Environmental Science and Pollution Research

https://doi.org/10.1007/s11356-018-3338-7

RESEARCH ARTICLE

Spatial variability and seasonal toxicity of dredged sediments

from Guanabara Bay (Rio de Janeiro, Brazil): acute effects
on earthworms
Christiane Monte 1,2 & Ricardo Cesar 3 & Ana Paula Rodrigues 1 & Danielle Siqueira 3 & Aline Serrano 3 & Leticia Abreu 3 &
Matheus Teixeira 3 & Mariana Vezzone 3,4 & Helena Polivanov 4 & Zuleica Castilhos 5 & Tácio de Campos 6 &
Glaucia G. M. Machado 7 & Weber F. Souza 7 & Wilson Machado 1

Received: 26 March 2018 / Accepted: 26 September 2018

# Springer-Verlag GmbH Germany, part of Springer Nature 2018

Abstract
The toxicity of dredged sediments from Guanabara Bay (Rio de Janeiro, Brazil) was evaluated using acute bioassays with Eisenia
andrei and metal determination. The sediments were collected in August 2014 (winter) and February 2015 (summer) and in five areas
distributed along the Bay: Port of Rio de Janeiro, Port of Niterói, Meriti River mouth, Iguaçu River mouth, and the Environmental
Protection Area (APA) of Guapimirim. The sediments were mixed with a ferralsol (a representative Brazilian tropical soil) in proportions
varying between 0 (pure soil) and 30%. The acute bioassays with E. andrei followed a standard protocol (ISO 11268-2:2012). Total
metal determination in the sediments was performed by ICP-OES. The medium lethal earthworm concentration (LC50) was estimated
through PriProbit analysis. The sediments from the APA of Guapimirim, which is a control area at the Guanabara Bay, were the only
ones whose total metal concentrations were in agreement with the limits established by Brazilian law for land disposal of dredged
sediments. However, the sediments collected in the APA of Guapimirim were the most toxic ones among the study areas due to very
high contents of salts in these materials. Winter sediments were generally more toxic compared to the summer ones due to the increase of
metal concentrations and salt precipitation to bottom sediments during the winter. The exceptions were (i) the sediments from APA of
Guapimirim, where the toxicity in the summer (LC50 = 3.99%) and winter (LC50 = 4.60%) were relatively similar to each other, since
the toxicity is linked to salt in excess; and (ii) the Iguaçu River mouth, where the presence of mangrove areas might be associated with
the filtering of pollution sources (winter LC50 = 12.67%; summer LC50 = 11.58%). In the Port of Rio de Janeiro, LC50 obtained in the
winter (7.30%) was almost three times lower than that found in the summer (19.64%). The sediments from Meriti River mouth showed
the highest total metal concentrations, were the most toxic sediments among the study areas (excluding the APA of Guapimirim), and its
winter LC50 (6.64%) was almost twice lower than that obtained in the summer (12.55%). By following the same tendency, summer
LC50 (17.52%) found for the sediment collected in the Port of Niterói was also higher than the value found in the winter (12.34%).
Finally, the dredged sediments from Guanabara Bay were toxic to earthworms in mixtures with pure ferralsol and winter samples were
generally more toxic than the summer ones, in agreement with the increase of metal and salt concentrations during the winter.

Keywords Guanabara Bay . Metal . Ferralsol . Eisenia andrei . Bioassay

Responsible editor: Philippe Garrigues

* Christiane Monte
christiane.monte@yahoo.com.br
1
UFF, Department of Geochemistry, Fluminense Federal University,
Outeiro São João Baptista, s/n. Centro, Niterói, RJ, Brazil
2
UFOPA, Department of Geology, Federal University of Western
Pará, Av. Vera Paz, s/n. Salé, Santarém, PA, Brazil
3 7
UFRJ, CCMN–Geosciences Institute. Department of Geography,
Federal University of Rio de Janeiro, Av. Athos da Silveira Ramos,
274–Cidade Universitária, Rio de Janeiro, RJ, Brazil
4
UFRJ. CCMN–Geosciences Institute. Department of Geology,
Federal University of Rio de Janeiro, Av. Athos da Silveira Ramos,
274–Cidade Universitária, Rio de Janeiro, RJ, Brazil
5
Centre for Mineral Technology, CETEM/MCTI, Av. Pedro Calmon,
900. Cidade Universitária, Rio de Janeiro, RJ, Brazil
6
PUC-Rio, Department of Civil Engineering, Pontifical Catholic
University of Rio de Janeiro, Rua Marquês de São Vicente 225/
301-L, Gávea, Rio de Janeiro, RJ 22453-900, Brazil
National Institute of Technology, INT. Analytical Chemistry
Division, Av. Venezuela, 82, sala 210, Praça Mauá, Rio de
Janeiro, RJ 20081-312, Brazil

