) and Ar12 (0.51%) have TOC levels two to
three times lower than those observed at the three stations in
the Ara sampling grid with the highest values (Ar8, Ar9 and
Ar10). The textural composition and hydrodynamics of these areas
is very similar.
According to Diz et al. (2006), TOC levels 2% to 4%, similar to
that observed at stations Ar8 and Ar9, are typical values for ne
grain sediments deposited in eutrophic environments.
The concentrations obtained for P were also equal to the values
obtained by Aston and Hewitt (1977; 102040 lg g1) and Carreira
and Wagener (1998, 369.812284.57 lg g1). In Santos Bay, the
area surrounding the submarine outfall diffusers, Cetesb (2007) recorded values ranging from 373.13 lg g1 to 1787.53 lg g1.
The presence of P in marine environments can occur naturally
or be human-induced. Phosphorus input is strongly dominated,
about 90%, by the supply from land, including point sources
(Rosenberg et al., 1990). Baturin (2003) suggested that value above
700 lg g1 indicate anthropogenic inuence. Excluding station
Ar5, all stations have levels of P indicative of anthropogenic activities, i.e., higher than 700 lg g1.
Also indicative of anthropogenic activities are the high levels of
Pinorg. In the present study, 6197% (average 83.7%) of P was in an
inorganic form. The dominance of Pinorg has been associated with
use of fertilizers and disposal of untreated sewage, containing
polyphosphates and orthophosphates (Aston and Hewitt, 1977;
Ozrio and Oliveira, 2001; Marins et al., 2007).
A strong linear correlation (Pearsons correlation coefcients)
was obtained between TOC and P (r = 0.82; p < 0.05), indicating
546
Table 2
Results of Pearsons correlation index obtained for Ara submarine outfall data (Mud = silt plus clay).
Mean density
Richness
H0
J
A. tepida
P cananeiaensis
*
***
Salinity
Temperature
Granules
Sand
Silt
Clay
Mud
CaCO3
TOC
Porg
Pinorg
0.17**
0.044*
0.42*
0.55*
0.33
0.06*
0.19**
0.17
0.13*
0.28*
0.10**
0.26*
0.25*
0.01*
0.46
0.64*
0.62*
0.06
0.78***
0.73*
0.45*
0.01*
0.03*
0.61*
0.72**
0.82
0.69**
0.25**
0.31*
0.75**
0.13**
0.18*
0.22**
0.16*
0.22*
0.32
0.71**
0.73
0.60*
0.20*
0.24***
0.64*
0.07**
0.01
0.40*
0.59*
0.62
0.14**
0.41*
0.31*
0.09***
0.15
0.26*
0.31***
0.36*
0.19*
0.14*
0.19*
0.09*
0.16*
0.32*
0.15*
0.01*
0.17*
0.37*
0.08*
0.71*
0.66*
0.49*
0.08*
0.03*
0.61*
0.06*
0.11*
0.23*
0.25*
0.47*
0.17*
0.73*
0.88*
0.73*
0.25*
0.36*
0.86*
0.46*
0.52*
0.34
p < 0.001.
p < 0.005.
p < 0.05.
**
Depth
0.73*
0.42**
0.05*
Table 3
Results of Pearsons correlation index obtained for Saco da Capela submarine outfall data (Mud = silt plus clay).
Mean density
Richness
H0
J
A. tepida
G. praegeri
*
**
***
p < 0.001.
p < 0.005.
p < 0.05.
Depth
Salinity
Temperature
Granules
Sand
Silt
Clay
Mud
CaCO3
TOC
Porg
Pinorg
0.47
0.1
0.06*
0.2*
0.52
0.28
0.73
0.42*
0.33*
0.16*
0.06*
0.05*
0.11
0.19
0.13*
0.03*
0.14
0.04
0.15***
0.42*
0.53
0.07
0.1*
0.35**
0.05*
0.51*
0.29*
0.33*
0.46*
0.53*
0.02
0.63*
0.59***
0.19*
0.47**
0.61
0.01***
0.47*
0.16
0.33***
0.36*
0.49***
0.27
0.09**
0.32*
0.06*
0.19
0.06
0.02***
0.14*
0.07*
0.03
0.07*
0.20**
0.21***
0.46*
0.04*
0.09*
0.36*
0.28*
0.06***
0.22*
0.01*
0.41*
0.25*
0.10*
0.01***
0.07*
0.04*
0.24*
0.31*
0.21*
0.07***
0.21*
0.01*
0.37*
0.38*
0.19*
0.22***
0.38*
0.46*
0.14*
0.35*
0.5*
0.23***
0.50**
0.30**
0.06**
0.32***
0.46***
that both elements have a common and allochthonous source, i.e.,

domestic sewage efuent disposal by submarine outfall.
Regarding sulphur, the highest levels were observed at station
Ar10, where the value obtained was 25 times higher than the levels at the other stations. A similar value was only observed at station Ar11 (0.46% of S), positioned 900 m away from Dutos e
Terminais Centro Sul DTCS, one of the largest petroleum terminals in Brazil. The sulphur distribution pattern, similar to pelitics
sediments (r = 0.90; p < 0.001), can be associated with FeS formation in a possibly reducing environment. Sulphur levels could also
suggest anaerobic organic matter degradation by sulphate-reducing bacteria. In normal aerobic marine environments, sulphur levels are lower than 0.13% (Turekian and Wedepohl, 1961); in this
sense, the values observed at stations Ar3 (0.18%), Ar5 (0.19%),
Ar8 (0.17%), Ar9 (0.20%) and Ar10 (0.46%) suggest an environment
experiencing anthropic inuence.
5.1.1.1. Organic matter origin and reducing potential in the supercial
sediments. Terrestrial and marine organic matter have relatively
distinct TOC/N elemental and TOC/Porg molar ratios. The fundamental difference is the elemental composition of the organic matter, i.e., TOC, N and P concentrations.
Proteins, which are the primary N compounds of phytoplankton
and zooplankton, have TOC/N ratios between 5 and 6; in contrast,
terrestrial vascular plants and their derivates in the sediments
have TOC/N ratios higher than 15 (Bordovskiy, 1965; Stein, 1991;
Twichell et al., 2002). Vascular plants are the main organic producers in the terrestrial environment, and consist mainly of cellulose
and lignin, which contain few nitrogen compounds (Bordovskiy,
1965; Sampei and Matsumoto, 2001). Values between 7 and 15
represent both marine and terrestrial organic compounds. Due to
the difference in ratios, values of TOC/N have been used as a representative proxy to identify the origin of organic matter.
The use of TOC/P molar ratios is also a relevant proxy to indicate
the source of organic matter, but its use is uncommon. Most studies have focused only on TOC/N ratios. There are at least two reasons for the preponderance of using TOC/N ratios rather than
TOC/P: (i) a result of the analytical ease of quantifying N along with
C using a CHN elemental analyzer and (ii) there is no simple analytical analogue for quantifying P (Ruttenberg and Goni, 1977. In
this study, the TOC/P molar ratio was used to complement the
information obtained by TOC/N ratios.
The organic matter of the supercial sediments sampled close
to the Ara submarine outfall has a predominantly terrestrial origin. The marine origin only was identied at stations Ar1 and Ar7.
A mixture of both marine and terrestrial organic matter was observed at station Ar6, as well as for stations Bck1, Ar11 and Ar12.
The values of TOC/N ratios obtained in this study are similar to
values estimated for sewage particulate matter reported elsewhere
(Emmeis et al., 2000: TOC/N 1015; Ruiz-Fernandez et al., 2002:
TOC/N 27; Cetesb, 2007: TOC/N 614).
According to intervals proposed by Ruttenberg and Goni (1977),
TOC/P molar ratios lower than 80 indicate a bacterial source, the
value of 106 indicates marine origin (phytoplankton and zooplankton), between 300 and 1300 indicates soft tissue terrestrial sources
and higher than 1300 indicates a woody terrestrial source.
The results of TOC/P ratios in this study indicate a bacterial
source for stations Ar3, Ar6, Ar7 and Ar10, and a mixture of marine
and terrestrial organic matter sources for all other stations. TOC/P
ratios might also indicate the oxidationreduction potential of the
supercial sediments. Low TOC/P values, similar to those obtained
in this study, can indicate anoxic conditions of the sampled sediments, due to high P2O5 concentrations (Riley and Chester,
1976). Based on this, the value of TOC/P ratios can indicate an increase of bacterial biomass for anaerobic organic matter
degradation.
547
The difference between the results obtained for the TOC/N and
TOC/P ratios can be explained as a consequence of TOC/P ratios in
aquatic plants and bacteria showing greater variability than TOC/N
ratios, due to higher consumption and storage exhibited by algae
and bacteria (Gchter and Meyer, 1993). Another important factor
is the grain size of sediments. In coarse sediments, N and especially
P can be preferentially degraded relative to TOC during sedimentation (Bader, 1955; Faganelli et al., 1988).
The use of TOC/S ratios to discriminate normal marine (oxic)
depositional environments from anoxic or semi-anoxic marine
environments is based on the process of biological sulphate reduction (Leventhal, 1982; Raiswell et al., 1987; Berner, 1989; Stein,
1991; Borrego et al., 1998). Microbial sulphate reductions using organic matter as a food source and sulphate as an oxygen source
(electron acceptor) takes place only under anoxic conditions
(Leventhal, 1982). Consequently, TOC/S ratios reect the reduction
of sulphate during decomposition of organic matter, and thus give
a qualitative indication of the redox condition of the depositional
environment (Raiswell et al., 1987; Borrego et al., 1998). TOC/S ratios values lower than 2.8 0.8 indicate sediments laid down under reducing conditions (Raiswell et al., 1987; Berner, 1989;
Stein, 1991; Morse and Berner, 1995; Lyons and Berner, 1992;
Borrego et al., 1998). In this sense, bottom sediments with reducing
conditions were observed at stations Ar1, Ar3, Ar5, Ar6, Ar7 and
Ar10. As expected, the background station Ar11 presented sediments with reducing characteristics. On the other hand, at stations
Bck1 and Ar12, the C/S ratios indicated oxic conditions in the sedimentwater surface.
The information obtained by TOC/S ratios are consistent with
the reducing environmental conditions observed in TOC/P ratios
(r = 0.84; p < 0.01, not demonstrated). In almost all of the stations
in which the origin of organic matter was identied as bacterial,
sediments presented reducing characteristics, with TOC/S ratios
lower than 3.
5.1.2. Live benthic foraminifera: species composition, distribution and

