Marine Pollution Bulletin xxx (xxxx) xxxx

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Marine Pollution Bulletin

journal homepage: www.elsevier.com/locate/marpolbul

Mercury accumulation in fish species along the Portuguese coast: Are there
potential risks to human health?
Filipe Costaa, , João P. Coelhob, Joana Baptistaa, Filipe Martinhoa, Maria E. Pereirac,
⁎

Miguel A. Pardala
a
CFE - Centre for Functional Ecology, Department of Life Sciences, University of Coimbra, 3000-456 Coimbra, Portugal
b
Department of Biology & CESAM & ECOMARE, University of Aveiro, Campus de Santiago, 3810-193 Aveiro, Portugal
c
Department of Chemistry and CESAM/REQUIMTE, University of Aveiro, Campus de Santiago, 3810-193 Aveiro, Portugal

ARTICLE INFO ABSTRACT

Keywords: This paper aimed at evaluating the total mercury content in five common fish species from the western European
Mercury Atlantic coastal waters, and the associated risk of consumption. Mercury concentrations in muscle of Atlantic
Food safety mackerel (Scomber scombrus), Atlantic chub mackerel (Scomber colias), European anchovy (Engraulis en-
Human health crasicolus), Atlantic horse mackerel (Trachurus trachurus) and European pilchard (Sardina pilchardus) ranged from
Marine fish
0.003 to 0.20 mg kg−1 wet weight, and no significant differences were observed between the average con-
centration in each species. A significant increasing trend in mercury content with fish size was observed for all
species (except for European anchovy), suggesting mercury bioaccumulation throughout their life cycle. Still, the
mercury content was far below the European Food Safety Authority and World Health Organization food safety
thresholds in all species, highlighting the low risk to human health due to the ingestion of these species and the
importance of consumer options for risk reduction.

1. Introduction
Fish consumption is highly recommended because it is considered
an important source of essential proteins, lipids, vitamins, minerals and
unsaturated fatty acids, such as Omega-3 (Bach-Faig et al., 2011;
Chahid et al., 2014). Besides preventing heart diseases, these compo-
nents also help reducing the risk of mental decline, depressions and
strokes. In the particular case of pregnant women, the consumption of
fish is recommended due to docosahexaenoic acid (DHA), essential fatty
acid, which helps developing the fetus brain (Kris-Etherton et al.,
2003). However, the consumption of fish also presents some risks, since
they can be an important source of potentially toxic elements, such as
mercury (Hg) (Burger, 2009).
Mercury (Hg) can reach ecosystems through natural sources such as
erosion or vulcanism. Nevertheless, the majority contamination pro-
cesses associated to mercury results mainly from anthropogenic activ-
ities, such as metal smelting, coal production, waste disposal and che-
mical synthesis (Burger and Gochfeld, 2009; Costa et al., 2011).
The biogeochemical cycle of mercury is very complex and may shift
rapidly between the atmospheric, terrestrial, aquatic and biota systems
(Liu et al., 2012). Once in the atmosphere, elemental mercury (Hg0) can
be converted into ionized mercury (Hg2+) by oxidation which may
return to the surface reaching soil, freshwater and aquatic systems
(Fitzgerald and Mason, 1996; Lamborg et al., 2014).
In aquatic ecosystems, the reduction of Hg2+ to its elemental form
(Hg0) associated with dissolved organic matter (DOM) and suspended
particulate matter (SPM) may occur, but in the presence of labile or-
ganic matter, a part of dissolved Hg can also be converted to methyl-
mercury (MeHg) through microbial activity (Lyons et al., 2017; Colla
et al., 2019). Hg may undergo complexation and reduction reactions
with dissolved organic matter (DOM) and suspended particulate matter
(SPM) in the water column, affecting its speciation, bioavailability and
mobility in aquatic environments (Ravichandran, 2004; Chakraborty
and Babu, 2015; Chakraborty et al., 2019). When this metal reaches the
aquatic ecosystems, it is accumulated by organisms throughout their
life cycle (i.e. bioaccumulation) and transported from low to high
trophic levels (i.e. biomagnification).
Mercury is considered highly toxic for human health even at low
concentrations (Zahir et al., 2005; Chakraborty, 2017). Human ex-
posure to Hg occurs essentially through fish consumption, specifically
the consumption of muscle tissues (filet). MeHg is the most deleterious
form of mercury, and can be found in the edible parts of the fish (Mieiro
et al., 2015). Methylmercury (MeHg) has high affinity for sulfhydryl
groups in proteins, tends to accumulate in organisms and may be

⁎
Corresponding author.
E-mail address: uc2012179058@student.uc.pt (F. Costa).

https://doi.org/10.1016/j.marpolbul.2019.110740
Received 3 June 2019; Received in revised form 14 November 2019; Accepted 14 November 2019
0025-326X/ © 2019 Elsevier Ltd. All rights reserved.