Introduction
Estuarine and fluvial systems from South American countries
have been impacted with domestic wastes and industrial ac-
tivities due to the expansion of urban areas and surge in agri-
culture activities. Most of these environments are silted, eu-
trophic, and highly contaminated with metals, petroleum hy-
drocarbons, and other organic substances (Machado et al.
2011; Cesar et al. 2014). Due to this reality, the dreading of
bottom sediments has become a common practice, and the use
of these materials as soil amendments in the agriculture, beach
nourishments, and expansion of wetlands is also frequent (Ho
et al. 2002; Munns et al. 2002; Vacha et al. 2011). However,
the presence of contaminants in these materials can cause
adverse effects on soil biota and should be carefully monitored
by using bioassays with ecologically representative soil organ-
isms (Cesar et al. 2014, 2017). In addition, the Brazilian law
for disposal of dredged sediments (CONAMA 454/ 2012 and
CONAMA 420/ 2009) is based on values idealized for tem-
perate ecosystems which do not reflect the characteristics of
tropical environments.
The earthworms are extensively used in bioassays due to
their abundance in tropical and temperate soils and their
important role in the soil food web. Besides that, they gen-
erally represent about 90% of soil biomass, consume large
amounts of soil, and are sensitive to the presence of xenobi-
otics (Sivakumar 2015; Usmani and Kumar 2015). The acute
bioassay with Eisenia andrei earthworms made part of ring-
test to determine the toxicity of three representative wastes.
The bioassays were performed by different European labo-
ratories and showed that this assay is a sufficiently robust
method to detect potentially toxic agents to edaphic fauna
(Moser and Römbke 2009). Cesar et al. (2014, 2017) also
used this acute assay to characterize the toxicity of dredged
sediments from Guanabara and Sepetiba bays (Rio de
Janeiro State, Brazil) and showed that such assay was sensi-
tive and adequate for a preliminary ecotoxicological
evaluation.
Over the last decades, the Guanabara Bay (Rio de Janeiro
State, Brazil) has been impacted by the discharge of indus-
trial and domestic wastes, and its bottom sediments, water,
and biota are highly contaminated with metals, organic sub-
stances, and fecal pathogens (Silva et al. 2007; Silveira et al.
2011; Rodrigues et al. 2011; Machado et al. 2011; Cesar et
al. 2014). The dredging of the sediments from the Guanabara
Bay is urgent to improve water circulation, navigation activ-
ities (mainly in Port areas), and especially to remediate
the ecosystems affected by pollution events. Furthermore,
the ecotoxicological evaluation of dredged sediments
Guanabara Bay could be used as good general model to
support the establishment of standard and sustainable values
for land disposal of polluted estuarine sediments in tropical
regions.
Environ Sci Pollut Res
This work aimed to evaluate spatial variability and seasonal
toxicity of dredged sediments from the Guanabara Bay. To
achieve to this purpose, dredged sediments were mixed with
a ferralsol sample (a representative tropical soil class) to pre-
pare gradients of sediment doses to be used in acute bioassays
with Eisenia andrei. Total and partial metal concentrations
were also determined in the sediments to support the interpre-
tation of ecotoxicological data. Our working hypotheses are:
(i) metal concentrations and the toxicity levels during the win-
ter are higher than those found in the summer; (ii) the earth-
worms are able to utilize the organic matter from domestic
wastes as potential food source.
Materials and methods
Samples
In September/2014 (winter) and March/2015 (summer),
samples of dredged sediment were collected at four points
along critical areas of contamination from Guanabara
Bay (Rio de Janeiro State, RJ, Brazil): Port of Niterói, Port
of Rio de Janeiro, Meriti River mouth, and Iguaçu River
mouth (Fig. 1). In addition, a sampling point at the
Environmental Protection Area (APA) of Guapimirim was
chosen as a reference of environmental quality, since it is the
most preserved area in the Guanabara Bay (Monteiro et al.
2011). Three samples were collected for each sampling
point and they were mixed to obtain a more representative
composite sample for each locality. The sediment samples
were dried at < 40 °C and, after that, mixed, homogenized,
and grounded.
Ferralsol was collected at the B horizon at the Duque de
Caxias Municipality (Rio de Janeiro State; 220 41′ 34.2″ S,
43° 17′ 14.5″W). The sample was dried at 25 °C and sieved
(2.0 mm) to remove roots and other large particles. Physical,
chemical, and mineralogical properties of this ferralsol were
previously determined by Cesar et al. (2014) and Alamino et
al. (2007) and are shown in the Table 1. Ferralsols are typically
acidic soils, contain high concentrations of iron and alumi-
num, low contents of nutrients (low natural fertility), and its
clay mineralogy is essentially composed by kaolinite,
gibbsite, and goethite. Ferralsols are geographically well-
distributed in tropical regions and are the most abundant soil
class in Brazil, where they are widely used in agriculture
practices.
Grain size and chemical characterization
The grain size of the sediment samples was determined
using approximately 1 g of wet sample added to a 50-mL
polypropylene tube with 40 mL of dispersant (sodium
hexametaphosphate 40 g L−1) and stirred during 24 h. After
Environ Sci Pollut Res

Fig. 1 Sampling points of dredged sediments at the Guanabara Bay (Rio de Janeiro, Brazil). PR = Port of Rio de Janeiro; PN = Port of Niterói; ME =
Meriti River mouth; IG = Iguaçu River Mouth; GUA = Environmental Protection Area (APA) of Guapimirim

stirring, the grain size was determined in a particle analyzer by

laser diffraction CILAS Shimadzu, model 1064, and the re-
Table 1 Physical and chemical properties of the ferralsol sample used in sults were calculated using the software GRADSTAT 1.0. The
bioassays. Data are taken from Alamino et al. (2007) and Cesar et al. (2012)
electric conductivity and pH (in water) of the dredged sedi-
Soil parameters Ferralsol ments were measured according to EMBRAPA ( 1997). The
organic carbon content (TOC) of the dredged sediments was
Texture Clay 58 determined by elementary analysis, using LECO SNS-2000
(%, n = 3) Silt 6 equipment.
Sand 36
pH (n = 3) H2O 4.2 Total metal determination
KCl 3.6
Sorption complex Mg+2 + Ca+ 0.2 Total concentration of iron (Fe), aluminum (Al), arsenic (As),
(cmolc/dm3, n = 3) 2
zinc (Zn), copper (Cu), lead (Pb), nickel (Ni), chromium (Cr),
K+ 0.02
and cadmium (Cd) in sediments was determined with 1 g of
Na+ 0.03
sample and addition of 40 mL of an acid solution composed of
CEC 2.3
2HF/HNO3/HClO4. The concentration of metals in soil ex-
Total concentrations Al 26.4
(%, n = 3) tracts was determined by inductively coupled plasma-optical
Fe 11.3
emission spectrometry (ICP-OES; Horiba Jobin Yvon, Ultima
Organic matter 0.22
(%, n = 3)
2). Total Hg concentrations were obtained from 0.5 g of sam-
ple using LUMEX equipment (RA-915+, Zeeman mercury
CEC cation exchange capacity spectrometer).

