Environ Monit Assess (2018) 190:214
https://doi.org/10.1007/s10661-018-6570-1
Bioacumulation of trace elements in the crab Ucides cordatus
(Linnaeus, 1763) from the macrotidal mangrove coast region
of the Brazilian Amazon
Bruna Mariáh da S. e Silva & Gundisalvo P. Morales &
Ana Lúcia N. Gutjahr & Kelson do C. Freitas Faial &
Bruno S. Carneiro
Received: 1 December 2017 / Accepted: 20 February 2018
# Springer International Publishing AG, part of Springer Nature 2018
Abstract In this study, trace element concentrations
were measured in chelipod and gill samples of the crab
U. cordatus by induced coupled plasma optical emission
spectrometry (ICP OES). The element average concen-
trations between the structures were statistically com-
pared. Gill concentrations of Cu and Zn were higher in
female crabs, while in chelipods, Pb concentrations
were higher in males. The concentration of Zn in crabs
from Curuçá City were higher than the recommended by
health agencies, but the provisional tolerable daily in-
take value (PTDI), for Zn and Cu, showed only 10 and
23% contribution, respectively. The bioaccumulation
factor was higher than 1 for Cu (gills and chelipods)
and Zn (only for chelipods), which suggests bioaccu-
mulation for these elements. Further metallomic and
oxidative stress analyses are suggested, in order to eval-
uate possible protein and/or enzymatic biomarkers of
toxicity.
Keywords Environmental contamination . Uca crab .
Estuary . Environmental impact . Human health
B. M. d. S. e. Silva (*) : G. P. Morales : A. L. N. Gutjahr
Centro de Ciências Naturais e Tecnologia, Travessa Enéas
Pinheiro, Universidade do Estado do Pará, 2626, CEP, Belém, PA
66095-100, Brazil
e-mail: brunamariah.quimica@gmail.com
K. d. C. Freitas Faial : B. S. Carneiro
Instituto Evandro Chagas, Rodovia BR-316 km 7 s/n - Levilândia,
Ananindeua, PA 67030-000, Brazil
Introduction
Mangroves are highly fertile ecosystems with signifi-
cant biomass production, located in potentially
floodable areas of both tropical and subtropical regions
and influenced by local rainfall and tidal regimes
(Pinheiro et al. 2008; Spalding et al. 2010). The fauna
of this biome consists of complex sets of animals that
can be resident, semi-resident, or visitors, with fish,
shrimps, and crabs being significant (Castro et al. 2008).
Among crustaceans, the Ucides cordatus crab
(Linneaus 1763) Decapoda: Ucididae is noteworthy, pop-
ularly known as the Uçá crab. This macroinvertebrate is
endemic to the mangroves of the Atlantic coast of the
American continent, distributed from Florida (USA) to
Santa Catarina (Brazil) (Melo 1996). The Uçá crab is a
semi-terrestrial crustacean that inhabits the inter-tidal re-
gion and performs important environmental functions,
such as litter processing, organic matter cycling, and
sediment bioturbation (Pinheiro and Fiscarelli 2001;
Nordhaus et al. 2006; Conde et al. 2000; Guest et al.
2006; Amouroux and Tavares 2005).
Sediments are an important environmental compart-
ment, formed by the continuous deposition of autochtho-
nous particles produced in the water column and
alochthonous particles originating from watersheds
(Bacon and Davidson 2008; da Silva et al. 2014). They
display a high sorption capacity and are able to accumu-
late polluting species (Föstner and Wittmann 1981;
Carvalho and Lacerda 1992), such as trace elements.
However, factors such as bioturbation and tidal flow
may remobilize these compounds (Litheraty et al. 1987)
214 Page 2 of 15
and, thus, affect water quality and favor bioaccumulation
and transfer exchanges in the food chain (Phillips 1977;
Mallns et al. 1984), which may pose risks to the equilib-
rium between the environment and human health.
Contamination by trace elements of anthropogenic
origin and bioaccumulation of these compounds have
become a worldwide concern (Kabata-Pendias 2011),
since these species belong to a class of substances inca-
pable of being biodegradated (Cordovil et al. 2014),
which, when accumulated, have the potential to become
toxic. To evaluate the levels of these pollutants in ecosys-
tems, several macrobenthic invertebrates (Koosej et al.
2017; Çoğun et al. 2017; Kaya and Turkoglu 2017;
