Marine Pollution Bulletin 60 (2010) 2022–2025

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Marine Pollution Bulletin

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Trace elements in farmed and wild gilthead seabream, Sparus aurata

Vincenzo Minganti *, Giuliana Drava, Rodolfo De Pellegrini, Camilla SiccardiDipartimento di Chimica e Tecnologie Farmaceutiche ed Alimentari, Università di Genova, Via Brigata Salerno 13, 16147 Genova, Italy

a r t i c l e i n f o

Keywords:AquacultureBioaccumulationMercury

0025-326X/$ - see front matter � 2010 Elsevier Ltd.doi:10.1016/j.marpolbul.2010.07.023

* Corresponding author. Tel.: +39 010 3532604; faxE-mail address: minganti@dictfa.unige.it (V. Minga

a b s t r a c t

In the present study, we sought to determine the concentration of several trace elements (total andorganic mercury, selenium, cadmium, lead, arsenic, copper, chromium, iron, manganese, molybdenum,vanadium and zinc) in muscle tissue of gilthead seabream (Sparus aurata), an edible finfish species thatis widely cultured in the Mediterranean area. The phenomenon of bioaccumulation and bioamplification(especially of mercury) was investigated by comparing farmed fish with wild specimens of the same spe-cies. Farmed specimens showed mercury and arsenic concentrations significantly lower than wild spec-imens, and no relationship was found between mercury concentration and body size. The lower level ofmethylmercury in farmed fish has important implications for consumer health.

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1. Introduction

Gilthead seabream (Sparus aurata, Linnaeus 1758) is a suitablespecies for extensive aquaculture in the Mediterranean, and itsproduction is growing considerably in this region: a total of257 tonnes were produced in 1980 and 125,335 tonnes were pro-duced in 2007 (FAO, 2010). In Italy, large-scale production wasdefinitively achieved in 1988–1989, and today Italy is among themajor producers (6% of total) in the Mediterranean (FAO, 2010).

Elevated mercury levels in blood samples from the general pop-ulation have been associated with fish consumption (Hightowerand Moore, 2003; Mahaffey et al., 2004). However, only a few pa-pers report comparisons of trace element concentrations betweenfarm-raised and wild animals (Sapkota et al., 2008). In this paper,we present the results of an investigation of trace elements (totaland organic mercury, selenium, cadmium, lead, copper, chromium,iron, manganese, molybdenum, vanadium, zinc and arsenic) inspecimens of gilthead seabream from an aquaculture plant in theLigurian Sea, Italy. The most important toxic trace elements(mercury, cadmium, lead and arsenic) and a series of essentialtrace elements (e.g., copper, iron, etc.) were considered. Data werecompared with results from wild specimens living in the sameenvironment.

Fish is known to contribute significantly to human exposure totoxic trace elements (mainly mercury), but limited data on the dif-ferences between farmed and wild fish are available (EFSA, 2005).

We sought to compare the bioaccumulation of trace metals inaquaculture products and to evaluate the potential human healthrisks associated with farmed fish consumption. Samples of food

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: +39 010 3532684.nti).

pellets were also occasionally collected during this research todetermine their trace element content.

2. Materials and methods

Specimens of farmed gilthead seabream were collected from the‘‘Aqua s.r.l.” aquaculture plant, which is located two kilometers off-shore in the Cavi di Lavagna, Ligurian sea, Italy (44�1702400N09�2004900E). Samples were collected every two or three monthsby obtaining specimens with standard lengths between 11 and20 cm. The food pellets used in the aquaculture plant were alsosampled. Wild specimens were occasionally obtained from localfishermen. Only a small number of samples were considered dueto the low catches of this species in the area.

During the experimental period, the fish presented a continuousincrease in body weight and length. At the time of their introduc-tion to the cages, the fish measured 11 cm in body length andweighed 40 g. The fish were removed for commercial purposeswhen they reached a length of 24–25 cm and a weight of400–500 g. Both the farmed and the wild organisms belonged tothe same growth curve as shown in Fig. 1. This assured that nomethods for growth acceleration were utilized in the captivityfarm.

The fish samples were stored at �27 �C until the analysis. Afterthawing, standard length and body weights were recorded for eachspecimen. Only the muscular tissue was used for the analysis. Sam-ples were freeze-dried and homogenized, and the fresh weight/dryweight ratio was calculated.

The samples (0.3 g dry weight) were mineralized with 4.5 ml of65% nitric acid (Suprapur, Merck, Darmstadt, Germany) in closedTeflon PFA vessels using a MDS 2000 (CEM Corporation, Matthews,NC, USA) microwave digestion system.