Metal geochemical fractioning
Additionally, to support the understanding of metal bioavail-
ability levels in the sediment samples, two acid weak extrac-
tions were performed: (F1–geochemical phase 1) ~ 1 g of dry
sample was stirred in 40 mL of 0.11 M acetic acid solution
during 16 h, and (F2–geochemical phase 2) ~ 1.5 g of dry
sample was stirred in 40 mL of 1 M hydrochloric acid solution
during 16 h. These two extractions were chosen to represent
the reactive/exchangeable geochemical phase, besides being
largely used in literature to determine potentially bioavailable
fractions of metals in coastal sediments (Monte et al. 2015;
Peña-Icart et al. 2014; Machado et al. 2011). The concentra-
tions of Cd, Cr, Cu, Fe, Pb, Ni, and Zn were determined using
a flame atomic absorption spectrometry (FAAS; Varian, mod-
el AA280FS). The contents of Al, As and Hg were not deter-
mined in those reactive geochemical phases. The detection
limits obtained for the three extraction methods are presented
on Table 2.
Given the fact that F1 is widely recognized as being a
weaker extraction compared to F2 one (Monte et al. 2015;
Peña-Icart et al. 2014; Machado et al. 2011), the geochemical
phase 3 (F3) was obtained through the subtraction between
total metal concentration and the concentration found in the
F2 extraction. In this case, F3 represents metal phases bound
to geochemical supports, such as organic matter, sulfides, or
Fe and Al oxyhydroxydes, whose bioavailability is generally
much lower compared to F2 extraction and especially com-
pared to F1.
Geoaccumulation index (IGEO) and metal-enrichment
factors
Total concentrations of metals and arsenic determined in the
dredged sediment were used to calculate the Geoaccumulation
index (IGEO) and metal-enrichment factors. The IGEO is a
logarithmic scale that allows classifying the sample by com-
paring the concentration obtained in the field with that deter-
mined for a regional geochemical background (Eq. 1) (Müller
1979). The background values were preferentially obtained
from the base of a sediment core from the APA of
Guapimirim dated from 1872, before representative inputs of
domestic and industrial wastes to the Guanabara Bay
(Monteiro et al. 2011). When the regional background was
not available for a specific metal, background values deter-
mined in the standard shale (Turekian and Wedepohl 1961)
were used. When such background values are used, a factor of
2.5 must be included in the equation to reduce regional differ-
ences (Müller 1979). The IGEO allows the categorization in
different classes of pollution varying between 0 (practically
non-polluted) and 6 (very strongly polluted).
IGEO ¼ Log2 Me=2:5* NBN Me ð1Þ
Environ Sci Pollut Res
where Me is the metal concentration in the sediment and
NBNMe is the metal background value. The background values
were obtained from the sediment core studied by Monteiro et
al. (2011), except for As, Cd, Cr, and Hg for which the back-
grounds determined in the standard shale were used (Zn =
70.2 mg/kg; Cu = 2.7 mg/kg; Pb = 14.9 mg/kg; Ni = 8.3 mg/
kg; Cr = 90 mg/kg; Hg = 0.04 mg/kg; As = 13 mg/kg; Cd =
0.25 mg/kg).
Metal-enrichment factors (EF) are used to evaluate contam-
ination levels associated with anthropic inputs of metals in
sediments. The identification of possible anthropic anomalies
is performed by normalizing metal concentrations (obtained in
the field and background concentrations) in relation to an el-
ement whose behavior is conservative and the source is pre-
dominantly lithogenic, such as Al, Fe, or Sc (Szafer et al.
1996). After normalizing the data according to the Eq. 2, when
the ratio between the normalized concentrations exceeds two
units, one could suppose that the anthropic contributions of a
specific metal in the sediment are representative. Iron back-
ground concentration (4.2%) was obtained in the base of the
sediment core studied by Monteiro et al. (2011) and was used
to normalize metal background values (the same ones used for
calculating IGEO).
ðM i =FeÞamostra
FE ¼ ð2Þ
ðM i =FeÞbackground
where: Mi = metal of interest.
Bioassays with Eisenia andrei
The definition of sediment doses to be used in bioassays was
based on previous ecotoxicological evaluation using Eisenia
andrei and dredged sediments from Sepetiba Bay (RJ, Brazil)
and Guanabara Bay (Cesar et al. 2017). The tested sediment
doses were: 0, 6, 12, 18, 24, and 30%, where 0% = pure
ferralsol. When necessary, lower doses (2 and 4%) were ap-
plied for the sediments whose toxicity was high. The earth-
worms used in the experiments were originated from labora-
tory cultures and maintained as described by Natal-da-Luz et
al. (2008). The bioassays were performed at 20 ± 2 °C and
under constant illumination (ISO 2012). Ten adult earthworms
(with a well-developed clitellum) were previously purged (on
moistened absorbent paper for 24 h), washed with distilled
water, and weighed before being inoculated in 500 g (dry
weight equivalent) of uncontaminated soil (0%) or mixtures
of soil and dredged sediment. The moisture of the test mix-
tures was adjusted to 40–50% of the water-holding capacity
(Natal-da-Luz et al. 2009).
The test was performed with four replicates, each one
consisting of a cylindrical plastic box (3.8 cm diameter and
6.4 cm height). Additional replicates with pure artificial soil
were prepared to attest the quality of the test. The composition
Environ Sci Pollut Res