Hosseini et al. 2016; Sidding et al. 2017; Pinheiro et al.
2012; Chiba et al. 2011; Marques et al. 2010; Adams and
Engel 2014) and bivalve mollusks (Marengoni et al.
2013; Urbano de Araújo et al. 2010) and fishes (Hosseini
et al. 2015) have been used as biomonitors.
In mangroves, the use of U. cordatus as biomonitor is
associated to its low dispersion power (Andrade et al.
2011), since it lives in the vicinity of its galleries and has a
slow growth rate, of about 8 years (Pinheiro and Fiscarelli
2001). These characteristics allow this crustacean to ex-
press the existing conditions in its environment, allowing
for inferences regarding trace element levels.
In Brazil, studies on U. cordatus are concentrated
mainly in the state of São Paulo, in southeast Brazil.
Ortega et al. (2016), for example, evaluated physiolog-
ical differences in Uçá populations that inhabit man-
groves with different levels of Cd contamination, while
Duarte et al. (2016, 2017) corroborated the use of this
crustacean as an organism capable of indicating the
conservation/degradation state of mangroves through
biological responses to contamination, and Banci et al.
(2017) investigated the genetic diversity of Uçá in man-
groves presenting different levels of pollution.
The municipality of Curuçá, situated at geographical
coordinates 00° 43′ 48″ S and 47° 51′ 06″ W, is located in
the Macrotidal Mangrove Coast region of the Amazon
(CMMA) and is an important fishing center (Souza
2010), with adequate areas for maritime navigation. This
aroused the interest of large companies regarding the
future construction of two projects, the Espadarte Port
and the Transhipment Floating Station, through which
cargo and ores from the state of Pará may be transported
to other regions in Brazil, as well as other countries. With
the operation of these waterway terminals, risks of chem-
ical spillages, effluent leakages, addition of trace
Environ Monit Assess (2018) 190:214
elements to the environment, and consequent possibility
for bioaccumulation and biomagnification of these spe-
cies in the aquatic biota are increased.
The crab U. cordatus is an important mangrove fauna
representative and is widely consumed by the human
Amazon population. Despite this, no studies that deal
with the accumulation of metals in the region are avail-
able in this organism.
Thus, considering the role of trace elements as pol-
lutants and the absence of bioaccumulation studies of
these compounds in crustaceans in the municipality of
Curuçá, in the Macrotidal Mangrove Coast region of the
Amazon, the aim of the present study was to evaluate
the accumulation of zinc (Zn), chromium (Cr), copper
(Cu), cadmium (Cd), and lead (Pb) in Ucides cordatus
crab gills and chellopod muscle tissue, verify if the
detected concentrations are within the limits established
by regulatory organizations and determine if bioaccu-
mulation processes for these elements are in place.
Methodology
Study area
The study area (Fig. 1) is located at the CMMA, a region
that extends from Marajó Bay, (Pará) to Ponta de
Tubarão, São José Bay (Maranhão) and comprises an
area of 7591.09 km2, corresponding to 56.6% of Brazil’s
total mangroves swamps (Souza Filho 2005). The
CMMA is characterized by low reliefs varying from 0
to 80 m, wide coastal plains that reach up to 70 km in
width, and an extensive adjacent continental shelf, ap-
proximately 200 km wide, extremely irregular, indented
and cut by several estuaries. This region is subject to a
semidiurnal macrotidal regime, with variations of
around 4 m at Guajará bay, Belém (PA), and 7.5 m at
São Marcos Bay, São Luís (MA). The climate is well
defined, hot, and humid from July to December and
rainy from January to May, with rainfall varying from
2500 to 3000 mm per year and average temperature
around 26 °C (Souza Filho 2005).
A range of the world’s largest continuous man-
grove swamps, of 370.64 km2, is located at Curuçá,
protected by the Mãe Grande Marine Extractive Re-
serve, created by presidential decree on December 13,
2002 (Brasil 2002). The coastal zone of the munici-
pality is dominated by mangroves, restingas, beaches,
Environ Monit Assess (2018) 190:214 Page 3 of 15 214
68°0'0"W 54°0'0"W 40°0'0"W
8°0'0"N