morphometry
Although diverse studies have been performed in coastal regions, there is not yet a total understanding of the ecological
dynamics of foraminifera. This lack of understanding occurs because marginal marine environments are very complex regions
where natural and anthropogenic stress can occur at the same time
(Alve, 1995; Armynot du Chtelet et al., 2004). Therefore, in some
occasions, it is difcult to interpret what proportion of observed local variation in the assemblage composition, abundance, diversity
patterns and morphology is due to natural or anthropogenic
changes (Alve, 1995).
In the present study, the results from the CCA and Pearson correlation index indicated that depth, grain size, sulphur and phosphorus are the main abiotic variables that inuence the
foraminifera assemblages.
The effects of sediment grain size on foraminifera assemblage
composition are still a matter of debate (Armynot du Chtelet
et al., 2008). Although Alve and Murray (1999) found no obvious
relationship between sediment grain size and species composition,
other researchers have obtained divergent results. Hendrix (1958),
Debenay et al. (2001) and Armynot du Chtelet et al. (2008) infer
that increases in density and richness of foraminifera are favoured
by ne particles, whereas other authors have observed the opposite relationship (Diz et al., 2004; Martins et al., 2006). In this study
an opposite relationship was observed in relation to foraminifera
parameters and ne particles.
Based on the fact that high organic matter levels strongly depend on the adsorption of ne particles (silt and clay), it is possible
to conclude that the organic matter in the sediments may be the
548
factor that really controls the composition and distribution pattern