Table 2 Detection limits found
for metal determinations in three Detection limits (mg kg−1) Al
different chemical extractions
Acetic acid extraction (FAAS) NA
Hydrochloric acid extraction NA
(FAAS)
Total extraction (ICP-OES) NC
NA not analyzed, NC not calculated
of the artificial soil follows the recommendations described by
Garcia (2004): 70% of quartz sand, 20% of kaolin, and 10% of
coconut shell dust. After 14 days of exposure, the surviving
organisms were counted and again maintained on moistened
absorbent paper for 24 h to purge the intestinal contents for
posteriorly weighed. The evaluation of biomass changes was
performed by using the average weight of the earthworms
before and after the exposure. The validity criterion of acute
tests assumed is an earthworm’s mortality lower than 10% in
replicates with artificial soil and pure ferralsol.
Statistical analysis
The sediment doses that caused 50% of mortality (LC50) and
the respective 95% confidence limits (CL) were obtained by
using the Priprobit 1.63 software (Sakuma 1998; http://bru.
gmprc.ksu.edu/proj/priprobit/download.asp). Significant
differences of mortality and biomass changes between the
test mixture and the pure soil (0%) were evaluated by
Kruskal-Wallis test, using the software STATISTICA ver-
sion 7.
Results
Metal concentrations, grain size, and chemical
characterization
Metal concentrations, grain size, and chemical properties of
the sediments are shown in Table 3. The values of pH were
generally close to neutral range (between 5.5 and 7.5), except
for the sediments from APA of Guapimirim and Iguaçu River
mouth, whose values were more acid. The electric conductiv-
ity determined for the sediments from APA of Guapimirim
was the highest one among the study areas. Clay contents
determined in the winter sediments were generally higher than
those found in the summer, except for the sediments collected
in the APA of Guapimirim. Most of sediment samples were
silty (> 70%), except the sample from Port of Rio de Janeiro in
the summer campaign (> 90% of sand). In both port areas,
sand contents determined in the summer were generally
higher than those obtained in the winter. Winter sediments
generally exhibited higher electric conductivity, total metal,
and TOC concentrations than those determined for the
As Cd Cu Cr Fe Hg Ni Pb Zn
NA 0.01 0.03 0.02 0.03 NA 0.04 0.1 0.06
NA NC 0.69 0.01 0.51 NA 0.53 0.45 0.01
0.04 0.10 0.2 0.01 NC 0.005 0.2 1.4 0.2
summer season, except for the sediments from the Iguaçu
River mouth and APA of Guapimirim. Because of that, the
ratios between winter and summer metal concentrations com-
monly exceeded the unity (1), especially in the Port of Rio
area, whose ratios were even higher than three (3) units.
In contrast to the other study areas, the sediments from
APA of Guapimirim were the only ones whose total metal
concentrations were in agreement with the Brazilian standards
for soil quality and land disposal of dredged sediments
(CONAMA 2009). Regarding the other sediments, most of
the disagreements with CONAMA ( 2009) are due to Zn,
Cu, and Pb concentrations. Among the study areas, the
Meriti River mouth showed the highest metal concentrations
and was the only area where Hg and Cd concentrations were
higher than the safety limits established by Brazilian law
(CONAMA 2009). Furthermore, the highest As concentration
was also detected for the winter sediment from the Meriti
River mouth and was higher than the limit established by
CONAMA ( 2009).
Metal geochemical fractioning
By considering the three tested geochemical phases (F1: ex-
tracted in 0.11 M acetic acid; F2: extracted in 1 M hydrochlo-
ric acid; F3: subtraction between total metal concentration;
and F2 concentration), all samples exhibited concentrations
below the detection limits for Cd on F1 and F2 extractions
(Fig. 2). Therefore, these results suggested that Cd is strongly
bound to Guanabara Bay sediments, possibly linked to organ-
ic complexes (F3). Cr concentrations on F1 were below the
detection limit and the concentrations in F2 corresponded to
an average of ~ 30% of the total concentration. Cu is mainly
found in F2 (extracted with 1 M HCl) for all sampling stations
(in average: ~ 50%), except for the APA of Guapimirim.
Similar behavior was found for Pb, where all samples had
more than 40% of Pb in the reactive phase (F2). Zn was main-
ly found on phase 1 (F1) and the sum of both reactive phases
(F1 plus F2) corresponds to more than 50% of its total con-
centrations in all sediment samples. Thus, Zn was the most
bioavailable metal. On the other hand, Fe and Ni were found
in low proportions in the reactive phases (< 40%). Regarding
the seasonality and the sampling stations located at river
mouths (Meriti and Iguaçu rivers), all metal concentrations
during the summer were higher in the reactive phases
Table 3 Values of pH, total organic carbon (TOC, in %), grain size (sand, silt, and clay, in %), electric conductivity (μS/cm), and total metal or metalloid concentrations (mg/kg) in the dredged sediments
from the Guanabara Bay (RJ, Brazil), and the rations between the values in the winter (W) and summer (S) seasons (W/S). * = higher than the limits established by CONAMA 420/ 2009 for terrestrial
disposal of dredged sediments in soil (As = 15 mg/kg; Cd = 1.3 mg/kg; Zn = .300 mg/kg; Cu = 60 mg/kg; Pb = 72 mg/kg; Ni = 30 mg/kg; Cr = 74 mg/kg; Hg = 0.5 mg/kg)

