Environmental Pollution 252 (2019) 270e280

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Environmental Pollution
journal homepage: www.elsevier.com/locate/envpol

Metal pollution in surface sediments from Rodrigo de Freitas Lagoon

(Rio de Janeiro, Brazil): Toxic effects on marine organisms☆
Mariana Vezzone a, b, *, Ricardo Cesar b, Denis Moledo de Souza Abessa c, Aline Serrano b,
Rodrigo Lourenço b, Zuleica Castilhos d, Ana Paula Rodrigues e, Fernando Cesar Perina c,
Helena Polivanov a
a
Federal University of Rio de Janeiro, UFRJ. CCMNeGeosciences Institute. Departament of Geology. Rio de Janeiro, RJ, Brazil, Av. Athos da Silveira Ramos, 274
e Cidade Universita
ria, Rio de Janeiro, RJ, Brazil
b
Federal University of Rio de Janeiro, UFRJ. CCMNeGeosciences Institute. Department of Geography, Rio de Janeiro, RJ, Brazil
c ~ ~o Vicente, SP, Sa
~o Paulo, Brazil
Sao Paulo State University (UNESP), Campus Litoral Paulista, Sa
d
Centre for Mineral Technology, CETEM/MCTI, Av. Pedro Calmon, 900. Cidade Universita
ria, Rio de Janeiro, RJ, Brazil
e
Federal University of Rio de Janeiro, UFRJ. Institute of Biology. Department of Marine Biology, Rio de Janeiro, RJ, Brazil

a r t i c l e i n f o a b s t r a c t

Article history: The Rodrigo de Freitas Lagoon (RFL - Rio de Janeiro, RJ, Brazil) is a highly polluted and eutrophic
Received 5 February 2019 lacustrine system, which has been often used for the practice of aquatic sports, including during the 2016
Received in revised form Summer Olympic Games. This study proposes the evaluation of metal concentrations in surface sedi-
15 May 2019
ments from the RFL before and after urban interventions performed for the 2016 Olympics, as well as
Accepted 18 May 2019
Available online 21 May 2019
their toxicity to the benthic amphipod Tiburonella viscana and embryos of the sea-urchin Echinometra
lucunter. Metal concentrations determined in 2017 were significantly higher than those obtained in 2015
(especially Cu, Cd and Ni), suggesting that the interventions performed to fulfill the requirements of the
Keywords:
Toxicity
Olympics increased metal contents in sediments. The sediments from the northern sector of the RFL were
Bioassays muddier, more organically enriched, exhibited higher metal concentrations and were more toxic to
Sea urchin T. viscana when compared to the sediments collected in the southern sector. This fact is particularly
Amphipod important since the practice of sports, including during the 2016 Olympics, has been preferably per-
Contamination formed in the northern sector. Metal distribution was strongly correlated with organic matter and mud
contents. The toxicity to E. lucunter embryos was high for both northern and southern sediments; most of
the samples led to 100% lack or abnormal embryonic development. The integration of physical, chemical
and ecotoxicological data indicates that the mortality to T. viscana was correlated with metal contents,
whereas the toxicity to E. lucunter was apparently related to the release of ammonia from the sediment
to water column. Finally, high metal concentrations and the toxicity to aquatic organisms evidence the
ecological risks to the biota from RFL.
© 2019 Elsevier Ltd. All rights reserved.

1. Introduction
Over the last decades, coastal and fluvial ecosystems from South
America countries have been impacted by inadequate manage-
ment/regulation of discharges of domestic and industrial wastes.
Many of these ecosystems are highly eutrophic and silted (Fonseca
☆
This paper has been recommended for acceptance by Prof. Wen-Xiong Wang.
* Corresponding author. Federal University of Rio de Janeiro, UFRJ.
CCMNeGeosciences Institute. Departament of Geology. Rio de Janeiro, RJ, Brazil, Av.

ria, Rio de Janeiro, RJ, Brazil.
Athos da Silveira Ramos, 274 e Cidade Universita
E-mail address: mvezzone@ufrj.br (M. Vezzone).
et al., 2011; Loureiro et al., 2009; Monte et al., 2018; Pereira et al.,
2007). This situation is particularly critical along estuarine and
lagoon systems from Rio de Janeiro state (Brazil), where the
expansion of urban and industrial areas have generated great
amounts of wastes containing metals, petroleum hydrocarbons,
pharmaceuticals, hormones, microplastics, fecal pathogens and
other pollutants (R. A. Cesar et al., 2014; de Carvalho and Baptista
Neto, 2016; Ribeiro et al., 2013; Stefens et al., 2007). The dredging
of bottom sediments has become an alternative to partially restore
these environments. In this context, the Brazilian legislation es-
tablishes norms for the management and disposal of dredged
sediments, which include the characterization of the dredged

