Marine Pollution Bulletin 189 (2023) 114739

Contents lists available at ScienceDirect

Marine Pollution Bulletin

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

Analysis of metals and metalloid in commercial fish species from the

Galapagos Marine Reserve: Toxicological and nutritional assessment
Eduardo Franco-Fuentes a, Nicolas Moity b, Jorge Ramírez-González b, Solange Andrade-Vera b,
Arturo Hardisson a, Carmen Rubio a, Soraya Paz a, Dailos González-Weller c, Carmen Rubio a,
Ángel J. Gutiérrez a, *
a
Toxicology Area, Department of Obstetrics and Gynecology, Pediatrics, Preventive Medicine and Public Health, Toxicology, Legal and Forensic Medicine and
Parasitology, Universidad de La Laguna, Spain
b
Charles Darwin Research Station, Charles Darwin Foundation, Av. Charles Darwin, Puerto Ayora, Gálapagos, Ecuador
c
Canarian Public Health Service, Central Laboratory, Santa Cruz de Tenerife, Spain

A R T I C L E I N F O A B S T R A C T

Keywords: Aquatic pollution derived from metal presence in the Galapagos Islands could affect biodiversity and human
Galapagos Islands health. This research provide a baseline on food safety in commercial fish species of the Galapagos Islands. We
Metals and metalloid sampled muscle tissue of pelagic (Acanthocybium solandri) and demersal (Caulolatilus affinis, Pontinus clemensi,
Food security
Hyporthodus mystacinus, and Paralabrax albomaculatus) species. Metal and metalloid concentrations per species
Toxicological assessment
Fisheries
were analyzed by Inductively Coupled Plasma Optical Spectrometry (ICP-OES). According to the Food and
Agriculture Organization (FAO) regulation none of the studied species should be ingested; and according to the
European Food Safety Authority (EFSA) regulation, all the studied species were above the Maximum Allowable
Concentration (MAC) for Cd. According to EFSA, C. affinis should not be commercialized. Finally, A. solandri,
P. clemensi and H. mystacinus do not represent a human health risk since its Margen of Safety (MoS) < 1 for
people of up to 100 kg of body weight.

1. Introduction
The expression “food security” is defined as “the constant availability
to access and afford for food” (Anani et al., 2020). Other definition
establish that food security exists when “at all times, all people, have
physic and socio-economic access to the necessary amount of safe and
nutritious food that supplies their diet for a healthy life (Rush, 2013)”.
Food security is also the second and third goal of the Sustainable
Development Goals (SDGs) established by United Nations (UN) in 2015
for the year 2030 (Anani et al., 2020).
Metals and metalloids deficiency in human health can cause diseases,
while in high quantities they can have toxic effects (Andersson et al.,
2012). The toxicity of each metal vary depending on their species, dose,
duration of exposure and environmental factors (pH, alkalinity, acidity
and temperature among others). Other characteristics such as their
speciation, mobility, solubility, accessibility and availability are also
very important, establishing as the most toxic metals those that have a
greater solubility since they have a higher mobility and bioavailability
(Nkwunonwo et al., 2020). Metals can reach aquatic ecosystems through
natural sources such as rock erosion, hydrothermalism and volcanism,
among others; and/or anthropogenic sources, such as fossil fuels com­
bustion, industrial discharges, or agrochemicals (Kojadinovic et al.,
2007). The aquatic pollution derived from its presence can affect
biodiversity, as well as human health (Araújo and Cedeño-Macias,
2016).
The Galapagos Islands exhibit one of the highest biodiversity, levels
of endemism and conservation of biological processes in the world; in
addition it is one of the places on Earth with the highest volcanic activity
(https://whc.unesco.org/). Therefore, the archipelago has a high
availability of metals derived from geological origin (Kurz and Geist,
1999). Fishing is a resource of great importance in these islands, rep­
resenting one of the most important economic activities and the main
food production activity (Araújo and Cedeño-Macias, 2016). In the ar­
chipelago, only small-scale artisanal fishing is allowed, supplying pro­
teins and nutrients to ~32,000 people (Ramírez-González et al., 2022).
Due to previous research results, and the few information available on

* Corresponding author.
E-mail address: ajguti@ull.edu.es (Á.J. Gutiérrez).

https://doi.org/10.1016/j.marpolbul.2023.114739
Received 14 December 2022; Received in revised form 9 February 2023; Accepted 13 February 2023
Available online 25 February 2023
0025-326X/© 2023 The Author(s). Published by Elsevier Ltd. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-
nc-nd/4.0/).
E. Franco-Fuentes et al.
the metallic concentration in fish species of the Galapagos (Muñoz,
2016; Franco-Fuentes et al., 2021a, 2021b; Franco-Fuentes et al., 2023),
we aim to increase the knowledge about metal concentration in muscle
tissue of commercial fish species, providing a baseline on fisheries food
security in Galapagos. In addition, we tried to elucidate if the metal
origin is internal or external to the archipelago.
2. Material and methods
2.1. Study area and fieldwork
The Galapagos Islands lies on the equator, approximately 1000 km
west of the coast of mainland Ecuador. The Archipelago consists in 13
major islands and over 200 islets and emergent rocks (Snell et al., 1996).
Moreover, it comprises urban and rural zones (~258 km2), the Gal­
apagos National Park (GNP ~ 7985 km2) and the Galapagos Marine
Reserve (GMR ~ 138,000 km2), that reaches 40 nautical miles out from
the coast (DPNG, 2014; INEC, 2019). The GMR was created in 1998 and
lies at the confluence of four currents: the Panama current, which is
strongest from December to June and brings warm water from the north
marking the wet season; the Humboldt and Cromwell currents, which
predominate from May to November and brings cold waters from the
south and west, respectively, marking the dry season; and the South-
Equatorial current, which influence varies all year long (Fig. 1). The
influence of these currents on the distribution of fish and macro-
Fig. 1. Area of the Galapagos Marine Reserve, main currents, and bioregions boundaries according to Edgar et al. (2004) and Moity (2019). Main harbors and non-
protected urban and rural areas.
2
Marine Pollution Bulletin 189 (2023) 114739
invertebrate communities across the archipelago allows the identifica­
tion of three major bioregions: Central-southeastern, Northern
(comprising the Far Northern and Northern regions) and Western
(comprising the Elizabeth and Western regions) (Edgar et al., 2004;
Sweet et al., 2007; Moity, 2019; Forryan et al., 2021).
2.2. Sampling
Muscle samples were collected between February–May 2019 from
fisher catch landings at Pelikan Bay dock in Puerto Ayora (Santa Cruz
Island, Galapagos). All the samples come from the Central southeastern
bioregion. Samples were taken from the inferior jaw or pectoral fin area
to reduce the damage of the sellable part of the fish. Aiming for having
an equal proportion of males and females of each species we sampled
four demersal species: Bighead tilefish (Caulolatilus affinis), Mottled
scorpionfish (Pontinus clemensi), Misty grouper (Hyporthodus mystaci­
nus), and White spotted sand-bass (Paralabrax albomaculatus); and one
pelagic species: Wahoo (Acanthocybium solandri). According to Taka­
shima and Hibiya (1995), sex was determined from the gonad color,
blood vessel density, size, and texture. Sex determination for some in­
dividuals were impossible because they were underdeveloped.
All organisms were measured (fork length, FL) to the nearest cm, and
weighed in fresh presentation (wet weight, wet wt.) to the nearest kg
(Table 1). After collection at Pelikan Bay dock, samples were mobilized
to the Charles Darwin Research Station for tissue separation and
E. Franco-Fuentes et al. Marine Pollution Bulletin 189 (2023) 114739