of foraminifera assemblage.
Organic matter at times favours an increase in both density and
richness of the foraminifera assemblages (Watkins, 1961; Bandy
et al., 1964a, 1964b, 1965; Nagy and Alve, 1987; Debenay et al.,
2001), and can be responsible for decreasing both parameters (Alve
and Naggy, 1986; Schafer et al., 1995; Armynot du Chtelet et al.,
2004; Burone et al., 2006). Additionally, in some cases, foraminifera appear totally independent of organic matter inputs (Setty
and Nigan, 1982). Organic matter might favour microfauna, with
the toxic threshold depending on the concentration in the sediments and the nature of the organic matter (Alve, 1995; Murray,
2001; Armynot du Chtelet et al., 2004).
TOC inuence on foraminifera assemblage was not observed by
CCA and Pearson correlation (see Table 2). However, in the stations
Ar1, Ar7, Ar9 and Ar10 a correlation pattern was observed. Stations
Ar1 (0.12% of TOC) and Ar7 (0.10% of TOC), whose samples contained lower TOC contents, had the highest mean densities of
foraminifera; station Ar7 also had the highest richness. An opposite
relationship occurred at stations Ar9 (3.37% of TOC) and Ar10
(1.49% of TOC); at both stations there were higher TOC levels and
decreased mean density and species richness.
The relationship between the distribution pattern of live benthic foraminifera (310 foraminifera per cm3) and TOC values
was opposite of that reported by some authors in areas with the
highest TOC levels. Gustafsson and Nordberg (2000), in Havstens
fjord (Swedish West Coast), recorded live benthic foraminifera
densities varying from 1 to 24 specimens per cm3 in samples with
34.1% of TOC. Diz et al. (2006) obtained, from supercial sediments of Ra de Vigo (North Spain), live benthic foraminifera with
a density ranging from 1 to 27 individuals per cm3 of sediment and
TOC levels ranging from 2% to 4%. Near Santos submarine outfall
(Santos Bay, Brazil), Cetesb (2007) recorded live benthic foraminifera ranging from 1 to 7 foraminifera per cm3 of sediment and TOC
values at 0.282%. At the Canche estuary (Pas-de-Calais, France),
Armynot du Chtelet et al. (2008) observed live benthic foraminiferal densities of 184 foraminifera per cm3 and TOC levels of 0.1
12.4%. The foraminifera density at stations Bck1, Ar11 and Ar12 are
very similar to the values obtained in 80% (except stations Ar9 and
Ar10) of the stations analysed near Ara. The foraminifera density
ranged from 4 to 10 individuals per cm3 of sediment, and TOC levels varied from 0.51% to 1.10%.
A negative relationship among foraminifera parameters and
Porg and sulphur was denoted (see Table 2).The lowest density,
richness and specic diversity were observed at station 10, where
sulphur levels were almost 25 times higher than values observed at other stations and Porg contents were nearly 24 times
higher. The same linkage among biotic parameters and sulphur
was observed at station Ar11, which had similar sulphur content
(0.46%).
Higher sulphur levels indicate low bottom currents and higher
organic matter deposition, the decomposition of which can cause
low oxygen levels and reducing conditions in the watersediment
surface. Therefore, the low density, richness and specic diversity
observed at station 10 can be a result of reducing conditions.
A. tepida is the dominant species at all stations analysed (average 38 8%). The dominance obtained in this study is similar to
that observed in studies in polluted coastal regions. On the Mediterranean coast of Israel, Yanko et al. (1994) observed relative
abundance ranging from 0% to 65% (average 22.6 17%). Cearreta
et al. (2002) recorded A. tepida (as Ammonia beccarrii) with a relative abundance of 3576% (average 61%). Ferraro et al. (2006)
found a relative abundance of 1.8100% (average 40.6%) in Naples
Harbour (Tyrrhenian Sea, Southern Italy). Burone et al. (2006) obtained a relative abundance ranging from 15.4% to 98% (average
65.1%) in the Montevideo coastal zone, Uruguay.
A. tepida is a eurybiotic species and is characteristic of nearshore areas and shallow bays, adapted to wide environmental variations in, for example depth, salinity, temperature, grain size, pH
and oxygen level, among other abiotic parameters (Bradshaw,
1961; Murray, 1991; Kitazato, 1994). At a pH of 2.0, A. tepida can
survive for a period of 25 min to 1 h 15 min (Bradshaw, 1961). This
species can survive in dysoxic and microxic marine environments
for 12 months (Kitazato, 1994); in anoxic incubation, it can endure for at least 24 h, indicating a capacity of facultative anaerobic
metabolism (Bradshaw, 1961; Moodley and Hess, 1992).
Due to its capacity to tolerate extreme environmental variations, A. tepida has been observed as the dominant species in studies of human-induced environmental changes, due to a decline of
stenobiotic species. A. tepida has been reported as the dominant
species in areas close to outfalls discharging sewage, heavy metals,
chemical and thermal pollution, fertilizing products, caustic sod,
chlorine complexes and hydrocarbons (Alve, 1991, 1995; Yanko
et al., 1994; Cearreta et al., 2002; Armynot du Chtelet et al.,
2004; Vilella et al., 2004; Burone et al., 2006; Ferraro et al., 2006;
Le Cadre and Debenay, 2006).
Despite the above description, A. tepida must be used carefully
as a pollution bioindicator. According to Alve (1995), the high
abundance of one species in an area affected by a particular efuent does not necessarily imply that it is the most tolerant species.
However, it can be the most successful opportunist, with a rapid
turnover rate and the ability to quickly colonize a disturbed area
almost independent of the type of contaminant. However, the
dominance of a low number of species, in this study one species,
indicates environmental stress (Cognetti, 1992).
P. cananeiaensis, the second most abundant species, is an herbivorous, epifaunal species characteristic of marine environment
(Debenay et al., 2001). It was rst recorded in the laguno-estuarine
complex of Cananeia-Iguape in 1995; nevertheless, its ecological
preferences were still not well recognized. Debenay et al. (2001),
in samples distributed in almost all SSC, recorded the relative
abundance of P. cananeiaensis in total assemblages to be higher
than 49%, however, the authors did not observe a relationship between its relative abundance and depth, temperature or salinity. In
this study, P. cananeiaensis occurred preferentially in stations with
high sulphur, Porg and silt content.
The foraminifera assemblages at stations Bck1, Ar11 and Ar12
are composed mainly of C. crassa f. media and Rosalina oridana.
C. crassa f. media is an infaunal and detritivorous species (Murray,
1991) observed in poor-oxygen environments (Bernhard and Sen
Gupta, 1999) and sediments enriched in organic matter (Alavi,
1988). In contrast, R. oridana has been related to coarser sediments, high hydrodynamics and well-oxygenated bottom waters
(Murray, 1991; Duleba et al., 2005). The highest relative abundance
of both species occurred in a deep environment (42 m), with grain
size typical of a stable environment (50% sand and 50% the ne
sedimentary fraction), low TOC and N contents and high sulphur
contents.
For the subenvironment study, A. tepida and P. cananeiaensis
were not associated with any species group. A. tepida, as the dominant species, could mask the results, and the ecological preferences of P. cananeiaensis were not well established.
The species group in organic-enriched environments includes
detritivore specimens, which are associated with higher organic
matter ux, low oxygen concentrations in interstitial pore water
and low bottom energy, such as Bolivina. cf. sphatulata, Bolivina
compacta, Bolivina doniezi and B. ordinaria, B. striatula, Bulimina
marginata, B. elegantissima, Pseudononion spp. and C. crassa f. media.
The species group in well-oxygenated environments is made up
of epifaunal specimens, most of them herbivore feeders, characteristic of high bottom hydrodynamic and low organic matter concentrations, such as Discorbis williamsoni, H. boueana, L. lobatula, N.
terquemi, R. oridana, Quinqueloculina milletti, Lepidoteuramina

ochracea and Trochammina sp.
Near Ara submarine outfall diffusers, the relative abundance
of bioindicator species for organic-enriched sediments (1543%)
was slightly higher than bioindicator species of well-oxygenated
environments (431%). The distribution pattern of the two groups
relates to the source of organic matter in the rst case and to grain
size in the second one. A strong relationship was observed between
the species of organic-enriched sediments and terrestrial organic
matter (TOC/N ratio > 12; r = 0.83 p < 0.5); on the other hand, there
is no relationship between species in well-oxygenated environments and any source of organic matter. In fact, species belonging
to well-oxygenated environments are strongly inuenced by the
coarse sand fraction (r = 0.82; p < 0.5) and, to a lesser extent, by
CaCO3 (r = 0.57; p < 0.05).
The inuence of environmental variables on foraminifera shell
size remains unclear. The organisms size can be a response to the
level of dissolved oxygen, high organic inputs or both variables,
after the degradation of excessive inputs of organic matter induces
reducing conditions at the sedimentwater interface. According to
some studies in highly productive environments, foraminifera
assemblages tend to be dominated by smaller sizes as a consequence of diminished dissolved oxygen at the sedimentwater
interface (Phleger and Soutar, 1973; Perez-Cruz and Machain-Castilho, 1990; Boltovskoy et al., 1991; Kaiho, 1994). However, it has also
been suggested that the small size of specimens is a characteristic
of areas of high productivity, as a consequence of rapid reproduction under favourable conditions characterised by an abundance
of food (Bernhard and Reimers, 1991; Diz et al., 2006). Consequently, if smaller size is a product of favourable conditions, high
density, richness and species diversity, as well as, low dominance
can be expected (Phleger and Soutar, 1973). The results obtained
in this study, such as low density and richness and dominance of
one species (A. tepida), indicate that the predominance of medium
and small-sized shells qualitatively indicates low oxygen concentrations at the sedimentwater interface, in agreement with species
composition. The station Ar12 had the same pattern of foraminifera
shell sizes, there was a predominance of medium-sized shells, but
small shells were also a signicant percentage (41%).
According to the description above, it is possible to infer that
the main factors that inuence the composition and distribution
of live benthic foraminifera near Ara submarine outfall diffusers
are the sediment textural composition, the concentration and quality of organic matter, which in this study is predominantly allochthonous (terrestrial), and oxygenation levels.
5.2. Saco da Capela sewage submarine outfall
5.2.1. Sedimentological analysis: grain size and geochemical
The Saco da Capela submarine outfall is located on the insular
side of SSC, with an average water depth of 21 m. The CW water
mass was noted during the sampling period.
High bottom hydrodynamics were observed close to the Saco da
Capela diffusers by a predominance of sand sedimentary fractions.
Although there is a constant input of sediment and organic matter
by Crrego da Cachoeira River, the high hydrodynamism avoids
preservation of ne particles.
However, despite the constant reworking of the sedimentary
fractions, there is no selectivity in grain size. The heterogeneity
of sedimentary fractions (i.e., granules to clay) occurs due to uctuation in the direction and intensity of bottom currents (Furtado
et al., 2008). High concentrations of ne sedimentary fractions
were observed at stations Sc9 and Sc10, indicating a diminishing
of bottom currents SE to NW of the disposal site and/or patches
originating due to the stations being positioned in the deepest
environments, 25 and 31 m.
549
Due to oceanographic conditions of the study area, i.e., coarser