Parameter Port of Niterói Port of Rio de Janeiro Meriti River Mouth APA of Guapimirim Iguaçu River Mouth

W S W/ W S W/ W S W/ W S W/ W S W/
S S S S S

pH 7.49 6.65 1.1 6.5 5.73 1.1 7.02 6.87 1.0 4.6 4.4 1.0 3.44 5.58 0.6
TOC 2.9 1.5 1.9 7.1 1.8 3.9 3.7 3.9 0.9 4.6 4.4 1.0 2.5 4.5 0.6
Cond. 95,200 33,630 2.8 91,600 38,070 2.4 89,232 50,670 1.8 110,580 108,180 1.0 51,925 67,760 0.8
Sand 0.0 11.6 – 8.2 97.8 – 0.0 3.9 – 0.0 0.0 – 0.0 0.0 –
Silt 80.5 81.4 – 84.9 2.0 – 81.5 83.8 – 74.4 77.0 – 76.5 84.0 –
Clay 19.5 7.0 – 6.9 0.2 – 18.5 12.3 – 25.6 23.0 – 23.5 16.0 –
As < 0.4 < 0.4 – < 0.4 < 0.4 – 3.4 3.9 0.9 5.8 5.0 1.2 12.50 3.5 3.6
Cd < 0.10 < 0.10 – < 0.10 < 0.10 – 2.90* 1.10 2.6 0.15 0.15 1.0 < 0.10 0.69 –
Zn 297 192 1.5 453* 203 2.2 791* 551* 1.4 105 100 1.1 106 331* 0.3
Cu 129.0* 100.0* 1.3 114.0* 32.0 3.6 134.0* 70.5* 1.9 18.5 18.2 1.0 12.5 62.2* 0.2
Pb 87.0* 59.4 1.5 86.7* 42.9 2.0 145.0* 96.9* 1.5 33.2 53.2 0.6 35.9 70.9 0.5
Ni 14.8 10.6 1.4 48.0* 15.4 3.1 45.1* 25.6 1.8 17.0 18.2 1.0 17.2 18.8 0.9
Cr 42.0 26.4 1.6 104.0* 26.4 3.9 507.0* 112.0* 4.5 47.8 47.6 1.0 68.8 140.0* 0.5
Hg 0.064 0.021 3.0 0.052 0.032 1.6 0.856* 0.466* 1.8 0.006 0.006 1.0 0.019 0.006 3.2
Fe (%) 2.8 1.8 1.6 2.5 1.8 1.4 3.4 3.9 0.9 5.0 5.1 1.0 6.1 4.2 1.5
Al (%) 6.3 5.2 1.2 4.8 5.2 0.9 9.6 9.3 1.0 8.6 9.3 0.9 8.1 9.4 0.9
Environ Sci Pollut Res
Environ Sci Pollut Res
Fig. 2 Cr, Cu, Fe, Ni, Pb, and Zn percentages in three different
geochemical phases of sediments from Guanabara bay, RJ-Brazil. F1 =
metals extracted in 0.11 M acetic acid, F2 = metals extracted in 1 M HCl,
F3 = subtraction between total metal concentration and F2 extraction. IG:
(F1 and F2) compared to the winter season. However, for both
Port areas (Niterói and Rio de Janeiro) and APA of
Guapimirim, the reactive phases (F1 and F2) showed higher
concentrations during the winter.
Geoaccumulation index (IGEO) and metal-enrichment
factors (EF)
The IGEO classes and the values of metal-enrichment factors
generally exhibited higher values in the winter compared to
the summer season (Table 4). The highest classes of IGEO
were observed for Zn, Cu, and Pb. The maximum values of
IGEO (classes 6 and 5) were detected for Cu in the Port of Rio
Iguaçu River; ME: Meriti River; PR: Port of Rio de Janeiro; PN: Port of
Niterói; GU: Guapimirim. W = sampling performed in winter; S =
sampling performed in the summer
de Janeiro and Meriti River mouth. On the other hand, the
classes for As were low for all the study areas (class 0). The
classes for Cd were also generally low (class 0), except for the
Meriti River mouth (classes 3 and 2) and the winter sediment
from Iguaçu River mouth (class 1). The classes for Hg were
only high for the sediments from Meriti River mouth (classes
4 and 3) and the winter sediment from the Port of Rio de
Janeiro (class 1).
The EF values for Zn, Cu, and Pb exceeded orders of mag-
nitude the value considered as being natural (i.e., without sig-
nificant anthropic contributions—2) (Table 4). The highest
values were obtained for the Cu, followed by Zn, Pb, Ni,
Hg, and Cd. The EF values for As and Cr were below two
 Environ Sci Pollut Res

Table 4 Classes of geoaccumulation indexes (Igeo), metal-enrichment sediment from Guanabara Bay (RJ, Brazil). Toxic values (LC50) are
factors (EF) and median lethal concentration (LC50) of Eisenia andrei expressed in percentage of sediment added to soil
exposed to a mixture of ferralsol with a summer or winter dredged

Port of Niterói Port of Rio de Janeiro Meriti River Mouth APA of Guapimirim Iguaçu River Mouth

Winter Summer Winter Summer Winter Summer Winter Summer Winter Summer

Igeo EF Igeo EF Igeo EF Igeo EF Igeo EF Igeo EF Igeo EF Igeo EF Igeo EF Igeo FE

As a a a a a a a a 0 0.3 0 0.3 0 0.4 0 0.5 0 0.7 0 0.3

Cd a a a a a a a a 3 14.3c 2 4.1c 0 0.5 0 0.7 a a 1 2.8c
Zn 3 6.3c 2 6.4c 3 10.8c 2 6.7c 4 13.9c 3 8.5c 1 1.3 0 1.2 1 1.0 3 4.7c
Cu 6 71.7c 6 86.4c 6 70.9c 4 27.7c 6 61.3c 5 28.1c 3 5.8c 3 5.6c 3 3.2c 3 23.0c
Pb 3 8.8c 2 9.3c 3 9.8c 2 6.7c 4 12.0c 3 7.0c 2 1.9 1 2.9c 2 1.7 1 4.8c
Ni 4 2.7c 1 0.1 3 9.7c 1 0.1 3 6.7c 2 1.2 2 1.7 0 0.6 2 1.4 2 1.6
Cr 0 0.7 0 0.7 0 1.9 0 0.7 2 7.0c 0 1.3 0 0.4 0 0.4 0 0.5 0 1.6
Hg 1 2.4c 0 1.2 0 2.2c 0 1.9 4 26.4c 3 12.5c 0 0.1 0 0.1 0 0.3 0 0.2
LC50 (%) 12.34 17.52 7.30 19.64b 6.64 12.55 4.60b 3.99b 12.67b 11.58b
(12.0–12.7) (17.2–17.9) (5.6–8.3) (6.3–6.9) (11.0–11.7)
a
The concentrations are lower than the detection limits
b
Data does not allow estimation of a 95% confidence interval
c
Values representing high contributions of anthropic sources (EF > 2; Szafer et al. 1996)