Table 1 quantity of fish that could be consumed per week with no adverse effects
Range of fork length (cm), total weight (kg), and sample size of muscle tissue for on health. Maximum Allowable Concentration (MAC) is the maximum
each species and 111 sex (UND = undetermined). concentration of a contaminant that an animal can legally have. An
Species Range of Range of n Male Female UND important concept used to characterize chemical exposure risks is the
fork length total Margin of Safety (MoS), which relate the No-Observed-AdverseEffect-
(cm) weight Level (NOAEL) obtained from animal toxicology studies and the esti­
(kg)
mated human exposure level or dose (Eq. (2)). MoS values >1 imply
Acanthocybium
127–169 13–27 10 3 2 5 possible adverse effects derived from fish consumption, and it was
solandri (Wahoo)
calculated with the following formula:
Caulolatilus affinis
29–39 0.3–0.6 7 3 3 1
(Bighead tilefish) EWI
Pontinus clemensi MOS = (2)
TWI
(Mottled 28–60 0.4–4 34 11 11 12
scorpionfish) Tolerable Weekly Intakes (TWI) are recommendations established by
Hyporthodus EFSA and FAO for toxic elements, and are the maximum concentration
mystacinus (Misty 47–150 3–26 13 1 4 7
of a contaminant from an animal that can be ingested without adverse
grouper)
Paralabrax effects (Codex, 1995; Aguilar et al., 2008; Efsa, 2009a, 2009b; EFSA
albomaculatus Panel on Contaminants in the Food Chain (CONTAM), 2010; EFSA Panel
32–55 0.6–2 5 3 0 2
(White-spotted on Contaminants in the Food Chain (CONTAM), 2015). In addition, we
sand-bass)
established the Recommended Intake Values (RIV) for nutritional ele­
ments, which establish the amount of fish that should be ingested per
week to achieve the RWI for each metallic element (Eq. (3)). This
parameter were obtained multiplying the Recommended Weekly Intake
standardization to 5 g with a with decimal precision scale Mettler Toledo
(RWI) established by EFSA and FAO (World Health Organization, 2004;
SB16001. After that, samples were labeled in Ziploc bags and stored in
EFSA Panel on Dietetic Products, 2013a, 2013b; EFSA Panel on Dietetic
cold (~5 ◦ C) until their transport to the Toxicology Area of the Uni­
Products, 2014; EFSA Panel on Dietetic Products, 2015; Efsa, 2016;
versity of La Laguna (Canary Islands, Spain), for processing and subse­
EFSA Panel on Nutrition, 2019) with the median of metal concentration
quent analysis of metal and metalloid concentration.
(mg of metal/kg of wet weight) shown in Table 2. The calculations for
each metallic element, according to TWI and RWI, are shown in Sup­
2.3. Sample processing for metal and metalloids concentration plementary material 2.
determination
RIV = RWI*Median (3)
Each sample were weighted with a Mettler Toledo Classic Plus Furthermore, we calculated the percentage of Weekly Contribution
PB153–S/Fact analytical scales with milligram precision. They were (%WC) of each metal, with the RWI being 100 % (Eq. (4)):
placed in porcelain capsules and dried in the oven at 70 ◦ C for 24 h to
EWI
remove the humidity. After, approximately 1.5 mL of 65 % concentrated %WC = *100 (4)
HNO3 were added to make a digestion before incineration. Samples were RWI
placed in muffle oven for 48 h at 450 ± 25 ◦ C until white ashes were
obtained (Lozano-Bilbao et al., 2018). We weighted the ashes and 2.5. Statistical analysis
filtered through a 1.5 % HNO3 with double distilled water until a so­
lution of 25 mL was obtained. Dissolved samples were placed into Statistical differences in metal and metalloids concentrations were
analysis jars to obtain metal and metalloids concentration by Inductively analyzed for the five species, and the information were pooled and
Coupled Optical Emission Plasma Spectrometry (ICP-OES) (Lozano-Bil­ tested between pelagic (A. solandri) and demersal species (C. affinis,
bao et al., 2018). P. clemensi, H. mystacinus, and P. albomaculatus). Normality of the results
According to the European Food Safety Authority (EFSA) and the were tested with the Kolmogorov-Smirnov and Shapiro-Wilk model, and
Food and Agriculture Organization of the United Nations (FAO), metals Levene test for homogeneity of variance (Zar, 1999; Pan, 2002). The
and metalloid were classified as toxic, macro, micro or trace elements. relationship between metal concentration, total fish weight and fork
Detection and quantification limits for the elements analyzed by ICP- length was determined by Pearson's correlation analysis. Our data did
OES are available in Supplementary material 1. not show a normal distribution, so we applied a non-parametric Krus­
kal–Wallis test to discriminate differences between individual samples,
2.4. Toxicological and nutritional assessment and a Mann-Whitney U post hoc test to establish whether there were
significant differences between pairs of data. A 95 % confidence interval
The Estimated Weekly Intake (EWI) were calculated multiplying the was chosen for all the tests (Rubio et al., 2017a, 2017b).
Metal Concentration (MC), in mg found in muscle tissue per kg of wet
weight; and the Consumption Per Week (CPW) was obtained according 3. Results
to Velasco and Anastacio (2014) fish consumption in the Galapagos (Eq.
(1)). Fish consumption in Santa Cruz Island was assessed in 8910 g per 3.1. Metal concentration in Galapagos fish species
capita per year, which results in a consumption of 178 g per capita per
week (based on an average of 50 weeks per year). We used 178 g of fish C. affinis showed the highest muscle metal concentrations of all
per week for adolescent and adults, and 80 g of fish per week for children species. In contrast, it is important to highlight that H. mystacinus
(Aranceta-Bartrina et al., 2019; Nutrición Comunitaria, 2019) since showed the lowest concentrations for most metals (Fig. 2). P. clemensi
there are no consumption data by age in Galapagos. Based on this figure, showed the second high Ca concentrations, with 1236.76 mg Ca/kg wet
we have estimated the consumption of fish by the population for each weight (Fig. 3). In addition, C. affinis and A. solandri showed the highest
species to carry out the risk assessment and the nutritional evaluation. Zn concentrations (22.07 and 21.56 mg Zn/kg wet weight, respectively).
Significant differences were observed for Pb, C. affinis having the
EWI = MC*CPW (1)
highest concentration (0.44 mg Pb/kg wet weight), followed by
The Maximum Weekly Intake (MWI) establish the maximum P. albomaculatus and A. solandri with 0.18 and 0.16 mg Pb/kg wet