https://doi.org/10.1016/j.envpol.2019.05.094
0269-7491/© 2019 Elsevier Ltd. All rights reserved.
 M. Vezzone et al. / Environmental Pollution 252 (2019) 270e280
sediments for geochemistry and toxicity (Brasil, 2012). The
maximum limits defined by this legislation are strongly based on
the Canadian and American sediment quality guidelines and do not
reflect the particular properties of tropical aquatic ecosystems
(Abessa et al., 2006; Torres et al., 2015). Thus, the conduction of
studies integrating geochemistry and toxicity are needed to avoid
underestimations of ecological risks in case of sediment dredging.
Sediment properties can influence biogeochemical behavior and
mobility of metals in aquatic systems. In this context, sediment
texture, clay mineralogy, pH, Eh, organic matter, salinity, dissolved
oxygen, sulfide contents, iron (Fe) and aluminum (Al) oxy-
hydroxides, and others, play a relevant role in metal distribution
in lagoon environments (Cipullo et al., 2018; da Fonseca et al., 2013;
Zhuang and Gao, 2014). The understanding of such processes is
extremely important to identify (i) the key-contaminants and
sediment characteristics that influence the bioavailability and
toxicity of metals, (ii) which ecological receptors are at most po-
tential risk of toxicity and strategies to reduce such risks, (iii) which
areas might benefit from remediation strategies, and (iv) the
appropriate techniques of remediation, including sediment
dredging and disposal. On the other hand, toxicity data are neces-
sary to provide direct evidence that contaminants are likely to
cause effects to the biota.
The interpretation of such data should consider the sediment
complexity, which includes interactions between sediment prop-
erties and chemicals and organisms, interactions between multiple
contaminants, and the ability of organisms to uptake, depurate and
be affected by contaminants. This type of information is crucial to
support decision-makers in actions of environmental control,
protection of biodiversity and to prevent noxious effects on human
health.
Geochemical and biological data should be integrated to un-
derstand metal toxicity in bottom sediments. In this respect, bio-
assays with eggs and embryos of sea urchins have been widely
applied to characterize the toxicity related to the water-sediment
interface (Nascimento et al., 2000; Pereira et al., 2018). Such em-
bryos are planktonic and sensitive to xenobiotics, including those
transferred from sediments to the water column. Acute and chronic
toxicity tests with amphipods are also commonly used to detect the
toxicity of metals in bottom sediments; amphipods have been
widely used in sediment quality assessments because of their
benthic habit, their sensitivity to many types of contaminants and
wide geographical distribution (Rodrigues et al., 2017). Sediment
toxicity tests have been used to monitor metal toxicity levels in
sediments worldwide (Hansen et al., 1996; Ho et al., 2002; Simpson
et al., 2017; Simpson and Spadaro, 2011; Vandegehuchte et al.,
2013), including some Brazilian estuarine systems (Abessa et al.,
2005; Camargo et al., 2015; Rodrigues et al., 2017), and their
application is requested by environmental agencies (Brasil, 2012).
From an ecological, commercial and recreational point of view,
coastal lagoon ecosystems are extremely important, since they (i)
protect coastal watershed areas and fishing activities, (ii) promote
the filtering of contaminants and play a vital role in quality of
coastal waters, including for the practice of aquatic sports (iii)
provide and protect a great diversity of habitats, including coastal
wetland habitats, submerged aquatic vegetation, tidal flats and
others, and (iv) play a crucial role in the biogeochemical cycle of
nutrients (Kennish and Paerl, 2010). Despite their ecological, social
and economic importance, coastal lagoons have become increas-
ingly impacted around the world; especially those located in or
close urbanized regions.
The Rodrigo de Freitas Lagoon (RFL) is located in the city of Rio
de Janeiro (RJ, Brazil) and has a perimeter of about 7.5 km and a
total area of 2.5
106 m2 (Gonzalez et al., 2010). This is the most
urbanized lagoon in Rio de Janeiro State, which has a single
271
connection with the sea (the Jardim de Ala Canal). The RFL is a
semi-confined system where water renewal is complex and the
marine water flux is superficial, leaving deeper layers unaffected
(Fonseca et al., 2014; Torres, 1990). The fresh water input comes
mainly from the Macacos, Cabeça and Rainha Rivers (Andreata
et al., 1997). The lagoon is undergoing accelerated degradation,
mainly caused by human interference (Gonzalez et al., 2010;
Lutterbach et al., 2001). The surroundings of the lagoon are densely
urbanized resulting in a large input of pollutants, such as garbage,
oil, and untreated domestic sewage to its main tributary rivers and
pluvial water galleries (Fonseca et al., 2014; Gonzalez et al., 2010).
In the RFL, previous studies reported metal concentrations
exceeding background levels (Loureiro et al., 2009), as well as fecal
contamination (Fonseca et al., 2014; Gonzalez et al., 2010), eutro-
phication, chemical contamination (Soares et al., 2012; Stefens
et al., 2007) and severe anoxia due to organic pollution (Brito and
Lemos, 1982); events of massive fish death also have been
frequently observed over time (Domingos et al., 2012). According to
Fonseca et al. (2014), the substances adsorbed by suspended matter
tend to settle out and become deposited in the bottom sediments of
the RFL. Besides providing the ecosystem services mentioned
above, the RFL is often used for the practice of aquatic sports,
fishing, tourism and the real estate value of its surrounding areas is
extremely high. Thus, the RFL could be used as a good general
model to understand the toxicity related to metal pollution in other
hypereutrophic urban lagoons in tropical regions. Last, but not
least, the monitoring of metal contents in sediments will clarify if
the interventions performed due to the 2016 Summer Olympics
were enough to improve the environmental quality levels.
This study consists of an integrated evaluation of sediment
quality from Rodrigo de Freitas Lagoon (RJ, Brazil) taking into
consideration geochemical and ecotoxicological aspects. Second-
arily, the study proposes the comparison between metal concen-
trations before and after dredging interventions performed for the
2016 Summer Olympics. To achieve to these purposes, total metal
determination and bioassays with T. viscana and E. lucunter were
applied to surface sediments collected along the lagoon. Metal-
enrichment factors were also applied to evaluate metal anthropic
contributions of pollution. The working hypotheses are: (i) organic
matter plays a crucial role in metal distribution in surface sedi-
ments; and (ii) the sediments collected in 2015 (before the 2016