(2) units for all the study areas. In addition, the lowest EF and
classes of IGEO were detected for the APA of Guapimirim
and Iguaçu River mouth, while the highest ones were ob-
served for the Meriti River mouth.
Bioassays with Eisenia andrei
The surveillance levels and biomass changes of earthworms
exposed to the dredged sediment-amended soils are shown in
Figs. 3 (Port of Rio de Janeiro), 4 (Port of Niterói), 5 (Meriti
River), 6 (Iguaçu River), and 7 (APA of Guapimirim). The
validity criterion of the earthworm acute test was fulfilled
since no mortality was found in replicates with artificial soil
and pure ferralsol (0% doses). The values of LC50 are demon-
strated in Table 4. In general, the winter sediments had higher
LC50 values than the summer ones, except for the sediments
from Iguaçu River mouth and APA of Guapimirim, whose
values were relatively similar in both seasons. In the Port of
Rio de Janeiro and the Meriti River mouth, winter LC50 values
were three and twice higher compared to the summer season,
respectively. The lowest LC50 values were detected for the
sediments from APA of Guapimirim, followed by Meriti
River mouth and the winter sediment from the Port of Rio
de Janeiro.
The mortality observed in soil/sediment mixtures showed
dose-response relationships for all study areas. Mortality
levels found in mixtures with the sediments from the Port of
Rio de Janeiro were significantly higher than those in control
for concentrations ≥ 18 and 8%, for summer and winter
seasons, respectively. The organisms exposed to the winter
sediment significantly increased their biomass for 6 and 12%
doses, while significant biomass loss was observed for 18%
dose. Biomass changes were significantly higher for all test
mixtures containing winter sediments (except for 24 and 30%,
since all the organisms were dead), while no significant bio-
mass changes were found in mixtures with summer sediment
(Fig. 3).
Regarding the sediments from Port of Niterói, significant
mortality was detected for concentrations ≥ 18 and 12%, for
summer and winter sediments, respectively (Fig. 4). For sum-
mer and winter sediments from Meriti River mouth, mortality
was significantly higher than that in control for doses ≥ 12
and 6%, respectively (Fig. 5). On the other hand, biomass
changes were generally insignificant for both summer and
winter sediments from Port of Niterói and Meriti River mouth.
Significant biomass loss was only detected for the 12% dose
with summer sediment from Meriti River mouth and the 12%
dose with winter sediment collected in the Port of Niterói.
Mortality detected in mixtures of ferralsol with both sum-
mer and winter sediments from Iguaçu River mouth were only
significant for doses ≥ 12%, and no significant biomass
changes were observed in organisms exposed to both sedi-
ments (Fig. 6). In contrast, all the doses applied with summer
and winter sediments collected in the APA of Guapimirim
caused significant lethal effects on the earthworms, except
for the 2% dose with summer sediment. The organisms ex-
posed to the 2, 4, and 6% doses with summer sediment and 2
and 4% with winter sediment increased their biomass levels.
Environ Sci Pollut Res

Fig. 3 Mortality and biomass

changes of earthworms (Eisenia
andrei) (n = 40) exposed to a
ferralsol treated with different
dosages of a dredged sediment
from the Port of Rio de Janeiro
(Guanabara Bay, Rio de Janeiro
State, Brazil). + = surveillance
significantly different from the
control (p < 0.05). * = biomass
significantly different from the
control (p < 0.05)

The only dose that induced significant loss biomass was 6%
treatment with summer sediment (Fig. 7).
Discussion
The predominance of neutral ranges of pH in the sediments is
probably due to the abundance of carbonated minerals in these
materials. The higher electric conductivity in winter sediment
samples is possibly due to changes in water temperature and
salinity. Paranhos and Mayr (1993), when studying physico-
chemical parameters in water samples from Guanabara Bay,
observed higher temperatures and lower salinities during the
rainy season (summer), while during the dry season (winter),
the temperatures were lower and salinities were higher, with-
out stratification. The toxicity and LC50 values obtained in the
acute tests generally agree with the increase of metal total
concentrations, IGEO classes, and EF values determined in
the sediments. The highest total metal concentrations, high
IGEO classes, and high values of EF obtained in the sediments
from Meriti River mouth and in the winter sediment from the
Port of Rio de Janeiro are, e.g., in agreement with very low
LC50 values obtained for these materials. Besides the highest
total concentrations, Meriti samples also exhibited the highest
contributions of metals (Cr, Cu, Ni, Pb, and Zn) on reactive
phases (F1 and F2), in agreement with the high toxicity of
these sediments. Cesar et al. (2017) also determined metal
concentrations in a dredged sediment sample from Meriti
River in 2011, and the values are similar to those obtained in
this research.
The Meriti River is located at the western Guanabara Bay,
and this region is recognized as the most impacted one of the
Bay system (Kjerfve et al. 1997), since it receives high
amounts of metallic effluents and domestic wastes (without
previous adequate treatment) from Metropolitan Region of
Rio de Janeiro State (Godoy et al. 1998; Machado et al.
2002, 2010). Furthermore, it is important to highlight that
Meriti River is well-known as a hotspot of Hg contamination
due to a Chlor-Alkali industry on its drainage basin. Because
of that, Hg concentration in the Meriti River sediments is
commonly almost 27 times above the background concentra-
tion, in agreement with high EF values and IGEO classes

Fig. 4 Mortality and biomass

changes of earthworms (Eisenia
andrei) (n = 40) exposed to a
ferralsol treated with different
dosages of a dredged sediment
from the Port of Niterói
(Guanabara Bay, Rio de Janeiro
State, Brazil). + = surveillance
significantly different from the
control (p < 0.05). * = biomass
significantly different from the
control (p < 0.05)
 Environ Sci Pollut Res