Please cite this article as: Filipe Costa, et al., Marine Pollution Bulletin, https://doi.org/10.1016/j.marpolbul.2019.110740
F. Costa, et al.
transmitted along the food chain (Mahaffey, 2005). In mammals mer-
cury contamination targets the brain, causing difficulty of locomotion,
reduced vision, tact, general weakness, tremors, loss of consciousness,
and ultimately death (Wolfe et al., 2003). Moreover, several disorders
in children and adults have been linked to the ingestion of high con-
centrations of MeHg. In pregnant women, once in the blood, MeHg is
easily transmitted to the fetus through the placenta, leading to a series
of neurological problems in terms of locomotion, speech and mental
retardation (Wolfe et al., 2003). Nevertheless, the risk associated to fish
consumption will always depend on the amount of fish being ingested,
the type of person consuming it and the fish species (Burger and
Gochfeld, 2008). In this sense, fish consumption guidelines have been
established worldwide (e.g. EFSA, WHO) to assure the safety of human
consumers, and that depend on variables such as body weight, fish
consumption rates and contaminant body burdens. Several approaches
have been developed by Joint Expert Committee on Food Additives
(JECFA) to determine the potential risk to human health throughout the
consumption of different fish species, such as Provisional tolerable
weekly intake (PTWI), estimated daily intake (EDI), Maximum Safe
Consumption (MSCA) and Hazard quotient (HQ).
Throughout the world, fishing activities are of major economic and
socio-cultural importance, as fish represents 16,6% of the animal pro-
tein and 6,5% of all protein consumed by the world population over the
years (EFSA Panel on Contaminants in the Food Chain, 2012; FAO,
2012). In most of the fish species, the level of mercury ranges from <
0.01 mg kg−1 to 0.5 mg kg−1, with the exception of some species such
as sharks and swordfish that can reach 1 mg kg−1 or higher
(Commission Regulation, 2006). Therefore, consumer preferences may
have a significant impact on the risk associated with fish consumption.
The relevance of consumption preferences will increase for the largest
fish consumer countries such as Portugal (55.9 kg/per capita/year),
Spain (45.2 kg/per capita/year) or France (33.9 kg/per capita/year),
considerably higher than the European Union (EU) average consump-
tion of nearly 25.1 kg/capita/year (EUMOFA, 2017).
With this in mind, the main goals of this work are to: (1) quantify
the total mercury content in the edible part of five common fish species
from the western European Atlantic coast; (2) evaluate the effect of
species and fish size on the mercury body burden; (3) evaluate the risk
of consumption of different species and respective size ranges to human
health, considering both EFSA and WHO reference values.
2. Materials and methods
2.1. Study site and fish sampling
Fish sampling took place at several sites along the Portuguese
coastline, located in south-western Europe. All samples were collected
from traditional beach seine fisheries (arte-xávega) between 2015 and
2017 and collected monthly during the main fishing season (April to
October).
This traditional fishery includes the use of wooden boats, with
6–9 m long. The boats go up to 2 km from shore deploying the nets into
the water, and returning to shore. Afterwards the nets are hauled
beachwards with the help of mechanical tractors. The beach seine nets
used for this study were approximately 280 m long, the central bag was
approximately 35 m long, with a stretched mesh size of 22 mm. For
more detailed information about this fishing method, see (Cabral et al.,
2003).
The selected species were Atlantic chub mackerel Scomber colias,
Atlantic mackerel Scomber scombrus, European anchovy Engraulis en-
crasicolus, Atlantic horse mackerel Trachurus trachurus and the
European pilchard Sardina pilchardus. The specimens were subsequently
divided into length classes according to commercial standards (Feijó
et al., 2012) (Table 1).
These five species have a high commercial importance since they
represent 820 thousand tons out of 4.3 million tons of the total marine
2
Marine Pollution Bulletin xxx (xxxx) xxxx
Table 1
Total lengths (cm) and length class (cm) for each species according to standard
values used by IPMA (Feijó et al., 2012).
Length S. colias S. scombrus T. trachurus E. encrasicolus S. pilchardus
class (cm) (cm) (cm) (cm) (cm) (cm)
Lc1 < 18 17–24 10–19 < 10 < 12
Lc2 18–28 24–31 19–28 10–12 12–15
Lc3 28–35 31–42 28–38 12–14 15–17
Lc4 35–49 42–63 38–45 14–18 17–20
fish caught in Europe in 2018 (EUMOFA, 2018). In Portugal, these
species represents more than half of the total marine fish caught in the