8°0'0"N
6°0'0"S

6°0'0"S
Legal Amazon

48°0'0"W 46°0'0"W 44°0'0"W

20°0'0"S

20°0'0"S
Marajó Bay

Gurupi Bay

1°0'0"S

1°0'0"S
34°0'0"S

34°0'0"S
0 325 650 1.300
km
Turiaçu Bay
68°0'0"W 54°0'0"W 40°0'0"W 48°0'0"W 47°50'0"W 47°40'0"W

P6
2°0'0"S

2°0'0"S
B.S. P5
Pará
Marcos
P3
P4
Maranhão

0°40'0"S

0°40'0"S
P2
3°0'0"S

3°0'0"S
0 30 60 120
P1
km
Curuçá
48°0'0"W 46°0'0"W 44°0'0"W
Magalhães Barata
macrotidal mangrove coast of the Brazilian Amazon

0°50'0"S

0°50'0"S
Marapanim

Vigia São João Da Ponta

São Caetano De Odivelas

0 2,75 5,5 11
Terra Alta km

48°0'0"W 47°50'0"W 47°40'0"W

Sampling points

Fig. 1 Geographic location of the sampling points: P1-00° 43′ 46, 9″ S/47° 50′ 49, 4″ W; P2-00° 42′ 08, 5″ S/47° 52 38, 4″ W; P3-00° 38′
12, 5″ S/47° 53′ 27, 5″ W; P4-00° 38′ 41, 4″ S/47° 53′ 53, 2″ W; P5-00° 35′ 03, 5″ S/47° 52′ 05, 5″ W; P6-00° 34′ 30, 0″ S/55° 54′ 22, 0″ W

and dunes. The interior is dominated by family agri- Sample collection and processing
culture, capoeiras in various growth stages, and scarce
remnants of terra firme forests (Pantoja et al. 2012). Crabs
Regarding the soil, the predominance is of medium-
textured yellow latossol soil and indiscriminate man- At each sampling point, three males and three females
grove soils (Brasil 2013). U. cordatus specimens (SISBIO authorization no.
49353-1/authentication code 81473453) were collected
by the arm method, which consists of the removal of the
Sampling sites animal from its gallery with the use of the collector’s
arms. After collection, the crabs were stored in individ-
To quantify the accumulation of trace elements in Uçá ual plastic bags, placed in polystyrene boxes with ice,
crabs and verify their distribution in sediments along the and transported to the Chemistry Laboratory at the State
Curuçá mangrove strip, six sampling points, P1, P2, P3, University of Pará (UEPA). All specimens were cleaned
P4, P5, and P6, were defined (Fig. 1). Their geograph- in running water, brushed to remove any sediment de-
ical coordinates were recorded with the aid of a Global bris, and subsequently washed with distilled water.
Positioning System (GPS). The biometric data, cephalothorax width and length
Points P1 and P2 are located in the central part of the (CW and CL, respectively), were measured using a
municipality, near the urban center of Curuçá, and are precision digital caliper (0.01 mm). The classification
subject to anthropic interference (waste disposal). The of the specimens according to gender followed the
other points are located further away from the municipal method reported by Pinheiro and Fiscarelli (2001). Pre-
headquarters, where there is no record of human activ- viously decontaminated stainless scissors and tweezers
ities that can contribute to the enrichment of the envi- were used for gills and chellipod muscle tissue dissec-
ronment with trace elements. tion. The gills were selected due to their osmoregulatory
214 Page 4 of 15
function (Mantel and Bliss 1983) and the chellipod
muscle tissue, because it is an edible portion of the
animal that has higher mass and can act as a vector for
contaminant transfer. Samples (n = 72) were frozen in
Eppendorf tubes (− 20 °C) and transported to the Dr.
Edilson Brabo Toxicology Laboratory at the Evandro
Chagas Institute (IEC) for trace element quantification.
Sediment sampling
At each sampling point, a sediment sample from the
crab galleries was collected manually with a
polychloroethene paddle. The samples were stored in
plastic bags, identified with the corresponding sampling
point, placed in polystyrene boxes, and transported to
the Dr. Edilson Brabo Toxicology Laboratory at the
(IEC 2013) for trace element quantification.
Analytical procedures
Crab sample digestion
Approximately 0.1 g of chellipod muscle tissue and gills
were weighed on a digital analytical balance (TE2145,
Sartorius AG, ± 0.0001 g precision) and freeze-dried in
Falcon®-type polypropylene tubes for 48 h in a L101
Liotes lyophilizer. After freeze-drying, the samples were
crushed using a mortar and pestle and digested in an acid
medium.
The digestion process followed the method described
by Vinas et al. (2000), in which 3.0 mL of high-purity
nitric acid (HNO3 ≥ 65% v v−1) and 1.0 mL of hydrogen
peroxide (H2O2 30% v v−1) (Sigma-Aldrich) are added
to the samples, which are then digested with the aid of a
CEM microwave radiation (Mars Xpress) and made up
to 50 mL with ultra-pure water.
Sediment sample digestion
The sediment samples were dried at room temperature
and disaggregated using an agatha mortar and pestle.
The digestion process was conducted with approximate-
ly 0.25 g of the sediment samples (in triplicate) with the
following volumes of mineral acids: 3 mL nitric acid
(HNO3 65% v v−1); 1.0 mL hydrochloric acid (HCl 36%
v v−1); and 1.0 mL hydrofluoric (HF 36% v v−1)
Environ Monit Assess (2018) 190:214
(Biotec)—all high purity, and 1.0 mL of hydrogen per-
oxide (H2O2 30% v v−1) (Sigma-Aldrich).
The digestion was carried out in a closed system
(CEM microwave, Mars Xpress) according to the meth-
od described by Bettinelli et al. (2000). After dissolu-
tion, 2 mL of a saturated boric acid H3BO3 solution (5%
v v−1) (Sigma-Aldrich) were added to the flask, for
complexation of the remaining fluorides, and the sam-
ples were made up to 25 mL with ultra-pure water.
Analytical performance parameters
Trace element concentrations were determined using
inductively coupled plasma optical emission spectrom-
etry (ICP OES, Vista-MPX CCD Simultaneous, Varian,
Mulgrave, Australia). Tables 1 and 2 present the Pb, Cd,
Cr, Cu, and Zn determination parameters. The limits of
detection (LOD) were calculated according to Eq. 1,
described by Snyder et al. (1997) and Harris (2008).
LOD ¼ 3:3 x s=S; ð1Þ
where s is the estimate of the standard deviation of the
response, which may be the estimate of the standard
deviation of the blank, the regression line equation, or
the linear coefficient of the equation, and S is the slope
or angular coefficient of the analytic curve (Snyder et al.
1997; Harris 2008). Table 1 presents the Pb, Cd, Cr, Cu,
and Zn determination parameters.
The accuracy of the method was assessed by analysis
of certified reference materials (CRM), namely DORM-
3 (Dogfish muscle, National Research Council Canada-
NRC) and DOLT-3 (Fish liver, NRC) for crabs, and
SRM 2710 (Montana soil, National Institute of
Standards and Technology-NIST) and SRM 1646a (Es-
tuarine sediment, NIST) for sediments. The recoveries
obtained for the evaluated elements ranged from 84.7 to
112.0% for sediments and from 95.2 to 112.4% for crabs
(Table 2). Thus, the method was considered adequate for
the analysis of trace elements.
Statistical analyses
Data analyses were performed using the BioEstat® 5.3,
Origin 6.0 and Minitab 14 softwares. To evaluate trace
element concentrations in the crab and sediment
Environ Monit Assess (2018) 190:214 Page 5 of 15 214

