Journal of Threatened
Taxa | www.threatenedtaxa.org | 26 December 2023 | 15(12): 24396–24401
ISSN 0974-7907
(Online) | ISSN 0974-7893 (Print)
https://doi.org/10.11609/jott.8765.15.12.24396-24401
#8765 | Received 04 October 2023 | Final received 21 November 2023 |
Finally accepted 28 November 2023
Nonessential elements (Al, As,
Cd, & Pb) in shrimps and mussels from
southeastern Brazil
Ana Paula Madeira Di Beneditto 1, Inácio Abreu Pestana 2, Dayvison Felismindo Lima 3
& Roberto Weider de Assis Franco 4
1–4 Universidade Estadual do Norte
Fluminense Darcy Ribeiro, Laboratório de Ciências Ambientais and Laboratório de Ciências Físicas,
Av. Alberto Lamego, 2000, Campos
dos Goytacazes, RJ, 28013-602, Brazil.
1 anapaula@uenf.br (corresponding author), 2 inacio@uenf.br,
3 lima@pq.uenf.br, 4 franco@uenf.br
Editor: Anonymity requested. Date of publication: 26 December 2023
(online & print)
Citation: Di Beneditto, A.P.M., I.A. Pestana,
D.F. Lima & R.W.deA.
Franco (2023). Nonessential elements (Al, As, Cd, & Pb)
in shrimps and mussels from southeastern Brazil. Journal of Threatened Taxa 15(12): 24396–24401. https://doi.org/10.11609/jott.8765.15.12.24396-24401
Copyright: © Di Beneditto et al. 2023. Creative Commons Attribution 4.0
International License. JoTT allows unrestricted use, reproduction, and distribution
of this article in any medium by providing adequate credit to the author(s) and
the source of publication.
Funding: Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) (grant no. 302.598/2021-9); Fundação Carlos Chagas Filho de Amparo à Pesquisa do Estado do Rio de Janeiro (FAPERJ) (grants no. E-26/210.498/2019, E-26/200.797/2021 and E-26/200.586/2022).
Competing interests: The authors declare no competing interests.
Author details: Di Beneditto, A.P.M.: PhD in Biosciences and Biotechnology; Professor at Universidade Estadual do Norte Fluminense Darcy Ribeiro; and specialist in conservation of marina fauna. Pestana, I.A.: PhD in Ecology and Natural Resources; Researcher at Universidade Estadual do Norte Fluminense Darcy Ribeiro; Professor at Universidade Federal Fluminense; and specialist in biogeochemistry and statistic modelling. Lima,
D.F.: PhD in Sciences;
Reseacher at Universidade Estadual do Norte Fluminense Darcy Ribeiro; and specialist in condensed matter. Franco, R.W.A.: PhD in Sciences - Applied Physics; Professor at Universidade Estadual do Norte Fluminense Darcy Ribeiro; and specialist in condensed matter.
Author contributions: APMDiB—project administration, funding acquisition, conceptualization and investigation, shrimps sampling, writing - original draft, writing - review & editing. IAP—conceptualization and investigation, formal analysis, writing - review & editing. DFL—mussels sampling, writing - review & editing.RWAF—project
administration, funding acquisition, mussels sampling, writing - review & editing.
Acknowledgements: We are indebted to fishers who
provided the shrimps for this study and to B.C.V. Oliveira for elements
determination. This research was funded by Conselho
Nacional de Desenvolvimento Científico
e Tecnológico (CNPq) (grant
no. 302.598/2021-9) and Fundação Carlos Chagas Filho
de Amparo à Pesquisa do Estado do Rio de Janeiro
(FAPERJ) (grants no. E-26/210.498/2019, E-26/200.797/2021 and
E-26/200.586/2022).
Abstract: The bioaccumulation of
nonessential elements (Al, As, Cd, & Pb) in
shrimps and mussels from southeastern Brazil (21°S–23°S) were compared. The
objective was to verify and confirm the differential responses of elemental
assimilation at both the taxonomic and spatial level. Two hypotheses were
predicted: i) shrimps have lower element
concentrations than mussels, and ii) both shrimps and mussels from the highly
polluted site have higher element concentrations. The results confirmed the
first hypothesis. The intense filter feeding activity of mussels explains the
taxonomic difference. The second hypothesis was not validated. Both shrimps and
mussels from the highly polluted site (Guanabara Bay) have lower elemental
concentrations than individuals from the less polluted site. This finding is
explained by the large inputs of sewage that result in partially reducing
conditions of the water and high sedimentation rates, maintaining elements
buried in anoxic sediment and making them unavailable for biological uptake. To
understand what drives the bioaccumulation of chemical elements in marine
animals it is necessary to know the species feeding habits and physiology, and
the habitat characteristics in each region.