3
E. Franco-Fuentes et al. Marine Pollution Bulletin 189 (2023) 114739

Table 2 In the case of H. mystacinus, we highlight the positive correlation

Median with interquartile range of concentrations of different metals and met­ between K and Mg. On the other hand, Cd and Fe were positively
alloids (mg of metal/kg of wet weight) in muscle of pelagic (A. solandri) and correlated in P. albomaculatus and P. clemensi. In P. albomaculatus,
demersal (C. affinis, P. clemensi, H. mystacinus and P. albomaculatus) species. In Mg–Na was positively correlated, while in P. clemensi the most
bold muscle of species that cannot be marketed in Europe and the USA according outstanding correlation was between K and Mg. The correlation figures
to legislation.
as well as P-values for all statistical tests are available in Supplementary
A. solandri C. affinis P. clemensi H. mystacinus P. albomaculatus material 4.
Toxic elements
Al 12.59 50.76 16.21 12.74 18.98 (12.31) 3.3. Toxicological assessment
(5.95) (49.08) (34.25) (24.84)
B 0.09 0.32 0.15 (0.16) 0.06 (0.09) 0.33 (0.04)
(0.02) (0.69)
C. affinis showed the highest EWI for all the toxic elements, while
Ba 0.65 3.77 0.95 (1.60) 0.58 (0.40) 1.65 (1.56) H. mystacinus showed the lowest. Furthermore, C. affinis was the species
(0.60) (1.86) with the highest human health risk for children adolescent and adults
Cd 0.14 1.24 0.14 0.05 (0.06) 0.34 (0.04) since its Cd concentrations showed MoS values up to 1 from 20 to 100 kg
(0.13) (0.95) (0.38)
of body weight, so the Maximum Weekly Intake (MWI) established for
Ni 0.14 0.43 0.10 (0.10) 0.07 (0.07) 0.10 (0.57)
(0.14) (0.37) this species is 40.18 g of this species (Tables 3 & 4). An ingest of 80 to
Pb 0.16 0.44 0.11 (0.18) 0.09 (0.08) 0.18 (0.67) 178 g/week of the remaining species did not represent a risk for human
(0.14) (0.56) health since they showed MoS values below 1 from 20 kg of body weight
Sr 1.73 4.96 2.54 (7.02) 1.04 (0.79) 2.63 (1.45) in the case of A. solandri, H. mystacinus and P. clemensi, and 40 kg of body
(3.82) (27.00)
weight in the case of P. albomaculatus. Nevertheless, P. albomaculatus
could represent a risk for people with 20 or less kg of body weight if they
Macroelements, microelements and trace elements
ingest 178 g/week of this species since their MoS values for Cd was 1.23,
Ca 236.26 8136.92 1236.76 228.68 359.89 (183.05)
(794.57) (9152.83) (4486.88) (242.78) so for that part of the population, we recommend not to ingest >144.85
Co 0.00 0.00 0.00 (0.01) 0.00 (0.00) 0.00 (0.00) g of P. albomaculatus per week (Table 3).
(0.00) (0.04)
Cr 0.12 0.34 0.17 (0.30) 0.06 (0.09) 0.29 (0.16) 3.4. Nutritional assessment
(0.06) (1.07)
Cu 1.16 7.71 1.78 (2.23) 1.022 (0.48) 1.28 (0.57)
(0.64) (10.02) Demersal species generally showed higher values of metal concen­
Fe 17.17 74.07 12.29 13.57 (8.55) 27.08 (7.69) tration than pelagic species. As with the toxic metals, C. affinis showed
(8.37) (106.51) (20.67) the highest EWI for most of the macro, micro and trace elements,
K 1764.28 3036.82 1889.65 1879.26
highlighting its Ca value of 650.95 mg Ca/week for children (80 g/week
(510.94) (3499.05) (1047.13) (142.11)
1771.45 of fish), and 1448.37 mg Ca/week for adolescent and adults (178 g/
(413.45) week of fish). Furthermore, H. mystacinus showed the lowest EWI of all
Li 1.89 3.70 1.46 (2.14) 1.15 (1.77) 2.70 (0.14) studied species. Comparing the EWI for Zn, A. solandri showed higher
(0.75) (4.05) values than the rest of species, with 1.76 mg Zn/week for children, and
Mg 266.77 361.07 337.79 203.94 329.11 (73.37)
3.93 mg Zn/week for adolescent and adults (Table 5).
(77.92) (589.42) (201.88) (51.88)
Mn 0.16 2.55 0.19 (0.36) 0.16 (0.20) 0.29 (0.34) Due to the arguments mentioned before, C. affinis had the highest
(0.04) (1.96) percentage of weekly contribution for most of the studied elements. An
Mo 0.01 0.08 0.02 (0.03) 0.00 (0.00) 0.01 (0.02) intake of 80 g of C. affinis represents the 18.59 and 15.97 % of weekly
(0.00) (0.16)
contribution for Ca and Fe that infants and children from 0 to 9 years of
Na 1749.73 2944.48 1545.30 1066.12 1675.82
(337.62) (2235.62) (518.84) (320.46) (208.28) age need. Moreover, the current intake of P. clemensis and
V 0.03 0.06 0.00 (0.06) 0.00 (0.03) 0.17 (0.11) P. albomaculatus represents on average 4 % of weekly contribution for Zn
(0.04) (0.23) in adolescents, and adult men and women. No species had a high
Zn 22.07 21.56 6.61 4.65 (8.73) 9.68 (6.63) nutritional intake of K, having all the studied species values that
(18.31) (20.55) (19.59)
represent approximately the 6 % of weekly contribution for infants and
children, and 1.3 % for adolescents and adults (Table 5).
weight, respectively; and finally, P. clemensi and H. mystacinus with 0.11
and 0.09 mg Pb/kg wet weight, respectively. Similarly, the Cd concen­ 4. Discussion
trations found in the species followed the next order, C. affinis > P.
albomaculatus > P. clemensi = A. solandri > H. mystacinus (Fig. 2). 4.1. Metal concentrations in fish species of the GMR and commercial
The median of the toxic, macro, micro and trace element concen­ implications
trations obtained from the studied species are shown in Table 2. More­
over, P-values for all statistical tests are available in Supplementary This research shows that pelagic species (A. solandri) has lower metal
material 3. concentrations than demersal species. These concentrations in demersal
species could be related to differences in their feeding habits, physico­
chemical parameters of the environment and/or the metal absorption
3.2. Correlations between fork length, total weight, and metal levels in from the sediments (Naccari et al., 2015). However, pelagic species
muscle tissue (A. solandri) has higher concentrations of Zn than demersal species,
while the latter have higher concentrations of K, Mg and Cr. These re­
Except for A. solandri, all studied species showed a positive correla­ sults agree with those found in previous studies (Franco-Fuentes et al.,
tion between fork length (FL) and total weight (TW). None of the spe­ 2021a, 2021b), where A. solandri also showed high values of Zn in liver
cies, except C. affinis, showed correlations between FL-metal or TW- and gonads. Moreover, their Zn and Cu concentrations (22.07 and 1.16
metal. A. solandri showed positive correlations between Ca–Cr, mg/kg of wet weight, respectively) where higher than those obtained in
Ca–Mg and Ca–Pb. Regarding C. affinis, Cu–Zn and K–Na concen­ Ghana (West Africa) by Kwaansa-Ansah et al., 2019 (0.019 and 0.118
trations were positively correlated, while Mo was negatively correlated mg/kg of wet weight, respectively). The differences in Zn and Cu con­
with FL and TW. centrations could be related to a lower activity of their metallothioneins,