Table 1Quality control. The results obtained for the Certified Reference Material TORT-2(Lobster hepatopancreas. Institute for Environmental Chemistry. National ResearchCouncil Canada. Ottawa. Canada). Concentrations are given in lg g�1 dry weight. Thevalues found are reported as the mean values of five determinations with 95%confidence intervals. Organic mercury concentration is reported as lg of Hg g�1, andthe certified value refers to methylmercury concentration (expressed as mercury).Percent recovery is also reported.

Element Certified value(lg g�1 dry wt.)

Found value(lg g�1 dry wt.)

Recovery(%)

As 21.6 ± 1.8 21.4 ± 1.9 99Cu 106 ± 10 91 ± 6 86Fe 105 ± 13 103 ± 8 98Hg-tot 0.27 ± 0.06 0.26 ± 0.02 96Hg-org 0.152 ± 0.013 0.14 ± 0.02 92Mn 13.6 ± 1.2 12.5 ± 0.9 92Zn 180 ± 6 177 ± 9 98

0 100 200 300 400 500 600Weight (g)

10

15

20

25

30St

anda

rd le

ngth

(cm

)

Wild

Farmed

Fig. 1. Growth (body weight in g vs. standard length in cm) of farmed (emptysquares) and wild (filled squares) Sparus aurata from the Ligurian Sea.

V. Minganti et al. / Marine Pollution Bulletin 60 (2010) 2022–2025 2023

After cooling, the solutions were transferred to 25 ml volumet-ric flasks and diluted to volume with ultra pure water (ElgastatUHQ, Elga Ltd., High Wycombe Bucks, UK). All glassware waswashed with 1–2 M nitric acid and rinsed with ultra pure water.The concentrations of the different elements in the resulting solu-tions were determined by atomic absorption and atomic emissionspectrometric methods.

Total mercury (Hg-tot) was determined by atomic absorptionspectrometry (model 560, Perkin–Elmer and Co., Germany) usingthe cold vapor technique after pre-concentration over gold (Au-CVAAS) following reduction with a 10% (w/v) tin(II) chloridedihydrate solution. Organic mercury (Hg-org) was measured byAu-CVAAS using 0.3 g of the sample after acidification with2 ml of 47% HBr, extraction in toluene (12 ml) and back-extrac-tion in 5 ml of 1% (w/v) L-cysteine solution. Mercury was reducedwith a solution of 50% (w/v) tin(II) chloride dihydrate and 10%(w/v) cadmium chloride in a basic medium (10% sodium hydrox-ide). Calibration was carried out by means of the standard addi-tion method. The detection limit of the method (computed asthree times the standard deviation of the blanks) was0.006 lg g�1 dry weight for Hg-tot and 0.006 lg g�1 dry weightfor Hg-org.

Copper, iron, manganese, zinc and arsenic were measured byatomic emission spectrometry with an inductively coupled plasmatorch (ICP-AES) using a J.Y. 24 (Jobin-Yvon, Longjumeau, France)equipped with a Cetac U-5000AT+ ultrasonic nebulizer (Cetac Tech-nologies Inc., Omaha, Nebraska, USA). Calibrations were done withaqueous standard solutions (Merck, Darmstadt, Germany) using4 lg ml�1 of yttrium as an internal standard. The detection limitsfor each metal were 0.1 lg g�1 dry weight for copper and manga-nese; 0.8 lg g�1 dry weight for iron; 0.4 lg g�1 dry weight for zincand 0.6 lg g�1 dry weight for arsenic.

The concentrations of chromium, molybdenum and vanadiumwere also measured by ICP-AES, but their levels were always belowthe limit of detection (0.1, 0.06, and 0.05 lg g�1 dry weight, respec-tively). The concentrations of selenium (HG-AAS), cadmium andlead (GF-AAS) were also measured and found to be below the limitof detection (0.2, 0.003, and 0.013 lg g�1 dry weight, respectively)for most of the samples. For this reason these elements have notbeen included in the discussion.

The same elements that were detected in fish samples were alsomeasured in the food pellets used in the aquaculture plant.

All analyses were carried out in duplicate. For each run, two‘‘blanks” were analyzed using the same procedure to check thepurity of reagents and any possible contamination. The accuracyof the analytical methods was verified by analyzing a Standard Ref-erence Material (TORT-2, Marine Reference Material for Trace Met-als, National Research Council of Canada, Ottawa, Canada). Theresults of the quality control showed very good agreement be-tween the measured concentrations and the certified values forall elements, and recovery was between 86% (Cu) and 99% (As)with a mean of 94 ± 5%. The results are reported in Table 1.

Statistical analysis was performed using SYSTAT� 10.2 (SPSSInc., Chicago, IL, USA).

3. Results and discussion

The results of the experiments described here are summarizedin Table 2. The biological parameters and the concentrations ofthe different elements are reported as the mean and range of themeasured values.