sediment fractions and high hydrodynamics, nutrients and S were
observed in a random distribution.
Although the average TOC and N contents were observed to be
equal near Ara outfall (average 1.10% and 0.03%), organic enrichment was not observed at the Saco da Capela for either variable.
TOC and N levels are evenly distributed among the stations sampled at the Saco da Capela site. TOC content at the background station Bck1 and stations Sc13 and Sc14 are also low. Nitrogen, except
at Sc13, has similar values obtained at the Saco da Capela stations.
Samples from station Sc13 had N contents eight times higher than
other ones; apparently, this high value can be associated with a
bloom of phytoplankton. This hypothesis is supported by TOC/N
ratios, which will be discussed subsequently.
Phosphorus levels indicating anthropogenic activities were observed only at stations Sc3 (778.5 lg g1), Sc8 (925.84 lg g1)
and Sc10 (745.05 lg g1). The values obtained are almost half as
much as values observed for samples analysed close to Ara.
Sulphur values in almost all stations are considerably low; values indicating anthropogenic inuence are only observed at stations Sc9 (0.16%) and Sc10 (0.14%). The distribution pattern is
strongly linked with the silt fraction (r = 0.94; p < 0.005) and to a
lesser extent with the clay fraction (r = 0.66; p < 0.5). Stations
Bck1 and Sc13 had slightly higher sulphur values, explained by
the high ne sedimentary fraction.
The difference of nutrients and sulphur levels obtained between
the Ara and Saco da Capela submarine outfalls can be related to
two factors. First, the outows are 4.5 times higher in the Ara
outfall; second, Saco da Capela outfall is positioned in environment
with higher hydrodynamics, hindering deposition of ne sedimentary fractions and consequently organic matter preservation.
5.2.2. Organic matter origin and reducing potential in the supercial
sediments
TOC/N elemental ratios identied organic matter that was predominantly terrestrial in origin near close to the Saco da Capela
submarine outfall. Marine and a mixture of marine and continental
sources were observed only at stations Sc6 and Sc11, respectively.
Only samples from Sc13 had a TOC/N ratio indicating a marine
source (TOC/N 0.98), corroborating the hypothesis of a phytoplankton bloom.
TOC/P molar ratios corroborate the results obtained for TOC/N
elemental ratios: most of the stations have organic matter of continental origin. A mixture of marine and continental origin was observed at stations Sc2, Sc6, Sc7 and Sc8. The higher values obtained
at stations Sc5, Sc9, Sc11 indicate woody debris, and values obtained at stations Sc2, Sc10 and Sc12 indicate soft tissues.
Considering the type of organic matter identied by TOC/P ratios, i.e., woody debris and soft tissues, it is possible to infer that
continental organic matter occurred mainly due to the proximity
of diffusers to the coastline (220 m) and to Crrego da Cachoeira
River, which drains in the Saco da Capela beach. Secondarily, is also
possible to infer the inuence of efuent disposal. The bacterial
origin was apparently associated with the increase of bacterial biomass that comes from organic matter decomposition.
C/S ratios analysed for Saco da Capela samples and background
sample indicated normal marine (oxic) sediments.
5.2.3. Live benthic foraminifera: species composition, distribution and
morphometry
Comparatively, the sediment volumes analysed at the Saco da
Capela (average 80 cm3) is slightly superior than volumes used
close to Ara Bay (average 20 cm3); consequently the density data
was lower (18 foraminifera per cm3; average 2). This fact apparently is associated with the textural composition of sediments. In
sediments with predominately coarse to very coarse sand, there
550
is a low number of benthic foraminifera, whereas high density is

present in ne sand and silty sand sedimentary fractions (Samir
and El-Din, 2001). A similar distribution pattern was observed in
this study, with high richness and specic diversity positively correlated with silt (see Table 3).
Despite this result, the CCA indicates that the distribution and
composition of species close to Saco da Capela are mainly inuenced by the depth and sediment grain size; the strong hydrodynamic of the study area must be considerate like an important
stressing factor.
Although not had been observed a signicant statistical correlation among foraminifera parameters and nutrients and sulphur
contents (see Table 3), the lowest richness (16 species) was found
in the station with the highest levels of TOC (Sc5; 2.27%).
G. praegeri and A. tepida are the main species identied in the
study area. G. praegeri is a passive suspension-feeding epifaunal
species (Murray, 1991), typical of well-oxygenated environments
with low organic matter concentrations (Altenbach et al., 2003;
Duleba et al., 2005; Martins et al., 2006). Its lowest relative abundance occurred at stations with high silt content (Pearson correlation) and low sulphur concentrations (CCA). A. tepida, according to
its distribution pattern, occurs in higher relative abundance in stations sampled in shallower water and in stations closer to coastline, i.e., stations 7 (26.8%) and 12 (28.7%).
In relation to the stations Bck1, Sc13 and Sc14, C. crassa f. media
(2131.1%) is the most abundant species, followed by B. ordinaria
(3.015.6%).
Organic ux (food) and oxygenation are the most important
parameters that regulate the composition of foraminifera assemblages (van der Zwaan et al., 1999). In areas of low nutrient content, such as the study area, there is almost always a food
limitation but no oxygen limitation; thus, the benthic foraminiferal
assemblage is relatively enriched by epifaunal species (Jorissen
et al., 1995; Jorissen, 1999).
Epifaunal species bioindicators of well-oxygenated environments are two times higher than infaunal species bioindicators of
organic-enriched environments; the relative abundances ranged
from 22.4% to 73% (average 41.4%) and from 9.2% to 34% (average
22%), respectively.
The main species that composed the group indicating a welloxygenated environment were G. praegeri, H. boueana, N. terquemi,
Cornuspira involvens, D. williamsoni, L. lobatula, R. oridana, Patelina
corrugata, Cibicides spp., Quinqueloculina spp., L. ochracea. As expected, the main abiotic factors that control the distribution pattern of this group are sandy sediments (r = 0.61; p < 0.001) and
sulphur levels (r = 0.57; p < 0.001). In contrast to that observed
close to the Ara submarine outfall, the epifaunal species group
identied near the Saco da Capela diffusers did not demonstrate
any relationship with the type of organic matter source (TOC/N
ratios).
The group of bioindicator species for organic-enriched environment is composed of B. striatula, Bolivina spp., B. striatula, Bulimina
pupoides, B. elegantissima, C. crassa f. media, Fursenkoina pontoni and
P. atlanticum. The main abiotic variables that inuence the relative
abundance of this association are ne sediments (r = 0.72; p < 0.05)
and sulphur levels (r = 0.73; p < 0.001).
The morphometric analysis results, i.e., a predominance of
medium-sized shells with a signicant percentage of large-sized
shells, corroborate the environmental characteristics observed
for grain size, geochemical data, distribution patterns and benthic foraminifera species. Based on the fact that shell size can
reect the oxygenation level and organic matter ux (Phleger
and Soutar, 1973; Perez-Cruz and Machain-Castilho, 1990; Boltovskoy et al., 1991; Bernhard and Reimers, 1991; Diz et al.,
2006), it is possible to conclude that the area near the Saco
da Capela submarine outfall diffusers is well-oxygenated with
a favourable food supply (organic matter). Macroforaminifera