Olympics) exhibit higher metal concentrations than the samples
obtained in 2017.
2. Materials and methods
2.1. Samples
Sixteen (16) samples of surface sediments (10 cm depth, about
5 kg per sample) were collected in July/2017 (dry season) (Fig. 1)
using a Van Veen grab sampler. The samples were dried at <35  C
and, after that, mixed and homogenized. After this step, the sam-
ples were sieved (0.02 mm). For the ecotoxicological evaluation, the
samples were maintained moistened, at 4  C and under darkness
during two (2). The selection of the sampling sites was based on
Vezzone et al. (2018), who studied metal distribution in surface
sediments collected in 2015.
The grain size of the sediment samples was determined by the
wet sieving method, according to EMBRAPA (1997). The determi-
nation of pH was performed in water and followed the method
described by EMBRAPA (1997). The total organic carbon contents
(TOC) were determined through the pyrolysis of the sample after
descarbonation, using LECO SNS-Equipment. The determination of
total phosphorous (TP) was performed by using a colorimetric
method (Aspila et al., 1976) and a spectrophotometry (Thermo
272 M. Vezzone et al. / Environmental Pollution 252 (2019) 270e280
Fig. 1. Sampling points of surface sediments in the Rodrigo de Freitas lagoon (Rio de
Janeiro, RJ, Brazil). S ¼ sample collected in the southern sector of the lagoon.
N ¼ sample collected in the northern sector of the lagoon.
Scientific, Genesys 10 S) on the absorbance of 880 nm.
2.2. Metal determination and enrichment-factors
Total concentrations of arsenic (As), zinc (Zn), cooper (Cu), lead
(Pb), nickel (Ni), cadmium (Cd) and chromium (Cr) in the sediments
sample were determined after an acidic extraction of one (1) gram
of sample using a mixture composed of HF:HNO3:HClO4 (2:1:1).
Metal contents in the extracts were quantified by Inductively
Coupled Plasma Optical Emission Spectrometry (ICP-OES). The
detection limits were 0.4 mg/kg, 0.2 mg/kg, 0.2 mg/kg, 1.4 mg/kg,
0.2 mg/kg, 0.01 mg/kg and 0.80 mg/kg for As, Cu, Zn, Pb, Ni, Cr and
Cd, respectively. To guarantee the quality of these results, the
samples were analyzed in triplicate and a reference material (NIST
sediment) was used. The analyses are considered satisfactory when
the recovery rates lie between 90% and 110%. In addition to that, the
error assumed for analyzing metal was <10% among the replicates.
The concentrations were compared to the threshold limits estab-
lished by the Brazilian government for the disposal of dredged
sediments in aquatic environments (Brasil, 2012).
Metal-enrichment factors (EF) are utilized to assess contami-
nation levels relative to anthropogenic inputs of metals in sedi-
ments. Possible anthropic anomalies are identified by normalizing
metal concentrations (those determined in the field and back-
ground concentrations) in relation to a conservative element
whose source is mainly lithogenic, such as Al, Fe or Sc (Szefer et al.,
1996). When the ratio between the normalized concentrations
exceeds two units (Equation (1)), the anthropic contributions of a
specific metal are considered significant. The background concen-
trations were obtained in the standard shale (Turekian and
Wedepohl, 1961). The use of these background values is recom-
mended by (Müller, 1979) when adequate regional values are not
available.
ðMi =AlÞsample
EF ¼ (1)
ðMi =AlÞbackground
Where: Mi ¼ metal of interest; and Al ¼ concentration of
aluminum.
2.3. Acute bioassay with amphipods (Tiburonella viscana)
The organisms used in the acute toxicity sediment tests were
obtained on sand bars at the Engenho D’a
gua beach (Ilha Bela, Sa
~o
Paulo State, Brazil) by using a hand sampler. After identification, the
animals were kept in 2-L polyethylene flasks filled with sediment
and seawater collected in the field. The animals remained in 2 L
flasks after collection for no more than 6 h (time necessary to finish
the amphipod sampling and return to the laboratory). In the field,
about 200 animals were introduced in each flask, in order to avoid
overcrowd. At the laboratory, the organisms were acclimated for
three (3) days in 10-L tanks containing filtered seawater and a layer
of 1 cm-sediment, at constant temperature (23 ±2  C), lighting and
aeration. The sediment collected to acclimatize the organisms was
used as control sample of the test. Finally, the dilution water con-
sisted of water collected close to Laje de Santos Marine State Park, a
protected area located 35 km offshore and which is considered
clean (Moreira et al., 2017); its salinity remains around 34±2 mg/kg.
The procedure adopted for these tests (ABNT, 2015) is based on
the exposure of adult individuals of a same range of size to the
sediments collected. Each test chamber consisted of a 600 mL
polyethylene flask, containing approximately 100 mL (z2 cm high)
of sediment and 400 mL of filtered seawater and 10 amphipods; 3
replicates were prepared per sample. Only healthy organisms (i.e. -
no deformities, normal appendix movements, fast reaction to me-
chanical stimulation and fast burrowing when in contact with
sediment) were used in the test. Ovigerous females were not used.
The test system was kept under controlled temperature (23 ±2  C),
constant lighting and aeration. After 10 days, the sediment of each
test-chamber was sieved (0.05 mm). After this step, the surviving
organisms were collected and observed at the microscope to
evaluate mortality levels. Missing organisms were considered dead.
During the test, total ammonia, pH, salinity and dissolved oxygen
were also monitored.
2.4. Embryo-larval development bioassay with sea-urchins
(Echinometra lucunter)
Adult sea-urchins were collected at Palmas Island (Guaruja
, Sa
~o
Paulo State, Brazil). The organisms were rapidly transported to the
laboratory, where they were maintained under controlled condi-
tions, in accordance with the procedures described by ABNT (2006).
The embryo-larval development of newly fertilized eggs of the sea-
urchin was evaluated considering four replicates, each one con-
sisting of 15 mL chambers filled with 2 mL of sediment and 8 mL
filtered seawater. Initially, the sediment (2 mL) was introduced in
the chamber. Then, a sieve (45 mm) was fixed immediately above
the sediment using a plastic ring to avoid direct contact of the
larvae with the sediment. After this step, 8 mL of filtered seawater
was added and the temperature was maintained at 25  C.
The spawning was induced by osmotic shock, by injecting of
1e2 mL of KCl (0.5 M) into the abdominal cavity of adult sea-
urchins. The gametes of different animals were carefully sepa-
rated, and 0.5 mL of sperm were separated, and then diluted in
24.5 mL, for sperm activation. The fertilization was performed by
adding 1e2 mL of sperm solution to the ovules solution. After
 M. Vezzone et al. / Environmental Pollution 252 (2019) 270e280 273