Table 1 Data regarding the calibration curves of the evaluated trace elements

Parameters Element

Essential Non-essential

Zn Cu Cd Pb Cr

Wavelength (nm) 213.85 327.39 226.50 220.35 267.71

Correlation coefficient (R2) 0.9985 0.9956 0.9918 0.9925 0.9992
Linear range (mg/L−1) 0.0–3.2 0.0–3.2 0.0–3.2 0.0–3.2 0.0–3.2
LOD μg g−1 0.0011 0.0028 0.0025 0.0005 0.0014

samples between the collection points, a principal com-
ponent analysis (PCA—scores and loadings), an 18 × 5
matrix (18 chellipod samples and 5 variables), was used,
and hierarchical cluster analysis (HCA—dendrogram)
were performed. Two tests were used to verify the
existence of significant differences between the mean
values of element concentrations per structure between
sexes and between structures for the same sex: the
Student t test, when data distribution was normal and
homoscedastic variance was present, and Mann-
Whitney test (U), when these conditions were not satis-
fied. The Shapiro-Wilk test (W) was used to analyze
data distribution. Pearson’s parametric correlation anal-
ysis was used to evaluate possible significant
relationships between biometric data and trace element
concentrations in chellipod muscle and gills. Signifi-
cance was set at p < 0.05.
Results and discussion
Trace element concentrations
In crab tissues among sampling points
In order to verify the trace element concentrations in
male chellipod samples between the collection areas, a
PCA was performed using an 18 × 5 matrix (18

Table 2 Analytical recovery of Pb, Cd, Cr, Cu, and Zn in certified reference material

CRM Element Observed value Certified value Recovery (%)

(mg kg−1) (mg kg−1)

DORM-3 Cu 14.7 15.5 ± 0.63 95.2

Cd 0.326 0.290 ± 0.020 112.4
Zn 51.6 51.5 ± 3.1 100.5
Pb 0.402 0.395 ± 0.050 101.7
Cr 2.12 1.89 ± 0.17 112
DOLT-3 Cu 32.3 31.2 ± 1.0 103.5
Cd 19.2 19.4 ± 0.6 98.9
Zn 117.3 86.6 ± 2.4 103.4
Pb 0.351 0.319 ± 0.045 110.0
SRM 2710 Cu 3306.4 2950 112.0
Cd 18.5 21.8 84.7
Zn 6366 6952 91.5
Pb 5263.5 5532 95.1
SRM 1646a Cr 35.6 40.9 87.0
214 Page 6 of 15 Environ Monit Assess (2018) 190:214

chellipod samples and 5 variables). In addition, to con-
firm the trends observed in the PCA, an HCA was also
applied. The tests indicate two groups, in which samples
from areas under anthropic influence resemble those not
subject to pollution sources. Therefore, the level of trace
elements intake from crab consumption is similar be-
tween areas. This may indicate that the pollutants are
being adsorbed by sediments (in the areas that receive
pollutants) and are unavailable to the local biota (Fig. 2).
Per tissue between sexes
The results obtained herein (Table 3) indicate statistical-
ly significant differences (p < 0.05) for the mean con-
centrations of trace elements in gills between sexes for
Cu and Zn, with females presenting the highest concen-
trations. These elements are essential in decapod crus-
taceans (Virga and Geraldo 2008), since Cu acts as an
important member of the hemocyanin respiratory pig-
ment and Zn as an activator of enzyme systems
(Rainbow 1997).
These elements can be introduced into living organ-
isms through water ingestion and respiration, or be
adsorbed through the skin (Virga et al. 2007). However,
both can be potentially toxic when available in excess in
the aquatic environment (Martins et al. 2011).
Macfarlane et al. (2000), while studying the terrestrial
crab Heloecius cordiformis, found that females accumu-
late higher Cu and Zn amounts when compared to
males, and indicated that this is a function of sexual