(shell size larger than 500 lm) were identied at 50% of the stations analysed.
6. Conclusions
By combining data from grain size and geochemical analyses, it
was possible to differentiate the types of environments where sewage submarine outfalls are located, as well as their efuent inuence on foraminifera assemblages.
The Ara submarine outfall (SSC continental side) is positioned
in a shallow environment with bottom circulation oscillating from
moderate to low. The oceanographic conditions and the diffusers
vicinity to the coastline contribute to the muddy sediments and
pollutants towards the inner part of the bay. The organic enrichment was denoted mainly by phosphorus and sulphur contents
and, to a lesser extent, by TOC values. TOC/S ratios indicated subenvironments with reducing signals and probable anaerobic organic matter degradation.
The Saco da Capela sewage submarine outfall (SSC insular side)
is placed in a high hydrodynamic environment. The constant
reworking of the sediments by bottom currents did not permit
preservation of either of the ne sedimentary fraction or organic
matter.
High P content found in both the Ara and Saco da Capela submarine environments indicates anthropic activities, which is associated with domestic efuent discharged.
Pearsons coefcients and the CCA demonstrated that the
foraminifera assemblage identied close to the Ara outfall has
been negatively inuenced by phosphorus and sulphur concentrations. Foraminifera were observed to have low density, richness
and specic diversity in stations with high phosphorus and sulphur
contents. The low oxygenation level is denoted by the predominance of detritivore species, which are associated in the literature
with higher organic matter ux, low oxygen in the interstitial pore
water and low bottom energy. The environmental stress near the
Ara outfall is inferred by dominance of a low number of species,
in this case A. tepida.
Close to the Saco da Capela submarine outfall, except for the
stations with high S content, the predominant species belong typically to environments with highly hydrodynamic conditions, welloxygenated bottom waters and low nutrient contents; there is no
evidence of environmental stress. Although A. tepida and G. praegeri were the most abundant species, a high number of rare species
was observed, indicating more environmental stability.
According to the results obtained, we inferred a harmful inuence on live benthic foraminifera due to continuous efuent discharged close to Ara. Close to the Saco da Capela diffusers,
until now environmental stress was not observed, which is linked
to the oceanographic conditions of the region where the diffusers
are positioned.
The sediment quality assessments obtained by geochemical and
foraminifera analysis indicate the need for improvements in the
current sewage treatment system.
Acknowledgements
This study have been supported by Fundao de Amparo Pesquisa do Estado de So Paulo (FAPESP, Brazilian agency). The
authors are grateful for assistance of the Isaac Jamil Sayeg (Scanning Electron Microscope Laboratory) and Sandra Andrade (Chemical and ICP-OES/MS Laboratory) Geoscience Institute of the
University of So Paulo. The authors would like to express sincere
thanks to Dr. Charles Sheppard and anonymous reviewers by suggestions and comments that improved this manuscript.
Appendix 1
1.1. Bioindicators species of organic-enriched environments
This group is composed for species dominant in the oxygendecient and organic rich environments, being that some species
are also associated to oxygen-minimum zone or in upwelling
zones. Despite the Bolivinids and Buliminids genera to be reported
in oxygenated environments (Debenay et al., 1997, 2001), these
genera burrow into oxygen-depleted layers may be able to survive
in anoxic conditions for even longer periods (Moodley and Hess,
1992). B. ordinaria (Hermelin and Shimmield, 1990; Martins
et al., 2007); B. striatula (Lutze and Coulbourn, 1984; Bernhard
and Sen Gupta, 1999; Martins et al., 2006); B. cf. sphatulata (Alavi,
1988; de Stigter et al., 1998; Martins et al., 2006); B. marginata
(Alavi, 1988; Alve and Bernhard, 1995; Bernhard and Sen Gupta,
1999; van der Zwaan and Jrissen, 1991; Burone and Pires-Vanin,
2006; Martins et al., 2006; Nagai et al., 2009), B. elegantissima
(Bernhard and Sen Gupta, 1999; Burone and Pires-Vanin, 2006);
P. atlanticum (Burone and Pires-Vanin, 2006; Nagai et al., 2009);
C. crassa f. media (Alavi, 1988; Bernhard and Sen Gupta, 1999), F.
pontoni (Bernhard and Sen Gupta, 1999); Trochammina spp.
(Schnfeld, 2002).
1.2. Bioindicators species of well-oxygenated environment
This group is composed for species frequently observed in welloxygenated bottom waters, high hydrodynamic and low nutrients
contents, such as G. praegeri (Altenbach et al., 2003; Duleba et al.,
2005; Martins et al., 2006), D. williamsoni (Nagai et al., 2009; Murray, 1991; Linke and Lutze, 1993); H. boueana (Barmawidjaja et al.,
1995 [as Hanzawaia concentrica]; Duleba et al., 2005); L. lobatula
(Williamson, 1985); L. ochracea (Martins et al., 2006; Murray,
1991); Quinqueloculina spp. (Kaiho, 1994; Martins et al., 2006; Nagai et al., 2009); R. oridana (Martins et al., 2006; Duleba et al.,
2005; Murray, 1991); N. terquemi (Duleba et al., 2005; Murray,
1991), Patelina corrugata (Martins et al., 2006; Murray, 1991), Cibicides spp. (Kaiho, 1994; Altenbach et al., 2003 [as Cibicides gerthi];
Duleba et al., 2005).
Supplementary data
Appendices 2 and 3 associated with this manuscript can be
found in the supplementary data. Supplementary data associated
with this article can be found, in the online version, at
doi:10.1016/j.marpolbul.2009.11.011.
References
Abessa, D.M.S., Carr, R.S., Rachid, B.R.F., Sousa, E.C.P.M., Hortelani, M.A., Sarkis, J.E.,
2005. Inuence of a Brazilian sewage outfall on the toxicity and contamination
of adjacent sediments. Marine Pollution Bulletin 50, 875885.
Alavi, S.N., 1988. Late Holocene deep-sea benthic foraminifera from Sea of Marmara.
Marine Micropaleontology 13, 213237.
Altenbach, A.V., Lutze, G.F., Schiebel, R., Schnfeld, J., 2003. Impact of interrelated
and independent ecological controls on benthic foraminifera: an example from
the Gulf of Guinea. Palaeogeography, Palaeoclimatology, Palaeoecology 197,
213238.
Alve, E., 1991. Benthic foraminifera in sediment cores reclecting heavy metal
pollution in Srfjord, Western Norway. Journal of Foraminiferal Research 21, 1
19.
Alve, E., 1995. Benthic foraminiferal responses to estuarine pollution: A review.
Journal of Foraminiferal Research 25, 190203.
Alve, E., Bernhard, J.M., 1995. Vertical migratory response of benthic foraminifera to
controlled oxygen concentrations in an experimental mesocosm. Marine
Ecology-Progress Series 116, 137151.
Alve, E., Murray, J., 1999. Marginal marine environments of the Skagerrak and
Kattegat: a baseline study of living (stained) benthic foraminiferal ecology.
Palaeogeography, Palaeoclimatology, Palaeoecology 146, 171193.
Alve, E., Naggy, J., 1986. Estuarine foraminiferal distribution in Sandebukta a branch
of the Oslo Fjord. Journal of Foraminiferal Research 16, 261284.
551
Armynot du Chtelet, E., Debenay, J.P., Soulard, R., 2004. Foraminiferal proxies for
pollution monitoring in moderately polluted harbors. Environmental Pollution
127, 2740.
Armynot du Chtelet, E., Bout-Roumazeilles, V., Rboulleau, A., Trentesaux, A., 2008.
Sediment (grain size and clay mineralogy) and organic matter quality control on
living foraminifera. Revue de Micropalontologie 52, 7584.
Aston, S.R., Hewitt, C.N., 1977. Phosphorus and carbon distributions in a polluted
coastal environment. Estuarine and Coastal Marine Science 5, 243254.
Bader, R.G., 1955. Carbon and nitrogen relations in surface and subsurface marine
sediments. Geochimica Cosmochimica Acta 7, 205211.
Bandy, O.L., Ingle, J.C.J.R., Resig, J.M., 1964a. Foraminiferal trends, laguna Beach
Outfall area, California. Limnology and Oceanography 9, 112123.
Bandy, O.L., Ingle, J.C.J.R., Resig, J.M., 1964b. Foraminifera, Los Angeles county outfall
area, California. Limnology and Oceanography 9, 124137.
Bandy, O.L., Ingle, J.C.J.R., Resig, J.M., 1965. Foraminiferal trends, Hyperion outfall,
California. Limnology and Oceanography 10, 314332.
Barmawidjaja, D.M., van der Zwaan, G.J., Jrissen, F.J., Puskaric, S., 1995. 750 years of
eutrophication in the northern Adriatic Sea: evidence from a benthic
foraminiferal record. Marine Geology 122, 367384.
Baturin, G.N., 2003. Phosphorus cycle in the ocean. Lithology and Mineral Resources
38, 101119.
Bergin, F., Kucuksezgin, F., Uluturhan, E., Barut, I.F., Meric, E., Avsar, N., Nazik, A.,
2006. The response of benthic foraminifera and ostracoda to heavy metal
pollution in Gulf of Izmir (Easter Aegean Sea). Estuarine, Coastal and Shelf
Science 66, 368386.
Berner, R.A., 1989. Biogeochemical cycles of carbon and sulfur and the effect on
atmospheric over Phanerozoic time. Palaeogeography, Palaeoclimatology,
Palaeoecology 75, 97122.
Bernhard, J.M., Reimers, C.E., 1991. Benthic foraminiferal population uctuations
related to anoxia: Santa Barbara Basin. Biogeochemistry 15, 127149.
Bernhard, J.M., Sen Gupta, B.K., 1999. Foraminifera of oxygen-depleted
environments. In: Sen Gupta, B.K. (Ed.), Modern Foraminifera. Kluwer
Academic Publishers, pp. 201216.
Boltovskoy, E., Giussani, G., Watanabe, S., Wright, R., 1980. Atlas of benthic shelf
foraminifera of southwest Atlantic. Dr. W. Junk, Netherlands. 147pp..
Boltovskoy, E., Scott, D.B., Medioli, F.S., 1991. Morphological variations of benthic
foraminiferal testes in response to changes in ecological parameters: a review.
Journal of Paleontology 65, 175185.
Bordovskiy, O.K., 1965. Accumulation of organic matter in bottom sediments.
Marine Geology 3, 3382.
Borrego, J., Lopes, M., Pendon, J.G., Morales, J.A., 1998. C/S ratios is estuarine
sediments of the Odiel River-mouth, S.W. Spain. Journal of Coastal Research 14,
12761283.
Bradshaw, J.S., 1961. Laboratory experiments in the ecology of foraminifera.
Contributions from the Cushman Foundation for Foraminiferal Research 12,
87106.
Burone, L., Venturini, N., Sprechmann, P., Valente, P., Muniz, P., 2006. Foraminiferal
responses to polluted sediments in the Montevideo coastal zone, Uruguay.
Marine Pollution Bulletin 52, 6173.
Burone, L., Pires-Vanin, A.M.S., 2006. Foraminiferal assemblages in Ubatuba Bay,
south-eastern Brazilian coast. Scientia Matina 70, 203217.
Carreira, R.S., Wagener, A.L.R., 1998. Speciation of sewage derived phosphorus in
coastal sediments from Rio de Janeiro, Brazil. Marine Pollution Bulletin 36, 818
827.
Cearreta, A., Irabien, M.J., Leorri, E., Yusta, I., Quintanilha, A., Zabaleta, A., 2002.
Environmental transformation of the Bilbao estuary, N. Spain: microfaunal and
geochemical proxies in the recent sedimentary record. Marine Pollution
Bulletin 44, 487503.
Cesar, A., Choueri, R.B., Riba, I., Moralles-Caselles, C., Pereira, C.D.S., Santos, A.R.,
Abessa, D.M.S., DelValls, T.A., 2007. Comparative sediment quality assessment
in different littoral ecosystems from Spain (Gulf of Cadiz) and Brazil (Santos
and So Vicente estuarine systems). Environmental International 33, 429
435.
Cognetti, G., 1992. Colonization of stressed coastal environments. Marine Pollution
Bulletin 24, 247250.
Companhia de Tecnologia de Saneamento Ambiental (Cetesb), 2007. Relatrio de
monitoramento de emissrio submarino. Secretaria de Estado do Meio
Ambiente, Srie Relatrio. 116pp..
Debenay, J. P., Andre, O., Bezie, S., Rambaud, S., 1997. Foraminifers used as
bioindicators in La Turballe harbor (Loire Atlantique, France). Coastal zone
monitoring and medium to long term forecasting. In: FrenchJapanese
International Symposium, Paris, October 68 (Abstracts).
Debenay, J.P., Duleba, W., Bonetti, C., Melo e Souza, S.H., Eichler, B., 2001. Pararotalia
cananeiaensis N. SP.: indicator of marine inuence and water circulation in
Brazilian coast and paralic environments. Journal of Foraminiferal Research 31,
152163.
de Stigter, H.C., Jrissen, E.J., van der Zwaan, G.J., 1998. Bathymetric distribution and
microhabitat portioning of live (Rose Bengal stained) benthic foraminifera along
a shelf to bathial transect in the southern Adriatic Sea. Journal of Foraminiferal
Research 28, 4065.
Diz, P., Francs, G., Costas, S., Souto, C., Alejo, I., 2004. Distribution of benthic
foraminfera in coarse sediments, Ra de Vigo, NW Iberian Margin. Journal of
Foraminiferal Research 34, 258275.
Diz, P., Francs, G., Rosn, G., 2006. Effects of contrasting upwellingdownwelling
on benthic foraminiferal distribution in the Ra de Vigo (NW Spain). Journal of
Marine Systems 60, 118.
552
Duleba, W., Debenay, J.P., 2003. Hydrodynamic circulation in the estuaries of