Previous studies have examined the trace element content infarmed and wild fish of several different species, and findings havesometimes been inconsistent. Yamashita et al. (2005) found mer-cury to be higher in farmed bluefin tuna (Thunnus species), butBalshaw et al. (2008) and Nakao et al. (2007 and 2009) reportedthat it was lower. Among freshwater species, farmed paddlefish(Polyodon spathula) showed lower methylmercury concentrations(Dasgupta et al., 2004) as did bluegill sunfish (Lepomis macrochirus,Ikem and Egilla, 2008). Kelly et al. (2008) found mercury concen-trations in wild salmon from British Columbia to be significantly(three-fold) higher than in farmed salmon, and this was in contrastwith the findings of Foran et al. (2004) who found no significantdifference.

We found that only mercury and arsenic showed significant dif-ferences (t-test p = 0.000) between farmed and wild fish (Table 2).Samples from wild fish showed mercury concentrations that were4.5 times higher than samples from farmed specimens, and the ar-senic concentration in wild fish was 6.4 times higher. Wild animalsshowed a slightly higher percentage (t-test p = 0.046) of organicmercury (mean 98% in wild versus 85% in farmed).

Usually mercury (and methylmercury) concentrations in fish in-crease according to size (Storelli et al., 2007). From the data pre-sented in Fig. 2, it is evident that no relationship exists betweenmercury concentration and standard length for farmed S. aurata(not enough data were collected from wild samples to be includedin this discussion). Trace elements were measured in food pelletsused in the aquaculture plant. The organic mercury (methylmer-cury) concentration in food pellets was found to be in the rangeof 0.002–0.03 lg g�1 dry weight. S. aurata is a carnivorous fish that

Table 2Mean ± standard deviation and range of standard length, body weight and trace element concentration in farmed and wild Sparus aurata (muscular tissue). The total number ofsamples (n) is also reported. Concentrations are expressed as lg g�1 dry weight. Organic mercury is reported as lg of Hg g�1 dry weight.

Length (cm) Weight (g) Hg-tot (lg g�1) Hg-org (lg g�1) Cu (lg g�1) Fe (lg g�1) Mn (lg g�1) Zn (lg g�1) As (lg g�1)

FARMEDn = 26 Mean 20.5 ± 3.9 305 ± 150 0.12 ± 0.02 0.10 ± 0.03 1.3 ± 0.3 10.3 ± 2.5 0.5 ± 0.2 15.9 ± 3.2 4.9 ± 1.4

Range 11.2–26.0 39–581 0.07–0.16 0.06–0.15 0.8–2.0 5.2–15.2 0.3–1.1 10.7–21.0 2.1–7.6

WILDn = 5 Mean 21.6 ± 2.2 271 ± 65 0.54 ± 0.21 0.54 ± 0.22 1.6 ± 0.4 14.4 ± 4.5 0.5 ± 0.1 18.2 ± 2.9 31.6 ± 8.5

Range 19.0–24.5 195–347 0.29–0.72 0.26–0.72 1.3–2.2 8.8–19.0 0.3–0.6 15.0–22.0 18.4–39.6

10 15 20 25 30Standard lenght (cm)

0.0

0.1

0.2

0.3

0.4

0.5

0.6

0.7

0.8

Hg-

t (µg

g-1d.

wt.)

Farmed

Wild

Fig. 2. Total mercury concentration (in lg g�1 dry weight) vs. standard length (cm)of farmed (empty squares) and wild (filled squares) Sparus aurata from the LigurianSea.

2024 V. Minganti et al. / Marine Pollution Bulletin 60 (2010) 2022–2025

feeds mainly on molluscs (particularly mussels), crustaceans andfish, and they are only occasionally herbivorous (Fisher et al.,1987). Molluscs are representative of the diet of wild S. aurata,

Table 3Trace element concentrations in gilthead sea bream (Sparus aurata), muscular tissue, froexpressed as lg g�1 dry weight.

Samplingarea

Weight(g)

Hg-tot(lg g�1)

Cu(lg g�1)

Fe(lg g�1)

Mn(lg g�1)

Ligurian Sea,farmed

305 ± 150 0.12 ± 0.02 1.3 ± 0.3 10.3 ± 2.5 0.5 ± 0.2

Ligurian Sea,wild

271 ± 65 0.54 ± 0.21 1.6 ± 0.4 14.4 ± 4.5 0.5 ± 0.1

Italyb 27–195 0.82 ± 0.20 10 ± 1Israel 188–309 0.47–0.73a

Turkey 95.1–674.5 2.84 ± 0.43 19.60 ± 7.84Turkey 1.239 13.166 1.266Turkey 89.9 ± 2.6 2.67 ± 0.26a 167.7 ± 16.25a 3.23 ± 0.47a