4
E. Franco-Fuentes et al.
Fig. 2. Horizontal line of boxes represent the median value, lower (grey) and upper (blue) box limits show interquartile range of metal concentration (expressed in
mg/kg wet weight) for the toxic metals found in muscle of the studied species. Demersal species are shown in light blue, while Pelagic species are in dark blue. (For
interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)
which are low molecular weight proteins rich in cysteine that play an
important role in Zn and Cu homeostasis and non-essential metals
detoxification. In addition, this species could also have different accu­
mulation patterns for those elements (Sevcikova et al., 2011; Ali et al.,
2014).
A. solandri also showed low concentrations of Fe and Pb (17.17 and
0.16 mg/kg wet weight, respectively) in muscle tissue compared to the
high levels of those elements found in liver (117.3 and 0.6 mg/kg wet
weight, respectively) in previous studies (Franco-Fuentes et al., 2021b).
This could be because liver is the target organ for these elements accu­
mulation (Jakimska et al., 2011). It has been shown that pelagic species
in the Galapagos have less metals concentration than demersal and
benthic species (Franco-Fuentes et al., 2021a, 2021b; Franco-Fuentes
et al., 2023). Thus, low concentrations of Cd showed by A. solandri could
be explained by its diet, since this species has a diet dominated by
epipelagic species (55.4 %), followed by mesopelagic species (33.4 %)
(Baque-Menoscal et al., 2012). Regarding Zn values, Ali et al. (2014)
established that in A. solandri there is an inverse relation between the
fish length and their Zn concentration in muscle, we did not find this
relationship in our results, perhaps because we had a reduced number of
samples for this species. Correlation analysis showed that Ca concen­
tration was positively correlated with Pb and Cr concentrations. These
results disagree with the arguments mentioned by Ghosh and Adhikari
(2006), in which high Ca levels are related to low Pb and Cr accumu­
lation due to Ca2+/Pb2+ and Ca2+/Cr6+ concentration ratio, causing a
decrease in Pb2+ and Cr6+ uptake through Ca2+ channel. The positive
correlations found in A. solandri (MgCa), C. affinis (K–Na),
P. albomaculatus (Mg–Na), and H. mystacinus-P. clemensi (Mg–K) could
be explained since the force that drives Mg and Ca reabsorption is the
electrical gradient created in the ascending loop of Henle, which is a
structure found in the nephrons, by Na reabsorption through the Na+/
K+/2Cl− cotransporter (Pérez González et al., 2009).
High metal concentrations were expected in P. clemensi, since this is a
5
Marine Pollution Bulletin 189 (2023) 114739
slow growing species and lives at least 17 years (Marín Jarrin et al.,
2018). However, compared to C. affinis and P. albomaculatus, P. clemensi
showed low concentrations of Cd and Pb (0.14 and 0.11 mg/kg wet
weight, respectively), which could explain its high Ca values (1236.76
mg/kg wet weight). Pb is analogous to Ca and penetrates the organism,
while Cd inhibits the Ca transfer with proteins, so due to its low con­
centrations these processes do not occur, allowing the organism to
accumulate higher levels of Ca (Moiseenko and Gashkina, 2020). This is
the first study to assess metals in the muscle tissue of this species and due
to the lack of information available for this species as well as for their
genus on metals, reliable comparisons cannot be made.
The highest metallic concentration in our study were found in
C. affinis. This species is still poorly studied in the Galapagos Islands.
Elorduy-Garay and Caraveo-Patiño (1994) established that the species
C. princeps feeds on benthic animals (especially on ostracods, which are
filter-feeder animals who easily accumulate metals from the environ­
ment). Previously, Cheng et al. (1979) found that marine invertebrates
of the Galapagos accumulate around 6 μg of Cd/g of wet weight, sug­
gesting that these concentrations could be derived from seawater.
Environment could also play an important role in the metal accu­
mulation of C. affinis, since Galapagos have a high volcanic activity,
which could favor the presence of these metallic elements in its sea­
waters (Llorente-Bousquets and Morrone, 2003). C. affinis also had the
highest Fe concentrations of all the studied species (74.07 mg/kg wet
weight). An excessive uptake of this element could affect the regulation
of Fenton's reaction, in which ferric cation catalyze hydrogen peroxide
to generate reactive oxygen species (ROS), that can degrade organic and
inorganic substances (Sevcikova et al., 2011). Furthermore, previous
studies showed that C. affinis also accumulates high quantities of other
metallic elements such as Cd, Al and Hg in hepatic and gonadal tissues
(Franco-Fuentes et al., 2021a, 2021b; Franco-Fuentes et al., 2023). The
high Cd values found in C. affinis of our study (1.24 mg/kg wet weight)
could be causing changes in fish body size, deformities in vertebra, and
E. Franco-Fuentes et al.
Fig. 3. Horizontal line of boxes represent the median value, lower (grey) and upper (blue) box limits show interquartile range of metal concentration (expressed in
mg/kg wet weight) for macro, micro and trace elements found in muscle of the studied species. Demersal species are shown in light blue, while Pelagic species are in
dark blue. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)
histological alterations such as modification of glutathione levels (GSH),
lipid peroxidation (LPO) of the cell membrane, and affect antioxidant
enzymes balance (Khayatzadeh and Abbasi, 2010; Sevcikova et al.,
2011; Authman et al., 2015).
The positive correlation found between Cu and Zn concentrations in
C. affinis could be explained by the fact that these elements take part as
cofactors in many enzymatic and metabolic activities (Bepari et al.,
2021). Nevertheless, the negative correlation observed between Mo-
Fork length and Mo-Total weight suggest that Mo contamination
decrease with fish age. The cause of this could be higher metabolic rates
in old fish, differences in feeding habitat between juveniles and adults, a
dilution effect with size, and faster growth than Mo accumulation (Agah
et al., 2009).
The species P. albomaculatus was the second demersal species with
highest metallic concentrations. This could be explained because we
sampled a reduced number of individuals (n = 5) and the majority were
adults (size of maturation = 37 cm total length), which could accumu­
late a greater number and concentration of metals; and also, because it is
a demersal species (Franco-Fuentes et al., 2021a, 2021b). To the best of
our knowledge, this is the first study to thoroughly estimate the metallic
concentrations in muscle tissue for this species. The research carried out
by Love et al. (2009) in Oil Platforms of Southern California Bight with
the species Paralabrax clathratus showed lower metallic concentrations
for Al (2.8 mg/kg dry weight), Cu (1 mg/kg dry weight) and Pb (0.07
mg/kg dry weight) than our study (19.98, 1.28 and 0.18 mg/kg wet
weight, respectively). However, P. clathratus showed a concentration of
22,000 mg of Ca/kg dry weight, while in our study P. albomaculatus
6
Marine Pollution Bulletin 189 (2023) 114739
showed 359.89 mg Ca/kg wet weight (Love et al., 2009).
P. albomaculatus also showed high Cd concentrations (0.34 mg/kg
wet weight). This could be related to their low Ca concentrations, which
could favor the increase competition of Cd with Ca in muscle tissue and
cause hypocalcemia. In this tissue, cytosolic Ca2+ activates calmodulin,
which is a low molecular weight intracellular acidic protein that allows
muscle fibers contraction. (Sánchez, 2016; Moiseenko and Gashkina,
2020). In addition, the positive correlation observed between Ca–Fe
concentrations in P. albomaculatus and P. clemensi does not agree with
theory since Cd replaces Fe in different proteins, i.e. hemoglobin (Nava-
Ruíz and Méndez-Armenta, 2011).
Finally, H. mystacinus had the lowest metallic concentrations of all
the studied species. Previous studies have shown that this species also
have low levels of metals in hepatic and gonadal tissues (Franco-Fuentes
et al., 2021b). This species is a top predator, deep-water demersal fish,
but its metal levels do not agree with the bioaccumulation process
(Fishbase, 2022), except for Hg, for which a high concentration has been
evidenced (Franco-Fuentes et al., 2023). Due to the lack of information
about the ecology and feeding habits of H. mystacinus in Galapagos, we
could not establish a certain conclusion on the bioaccumulation of Hg
but none of the rest of metals.
The only human contamination sources come from terrestrial ac­
tivities and inhabited harbors, so we hypothesize that the high con­
centration of metallic elements observed in our study could derive from
the vulcanism of the Galapagos Archipelago. For instance, Cd is a usual
element in the Earth's crust, but erosion, volcanos, fumarolic activity
and hydrothermalism can supply this element to the local environments
E. Franco-Fuentes et al. Marine Pollution Bulletin 189 (2023) 114739