mixing sperm and ovules solutions, the fertilization success was
checked on microscope. After that, a certain volume of the solution
of freshly fertilized eggs was added to each replicate, in order to
achieve about 300e500 eggs in each test chamber (10 mL). The test
was conducted under 8:16 h (light/dark) period and at 20 ± 2  C.
After approximately 36 h of exposure, when 80% of the control
larvae reached the plateaus stage, the embryos were fixed by
adding 4% neutralized formalin to the test chambers. Before and
after the test, ammonia concentrations, pH, salinity levels and
dissolved oxygen were measured.
2.5. Statistical analysis
The normality and homocedascity of the ecotoxicological data
were verified by Shapiro-Wilks and Bartlett's tests, respectively.
The results were compared with their respective control samples
by applying the Student t’-test by using the software Statistica 6.0.
Thus, the samples were considered toxic when the differences
between field and control samples were significant (p  0.05).
Regarding metal concentrations, the variance analysis was applied
to check the significance of the differences between northern and
southern sediments, as well as the differences obtained between
2015 and 2017. Given the fact that the normality of the data was
violated for some parameters, a non-parametric Kruskal-Wallis
ANOVA test was used. The maps were prepared by using the soft-
ware ArcGis 10.4.1.
To integrate all the parameters and to check possible correla-
tions among the data, the Principal Component Analysis (PCA) was
applied. The Cluster analysis was applied to classify the samples in
different groups by integrating all the data. The parameters
considered for these analyses were (n ¼ 15): metal concentrations;
pH; TOC; TP; mud content; mortality of T. viscana, and embryo-
larval toxicity to E. lucunter. These statistical analyses were per-
formed by using the software R version 3.5.1.
3. Results
3.1. Physical and chemical characterization of the sediments
The results of texture, pH, TOC, Fe, Al and P are in Table 1, which
also include data obtained in June/2015 by Vezzone et al. (2018) for
the same sampling sites. The sediments are predominantly
composed of mud (silt þ clay). Sand contents were higher in the
southern sector (46.8 ± 26.7%) than in the northern one
(8.0 ± 2.8%). When comparing data from the northern sector be-
tween 2015 and 2017, sand and mud contents were significantly
different (Kruskal-Wallis, p < 0.05). Mud contents in 2017 were
higher than the ones determined in 2015 (Kruskal-Wallis, p < 0.05).
The determination of pH showed that the samples were slightly
acidic. The northern sediments tended to be more acidic compared
to the southern ones. The sediments collected in the northern
sector in 2017 were less acidic than the ones collected in 2015
(Kruskal-Wallis, p < 0.05). No significant differences were found
between mean Al contents between 2015 and 2017 while mean Fe
concentrations exhibited higher values in 2017 (Kruskal-Wallis,
p < 0.05).
In general, TOC contents in the sediments tended to be high,
especially in the northern sector (maximum concentra-
tion ¼ 10.1%). When comparing TOC data between 2015 and 2017,
northern sediments presented levels significantly higher than the
southern ones (Kruskal-Wallis, p < 0.05). Similar to the TOC con-
tents, the concentrations of P were also high, mainly in northern
sediments (Kruskal-Wallis, p < 0.05). However, no significant dif-
ferences between P contents in 2015 and 2017 were found.
3.2. Metal concentrations in sediments
Table 2 shows the results related to metal concentrations in
sediments collected in 2015 (Vezzone et al., 2018) and in 2017. The
concentrations per sampling site are available in the supplemen-
tary material. In 2017, northern sediments revealed significantly
higher metal concentrations compared to the southern sector
(Kruskal-Wallis, p < 0.05), except for Ni and Cr. Mean metal con-
centrations in sediments show a general tendency of increasing in
2017. However, when considering the significance of the differ-
ences between 2015 and 2017, general mean values were only
significantly different for Cu, Ni and Cd (Kruskal-Wallis, p < 0.05),
while no significant differences were found for the other metals. Cd
and As concentrations in 2015 were below the detection limits. If on
one hand As concentrations remained below the detection limit in
2017, on the other hand Cd concentrations were extremely high,
especially in the northern section.
Fig. 2 shows metal concentrations in each sediment sampling
site in 2015 (Vezzone et al., 2018) and 2017. In general, in 2017
metal concentrations in northern sediments exceeded the Level
One (limit of low probability of adverse effects on biota e (Brasil,
2012) established by Brazilian law for almost all metals, except
for Cr and Ni. In contrast, some Ni concentrations (n ¼ 3) in the
southern section exceeded the Level One. Chromium was the only
metal whose concentrations in 2015 and 2017 were below the legal
limit. In terms of number of sampling sites where the concentra-
tions of metals in sediments exceeded the Level One, the results