whole Portuguese territory in 2018, (62,747 tons out of 99,834 tons)
and one third of the economic value associated to fisheries in Portugal
(INE, 2018).
2.2. Laboratory procedures
A total of 738 individuals were weighed and measured, and a
sample of dorsal muscle tissue collected, freeze-dried and homogenized
to a fine powder and stored dry until further analysis. T-Hg was
quantified by thermal decomposition atomic absorption spectrometry
with gold amalgamation, using a LECO AMA-254 (Advanced Mercury
Analyzer). Briefly, samples are placed into a pre-cleaned combustion
boat and inserted in a quartz combustion catalytic tube. The sample is
firstly dried at 120 °C prior to combustion at 680–700 °C in an oxygen
atmosphere. The mercury vapor is collected in a gold amalgamator and
after a delay period heated at 900 °C. This releases the mercury which is
transported to a heated cuvette (120 °C) and then quantified by atomic
absorption spectroscopy using a silicon UV diode detector. The limit of
detection (LOD) of this methodology is 0.01 ng absolute mercury. The
accuracy and precision of the method were assessed through daily re-
plicate analysis of certified reference material (CRM) Dorm-4, used as
CRM for fish muscle tissue samples. Precision of the method was always
better than 10% (n = 39), with a recovery efficiency of 82 ± 9.5%
(n = 156).
2.3. Potential risk to human health
Several approaches were used to determine the potential risk to
Portuguese human health throughout the consumption of different
species and Length classes. Similar calculations were performed for
other southern European countries, Spain and France, once these
countries are the second and third fish consumers in Europe to test if
the samples comply with the established PTWI for three main groups of
consumers (men and women over 19 years), children (2–6 years) and
pregnant women (16–49 years).
The World health organization (WHO) (Additives, 2016), The Eur-
opean Food Safety Authority (EFSA) (Commission Regulation, 2006)
and United States Food and Drug Administration (FDA) (Evans et al.,
2002), developed regulation to set the maximum amount of con-
tamination allowed in foodstuff. For the EU, the maximum levels al-
lowed for T-Hg in fishery products, fish muscle and crustaceans is
0.5 mg kg−1 wet weight (Commission Regulation, 2006). Despite that
some species have a maximum level of 1.0 mg kg−1 wet weight, the
studied species should comply with the 0.5 mg kg−1 wet weight
threshold established by the European and American standards (Evans
et al., 2002; Commission Regulation, 2006). The notable difference in
mercury legislation between these two groups (common fish and pre-
datory fish) is not based on scientific knowledge. Predatory fish gen-
erally have higher methylmercury contamination than other fish spe-
cies and so, they present a higher risk to consumers than other species.
Current legislation is based on economic, political and social interests,
rather than studies evaluating the ecotoxicological risk of these
amounts of mercury for human health.
F. Costa, et al.
2.3.1. Provisional tolerable weekly intake (PTWI)
Considering that the amount of fish ingested varies across different
communities, estimates have been made to determine the maximum
safe amount of mercury a person can receive over a period of time. The
Joint Food and Agriculture Organization/World Health Organization
(FAO/WHO) Expert Committee on Food Additives has established
regulatory guidelines, expressed in the form of provisional tolerable
weekly intake (PTWI). According to EFSA (EFSA Panel on
Contaminants in the Food Chain, 2012), the PTWI for inorganic mer-
cury is 4 μg kg−1 body weight/week. For MeHg this value is
1.6 μg kg−1 body weight/week, and for risk groups (pregnant women
and children), the limit is reduced to 1.3 μg kg−1 body weight/week
(EFSA Scientific Committee, 2015). The PTWI was calculated according
to the following equation:
PTWI = C X AvC/bw
where C (μg g−1 wet weight (ww) of fish) is the mean concentration of
contaminant in the fish fillet, AvC is the average consumption of fish
per week, and bw is the average body weight of the risk group.
2.3.2. Estimated daily intake (EDI)
The estimated daily intake (EDI, μg kg−1 bw/day) was calculated
with the following equation (Vinceti et al., 2014):
EDI = [C × AvC]/bw
where, C (μg g−1 ww of fish) is the mean metal concentration in muscle
tissue, AvC is the average consumption of fish per day, and bw is the
average body weight. The EDI values where compared to the estab-
lished values of reference doses (RfD), 0.1 μg g−1 wet weight of fish for
Hg (US-EPA, 2017). This 0.1 μg g−1 ww of fish represents the amount of
Hg a person of 70 kg may ingest daily, and that is unlikely to produce