Table 3
Toxic metals in muscle of the studied species: Estimated Weekly Intake (EWI-mg of metal/kg of body weight per week), Maximum Weekly Intake (MWI-kg of fish/
week), and Margin of Safety (MoS) for different adolescent and adult body weight (kg bw), with an ingest of 178 g/week of the studied species. In Bold MoS >1.
Species (common name) EWI 20 kg 40 kg 60 kg 80 kg 100 kg

MoS MWI MoS MWI MoS MWI MoS MWI MoS MWI

Al 2.24 0.11 1.59 0.06 3.18 0.04 4.76 0.03 6.35 0.02 7.94
B 0.02 0.00 238.13 0.00 476.26 0.00 714.39 0.00 952.52 0.00 1190.65
Ba 0.12 0.00 42.89 0.00 85.77 0.00 128.66 0.00 171.54 0.00 214.42
Acanthocybium solandri (Wahoo) Cd 0.03 0.50 0.36 0.25 0.71 0.17 1.07 0.13 1.42 0.10 1.78
Ni 0.03 0.02 11.72 0.01 23.44 0.01 35.16 0.00 46.88 0.00 58.60
Pb 0.03 0.33 5.40 0.16 1.08 0.11 1.62 0.08 2.16 0.07 2.70
Sr 0.31 0.02 10.47 0.01 20.94 0.01 31.41 0.00 41.89 0.00 52.36
Al 9.04 0.45 39.40 0.23 0.79 0.15 1.18 0.11 1.58 0.09 1.97
B 0.06 0.00 68.37 0.00 136.75 0.00 205.12 0.00 273.49 0.00 341.87
Ba 0.67 0.02 7.43 0.01 14.86 0.01 22.28 0.01 29.71 0.00 37.14
Caulolatilus affinis (Bighead tilefish) Cd 0.22 4.43 0.04 2.21 0.08 1.48 0.12 1.11 0.16 0.89 0.20
Ni 0.08 0.05 3.09 0.02 7.70 0.02 11.54 0.01 15.39 0.01 19.24
Pb 0.08 0.91 0.19 0.45 0.39 0.30 0.59 0.23 0.78 0.18 0.98
Sr 0.88 0.05 3.67 0.02 7.34 0.02 11.00 0.01 14.67 0.01 18.34
Al 2.89 0.14 1.23 0.07 2.47 0.05 3.70 0.04 4.93 0.03 6.17
B 0.03 0.00 144.13 0.00 288.26 0.00 432.39 0.00 576.52 0.00 720.65
Ba 0.17 0.01 29.45 0.00 58.91 0.00 88.36 0.00 117.81 0.00 147.26
Pontinus clemensi (Mottled scorpionfish) Cd 0.03 0.53 0.34 0.27 0.67 0.18 1.01 0.13 1.34 0.11 1.68
Ni 0.02 0.01 16.39 0.01 32.78 0.00 49.16 0.00 65.55 0.00 81.94
Pb 0.02 0.23 0.76 0.12 1.52 0.08 2.28 0.06 3.04 0.05 3.80
Sr 0.45 0.02 7.16 0.01 14.31 0.01 21.47 0.01 28.63 0.00 35.79
Al 2.27 0.11 1.57 0.06 3.14 0.04 4.71 0.03 6.28 0.02 7.85
B 0.01 0.00 345.28 0.00 690.55 0.00 1035.83 0.00 1381.10 0.00 1726.38
Ba 0.10 0.00 48.10 0.00 96.20 0.00 144.30 0.00 192.40 0.00 240.50
Hyporthodus mystacinus (Misty grouper) Cd 0.01 0.19 0.92 0.10 1.85 0.06 2.77 0.05 3.69 0.04 4.62
Ni 0.01 0.01 21.82 0.00 43.63 0.00 65.45 0.00 87.26 0.00 109.08
Pb 0.02 0.18 0.98 0.09 1.95 0.06 2.93 0.05 3.91 0.04 4.89
Sr 0.19 0.01 17.45 0.01 34.89 0.00 52.34 0.00 69.79 0.00 87.23
Al 3.38 0.17 1.05 0.08 2.11 0.06 3.16 0.04 4.21 0.03 5.27
B 0.06 0.00 66.11 0.00 132.22 0.00 198.33 0.00 264.44 0.00 330.55
Ba 0.30 0.01 16.88 0.01 33.77 0.00 50.65 0.00 67.54 0.00 84.42
Paralabrax albomaculatus (White-spotted sand-bass) Cd 0.06 1.23 0.14 0.61 0.29 0.41 0.43 0.31 0.58 0.25 0.72
Ni 0.02 0.01 15.76 0.01 31.53 0.00 47.29 0.00 63.05 0.00 78.81
Pb 0.03 0.38 0.47 0.19 0.95 0.13 1.42 0.09 1.89 0.08 2.36
Sr 0.47 0.03 6.90 0.01 13.81 0.01 20.71 0.01 27.62 0.01 34.52