Fig. 5 Mortality and biomass

changes of earthworms (Eisenia
andrei) (n = 40) exposed to a
ferralsol treated with different
dosages of a dredged sediment
from the mouth of the Meriti
River (Guanabara Bay, Rio de
Janeiro State, Brazil). + =
surveillance significantly
different from the control (p <
0.05). * = biomass significantly
different from the control (p <
0.05)

found in this work. Other authors (Rego et al. 1993; Barrocas
and Wasserman 1995; Wasserman et al. 2000; Covelli et al.
2012) also indicate high Hg concentrations and high IGEO
classes for bottom sediments from Meriti River. In addition,
Pinto (1995), when applying a sequential extraction method-
ology to detail metal mobility and bioavailability in the first
10 cm of surface sediments, suggested that mercury was main-
ly linked to organic matter (80%). The other 20% of reminis-
cent Hg was equally distributed in two geochemical phases: (i)
complexed with humic acids and (ii) forming stable sulfides.
Fiori et al. (2013) tested a potential aquatic ecological risk
index for sediment samples from the northwest region of
Guanabara bay (that includes Meriti River) and suggested that
Hg and Cu are responsible for the very high ecological risk
found for this region.
Regarding the seasonality, the observed trend of higher met-
al concentrations in the reactive phase (F1 and F2) during the
summer for both rivers and the opposite for both port areas
clearly suggests that environmental changes on the rivers may
be due to inputs in the rainfall levels (Utete et al. 2013).
Besides that, at the areas where freshwater has no direct
influence, the changes on currents and hydrodynamics could
play an important role in metal bioavailability due to changes
on physical-chemical characteristics (such as salinity, nutrients,
chlorophyll-a; Paranhos et al. 1998) or even due to natural
sediment resuspensions. At the Guanabara Bay, it is also
well-known that the current at the entrance of the bay is more
intense and that the circulation inside the bay is a composition
of gravitational and residual tide circulation (Fistarol et al.
2015). Paranhos et al. (1998) also described that the influence
of tidal circulation was twice as high as the influence of sea-
sonality at areas near the bay’s entrance. The entrance of ocean
swells associated with meteorological frontal passages and the
tidal flood dominance of bottom current can influence the grain
size of the sediments at the Guanabara Bay entrance, especially
at the eastern margin of the central channel (Baptista-Neto et al.
2006). These alterations can occur in the Port of Rio de Janeiro
and may play an important role in the bioavailability of metals
and grain size, as shown in Table 3.
In contrast to the other study areas, APA of Guapimirim is
considered a control area at the Guanabara Bay and, as ex-
pected, metal concentrations measured in their sediments are

Fig. 6 Mortality and biomass

changes of earthworms (Eisenia
andrei) (n = 40) exposed to a
ferralsol treated with different
dosages of a dredged sediment
from mounth of the Iguaçu River
(Guanabara Bay, Rio de Janeiro
State, Brazil). + = surveillance
significantly different from the
control (p < 0.05). * = biomass
significantly different from the
control (p < 0.05)
Environ Sci Pollut Res
Fig. 7 Mortality and biomass
changes of earthworms (Eisenia
andrei) (n = 40) exposed to a
ferralsol treated with different
dosages of a dredged sediment
from Environmental Protection
Area (APA) of Guapimirim
(Guanabara Bay, Rio de Janeiro
State, Brazil). + = surveillance
significantly different from the
control (p < 0.05). * = biomass
significantly different from the
control (p < 0.05)
in fact low and below the safety limits established by Brazilian
law (CONAMA 2009). Farias et al. (2007) also indicated very
low metal contamination levels for the sediments from APA of
Guapimirim. However, LC50 values observed in the acute
tests are contradictorily the lowest ones among the study
areas. A probable hypothesis for such low LC50 values might
be the high salinity of these sediments. In this respect, the
electric conductivity determined in the sediments from APA
of Guapimirim was very high, and it is well-known that earth-
worms are very sensible to wastes containing high concentra-
tions of salt (Bianchi 2013). Also, Owojori et al. (2009), when
performing bioassays with Eisenia fetida in salinized artificial
soils, suggested that the exposure to NaCl was extremely toxic
to those organisms.
Vezzone et al. (2017) studied the toxicity of marine salts to
Eisenia andrei using the same ferralsol sample (used in this
research) contaminated with sea water, and the data suggested
that in fact, the acute toxicity of the sediments from APA of
Guapimirim is most probably due to their high salt contents. In
addition and contrasting to the other study areas, the sediments
from APA of Guapimirim were collected outside a river
mouth, besides being nearby a mangrove area, with shallow
waters. These characteristics of the sampling point may have
favored the evaporation of the water and salts precipitation.
Also, the absence of significant seasonal toxicity for the sed-
iments from APA of Guapimirim is probably due to their high
salt contents, since electric conductivity values do not show
significant differences between summer and winter. If on one
hand, no significant seasonal toxicity was found in this work
by using a terrestrial organism (Eisenia andrei) that is very
sensible to salts, on the other hand, Maranho et al. (2010)
detected significant acute toxicity in surface sediments from
APA of Guapimirim using bioassays with a marine amphipod
Tiburonella viscana in the dry season. These authors sug-
gested that the hydrodynamics could explain why legally
protected areas presented signs of environmental degradation
in terms of chronic toxicity.
The LC50 values observed for the sediments collected in
the Iguaçu River mouth are similar to each other, despite the
changes on metal mobility during summer, as well as the
increase on the reactive phases. This lower and similar toxicity
(in comparison with the other sampling points and seasonality,
respectively) might be associated with mangrove zones with
capacity of filtering metal pollution sources, reducing seasonal
toxicity differences. By supporting this hypothesis, Machado
et al. (2004), when studying metal contamination in sediment
cores from Meriti River estuarine system, showed that organic
matter and sulfides from mangroves zones were able to adsorb
great amount of metals and reduce their geochemical mobility,
thus suggesting that the preservation of mangrove areas at the
Guanabara Bay was crucial to filter contamination sources.
On the other hand, for both port areas, winter sediments
were generally more toxic than the summer ones, in agree-
ment with the increase of metal contents, especially the in-
crease on the bioavailable chemical forms, TOC and electric
conductivity observed for the winter sediments, supporting
our first working hypothesis. Especially for Port of Rio de
Janeiro, where the grain size characteristics drastically
changed between the winter and summer, the increase of en-
ergy input of river waters or differences on currents during the
summer, with capacity of depositing more sandy materials
could have decrease the toxicity. Sandy materials are able to
adsorb lower amounts of metals, organic matter, and salts due
to its low specific contact surface (Cesar et al. 2011), reducing
the metal concentrations in the samples of Port of Niterói and
Port of Rio de Janeiro and their toxicity. Also, the higher
toxicity found during winter for both port areas could be due
to the characteristics of a dry season (winter). The reduction of
pluvial precipitation levels may have caused: (i) the increase
of salt concentration in the water column, inducing the precip-
itation of metals and salts to bottom sediments and (ii) the
higher contributions of reactive phases in winter samples,
which could increase metal bioavailability levels and, conse-
quently, their toxicity. In agreement with our data, Baptista
 Environ Sci Pollut Res