Table 1
Sand contents, mud (silt þ clay) contents, pH, total phosphorus (P), total organic carbon (TOC), total iron (Fe) and total aluminum (Al) in surface sediments collected in the
Rodrigo de Freitas Lagoon (RJ, Brazil) in June/2015 and August/2017. Data from 2015 were taken from Vezzone et al. (2018). Min ¼ minimum value. Max ¼ maximum value.

Variable Year General Average (n ¼ 15) Southern Sector (n ¼ 10) Northern Sector (n ¼ 5)

Average ± Std Min Max Average ± Std Min Max Average ± Std Min Max

Mud (%) 2015 61 ± 26 1 95 51 ± 26 1 95 83 ± 5 76 90

2017 65 ± 29 17 96 53 ± 27 17 91 92 ± 3 89 96
Sand (%) 2015 39 ± 26 6 99 49 ± 26 6 99 17 ± 5 10 24
2017 35 ± 29 4 83 47 ± 27 9 83 8±3 4 11
pH 2015 5.5 ± 1.3 3.8 7.3 6.2 ± 0.9 4.4 7.3 4.0 ± 0.2 3.8 4.3
2017 6.0 ± 1.2 4.0 7.6 6.4 ± 1.1 4.2 7.6 5.1 ± 0.8 4.0 6.2
P (mg/kg) 2015 517 ± 189 74 855 429 ± 157 5 631 693 ± 105 588 855
2017 511 ± 187 122 715 506 ± 155 122 660 639 ± 85 521 715
TOC (%) 2015 3.8 ± 1.7 0.3 6.7 3.2 ± 1.7 0.3 6.7 5.2 ± 0.5 4.4 5.6
2017 4.9 ± 2.0 0.6 10.1 4.1 ± 1.5 0.6 5.9 6.6 ± 2.0 5.4 10.2
Fe (%) 2015 2.7 ± 0.9 0.3 3.4 2.4 ± 0.9 0.3 3.3 3.2 ± 0.2 3.0 3.4
2017 3.3 ± 1.0 1.4 4.7 3.0 ± 1.0 1.4 4.7 4.0 ± 0.4 3.6 4.4
Al (%) 2015 5.6 ± 1.9 0.9 8.1 4.8 ± 1.8 0.9 7.4 7.1 ± 0.7 6.2 8.1
2017 5.8 ± 2.5 2.0 10.4 5.7 ± 2.2 2.4 9.1 5.9 ± 3.5 2.0 10.4
274 M. Vezzone et al. / Environmental Pollution 252 (2019) 270e280

Table 2
Metal concentrations (average ± standard deviation) in surface sediments collected in the Rodrigo de Freitas Lagoon (Rio de Janeiro, RJ, Brazil) in June/2015 and August/2017,
including the comparison with limits established by Brazilian law (Levels 1 and 2 - CONAMA 454/2012). The data from 2015 was obtained from Vezzone et al. (2018).
Min ¼ minimum value. Max ¼ maximum value. Level 1* ¼ limit of low probability of adverse effects on biota. Level 2** ¼ limit of high probability of adverse effects on biota.

Variable Year General Average (n ¼ 15) Southern Sector (n ¼ 10) Northern Sector (n ¼ 5) CONAMA 454 (2012)

Average ± Std Min Max Average ± Std Min Max Average ± Std Min Max Level 1* Level 2**

Zn (mg/kg) 2015 178 ± 95* 13 305 111 ± 65 13 221 284 ± 16* 271 305 150 410
2017 241 ± 92* 84 366 176 ± 63* 84 311 338 ± 27* 308 366
Cu (mg/kg) 2015 41 ± 17* 17 64.3 30 ± 9 17 47 60 ± 3* 56 64 34 270
2017 59 ± 20* 32 88 45 ± 9* 32 72 82 ± 5* 77 88
Pb (mg/kg) 2015 61 ± 37* 6 122 36 ± 22 6 73 103 ± 22* 72 122 46.7 218
2017 66 ± 23* 37 103 50 ± 11* 37 82 91 ± 11* 78 103
Ni (mg/kg) 2015 14 ± 3 8 19 15 ± 3 8 19 16 ± 1 14 17 20.9 51.6
2017 19 ± 7 9 39 19 ± 10 9 39 20 ± 0.4 19 20
Cd (mg/kg) 2015 <0.8 <0.8 <0.8 <0.8 <0.8 <0.8 <0.8 <0.8 <0.8 1.2 7.2
2017 1.6 ± 0.3* 1.1 2.1 1.3 ± 0.2* 1.1 1.8 1.8 ± 0.2* 1.6 2.1
Cr (mg/kg) 2015 36 ± 12 3 56 34 ± 15 3 49 43 ± 8 33 56 81 370
2017 41 ± 16 3 74 41 ± 17 3 74 49 ± 2 47 53