(Kakkar and Jaffery, 2005). Nevertheless, it is necessary to carry out
long-term monitoring of metals in the studied species, increase the
sample size, include monitoring of the water column and the substrate,
and of different representatives of the food chain to uncover the origin of
these metals in Galapagos fish.
4.2. Food security implications of toxic elements
The European Food Safety Authority (EFSA) establish a Maximum
Allowable Concentration (MAC) for Pb and Cd of 0.30 and 0.05 mg/kg of
wet weight respectively, according to Regulation (EC) No. 1881/2006 of
December 19, 2006, with modification in Regulation (EU) No. 2015/
1005 of June 25, 2015 (CE/UE, 2006; EFSA Panel on Nutrition, 2019);
and Regulation (EC) No. 1881/2006 of December 19, 2006, with
amendment to the Regulation (EU) No. 488/2014 of May 12, 2014 (CE/
UE, 2006). Based on these parameters, all studied species were above the
MAC for Cd, while C. affinis was the unique species that exceed the MAC
for Pb (Table 2). Therefore, taking this into account, C. affinis should not
be commercialized. Moreover, we cannot establish if the rest of toxic
elements exceed the limits of MAC because there is not enough infor­
mation available about their health implications, so we highlight the
importance of increasing the knowledge about these elements, as well as
their legislation.
Based on the average of 80 and 178 g of fish per week in Galapagos
and the Margin of Safety (MoS), the species C. affinis exhibit Cd toxic risk
for people from 20 to 90 kg. Cd is less likely to cause toxicity to people
with 100 kg of body weight or over. However, we recommend not
ingesting >2 g of C. affinis per kg of body weight (i.e. 140 g for a person
of 70 kg) because of the high Cd toxicity.
We highlight that the rest of species (A. solandri, P. clemensi and
H. mystacinus) do not represent a risk to human health since its MoS
values were below 1 for body weights of 20 to 100 kg, so it would be
recommendable not to exceed the weekly ingestion of C. affinis and
follow a balanced diet with the rest of species.
Finally, the results derived from this research should be studied and
considered by the health authorities in Ecuador due to the characteris­
tics of Cd in the metabolism. Its biological life has been estimated at
5–10 years in liver, while its toxicity derives from loss of homeostatic
control, renal damage, gastrointestinal disorders, and enzymatic inhi­
bition among others (Provoste, 2008).
4.3. Nutritional assessment of macro, micro and trace elements
The highest Estimated Weekly Intake (EWI) with a consumption of
178 g/week consumption of 80 and 178 g/week of fish for all macro­
elements, microelements and trace elements studied was observed in the
species C. affinis, indicating that this species could have a high nutri­
tional content. We highlight its high Ca concentrations (650.95 mg Ca/
week for children, and 1448.37 mg Ca/week for adolescent and adults),
representing the 18.59 % and the 15.92 % of the recommended weekly
intake (RWI) for children and adolescent, respectively. Ca is an impor­
tant element for bones and teeth maintenance, muscle contraction and
neural transmission (World Health Organization, 2004). Therefore,
these results are similar to those found in previous studies realized with
the species Caulolatilus princeps, who also showed high metallic con­
centrations in their tissues (Franco-Fuentes et al., 2021a, 2021b).
C. affinis also showed high Fe levels (13.19 mg of Fe/kg of body weight),
representing the 15.97 % of RWI for children if they consume 80 g/week
of this species. However, it is recommendable to control the ingestion of
this species due to its high Cd concentrations.