Keywords: Artemesia longinaris, Atlantic Ocean, Brazilian
coast, hazardous elements, Penaeus brasiliensis, Penaeus paulensis, Perna perna, pollution, Rio de Janeiro State, Xiphopenaeus kroyeri.
INTRODUCTION
Fish and shellfish are important
to food security because they are readily available sources of animal protein
that people can self-harvest throughout the year (Henchion
et al. 2017). Thus, it is important to determine if the target species are safe
for consumption regarding the presence of harmful agents (bacteria, viruses,
parasites) and / or the concentration of chemicals (nonessential elements and
other pollutants) (WHO 2019). In the aquatic environment, nonessential elements
can concentrate in all compartments (water, sediment, and biota), reaching
consumers via trophic transfer (Ali et al. 2019). The concentrations of
chemical elements tend to be higher in more industrialized and populous areas
than in areas with lower anthropic influence (Wang et al. 2013; Delgado et al.
2023).
Aluminum (Al), arsenic (As),
cadmium (Cd), and lead (Pb), for instance, are
biologically nonessential elements with known adverse effects. Toxic effects of
Al, for instance, induce oxidative stress, immunologic alterations, and other
metabolic disorders (Igbokwe et al. 2019). Arsenic is responsible for several
types of cancer, especially those affecting the skin (Palma-Lara et al. 2020).
Cadmium and Pb are related to neurological and kidney
damage (WHO 2019). The concentrations of these elements in the fishery
resources are highly variable among species (Wang et al. 2013; Silva et al.
2021).
Shrimps of the Penaeidae family are targeted by marine fisheries worldwide
(FAO 2020). In Brazil, they are key resources for the economy of coastal
communities (Boos et al. 2016). In southeastern Brazil, Xiphopenaeus
kroyeri Heller, 1862, Artemesia
longinaris Bate, 1888, Litopenaeus
schmitti Burkenroad,
1936, Penaeus brasiliensis
Latreille, 1817, and P. paulensis
Perez Farfante, 1967 are the main target species
(Boos et al. 2016). Shrimps are omnivorous secondary consumers with high
feeding plasticity, ingesting mainly other benthic invertebrates, particulate
organic matter, and benthic algae (Albertoni et al.
2003; Di Beneditto et al. 2012; Willems et al. 2016).
Shrimps accumulate chemical elements mainly from feeding, whether essential or
nonessential for their metabolism (Boudet et al.
2019; Di Beneditto et al. 2023).
In Brazil, the mussel Perna perna (L.) (Mytilidae family) is a naturalized exotic species that has
become the main species of Brazilian mussel farming (Resgalla
et al. 2008; Silva et al. 2018). The high abundance of P. perna off the Brazilian coast has made it a key
resource for traditional communities that practice extractive fishing (Antunes
& Mesquita 2018). Mussels are suspension-feeding organisms that obtain
nutrition by filtering particulate organic matter, comprising algae, detritus,
and bacteria, out of the water column (Berry & Schleyer
1983). Due to their intense filtering activity, bivalve mollusks have a
well-known capacity to accumulate chemical elements in different tissues, with
overall higher concentrations than other marine organisms, such as fish,
shrimp, crabs, and cephalopods, from the same area (Wang et al. 2013; Catry et al. 2021).
This study compares the
concentrations of the nonessential elements Al, As, Cd and Pb
in the edible portion of shrimps and mussels from southeastern Brazil (220S,
430W and 230S, 410W) to verify taxonomic and
spatial patterns regarding element assimilation. We predicted two hypotheses: i) shrimps have lower element concentrations than mussels,
and ii) shrimps and mussels from highly polluted sites have higher element
concentrations.