any health effects (US-EPA, 2012).
2.3.3. Maximum safe consumption (MSCA)
The maximum safe consumption (MSCA, kg fish ww/day) indicates
the maximum amount for a safe daily consumption of a particular
species, due to the potential toxicity associated to that species from a
given contaminant. For mercury the RfD has been established at
0.1 μg kg−1 bw/day (US-EPA, 2017). The calculations were performed
with the following equation (Rodriguez y Baena et al., 2013):
MSCA = bw × RfD/C × 1000
where bw is the average body weight for the different risk groups, C
(μg g−1 ww of fish) is the mean metal concentration in muscle tissue,
and RfD is the reference dose.
2.3.4. Hazard quotient (HQ)
The Hazard Quotient (HQ) was estimated for each length class of
the five selected species by dividing the EDI by the RfD (Onsanit et al.,
2010). In the end, values below 1 indicate that even for more sensitive
groups (such as pregnant women and children) consumption of these
species/size classes represents no danger in terms of health effects. In
contrast, values above 1 indicate a high probability for long term health
effects (Copat et al., 2012a).
HQ = EDI/RfD
Table 2
Minimum (min), maximum (max), mean ( x ) and standard deviation (SD) values of T-Hg found in S. colias, S. scombrus, T. trachurus, E. encrasicolus and S. pilchardus.
The units are mg.kg −1 ww.
Parameters S. colias S. scombrus
Minimum 0.012 0.019
Maximum 0.090 0.109
Mean 0.034 0.043
Standard deviation 0.013 0.015
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2.4. Data analysis
Pearson rank correlations (r) between total-length and T-Hg con-
centrations were performed to relate fish size with T-Hg burdens.
Differences in the bioaccumulation patterns over the lifespan of each
species and length-classes were assessed by non-parametric ANOVA
(Kruskal-Wallis), following Dunn's multiple comparisons tests whenever
significant differences were found. Non-linear regressions were per-
formed between T-Hg and total-length for each species. These analyses
were performed using SigmaPlot 14.0 software.
Consumption risk assessment was evaluated for the general popu-
lation (men and women over 19 years) and two risk groups: children
(2–6 years) and pregnant women (16–49 years). In order to carry out all
the calculations, the average consumption of the Portuguese and
European populations and the advised consumption for the different
risk groups were considered: 1069 g per week for Portugal and 480 g
per week for Europe (EUMOFA, 2017).
Since only T-Hg was quantified in the samples, and the PTWI values
for the risk groups (children and pregnant women) refer to MeHg, all
data were converted to MeHg. For this conversion, a “worst-case sce-
nario” approach was selected based on published literature, which in-
dicate that the proportion of methylmercury in the total mercury body
burden is higher than 80% (Andersen and Depledge, 1997), or ranging
from 70 to 90% (Mieiro et al., 2011); hence, a fraction of 90% of MeHg
was assumed for all samples.
3. Results
3.1. Mercury in fish muscle
Mercury concentrations in the studied species were low, circa 12–15
times below the regulatory limit of 0.5 mg kg −1 ww of contaminant in
fish, established by EFSA Panel on Contaminants in the Food Chain,
2012. Since the length classes assigned to each species were different
from species to species, the average length of each species and the
corresponding T-Hg concentration were used for comparison between
species. In this case, no significant differences were found between
species T-Hg levels (F = 2.718, p = .07). The minimum (min), max-
imum (max), mean ( x ) and standard deviation (SD) values are shown
below (Table 2).
3.2. Relationship between length class and mercury concentration
Despite dealing with very low concentrations, it is important to
understand the lifespan bioaccumulation pattern of these five species
(Forrester et al., 1972) (Monteiro and Lopes, 1990) since consumers
prefer certain size classes of each species. Considering all size classes,
strong and positive significant relationships were observed between
total length and mercury concentrations for all species, with the ex-
ception of E. encrasicolus, which presented a weak, but still significant
positive relationship (S. colias r = 0.833, p < .05; S. scombrus
r = 0.758, p < .05; T. trachurus r = 0.869, p < .05; E. encrasicolus
r = 0.171, p < .05; S. pilchardus r = 0.692, p < .05; Table 3, Fig. 1).
The trend for increasing T-Hg with length was further confirmed for
S. colias, S. scombrus, T. trachurus and S. pilchardus, as significant
T. trachurus E. encrasicolus S. pilchardus
0.004 0.014 0.007
0.204 0.204 0.070
0.043 0.034 0.0025
0.015 0.022 0.013
F. Costa, et al. Marine Pollution Bulletin xxx (xxxx) xxxx