Fig. 2. Total metal concentrations in surface sediments from Rodrigo de Freitas Lagoon (Rio de Janeiro, RJ, Brazil) in June/2015 and August/2017, including the comparison with the
threshold limits defined by Brazilian law (Brasil, 2012) for sediment quality. The dashed line means the Level 1 proposed by Brazilian Law (limit of low probability of adverse effects
on biota). Cd concentrations in 2015 were below the detection limit (0.8 mg/kg). S ¼ sample collected in the southern sector of the lagoon. N ¼ sample collected in the northern
sector of the lagoon.

indicate the following order in 2017: Cu (n ¼ 14) > Zn (n ¼ 13) > Pb general, EF values obtained in 2015 were lower than those deter-
(n ¼ 11) > Cd (n ¼ 10) > Ni (n ¼ 3) > Cr (n ¼ 0). mined in 2017. Also, EF values in northern sediments were gener-
ally higher than those found in sediments from the southern
portion of RFL. In terms of mean values of EF in 2017, the results
3.3. Metal enrichment-factors
indicate the following order: Cd (EF ¼ 7.9 ± 1.6) > Pb
(EF ¼ 5.6 ± 4.0) > Zn (EF ¼ 4.3 ± 3.4) > Cu (EF ¼ 2.3 ± 1.8) > Cr
Fig. 3 shows the values of metal enrichment-factor (EF) in each
(EF ¼ 0.8 ± 0.6) > Ni (0.5 ± 0.3). All the sediments showed EF values
sediment sampling site in 2015 (Vezzone et al., 2018) and 2017. In
 M. Vezzone et al. / Environmental Pollution 252 (2019) 270e280 275

Fig. 3. Metal enrichment-factors (EF) in bottom sediments from Rodrigo de Freitas Lagoon (Rio de Janeiro, RJ, Brazil) in June/2015 and August/2017. The data from 2015 were taken
from Vezzone et al. (2018). The dashed line means the Level that indicates the limit for significant anthropic contribution of metals. Cd concentrations in 2015 were below the
detection limit (0.8 mg/kg) and, due to this reason, EF values are not indicated in Figure. S ¼ sample collected in the southern sector of the lagoon. N ¼ sample collected in the
northern sector of the lagoon.

that indicate anthropic contributions (EF > 2) for Cd and Pb, while toxicity in comparison with the control sample, except those
no sediment sample exceeded two (2) units for Ni. In 2017, the collected in the S1 and S2 sampling sites.
sampling site exhibiting the highest EF values was N10; this was the
only sediment which EF was higher than two (2) units for Cr. 3.5. Chronic bioassays with sea-urchins (Echinometra lucunter)

3.4. Acute bioassays with amphipods (Tiburonella viscana)
Fig. 4a shows the distribution of lethal effects to T. viscana
exposed to surface sediments from Rodrigo de Freitas Lagoon. The
test was considered valid, since mean mortality observed in the
control sample was lower than 15%. The results suggest that mor-
tality was higher in the northern sediments. However, the mortality
can be considered high for both sections of the lagoon, since the
lowest mortality effects generally included at least 40e50% of the
organisms, indicating that the southern sediments were also toxic
to T. viscana. In this respect, all the sediments exhibited significant
Fig. 4b shows the distribution of toxicity levels (abnormalities in
the embryo-larval development) to E. lucunter exposed to surface
sediments from Rodrigo de Freitas Lagoon. This test was considered
valid, since the toxicity in the control sample was lower than 20%.
All the samples exhibited significant toxicity on the sea-urchin
embryos.
If on one hand the toxicity to T. viscana was higher in northern
sediments, on the other hand the sediment toxicity to E. lucunter
was elicited in sediments from both sections. Regarding E. lucunter,
the exceptions were the samples from S1, S2, S4 and S8, which
caused lower rates of abnormalities on the exposed organisms, but
276 M. Vezzone et al. / Environmental Pollution 252 (2019) 270e280

Fig. 4. Spatial variability of (a) mortality levels of Tiburonella viscana and (b) anomalies on embryo-larval development of Echinometra lucunter exposed to surface sediments from
Rodrigo de Freitas Lagoon (Rio de Janeiro, RJ, Brazil).

were significantly toxic as well (at least between 49 and 59%).
3.6. Integrative analysis
Fig. 5 and Table 3 show the results of the PCA. The PC1 and PC2
explained 70.8% of the variances of the data (49.2% and 21.6%,
respectively). The results indicate that the mortality of T. viscana
and the concentrations of Cd, Pb, Zn and Cu correlated to PC1 and
are associated. The PC2 indicates that the organic enrichment (TOC
and P contents) is inversely correlated to the increase of Ni, Cr and
Fe. The PCA analysis also suggests that in fact northern samples
generally had lower quality in comparison with those from the
south portion of the RFL. Despite the comparison with the northern
sediments, it is important to highlight that some southern samples
exhibited high toxicity levels and can be considered extremely
polluted. The toxicity to E. lucunter was not associated with any PC,