estao ecolgica Juria-Itatins, Brazil, inferred from foraminifera and
thecamoebian assemblages. Journal of Foraminiferal Research 33, 6293.
Duleba, W., Coimbra, J.C., Petri, S., Barbosa, C.F., 2005. Foraminferos tecamebase
ostracodes recentes utilizados como bioindicadores em estudos ambientais
brasileiros. In: Sousa, C.R.G., Suguio, K., Santos, M., Oliveira, P.E. (Eds.),
Quaternrio do Brasil. ABEQUA. Editora Holos, Ribeiro Preto, pp. 176
201.
Emmeis, K.C., Struck, U., Leipe, T., Pollehne, F., Kunzendorf, H., Christiansen, C., 2000.
Changes in the C, N, P burial rates in some Baltic Sea sediments over the last 150
years-relevance to P regeneration rates and the phosphorus cycle. Marine
Geology 167, 4359.
Faganelli, J., Malej, A., Pezdic, J., Malacic, V., 1988. C:N:P ratios and stable C isotopic
ratios as indicator of sources of organic matter in the Gulf of Trieste (northern
Adriatic). Oceanologia Acta 11, 377382.
Ferraro, L., SprovieriI, M., Alberico, I., Lirer, F., Prevedello, L., Marsella, E., 2006.
Benthic foraminifera and heavy metals distribution: a case study from de
Naples Harbour (Tyrrhenian Sea, Southern Italy). Environmental Pollution 142,
274287.
Frontalini, F., Coccioni, R., 2008. Benthic foraminiferal for heavy metal pollution
monitoring: A case study from the central Adriatic Sea coast of Italy. Estuarine
Coastal and Shelf Science 76, 404417.
Furtado, V.V., Barcellos, R.L., Conti, L.A., Rodrigues, M., Mahiques, M.M., 2008.
Sedimentao. In: Pires-Vanin, A.M. (Ed.), Oceanograa de um ecossistema
subtropical: Plataforma de So Sebastio, SP. Editora da Universidade de So
Paulo (EDUSP), pp. 141180.
Gchter, R., Meyer, J.S., 1993. The role of microorganisms in mobilization and
xation of phosphorus in sediments. Hydrobiology 253, 103121.
Gauch, H.G., 1982. Multivariate analysis in community ecology. Cambridge
University Press, Cambridge.
Gross, M.G., 1971. Carbon determination. In: Carver, R.E. (Ed.), Procedures in
Sedimentary Petrology. Wiley, New York, pp. 573596.
Gustafsson, M., Nordberg, K., 2000. Living (Stained) benthic foraminifera and their
response to the seasonal hydrographic cycle, periodic hypoxia and to primary
production in Havstens fjord on the Swedish West Coast. Estuarine, Coastal and
Shelf Science 51, 743761.
Hendrix, W.E., 1958. Foraminiferal shell form, a key to sedimentary environment.
Journal of Paleontology 32, 649660.
Hermelin, J.O.R., Shimmield, G.B., 1990. The importance of the oxygen minimum
zone and sediment geochemistry in the distribution of recent benthic
foraminifera in the northwest Indian Ocean. Marine Geology 91, 129.
Horton, B.P., Edwards, R.J., Lloyd, J.M., 1999. UK intertidal foraminiferal
distributions: implications for sea-level studies. Marine Micropaleontology
36, 205223.
Jorissen, F.J., 1999. Benthic foraminiferal microhabitats below the sedimentwater
interface. In: Sen Gupta, B.K. (Ed.), Modern Foraminifera. Kluwer Academic
Publishers, Dordrecht, pp. 161179.
Jorissen, F.J., Stigeter, H.C., Widmark, J.G.V., 1995. A conceptual model explaining
benthic foraminiferal microhabitats. Marine Micropaleontology 26, 315.
Kaiho, K., 1994. Benthic foraminiferal dissolved-oxygen index and dissolved-oxygen
levels in the modern ocean. Geology 22, 719722.
Kitazato, H., 1994. Foraminiferal microhabitats in four marine environments around
Japan. Marine Micropaleontology 24, 2941.
Lamparelli, C.C., 2007. Commissioning and monitoring challenges regarding ocean
outfalls: So Paulo State experience. In: Lamparelli, C.C., Ortiz, J.P. (Eds.),
Submarine Outfalls: Design, Compliance and Environmental Monitoring.
Secretaria do Meio ambiente, So Paulo, pp. 1123.
Larssoneur, C., Bouysse, P., Aufret, J.P., 1982. The supercial sediments of The
English Channel and its western approach. Sedimentology 19, 851864.
Le Cadre, V., Debenay, J.P., 2006. Morphological and cytological responses of
Ammonia (foraminifera) to cooper contamination: Implications for the use of
foraminifera as bioindicators of pollution. Environmental Pollution 143, 304
317.
Legg, J.O., Black, C.A., 1955. Determination of organic phosphorus in soils: II. Ignition
method. Soil Science Society of America Proceedings 19, 139143.
Leventhal, J.S., 1982. An interpretation of carbon and sulfur relationships in Black
Sea sediments as indicators of environments of deposition. Geochimica et
Cosmochimica Acta 47, 133137.
Linke, P., Lutze, G.F., 1993. Microhabitat preferences of benthic foraminfera a
static concept or a dynamic adaptation to optimize food acquisition? Marine
Micropaleontology 20, 215234.
Lutze, G.F., Coulbourn, W.T., 1984. Recent benthic foraminifera from the continental
margin of Northwest Africa: community structure and distribution. Marine
Micropaleontology 8, 361401.
Lyons, T.W., Berner, R.A., 1992. Carbonsulfuriron systematics of the uppermost
deep-water sediments of the Black Sea. Chemical Geology 99, 127.
Marins, R.V., Paula Filho, F.J., Rocha, C.A.S., 2007. Geoqumica do fsforo como
indicadora da qualidade ambiental e dos processos estuarinos do Rio Jaguaribe
Costa nordeste oriental brasileira. Qumica Nova 30, 12081214.
Martins, V., Jouanneau, J.-M., Weber, O., Rocha, F., 2006. Tracing the late Holocene
evolution of the NW Iberian upwelling system. Marine Micropaleontology 59,
3555.
Martins, V., Dubert, J., Jouanneau, J.-M., Weber, O., Silva, E.F., Patinha, C., Dias, J.M.A.,
Rocha, F., 2007. A multiproxy approach of the Holocene evolution of shelfslope circulation on the NW Iberian Continental Shelf. Marine Geology 239,
118.
McGann, M., Alexander, C.R., Bay, S.M., 2003. Response of benthic foraminifers to
sewage discharge and remediation in Santa Monica Bay, California. Marine
Environmental Research 56, 299342.
Miranda, L.B., Castro Filho, B.M., 1995. Variabilidade da circulao e do transporte
de volume no Canal de So Sebastio (SP). Publicao especial do Instituto
Oceanogrco 11, 19.
Mojtahid, M., Jorissen, F., Pearson, T.H., 2008. Comparison of benthic foraminiferal
and macrofaunal responses to organic pollution in the Firth of Clyde (Scotland).
Marine Pollution Bulletin 56, 4276.
Moodley, L., Hess, C., 1992. Tolerance of infaunal benthic foraminfera for low and
high oxygen concentrations. Biological Bulletin 183, 9498.
Morse, J.W., Berner, R.A., 1995. What determines sedimentary C/S ratios?
Geochimica et Cosmochimica Acta 59, 10731077.
Murray, J.W., 1991. Ecology and Paleoecology of Benthic Foraminifera. Longman
Scientic and Technical, London. 397pp.
Murray, J.W., 2001. The niche of benthic foraminifera, critical thresholds and
proxies. Marine Micropaleontology 41, 17.
Murray, J.W., 2003. Foraminiferal assemblage formation in depositional sinks on the
continental shelf west of Scotland. Journal of Foraminiferal Research 33, 101
121.
Nagai, R.H., Sousa, S.H.M., Burone, L., Mahiques, M.M., 2009. Paleoproductivity
changes during the Holocene in the inner shelf of Cabo Frio, southeaster
Brazilian continental margin: benthic foraminifera and sedimentological
proxies. Quaternary International 206, 6271.
Nagy, J., Alve, E., 1987. Temporal changes in foraminiferal faunas and impact of
pollution in Sandebukta, Oslo fjord. Marine Micropaleontology 12, 109128.
Ozrio, V.K.L., Oliveira, W., 2001. Polifosfatos em detergentes em p comerciais.
Qumica Nova 24, 700708.
Perez-Cruz, L.L., Machain-Castilho, M.L., 1990. Benthic foraminfera of the oxygen
minimum zone, continental shelf of the Gulf of Tehuantepec, Mxico. Journal of
Phleger, F.B., Soutar, A., 1973. Production of benthic foraminifera in three east
Pacic oxygen minima. Micropaleontology 19, 110115.
Pielou, E.C., 1969. The measurement of diversity in different types of biological
collections. Journal of Theoretical Biology 13, 131144.
Raiswell, R., Buckley, F., Berner, R.A., Anderson, T.F., 1987. Degree of pyritization of
iron as a palaeoenvironmental indicator of bottom-water oxygenation. Journal
of Sedimentary Petrology 58, 812819.
Riley, J.P., Chester, R., 1976. Chemical Oceanography. Academic Press Inc. Ltd.,
London. 414pp..
Rosenberg, R., Elmgre, R., Fleisher, S., Jonsson, P., Persson, G., Dahlin, H., 1990.
Marine eutrophication case studies in Sweden. Ambio 19, 102108.
Ruiz-Fernandez, A.C., Hillaire-Marcel, C., Ghaleb, B., Soto-Jimnez, Paez.-Osuna, F.,
2002. Recent sedimentary history of anthropogenic impacts on the Culiacan
River Estuary, northwestern Mxico: geochemical evidence from organic matter
and nutrients. Environmental Pollution 118, 365377.
Ruttenberg, K.C., Goni, M.A., 1997. Phosphorus distribution, C:N:P: ratios, and d13Coc
in artic, temperate, and tropical coastal sediments: tools for characterizing bulk
sedimentary organic matter. Marine Geology 139, 123145.
Samir, A.M., El-Din, A.B., 2001. Benthic foraminiferal assemblages and
morphological abnormalities as pollution proxies in two Egyptian bays.
Marine Micropaleontology 41, 193227.
Sampei, Y., Matsumoto, E., 2001. C/N ratios in a sediment core from Nakaumi
Lagoon, southwest Japan-usefulness as an organic source indicator.
Geochemical Journal 35, 189205.
Scanes, P., 2007. Monitoring environmental impact of ocean disposal of sewage. In:
Lamparelli, C.C., Ortiz, J.P. (Eds.), Submarine Outfalls: Design, Compliance and
Environmental Monitoring. Secretaria do Meio ambiente, So Paulo, pp. 119
130.
Schafer, C.T., Winters, G.V., Scott, D.B., Pocklington, P., Cole, F.E., Honig, C., 1995.
Survey of living foraminifera and polychaete populations at some Canadian
aquaculture sites: potential for impact mapping and monitoring. Journal of
Schnfeld, J., 2002. Recent benthic foraminiferal in deep high-energy environments
from the Gulf of Cadiz (Spain). Marine Micropaleontology 44, 141162.
Setty, M.G.A.P., Nigan, R., 1982. Foraminiferal assemblages and organic carbon
relationship in benthic marine ecosystem of wester Indian continental shelf.
Indian Journal of Marine Sciences 11, 225232.
Shannon, C.E., Weaver, W., 1948. The Mathematical Theory of Communication.
University of Illinois Press, Urbana.
Stein, R., 1991. Accumulation of organic carbon in marine sediments. Results from
the Deep Sea Drilling Project/Ocean Drilling Program. In: Bhattacharji, S.,
Friedman, G.M., Neugebauer, H.J., Seilacher, A. (Eds.), Lecture Notes in Earth
Sciences. Springer, Berlin, p. 17pp..
Suguio, K., 1973. Introduo Sedimentologia. Ed. Edgard Blcher/EDUSP, So
Paulo. 317pp..
ter Braak, C.J.F., 1994. Canonical community ordination. Part I: Basic theory and
linear methods. Ecoscience 1, 127140.
ter Braak, C.J.F., Smilauer, P., 2002. CANOCO Reference Manual and Users Guide to
Canoco for Windows: Software for Canonical Community Ordination. Verso
4.5. Microcomputer Power, Ithaca, NY. 500pp..
Turekian, K.K., Wedepohl, K.H., 1961. Distribution of the Elements in some major
units of the Earths crust. Geological Society of America Bulletin 72, 175.
Twichell, S.C., Meyers, P.A., Diester-Haass, L., 2002. Signicance of high C/N ratios in
organic-carbon-rich Neogene sediments under the Benguela Current upwelling
system. Organic Geochemistry 33, 715722.