Table 3 consumer groups (Fig. 2). However, the calculations performed for T.
Non-Linear equations between T-Hg and T-Length for S. colias, S. scombrus, T. trachurus size class Lc3 (1.8 μg kg−1 bw) exceeded the adult PTWI
trachurus, E. encrasicolus and S. pilchardus. (1.6 μg kg−1 bw, Table 4 but not for children and pregnant women
Species T-Hg vs T-Length (Eq) R2 (0.56 μg kg−1 bw and 0.90 μg kg−1 bw), respectively.
If the consumption of fish was based on fish from the Portuguese
Scomber colias y = 0.0064 ∗ 1.0659X 0.84 coast, and assuming an average body weight of 70 kg and the same
Scomber scombrus y = 0.0066 1.0723X 0.79
guidelines for the risk groups, considering the average consumption
∗
Trachurus trachurus y = 0.0040 ∗ 1.1071X 0.96
Engraulis encrasicolus y = 0.0204 ∗ 1.0323X 0.17 rates of both Spain (867 g/week) and France (650 g/week) (EUMOFA,
Sardina pilchardus y = 0.0022 ∗ 1.1510X 0.82 2017), all species were considered safe choices for consumption, given
that all the obtained values of weekly intake for Spain and France were
well below the 1.6 μg kg−1 bw threshold (Table 4).
differences between size classes were observed, which point to a The estimated daily intake (EDI) of MeHg for S. colias, S. scombrus,
bioaccumulation of Hg throughout their life cycle (S. colias H = 94.070; T. trachurus and S. pilchardus was higher than the established reference
p < .001; S. scombrus H = 38.520, p < .001; T. trachurus dose (RfD) of 0.1 μg kg−1 bw/day (USEPA, 2017), particularly in the
H = 68.261, p < .001; S. pilchardus H = 66.114, p < .001; Fig. 1). larger fish (Table 5). For E. encrasicolus, the EDI value was lower than
However, in the particular case of S. pilchardus (Fig. 1e), a significant the established reference dose (Table 5).
increase in T-Hg with size was only observed after approximately 15 cm The Maximum Safe Consumption (MSCA, kg fish ww/day) was
length. Up to that point, a decrease in mercury concentrations is visible found to be high enough in order for a 70 kg person to eat these species
(Fig. 1e). On the other hand, no effect of size on Hg body burdens was safely, considering the amount of MeHg assumed in our specimens and
found for E. encrasicolus when considering the different size classes, but different between classes and species (Table 5).
rather a heterogeneous and non-significant distribution over their life Similarly, as observed with the EDI values, the largest specimens of
cycle (H = 2.272, p = .321, Fig. 1d). S. colias, S. scombrus, T. trachurus and S. pilchardus present fairly high
HQ values, indicating potential health issues associated with the intake
3.3. Human risk assessment of MeHg present in consumed fish. Again, in E. encrasicolus the HQ
values for all length class were low enough that even the most sensitive
Taking into account the consumption advisories for children populations are unlikely to present health effects due to the consump-
(2–6 years, 120 g per week) and pregnant women (16–49 years, 330 g tion of this species (Table 5).
per week) (EPA and FDA, 2017), the average consumption of the Por-
tuguese population for men and women over 19 years (1069 g per 4. Discussion
week), and the assumed average concentration of MeHg present in our
samples, the PTWI indicated that the ingestion of S. colias, S. scombrus, This paper is one of the first to quantify T-Hg in species of com-
E. encrasicolus and S. pilchardus in general poses no risk for any of the mercial interest, and to relate with the regulatory threshold for