METHODS
The samplings were performed
between 2020–2022 in the coastal waters of Rio de Janeiro State, Southeast
Brazil (Figure 1). The sampling sites were named sites I and II. Site I is less polluted, facing an open sandy beach in northern Rio
de Janeiro State (Figure 1). At this site, we sampled the shrimps X. kroyeri and A. longinaris
and the mussel P. perna. Site II is highly
polluted, located inside the Guanabara Bay (Rio de Janeiro municipality), which
is a semi enclosed oceanic bay with 400 km2, densely populated (~12 million
people live around it) and industrialized (~6,000 industries around it) (Figure
1). At this site, we sampled the shrimps P. brasiliensis
and P. paulensis and the mussel P. perna. All shrimps were sampled from local fisheries,
while mussels were sampled directly from rocky intertidal zones.
After sampling, the individuals
were stored in clean plastic bags inside an icebox and transported to the
laboratory. The abdominal muscle (edible portion) of each shrimp and the soft
tissue of each mussel (edible portion) were removed, stored in a dry sterile bottle,
frozen (-20 °C), freeze-dried and homogenized to a fine powder using a mortar
and pestle. The
nonessential elements Al, As, Cd, & Pb were
determined in each individual using ICP‒OES (Inductively Coupled Plasma-Optical
Emission Spectrometry, Model 720 ES, Varian Liberty Series II, USA). Freeze-dried muscle (0.5 g) was solubilized in 10 mL of 65%
HNO3 and heated in a digester block. Subsequently, samples were
resuspended in 5 mL of 0.5% HNO3 at 60 °C, filtered and brought to a
final volume of 20 mL with 0.5% HNO3. An analytical control solution
was prepared to check for contamination, and a reference material (DORM-4 fish
protein, National Research Council of Canada) was analyzed to test the
precision and accuracy (recovery values above 90%). The coefficients of
variation among analytical replicates were <10%. All concentrations were
determined in µg g-1 of dry weight.
Statistical analyses were
performed using the R program (R Core Team 2023) considering a type I error of
5% (α = 0.05). Descriptive statistics are reported as the median and
interquartile range. An analysis of variance (ANOVA) followed by Tukey’s test
was used to evaluate the differences in the element concentrations regarding
taxonomic groups and sampling sites. Mathematical transformations were used
whenever necessary to meet the assumptions of normality, linearity, and
homoscedasticity of residues using a maximum likelihood function (Venables & Ripley 2002). ANOVA assumptions were
validated using diagnostic plots (Altman & Krzywinski
2016).
In addition to comparing each
element separately, we also calculated and compared the normalized total load
between taxonomic groups and sampling sites. It provides a holistic view of the
elements’ pathways, as detailed in Agostinho et al. (2021). The normalized
total load represents the sum of element concentrations in each individual
weighted by the number of elements detected in that individual (element load),
as follow:
RESULTS AND DISCUSSION
Samplings included two shrimp
species from each site (site I: A. longinaris
and X. kroyeri; and site II: P. brasiliensis and P. paulensis),
and to avoid biased interpretation, we tested whether the element concentration
was species dependent. The ANOVA results showed that in most cases (75%), the
species from the same site did not show significant differences (p >0.05)
regarding element concentrations. Therefore, we grouped them only as ‘shrimps’
for further comparisons.
The results confirmed the first
hypothesis that shrimps do have lower element concentrations than mussels,
except for As at site I (Table 1 & Figure 2). This finding was corroborated
by the normalized total load of nonessential elements, which was 13 times and
25 times lower in shrimp than in mussels at sites I and II, respectively (Table
1). The higher elemental concentration in the tissues of bivalve mollusks
concerning other marine organisms (invertebrates and vertebrates) that share
the environment is well documented elsewhere (e.g., Wang et al. 2013; Suami et al. 2019; Catry et al.
2021). The higher concentrations are explained by the suspension-feeding habit
of bivalves, with intense filtering activity, the elements are transferred to
the tissues through phytoplankton, which is at the base of the marine food
chains (Santos & Boehs 2023).
Conversely, the results did not
support the second hypothesis predicted in this study. Both shrimps and mussels
from the highly polluted site (site II) had lower elemental concentrations than
individuals from the less polluted site (site I) (Table 1 & Figure 2). The
normalized total load of nonessential elements followed the same trend: six
times lower in shrimps from site II and three times lower in mussels from site
II (Table 1). The only exception was the Pb
concentration in mussels, which was higher in individuals from site II.