Fig. 2 a Score graph of the Cd,

Cr, Cu, Pb, and Zn variables for
chelipod samples between the
collection points (P1: 1, 2, 3; P2:
4, 5, 6; P3: 7, 8, 9; P4: 10,11,12;
P5: 13,14,15; P6: 16,17,18). b
Dendrogram obtained for the crab
samples (n = 18) by the HCA, for
the Cd, Cr, Cu, Pb, and Zn
variables between the collection
points (P1: 1, 2, 3; P2: 4, 5, 6; P3:
7, 8, 9; P4: 10, 11, 12; P5: 13, 14,
15; P6: 16, 17, 18)
Environ Monit Assess (2018) 190:214 Page 7 of 15 214

Table 3 Element concentrations (dry weight) in male (M) and males and females (Table 3). This may be associated to
female (F) U. cordatus gills and chellipod muscle tissue sampled
the fact that this organ is the most important site for ionic
from Curuçá, Pará, Brazil
and respiratory exchanges (Boitel and Truchot 1989)
Element Sex Chellipod concentrations Gill concentrations and shows high permeability and passive adsorption of
(μg g−1) (μg g−1) dissolved trace elements (Rainbow 1988).
Essential
Chellipod muscle tissue was the main accumulation
site for Zn (p < 0.05) in both sexes, which may be
Cu M 28.9–42.29 119.3–159.5
related to the performance of this element in muscle
(35.0 ± 4.8) (141.7 ± 15)
contraction or the presence of metal-bound proteins
Cu F 32.1–47.5 143.9–189.9
(Bryan 1967; Eisler 1981). Similar results were found
(42.4 ± 6.3) (169.5 ± 18)
for the decapod species Portunus pelagicus (Al-
Zn M 300–346 84.8–103.8
Mohanna and Subrahmanyam 2001), and Callinectes
(315.5 ± 17) (92 ± 8.5)
sapidus (Jop et al. 1997). It is noteworthy that Zn is an
Zn F 262.6–359.7 90–128.2
essential element for crabs; however, at high levels, it
(315.8 ± 38) (116.4 ± 15)
can become toxic (Phillips and Rainbow 1993) and
Non-essential
cause decreases in oxygen consumption and growth
Cd M 0.0025–0.12 0.08–0.3 delays (Wu and Chen 2005; Barbieri 2009).
(0.03 ± 0.050) (0.2 ± 0.10)
Cd F < 0.0025 0.0025–0.2
* (0.1 ± 0.081) Biometric data
Cr M 1.4–2.7 4.3–5.4
(2.3 ± 0.51) (4.9 ± 0.42) The biometric data of cephalothorax width (CW) and
Cr F 0.9–4.6 4.5–9.2 cephalothorax length (CL) ranged from 45 to 81 mm
(2.5 ± 1.4) (6.4 ± 1.8) and from 37 to 55 mm, respectively. Pearson’s paramet-
Pb M 0.0005–2.3 0.7–4.7 ric correlation for body size and trace element concen-
(1.0 ± 0.91) (2.3 ± 1.4) tration in the evaluated tissues showed positive correla-
Pb F 0.0005–3.5 0.008–3.0 tions between Cd and both CW and CL (r = 0.6053; r =
(0.9 ± 1.4) (1.9 ± 1.3) 0.6129) and negative correlations between Cr (r = −
*Not established; minimum-maximum values; (means ± standard
0.6141; r = − 0.6272) and Zn (r = − 0.6299; r = −
deviation) 0.6345) in gills. However, the determination coefficients
were not representative and could not be used to
maturity. This reproductive specificity for females can correlate the concentration of these elements to CW
explain the differences in the concentrations of these and CL.
elements between sexes observed in the present study. Cu and Pb were not correlated to the biometric data,
When comparing chellipod element concentrations similarly to what was observed in the study by Pinheiro
between sexes, a statistically significant difference et al. (2012) regarding U. cordatus from the Cubatão
(p < 0.05) was observed for Cu. The greater accumula- region, Brazil, and contrasting to the reports by Andrade
tion of Cu in females may occur due to the need for this et al. (2011) regarding Callinectes ornatus at the
element for the production of egg yolks (Virga and Iquapari Lagoon in the state of Rio de Janeiro, (negative
Geraldo 2008) as well as due to the different metabolic correlation for Cu and positive for Zn) and Virga and
activities and growth rates between sexes (Barrento et al. Geraldo (2008) who observed an accumulation trend in
2009; Yilzmar and Yilzmar 2007). Callinectes sp., with smaller individuals presenting
higher Cu, Zn, Cd, Cr, and Pb concentrations.
These variations may be related to the ecological and
Between tissues in the same sex physiological differences of each organism, or may be
associated with environmental specificities that may
When comparing the trace element concentrations be- affect the bioavailability of these elements and, there-
tween the tissues per sex, gills were shown to accumu- fore, cause different bioaccumulation patterns (Ribeiro
late higher amounts (p < 0.05) of Cr, Cu, and Cd in both et al. 2005; Burattini and Brandelli 2006).
214 Page 8 of 15 Environ Monit Assess (2018) 190:214