Fig. 1. Relationship between total length (LC in cm; length classes are identified by different colors, 1 dark blue, 2 light blue, 3 yellow, 4 orange) and T-Hg (μg g−1) of
the study species. a) S. colias; b) S. scombrus; c) T. trachurus; d) E. encrasicolus; e) S. pilchardus. (For interpretation of the references to colour in this figure legend, the
reader is referred to the web version of this article.)

4
F. Costa, et al. Marine Pollution Bulletin xxx (xxxx) xxxx

Fig. 2. Portuguese weekly intake of Hg for different risk groups through the consumption of a) S. colias, b) S. scombrus, c) T. trachurus, d) E. encrasicolus and e) S.
pilchardus, considering the different length classes (L in cm and different colors: 1 dark blue, 2 light blue, 3 yellow, 4 orange). The PTWI limit for men and
women > 19 years is represented by horizontal red line at 1.6 μg kg−1 bw, and the PTWI for children (2–6 years) and pregnant (16–49 years) is represented by a
horizontal black line at 1.3 μg kg−1 bw. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)

Table 4
Provisional tolerable weekly intake for T-Hg through the consumption of different lengths class (cm) of S. colias, S. scombrus, T. trachurus, E. encrasicolus and S.
pilchardus, in three different countries, Portugal, Spain and France for men and women over 19 years old. Maximum values obtained for each species and country is
highlighted in bold. Units are μg kg−1 bw/week and the limit for PTWI is 4 μg kg−1 bw/week.
Country Length class (cm) S. colias S. scombrus T. trachurus E. encrasicolus S. pilchardus

Portugal Lc1 0.26 0.46 0.27 0.27 0.18

Lc2 0.44 0.63 0.53 0.46 0.27
Lc3 0.69 1.04 1.80 0.49 0.49
Lc4 1.18 – – 0.47 0.72
Spain Lc1 0.21 0.37 0.22 0.22 0.15
Lc2 0.36 0.51 0.43 0.37 0.22
Lc3 0.56 0.84 1.46 0.40 0.40
Lc4 0.95 – – 0.38 0.58
France Lc1 0.16 0.28 0.17 0.17 0.11
Lc2 0.27 0.38 0.33 0.28 0.17
Lc3 0.42 0.63 1.10 0.30 0.30
Lc4 0.72 – – 0.29 0.44

different groups of risk: men and women > 19 years, children
(2–6 years) and pregnant women (16–49 years), considering all the
established legislation for consumable foodstuff.
4.1. Mercury accumulation in different fish species
Overall, T-Hg levels from the five studied species were considered
low. Mercury in fish muscle was found to be well below current reg-
ulatory thresholds, circa 12–15 times the established limits (0.5 mg kg
−1
ww of fish), meaning that all species are in accordance with
European food safety legislation (Commission Regulation, 2006). Cur-
rent results are within the same range as previous studies performed in
the Portuguese coast (Vieira et al., 2011), suggesting that these species
reflect the low mercury bioavailability of Portuguese coastal waters.
The fact that the overall average Hg body burden was similar between
species reinforces this assumption, pointing to an environmentally-
regulated Hg mercury bioaccumulation. In agreement with this hy-
pothesis, the same species were reported to have higher Hg body bur-
dens in the Mediterranean Sea (Copat et al., 2018), which may be re-
lated with the higher average water temperature and consequent