7
E. Franco-Fuentes et al. Marine Pollution Bulletin 189 (2023) 114739

Table 4 RWI; while for Na, the concentrations were about 300 mg of Na/kg of
Toxic metals in muscle of the studied species: Estimated Weekly Intake (EWI-mg body weight, representing the 3.20 % for children and the 2 % for ad­
of metal/kg of body weight per week), Maximum Weekly Intake (MWI-kg of olescents and adults of the RWI. These results could be explained
fish/week), and Margin of Safety (MoS) for different children body weight (kg because K and Na participate in the osmotic balance, which regulate the
bw), with an ingest of 80 g/week of the studied species. In Bold MoS >1. concentration of substances inside and outside the cells (World Health
Species (common EWI 20 kg 40 kg Organization, 2004; EFSA Panel on Nutrition, 2019).
name) Our research demonstrates that A. solandri could be an excellent
MoS MWI MoS MWI
nutritional source of Zn, since it showed the highest concentrations for
Al 1.01 0.05 1588.06 0.03 3176.11
B 0.01 0.00 238,129.88 0.00 476,259.75 this microelement (3.93 mg of Zn/kg of body weight). A weekly inges­
Ba 0.05 0.00 42,885.77 0.00 85,771.55 tion of 178 g of A. solandri represents the 5.25 %, 6.53 %, 8.02 % and
Acanthocybium
solandri (Wahoo)
Cd 0.01 0.22 355.85 0.11 711.70 11.45 % of the RWI for children, adolescents, and adults (men and
Ni 0.01 0.01 11,719.61 0.00 23,439.23 women), respectively. This element participates in cellular respiration,
Pb 0.01 0.15 539.78 0.07 1079.56
Sr 0.14 0.01 10,471.49 0.00 20,942.98
DNA and RNA replication, as well as a cofactor of at least 200 enzymes
Al 4.06 0.20 393.99 0.10 787.98 (Rubio et al., 2007). Finally, the species H. mystacinus does not stand out
B 0.03 0.00 68,373.33 0.00 136,746.67 in the contribution of any macroelement, microelement or trace element
Caulolatilus affinis
Ba 0.30 0.01 7427.66 0.01 14,855.32 (as well as found in Franco-Fuentes et al. (2021b) in hepatic and gonadal
Cd 0.10 1.99 40.18 1.00 80.37
(Bighead tilefish) tissues). However, its high Hg concentrations suggest to limit its weekly
Ni 0.03 0.02 3848.31 0.01 7696.63
Pb 0.04 0.41 196.02 0.20 392.04 ingestion (see in Franco-Fuentes et al., 2023).
Sr 0.40 0.02 3668.07 0.01 7336.13
Al 1.30 0.06 1233.20 0.03 2466.39 4.4. Uncertainty
B 0.01 0.00 144,130.11 0.00 288,260.22
Pontinus clemensi Ba 0.08 0.00 29,452.80 0.00 58,905.60
(Spotted Cd 0.01 0.24 335.63 0.12 671.25
As mentioned in previous studies (Franco-Fuentes et al., 2021a,
scorpionfish) Ni 0.01 0.00 16,387.78 0.00 32,775.56 2021b; Franco-Fuentes et al., 2023), our study is biased since all the
Pb 0.01 0.11 760.99 0.05 1521.97 samples come only from the Central-south-eastern bioregion and have a
Sr 0.20 0.01 7157.41 0.01 14,314.82 relatively small sample size. However, a similar sampling size has
Al 1.02 0.05 1569.57 0.03 3139.13
already been successfully used in other studies (Staudinger, 2011).
B 0.01 0.00 345,276.24 0.00 690,552.47
Hyporthodus Ba 0.05 0.00 48,099.05 0.00 96,198.10 Metal concentration found in the fish species studied is assumed to
mystacinus (Misty Cd 0.00 0.09 923.54 0.04 1847.08 derive from the vulcanism of the archipelago, but it could also be due to
grouper) Ni 0.01 0.00 21,816.09 0.00 43,632.18 currents effects. It has been proven that the Cromwell upwelling adds
Pb 0.01 0.08 977.48 0.04 1954.95 high quantities of Fe to the water column on the west of Isabela Island
Sr 0.08 0.00 17,446.57 0.00 34,893.14
Al 1.52 0.08 1053.33 0.04 2106.67
(Palacios, 2004), so at least this deep current could be contributing in
B 0.03 0.00 66,110.27 0.00 132,220.54 adding Fe, and associated metals, to the ocean system. Furthermore, the
Paralabrax
Ba 0.13 0.00 16,884.12 0.00 33,768.24 studies on metal concentrations in fish species of the Galapagos Marine
albomaculatus
(White-spotted
Cd 0.03 0.55 144.85 0.28 289.69 Reserve are scant and very recent (Muñoz-Abril et al., 2022; Franco-
Ni 0.01 0.01 15,762.62 0.00 31,525.24
sand-bass) Fuentes et al., 2021a, 2021b; Franco-Fuentes et al., 2023). In addition,
Pb 0.01 0.17 472.74 0.08 945.47
Sr 0.21 0.01 6904.69 0.01 13,809.38 this study could not include samples from different seasons or stages of
the species life cycle which that could affect fish metal concentrations.
So, long-term studies should be carried out in order to obtain reliable
With an estimated average consumption of 178 g/week, results and stronger evidence.
P. albomaculatus also had high Fe concentrations (4.82 mg of Fe/kg of
body weight), supplying the 4.39 % for adolescent and, 6.04 % and 3.51 4.5. Future research
% of the RWI for men and women, respectively. Moreover, P. clemensi
was the second species that showed the highest contribution of Ca Continuing research in fish metal content will help to increase
(220.14 mg of Ca/kg of body weight), representing the 2.42 % and the knowledge about the contribution of seafood in food safety and nutrition
3.14 % of the RWI for adolescent and adults, respectively. P. clemensi of the Galapagos population (including its fluctuant touristic popula­
also provides the highest amounts of Mg (60.13 mg of Mg/ kg of body tion). In the future, a greater number of samples should be sampled, as
weight), representing the 6.43 %, 3.73 %, and 3.30 % and 3.90 % of the well as collecting them in the cold and dry seasons to verify if the
RWI for children, adolescents and adults (men and women), respec­ changes in metal concentration comes from seasonal variation. In
tively. Other alternatives with high Mg levels are A. solandri (47.49 mg addition, other bioregions of the GMR should be also sampled to check
of Mg/kg of body weight) in the case of children (5.08 % of the RWI), the existence of spatial differences in metal concentration of the species
and P. albomaculatus (58.58 mg of Mg/kg of body weight) for adult men per bioregion since, for example, the Western bioregion has more in­
and women (3.22 % and 3.80 % of the RWI). Therefore, our results fluence of Fe derived from the Cromwell current (Palacios, 2004). This
indicate that both P. albomaculatus and P. clemensi are good sources of research area still needs to be further expanded since overall, we only
Fe, Mg and Ca, which are highly important nutritional elements. For studied information on ten species of the ~70 commercially available
instance, Mg act as a catalyst and regulator in >300 enzymatic systems; (Molina et al., 2004). However, most of them (all but S. violacea and
while, Fe plays a role in oxygen transport and in many tissues is part of C. hyppurus) are among the top catches by weight (Ramírez-González
many enzymatic systems (World Health Organization, 2004). et al., 2022). Future studies should concentrate on including the sword
It should be taken into account that P. clemensi also had high Cu fish, Galapagos and yellow mullets and the Galapagos sheephead wrasse
concentrations (0.32 mg of Cu/kg of body weight), which represent the to complete the metallic content studies of the most caught species.
3.49 % of the RWI for adolescent, 2.84 % for adult men and, 3.49 % for Finally, studies on metallothioneins (MT), as well as stable isotopes
adult women. This micronutrient plays an important role in cellular (δ15N) could be included to elucidate the role of the differences in fish
metabolism (Gárriz et al., 2019). diet with metal content.
All species (except C. affinis) provide similar amounts of K and Na in
children, adolescents, and adults. Regarding K, C. affinis provide 5. Conclusions
approximately 330 mg of K/kg of body weight, which represents the
4.62 % for children and the 1.30 % for adolescents and adults of the This research, in conjunction with the series of previous studies

8
E. Franco-Fuentes et al. Marine Pollution Bulletin 189 (2023) 114739

Table 5
Macroelements, microelements and trace elements: Estimated Weekly Intake (EWI-mg of metal/kg of body weight per week) derived from the consumption (muscle) of
the studied species, RIV (Recommended Intake Value, in kg of fish/week) and WC (Weekly Contribution) for different human ages.
Species (common name) EWI (80 g fish/ Infants and EWI (178 g fish/ Adolescent Adult (19–65 years)
week) children (0–9 week) (10–18 years)
Male Female Male Female
years)