Neto et al. (2005) also described high concentrations of Cr, monitoring. Such studies will support the definition of zones
Cu, Pb, and Zn and IGEO classes for surface sediments from to be primarily dredged at the Guanabara Bay, as well as the
Port of Niterói. On the other hand, Abreu et al. (2016) did not adequate season to perform the dreading taking into consider-
find a well-defined seasonality on metal concentrations in sur- ation the toxicity of the dredged sediment to soil organisms.
face sediments from Guanabara bay, and the IGEO classes
were generally lower than those found in this work for the
APA of Guapimirim and Port of Rio de Janeiro.
Conclusions
The significant earthworm biomass losses detected in the
bioassays are generally related to the exposure to significant
The dredged sediments from Guanabara Bay were toxic to
lethal doses. On the other hand, the increase of earthworm
earthworms in mixtures with pure ferralsol. Except for the
biomass observed for the summer sediment from the Port of
sediments collected in the Iguaçu River mouth and APA of
Rio de Janeiro and winter and summer sediments from APA of
Guapimirim, winter sediments were more toxic than the sum-
Guapimirim might be due to: (i) the fact that the organisms
mer ones, in agreement with the increase of total metal con-
may have used the organic matter from domestic wastes as
centrations and salt concentrations during the winter. On the
source of food, especially in the Port of Rio de Janeiro,
other hand, such tendency must be confirmed by evaluating
supporting our second working hypothesis. Cesar et al.
more sediment samples along more years of monitoring. The
(2012) and Carbonell et al. (2009), e.g., when studying the
toxicity of marine salts played a very important role in the
toxicity of sewage sludge-amended soils by applying bioas-
toxicity observed for the sediments from APA Guapimirim,
says with E. andrei, suggested that the earthworms could be
while the presence of mangrove zones may support the filter-
able to utilize polluted organic matter as source of energy; (ii)
ing of pollution sources, inducing the absence of significant
the occurrence of hormones and pharmaceuticals (not evalu-
seasonal toxicity.
ated in this study) commonly present in domestic wastes, with
The organisms exposed to the mixtures of ferralsol with
potential of causing disturbances in the endocrine system
winter sediment from Port of Rio de Janeiro and APA of
(Kavlock et al. 1996; Berge and Vulliet 2015). Cesar et al.
Guapimirim increased their biomass when exposed to low
(2015), when investigating the toxicity of dredged sediments
dosages of sediment application. Perhaps, the earthworms
from Cunha channel (also at the Guanabara Bay) by using
may have utilized the organic matter from domestic wastes as
chronic tests with E. andrei, suggested that hormones and
a source of food. However, other hypothesis must be also taken
pharmaceuticals could induce the increase of earthworm bio-
into account, such as the influence of marine salts in excessive
mass levels; and (iii) the excessive absorption of water by
bioaccumulation of water to maintain osmotic equilibrium, as
earthworms due to the abundance of salts in these sediments,
well as the effects of hormones and pharmaceuticals on the
especially in the APA of Guapimirim. In fact, Bianchi (2013),
endocrine system of the test organisms. In the near future, these
when investigating the toxicity of bauxite wastes (with high
dredged sediments will be also tested with other soil organisms
amounts of salts) by performing chronic bioassays with E.
(e.g., Caenorhabditis elegans, Folsomia candida, Hypoaspis
andrei, also indicated that the organisms increased their
aculeifer) to provide a better understanding of effects of
weight by absorbing excessive amounts of waters. Such ex-
dredged sediments from estuarine sediments to soil fauna.
cessive accumulation of water could consist of a strategy to
maintain the osmotic equilibrium. Guzyte et al. (2011) also Funding information We would like to thank the CNPq (National
detected an increase of earthworms (Eisenia fetida) biomass Brazilian Council for Scientific and Technological Development) and
when the organisms were exposed to non-lethal dosages of CAPES (Coordination for the Improvement of Higher Level-or
NaCl in bioassays with salinized artificial soils. Education-Personnel) Institutions for providing grants for Christiane
Monte, Ana Paula Rodrigues, Danielle Siqueira, Aline Serrano e
The ecotoxicological effects observed in the acute bioas- Matheus Teixeira. This study was supported by CNPq (process number
says are certainly due to additive, antagonistic, and synergetic 481898/2012-3).
effects of metals, salts, and other pollutants (such as hor-
mones, pharmaceuticals, petroleum hydrocarbons, and agro-
chemicals—not evaluated in this study) on the organisms
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