van der Zwaan, G.J., Duijnstee, I.A.P., den Dulk, M., Ernest, S.R., Jannink, N.T.,
Kouwenhoven, T.J., 1999. Benthic foraminifers: proxies or problems? A review
of paleoecological concepts. Earth Science Reviews 46, 213236.
van der Zwaan, G.J., Jrissen, F.J., 1991. Biofacial patterns in river-induced shelf
anoxia. In: Tyson, R.V., Pearson, T.H. (Eds.), Modern and Ancient Continental
Shelf Anoxia, vol. 58. Geological Society, London, pp. 6582 (Special Publication).
Vilella, C.G., Batista, D.S., Baptista-Neto, J.A., Crapez, M., Mcallister, J.J., 2004. Benthic
foraminfera distribution in high polluted sediments from Niteri Harbor
(Guanabara Bay), Rio de Janeiro, Brazil. Annals of the Brazilian Academy of
Sciences 76, 161171.
Walton, W.R., 1952. Techniques for recognition of living foraminifera. Contribution
of Cushman Foundation for Foraminiferal Research 3, 5660.
553
Watkins, J.G., 1961. Foraminiferal ecology around the Orange County, California,
ocean sewer outfall. Micropaleontology 7, 199206.
Wentworth, C.K., 1922. A scale of grade and class terms for clastics sediments.
Journal of Geology 30, 377392.
Werme, C., Hunt, C.D., 2004. Outfall Monitoring Overview. Massachusetts Water
Resources Authority, Boston. Report 13. pp. 97.
Williamson, M.A., 1985. Recent foraminiferal diversity on the continental margin off
Nova Scotia, Canada. Journal of Foraminiferal Research 15, 4351.
Yanko, V., Kronfeld, J., Flexer, A., 1994. Response of benthic foraminifera to various
pollution sources: implications for pollution monitoring. Journal of