Trace elements in sediment Council of Ministers of the Environment (CCME),

Concentration and distribution
throughout the collection points
Except for Zn, all other elements presented higher con-
centrations at P6. This may be associated with a higher
relief slope at this point, contributing to the natural
erosion process, or related to sediment type and
granulometry.
Trace element analyses in sediments allow for the
detection of pollutants that may be absent or present
only in small concentrations in the water column.
Knowledge on the distribution of these elements in
coastal sediments provides a record of the spatial and
temporal history of a particular region or ecosystem
(Davies et al. 2006). No specific legislation establish-
ing limits for trace element concentrations in estua-
rine sediments is available in Brazil. In order to verify
the impact caused by the presence of these elements
and sediment quality regarding chemical pollutants,
the criterion established by the Canadian legislation
(Canada 1999) and adopted by the Environmental
Company of the State of São Paulo (CETESB) was
considered herein. According to the Canadian
two limits and three ranges for saline and saline water
sediments exist: the threshold effect level, or TEL,
which indicates the level below which there is no
adverse effect on the biological community; probable
effect level, or PEL, which is the level above which
adverse effects on the community are likely to occur
and the range between TEL and PEL, representing the
possible occurrence of adverse effects on the biolog-
ical community.
Table 4 displays the results for the sediments at
collection points P1 to P6, as well as the TEL-PEL
levels for the elements evaluated herein. Cd concentra-
tions were higher than both the TEL and PEL, which
may represent the probable occurrence of adverse ef-
fects to the biological community. Cr was present at
concentrations higher than the TEL and lower than the
PEL, while the other elements were present in concen-
trations below the established limits.
Comparison between sampling points
A concentração de elementos traços nos sedimentos
entre os pontos de coleta foi avaliada por meio da
PCA, utilizando uma matriz 18 × 5 (18 amostras de

Table 4 Sediment trace element concentrations (μg g−1) determined in triplicate, from U. cordatus galleries at Curuçá, Pará, and reference
values established by the Canadian Council of Ministers of the Environment (CCME)

Sampling point Element

Non-essential Essential

Cd Cr Pb Zn Cu

P1 3.9–4.2 51.4–51.6 15.9–19.8 65.0–65.3 9.0–9.3

(4.1 ± 0.16) (51.5 ± 0.16) (17.8 ± 2.7) (65.1 ± 0.24) (9.2 ± 0.24)
P2 4.0–4.1 49.0–50.1 19.6–22.9 69.1–69.3 8.9–9.7
(4.0 ± 0.07) (49.5 ± 0.57) (20.7 ± 1.8) (69.2 ± 0.12) (9.4 ± 0.46)
P3 4.6–4.9 58.7–60.5 21.9–22.5 66.0–68.1 10.3–10.7
(4.7 ± 0.18) (59. 6 ± 0.91) (22.2 ± 0.30) (66.8 ± 1.1) (10.5 ± 0.18)
P4 3.6–4.0 44.5–45.2 10.9–14.9 106.6–109.3 9.0–9.2
(3.7 ± 0.20) (44.8 ± 0.36) (12.5 ± 2.1) (107.8 ± 1.3) (9.1 ± 0.12)
P5 4.7–4.8 60.3–61.6 12.7–17.8 73.3–75.7 12.1–12.3
(4.7 ± 0.06) (61.2 ± 0.78) (15.7 ± 2.6) (74.2 ± 1.3) (12.2 ± 0.14)
P6 5.6–5.9 86.4–87.1 17.0–25.5 86.2–87.2 13.3–14.5
(5.8 ± 0.13) (86.8 ± 0.36) (21.5 ± 4.2) (87.0 ± 0.18) (13.8 ± 0.63)
TEL 0.6 37.3 35.0 123 35.7
PEL 3.5 90.0 91.3 315 197

*Minimum-maximum values; (means ± standard deviation)

Environ Monit Assess (2018) 190:214 Page 9 of 15 214

Fig. 3 Score graphs (a) and

loadings (b) for the variables Cd,
Cr, Cu, Pb, and Zn in the sediment
samples from the crab galleries
Group 1
between the collection points (P1: Group 2
1, 2, 3; P2: 4, 5, 6; P3: 7, 8, 9; P4:

Secundary components
10, 11, 12, 13, 14, 15; P6: 16, 17,
18). c Dendrogram obtained for
the sediment samples (n = 18) by
HCA from the Cd, C, Cu, Pb, and
Zn variables (P1: 1, 2, 3; P2: 4, 5,
6; P3: 7, 9, 9; P4: 10, 11, 12; P5:
13, 14, 15; P6: 18) Group 3

Group 4

(A) Principal components

Pb
Secondary components

Cd
Cr

Cu

Zn

(B) Principal components

Sample bonding dendrogram and euclidean distance

Similarity

(C) Samples

sedimentos e 5 variáveis). As tendências de confirmadas pelo HCA (Fig. 3c). Os testes

correlações observadas por meio das PCA foram mostraram que a concentração de elementos traços
214 Page 10 of 15 Environ Monit Assess (2018) 190:214

nas áreas sob influência antrópica é similar (grupo 1).
Os demais grupos (2, 3, e 4) correspondem aos
pontos que estão livres de descarte de poluentes.
Figure 3a illustrates the similarities between the sam-
ples (scores), while Fig. 3b illustrates the similarity
between the variables (loadings).
element is in its available form. Therefore, methods
capable of indicating the bioaccumulation process and
not only quantifying trace element concentrations must
be applied, since low concentrations in the sediments do
not imply unavailability to organisms.

Bioaccumulation factor Comparison of trace element concentrations

The ability of U. cordatus to accumulate trace elements
was determined by means of the bioaccumulation factor
(BF) calculated according to Eq. 2, described by Negri
et al. (2006).
Metal concentration in the body compartmentðMCBCÞ
BF ¼
Metal concentration in the sedimentðMCSÞ
ð2Þ
Bioaccumulation is recognized when trace element
concentrations in organisms are higher than in sediment.
When MCBC ≥ 1 bioaccumulation is considered to
have occurred (Klavins et al. 1998), bioaccumulation
is characterized by a process in which a chemical is
absorbed by the body through diverse routes, as occurs
in the environment, such as food ingestion, or through
environmental compartments (Arnot and Gobas 2006).
The BF was calculated for male crab gills and
chellipod tissue. The results obtained herein suggest
bioaccumulation of Cu and Zn. Similar results were
observed for Carcinus sp. (Falusi and Olanipekun
2007). For Cu, the BF was higher for gills, whereas
for Zn, bioaccumulation occurred only in the chellipod
tissue. These results corroborate the bioaccumulation
trend of these elements in specific organs.
Although Cu concentrations were below the TEL,
BF values indicate that the largest fraction of this
in U. cordatus chellipod muscle tissue with levels
recommended by health agencies and daily trace
element intake by the human population
The Food and Agriculture Organization of the United
Nations (FAO), the United States Environmental Pro-
tection Agency (EPA), the World Health Organization
(WHO), European Community Regulation (EU), Euro-
pean Commission (EC), and the United Kingdom Min-
istry of Agriculture, Fisheries and Food (MAFF) are
international organizations that regulate the tolerable
levels of trace elements and inorganic contaminants in
food. In Brazil, this regulation is carried out by the
National Sanitary Surveillance Agency (ANVISA). Ta-
ble 4 displays the mean values obtained herein alongside
the maximum permissible values recommended by the
FAO/WHO, EU, EC, MAFF, ANVISA, and the con-
centration ranges considered adequate by the EPA.
In the present study, Zn concentrations were above
the maximum permissible limits. Pb concentrations
were above the EU recommended value, but well below
the other recommendations. The concentrations for the
other elements were lower than those established by
most health agencies (Tables 5 and 6). Although the
mean Cr content was higher than that allowed by the
Brazilian legislation, concentrations are still far below
those established by the FAO/WHO.

Table 5 Mean concentrations (μg g−1, wet weight) of the elements determined in muscle tissue of U. cordatus males and females from
Curucá, Pará, Brazil compared to the maximum limits recommended by health organizations

Element Organization Curuçá-PA

Non-Essential FAO/WHO Brazil EPA EC EU MAFF Males Females

Cd 1 1 0.1–2.0 0.05 0.1 0.2 < 0.01 < 0.01
Cr 12 0.1 0.1–0.9 – – – 0.46 0.50
Pb 2 2 0.1–0.8 0.2 0.1 2.0 0.21* 0.19*
Essential
Cu 30 30 1.0–20.0 – 10 20 7.01 8.49
Zn 50 50 10.0–30.0 – – 50 63.10* 63.17*