Turkey 56.13 3.25-9.15Turkey 54.1 0.55-0.82 7.16-16.5Turkey 140.33 ±

7.3518.58 ± 1.72a 28.75 ± 1.29a 1.16 ± 0.00a

Spain 0.30 ± 0.040 .13–0.60a

Spain 1.87

a Concentrations converted to d. wt. using 4.31 as factor.b Farmed.

and previous reports on molluscs collected in the northwesternMediterranean show higher methylmercury concentrations. Thisexplains why wild animals have a higher concentration in mercuryat the time of collection. Indeed Claisse et al. (2001) report meth-ylmercury concentrations in the range 0.04–0.09 lg g�1 dry weightin France and Ipolyi et al. (2004) report levels in the range 0.02–0.12 lg g�1 dry weight in Sardinia (Italy).

The total arsenic concentration is higher in wild specimens, butthe inorganic arsenic (Group 1, which is carcinogenic to humans) isusually very low in fish (Kholmeyer et al., 2002), and therefore fishconsumption is not considered to be a significant health risk (EFSA,2005).

For the other elements listed in Table 2 (copper, iron, manga-nese and zinc), there are no significant (p < 0.006) differences be-tween farmed and wild samples.

A comparison of published data for S. aurata is presented inTable 3. Few data are available for total mercury and no significantdifferences have been reported. No data for organic mercury areavailable in literature. Copper and iron show similar concentra-tions except in the case of Uysal et al. (2008) and Türkmen et al.(2009), which reported only on iron. Our data are in agreementwith published results for copper, iron and zinc (Canli and Atli,2003). Furthermore, our study was conducted with a similar sam-ple size. The lack of agreement in data for zinc prevents any com-ment on the abundance of this element in wild and farmed species.Few comparisons are possible for arsenic, and it is very difficult todraw conclusions about cadmium and lead where the observed dif-ferences are very large.

m the Mediterranean. Concentrations (mean and standard deviation, or range) are

Zn(lg g�1)

As(lg g�1)

Cd(lg g�1)

Pb(lg g�1)

Reference

15.9 ± 3.2 4.9 ± 1.4 <0.003–0.022

<0.013–0.139

This work

18.2 ± 2.9 31.6 ± 8.5 <0.003–0.007

<0.013–0.027

This work

16 ± 3 Carpenè et al. (1999)Yannai and Sachs (1978)

26.66 ± 7.62 0.37 ± 0.11 5.54 ± 0.74 Canli and Atli (2003)4.837 1.341 2.314 Türkmen et al. (2005)59.9 ± 9.22a 1.29 ± 0.22a 1.94 ± 0.22a Türkmen et al. (2009)33.4-67.75 0.12–0.13 Dural et al. (2006)8.82-76.98 0.64–2.44 Dural et al. (2007)30.56 ± 2.59a Uysal et al. (2008)

Ortega-García et al. (2009)

44.86 13.58 0.01 3.68 Vicente-Martorell et al.(2009)

V. Minganti et al. / Marine Pollution Bulletin 60 (2010) 2022–2025 2025

4. Conclusions

Fish is a significant part of the human diet. It represents animportant source of protein and contains essential componentsfor a healthy nutrition, such as the x-3 long-chain polyunsaturatedfatty acids that have been show to have positive effects on infantdevelopment (Mahaffey, 2004).

However, fish contains methylmercury and is the major sourceof this contaminant for humans (Hightower and Moore, 2003;Mahaffey, 2004; Mahaffey et al., 2004).

In a recent report, the Joint FAO/WHO Expert Committee onFood Additives and Contaminants (JECFA) confirmed that anamount of 1.6 lg/kg body weight/week of methylmercury is a Tol-erable Weekly Intake (PTWI) and that this level should not be ex-ceeded by women of childbearing age or by children (WHO, 2006).To balance the nutrient benefits and the negative consequences ofmethylmercury exposure, a limitation on the number of fish por-tions consumed per week has been suggested. Therefore, lowermethylmercury concentrations in farmed specimens will haveimportant implications for consumer health. In fact, on the basisof the present study, methylmercury intake remains below the rec-ommended limits even if the amount of farmed fish consumed isfour times higher than wild fish. This may be important for sensi-tive subjects such as children less than 15-years old.

However, it is important to note that the present study is specif-ically aimed at evaluating the trace element content and does nottake into account important quality parameters or other contami-nants, such as persistent organic pollutants, antibiotic residues,parasites and viruses. Evaluation of these contaminants is essentialfor understanding the human health risks associated with con-sumption of farmed fish versus wild fish (Sapkota et al., 2008).

Acknowledgements

The authors thank the staff of ‘‘AQUA s.r.l” (Cavi di Lavagna,Genova) for providing the samples used in this study.

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