Caracterização Ambiental

Enviado por

Dados do documento

Descrição original:

Título original

Direitos autorais

Formatos disponíveis

Compartilhar este documento

Compartilhar ou incorporar documento

Opções de compartilhamento

Você considera este documento útil?

Este conteúdo é inapropriado?

Direitos autorais:

Formatos disponíveis

Caracterização Ambiental

Enviado por

Direitos autorais:

Formatos disponíveis

Marine Pollution Bulletin 60 (2010) 536553

Contents lists available at ScienceDirect

Marine Pollution Bulletin

Analysis of foraminifera assemblages and sediment geochemical properties

* Corresponding author. Tel.: +55 11 30911988.

A.C. Teodoro et al. / Marine Pollution Bulletin 60 (2010) 536553

Fig. 1. Studies area and sampling grid.

The SSC is about 25 km long with two large entrances, 67 km

Centro Sul DTCS) and oceanic disposal of domestic sewage by

3. Materials and methods

A.C. Teodoro et al. / Marine Pollution Bulletin 60 (2010) 536553

and equitability (J) was calculated according to the Pielou index

A.C. Teodoro et al. / Marine Pollution Bulletin 60 (2010) 536553

Sediment mean grain ranged from 1.81U to 4.12U, and grain

The C/S ratios oscillated from 0.8 to 19.9.

A.C. Teodoro et al. / Marine Pollution Bulletin 60 (2010) 536553

The temperature and salinity values in the bottom water ranged

Sediment mean grain ranged from 0.39U to 3.94U, and grain

A.C. Teodoro et al. / Marine Pollution Bulletin 60 (2010) 536553

sand. The percentages of sandy sediments ranged from 53.2% to

A.C. Teodoro et al. / Marine Pollution Bulletin 60 (2010) 536553

to 25.28% (average 14.5%). Granules occurred only at stations Sc2,

A.C. Teodoro et al. / Marine Pollution Bulletin 60 (2010) 536553

The S content ranged from 0.003% to 0.163% (average

of foraminifera shells (Fig. 5). The percentage of small shells ranged

A.C. Teodoro et al. / Marine Pollution Bulletin 60 (2010) 536553

Fig. 6. Ordination diagram of species-environment relation.

Cumulative percentage variance

(Lutze and Coulbourn, 1984; Martins et al., 2006). The distributions

size and salinity are the most important environmental variables

A.C. Teodoro et al. / Marine Pollution Bulletin 60 (2010) 536553

ows at a rate of 140 L s1. These regions presented the highest

A.C. Teodoro et al. / Marine Pollution Bulletin 60 (2010) 536553

A.C. Teodoro et al. / Marine Pollution Bulletin 60 (2010) 536553

that both elements have a common and allochthonous source, i.e.,

5.1.2. Live benthic foraminifera: species composition, distribution and

A.C. Teodoro et al. / Marine Pollution Bulletin 60 (2010) 536553

factor that really controls the composition and distribution pattern

A.C. Teodoro et al. / Marine Pollution Bulletin 60 (2010) 536553

terquemi, R. oridana, Quinqueloculina milletti, Lepidoteuramina

Due to oceanographic conditions of the study area, i.e., coarser

A.C. Teodoro et al. / Marine Pollution Bulletin 60 (2010) 536553

is a low number of benthic foraminifera, whereas high density is

a favourable food supply (organic matter). Macroforaminifera

A.C. Teodoro et al. / Marine Pollution Bulletin 60 (2010) 536553

A.C. Teodoro et al. / Marine Pollution Bulletin 60 (2010) 536553

Duleba, W., Debenay, J.P., 2003. Hydrodynamic circulation in the estuaries of

A.C. Teodoro et al. / Marine Pollution Bulletin 60 (2010) 536553

Você também pode gostar