5
F. Costa, et al. Marine Pollution Bulletin xxx (xxxx) xxxx

Table 5 E. encrasicolus, larger fish presented higher mercury concentration than

Provisional tolerable weekly intake (PTWI), Estimated daily intake (EDI), smaller fish, as a result of continuous exposure to contaminants and
Maximum Safe Consumption (MSCA) and Hazard Quotient (HQ) for MeHg consequent accumulation with time. Similar findings have been pre-
through the consumption of different length class (cm) of S. colias, S. scombrus, viously reported for other species and locations (Joiris et al., 2000;
T. trachurus, E. encrasicolus, and S. pilchardus for men and women over 19 years
Storelli et al., 1998; Storelli and Marcotrigiano, 2000). Still, some de-
old. The maximum values obtained for each species are highlighted in bold;
gree of uncertainty exists regarding bioaccumulation patterns with
length classes without specimens to perform all the calculations are represented
size/age, as Hg concentrations have also been reported to correlate
with one dash. Maximum level for PTWI is 1.6 μg kg−1 bw/week for women
(> 19) and 1.3 μg kg−1 bw/week for children and pregnant women. EDI has a negatively with fish size for T. trachurus (Vieira et al., 2011). However,
maximum level of 0.1 μg kg−1 bw/day and for HQ > 1 indicates risk and < 1 the size range of specimens reported in that study was considerably
indicates no Risk. smaller (28.3–33.9 cm) than in the present study (6.2–36.6 cm), which
may justify the different accumulation patterns observed.
Species Length class PTWI EDI (μg g−1 MSCA HQ
(cm) (μg kg−1 bw/day) (kg/day)
These findings will have a significant impact on the risk associated
bw/week) with the consumption of fish, as consumer choices between different
fish species and size will determine the amount of mercury associated
S. colias Lc1 (< 18) 0.26 0.037 0.412 0.372 with a fish-based diet. While all samples analyzed were well within
Lc2 0.443 0.063 0.241 0.634
Lc3
(18–28)
0.687 0.098 0.156 0.984
current food safety legislation for mercury, the associated risk may still
(28–35)
Lc4 (35–49) 1.176 0.168 0.091 1.683 be of concern. Among the several risk assessment guidelines that con-
S. scombrus Lc1 (17–24) 0.458 0.066 0.233 0.656 cern Hg, some are more protective than others, and risk assessment
Lc2 (24–31) 0.626 0.09 0.171 0.896 results therefore may vary depending on the methodology.
Lc3 (31−32) 1.038 0.149 0.103 1.486
T. trachurus Lc1 (10–19) 0.275 0.039 0.389 0.393
Lc2 (19–28) 0.535 0.077 0.2 0.765 4.2. Risk assessment
Lc3 (28–38) 1.802 0.258 0.059 2.579
E. encrasicolus Lc1 (< 10) 0.275 0.039 0.389 0.393 The European Guidelines established a PTWI limit of 1.6 μg kg−1
Lc2 (10−12) 0.458 0.066 0.233 0.656 bw/week for MeHg in adults (men and women over 19 years), while
Lc3 0.489 0.07 0.219 0.699
Lc4
(12–14)
0.473 0.068 0.226 0.678
more restrictive guidelines apply to more sensitive consumer groups
(14–18)
S. pilchardus Lc1 (< 12) 0.183 0.026 0.583 0.262 such as pregnant women and children (1.3 μg kg−1 bw/week)(EFSA
Lc2 (12–15) 0.275 0.039 0.389 0.393 Scientific Committee, 2015). Considering that the average weight in the
Lc3 (15–17) 0.489 0.07 0.219 0.699 European population is about 70 kg (Stevens et al., 2012), the average
Lc4 0.718 0.103 0.149 1.027
(17–20)
fish consumption in Portugal (approximately 1069 g per week,
EUMOFA, 2017) and the average Hg concentration for each fish species,
the five species are considered safe to eat. However, similar calculations
increased Hg bioavailability (Dijkstra et al., 2013).
for all size classes revealed a significant risk associated with the largest
Despite the similar overall average T-Hg concentration, a more in-
T. trachurus size class Lc3 (1.8 μg kg−1 bw), which present values higher
depth analysis of size-related Hg body burden revealed distinct bioac-
than the established limit. Under those specific conditions, a maximum
cumulation patterns among the studied fish species. Similar findings
of 900 g of T. trachurus should be consumed to be under the 1.6 μg kg−1
have already been documented in previous studies, which can be re-
bw/week guidelines. Considering an average weight of 70 kg for a
lated with distinct feeding habits, lifespan or other species-specific
pregnant women and the recommended fish consumption for this risk
traits (Phillips et al., 1980; Storelli et al., 1998, 2003) while S. colias, S.
group (330 g per week, EPA and FDA, 2017), it is considered that all
scombrus and T. trachurus are considered piscivorous species, S. pil-
five species can be a good choice for consumption. For children be-
chardus and E. encrasicolus are planktivorous species (IUCN, 2018) and
tween 2 and 6 years (average weight of 15.8 kg) and considering the
feed on lower trophic levels. It was therefore expected that S. pilchardus
advised fish consumption for this consumer group (120 g per meal, EPA
and E. encrasicolus showed similar bioaccumulation patterns since they
and FDA, 2017), all five species stand below the limits and can also be
have the same feeding habits. S. colias and S. scombrus were found to
considered safe choices.
have similar Hg accumulation patterns with size, while the planktivore
For other southern European countries such as Spain and France,
S. pilchardus mercury accumulation curve resembles more that of the
with lower annual average consumption rates (45.2 Kg/year for Spain
piscivore T. trachurus, rather than that of E. encrasicolus. One possible
and 33.9 Kg/year for France), all risk calculations were lower, and so,
explanation can be related with the high affinity of Hg for lipid contents
all the five species were considered safe to eat. This highlights the need
present in fish muscle (Girault et al., 1997). Indeed, S. pilchardus has a
to adjust food safety advisories to regional consumption patterns, which
higher lipid content compared to E. encrasicolus (Tanakol et al., 2012),
will greatly influence the risk associated with fish consumption.
and would presumably present a higher affinity for Hg than E. en-
In addition to the PTWI calculations, three others widely used risk
crasicolus. Another possible explanation for the differences found be-
assessment methodologies were also used to evaluate the consistency
tween both species is the distinct lifespan of the two species; while E.
between food safety guidelines. Calculations for EDI were performed to
encrasicolus is a relatively short-lived species (3–5 years) with a high
determine if the average daily consumption is above or below the re-
growth rate (ICES, 2009), the life expectancy of S. pilchardus is higher
ference dose for mercury (0.1 μg g−1 ww of fish) (US-EPA, 2017). With
(15 years) (Muus and Nielsen, 1999), and will therefore be exposed to
the exception of E. encrasicolus, results showed that the consumption of
contaminants for a longer period. A similar explanation may justify the
the largest fish sizes leads to a contaminant intake higher than the es-
higher Hg concentrations observed in the largest T. trachurus speci-
tablished limit (US-EPA, 2012). These results are consistent with those
mens, when compared with the other piscivorous species of similar size.
found for the Maximum Safe consumption (MSCA, US-EPA, 2017) and
While the life expectancy of S. colias and S. scombrus are 13 and 15 years
HQ (Copat et al., 2012a), which highlighted some risk associated with
(Cengiz, 2012) (Costa et al., 2017), respectively, T. trachurus can reach
the consumption of the largest S. colias, S. combrus, T. trachurus and S.
up to 40 years (Abaunza et al., 2003) and thus being able to accumulate
pilchardus considering the average daily consumption of the Portuguese
contaminants for a longer time. However, further analysis into these
population (153 g of fish).
species are necessary to fully understand the different lifespan bioac-
These results highlight the effect of consumer choices in the risks
cumulation patterns observed.
associated with fish and seafood consumption. The choice of species
Besides being possible to observe different patterns of bioaccumu-
highly influences the amount of contaminants ingested, but also the size
lation among species, results demonstrated that, with the exception of
of the fish consumed. Considering the present study, two congeneric