*Values above the maximum permissible levels established by health agencies

Environ Monit Assess (2018) 190:214 Page 11 of 15 214

Table 6 Consumption of crabmeat by the human population in The WHO has proposed provisional maximum
comparison to the provisional tolerable daily intake (PTDI) of
daily intake limits of these elements with the aim of
trace elements established by the World Health Organization, for
an adult person of 60 kg guiding the sanitary surveillance organs. The provi-
sional values of tolerable daily intake (PTDI-) [65]
Element PTDI WHO Mean ingestion of 100 g for the analyzed elements are presented in Table 4
(wet weight) of crab meat
and were determined considering a mean human
Non-essential body mass of 60 kg.
Cd 60 μg day−1 1 μg day−1 (1.6%) With the results found in the muscle of the male crabs
Cr 1000 μg day −1
46 μg day−1 (4.6%) listed in Table 5, the average ingestion of trace elements
Cu 3000 μg day −1
701 μg day−1 (23%) per 100 g of crabmeat was determined. The males were
Essential chosen, because female consumption is prohibited, ac-
Zn 60,000 μg day−1 6310 μg day−1 (10%) cording to the Brazilian Institute of Environment and
Pb 210 μg day−1
21 μg day−1 (10%)
Natural Renewable Resources (IBAMA). In order to
obtain 1 kg of meat from this crustacean, 25 to 30
animals are needed (IBAMA 2007), and the average
The data obtained in dry weight were converted to consumption of the population is around three crabs.
wet weight and compared to the limit values established Thus, the corresponding mass will be of approximately
by the international regulatory agencies. This conver- 100 g of crabmeat.
sion was performed by dividing the value obtained in The contribution to the PTDI due to the con-
dry weight by 5.0 (Jesus et al. 2003). sumption of crabmeat is more significant for Cu
Considering that the Uçá crab is one of the main (23%—Table 4), although it does not seem to indi-
fishing resources explored in the municipality of Curuçá cate health risks, since the normal adult diet varies
and is widely consumed as a protein source by the from 2000 to 5000 μg Cu day−1 (ILSI 2014). Thus,
human population of Pará, this crustacean can be a the consumption of mangrove crabs from Curuçá
significant source of trace elements. Thus, it is important does not represent health risks, even though Zn
to determine the contribution of this decapoda with levels were above the limit recommended by the
regard to daily trace element intake. health agencies.

Table 7 Mean concentrations of trace elements μg g−1 in U. cordatus crabs from different areas of Brazil

Study area Species Element

Essential Non-essential

Zn Cu Cd Pb Cr

Curuçá, PAa U. cordatus 63.10 7.01 0.01 0.21 0.46

Baía de Todos os Santos, BAb U. cordatus 72.42 16.62 0.05 * *
Estuário dos Rios Jundiaí e Pontegi, RNc U. cordatus 68.72 10.65 0.13 3.87 0.36
Baía de Vitória, ESd U. cordatus 62 4.8 0.021 * *
Cubatão, SPe U. cordatus * 5.31 0.10 < L.D 0.25
f
Baixada Santista, SP U. cordatus 67.0 11.0 < L.D < L.D *
*
Not analyzed
a
Present study
b
Ramos (2012)
c
Lopes (2012)
d
Jesus et al. (2003)
e
Pinheiro et al. (2012)
f
Merfa (2010)
214 Page 12 of 15
Mean concentration of trace elements μg g−1 (wet
weight) in Ucides cordatus from different regions
of Brazil
In general, trace element concentrations observed for
the Curuçá crab samples were lower than the concen-
trations found in other regions of Brazil (Table 7).
However, although Curuçá shows only incipient
sources of pollution, higher concentrations of Zn,
Cu, and Cr were found when compared to crabs from
Rio Grande do Norte and Cubatão (São Paulo), areas
known to be intensely affected by urban and indus-
trial waste pollution. However, it is known that most
of the soils of the study area originate from the
Barreiras Formation and are largely leached by in-
tense tropical weathering, similar to the behavior
observed in other Amazon soils (Berrêdo et al.
2008). Thus, it can be presumed that these concen-
trations may be related to natural trace element back-
ground, and, therefore, show a natural, non-anthro-
pogenic, origin.
Conclusions
The present study provided information on the accu-
mulation of Cu, Zn, Pb, Cd, and Cr and in
U. Cordatus crabs in Amazon macrotidal mangroves
and indicates that this crustacean could be used as a
sentinel contamination organism. Regarding the ana-
lyzed elements, the results obtained herein suggest no
risks to humans in relation to the provisional tolera-
ble daily intake, as values for the evaluated elements
did not surpass 23%. The bioaccumulation factor was
higher than 1 for Cu (gills and chelipods) and Zn
(only for chelipods), which suggests bioaccumulation
for these elements. Further metallomic and oxidative
stress analyses are suggested, in order to evaluate
possible protein and/or enzymatic biomarkers of
toxicity.
Acknowledgments The authors would like to thank the
Evandro Chagas Institute (IEC) and the Dr. Edilson Brabo
Ecotoxicology Laboratory by the collaboration in carrying
out the analyses. Thanks are also due to the Coordination of
Improvement of Higher Education Personnel (CAPES) for
financial assistance.
Environ Monit Assess (2018) 190:214
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