RIV %WC RIV %WC RIV %WC

Ca 18.90 14.81 0.54 42.05 38.52 0.46 29.63 0.60

K 141.14 2.98 2.68 314.04 13.89 1.28 13.89 1.28
Mg 21.34 1.57 5.08 47.49 6.04 2.95 6.82 5.77 2.61 3.08
Na 139.97 5.20 1.53 311.45 8.00 2.22 8.00 2.22
Cr 0.01 3.02 2.65 0.02 4.64 3.84 3.19 5.59
Acanthocybium solandri (Wahoo)
Cu 0.09 6.61 1.21 0.21 7.81 2.28 9.61 7.81 1.85 2.28
Fe 1.37 2.16 3.70 3.06 6.40 2.78 4.65 7.99 3.83 2.23
Mn 0.01 21.32 0.37 0.03 127.92 0.14 127.92 0.14
Mo 0.00 8.19 0.97 0.00 53.26 0.33 53.26 0.33
Zn 1.76 1.52 5.25 3.93 2.73 6.53 2.22 1.55 8.02 11.45
Ca 650.95 0.43 18.59 1448.37 1.12 15.92 0.86 20.69
K 242.94 1.73 4.62 540.55 8.07 2.21 8.07 2.21
Mg 28.88 1.16 6.87 64.27 4.46 3.99 5.04 4.27 3.53 4.17
Na 235.55 3.09 2.58 524.12 4.76 3.74 4.76 3.74
Cr 0.02 1.11 7.22 0.06 1.70 10.46 1.17 15.23
Caulolatilus affinis (Bighead tilefish)
Cu 0.61 1.00 8.01 1.37 1.18 15.09 1.45 1.18 12.26 15.09
Fe 5.92 0.50 15.97 13.19 1.48 12.00 1.08 1.85 16.52 9.61
Mn 0.20 1.37 5.84 0.46 8.21 2.17 8.21 2.17
Mo 0.01 0.87 9.24 0.01 5.63 3.16 5.63 3.16
Zn 1.72 1.56 5.13 3.84 2.79 6.38 2.27 1.59 7.83 11.19
Ca 98.94 2.83 2.82 220.14 7.36 2.42 5.66 3.14
K 151.17 2.78 2.87 336.36 12.96 1.37 12.97 1.37
Mg 27.02 1.24 6.43 60.13 4.77 3.73 5.39 4.56 3.30 3.90
Na 123.62 5.89 1.35 275.06 9.06 1.96 9.06 1.96
Cr 0.01 2.13 3.75 0.03 3.27 5.44 2.25 7.92
Pontinus clemensi (Mottled scorpionfish)
Cu 0.14 4.31 1.85 0.32 5.09 3.49 6.27 5.09 2.84 3.49
Fe 0.98 3.02 2.65 2.19 8.94 1.99 6.49 11.16 2.74 1.59
Mn 0.01 17.65 0.45 0.04 105.87 0.17 105.87 0.17
Mo 0.00 3.27 2.45 0.00 21.22 0.84 21.22 0.84
Zn 0.52 5.08 1.57 1.18 9.10 1.96 7.41 5.18 2.40 3.43
Ca 18.24 15.31 0.52 40.71 39.79 0.45 30.61 0.58
K 141.71 2.96 2.69 315.32 13.83 1.29 13.83 1.29
Mg 16.31 2.06 3.88 36.30 7.89 2.25 8.92 7.55 1.99 2.36
Na 85.20 8.54 0.93 189.77 13.13 1.36 13.13 1.36
Cr 0.00 5.51 1.45 0.01 8.47 2.10 5.82 3.06
Hyporthodus mystacinus (Misty grouper)
Cu 0.08 7.53 1.06 0.18 8.90 2.00 10.96 8.90 1.62 2.00
Fe 1.08 2.73 2.92 2.42 8.10 2.20 5.88 10.11 3.03 1.76
Mn 0.01 21.31 0.37 0.03 127.88 0.14 127.88 0.14
Mo 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00
Zn 0.37 7.21 1.10 0.83 12.93 1.38 105.21 7.37 1.69 2.42
Ca 28.79 9.73 0.82 64.06 25.29 0.70 19.45 0.92
K 150.34 2.79 2.86 334.51 13.04 1.37 13.04 1.37
Mg 26.32 1.28 6.26 58.58 4.89 3.64 5.53 4.68 3.22 3.80
Na 134.06 5.43 1.47 298.30 8.35 2.13 8.35 2.13
Paralabrax albomaculatus (White-spotted Cr 0.02 1.30 6.14 0.05 2.00 8.90 1.38 12.95
sand-bass) Cu 0.10 5.98 1.33 0.23 7.06 2.52 8.70 7.06 2.05 2.52
Fe 2.16 1.37 5.84 4.82 4.06 4.39 2.95 5.07 6.04 3.51
Mn 0.02 11.75 0.68 0.05 70.51 0.25 70.51 0.25
Mo 0.00 3.82 2.09 0.00 24.84 0.72 24.84 0.72
Zn 0.77 3.47 2.30 1.72 6.21 2.86 5.06 3.54 3.52 5.03

already published of fish metal content (Franco-Fuentes et al., 2021a,
2021b; Franco-Fuentes et al., 2023), provides a baseline on food safety
in ten commercial fish species of the Galapagos Islands by estimating the
muscle concentration of macroelements, microelements, trace elements
and toxic metals. Our data shows that pelagic species (A. solandri) has
higher concentrations of Zn than demersal species, while the latter have
higher concentrations of K, Mg and Cr. These results could be explained
by differences in their feeding habits, physicochemical parameters of the
environment they live in and/or the metal absorption from the sedi­
ments. We hypothesize that the high concentration of metallic elements
observed in our study could derive from the vulcanism of the Galapagos
Archipelago, since the only human contamination sources come from
terrestrial activities and inhabited harbors. C. affinis showed the highest
metallic concentrations of all species, while H. mystacinus had the lowest
metallic concentrations of all it. Nevertheless, the negative correlation
observed between Mo-Fork length and Mo-Total weight could be due to
higher metabolic rates in old fish, differences in feeding habitat between
juveniles and adults, a dilution effect with size, and/or faster growth
than Mo accumulation.
Ecuador does not have its own regulation for metals in edible/
commercial fish species yet, so evaluation was made using the European
Union legislation (CE/UE, 2006). According to the CE/UE, none of the
species could be marketed in Europe because all Cd levels exceeded the
limit of 0.05 mg/kg wet weight (0.10 mg/kg wet weight for Thunnus sp)
all studied species were above the Maximum Allowable Concentration
(MAC) for Cd, while C. affinis was the unique species that also exceed the
MAC for Pb. Regarding the MoS for Pb, P. albomaculatus only showed
values above 1 if people with 20 kg of body weight or less ingest more
than 178 g/week of this species, so we recommend not ingesting >7.2 g
of P. albomaculatus per kg of weight (i.e. 144.9 g for a person of 20 kg).
A. solandri, P. clemensi and H. mystacinus do not represent a human
health risk since its MoS values were below 1 for people of up to 100 kg

9
E. Franco-Fuentes et al.
of body weight. C. affinis showed the highest Estimated.
Weekly Intake (EWI) for all nutritional elements studied. However, it
is recommendable to control the ingestion of this species due to its high
Cd concentrations. Our results indicate that both P. albomaculatus and
P. clemensi are good sources of Fe, Mg and Ca, while a weekly ingestion
of 80 g of A. solandri represents the 5.25 % of the Zn RWI for children,
while the ingestión of 178 g of A. solandri represents the 6.5 %, 8.0 %
and 11.5 % of the Zn RWI for adolescents, adult men and adult women,
respectively. Finally, due to the low values for Cd and Pb found in
H. mystacinus its intake should be recommended to have a balanced diet
with the rest of species. However, due to its high Hg values, it should be
consumed in moderation (a maximum of 72 g/week for a 70 kg person)
to avoid health problems (Franco-Fuentes et al., 2023).
Supplementary data to this article can be found online at https://doi.
org/10.1016/j.marpolbul.2023.114739.
CRediT authorship contribution statement
Sampling data and analysis were performed by all authors. EFF, NM
and AJG leads the paper writing and all authors contributed to the
interpretation of the results and the drafts reviews.
Declaration of competing interest
The authors declare that they have no known competing financial
interests or personal relationships that could have appeared to influence
the work reported in this paper.
Data availability
Data will be made available on request.
Acknowledgements
We would like to thank to the Charles Darwin Foundation and the
Galapagos National Park Directorate for their help in this study. We owe
a special thanks to artisanal fishers Luis Bonilla, Jaime Asencio, Jona­
than Erazo and Nelson Ibarra who kindly contributed with samples for
this study. The research was done under the Galapagos National Park
Directorate permit PC-33-21. Finally, we would like to thank the Leona
M. and Harry B. Helmsley Charitable Trust and the Gordon and Betty
Moore Foundation for their support in funding this research. This pub­
lication is contribution number 2478 of the Charles Darwin Foundation
for the Galapagos Islands.
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