Fig. 5. Bi-dimensional ordination of PCA results using geochemical and ecotoxicological data obtained from sediments from Rodrigo de Freitas Lagoon, Rio de Janeiro, RJ, Brazil
(PC1
PC2). S ¼ sample collected in the southern sector of the lagoon. N ¼ sample collected in the northern sector of the lagoon.
 M. Vezzone et al. / Environmental Pollution 252 (2019) 270e280 277

Table 3 The increase of mud contents in northern sediments is correlated

Principal component analysis (PCA) based on chemical contamination and toxicity with the organic enrichment (TOC and P) due to the low hydro-
levels to Tiburonella viscana and Echinometra lucunter exposed to surface sediments
from Rodrigo de Freitas Lagoon (Rio de Janeiro, RJ, Brazil).
dynamics and inputs of pollutants by sewage contaminated rivers,
direct discharge of sewage and urban runoff (Fisher-Power et al.,
Variables PC1 PC2 2016; Fo €rstner and Wittmann, 1981), inducing the occurrence of
T. viscana mortality 0.7741 0.0431 reducing conditions in the northern section of the lagoon (Brito and
E. lucunter toxicity 0.3815 0.0345 Lemos, 1982; Fonseca et al., 2014; Gonzalez et al., 2010). Because of
pH ¡0.7923 0.3119
that, northern sediments were more acidic than southern ones.
COT 0.6732 0.5521
P 0.5946 0.7178 Therefore, all these factors together (presence of pollution sources,
Zn 0.9265 0.2892 low hydrodynamics and high contents of mud) result in the pref-
Cu 0.9746 0.0653 erential accumulation of organic matter in northern sediments. In
Pb 0.9332 0.1676
this respect, organic matter is well-known by its capacity of
Ni 0.2382 ¡0.9127
Cd 0.9226 0.1288
forming stable complexes with metals (Fathollahzadeh et al., 2015;
Cr 0.5224 ¡0.7344 Tessier et al., 1979). Due to this reason, metal concentrations in
Fe 0.7081 ¡0.5241 northern sediments were generally higher when compared to the
Al 0.2756 0.1972 southern ones, confirming our first working hypothesis. In fact,
Mud 0.7824 ¡0.5161
most of metal concentrations in northern sediments exceeded the
Eigenvalues 7.38 3.23
threshold limits defined by Brazilian law for sediment quality.
Variances (%) 49.2 21.6 The increase of metal concentration in 2017 (compared to 2015)
Cumulative Vars (%) 49.2 70.7 is probably due to dredging interventions that were performed in
Bold-marked indicates significant correlation. the lagoon in order to fulfill the requirements of the 2016 Summer
Olympics, although this scenario cannot be replicated. This fact
refuses our second working hypothesis. Such interventions were
thus it was not primarily associated with metals or sedimentolog- mainly conducted in the northern section of the lagoon, where the
ical factors (Table 3). practice of aquatic sports during the Olympics was preferably
The cluster analysis is presented in Fig. 6. When considering the performed. The highest EF values were found in the northern sector
integration of all data studied in this work, the results suggest that of the lagoon, in agreement with the elevated concentrations of
the northern section of the lagoon presents a worse condition, metal observed in these localities. The highest metal concentra-
indicating that metal concentrations and toxicity levels are higher tions and EF values were detected for Cd, Zn, Pb and Cu. The main
in northern sediments. anthropic sources of such metals are probably related to the
discharge of domestic wastes and stormwater rainfall, the corrosion
of pluvial water galleries and urban runoff (Fonseca et al., 2011;
4. Discussion
Vezzone et al., 2018). The characterization of these sources should
be better investigated in further studies. In general, the results
Northern sediments generally exhibited high contents of mud
suggest that the urban interventions performed in the lagoon to
since the northern section of the lagoon shows low hydrodynamics.
fulfill the requirements of the Olympics got sediment quality worst
On the other side, the southern section is connected to the Jardim
since they did not take into account metal-polluted sub-superficial
de Alah Canal, which is a source of sandy marine sediments to the
sediment resuspension. Instead, the contamination levels increased
lagoon and also an input of marine waters that may cause the
after those interventions.
resuspension and washing of fine particles and TOC in this region.
Some possible factors may explain such unexpected results. The
dredging could have caused the resuspension of fine particles,
metal-rich sediment particles to the water column, and their
gradual deposition after the dredging could have increased the
concentration of metals. Loureiro et al. (2012), when studying
metal distribution in sediments from Rodrigo de Freitas Lagoon,
also suggest that dredging interventions were able to increase
metal concentration in surface sediments. Another possible
explanation could be related to higher levels of contamination of
the formerly sub-superficial layers of sediments, which became the
new sediment surface after the dredging. A third factor may be
related to possible urban interventions around the lagoon; instal-
lation of new pollution sources or construction of storm water
galleries or urban water drains to the lagoon that could increase the
input of metals to RFL (Karlsson et al., 2010; Pereira et al., 2007; Pitt
et al., 1995; Prestes et al., 2006; Sutherland and Tolosa, 2000). In
this context, even though some galleries had been constructed to
drain pluvial waters directly to the ocean (through submarine
outfall), this transference has been only made in periods of dry
weather. Further studies are required to explain the mechanisms
involved in the increasing concentrations of metals in superficial
sediments after a supposedly remediation by using dredging.