6
F. Costa, et al.
species (S. colias and S. scombrus) were found to have distinct con-
taminant body burdens and associated risk at equivalent sizes. The
choice of consuming S. colias over S. scombrus will significantly reduce
the amount of mercury ingested, and therefore the associated toxicity
risk. The same occurs with S. pilchardus and E. encrasicolus, with the
latter emerging as the safest choice from all the studied species, as
observed previously in the Mediterranean Sea (Copat et al., 2012b).
Regarding fish size, opting for the consumption of the same amount of
fish but from smaller/younger fish will again reduce the ingestion of
contaminants, and potentially contribute to prevent health issues. This
highlights the significant role of consumers in the minimization of risk
associated with fish consumption, and the need to inform and educate
the general public about these important choices.
5. Conclusions
The species S. colias, S. scombrus, E. encrasicolus and S. pilchardus
presented mercury concentrations well below the regulatory threshold
for human consumption. However, T. trachurus, in Length Class 3 (LC3),
presented values above the limits for human consumption. Despite si-
milar average concentrations between species, differences were ob-
served in the species bioaccumulation patterns, with a significant effect
of body size for all species except E. encrasicolus. Overall, no or reduced
risk exists from the consumption of these species, but these may still be
minimized through consumer options, such as the choice of species and
fish size.
CRediT authorship contribution statement
Filipe Costa:Writing - original draft, Formal analysis,
Investigation.João P. Coelho:Validation, Methodology,
Supervision.Joana Baptista:Conceptualization.Filipe Martinho:-
Conceptualization.Maria E. Pereira:Resources.Miguel A.
Pardal:Supervision.
Declaration of competing interest
The authors declare that they have no known competing financial
interests or personal relationships that could have appeared to influ-
ence the work reported in this paper.
Acknowledgements
This work received funds from the project ReNATURE - Valorization
of the Natural Endogenous Resources of the Centro Region (Centro
2020, Centro-01-0145-FEDER-000007). JPC is funded by the Integrated
Program of SR&TD ‘Smart Valorization of Endogenous Marine
Biological Resources Under a Changing Climate’ (Centro-01-0145-
FEDER-000018), co-funded by Centro 2020 program, Portugal 2020
and the European Regional Development Fund. F. Martinho is funded
by national funds (OE), through FCT (Portuguese Foundation for
Science and Technology), I.P., in the scope of the framework contract
foreseen in the numbers 4, 5 and 6 of the article 23, of the Decree-Law
57/2016, of August 29, changed by Law 57/2017, of July 19.
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