Site II is Guanabara Bay (Figure
1). This semi-enclosed coastal bay suffers from several forms of anthropogenic
impact threats. The edge and surroundings of this bay are heavily urbanized,
receiving inputs from industrial and domestic sewage and residuals of crops
(Soares-Gomes et al. 2016). Thus, a higher nonessential element concentration
in organisms at site II would be expected. Site I, in turn, is an open coastal
area of northern Rio de Janeiro State, sparsely populated, and whose only
noteworthy anthropogenic activity in coastal waters is the Açu Harbor cargo
handled (solid and liquid bulk, iron ore and oil) that began in 2014 (Zappes et al. 2016).
The unexpected result regarding
the spatial pattern of element assimilation by the target species can be
explained by the geochemistry of Guabanara Bay.
Carvalho & Lacerda (1992) stated that element
(Zn, Cu, Cd, Pb, Mn, & Ni) concentrations
determined in the marine organisms (benthic algae, crustaceans, and mollusks)
of Guanabara Bay were very low compared to those in other contaminated sites
along Rio de Janeiro State, and they were even comparable with those in
noncontaminated sites. The authors concluded that the large sewage inputs
reduce conditions in the bay’s water. These conditions, combined with high
sedimentation rates, result in the immobilization of elements in the sediment.
Consequently, these elements become unavailable for biological uptake. The same
geochemistry pattern and its influence in the elements’ bioavailability is
reported elsewhere, as presented in the review done by Zhang et al. (2014).
The difference in the element
concentrations was driven by the environment in which the target species
(shrimp and mussel) belonged. The preliminary ANOVA that compared the elemental
concentration in different shrimp species (site I: A. longinaris
and X. kroyeri; and site II: P. brasiliensis and P. paulensis)
showed that the difference in element concentrations is not species dependent,
supporting this affirmation. The target species from a polluted site did not
contain a necessarily high load of nonessential elements compared with those
from a less polluted site due to spatial variation in the elements’
bioavailability (Carvalho & Lacerda 1992; Zhang
et al. 2014).
In conclusion, mussels had higher
nonessential elements load than shrimps due to differences in their feeding
habits and, consequently, bioaccumulation of these elements. The spatial
approach showed that the geochemistry pattern of the sampling sites was
probably the major influence for the elements’ bioavailability, regardless of
the target species. To understand what drives the bioaccumulation of chemical
elements in marine organisms, it is necessary to know their feeding habits and
physiology, besides the habitat characteristics in each region. This
understanding of species for commercialization and human consumption, such as
the shrimps and mussels analyzed in this study, is even more important since it
affects both the local economy and public health.
Table 1. Concentration (µg·g-1
dry weight) of nonessential elements (Al, As, Cd, & Pb)
and normalized total load in the edible portion of shrimps and mussels from two
sampling sites in Rio de Janeiro State, southeastern Brazil. Data are presented
as the median ± interquartile range, and n values are the sample size.
|
Site I less polluted |
A. longinaris (n = 58) |
X. kroyeri (n = 57) |
Shrimps grouped (n = 115) |
Perna perna (n = 13) |
|
Al |
86.1 ± 35.6 |
84.4 ± 125.3 |
85.5 ± 58.5 |
1,781.5 ± 846.9 |
|
As |
25.8 ± 9.6 |
20.3 ± 11.6 |
23.6 ± 12.4 |
14.4 ± 6.0 |
|
Cd |
0.1 ± 0.1 |
0.2 ± 0.1 |
0.2 ± 0.1 |
0.5 ± 0.2 |
|
Pb |
0.8 ± 0.4 |
0.7 ± 0.4 |
0.7 ± 0.4 |
1.0 ± 1.0 |
|
Normalized total load |
35.4 ± 19.3 |
449.9 ± 212.8 |
||
|
Site II highly polluted |
P. brasiliensis (n = 41) |
P. paulensis (n = 39) |
Shrimps grouped (n = 80) |
Perna perna (n = 17) |
|
Al |
13.3 ± 18 |
28.1 ± 29.6 |
16.8 ± 25.5 |
614.3 ± 345.7 |
|
As |
3.8 ± 2.7 |
2.7 ± 1.8 |
3.1 ± 2.1 |
6.9 ± 2.1 |
|
Cd |
0.1 ± 0.1 |
0.1 ± 0.1 |
0.1 ± 0.1 |
0.3 ± 0.1 |
|
Pb |
0.1 ± 0.1 |
0.1 ± 0.1 |
0.1 ± 0.1 |
3.2 ± 2.1 |
|
Normalized total load |
6.3 ± 7.5 |
157.1 ± 86.3 |
||
For
figures - - click here for full PDF
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