Vezzone et al. (2018), when applying a potential ecological risk
Fig. 6. Cluster analyses showing the similarity among the sampling points of surface
sediments collected in the Rodrigo de Freitas Lagoon (Rio de Janeiro, RJ, Brazil).
index (PERI e Håkanson, 1980) related metal pollution in sediments
S ¼ sample collected in the southern sector of the lagoon. N ¼ sample collected in the to predict noxious effects on aquatic biota from the Rodrigo de
northern sector of the lagoon. Freitas Lagoon in 2015, suggested that the ecological risk was low,
278 M. Vezzone et al. / Environmental Pollution 252 (2019) 270e280
even though metal concentrations have exceeded the threshold
limits proposed by Brazilian law. In contrast to these results, our
bioassays revealed toxicity to T. viscana and E. lucunter embryos.
The toxicity to T. viscana was higher in northern sediments than
in southern ones and is strongly correlated with metal concentra-
tions and organic enrichment. The occurrence of high Cd, Zn, Pb
and Cu concentrations may explain such high toxicity levels since
these metals are known to be toxic to amphipods and marine or-
ganisms (Ahsanullah and Florence, 1984; Bat et al., 1998; Besser
et al., 2005; Spehar et al., 1978). These data are in agreement
with results found in other tropical estuarine systems and marine
areas in Brazil, whose toxicity was also highly correlated with the
increase of metal concentrations (Abessa et al., 2005; A. R. Cesar
et al., 2014; Rodrigues et al., 2017). Tiburonella viscana has
benthic habit, can ingest significant amounts of metal-
contaminated sediments or organic matter (Abessa et al., 1998)
and is apparently a very good bioindicator of sediment quality.
Metal uptake by T. viscana is highly dependent on sediment prop-
erties (Ahlf et al., 2009). In this respect, T. viscana can be exposed by
both ingestion and dermal contact with dissolved metals. The
gastric content of these organisms is able to induce metal desorp-
tion from sediment particles, when metal become more bio-
acessible to the metabolism (Ahlf et al., 2009).
On its hand, toxicity to E. lucunter was observed in both northern
and southern sediments. Thus, the toxicity to E. lucunter, in a
sediment-water interface test and is dependent on the transference
of contaminants from the sediments to water column, which in-
cludes metals and other substances. Thus, in further studies the
employment of selective acid extractions to determine potentially
bioavailable metal contents are highly recommended (Amato et al.,
2014). The monitoring of ammonia contents during the test
revealed concentrations that exceeded the limit of toxicity (11 mg/
L) for some samples (S4, N10, N11, N12, N13, S14, S15, S16) and
partially explains such high toxicity levels. Abessa et al. (2017),
when assessing the quality of sediments from marine protected
areas along the coast of Sa ~o Paulo (Brazil), suggested that the
toxicity to another tropical species of sea-urchin (Lytechinus varie-
gatus) was positively correlated to the release of ammonia to the
water column. On the other hand, the presence of ammonia causes
increased toxicity of metals (Camargo et al., 2015). Further studies
focused on the detailing of metal mobility in sediments may better
clarify these issues. In this context, the application of analytical
procedures involving metal sequential extraction and selective
extractions (using weak acidic extractors) (DePaula and Mozeto,
2001; Duodu et al., 2017; Tessier et al., 1979) or accumulation of
metals in biomonitor organisms (such as bivalves) are strongly
recommended.
5. Conclusions
The sediments from the Rodrigo de Freitas Lagoon were toxic to
T. viscana and especially to E. lucunter, and the toxicity can be
explained by the concentrations of metals and their combination
with ammonia. Metal concentrations in 2017 increased in com-
parison with data from 2015. Thus, urban interventions performed
in the RFL before the 2016 Summer Olympics negatively altered the
quality of the sediments. Metal distribution was highly correlated
with organic matter contents, nutrients, mud contents and low
values of pH. Furthermore, sediments from the northern sector of
RFL caused higher mortality rates on T. viscana and exhibited higher
metal concentrations than the sediments from the souther sector.
These results can support the establishment of programs focused
on public health and pollution control in the RFL, including the
identification of critical areas and the definition of the most
appropriated alternatives of remediation.
In further studies, ecotoxicological tests with local water sam-
ples and sediment tests with organisms from other trophic levels
are strongly recommended to support a better understanding of
the ecotoxicological risks of metals in the RFL. In addition, metal
mobility in sediments should be more carefully characterized in
order to evaluate its transference to water column.
Acknowledgments
The authors would like to thank the colleagues from the Mineral
Analysis Group (COAM) of the Centre for Mineral Technology
(CETEM/MCT) for their help in the chemical determinations.
Mariana Vezzone and Aline Serrano were supported by grants from
the National Brazilian Council for Scientific and Technological
Development (CNPq). The authors are also grateful to our col-
leagues from NEPEA-UNESP, for their support during the toxicity
tests. DMSA thanks CNPq (PQ 311609/2014-7). Finally, the authors
thank Dr. Wilson Machado from Federal Fluminense University for
the support with P analysis.
Appendix A. Supplementary data
Supplementary data to this article can be found online at
https://doi.org/10.1016/j.envpol.2019.05.094.
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